Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome

Abstract

Background:
Persistent Sport-Related Post-Concussion Syndrome is often diagnosed with any type of prolonged PCS symptoms. However, there are not specific diagnostic criteria for PPCS such that misdiagnosis often occurs. Further, the signs and symptoms of PCS overlap with other common illnesses such as depression, anxiety, migraines, ADHD and others. Misdiagnosis may lead to less than efficacious treatment, resulting in prolonged symptoms.

Objective:
This article will review relevant evidence-based literature on PCS, pointing out the lack of a systemic diagnostic framework. It will also provide evidence that highlights the multiple conflicting findings in the literature. This article will posit the BioPsychoSocial framework as the best diagnostic framework for understanding the impact of concussions on the person and to generate individualized and personal interventions.

Methods:
A narrative review of sport concussion-related articles was conducted, after extensive searches of relevant and non-relevant literature by each author, as well as articles recommended by colleagues. Articles varied from American Academy of Neurology Class I to IV for evaluation and critique. Class IV articles were reviewed, as there is much public misconception regarding sport and other concussion treatment that needed identification and discussion.

Results:
Articles reviewed varied by quality of research design and methodology. Multiple symptoms, recovery patterns and rehabilitation treatment approaches are purported in the sport-related concussion literature. Current consensus data as well as the mixed and contradictory findings were explored.

Conclusions:
Persistent Sport-Related Post-Concussion Syndrome is a topic of great interest to both professionals and the general public. There is much misunderstanding about the etiology, causation, diagnostic formulations, symptom presentation, prolonging factors and treatment involved in this syndrome. This article posits an individualized multi-system diagnostic formulation, examining all relevant factors, as generating the best interventions for neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome.

Full text

NeuroRehabilitation 46 (2020) 167–180
DOI:10.3233/NRE-192966
IOS Press
167
Neurorehabilitation of Persistent
Sport-Related Post-Concussion Syndrome
Alanna Condera, Robert Condera,∗and Christopher Friesenb
aCarolina Neuropsychological Service, Raleigh, NC, USA
bNiagara Neuropsychology, Grimsby, Ontario, Canada
Abstract.
BACKGROUND: Persistent Sport-Related Post-Concussion Syndrome is often diagnosed with any type of prolonged PCS
symptoms. However, there are not specific diagnostic criteria for PPCS such that misdiagnosis often occurs. Further, the
signs and symptoms of PCS overlap with other common illnesses such as depression, anxiety, migraines, ADHD and others.
Misdiagnosis may lead to less than efficacious treatment, resulting in prolonged symptoms.
OBJECTIVE: This article will review relevant evidence-based literature on PCS, pointing out the lack of a systemic
diagnostic framework. It will also provide evidence that highlights the multiple conflicting findings in the literature. This
article will posit the BioPsychoSocial framework as the best diagnostic frameworkfor understanding the impact of concussions
on the person and to generate individualized and personal interventions.
METHODS: A narrative review of sport concussion-related articles was conducted, after extensive searches of relevant
and non-relevant literature by each author, as well as articles recommended by colleagues. Articles varied from American
Academy of Neurology Class I to IV for evaluation and critique. Class IV articles were reviewed, as there is much public
misconception regarding sport and other concussion treatment that needed identification and discussion.
RESULTS: Articles reviewed varied by quality of research design and methodology. Multiple symptoms, recovery patterns
and rehabilitation treatment approaches are purported in the sport-related concussion literature. Current consensus data as
well as the mixed and contradictory findings were explored.
CONCLUSIONS: Persistent Sport-Related Post-Concussion Syndrome is a topic of great interest to both professionals
and the general public. There is much misunderstanding about the etiology, causation, diagnostic formulations, symptom
presentation, prolonging factors and treatment involved in this syndrome. This article posits an individualized multi-system
diagnostic formulation, examining all relevant factors, as generating the best interventions for neurorehabilitation of Persistent
Sport-Related Post-Concussion Syndrome.
Keywords: Concussion, sport concussion, mild traumatic brain injury, Post-Concussion Syndrome, biofeedback
1. Introduction
Persistent sport-related concussion (SRC) is
widely discussed both in the academic literature and
popular press. Many academic review papers cite
pre-existing medical and psychosocial factors for
∗Address for correspondence: Robert Conder, Carolina Neu-
ropsychological Service, Raleigh, NC, USA. Tel.: +1 919 859
9040; E-mail: Bconder10@gmail.com.
prolonging what should be a time-limited neuro-
physiological condition. Moreover, while traditional
neuroimaging and clinical biomarkers typically do
not show positive findings, experimental measures
of brain functioning reveal abnormalities for weeks
to months post-injury, even after clinical symptoms
have resolved (Institute of Medicine, 2013). Over
the past two decades, the field of concussion has
progressed from a propensity to under-diagnose con-
cussions and minimize their potential for persistent
ISSN 1053-8135/20/$35.00 © 2020 – IOS Press and the authors. All rights reserved

