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Cumulative purposeful soccer heading can lead to compensatory Cumulative purposeful soccer heading can lead to compensatory
changes in brain activity during combined moderate exercise and changes in brain activity during combined moderate exercise and
cognitive load in female youth soccer players cognitive load in female youth soccer players
Alexandra Harriss,
The University of Western Ontario
Supervisor: Dickey, James P.,
The University of Western Ontario
Joint Supervisor: Walton, David M.,
The University of Western Ontario
A thesis submitted in partial ful;llment of the requirements for the Doctor of Philosophy degree
in Health and Rehabilitation Sciences
© Alexandra Harriss 2020
Follow this and additional works at: https://ir.lib.uwo.ca/etd
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Recommended Citation Recommended Citation
Harriss, Alexandra, "Cumulative purposeful soccer heading can lead to compensatory changes in brain
activity during combined moderate exercise and cognitive load in female youth soccer players" (2020).
Electronic Thesis and Dissertation Repository
. 7262.
https://ir.lib.uwo.ca/etd/7262
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ii
Abstract
Head trauma that occurs during sporting events is responsible for an increasing number of
emergency department visits in Canada and is associated with an increased risk of
developing neurodegenerative diseases.
While head injury in American football has been
extensively studied, it cannot be extrapolated to non-helmeted sports. Approximately 265
million people are actively participating in soccer and many are 18 years of age and younger.
Soccer is unique in that players use their head to redirect the ball; however, the effects of
cumulative purposeful soccer heading on brain health are unknown. Accordingly, the
objective of this thesis was to quantify head impact magnitudes that female youth soccer
players sustain during games and evaluate their influence on electrophysiological functioning
both at rest and exercise. This was achieved through three research projects that studied
female youth soccer players for an entire soccer season and investigated repetitive soccer
heading using methodological equipment including, game video analysis, headbands
instrumented with wireless microsensors, as well as electroencephalogram (EEG) recordings.
Results indicated that the median number of headers experienced during a single game was
one, while the maximum is nine, and minimum is zero (Chapter 2). Furthermore, player age
is positively associated with an increasing number of purposeful soccer headers, but there is
no association between head impact location and game scenario (Chapter 2). Chapter 3
reveals that game scenario and head impact location significantly affect both linear head
acceleration and rotational head velocity magnitudes. As an initial attempt to detect
neurocognitive change (Chapter 4), EEG recordings revealed a statistically significant
increase in EEG power during exercise compared to rest at each EEG frequency band
(Alpha1, Alpha2, Beta1, Beta2, Theta). These differences were amplified when cumulative
number of headers were considered, but only for Alpha1, Alpha2 and Beta2. In conclusion,
this thesis shows cumulative soccer heading experienced by female youth soccer players
could lead to neurocognitive changes after one season of soccer. Furthermore, exercise may
help to reveal sub-clinical brain changes due to cumulative soccer heading that are not shown
at rest. These findings can help guide data-driven approaches to improve player safety in
youth soccer.
iii
Keywords
Adolescent, concussion, head impacts, brain injury, repetitive, girls, sports, prevention,
coaching, football.
iv
Summary for Lay Audience
While there are numerous personal and societal benefits from participation in sport, head
injuries are a healthcare concern that are responsible for an increasing number of emergency
department visits. More recently, evidence highlights that repetitive head impacts
experienced through sport may be responsible for the onset of long-term cognitive deficits
including Alzheimer’s Disease and Chronic Traumatic Encephalopathy (CTE). Considerable
research has evaluated American football, while females and adolescents are understudied;
even though females have a higher rate of head injury compared to males, and adolescents
report more prolonged symptomology. In soccer, players experience repetitive head impacts
through purposeful soccer heading; however, their cumulative effects are unknown.
Determining the relationship between purposeful soccer heading and brain function can help
inform evidence-based interventions to improve player safety. Accordingly, this thesis seeks
to delineate the relationship between repetitive head impacts and brain health by evaluating
purposeful soccer heading in female youth soccer players. Game video was recorded during
an entire season of soccer, and players wore headbands containing microsensors to quantify
head impact accelerations. Purposeful headers were characterized by head impact location
(front, top, side), player position (defense, midfield, forward) and game scenario (corner
kick, throw in, goal kick etc.). In addition, measures of brain activity were collected using
electroencephalogram (EEG) recordings to determine changes in brain function, related to
cumulative purposeful soccer heading. The findings from this thesis indicate that female
youth soccer players frequently head the ball during soccer games, and increasing player age
is associated with an increasing number of headers experienced. In addition, the head impact
accelerations that result from purposeful soccer heading depend on game scenario as well as
head impact location. Lastly, our EEG measures indicate that brain activity increases
compared to rest during combined exercise and cognitive load, and that an increasing number
of cumulative headers amplifies this difference. These results provide important information
to help develop evidence-based criteria to reduce the risk of head injury that results from
repeated head impacts, and could improve the safety of players in the short- and long-term.
v
Co-Authorship Statement
This thesis contains material from three published manuscripts (Chapter two, Chapter three,
Chapter four) that encompass the collaborative work of researchers and co-authors.
Alexandra Harriss is the primary author of all of the chapters contained in this thesis. She
identified and researched this topic, designed studies, as well as collected, analyzed, and
drafted each of the manuscripts prior to publication. Chapters two, three, and four were co-
authored by Dr. James P. Dickey (Professor in the School of Kinesiology, Faculty of Health
Science, Western Ontario), Dr. David M. Walton (Associate Professor in the School of
Physical Therapy, Faculty of Health Science), and Dr. Andrew M. Johnson (Associate
Professor in the School of Health Studies, Faculty of Health Science). These co-authors
contributed to the research design and findings, as well as reviewed and revised manuscripts
prior to publication. Lastly, Dr. James WG. Thompson co-authored Chapter four (Evoke
Neuroscience Inc, New York, NY, USA). He contributed to the research design and findings
and analysis of Chapter 4 as well as reviewed and edited the final manuscript prior to
publication.
vi
Acknowledgments
First, I would like to thank Dr. Jim Dickey, my supervisor. I cannot find that shining word or
glowing phrase that expresses how grateful I am for your mentorship. Jim, you have
supported me throughout these last five years, encouraging me to explore my passion in
research and in life. I think that is what truly makes you an incredible supervisor, my PhD
journey was not purely about research and academia, but extended to all facets of my life.
Thank you for your countless hours spent collecting data with me, supporting me at
conferences, data analysis, revisions, and meetings, but also teaching me that no work gets
done without a Starbucks coffee. I promise if I ever have a lab of my own, I will greet my
students with the same inspiration, energy, mentorship and kindness that you have shown me.
It was an absolute privilege to be your student.
I would also like to thank my joint-supervisor Dr. David Walton, for his guidance throughout
each stage of my research, and constructive suggestions that were determinant for the
accomplishment of the work presented in this thesis. I am extremely grateful for your
positivity, motivation and commitment to my PhD journey.
Dr. Andrew Johnson, thank you for your support and encouragement during my PhD. From
our meetings, you taught me that my academic career could be whatever I wanted it to be,
and that I had the power to create my own path and be different. Thank you for having the
confidence in my research abilities and of course, for teaching me that RStudio is truly better
than SPSS.
Gerry Iuliano and Paul Walker at GForceTracker as well as Dr. James Thompson at Evoke
Neuroscience, thank you for supporting my research and making my idea come to life. This
dissertation was a project of passion. Your in-kind contributions of equipment and technical
support gave me the opportunity to make my dream a reality.
I would also like to thank Gary Miller, and Gabriel Assis at the Ontario Soccer Association,
as well as the Burlington Bayhawks female youth soccer teams, coaching staff and
administration. Thank you for allowing me the opportunity to bring my passion for soccer
into my research.
vii
To my labmates, who always kept a sense of humor in the lab when I had lost mine. Thank
you for always supporting me throughout the “big” PhD moments. I would also like to
sincerely thank Marquise Bonn, Emilie Woehrle, Jeffrey Brooks, Gordon Barkwell, and
Ryan Frayne. When I look back on our time in the lab together, it is filled with memories of
endless laughter. I wish you all nothing but the best in life.
Karl, we have ran up mountains together, camped under the stars, learned Arizona does in
fact have snow and have drank way too many Americanos. Thank you for bringing adventure
into my life and always supporting me, especially in times that I doubted myself. Thank you
for always making me a part of your life, even when we were 3,500km away from eachother.
This journey would not have been the same without you, especially with your graphing skills
and ggplot.
To my brothers, Steffan and Nicholas, thank you for being part of my foundation. Your
words of advice and support has meant the world, and I am deeply grateful to have brothers
like you. Finally, to my Mom and Dad, a while ago a friend asked me “what is the one thing
you are most grateful for from your parents growing up”? To this question, I simply
responded “they were always there” - a fact that remains true to this day. There are not
enough words to describe how thankful I am to the both of you. I grew up showered by your
love, comforted by your words and motivated by your lives. Thank you for being the most
incredible parents.
Thank you everyone for making this journey one of the most incredible life experiences.
viii
Table of Contents
Abstract ............................................................................................................................... ii
Summary for Lay Audience ............................................................................................... iv
Co-Authorship Statement.................................................................................................... v
Acknowledgments.............................................................................................................. vi
Table of Contents ............................................................................................................. viii
List of Tables ..................................................................................................................... xi
List of Figures ................................................................................................................... xii
Chapter 1 ............................................................................................................................. 1
1 Introduction .................................................................................................................... 1
1.1 Overall Purpose ....................................................................................................... 7
1.2 Chapter 2 Purpose ................................................................................................... 8
1.3 Chapter 3 Purpose ................................................................................................... 8
1.4 Chapter 4 Purpose ................................................................................................... 8
1.5 References ............................................................................................................... 9
Chapter 2 ........................................................................................................................... 17
2 The number of purposeful headers female youth soccer players experience during
games depends on player age but not player position .................................................. 17
2.1 Introduction ........................................................................................................... 18
2.2 Methods................................................................................................................. 20
2.2.1 Participants ................................................................................................ 20
2.2.2 Protocol ..................................................................................................... 20
2.2.3 Data Analysis ............................................................................................ 21
2.3 Results ................................................................................................................... 22
2.4 Discussion ............................................................................................................. 24
2.5 Conclusion ............................................................................................................ 28
ix
2.6 References ............................................................................................................. 29
Chapter 3 ........................................................................................................................... 32
3 Head Impact magnitudes that occur from purposeful soccer heading depend on game
scenario and head impact location ............................................................................... 32
3.1 Introduction ........................................................................................................... 33
3.2 Material and methods ............................................................................................ 35
3.2.1 Participants ................................................................................................ 35
3.2.2 Instrumentation ......................................................................................... 35
3.2.3 Study Protocol ........................................................................................... 36
3.3 Results ................................................................................................................... 37
3.4 Discussion ............................................................................................................. 39
3.5 References ............................................................................................................. 43
Chapter 4 ........................................................................................................................... 47
4 Cumulative soccer heading amplifies the effects of brain activity observed during
concurrent moderate exercise and continuous performance task in female youth soccer
players .......................................................................................................................... 47
4.1 Introduction ........................................................................................................... 48
4.2 Methods................................................................................................................. 49
4.2.1 Participants ................................................................................................ 49
4.2.2 Electroencephalogram recordings ............................................................. 50
4.2.3 Experimental Protocol .............................................................................. 51
4.2.4 Data Analysis ............................................................................................ 52
4.3 Results ................................................................................................................... 53
4.3.1 Continuous performance test .................................................................... 53
4.3.2 Alpha1 ....................................................................................................... 54
4.3.3 Alpha2 ....................................................................................................... 54
4.3.4 Beta1 ......................................................................................................... 56
x
4.3.5 Beta2 ......................................................................................................... 56
4.3.6 Theta ......................................................................................................... 58
4.4 Discussion ............................................................................................................. 58
4.5 Conclusions ........................................................................................................... 61
4.6 References ............................................................................................................. 62
Chapter 5 ........................................................................................................................... 65
5 Discussion .................................................................................................................... 65
5.1 References ............................................................................................................. 71
Curriculum Vitae .............................................................................................................. 74
xi
List of Tables
Table 2.1. Description of Game Scenario. .............................................................................. 21
Table 2.2. Number of headers players performed based on player age and position during a
single 90-minute (U15) and 75-minute soccer game (U13, U14). ......................................... 23
Table 2.3. Headers characterized by head impact location and age. ...................................... 24
Table 2.4. Headers characterized by head impact location and kicking scenario. .................. 24
Table 3.1. Description of game scenario. ............................................................................... 36
Table 3.2. Linear acceleration and rotational velocity resulting from different game scenarios.
................................................................................................................................................. 37
Table 3.3. Linear acceleration and rotational velocity resulting from different head impact
locations. ................................................................................................................................. 38
Table 4.1. Continuous performance test omission errors and commission errors. ................. 53
xii
List of Figures
Figure 4.1 Interaction plot illustrating the spectral power in Alpha1 band between electrode
site and experiment condition (rest and exercise). The points indicate least square means and
error bars represent standard error. Asterisk (*) represents statistically significant differences
between rest and exercise (p < 0.05). ...................................................................................... 55
Figure 4.2 Interaction plot illustrating the spectral power in Alpha2 band between electrode
site and experiment condition (rest and exercise). The points indicate least square means and
error bars represent standard error. Asterisk (*) represents statistically significant differences
between rest and exercise (p < 0.05). ...................................................................................... 56
Figure 4.3 Interaction plot illustrating the spectral power in Beta2 band between electrode
site and experiment condition (rest and exercise). The points indicate least square means and
error bars represent standard error. Asterisk (*) represents statistically significant differences
between rest and exercise (p < 0.05). ...................................................................................... 57
1
Chapter 1
1 Introduction
Mild-traumatic brain injury (mTBI), which includes sport-related concussion, is common
among athletes where up to 3.8 million mTBI injuries related to sport and recreational
activities occur each year.
1,2
Head injury in sport has led to an increasing number of
emergency department visits in Canada
3,4
and across the globe.
1
Furthermore, emerging
evidence has identified that sports related head injury is associated with an increased risk
of developing neurodegenerative diseases including, chronic traumatic encephalopathy
(CTE)
5
and Alzheimer’s disease.
6
These health conditions result in a substantial health
and financial burden to individuals, families and communities, and incurs significant
economic costs to healthcare.
7
The most recent international consensus statement on sport-related concussion defines
concussion as a traumatic brain injury that is caused by biomechanical forces.
8
The
brain’s pathophysiological response to concussion has been described previously in
animal models.
9,10
Following concussion injury, neurological sequalae can include
neuronal depolarization, release of excitatory neurotransmitters, ionic shifts, altered
glucose metabolism and cerebral blood flow as well as impaired axonal function.
11,12
One
of the hallmarks of concussion injury is that the neurological signs and symptoms
associated with injury occur in the absence of macroscopic neuronal damage.
11
Furthermore, concussions are a difficult injury to diagnose, evaluate, and manage as there
is no single clinical or diagnostic test to reliably and immediately identify them.
Clinically, the immediate signs and symptoms of concussion can include confusion,
memory disturbance, dizziness, headache, nausea and visual disturbance.
13
While most
players recover within seven to ten days following concussion, concussion-related
symptoms may last for weeks, months or even persist in some cases.
14,15
These injuries
are particularly worrisome since sport-related concussions may be associated with
second-impact syndrome as well as progressive neurodegenerative diseases later in life.
16
2
Currently, the majority of concussion research has evaluated American football, but such
findings cannot be extrapolated to non-helmeted sports, nor to vulnerable populations.
Several experts advocate for research into sports related head injury, with specific
emphasis on vulnerable populations such as, youths and female athletes.
17
This is
especially important since sport participation is encouraged in an effort to improve
physical health, and also enhance psychological and social health outcomes. Current
clinical evidence demonstrates that youths and females are at a greater risk of sports
related head trauma including concussion and prolonged recovery compared to adult
males.
18–21
An 11-year prospective study in high school sports reveals that female soccer
has the highest concussion rate among female sports, and the second highest overall
concussion rate (0.35 per 1000 athletic exposures) after American football.
18
Furthermore, concussions represent a greater proportion of total injuries in female
athletes, where almost 16% of total sport-related injuries are concussions, while only up
to 11% of total sport-related injuries are concussions for males.
20–22
Nevertheless, there is
still limited data from youth and female populations.
The human brain is a complex system. From birth to early adulthood, the developing
brain undergoes rapid changes in neuronal synapses, myelination,
23
and metabolism.
24,25
While adolescents may indeed have greater capacity for neuroplasticity,
26
the developing
brain has distinct immaturities
27
and may be more vulnerable to head injury.
23
For
example, significant changes in neuronal synapses occur in the developing brain, and
certain brain regions develop at different times.
28
The degree of myelination differs, in
that the amount of myelin increases throughout the brain in later years of development.
Rodent models demonstrate that the pathologies of concussion between myelinated and
unmyelinated fibers are different.
23
Damage to unmyelinated axons may influence the
degree of morbidity associated with head injury and myelination may provide protection
against head injury. Consequently, the less myelinated immature brain of youth athletes
may be more vulnerable to head injury. In addition, youth athletes have an immature
musculoskeletal system, which may influence head injury. For example, cervical strength
as well as head and neck size can influence the magnitude of peak linear and rotational
head accelerations.
29
Compared to adults, youth athletes have less-developed cervical
3
musculature. Accordingly, youth athletes may not be as effective at transferring energy
that is directed at the head throughout the rest of their body, and ultimately increasing
their risk for head injury.
12
Collectively, such differences in brain and musculoskeletal
development between youth and adulthood suggest that the developing brain responds
differently to head injury and may be more vulnerable.
Many researchers investigating head injury in sport conclude that females have a higher
incidence rate of concussion compared to males
30
as well as have more neurological
deficits and delayed symptom resolution.
31,32
A recent study on children and adolescent
concussion-related emergency department visits or physician visits revealed a 5.5 fold
increase in concussion rates from 2003 to 2013.
30
The authors concluded that females had
the greatest increase in concussion rates (6.3-fold increase) compared to males (3.6-fold
increase). Clearly, there is a need to understand heady injury in such populations.
Approximately 4% of the world’s population ( 265 million people) are actively playing
soccer worldwide and many of these players are 18 years of age and younger.
33
Internationally, soccer is one of the fastest growing sports for youths and females; and
while it is associated with various health benefits including improved cardiovascular
fitness,
34
there is risk of head injury, including concussion.
35,36
For example, concussion
is the second most common injury reported in soccer, representing 24% of all injuries
sustained.
37
The incidence of soccer related concussions range between 0.22 to 1.2
concussions per 1000 athletic exposures,
18,21,22,38
and the rate of concussions increases
with increasing player age.
39
Furthermore, soccer is unique in that players are actively
encouraged to use their head to redirect the ball, a technique referred to as purposeful
soccer heading.
20
Purposeful heading in soccer is an integral part of the game, it is a
complex skill, requiring players to develop the ability to judge the trajectory of the ball
and coordinate their body movements accordingly. Purposeful soccer heading presents an
opportunity to understand head injury in youth and females in what is a naturally
occurring environment.
4
Over the last two decades, concerns have also been raised surrounding the potential short-
and long-term neurological complications associated with repetitive head impacts
sustained during sports such as American football, ice hockey and soccer. These
repetitive head impacts are often referred to as subconcussion impacts.
40
While these
subconcussion impacts were initially thought to be harmless, since there are no
immediate signs and symptoms of brain injury, these impacts lead to neurocognitive
impairment over time, even in athletes without a history of concussion.
40
In soccer,
players experience subconcussion head impacts through purposeful soccer heading,
which accounts for the majority of head impacts that players experience.
41
The number
of repetitive head impacts from purposeful soccer heading per playing hour ranges from
1.8 in females to 2.7 in males.
42
Accordingly, a player who heads the ball several times
per game (such as a defender or midfielder) could perform more than 1,000 purposeful
soccer headers over the course of a 15-year playing career regardless of playing level.
While the threshold for acute symptomatic head injury is unknown, a theoretical
threshold of linear acceleration (82g) and rotational acceleration (5900 rad/s
2
) is thought
to have a 50% probability of causing a concussion.
43
Laboratory studies have quantified
both the linear and angular head impact accelerations associated with purposeful soccer
heading.
44–46
One laboratory study reveals that player age does not affect head impact
accelerations at constant ball velocities, but there is a significant difference in head
impact accelerations between males and females.
47
Female soccer players experience
larger linear and rotational head impact accelerations (40.9 ± 13.3 g; 3279 ± 1065 rad/s²)
compared to males (27.6 ± 8.5 g, 2219 ± 823 rad/s²), which may be related to intrinsic
factors such as, neck strength. Nevertheless, these impact magnitudes are much lower
than the theoretical trauma threshold.
43
However, the neurocognitive consequences that
result from purposeful heading in soccer are unknown, but could be associated with
dementia in later life.
48
Currently, there is minimal objective evidence evaluating the frequency and magnitude of
head impacts during youth soccer. Self-report methods for quantifying soccer heading
frequency are cautioned, as recent evidence demonstrates youth players may overestimate
5
heading exposure by up to 51%.
49
In addition, data collected from youth soccer
scrimmages
50
and weekend soccer tournaments
51
reveal that purposeful soccer heading
leads to linear head impact accelerations up to 62.9 g. Head impact magnitudes recorded
using sensors positioned in helmets reveal no specific concussion threshold, but can be
used to predict the likelihood of concussion.
52
Such technology may prove useful to
quantify and evaluate cumulative head impact burden in youth soccer. Still, the majority
of studies that measure on-field head impact accelerations are in collegiate athletes,
41,53–
56
and may not be generalizable to youth populations. For example, one study
demonstrates that the largest head impact accelerations female collegiate soccer players
experience during games occurs from goal kicks and drop kicks.
55
Yet, such data has not
been measured during youth soccer games. While one laboratory study suggests player
age does not influence the resulting head impact magnitudes from purposeful soccer
heading;
47
such conclusions may be different in varying sporting environments such as
practices and games. Other investigations in American football have quantified head
impact characteristics; concluding that player position and impact location are significant
factors in accounting for differences in head impact magnitudes.
57,58
Objective
evaluations of head impact magnitudes such as player position, game scenario, and head
impact location would prove useful in youth soccer age groups to help limit cumulative
head impact burden.
Currently, there is no consensus on whether the cumulative effect of purposeful soccer
heading leads to neurocognitive changes. This may be due to differences in
methodologies, confounding variables, populations, outcome measures, and
neuropsychological testing. Studies reveal no differences in neurocognitive testing
performance or symptomology between low-, moderate-, and high-exposure header
groups,
59
as well as no differences in neuropsychological testing performance,
60
following a 15-minute heading session. Other research has also observed no association
between repetitive soccer heading and decreases in neurocognitive functioning.
45–49
Conversely, other emerging evidence reveals that repetitive soccer heading is associated
with altered brain neurochemistry,
66
biochemical markers of brain tissue damage
67
as
well as structural changes in the brain.
68–70
Short-term effects of purposeful soccer
6
heading are also highlighted in reduced postural control,
71
headache
72
and near point
convergence.
73
Nevertheless, due to inconsistent findings, there is no consensus on
whether repetitive soccer heading should be banned from youth soccer.
74,75
The United States Soccer Federation eliminated purposeful soccer heading in players
under ten years of age and limited heading to only practices in players aged 11 to 13.
76
If
heading restrictions and limitations are implemented in youth soccer, decisions need to be
data-driven that are based on youth soccer players. To determine whether exposing
youths to repetitive head impacts can result in short- and long-term harm and accelerate
neurodegenerative diseases, we need to characterize head impact exposures experienced
by youth players and use reliable measures to assess neurocognitive changes. If we are
able to identify that purposeful soccer heading is a modifiable risk factor of brain injury,
this could help reduce the rate of developing neurodegenerative diseases in the future,
leading to improved public health in the long-term.
Considerable effort has been devoted to advanced neuroimaging techniques and serum
blood markers, to identify diagnosis and prognosis of sports related head trauma.
77–81
However, the associated costs, invasiveness, limited access to equipment as well as
potential risk of harm due to small doses of radiation, reduce their clinical utility.
82
Low
risk, non-invasive tests of brain function such as electroencephalogram (EEG) offer
critical advantages over other imaging techniques to understand repetitive head impact
exposures including, purposeful soccer heading. EEG recordings measure brain activity,
and is cost effective, portable, and accessible to the public and healthcare teams. This
technique positions surface electrodes on the scalp to record the electrical activity
generated by the underlying brain structures.
83
In specific, EEG records synaptic
excitation of the dendrites of pyramidal neurons in the cerebral cortex.
84
EEG captures
brain waves that are categorized into frequency bands including Theta (4.0–7.9 Hz),
Alpha1 (8.0–9.9 Hz), Alpha2 (10.0–12.9 Hz), Beta1 (13.0–17.9 Hz), and Beta2 (18.0–
29.9 Hz).
85,86
Unlike imaging modalities such as fMRI and PET, EEG provides high
temporal resolution.
84
Accordingly, complex patterns of neuronal activity can be recorded
immediately following stimulus administration.
83
EEG is widely used to study the brain
organization of cognitive processes such as perception, memory, and attention.
83
The
7
non-invasive procedure can be applied repeatedly to healthy individuals as well as patient
populations with no risk or harm.
In mTBI research, EEG recordings can successfully evaluate the degree of head injury,
87–
91
and detect subtle abnormalities in brain neurons and networks, even in asymptomatic
athletes.
92
For instance, spectral EEG recordings reveal abnormal brain functioning in
people diagnosed with a concussion that had otherwise cleared clinical testing measures,
such as the Immediate Post-Concussion Assessment and Cognitive Test (ImPACT).
93
Individuals that have normal clinical testing scores with abnormal EEG findings may be
exhibiting some type of compensatory brain mechanism. The cumulative effects of
repetitive soccer heading may show similar EEG findings, in that participants can
successfully perform a neurocognitive task, but only by engaging additional brain
resources to compensate for the inability to produce the necessary power. A continuous
performance task (CPT) requires patients to respond to target stimuli or refrain from
responding to non-target stimuli. The omission and commission errors obtained during
CPTs provide valuable information regarding inattention and impulsivity, respectively.
94
It is expected that brain activity abnormalities will become amplified when the task
requires additional effort, such as moderate exercise. This approach reflects the clinical
experience that exercise can exacerbate concussive symptoms,
8,95
and may highlight
neurophysiologic changes compared to resting conditions. Moderate exercise combined
with EEG data collection has been successfully used to monitor the brain activity in
healthy individuals.
96,97
It is not known whether cumulative head impacts affect how the
brain responds to increases in physiological stress combined with cognitive load, similar
to that seen in concussion.
1.1 Overall Purpose
The overall objective of this thesis is to delineate the relationship between repetitive head
impacts experienced during female youth soccer games and their influence on
electrophysiological functioning both at rest and under physiological stress (exercise).
This was achieved through three research projects involving female youth soccer players
for an entire soccer season and investigated repetitive soccer heading using
8
methodological equipment including, game video analysis, headbands instrumented with
biomechanical sensors, as well as electroencephalogram (EEG) recordings.
1.2 Chapter 2 Purpose
To describe head impacts from players on three competitive female youth soccer age
groups and compare the number of headers that players perform based on player age,
position, and impact location.
1.3 Chapter 3 Purpose
To quantify the linear and angular head impact accelerations that result from purposeful
heading during female youth soccer games, and whether the magnitude of head impact
accelerations differ depending on the game-scenario and head impact location.
1.4 Chapter 4 Purpose
To explore the relationship between cumulative purposeful soccer heading and
electrophysiological brain functioning during a single season of female youth soccer.
9
1.5 References
1. Gaw CE, Zonfrillo MR. Emergency department visits for head trauma in the
United States. BMC Emerg Med 2016; 16: 5.
2. Langlois JA, Rutland-Brown W, Wald MM. The Epidemiology and Impact of
Traumatic Brain Injury: A Brief Overview. J Head Trauma Rehabil 2006; 21:
375–378.
3. McFaull S, Subaskaran J, Branchard B, et al. At-a-Glance – Emergency
department surveillance of injuries and head injuries associated with baseball,
football, soccer and ice hockey, children and youth, ages 5 to 18 years, 2004 to
2014. Health Promot Chronic Dis Prev Can 2016; 36: 13–14.
4. Matveev R, Sergio L, Fraser-Thomas J, et al. Trends in concussions at Ontario
schools prior to and subsequent to the introduction of a concussion policy - an
analysis of the Canadian hospitals injury reporting and prevention program from
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17
Chapter 2
2 The number of purposeful headers female youth soccer
players experience during games depends on player
age but not player position
A version of this manuscript has been published: Harriss A, Johnson AM, Walton DM, et
al. The number of purposeful headers female youth soccer players experience during
games depends on player age but not player position. Sci Med Footb 2019; 3: 109–114.
Doi: 10.1080/24733938.2018.1506591
18
2.1 Introduction
Purposeful soccer heading can account for up to 90% of the head impacts that players
sustain during soccer games.
1,2
Recent work indicates that purposeful soccer heading
does not appear to cause concussions in high school soccer players;
3,4
however, repetitive
heading exposure may lead to subsequent neurological disorders over time.
5
Nevertheless, methodological short comings make findings inconclusive. For example,
one group describes a dose-relationship response between years of professional soccer
participation and risk of developing amyotrophic lateral sclerosis (ALS).
6
However, this
study recruited a small number of participants and no follow-up studies confirm a causal
link.
Neuroimaging studies show that repetitive sub-concussive head impacts may be
associated with abnormal changes in white matter integrity. For instance, soccer players
without a history of concussion demonstrated increases in radial and axial diffusivity in
areas of the brain such as the inferior frontal gyrus, compared to swimmers.
7
This study,
however, did not quantify heading frequency in their sample, and while comparisons can
be made between the control swimmers group, we cannot conclude whether purposeful
soccer heading is responsible for these neural alterations. Other neuroimaging work
reveals increased heading exposure is associated with abnormal white matter
microstructure and poor memory scores in amateur soccer players.
8
This study only
recruited 39 amateur soccer players, with no control group for comparison. Furthermore,
recent work in male soccer players shows alterations in neurophysiological and
neuropsychological indices of cognitive function.
9
Still, heading exposures were
estimated retrospectively by players, and therefore may not accurately represent true
heading exposures.
10
The possible effects of heading are even more concerning for youth
soccer players,
11,12
as their brains are still developing
13
and may be more vulnerable to
the possible neurological effects of repetitive heading.
To fully explore the potential association between purposeful heading and brain health, it
is necessary to evaluate the head impacts (type, direction, number) that players incur over
an entire soccer season rather than a single game or practice. While heading behavior of
19
collegiate players has previously been measured throughout entire soccer seasons,
2,14,15
youth purposeful heading behavior has not been extensively studied. Accordingly, there
is a critical knowledge gap regarding this vulnerable population. Among collegiate soccer
players, the number of headers that players perform during a game varies between
positions.
2,15
As well, collegiate players perform, on average, a greater number of headers
than high school players.
14
These data do not exist for youth age groups. Similarly,
purposeful heading behaviors may vary between different age groups but this potentially
important moderator has yet to be empirically explored.
Furthermore, the quality of heading impact
16
and impulse arising as a function of the
impact velocity of the ball and head
17
are also expected to have an effect on forces
accrued from each individual header. Proper heading technique requires players to
engage their neck musculature as well as meeting the ball with the os frontale (forehead)
rather than the vertex (top of the head).
18
Improper heading technique, such as poor
muscle activation, may lead to greater head impact accelerations.
16,19
Moreover,
depending on soccer ball velocity, the magnitude of each purposeful header varies based
on game scenario such as a throw-in compared to a goal kick.
17
As a result, certain game
scenarios combined with improper heading technique could create even larger head
impact magnitudes. Therefore, it is important to identify whether heading technique
varies across different youth age groups, but also whether heading technique varies based
on game scenario. This information could help inform possible rule revisions for heading
in youth soccer, and may inform coaching and training in the development of proper
heading technique. The purpose of this observational study was to describe purposeful
heading from three competitive youth soccer age groups and compare the number of
purposeful headers a player performs based on player age, position, and impact location.
We hypothesized that there would be differences in head impact location between player
age as well as the game scenario such as drop kicks, goal kicks, and throw-ins.
20
2.2 Methods
2.2.1 Participants
A convenience sample of three elite (Ontario Player Development League – OPDL)
female soccer teams from three different youth age groups in the city of Burlington,
Ontario, Canada [under-13 (U13); under-14 (U14); and under-15 (U15)] were recruited
for this study. Each of the three teams participated in 20 regular season games over a six-
month period. Purposeful heading data were captured for each team as well as the
opposing team for each match. Each team and their opposition consisted of up to 18
players per team, with 11 players per team participating on the field at a time. This study
was part of a larger scale study exploring the associations between header exposure and
brain activity, and some preliminary findings have been previously reported.
10
All players
and their legal parent guardians provided written informed consent prior to participation.
This study protocol was approved by the Health Science Research Ethics Board at the
University of Western Ontario.
2.2.2 Protocol
Game video was recorded and analyzed for all regular season games using a Sony Vixia
HD camera mounted to a telescoping tower (EVS25, Endzone Video Systems, Sealy,
Texas, United States). Each game video was uploaded to a video analysis software
program (dba HUDL, Agile Sports Technologies Inc., Lincoln, Nebraska, United States).
The game videos for each age group were reviewed using this video software tool. We
also used the software tool to identify each purposeful header impact. Headers were
classified according to the team, player, player position, head impact location, and game
scenario by a single rater using a standardized rubric created for this study. Player
positions were defined as: defense, forward, and midfield. Goalies were excluded from
header analysis as they did not perform a single purposeful header. Head impact locations
were classified as: front, side, top of the head, back and face. In addition, the game
scenario for each head impact was classified as: pass, goal kick, drop kick, deflection,
corner kick, throw-in and free kick. Scenarios are described in Table 2.1.
21
Table 2.1. Description of Game Scenario.
2.2.3 Data Analysis
To ensure a single rater was appropriate to review game video, a subset of five soccer
games were reviewed separately by a researcher and a trained expert in soccer. The
interrater reliability of purposeful header impact identification from game videos was
assessed using Cohen’s Kappa. The number of purposeful headers that players performed
during all games are reported descriptively as median, minimum, and maximum. In
addition, purposeful headers for the Burlington U13, U14, and U15 teams were captured
for their entire season, therefore we also report the median number of headers that players
experience throughout an entire soccer season. Each team and their opponent has 10
players (not including goalies) on the field at a given time. The U13 and U14 players
participated in 75-minute soccer games, and U15 players had 90-minute soccer games.
Accordingly, incidence rates were calculated as the quotient between purposeful soccer
heading exposure and total exposure hours.
20
The incidence of purposeful headers are
presented as per 1000 match hours.
To identify predictors of the number of purposeful headers that players performed during
games, a linear mixed effects model was used with player age (U13, U14, U15) and
player position (midfield, forward, defense) entered as fixed effects. It was expected that
some players would be more or less inclined to perform purposeful headers, and also that
Description of scenario
Kick taken from the corner of the field.
Kick made by goalie by dropping the ball from the hands and
kicking it before it touches the ground.
Kick from a stationary ball awarded to one team as a penalty for a
foul by the opposition.
Kick taken from the six-yard box after the ball has gone over the
goal line by the attacking team.
Player throwing the ball in from the sideline.
Ball kicked from the ground into the air during regular game play
Ball being deflected off player before header occurred.
22
the number of purposeful headers within each game may be affected by the unique
combination of players on the field during that time. Therefore, individual differences
and game differences were modelled as random effects. To determine the model-of-best-
fit for the purposeful heading data, four separate models (null hypothesis, age effects
only, position effects only, and age by position interactions) were tested. The null model
consisted of the dependent variable (total number of purposeful headers) predicted only
by error (i.e., the random effects), the age and position effects models tested age and
position as fixed effects within the analysis, and the interaction model added the
intersection of age and position to the prediction equation. In evaluating the goodness-of-
fit among the models, the age and position models were compared with the null model,
while the interaction model was compared with a model in which age and position were
allowed to predict number of purposeful headers without interacting. Differences among
levels of the fixed effect were tested using t-tests, evaluated with a Satterthwaite
approximation of the degrees of freedom.
21
A chi-square test was used to assess the statistical significance of the influence of head
impact location (front, side, top) and age (U13, U14, U15) on purposeful heading, as well
as head impact location and the game scenario where the purposeful header occurred. All
statistical analyses were completed using R (R Core Team, 2017), with mixed effects
models evaluated using the lme4
22
and lmerTest
23
packages. Experiment-wise alpha was
held to 0.05 within all families of comparisons.
2.3 Results
We observed a substantial interrater reliability for the subset of five games that were
scored by two researchers (κ=0.76, 95% CI [0.4 to 1.0]). Accordingly, based on this level
of reliability,
24
all of the remaining videos were evaluated by a single rater. In total, there
were 1,661 purposeful headers captured during the 20-game season. The U13 players
performed 404 purposeful headers, U14 players 589 purposeful headers, and U15 players
668 purposeful headers. None of the players experienced a concussion during games that
resulted from purposeful heading. The median number of purposeful headers experienced
for the entire soccer season of the Burlington teams increased with age: U13 median = 6
23
(range 1 to 42), U14 = 17 (1 to 56), U15 = 23 (4 to 66). The incidence of purposeful
heading was 74.04 (95% CI [73.9, 74.6]) purposeful headers per 1000 match hours.
For all age groups, the median number of purposeful headers experienced during games
was one, and the minimum number of purposeful headers was zero. The maximum
number of purposeful headers performed during a single game by a U13 player was eight,
and nine for both U14 and U15 players. Age had a statistically significant effect on the
number of purposeful headers that a player performs [
2
(2) = 10.33, p = 0.006]. U15
players head the ball more during games compared to U14 [t(360) = 2.13, p = 0.034] and
U13 [t(146) = 3.15, p = 0.001] players.
Player position had no statistically significant effect on the number of purposeful headers
that a player performs [
2
(2) = 3.09, p = 0.21], and the interaction between age and
position had no statistically significant effect on the number of purposeful headers that a
player performed [
2
(4) = 5.48, p = 0.24]. The number of purposeful headers that players
performed during games based on position and age are reported in Table 2.2.
Table 2.2. Number of headers players performed based on player age and position
during a single 90-minute (U15) and 75-minute soccer game (U13, U14).
No purposeful headers occurred at the back of the head (occipital) or face, therefore were
not included in head impact location analysis (Table 2.3). Our results indicated a
statistically significant association between head impact location and age [χ
2
(4) = 10.40,
p = 0.034] (Table 3). There was no significant association between head impact location
and game scenario [χ
2
(12) = 12.02, p = 0.44] (Table 2.4). However, the most frequent
purposeful heading scenarios resulted from long-range passes (42.4%) and throw-ins
(26.7%).
U13
U14
U15
Median
Range
Median
Range
Median
Range
Midfield
1
0 - 8
1
0 – 7
2
0 – 9
Defense
1
0 - 6
1
0 – 9
2
0 – 8
Forward
1
0 - 7
1
0 - 4
1
0 - 4
24
Table 2.3. Headers characterized by head impact location and age.
Table 2.4. Headers characterized by head impact location and kicking scenario.
2.4 Discussion
Relatively little information is known about the heading behaviors and header burden
among different youth age groups. Therefore, the current study followed three
competitive youth soccer teams for an entire soccer season to evaluate purposeful
heading behaviors. Results from this study indicate that the number of purposeful headers
performed by players increases as player age increases. Furthermore, our findings reveal
that the U14 players make contact with the ball using the front of their head less
frequently than expected, and strike the ball with the top of their head more frequently
than expected. In addition, the U13 players make contact with the ball using the side of
their head less frequently than expected. However, there is no significant association
between head impact location and game scenario.
Head Impact Location
Age
Front
Top
Side
Back
Face
U13
271
124
9
0
0
U14
352
209
28
0
0
U15
439
199
30
0
0
Head Impact Location
Game Scenario
Front
Side
Top
Total # of headers
Corner Kick
45
2
17
64
Drop Kick
97
3
52
152
Free Kick
42
3
24
69
Throw In
271
22
151
444
Long Range Kick
453
29
222
704
Goal Kick
42
3
24
69
Deflection
125
8
46
179
25
Youth soccer teams participating in the Ontario Player Development League are limited
to a maximum number of training hours per week. Players on the U13 and U14 teams are
allowed up to 6 hours of training per week, while U15 age groups are allowed up to 7.5
hours of training per week (excluding games and sport sciences related training).
Nevertheless, while the Ontario Player Development league has requirements that players
need to be educated through training on increased heading skills, there are no
requirements to heading limitations/restrictions. Given our findings reveal that players in
all age groups struck the ball with the top of their heads (improper heading) between 30
and 35% of the time, it may be that there should be consideration for improved header
training in youth age groups.
Recent guidelines for limiting and restricting soccer heading have been implemented in
the United States
25
with the intent of reducing concussion risk. This initiative was created
due to the concern that repetitive head impacts could lead to both short-
26
and long
term
27,28
neurological impairments. Youth players may be more vulnerable to the
potential neurological consequences that result from repetitive head impacts due to
ongoing brain development.
29
Consequently, as a precaution, this initiative bans heading
for youth players ten years old and younger, while players between 11-13 years old can
only perform up to 20 headers per week or 30-minutes of heading drills during practice.
Nevertheless, these heading limits are arbitrary. In our study, the maximum number of
purposeful headers that each age group performed during games were greater than
previous work evaluating head impacts during youth soccer tournaments
1
and female
youth soccer scrimmages.
30
These differences may be due to shorter duration of soccer
tournaments and scrimmages compared to regular 90-minute season games.
While previous work has associated cumulative heading with changes in white matter
microstructure,
8
electrophysiological changes,
9
as well as symptoms associated with
concussion,
31
the number of headers experienced by these studies are greater than our
sample. The number of purposeful headers is particularly important since transient
changes in corticomotor inhibition have been measured following 20 consecutive headers
over a ten-minute period;
32
however, these laboratory findings are limited to recreating
game situations in controlled/artificial settings, which lack external validity. Furthermore,
26
in our sample youth players experience a smaller number of purposeful headers, over a
larger amount of time, during games. Consequently, most laboratory studies may not
accurately represent true heading exposures for this age group
19,32
as well as studies that
estimate heading exposures from player self-report.
8,33
The long-term impact of whether
improper heading technique leads to worse neurological sequalae, compared to proper
heading technique is unknown. Our results illuminate realistic heading exposures for
these youth age groups and accordingly, may be helpful to inform laboratory studies
examining the relationship between heading exposure and potential neurological
sequelae. In turn, this will help to develop rules and regulations for youth players based
on youth data rather than relying on findings from controlled laboratory studies or
extrapolating findings from collegiate player data.
In our study sample, 29-35% of purposeful headers experienced by all age groups were
performed with the top of the head. This is concerning because head impact location may
lead to greater head impact accelerations. For instance, one study indicated that during
female youth soccer scrimmage front and side headers result in greater rotational head
accelerations compared to the back of the head.
30
While the authors reported no
differences in magnitude of linear or rotational acceleration between the top and front of
the head, only 47 headers were captured and compared. Furthermore, heading technique
is influenced by both muscle pre-tensing, and head-torso alignment, which can decrease
the magnitude of linear accelerations following heading, but is less consistent for
reducing rotational acceleration.
16
Finally, there are differences in how these skull
accelerations relate to actual brain strains, such that lateral impacts to the head could
result in higher shear stress compared to frontal head impacts.
34
Compared to collegiate female players,
15
our findings demonstrate that youth females
experience less headers during their soccer season, even when participating in a greater
number of season games. Moreover, in contrast to collegiate players,
2,15
the number of
headers that youth players perform do not vary between player positions. In our current
study, the majority of purposeful headers resulted from throw-ins and long-range passes,
which according to previous work results in lower impact magnitudes compared to goal
27
drop kicks and goal kicks.
17
Future studies should quantify these impacts over an entire
youth soccer season using wearable acceleration sensors to quantify head impact
exposures.
There are some limitations to our current findings. Firstly, this study only captures
heading behaviors for female youth soccer players in the Ontario Player Development
League, and therefore we cannot comment on whether other soccer leagues and/or
calibers would show similar purposeful heading exposures. Female soccer players have a
greater rate of concussion compared to male soccer players;
35
however, heading should
be described in male soccer seasons as previous work indicates males head the ball more
frequently than females.
1
It is possible male soccer players engage in more aggressive
play during games compared to females, contributing to their increased purposeful
heading burden. Furthermore, our heading data only includes games and not practices,
therefore we cannot comment on any differences in heading behaviors, nor the number of
purposeful headers, between games and practices. Also, our study only assessed
purposeful headers and did not include unintentional head impacts. Lastly, the low
number of headers per game per player was challenging to analyse using inferential
statistics.
We believe our results provide important information towards data-driven approaches to
help guide decisions regarding heading restrictions in youth soccer. The magnitude of
head impact accelerations in youth soccer have been quantified in some youth age
groups;
1,30
however, the understanding of the cumulative effects of these subconcussive
impacts remains unknown. Therefore, larger-scale, longitudinal studies are needed to
help understand whether there is a relationship between the magnitude of these impacts
and brain health. Such studies will help inform decisions regarding game scenarios
associated with larger head impact accelerations, and drive clinical decisions regarding
possible heading thresholds. While youth players experience fewer head impacts than
collegiate teams, our study shows that purposeful heading in youth soccer is a frequent
and expected part of the game that requires further investigation.
28
2.5 Conclusion
The current study captured purposeful headers from players on three competitive youth
age groups as well as their opposition, and compared the number of purposeful headers
that a player performs based on player age, position, impact location, and game scenario.
We observed that the number of purposeful headers that youth players perform increases
as player age increases; however, proper heading technique, as judged by head impact
location, is not influenced by player age. Furthermore, head impact location is not
influenced based on the game scenario. Although youth players experience fewer
purposeful headers during games, as well as entire soccer seasons, compared to collegiate
players, purposeful heading is a frequent part of youth soccer.
29
2.6 References
1. Chrisman SPD, Mac Donald CL, Friedman S, et al. Head Impact Exposure During
a Weekend Youth Soccer Tournament. J Child Neurol 2016; 31: 971–978.
2. Press JN, Rowson S. Quantifying Head Impact Exposure in Collegiate Women’s
Soccer. Clin J Sport Med 2017; 27: 104–110.
3. Comstock RD, Currie DW, Pierpoint LA, et al. An Evidence-Based Discussion of
Heading the Ball and Concussions in High School Soccer. JAMA Pediatr 2015;
169: 830–837.
4. Kerr ZY, Campbell KR, Fraser MA, et al. Head Impact Locations in U.S. High
School Boys’ and Girls’ Soccer Concussions, 2012/13–2015/16. J Neurotrauma
2019; 36: 2073–2082.
5. Meyer T, Reinsberger C. Do head injuries and headers in football lead to future
brain damage? A discussion lacking appropriate scientific diligence. Sci Med
Footb 2018; 2: 1–2.
6. Chio A. Severely increased risk of amyotrophic lateral sclerosis among Italian
professional football players. Brain 2005; 128: 472–476.
7. Koerte IK, Ertl-Wagner B, Reiser M, et al. White Matter Integrity in the Brains of
Professional Soccer Players Without a Symptomatic Concussion. JAMA 2012; 308:
1859.
8. Lipton ML, Kim N, Zimmerman ME, et al. Soccer Heading Is Associated with
White Matter Microstructural and Cognitive Abnormalities. Radiology 2013; 268:
850–857.
9. Moore RD, Lepine J, Ellemberg D. The independent influence of concussive and
sub-concussive impacts on soccer players’ neurophysiological and
neuropsychological function. Int J Psychophysiol 2017; 112: 22–30.
10. Harriss A, Walton DM, Dickey JP. Direct player observation is needed to
accurately quantify heading frequency in youth soccer. Res Sports Med 2018; 26:
191–198.
11. Tarnutzer AA, Straumann D, Brugger P, et al. Persistent effects of playing football
and associated (subconcussive) head trauma on brain structure and function: a
systematic review of the literature. Br J Sports Med 2017; 51: 1592–1604.
12. Chiampas GT, Kirkendall DT. Point-counterpoint: should heading be restricted in
youth football? Yes, heading should be restricted in youth football. Sci Med Footb
2018; 2: 80–82.
30
13. Toledo E, Lebel A, Becerra L, et al. The young brain and concussion: Imaging as a
biomarker for diagnosis and prognosis. Neurosci Biobehav Rev 2012; 36: 1510–
1531.
14. McCuen E, Svaldi D, Breedlove K, et al. Collegiate women’s soccer players suffer
greater cumulative head impacts than their high school counterparts. J Biomech
2015; 48: 3720–3723.
15. Lynall RC, Clark MD, Grand EE, et al. Head Impact Biomechanics in Women’s
College Soccer. Med Sci Sports Exerc 2016; 48: 1772–1778.
16. Shewchenko N. Heading in football. Part 2: Biomechanics of ball heading and
head response. Br J Sports Med 2005; 39: i26–i32.
17. Caccese JB, Lamond LC, Buckley TA, et al. Reducing purposeful headers from
goal kicks and punts may reduce cumulative exposure to head acceleration. Res
Sports Med 2016; 24: 407–415.
18. Gallant C, Drumheller A, McKelvie SJ. Effect of Improper Soccer Heading on
Serial Reaction Time Task Performance. Curr Psychol 2017; 36: 286–296.
19. Gutierrez GM, Conte C, Lightbourne K. The Relationship between Impact Force,
Neck Strength, and Neurocognitive Performance in Soccer Heading in Adolescent
Females. Pediatr Exerc Sci 2014; 26: 33–40.
20. Knowles SB, Marshall SW, Guskiewicz KM. Issues in estimating risks and rates in
sports injury research. J Athl Train 2006; 41: 207–215.
21. Schaalje GB, McBride JB, Fellingham GW. Adequacy of approximations to
distributions of test statistics in complex mixed linear models. J Agric Biol Environ
Stat 2002; 7: 512–524.
22. Bates D, Mächler M, Bolker B, et al. Fitting Linear Mixed-Effects Models Using
lme4. J Stat Softw; 67. Epub ahead of print 2015. Doi: 10.18637/jss.v067.i01.
23. Kuznetsova A, Brockhoff PB, Christensen RHB. lmerTest Package: Tests in
Linear Mixed Effects Models. J Stat Softw; 82. Epub ahead of print 2017. Doi:
10.18637/jss.v082.i13.
24. McHugh ML. Interrater reliability: the kappa statistic. Biochem Medica 2012; 22:
276–282.
25. USAClubSoccer. Recognize to recover. Implementation guidelines for US soccer
player safety campaign concussion initiatives- heading for youth players. 2016.
26. Bahrami N, Sharma D, Rosenthal S, et al. Subconcussive Head Impact Exposure
and White Matter Tract Changes over a Single Season of Youth Football.
Radiology 2016; 281: 919–926.
31
27. Montenigro PH, Alosco ML, Martin BM, et al. Cumulative Head Impact Exposure
Predicts Later-Life Depression, Apathy, Executive Dysfunction, and Cognitive
Impairment in Former High School and College Football Players. J Neurotrauma
2017; 34: 328–340.
28. Omalu BI, Hamilton RL, Kamboh IM, et al. Chronic traumatic encephalopathy
(CTE) in a National Football League Player: Case report and emerging
medicolegal practice questions. J Forensic Nurs 2010; 6: 40–46.
29. Paus T. Growth of white matter in the adolescent brain: Myelin or axon? Brain
Cogn 2010; 72: 26–35.
30. Hanlon EM, Bir CA. Real-Time Head Acceleration Measurement in Girls’ Youth
Soccer: Med Sci Sports Exerc 2012; 44: 1102–1108.
31. Stewart WF, Kim N, Ifrah CS, et al. Symptoms from repeated intentional and
unintentional head impact in soccer players. Neurology 2017; 88: 901–908.
32. Di Virgilio TG, Hunter A, Wilson L, et al. Evidence for Acute
Electrophysiological and Cognitive Changes Following Routine Soccer Heading.
EBioMedicine 2016; 13: 66–71.
33. Webbe FM, Ochs SR. Recency and Frequency of Soccer Heading Interact to
Decrease Neurocognitive Performance. Appl Neuropsychol 2003; 10: 31–41.
34. Zhang L, Yang KH, King AI. Comparison of Brain Responses Between Frontal
and Lateral Impacts by Finite Element Modeling. J Neurotrauma 2001; 18: 21–30.
35. Marar M, McIlvain NM, Fields SK, et al. Epidemiology of Concussions Among
United States High School Athletes in 20 Sports. Am J Sports Med 2012; 40: 747–
755.
32
Chapter 3
3 Head Impact magnitudes that occur from purposeful
soccer heading depend on game scenario and head
impact location
A version of this manuscript has been published: Harriss A, Johnson AM, Walton DM, et
al. Head impact magnitudes that occur from purposeful soccer heading depend on the
game scenario and head impact location. Musculoskelet Sci Pract 2019; 40: 53–57. doi:
10.1016/j.msksp.2019.01.009
33
3.1 Introduction
The potential for long-term neurological impairment resulting from repetitive head
impacts is a concern for athletes participating in contact and collision sports such as ice
hockey, rugby, and American football.
1,2
Emerging evidence also shows neurocognitive
effects associated with purposeful soccer heading.
3–6
Observational research has
determined that under-14 youth female soccer players can perform up to nine purposeful
headers during a single soccer game, and can accumulate more than 50 purposeful
headers during a soccer season.
7
While the cumulative linear and rotational head impact
accelerations experienced by collegiate players
8
are greater than that of high school
players,
9
the developing brains of younger players
10
may be more vulnerable to
neurological impairments, even at lower head impact accelerations and cumulative loads.
In 2016 the United States Soccer Federation announced the Recognize to Recover
program to limit the number of purposeful headers that youth players perform.
11,12
This
initiative bans heading for players younger than ten years old, and limits the number of
headers that players aged 11-13 can perform during practices. These thresholds for safe
headers were defined through expert consensus rather than empirical evidence, raising
questions as to their appropriateness for preventing neurocognitive problems. Other
leagues have used data-driven models to reduce the incidence of impacts during sport.
13,14
For example, the number of head impacts that collegiate American football players
experience during practices is limited by imposing practices with no equipment, and
enforcing that no tackling occurs during these practices.
15
We cannot create empirically-
derived guidelines for this vulnerable population without such data for youth soccer.
Several studies have quantified the magnitude of head impact accelerations during soccer
games
16–18
though few have fully characterized these head impacts as far as their context
is concerned. For example, one study evaluating female collegiate soccer players
revealed that purposeful headers occurring from common maneuvers such as “shots” and
“clears” result in larger linear head accelerations compared to “passes”;
8
however, it did
not report rotational head accelerations that may be a better predictor of neurological
34
consequences of repetitive head impacts.
19
Most such work has been conducted on adult
collegiate players,
8,9,16,17,20,21
and youth players have been relatively understudied.
22,23
Purposeful headers account for the majority of impacts sustained by female youth soccer
players during scrimmages, and result in large peak linear and rotational accelerations
(4.5 – 62.9 g and 444.8 – 8869.1 rad/s
2
, respectively).
24
Other work has quantified youth
head impacts during weekend soccer tournaments and report similar impact
magnitudes.
22
Youth players have reduced head mass and neck strength, compared to
adults, which may lead to larger head accelerations with impact.
25,26
One group revealed
that female high school soccer players showed moderate, consistent negative correlations
between neck strength (flexion, extension, left lateral flexion, and right lateral flexion)
and resultant linear head acceleration in header drills.
27
Other work indicates greater head
size and neck strength are associated with lower peak linear and rotational
accelerations,
28
while sex and age may not influence head impact accelerations.
29
Cellular, structural, and metabolic changes,
30
as well as neurocognitive outcome
measures such as, verbal learning
31
are also critical components to understanding
impairment that results from heading. Although the number of headers alone is unlikely
to be enough to fully understand the risk of purposeful heading, the game scenario in
which the header occurred may also influence the head impact magnitude. For example,
“drop kicks” and “goal kicks” result in significantly larger head accelerations than
“kicks”.
18
Laboratory,
21
and on-field,
23
studies reveal that head impact location influences the
magnitude of linear and rotational head accelerations that result from purposeful soccer
heading. Accordingly, to fully understand the linear and rotational head accelerations that
result from purposeful heading in youth soccer, game scenario and head impact location
may provide valuable information for developing informed guidelines in youth soccer.
The purpose of this study was to quantify the linear and angular head kinematics that
result from purposeful heading during youth soccer games, and to determine whether the
magnitude of these head impacts are influenced by the game scenario and head impact
35
location. Consistent with previous work
18,21,23,32
it is hypothesized that purposeful headers
occurring from drop kicks will result in the largest linear head accelerations, and that
purposeful headers occurring from corner kicks will result in the largest rotational
velocity. Furthermore, we hypothesize that purposeful headers performed with the top of
the head will result in larger head accelerations compared to the front or side of the head.
3.2 Material and methods
3.2.1 Participants
This observational study recruited a convenience sample of 36 female soccer players (13.4
(SD 0.9) years old, 1.6 (SD 0.1) m, 50.6 (SD 8.7) kg) from three elite youth soccer teams
(U13, U14, U15) participating in the Ontario Player Development League (OPDL). Players
competed in one game per week during their soccer season. Players also participated in
weekly practices; however, these data were not recorded. Written informed consent from
parents and written informed assent from players was obtained prior to participation. This
study was approved by the Health Sciences Research Ethics Board at The University of
Western Ontario.
3.2.2 Instrumentation
Head impacts for each game were recorded using wireless sensors (GForce Tracker
(GFT2), Artaflex Inc., Markham, Ontario, Canada) at the back of the head that were
secured with a headband, similarly to other work.
18,27
The GForce Tracker sensors contains
a tri-axial accelerometer and a tri-axial gyroscope that measure linear acceleration, and
rotational velocity, respectively. The sensors triggered when head impacts exceeded a
linear acceleration of 7 g, as preliminary data measured prior to the soccer season indicated
that purposeful header impacts can be as low as 8 g. The devices recorded 8 ms of data
preceding the threshold and 32 ms of the data following the threshold. Linear accelerations
were sampled at 3000 Hz, and filtered through an onboard analog low-pass filter with a
cutoff frequency of 300 Hz. Rotational velocity was sampled at 800 Hz, and low pass
filtered with a cutoff frequency of 100 Hz. All data were time stamped and stored on the
sensors’ onboard memory. Although some researchers have incorporated a rigid body
36
kinematic transformation to predict the accelerations at the center of mass of the head,
18,29
we report impact measurements based on sensor data, similarly to some other
researchers.
27,33,34
Following each game, head impact data were uploaded to a cloud-based
server. Peak linear acceleration, and peak rotational velocity for each head impact were
extracted for further analysis.
3.2.3 Study Protocol
A total of 60 regular season games (20 games per team) were recorded using a Sony
Vixia HD camera that mounted to a telescoping system (EVS25, Endzone Video
Systems, Sealy, Texas, United States). Game video was uploaded to a video analysis
software program (dba HUDL, Agile Sports Technologies Inc., Lincoln, Nebraska,
United States). An appointed researcher matched each purposeful header from the video
with the associated peak linear acceleration and peak rotational velocity collected from
the sensor. One rater was deemed appropriate for this analysis based on previous work.
7
The appointed researcher also categorized heading events by game scenario (Table 3.1)
as well as head impact location: front, top, back, and side of the head.
Table 3.1. Description of game scenario.
Descriptive statistics for peak linear acceleration and peak rotational velocity are reported
37
as mean and standard deviation. Both linear acceleration and rotational velocity were
evaluated using a linear mixed effects model to test whether the game scenario and head
impact location predicted head impact magnitude resulting from purposeful heading.
Game scenario (pass, shots, free kick, corner, deflection, goal kick, drop kick, throw-in),
and head impact location (top, front, side, back) were entered as fixed effects. Individual
differences and game differences were modelled as random effects. To determine the
model of best fit, four separate models were tested: null hypothesis, game scenario by
head impact location interactions, including their main effects. All statistical analyses
were carried out using R
35
with linear mixed effects models evaluated using lme4
36
and
lmerTest.
37
Effect sizes can be misleading and inaccurate when using linear mixed effect
modelling,
36
and are therefore not reported. Statistical significance was defined using a
threshold of 0.05.
3.3 Results
A total of 434 purposeful headers were identified from video analysis with matching
events recorded with microsensors. Overall, the mean linear head acceleration
experienced by players was 18.8 (SD 10.2) g, and the mean rotational velocity was
1039.0 (SD 571.3) °/s. The majority of purposeful headers occurred from passes in the air
and throw-ins (Table 3.2). On average, purposeful headers that occurred from shots
resulted in the largest linear head acceleration, while corner kicks resulted in the largest
rotational velocity (Table 3.2).
Table 3.2. Linear acceleration and rotational velocity resulting from different game
scenarios.
In terms of head impact location, headers that occurred on the top of the head resulted in
Game Scenario
Frequency (%)
Linear Acceleration (g)
Rotational Velocity (°/s)
Pass in air
179 (41%)
19.74 ± 10.86
1098.29 ± 590.95
Throw In
129 (30%)
17.33 ± 6.67
959.22 ± 488.34
Deflection
43 (10%)
12.55 ± 4.02
793.87 ± 521.58
Punt
35 (8%)
20.40 ± 16.14
1021.34 ± 614.82
Shot
20 (5%)
27.35 ± 13.11
1202.30 ± 497.81
Goal Kick
16 (4%)
20.11 ± 6.88
1206.75 ± 765.43
Corner
12 (2%)
22.92 ± 7.21
1447.42 ± 589.80
38
the largest linear acceleration and rotational velocity (Table 3.3). Most purposeful
headers were performed by players using the front of their head. No purposeful headers
occurred using the back of the head, and therefore this header location was not
considered in the statistical analyses.
Table 3.3. Linear acceleration and rotational velocity resulting from different head
impact locations.
The mixed effects model evaluating linear acceleration revealed that game scenario had a
statistically significant effect on the linear acceleration that resulted from purposeful
headers, compared to the null model [χ
2
(6) = 37.97, p = 0.0001]. Headers that occurred
from passes in the air resulted in larger linear head accelerations as compared to
deflections [t(417.79) = - 3.88, p = 0.0001], and smaller linear head accelerations as
compared to shots [t(426.93) = 3.70, p = 0.002]. There were no other statistically
significant findings for game scenario. Head impact location did not significantly
influence linear head accelerations [χ
2
(2) = 1.81, p = 0.40]. There was a statistically
significant interaction between head impact location and game scenario on linear head
acceleration, since the interaction model fit the data significantly better than the main
effects model [χ
2
(9) = 20.10, p = 0.02]. Drop kicks resulted in significantly larger linear
head accelerations when completed with the top of the head compared to the front of the
head [t(410.26) = 3.34, p = 0.001].
The mixed effects model evaluating rotational velocity indicated that game scenario had a
statistically significant effect on the rotational velocity that resulted from purposeful
headers [χ
2
(6) = 20.84, p = 0.002]. Passes in the air resulted in significantly larger
rotational head velocities compared to deflections [t(419.58) = 3.20, p = 0.001] and
throw-ins [t(425.98) = 2.18, p = 0.03]. Furthermore, the rotational head velocity from
Head Impact
Location
Frequency
Linear
acceleration (g)
Rotational
velocity (°/s)
Front
277
18.35 ± 8.50
951.88 ± 550.52
Top
137
19.69 ± 12.23
1215.44 ± 588.56
Side
20
19.41 ± 14.89
1037.66 ± 469.62
Back
0
n/a
n/a
39
purposeful headers varied significantly between head impact locations
[χ
2
(2) = 18.15, p = 0.0001]. Purposeful headers that occurred at the top of the head
resulted in larger rotational velocities compared to the front of the head [t(429.49) = 4.30,
p = 0.0001]. There was no statistically significant difference in rotational velocity
between purposeful headers that occurred at the front of the head compared to the side of
the head [t(430.35) = 0.54, p = 0.59]. The game scenario did not significantly influence
the rotational head velocity for the different head impact locations [interaction not
statistically significant: χ
2
(9) = 8.89, p = 0.45].
3.4 Discussion
While the United States Soccer Federation implemented heading guidelines with the
intent of reducing youth heading exposure,
11
there is relatively little information about
linear and angular heading kinematics for this age group.
22,23,38
Understanding the
frequency, magnitude and on-field characteristics of purposeful heading will provide
valuable information to soccer federations to develop data-driven models designed to
limit youth cumulative heading exposure. We observed that head impact location affected
head impact magnitudes; purposeful headers occurring on the top of the head result in
larger rotational velocities compared to the front of the head. When considering both
game scenario and head impact location, we found that purposeful headers occurring
from drop kicks completed with the top of the head had the largest linear head
acceleration magnitudes. However, this relationship was not maintained for rotational
head velocity where there was no interaction between game scenario and head impact
location.
The head impact accelerations experienced by the youth soccer players in our study were
comparable to earlier work that quantified purposeful headers during youth soccer
scrimmages
23
and games;
22,38
however, these studies did not categorize headers by the
soccer game scenario. This component of soccer heading is important as we observed that
there were significant differences in impact magnitudes between the various game
scenarios. For example, we observed that purposeful headers occurring from deflections
result in reduced linear head acceleration and rotational head velocity compared to passes
40
in the air. Such differences in head impact magnitude between the various game scenarios
were likely due to varying ball velocities in these situations. For example, controlled
laboratory testing has reveal that headers performed with soccer balls projected at
13.4 m/s result in smaller head impact accelerations compared to 22.4 m/s (30.6 ± 6.2 g
vs. 50.7 ± 7.7 g, respectively).
24
As well, soccer ball velocity is reduced when the ball
bounces from the ground, or off another player (i.e. deflections), which would lead to a
smaller head impact acceleration compared to a pass in the air or goal kick.
One research study suggests that limiting purposeful headers from drop kicks and goal
kicks could help reduce the cumulative load of heading in female collegiate soccer;
18
however, our findings indicate this strategy may not be effective for youth age groups.
Drop kicks and goal kicks occurred infrequently in our study, and therefore do not add
substantially to the cumulative heading load experienced by youth players. Passes in the
air accounted for the greatest proportion (41%) of purposeful headers performed by youth
players, and shots were the only game scenario that resulted in larger head impact
acceleration magnitudes. Passing the ball on the ground, rather than in the air could help
reduce the number of recorded headers in this study sample by as much as 41%.
Previous work also indicates that repetitive long-range headers, can negatively influence
cognitive functions. For example, soccer players who perform a greater number of long-
range headers have slower reaction times on pointing tasks compared to players with
fewer long-range headers.
39
However, other work shows no negative changes in
computerized neurocognitive functioning among both male and female youth soccer
players.
40
It is possible that repetitive exposure to specific purposeful headers, such as
long-range kicks, may be more likely to impair cognitive functioning in youth soccer
players. Accordingly, limiting the number of purposeful headers that youth players
perform from long-range passes in the air could reduce their overall heading exposure.
Previous work has identified differences between head impact location and the magnitude
of head impact accelerations in female youth soccer players.
23
Our findings demonstrate
that purposeful headers performed using the top of the head result in larger rotational
41
velocities compared to the front of the head, while headers performed using the side of
the head did not influence rotational head velocity magnitude compared to the front of the
head. These results indicate that players should be trained to execute proper heading
technique, impacting the ball with the front of their heads, as this reduces the magnitude
of the linear head impact accelerations. In contrast, improper heading technique (i.e.
headers performed with the top of the head) can result in larger rotational velocities as
well as shear forces.
41
These findings support US Soccer’s stance that limiting the overall
head impact exposure in soccer, rather than only concussive impacts, is an important
aspect of policy development and player safety.
12
There are some limitations to the current study that should to be acknowledged. The
impact magnitudes in this paper are based on sensor data rather than predictions for the
head center of mass. This study only quantified head impact accelerations for female
youth soccer players during soccer games, and not practices. This study provides
meaningful data about purposeful heading for a population that is notably absent in head
injury literature; however, we cannot make any comparisons between sexes or different
soccer leagues/calibers. Recent findings suggest that heading may cause greater head
injury in female soccer players compared to males,
42
and accordingly these findings are
pertinent to this at-risk population. The data presents both the linear and angular head
impact kinematics for different game scenarios and head impact locations, but we do not
report head impact exposure per player. A comparison paper presents information on the
different game scenarios and head impact location per player for purposeful headers.
43
Our study only quantified impacts that resulted from purposeful headers, and did not
consider non-header impacts. Non-header impacts occur infrequently compared to
purposeful heading events,
8
and therefore may not substantially contribute to overall head
impact exposure. However, unintentional headers may pose a greater risk of CNS
symptoms than intentional headers.
44
It is important to recognize that non-header
impacts, such as player to player contact, would be a separate focus for rule changes
compared to intentional heading.
Our findings show that purposeful heading in female youth soccer is a common activity,
that occurs from various game scenarios, but predominately passes in the air and throw-
42
ins. While similar impact magnitudes were recorded from each of the various scenarios,
limiting headers from passes in the air could help reduce youth heading exposure by up to
41%. Furthermore, while most headers were performed using the front of the head,
players still use the top of their head for almost one-third of purposeful headers. This is a
concern because the rotational head velocity was larger for headers performed with the
top of the head compared to the front of the head. Coaching strategies should focus on
methods for limiting the number of headers that players perform, perhaps by encouraging
players to avoid heading passes in the air, but also educate players on heading technique
to reduce cumulative heading burden.
43
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13. Black AM, Macpherson AK, Hagel BE, et al. Policy change eliminating body
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Impacts: An Injury Risk Function for Concussion. Ann Biomed Eng 2012; 40: 1–
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a Weekend Youth Soccer Tournament. J Child Neurol 2016; 31: 971–978.
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Soccer. Med Sci Sports Exerc 2012; 44: 1102–1108.
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on S100B, sideline concussion assessments and head impact kinematics. Brain Inj
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Reducing Risk for Concussion in High School Sports. J Prim Prev 2014; 35: 309–
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27. Gutierrez GM, Conte C, Lightbourne K. The Relationship between Impact Force,
Neck Strength, and Neurocognitive Performance in Soccer Heading in Adolescent
Females. Pediatr Exerc Sci 2014; 26: 33–40.
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predict linear and rotational acceleration during purposeful soccer heading. Sports
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acceleration during purposeful soccer heading. Res Sports Med 2018; 26: 64–74.
30. Kawata K, Tierney R, Phillips J, et al. Effect of Repetitive Sub-concussive Head
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31. Janda DH, Bir CA, Cheney AL. An evaluation of the cumulative concussive effect
of soccer heading in the youth population. Inj Control Saf Promot 2002; 9: 25–31.
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The Engineering of Sport 6. New York, NY: Springer New York, pp. 81–86.
33. Muise DP, MacKenzie SJ, Sutherland TM. Frequency and Magnitude of Head
Accelerations in a Canadian Interuniversity Sport Football Team’s Training Camp
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Cognitive Testing. Orthop J Sports Med 2018; 6: 232596711876103.
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lme4. J Stat Softw; 67. Epub ahead of print 2015.
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Linear Mixed Effects Models. J Stat Softw; 82. Epub ahead of print 2017
38. Chrisman SPD, Ebel BE, Stein E, et al. Head Impact Exposure in Youth Soccer
and Variation by Age and Sex. Clin J Sport Med 2019; 29: 3–10.
39. Koerte IK, Nichols E, Tripodis Y, et al. Impaired Cognitive Performance in Youth
Athletes Exposed to Repetitive Head Impacts. J Neurotrauma 2017; 34: 2389–
2395.
40. Kontos AP, Dolese A, Elbin RJ, et al. Relationship of soccer heading to
computerized neurocognitive performance and symptoms among female and male
youth soccer players. Brain Inj 2011; 25: 1234–1241.
46
41. Elkin BS, Gabler LF, Panzer MB, et al. Brain tissue strains vary with head impact
location: A possible explanation for increased concussion risk in struck versus
striking football players. Clin Biomech 2019; 64: 49–57.
42. Rubin TG, Catenaccio E, Fleysher R, et al. MRI-defined White Matter
Microstructural Alteration Associated with Soccer Heading Is More Extensive in
Women than Men. Radiology 2018; 289: 478–486.
43. Harriss A, Johnson AM, Walton DM, et al. The number of purposeful headers
female youth soccer players experience during games depends on player age but
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47
Chapter 4
4 Cumulative soccer heading amplifies the effects of
brain activity observed during concurrent moderate
exercise and continuous performance task in female
youth soccer players
A version of this manuscript has been published: Harriss, A., Johnson, A.M., Thompson,
J., Walton, D.M., Dickey, J.P. Cumulative soccer heading amplifies the effects of brain
activity observed during concurrent moderate exercise and continuous performance task
in female youth soccer players. J Concussion. doi: 10.1177/2059700220912654
48
4.1 Introduction
Most soccer-related head injuries occur from contact with other players;
1
however,
soccer players routinely experience head impacts through purposely heading the ball.
Purposeful soccer heading occurs when players deliberately use their head to direct the
soccer ball. There is concern that cumulative head impacts through purposeful soccer
heading may influence neurological functioning. For example, some studies show that
repetitive head impacts, such as purposeful soccer heading, do not lead to immediate
changes in neuropsychological testing or advanced neuroimaging,
2–4
while other
investigations report adverse sequelae. Using diffusion-tensor imaging, one group
reported that the number of headers a soccer player performed within the last year was
associated with the degree of axonal injury for specific regions of interest.
5
Another study
revealed, elite male soccer players show evidence of increased radial and axial diffusivity
in areas of the brain including the corpus callosum, over the course of a normal season.
6
Similar neuroimaging findings have also been reported in American football players who
experience repetitive head impacts.
7,8
Collectively, these findings indicate that
cumulative head impacts may cause impairments in areas of the brain that are not
explained by a history of a diagnosed concussion.
Electroencephalogram (EEG) recordings reveal abnormal brain functioning in people
diagnosed with a concussion, yet they have normal clinical concussion test scores.
9
Similarly, EEG abnormalities are shown in people diagnosed with a concussion while
performing virtual reality balance and spatial tasks.
10
Taken together, these findings
suggest that some type of compensatory brain mechanism is occurring to achieve what
appears to be normal functioning. A continuous performance test (CPT) presents patients
with stimuli that requires them to respond to target stimuli or refrain from responding to
non-target stimuli. Omission and commission errors during CPTs provide valuable
information regarding inattention and impulsivity, respectively.
11
Omission errors result
when the participant fails to respond to target stimuli, whereas commission errors result
when the participant responds to non-target stimuli.
49
The cumulative effects of purposeful soccer heading may demonstrate EEG abnormalities
that are currently reported in patients diagnosed with a concussion
9,10
in that participants
can successfully perform a CPT by engaging additional brain resources to compensate for
the injured brain areas. It is expected that these abnormalities will become amplified with
additional effort, such as moderate exercise,
12–14
making neurological deficits more
readily identifiable.
Heading is a frequent part of youth soccer,
15
yet this population is understudied. The
youth age period is a sensitive time for the developing brain,
16
potentially rendering this
group more vulnerable to the negative effects of purposeful heading. Still, it is not known
whether purposeful heading can lead to abnormal brain activity during or after a single
soccer season. Accordingly, the purpose of this study was to explore the relationship
between cumulative purposeful soccer heading and electrophysiological brain functioning
during a single season of female youth soccer. We examined female youth soccer players
as they have a higher risk of concussion.
17
This study examined a spectral analysis of
EEG to determine whether youth female soccer players demonstrate spectral changes in
EEG activity at electrode locations Fp1, Fp2, F3, F4, F7, F8, C3, and C4 at rest and
during moderate exercise, while participants completed a CPT. Previous studies show
increases in brain activity as a result of exercise.
18,19
Accordingly, our hypothesis was
that exercise will result in increased EEG activity for each frequency band across all
electrode sites compared to rest. In addition, we hypothesized that these differences
between rest and exercise would be amplified as players experience a greater number of
cumulative purposeful headers.
4.2 Methods
4.2.1 Participants
Twenty-four elite female soccer players from three different youth age groups (under 13,
under 14, and under 15) were recruited for this study. All players were part of the Ontario
Player Development League, and competed in 20 regular season games during a six-
month period. Participants were excluded if they were diagnosed with a concussion
50
during the season or within the previous six months, or if they had a diagnosed learning
disability or any neurological or psychiatric disorders. Participant assent and parent
consent were obtained prior to participation. This study protocol was approved by the
Health Sciences Research Ethics Board at the University of Western Ontario (HSREB#
107948).
4.2.2 Electroencephalogram recordings
In accordance with the International 10-20 system,
20
22 electrodes were positioned on
the participants scalp using a spandex EEG recording cap (Electro-Cap. Eaton, OH, USA:
Electro-Cap, International). Nineteen scalp locations were recorded, and all leads used
linked ears as reference, and AFz as the ground. Impedances at all recording sites were
below10 kΩ. Electroencephalogram recordings were twenty minutes in duration (ten
minute resting, ten minute moderate exercise) and completed using the eVox system
(Evoke Neuroscience, Inc., New York, NY). The system bandwidth defined by post-
processing filters was 1–30 Hz, and the sampling frequency was 250 Hz. Since the
antialiasing filter only attenuated the signals to 20% at 60 Hz (Smith 1997), a 60 Hz
notch filter was employed to further attenuate any potential signal from power mains.
21
Data were recorded to a Dell Latitude E6440 laptop running an i7 processor.
EEG frequencies were divided into the following bands: Theta (4.0 - 7.9 Hz), Alpha1 (8.0
- 9.9 Hz), Alpha2 (10.0 - 12.9 Hz), Beta1 (13.0 - 17.9 Hz), Beta2 (18.0 - 29.9 Hz).
22,23
Female soccer players frequently experience the majority of purposeful soccer headers on
the front and top of the head.
24
Accordingly, we assessed power for each frequency band
at electrode sites at the frontal (Fp1 & Fp2), mid-frontal (F3 & F4), lateral-frontal (F7 &
F8), and central (C3 & C4) locations as these electrodes are preferentially influenced by
neural activity close to these regions, though also affected by neural activity from more
distant areas due to volume conduction. Temporal electrode sites were not assessed due
to excessive contamination with artifact from masseter muscle activation.
Off-line analysis was performed using Evoke Neuroscience’s Report Generator software.
Artifact removal and data filtering were specifically tuned for exercise condition, and
51
were used to process the resting conditions as well. Data were manually inspected and
segments that contained movement artifacts or excessive muscle activity at any electrode
site were eliminated from further analyses. Independent component analysis was used to
detect and correct eye blinks in order to improve signal quality.
4.2.3 Experimental Protocol
Video from each of the 20 matches was recorded using a Sony Vixia HD camera
mounted to a telescoping tower (EVS25, Endzone Video Systems, Sealy, Texas, United
States). The game video was analyzed using a video analysis software tool (dba HUDL,
Agile Sports Technologies Inc., Lincoln, Nebraska, United States) and the number of
headers was recorded by one researcher for all games. Previous research has determined
that one rater is sufficient to reliably record the number of purposeful soccer headers.
15
Participants avoided caffeine and high intensity physical activity on each of the testing
days. EEG testing was conducted at four time points during the soccer season: baseline,
two mid-seasons, and a post-season measure. At baseline, anthropometric data and
concussion history were collected. Participant EEG were recorded at two conditions, rest
and during moderate exercise. During each condition participants completed a CPT,
whereby either target (big circle) or non-target (small circle) stimuli were presented on a
computer monitor at defined time intervals and the participants responded. The
participants were instructed to press a button as quickly as possible when presented with
the target stimuli, and refrained from responding to non-target stimuli. Omission errors
occurred when the participant failed to respond to target stimuli. Commission errors
occurred when the participant responded to non-target stimuli.
For the moderate exercise condition, a cycle ergometer was used to limit movement
artifact.
18
Preferred seat height and handle bar position was consistent across sessions.
Participants selected a cycling cadence that they could maintain throughout the entire ten
minutes. Biking intensity increased each minute throughout the test, based on participant
mass and rpm, similarly to other concussion exercise protocols.
25
The Borg rating of
perceived exertion (RPE) scale
26
was used at the start and end of the rest and exercise
52
condition. This scale is a simple numeric list and participants verbally reported a number
between 6 (no exertion at all) to 20 (maximal exertion) corresponding to their perceived
exertion. Participants rested for up to ten minutes between conditions.
4.2.4 Data Analysis
The mean and range are reported for the number of cumulative purposeful headers at
each testing time-point. Descriptive statistics for participant demographics and RPE
during each condition (rest and exercise) are reported as means and standard deviations.
In order to ensure that the effects of sustained exercise were present, we chose to analyze
the second half of both the exercise and rest conditions, and treated the initial five
minutes as warm-up periods.
Commission and omission errors are reported as median and range as they were not
normally distributed. A Wilcoxon signed-rank test was used to determine the statistical
significance of the differences in commission errors between rest and exercise. The same
analysis was used for omission errors. These analyses were carried out in IBM SPSS
Statistics (version 25). A p-value of < 0.05 was considered statistically significant.
The EEG signals were digitized using a separate 24-bit analog-to-digital converter for
each channel. Power for Theta, Alpha1, Alpha2, Beta1, and Beta2 were considered as
dependent variables. A linear mixed effects model evaluated whether the main effects of
testing time, experimental condition (rest, exercise), and electrode site (Fp1, Fp2, F3, F4,
F7, F8, C3, C4) predicted EEG power for each dependent variable. Testing time,
experimental condition, and electrode site were entered as fixed effects to determine
whether the main effects model predicted EEG power for each dependent variable. This
main effects model was tested against a null model consisting of only subject variance.
Cumulative number of headers was then entered into the main effects model as a random
effect, and this revised model was tested against the original main effects model to
determine whether or not accounting for this source of error significantly improved the
prediction. The interaction (condition by site) was then tested against the main effects
model that included cumulative headers. A p-value < 0.05 was considered significant.
53
4.3 Results
One player sustained a concussion during the soccer season and was excluded from
analysis. The mean age of the remaining 23 participants was 13.1 (SD 0.8) years old,
with a mass of 49.5 (SD 8.6) kg and height of 1.6 (SD 0.1) m. The average cumulative
number of purposeful headers at follow-up was 6.4 (range: 0 - 29), 15.4 (range: 1 - 49),
and 23.5 (range: 6 - 61) at follow-ups one, two and post-season, respectively.
4.3.1 Continuous performance test
At each testing session, all players successfully completed the rest and exercise condition.
Overall, average RPE difference before (6.55 SD 1.02), and after (6.86 SD 1.75) the rest
condition was not statistically significant (p = 0.34). During exercise, participants cycled
at 57.30 (SD 6.31) rpm. RPE statistically significantly increased throughout the exercise
condition (before 6.59 SD 1.30, after 15.7 SD 1.7). Median errors for omission and
commission scores are presented in Table 4.1.
Table 4.1. Continuous performance test omission errors and commission errors.
There was a statistically significant difference between rest and exercise omission scores,
in that omission errors increased during exercise compared to rest at baseline (z = -3.87, p
= 0.001), follow-up 1 (z = -3.56, p = 0.001), follow-up 2 (z= -3.10, p = 0.002), and post-
season (z = -2.26, p = 0.024). Conversely, there were no statistically significant
differences in rest and exercise commission errors at all testing sessions: baseline (z = -
1.18, p = 0.24), follow-up 1 (z = -0.13, p = 0.90), follow-up 2 (z = -0.85, p = 0.40), and
post-season (z = 0.29, p = 0.77). Regardless of experimental condition, all players scored
Condition
Outcome
measure
Baseline
Follow up
1
Follow up
2
Post
Season
Rest (median %,
range)
Omission
0.0 (0.0-
8.57)
0.0 (0.0-
11.43)
2.86 (0.0-
11.43)
0.0 (0.0-
48.57)
Exercise (median
%, range)
Omission
11.43 (0.0-
54.29)
11.43 (0.0-
34.29)
5.71 (0.0-
40.0)
7.41 (0.0-
45.71)
Rest (median %,
range)
Commission
1.63 (0.0-
3.27)
0.41 (0.0-
4.49)
0.0 (0.0-
3.27)
0.41 (0.0-
3.27)
Exercise (median
%, range)
Commission
0.82 (0.0-
4.90)
0.41 (0.0-
7.76)
0.0 (0.0-
4.90)
0.41 (0.0-
2.04)
54
within normal ranges for omission and commission errors, and there was no statistical
evidence that cumulative headers influenced the number of omission and commission
errors. Therefore, cumulative number of headers were not considered in this analysis.
4.3.2 Alpha1
Considering the Alpha1 frequency band, the main effects model (experimental condition,
site, and testing time) were significantly better at predicting EEG power compared to the
null hypothesis [χ
2
(11) = 533.94, p < 0.0001]. When cumulative headers were entered as
a random effect, the main effects model was statistically significantly improved at
predicting EEG power [χ
2
(1) = 84.36, p < 0.0001]. The interaction model (condition by
site) was significantly better at predicting these data compared to the main effects model
[χ
2
(7) = 56.09, p < 0.0001]. Exercise caused EEG power to increase compared to the rest
condition (Figure 4.1). Specifically, a statistically significant difference in EEG power
between rest and exercise was demonstrated at the frontal electrode sites (Fp1: 0.15 μV
2
SE 0.02, t(1205)=7.29, p < 0.0001; Fp2: 0.14 μV
2
, SE 0.02, t(1205)=6.43, p < 0.0001;
F3: 0.08 μV
2
, SE 0.02, t(1205)=3.9, p = 0.0001; F4: 0.07 μV
2
, SE 0.02, t(1205)=3.35,
p = 0.008; F7: 0.14 μV
2
, SE 0.02, t(1205)=6.61, p < 0.001; F8: 0.14 μV
2
, SE 0.02,
t(1205)=6.64, p < 0.001). There were no statistically significant differences at central
electrode sites (C3: 0.03 μV
2
, SE 0.02, t(1205)=1.41, p = 0.16; C4: 0.01 μV
2
, SE 0.02,
t(1205)=0.35, p = 0.72).
4.3.3 Alpha2
Alpha2 power demonstrated that the main effects model (experimental condition, site,
and time) was significantly better at predicting the data than the null model [χ
2
(11) =
461.64, p < 0.0001]. When cumulative headers were entered as a random effect, the main
effects model was significantly better at predicting EEG power [χ
2
(1) = 29.09, p <
0.0001]. The interaction model (condition by site) was significantly better at predicting
EEG power than the main effects [χ
2
(7) = 33.81, p < 0.0001]. Exercise caused EEG
power to increase compared to the rest condition (Figure 4.2). In particular, a statistically
significant difference in EEG power between rest and exercise were demonstrated at the
frontal sites (Fp1: 0.11 μV
2
, SE 0.02, t(1206)=6.37, p < 0.0001; Fp2: 0.10 μV
2
,
55
SE 0.02, t(1206)=5.86, p < 0.0001; F3: 0.08 μV
2
, SE 0.02, t(1206)=4.64, p = 0.0001; F4:
0.08 μV
2
, SE 0.02, t(1206)=4.26, p < 0.001; F7: 0.11 μV
2
, SE 0.02,
t(1206)=6.12, p < 0.0001; F8: 0.11 μV
2
, SE 0.02, t(1206)=6.07, p < 0.0001). There were
no statistically significant differences at central electrode sites (C3: 0.04 μV
2
, SE 0.02,
t(1206)=1.93, p = 0.05; C4: 0.01 μV
2
, SE 0.02, t(1206)=0.52, p = 0.60).
Figure 4.1 Interaction plot illustrating the spectral power in Alpha1 band between
electrode site and experiment condition (rest and exercise). The points indicate least
square means and error bars represent standard error. Asterisk (*) represents statistically
significant differences between rest and exercise (p < 0.05).
56
Figure 4.2 Interaction plot illustrating the spectral power in Alpha2 band between
electrode site and experiment condition (rest and exercise). The points indicate least
square means and error bars represent standard error. Asterisk (*) represents statistically
significant differences between rest and exercise (p < 0.05).
4.3.4 Beta1
Considering the Beta1 power, the main effects (experimental condition, site, and time)
were significantly better at predicting the data than the null hypothesis model [χ
2
(11) =
452.79, p < 0.0001]. The main effects model was significantly better at predicting EEG
power when cumulative number of headers were entered as a random effect [χ
2
(1) =
68.71, p < 0.0001]. The interaction model (condition by site) was not better at predicting
EEG power than the main effects [χ
2
(7) = 2.33, p = 0.93].
4.3.5 Beta2
Considering the Beta2 power, the main effects (experimental condition, site, and time)
were significantly better at predicting the data than the null hypothesis model [χ
2
(11) =
199.25, p < 0.0001]. When cumulative headers were entered as a random effect, the main
57
effects model was significantly better at predicting EEG power [χ
2
(1) = 13.10, p <
0.0001]. The interaction model (condition by site) was significantly better at predicting
EEG power than the main effects [χ
2
(7) = 20.65, p < 0.004]. Exercise caused EEG power
to increase compared to the rest condition (Figure 4.3). A statistically significant
difference in EEG power between rest and exercise were demonstrated at electrode sites
Fp1 ( 0.01 μV
2
, SE 0.02, t(1209)=1.19, p = 0.004), F3 ( 0.07 μV
2
, SE 0.02, t(1209)=4.20,
p < 0.0001), F4 (0.06 μV
2
, SE 0.02, t(1209)=3.87, p < 0.001), F8 (0.05 μV
2
, SE 0.02,
t(1209)=2.89, p = 0.004), C3 (0.08 μV
2
, SE 0.02, t(1209)=4.84, p <0.0001), C4
(0.08 μV
2
, SE 0.02, t(1209)=4.80, p < 0.0001). There were no statistically significant
differences at electrode sites Fp2 (0.01 μV
2
, SE 0.02, t(1209)=0.35, p = 0.72), and F7
(0.03 μV
2
, SE 0.02, t(1209)=1.67, p = 0.10).
Figure 4.3 Interaction plot illustrating the spectral power in Beta2 band between
electrode site and experiment condition (rest and exercise). The points indicate least
square means and error bars represent standard error. Asterisk (*) represents statistically
significant differences between rest and exercise (p < 0.05).
58
4.3.6 Theta
The main effects model (experimental condition, site, and time) were statistically
significant for Theta power [χ
2
(11) = 508.16, p < 0.0001]. When cumulative number of
headers was entered into the model as a random effect, the main effects model was
significantly better at predicting EEG power [χ
2
(1) = 130.91, p < 0.0001]. The interaction
model (condition by site) did not better predict EEG power than the main effects [χ
2
(7) =
13.77, p = 0.06].
4.4 Discussion
This study evaluated changes in neurophysiological functioning at different times over
the course of a female youth soccer season. Consistent with our hypothesis, EEG power
during exercise increased at each frequency band compared to rest. As players
experienced a greater number of cumulative purposeful headers, these differences in EEG
power between conditions were amplified, but only for Alpha1 and Alpha2 power at all
electrode locations, but C3 and C4 as well as Beta2 for all electrode locations, but Fp2
and F7.
Similar to previous work,
10
our CPT outcome measures suggest normal functioning,
while EEG recordings reveal that the exercise condition had increased Alpha as well as
Beta2 power compared to rest. Notably, players that experienced a greater number of
cumulative purposeful headers showed a statistically significant increase in Alpha and
Beta2 when engaged in moderate exercise. Since the same effect was not seen at rest,
these findings suggest that moderate exercise can amplify differences in cortical
functioning and may serve as a more sensitive test of impairment in Alpha1, Alpha2 and
Beta2 functioning. Although there were statistically significant main effects, none of the
interaction models for the remaining frequency bands were better at predicting EEG
power. Continuous performance task findings revealed a statistically significant increase
in omission errors during exercise compared to rest. This is consistent with previous
work, in that error rates increased with exercise intensity
27,28
. We did not observe any
59
statistically significant changes in commission errors between conditions, suggesting no
impulsivity or hyperactivity behaviors during the CPT.
Previous work has used exercise to evaluate concussion injury as well as recovery.
12–14
However, we are unaware of any studies that have examined the effects of cumulative
header impacts on brain function when measured during moderate exercise. Previous
work has shown EEG activity appears to increase during and after exercise in otherwise
healthy people.
18
Our findings revealed statistically significant increases in Alpha1,
Alpha2 and Beta2 power between rest and exercise. This difference was amplified when
cumulative purposeful headers were incorporated into the model as a covariate. The
impact of brain injury on alpha power has received much attention due to its possible
association with several brain processes, such as its inhibitory control mechanisms.
Following mild traumatic brain injury (mTBI), one study showed alpha power
suppression during balance tasks pre- and post-mTBI injury.
30
Other work has shown
neurophysiological abnormalities in concussed athletes compared to controls including
decreased whole brain beta and theta power during EEG baseline testing, as well as
reductions in frontal beta power during ImPACT testing that achieved a similar level of
performance on clinical tests.
10
These findings suggest that patients with mTBI injuries
utilize compensatory neural processes - adaptive strategies and altered brain resources to
successfully perform required tasks. It is possible that our findings indicate such
compensatory mechanisms.
In collegiate soccer players, there is accumulating evidence indicating a possible
association between repetitive head impacts and abnormal changes in neural functioning
31
and structure.
32
However, in youth soccer players, findings from neuropsychological
testing batteries have not observed neurocognitive impairment immediately following
soccer heading,
3
a weekend soccer tournament,
2
or one month of soccer participation.
33
The lack of findings for neuropsychological testing have been purported to be due to
compensatory processes that allow for normal overt behavior function in spite of altered
neurological processes. Our findings show that cumulative purposeful soccer heading
may be associated with negative changes in neurological function and processes, in
60
female youth soccer players, as indicated by increased alpha power. The novel aspect of
this study is that we have demonstrated that measures of EEG power during exercise have
the potential to inform researchers and clinicians, such as physiotherapists, of possible
cognitive deficits, even at the subclinical level. This information may help provide the
opportunity for early intervention remediation for individuals that do not show clinical
symptoms.
There are some limitations to our study that should be considered. This study only
recorded purposeful soccer headers during games and did not consider practices or non-
header impacts (such as head to ground). Purposeful soccer heading has become a health
concern,
5
particularly for youth players.
34
In addition, we only evaluated female youth
soccer players. Youth male soccer players perform a greater number of headers compared
to youth female soccer players during games
35
and practices.
36
Still, female youth soccer
players experience a greater number of concussions as well as larger peak linear and
rotational header accelerations compared to males.
37
Our study only reported omission
and commission errors. We did not report reaction time as it can be challenging when
working with special populations.
27
We only reported EEG from anterior sites due to
their role in early deployment of cognitive processes, specifically the top-down
processes.
38
Recent imaging work also reveals abnormal findings in the anterior region
of the brain related to soccer heading such as, frontal temporal atrophy.
32
However, this
study did not assess temporal electrode sites such as, T3, T4, T5, T6 due to contamination
from masseter muscle activation, particularly during exercise. Accordingly, it is not
known whether EEG activity would show meaningful differences in the temporal region,
as well as other locations of the brain, such as the posterior region.
While the majority of studies evaluating cumulative soccer heading assessed participants
at rest, we explored the effects of cumulative soccer heading during moderate exercise.
Omission and commission errors obtained during the CPT reveal that participants at rest
are able to achieve normal clinical testing scores; however, increasing task complexity
(exercise) reveals statistically significant increases in omission error scores. In addition,
EEG recordings show that moderate exercise leads to significant increases in alpha
61
activity compared to rest, and that cumulative number of headers amplified this
difference. This suggests that players that experience a greater number of cumulative
headers throughout the season produce increased alpha power during exercise. We
believe that this increased alpha power reflects a compensatory mechanism in that by
engaging additional brain resources, participants can successfully perform a continuous
performance test.
4.5 Conclusions
The implications of cumulative soccer heading on brain function in youth soccer players
are unknown and understudied. Our findings show that neuropsychological outcome
measures (such as omission and commission errors) may show normal cognitive
functioning, but that EEG recordings during moderate exercise show sub-clinical
neurocognitive dysfunction related to cumulative soccer heading. This study evaluated
female youth soccer players for one season of play, and it is not known whether males, or
other ages, or duration of study, or soccer calibers, will show similar findings. While
omission and commission error scores were within normal clinical scores, measuring
EEG recordings during exercise may reveal sub-clinical impairments resulting from
cumulative soccer heading.
62
4.6 References
1. Pickett W. Head injuries in youth soccer players presenting to the emergency
department * Commentary. Br J Sports Med 2005; 39: 226–231.
2. Chrisman SPD, Mac Donald CL, Friedman S, et al. Head Impact Exposure During
a Weekend Youth Soccer Tournament. J Child Neurol 2016; 31: 971–978.
3. Gutierrez GM, Conte C, Lightbourne K. The Relationship between Impact Force,
Neck Strength, and Neurocognitive Performance in Soccer Heading in Adolescent
Females. Pediatr Exerc Sci 2014; 26: 33–40.
4. Kaminski TW, Wikstrom AM, Gutierrez GM, et al. Purposeful heading during a
season does not influence cognitive function or balance in female soccer players. J
Clin Exp Neuropsychol 2007; 29: 742–751.
5. Lipton ML, Kim N, Zimmerman ME, et al. Soccer Heading Is Associated with
White Matter Microstructural and Cognitive Abnormalities. Radiology 2013; 268:
850–857.
6. Koerte IK, Ertl-Wagner B, Reiser M, et al. White Matter Integrity in the Brains of
Professional Soccer Players Without a Symptomatic Concussion. JAMA 2012; 308:
1859.
7. Breedlove EL, Robinson M, Talavage TM, et al. Biomechanical correlates of
symptomatic and asymptomatic neurophysiological impairment in high school
football. J Biomech 2012; 45: 1265–1272.
8. Poole VN, Breedlove EL, Shenk TE, et al. Sub-Concussive Hit Characteristics
Predict Deviant Brain Metabolism in Football Athletes. Dev Neuropsychol 2015;
40: 12–17.
9. Munia TTK, Haider A, Schneider C, et al. A Novel EEG Based Spectral Analysis
of Persistent Brain Function Alteration in Athletes with Concussion History. Sci
Rep 2017; 7: 17221.
10. Teel EF, Ray WJ, Geronimo AM, et al. Residual alterations of brain electrical
activity in clinically asymptomatic concussed individuals: An EEG study. Clin
Neurophysiol 2014; 125: 703–707.
11. Leark RA, Greenberg LM, Kindschi CL, Dupuy TR, et al. The TOVA Company.
Test of variables of attention continuous performance test. 2007.
12. Hilz MJ, DeFina PA, Anders S, et al. Frequency Analysis Unveils Cardiac
Autonomic Dysfunction after Mild Traumatic Brain Injury. J Neurotrauma 2011;
28: 1727–1738.
63
13. Gall B, Parkhouse W, Goodman D. Heart Rate Variability of Recently Concussed
Athletes at Rest and Exercise: Med Sci Sports Exerc 2004; 36: 1269–1274.
14. Woehrle E, Harriss AB, Abbott KC, et al. Concussion in Adolescents Impairs
Heart Rate Response to Brief Handgrip Exercise: Clin J Sport Med 2018; 1.
15. Harriss A, Walton DM, Dickey JP. Direct player observation is needed to
accurately quantify heading frequency in youth soccer. Res Sports Med 2018; 26:
191–198.
16. Paus T. Growth of white matter in the adolescent brain: Myelin or axon? Brain
Cogn 2010; 72: 26–35.
17. Kerr ZY, Cortes N, Caswell AM, et al. Concussion Rates in U.S. Middle School
Athletes, 2015–2016 School Year. Am J Prev Med 2017; 53: 914–918.
18. Bailey SP, Hall EE, Folger SE, et al. Changes in EEG during graded exercise on a
recumbent cycle ergometer. J Sports Sci Med 2008; 7: 505–511.
19. Gutmann B, Mierau A, Hülsdünker T, et al. Effects of Physical Exercise on
Individual Resting State EEG Alpha Peak Frequency. Neural Plast 2015; 2015: 1–
6.
20. Jasper HA. The Ten-Twenty System of the International Federation.
Electroencephalogr Clin Neurophysiol 1958; 10: 371–375.
21. Smith SW. The scientist and engineer’s guide to digital signal processing. San
Diego, Calif.: California Technical Pub., 1999.
22. Harada H, Shiraishi K, Kato T, et al. Coherence analysis of EEG changes during
odour stimulation in humans. J Laryngol Otol 1996; 110: 652–656.
23. Mazzotti DR, Guindalini C, Moraes WA dos S, et al. Human longevity is
associated with regular sleep patterns, maintenance of slow wave sleep, and
favorable lipid profile. Front Aging Neurosci; 6. Epub ahead of print 24 June 2014.
24. Harriss A, Johnson AM, Walton DM, et al. The number of purposeful headers
female youth soccer players experience during games depends on player age but
not player position. Sci Med Footb 2019; 3: 109–114.
25. Leddy JJ, Willer B. Use of Graded Exercise Testing in Concussion and Return-to-
Activity Management. Curr Sports Med Rep 2013; 12: 370–376.
26. Williams N. The Borg Rating of Perceived Exertion (RPE) scale. Occup Med
2017; 67: 404–405.
27. Shalev N, Humphreys G, Demeyere N. Manipulating perceptual parameters in a
continuous performance task. Behav Res Methods 2018; 50: 380–391.
64
28. Labelle V, Bosquet L, Mekary S, et al. Decline in executive control during acute
bouts of exercise as a function of exercise intensity and fitness level. Brain Cogn
2013; 81: 10–17.
29. Klimesch W. EEG alpha and theta oscillations reflect cognitive and memory
performance: a review and analysis. Brain Res Rev 1999; 29: 169–195.
30. Slobounov S, Sebastianelli W, Hallett M. Residual brain dysfunction observed one
year post-mild traumatic brain injury: Combined EEG and balance study. Clin
Neurophysiol 2012; 123: 1755–1761.
31. Moore RD, Lepine J, Ellemberg D. The independent influence of concussive and
sub-concussive impacts on soccer players’ neurophysiological and
neuropsychological function. Int J Psychophysiol 2017; 112: 22–30.
32. Adams J, Adler CM, Jarvis K, et al. Evidence of Anterior Temporal Atrophy in
College-Level Soccer Players: Clin J Sport Med 2007; 17: 304–306.
33. Chrisman SPD, Ebel BE, Stein E, et al. Head Impact Exposure in Youth Soccer
and Variation by Age and Sex. Clin J Sport Med 2019; 29: 3–10.
34. Comstock RD, Currie DW, Pierpoint LA, et al. An Evidence-Based Discussion of
Heading the Ball and Concussions in High School Soccer. JAMA Pediatr 2015;
169: 830–837.
35. Janda DH, Bir CA, Cheney AL. An evaluation of the cumulative concussive effect
of soccer heading in the youth population. Inj Control Saf Promot 2002; 9: 25–31.
36. Kontos AP, Dolese A, Elbin RJ, et al. Relationship of soccer heading to
computerized neurocognitive performance and symptoms among female and male
youth soccer players. Brain Inj 2011; 25: 1234–1241.
37. Caccese JB, Buckley TA, Tierney RT, et al. Sex and age differences in head
acceleration during purposeful soccer heading. Res Sports Med 2018; 26: 64–74.
38. Polich J. Updating P300: An integrative theory of P3a and P3b. Clin Neurophysiol
2007; 118: 2128–2148.
65
Chapter 5
5 Discussion
This thesis characterizes purposeful soccer headers that female youth players experience
throughout a season of soccer, and the associated head impact magnitudes. We also
investigated whether the cumulative head impact burden experienced by female youth
soccer players leads to changes in brain function during combined exercise and cognitive
load. The findings of this thesis reveal statistically significant differences in the number
of headers performed among the different youth age groups, which were not significantly
different between the different player positions. Interestingly, both linear head
acceleration and rotational head velocity vary significantly between head impact location
as well as game scenario. Finally, players who experience a greater number of headers
throughout their soccer season demonstrate increased brain activity for Alpha1, Alpha2,
and Beta2 during combined exercise and cognitive load.
The total number of headers that a player experienced during a single soccer game in this
thesis was greater compared to youth soccer scrimmages
1
and weekend tournaments.
2
In
contrast, another group evaluating heading exposures during soccer games for players
between nine and fifteen years of age, revealed that players experience on average 1.64
headers per game.
3
This is greater than the median number of headers recorded in this
thesis. The duration of playing time in regular season games is longer compared to
playing time in scrimmages and tournaments, which may explain these differences in
heading exposures. Furthermore, this thesis identified that player age is related to the
number of headers a player performs. This is consistent with previous work in youth
soccer, which demonstrates a trend between increasing number of headers and increasing
player age.
3,4
Compared to collegiate findings,
5
collegiate players experience a greater
number of purposeful soccer headers compared to our study sample. Interestingly, in
terms of player position, while mean values for heading exposure indicate that the
midfielders head the ball more often in our study sample, these findings were not
statistically different compared to the other player positions. These findings were similar
to one epidemiological study evaluating youth heading exposures.
3
66
The biomechanical sensor data revealed that the mean linear head acceleration and mean
rotational head velocity experienced by female youth soccer players is 18.8 (SD 10.2) g,
and 1039.0 (SD 571.3)/s, respectively. The linear head accelerations measured in this
study are smaller than linear head accelerations reported in controlled laboratory
scenarios. For example, the mean linear head impact accelerations that result from
purposeful soccer heading in youth players is 38.5 (SD13.6) g when soccer balls are
projected at 11.2 m/s.
6
Another laboratory study demonstrated that soccer balls projected
at 13.4 m/s and 22.4 m/s result in head impact accelerations of 30.6 (SD 6.2) g and
50.7 (SD 7.7)g.
7
It is possible laboratory studies do not accurately reflect head impact
magnitudes that occur during regular soccer games, as games scenarios and head impact
location can result in varying ball velocities.
On field analysis among youth age groups demonstrate comparable head impact
magnitudes to our current findings.
1,2
In contrast, one study measuring head impacts over
a one-month period reported median linear head accelerations in females of 47.4 g and
males of 33.3 g,
4
which are larger compared to the findings reported in this thesis. The
variability in head impact magnitudes across these studies may be due to the use of
different biomechanical sensors and methodological protocols. For instance, the high
triggering threshold for one study
4
(15 g) means that they did not measure lower head
impact magnitudes. It is recommended that head impact data should use a 10 g impact
threshold,
8
and accordingly the 15 g impact threshold would overestimate mean linear
head accelerations. When comparing our biomechanical sensor data to collegiate players,
youth athletes experience similar
5
or possibly smaller linear head impact magnitudes.
9,10
In addition, this thesis identified that purposeful headers from shots result in the largest
linear head accelerations, while purposeful headers that occurred from corner kicks result
in the largest rotational head velocities. These findings are different compared to
collegiate data. For example, larger linear head accelerations and rotational head
accelerations occur from goal kicks and drop kicks during collegiate soccer games.
11
Another study indicates that shots and clears result in larger linear head accelerations
67
compared to passes;
10
however, this study did not measure rotational head velocity.
Furthermore, our results indicate that all players, regardless of age, will perform incorrect
heading technique. This is concerning since improper heading technique (top of the head)
was related to greater linear head accelerations and rotational head velocities compared to
proper heading technique (front of the head). These findings have also been observed in
soccer scrimmages.
1
It is possible that youth soccer players may not be as proficient with
judging soccer ball trajectory in the various game scenarios or are unable to coordinate
the necessary body movements to successfully head the ball with proper technique. This
skill is something coaches can educate players to help them acquire the necessary
techniques for tracking the soccer ball in flight and appropriately coordinating their
actions.
In healthy individuals, EEG can be used to track the increases in cortical activity that
accompany exercise. For example, increases in EEG power are revealed in the frontal
regions during high intensity cycling
12
as well as during graded exercise combined with
cognitive load.
13
Our EEG findings revealed statistically significant increases in brain
activity during combined exercise and cognitive load across all frequency bands.
However, when the cumulative number of headers was considered, these differences in
brain activity between conditions were further amplified for the Alpha1, Alpha2, and
Beta2 frequency bands. The amplification of cortical activity in these frequency bands
suggests that a possible compensatory mechanism is occurring to provide the necessary
brain power to successfully complete the task.
In asymptomatic patients recovering from concussion, EEG is able to detect residual
abnormalities that are not shown at rest.
14
The authors demonstrated that the YMCA Bike
protocol significantly increased absolute power for alpha, beta, delta and theta across all
brain regions in the asymptomatic concussion group, compared to controls. Nevertheless,
EEG findings in concussion are inconsistent across studies. Patients diagnosed with a
concussion demonstrate reductions in alpha
15–17
and beta power.
15,18,19
Our study did not
identify any statistically significant changes in theta power related to cumulative head
impact burden, which is different from concussed individuals. Some research groups
68
indicate changes in theta frequency bands related to concussion injury; however, the
outcome measures used and direction of effects are not consistent. For example, relative
to baseline or control data, athletes diagnosed with a concussion demonstrate lower theta
power,
14,15,20
increased theta coherence
18
and increased frontotemporal theta power.
21
Still, electroencephalogram findings that evaluate the consequences of repetitive head
impacts as well as concussion vary. These differences are possibly explained due to
different research methodologies, populations, outcome measures, and testing paradigms.
Limitations on purposeful soccer heading were implemented by the US Soccer
Federation.
22
This legislation bans heading for youth players 10 years of age and
younger, while players 11 and 12 years of age may engage in a limited number of headers
per week. Currently, there is little scientific evidence that supports the age-specific
guidelines imposed by the US Soccer Federation. Prevention strategies in other sports
such as American football, have successfully implemented data-driven guidelines to limit
head impact exposure and risk. For example, reducing tackling by regulation of practice
equipment worn by American football players reduces the number and magnitude of
repetitive head impacts players experience.
23
For soccer, a common mechanism of sport-
related concussions occur from aerial challenges related to soccer heading.
24
Furthermore, this thesis demonstrates that the majority of purposeful soccer headers
occur from long-range kicks and throw-ins. Clearly, an emphasis on ball control could
help to minimize aerial challenges as well as the majority of heading scenarios in youth
soccer. Accordingly, this simple coaching strategy could help reduce overall cumulative
head impact burden as well as concussion risk in youth soccer.
Neck strengthening has been proposed as a possible modifiable risk factor to reduce head
impact accelerations and concussion incidence; however, findings are not consistent
across the various studies. One laboratory study reveals that sternocleidomastoid strength
significantly predicts both linear and rotational head impact acceleration, while head
mass significantly predicts rotational head acceleration.
25
Another study had participants
perform eight-weeks of isotonic cervical muscle training, which led to increased neck
girth in females, and increased isometric strength in cervical flexors for males, and
69
cervical extensors for females. However, these improvements in neck strength were not
associated with decreases in head acceleration.
26
The authors concluded that while
participants reveal improvements in neck strength, the neuromuscular changes required to
improve dynamic restraint and reduce head acceleration do not occur.
When we consider limiting or restricting heading exposure, the age of the participants
must be taken into account. The brain is still developing during adolescence, with distinct
immaturities in white matter
27,28
that are more vulnerable to injury. For instance, youths
demonstrate an increased number of unmyelinated axonal tracts that are more suspectable
to damage compared to myelinated axonal tracts.
29
Currently, there are no studies that
empirically investigate the effects of age-dependent restrictions on heading. Clinical
evidence has long demonstrated that the developing brain shows unique responses to
brain injury compared to adults. Accordingly, research regarding repetitive head impacts
in various youth age groups is essential to establishing data-driven guidelines. Future
work should be directed towards understanding age-related differences in response to
repetitive head impact exposure that will aid in such data-driven models to develop age-
relevant clinical management guidelines and identifying risk of brain injury.
There are some limitations that should be considered in this thesis. Firstly, this thesis only
assessed purposeful soccer heading in female youth soccer players. Male soccer players
experience a greater number of head impacts compared to female players, yet female
soccer players sustain larger head impact magnitudes.
4
Accordingly, given such
differences, future studies should investigate sex-related differences in response to
repetitive head impact exposures. Nevertheless, it is not known whether youth males
would show similar EEG findings as demonstrated in this thesis. In addition, due to the
nature of the experimental protocol, movement artifact in the EEG signal may have
occurred, and accordingly, efforts to minimize signal artifacts were taken. For example,
data were manually inspected and segments that contained movement artifacts or
excessive muscle activity at any electrode site were eliminated. In addition, independent
component analysis was used to remove eye blinks similar to previous work.
12
Our
findings are also limited to the frontal electrode regions, and therefore we are unable to
70
comment on other electrodes sites. However, the frontal and temporal lobes appear to be
most vulnerable to concussion injury,
30
and disruption in these areas are associated with
impaired executive function, learning and memory, as well as behavioral changes.
31
Given that the EEG device is portable and more affordable compared to other imaging
modalities (MRI, DTI), the use of EEG to evaluate head injury is expected to increase.
Our EEG results expand on previous work performed on healthy individuals, showing
that combined task and cumulative number of headers are associated with greater neural
activation in the frontal regions. Such findings could be valuable in developing models to
reveal residual neurocognitive deficits associated with repetitive head impacts as well as
in sport-related concussion. Yet, whether a correlation exists between repetitive head
impacts and concussive injury has not been established. Future research should evaluate
the early signs of head injury resulting from cumulative head impact burden across
athletes of different ages and sex.
In conclusion, female youth soccer players experience frequent head impacts during a
season of soccer, and some of these impacts are comparable to those experienced by
collegiate soccer players. Furthermore, the cumulative head impact burden resulting from
purposeful soccer heading is associated with underlying subclinical changes that become
apparent during combined exercise and cognitive load. This thesis identifies that youth
athletes that are exposed to cumulative head impacts exhibit neurocognitive changes, as
indicated by EEG. These results provide evidence for the need of data-driven models to
identify players at risk for brain injury during the soccer season. Such information could
help to establish preventative guidelines through early detection of players at risk for
brain injury.
71
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Curriculum Vitae
Name: Alexandra Harriss
Post-secondary University of Guelph
Education and Guelph, Ontario, Canada
Degrees: 2008 – 2012 BSc
University of Guelph
Guelph, Ontario, Canada
2012-2013 MSc
The University of Western Ontario
London, Ontario, Canada
2018-Present MPT
The University of Western Ontario
London, Ontario, Canada
2015-2020
Honors and Province of Ontario Graduate Scholarship
Awards: 2016-2017, 2017-2018, 2018-2019, 2019-2020
University of Western Ontario Entrance Graduate Scholarship
2016-2017, 2017-2018, 2018-2019, 2019-2020
Ontario Women’s Health Scholars Award
2019-2020
Related Work Teaching Assistant
Experience The University of Western Ontario
January 2017- April 2017
Adolescent Concussion Research Coordinator
The University of Western Ontario
2017-2018
Publications:
1. Harriss A, Johnson A, Thompson J, Walton D, Dickey J. A continuous
performance task during moderate exercise amplifies the effects of cumulative
soccer heading on brain activity in female youth soccer players. Submitted to:
Journal of Concussion. Accepted: Febrary,2020.
2. Manning K, Brooks J, Fischer L, Blackney K, Harriss A, Brown A, Bartha R,
Doherty T, Dickey JP, Jevremovic, T, Barreira C, Fraser D, Holmes J, Dekaban G,
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& Menon R. Structural and functional neuroimaging changes in female rugby
players with and without a history of concussion. Accepted: Neurology, Dec 2019.
3. Harriss A, Johnson A, Walton D, & Dickey JP. (2019). Head impact magnitudes
that occur from purposeful soccer heading depend on the game scenario and head
impact location. Musculoskeletal science and practice, 40, 53-57.
4. Harriss A, Walton DM, & Dickey JP. (2019). The number of purposeful headers
female youth soccer players experience during games depends on player age but
not player position. Science and Medicine in Football, 3(2), 109-114.
5. Harriss A, Abbott K, Humphreys D, Daley M, Moir ME, Woehrle E, Fischer L,
Fraser D, & Shoemaker JK. (2019). Concussion symptoms predictive of adolescent
sport-related concussion injury. Clinical journal of sport medicine: official journal
of the Canadian Academy of Sport Medicine.
6. Harriss A, Walton D, & Dickey JP. (2018). Direct player observation is needed to
accurately quantify heading frequency in youth soccer. Research in sports
medicine, 26(2), 191-198.
7. Woehrle E, Harriss A, Abbott K, Moir ME, Fischer L, Fraser D, & Shoemaker JK.
(2018). Concussion in Adolescents Impairs Heart Rate Response to Brief Handgrip
Exercise. Clinical journal of sport medicine: official journal of the Canadian
Academy of Sport Medicine.
8. Harriss A, & Brown SH. (2015). Effects of changes in muscle activation level and
spine and hip posture on erector spinae fiber orientation. Muscle & nerve, 51(3),
426-433.
9. Lerer A, Nykamp SG, Harriss A, Gibson TW, Koch TG, & Brown SH. (2015).
MRI-based relationships between spine pathology, intervertebral disc
degeneration, and muscle fatty infiltration in chondrodystrophic and non-
chondrodystrophic dogs. The Spine Journal, 15(11), 2433-2439.
Refereed conference proceedings
1. The effects of moderate exercise and cumulative purposeful heading exposure on
electroencephalogram activity in female youth soccer players. ABI, New Orleans,
Louisiana, February 2020.
2. Moderate Exercise Can Be Used to Detect Subclinical Changes in Alpha Activity
Related to Cumulative Soccer Heading. IBIA, Toronto, Ontario, March 2019.
3. Structural and functional neuroimaging changes in female rugby players with and
without a history of concussion. International Society for Magnetic Resonance in
Medicine, Montreal, May 2019.
4. The Impact of Aerobic Exercise Training on Autonomic Function During the
Acute Phase of Adolescent Sport-Related Concussion. Experimental Biology, San
Diego, April 2018
5. Heart Rate and Heart Rate Variability Responses are Similar during Static
Exercise in Healthy Seated Adults and Concussed Supine Adolescents.
Experimental Biology, San Diego, April 2018
6. The Effects of Subconcussive Impacts on Heart Rate Variability in Female Youth
Soccer Players. Experimental Biology, San Diego, April 2018
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7. Investigation of Neural Cardiac Dysregulation Using Brief 30% Isometric
Handgrip Protocol in Adolescents Diagnosed With Concussion. CASEM-AQMS
Sport Medicine Conference, Montreal, June 2017.
8. Comparison of Self-Report Symptom Endorsement Between Acutely Concussed
Adolescents and Healthy, Age-Matched Controls. CASEM-AQMS Sport
Medicine Conference, Montreal, June 2017.
9. Head Accelerations Experienced From Purposeful Heading Are Equivalent to
Non-Header Impacts in Youth Soccer. CASEM-AQMS Sport Medicine
Conference, Montreal, June 2017
Conference contributions (other than in refereed conference proceedings)
Conference Abstracts Accepted as Talks
1. Invited speaker. Everything in Sport: Rowan’s Law Panel. Vaughan, Ontario,
May 2019.
2. Head Impacts in youth soccer: Where do we go from here? Invited Keynote
Speaker: First annual QCAC 2018: Prevention, Awareness, and Support.
Kingston, November 2018.
3. Evaluating head impacts in youth soccer and improving rehabilitation outcomes
with exercise. Invited Speaker: Exercise is Medicine, Spoken Science Speaker
Series. March 2018.
4. Head impacts in youth soccer players: Lessons learned from intensively studying
a season of soccer. Invited Speaker: National Orthopedic Symposium, London
October 2017.
5. Should heading be a part of soccer? Using wearable technology and video
analysis to understand head impacts during a youth soccer season. See the Line,
London, October 2017.
6. Understanding the Relationship Between Head Impact Exposures and Brain
Function in Youth Soccer Players. Ontario Soccer Summit, Trent University,
March 2017.
7. We know that soccer has a high rate of concussions, but how large and numerous
are the head impacts? Exercise is medicine, June 2016.
8. Wraparound field to finite element modeling approach for evaluating
biomechanical responses to head impacts in soccer. Canadian Society of
Biomechanics, August 2018.
Conference Abstracts Accepted as Posters
1. Verification of a protocol to quantify athlete-equipment interface forces: an
evaluation of applied forces from ice hockey goaltender leg pads. Canadian
Society of Biomechanics, August 2018.
2. Autonomic dysregulation in heart rate responses to brief static handgrip exercise
in concussed adolescents. Exercise is Medicine Canada National Student
Conference. Accepted. London, June 2018.
3. Development and verification of a protocol to quantify athlete-equipment
interface forces: an evaluation of applied forces from ice hockey goaltender leg
pads. American Society of Biomechanics, March 2017.
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4. Head Impacts in Youth Soccer are comparable to American Football. Western
Research Forum: Mosiac, Western University, March 10 2017.
5. We know that soccer has a high rate of concussions but how large are these head
impacts? Research on Concussion Spectrum of Disorders, Toronto, January 21
2017.
6. Biomechanical Head Impact Exposures in Youth Soccer and the Relationship to
Cognitive and Brain Function, Canadian Society of Biomechanics, Hamilton, July
22 2016.
7. We know that soccer has a high rate of concussions, but how large and numerous
are the head impacts? Exercise Is Medicine, Western University, June 23 2016.
8. Effects of changes in muscle activation level and spine and hip posture on erector
spinae fiber orientation. World Congress of Biomechanics (Boston, July 2014),
Western University Bone and Joint Conference (Western University, July 2013).
Other contributions: Invited Lectures, Presentations and Knowledge Translation
1. Abstract: “The impact of aerobic exercise training on autonomic function in
adolescent sport-related concussion” selected by the communications committee
mainstream media for the 2018 Experimental Biology meeting (San Diego, 2018).
2. Concussion Research at Western University: Prevention and Improving
Rehabilitation Treatment. Class: Medical Issues in Exercise and Sport (Kin
4437a), University of Western Ontario, London, Professor: Dr. Lisa Fischer
(November 2017)
3. Baseline testing for Western University varsity teams. Fowler Kennedy Sports
Medicine Clinic (September 2017). Dr. Lisa Fischer, London Ontario.
4. Public outreach about sport-related concussions in youth sports and baseline
testing. Fowler Kennedy Sports Medicine Clinic (September 2017). Dr. Lisa
Fischer, London Ontario.
5. Preliminary Findings: Ontario Player Development Head Impact Study
(Distributed to Ontario Soccer Association, and Burlington Youth Soccer Club –
November 2016)
6. Major Impact – study draws much needed attention to female athletes and
concussion risks - Western News (September 2016)
7. Ontario Player Development League: Study Update from Western University
(August 2016)
8. Wearable Technology allows researchers to study ‘real-time’ head impact in
soccer – Western News (June 2016)
9. Study to probe head hits’ impact in girls soccer – London Free Press (June 2016)
10. The OPDL Spotlight Series – Concussion testing (May 2016)
11. Understanding repetitive head impacts in adolescent females. National radio
interviews for CBC News (Edmonton, Victoria, Calgary, Vancouver, Toronto,
Kelowna, White Horse, Regina) (May 2016)
12. Guest Lecturer. Joint biomechanics and methodology for calculating shear and
compression forces during dynamic movements. SCMA*3100, University of
Guelph-Humber (February 2013).