168 A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome
sequelae, to rapid and global expansions in concus-
sion awareness, detection and formal protocols for
response. In its latest dialectic iteration, there is now
almost paranoia in popular press articles suggesting
that even a minor impact head strike sustained in any
sport, at any age, by any person could potentially
lead to persistent SRC or dire progressive degenera-
tive neurologic illness known under the moniker of
Chronic Traumatic Encephalopathy (CTE). Former
staunch advocates for collision sports and “playing
hard” are now questioning the safety and value of
youth participation in sports with concussion poten-
tial. Within this context, there is a need for frank,
data-driven appraisal and interpretation of extant data
to inform views on factors that influence concus-
sion risk, management and recovery. The two-fold
purpose of this article is to: (a) review the evidence-
based literature that establishes the incidence and
prevalence of sport concussion and examines its
neuropathophysiology, sequelae, and factors influ-
encing risk for protracted recovery; and (b) critically
review established and emerging rehabilitation inter-
ventions for ameliorating persistent symptoms or
deficits resulting from refractory SRC. Given the lim-
ited extent of Class 1 empirical data available, this
article also will evaluate research regarding persis-
tence of SRC and proposed rehabilitation treatment
alternatives which may be promising but currently
lack scientific rigor.
1.1. Definitions of sport concussion and post
concussion syndrome
An updated consensus definition of sport con-
cussion was developed at the 5th International
Conference on Concussion in Sport held in Berlin,
October 2016 (hereafter referred to as the “2016
Berlin Consensus Statement”). This document pro-
vides an international foundation that can help in
establishing reliability of diagnosis across profes-
sional disciplines, sports, and geographic locations.
This lengthy, empirically and clinically-driven con-
sensus statement document should be consulted in
its entirety (McCrory et al, 2017). This document
delineates four core criteria for diagnosing a sport
concussion: (a) a TBI injury induced by biome-
chanical forces including direct or indirect trauma
to the head, face, neck or elsewhere on the body
with an impulsive force transmitted to the head;
(b) rapid onset of short-lived impairment of neuro-
logic function that resolves spontaneously, although
sometimes symptoms evolve over a time period; (c)
negative standard neuroimaging reflecting a func-
tional rather than structural injury and with or without
a loss of consciousness; and (d) resolution of clin-
ical and cognitive features typically following a
sequential course, although in some cases symp-
toms may be prolonged. The accepted etiology of
SRC is that postulated by Giza and Hovda (2001)
of a neurometabolic cascade at a cellular level that
essentially is based on a mismatch between glu-
cose metabolism and hyper-glycolysis and reduced
cerebral blood flow. In a majority of these animal
studies, the metabolic cascade restores to homeosta-
sis in about a seven-day period, with no irreversible
damage at a cellular level in these animal models.
This phenomenon has been extended to humans based
on similar time courses for symptom presentation
and resolution (McCrea, Prichep, Powell, & Chabot,
2010). The 2016 Berlin Consensus in Sport position
paper is useful on a number of fronts, but has yet to
be fully disseminated by medical practitioners and
researchers, even those familiar with the consensus
guidelines promulgated by the previous 2012 Zurich
Consensus Statement (McCrory et al., 2013).
The lack of consistent and reliable diagnostic con-
cussion criteria also has added to confusion and
misdiagnosis of the condition termed Post Concus-
sion Syndrome (PCS). Initially, a symptom course
lasting three months after a diagnosed concussion was
the standard required to meet diagnostic criteria for
PCS. More recently, PCS has problematically been
clinically diagnosed within a matter of days or weeks
based primarily on mechanism of injury and resulting
symptoms. This lack of diagnostic rigor is problem-
atic with regard to tracking prevalence and recovery
patterns, as well as researching PCS subtypes and
response to treatment intervention. The American
Medical Society for Sports Medicine (Harmon et al,
2013) as well as the recent 2016 Berlin Consensus
in Sport Group and other professional organizations’
position papers differ slightly, but shared features
among all diagnostic formulae identify PCS as: (a)
a physical hit or concussive force impact with gener-
ally immediate sequelae; (b) core resulting symptoms
including headaches, balance problems, dizziness,
fatigue, sleep disturbance (either sleeping too little
or too much), noise/light sensitivity, visual changes,
and dysregulated mood; (c) symptom course persist-
ing beyond the expected recovery period of weeks to
months post-injury, (d) with refractory symptoms not
better explained by another etiology or maintained

A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome 169
by secondary factors such as litigation or psychoso-
cial gain. Despite general agreement on these criteria,
there is a dire need for consensus in PCS diagnostic
formulation.
1.2. Prevalence and demographics of sport
concussion injuries
Overall, the CDC estimates 3 to 5 million con-
cussions per year, a majority of which are due to
accidents such as automobile accidents, falls in the
elderly, and 17 percent due to sports (Centers for
Disease Control and Prevention, 2011 & 2013).
Of the estimated 45 million children and adoles-
cents participating in organized or recreational sports
(Ewing & Seefeldt, 2002), an estimated 5 to 10%
receive a SRC with an emergency room presenta-
tion (Gilchrist, Thomas, Xu, McGuire, & Coronado,
2011). An additional 15 million adults participate in
organized recreational sports. These figures are esti-
mates based upon emergency room admissions which
are acknowledged to underestimate prevalence, as
many SRC do not receive medical care, especially
at the level of emergency room presentation. At the
college level of the 450,000 players participating in
all sports, over 160,000 participate in sports iden-
tified as concussion generating (NCAA, 2012). At
the professional level, there are fewer but more elite
athletes participating, with an estimated 1600 play-
ers at some level in the National Football League,
and about the same number in the National Hockey
League. Concussion risk potential from such partici-
pation must be weighed against the well documented
positive gains provided by sports participation
on physical, social and intellectual development
(Rieck, Jackson, Martin, Petrie & Greenleaf, 2013;
Weiss, Kipp & Bolter, 2012) and mental health
(Ahn & Fedewa, 2011).
Breakdown by sport and age indicates that a major-
ity of youth concussions presenting to Emergency
Departments and recorded as part of the surveillance
studies in the United States are from playground and
bicycle accidents. Once organized sports begin in the
US public and private school settings, SRC preva-
lence data follow age and gender demographics for
participation in contact/collision sports. Accordingly,
American football and hockey in males and Soc-
cer (European football), field hockey and volleyball
injuries in females are primary SRC generators in the
high school and collegiate population. At the profes-
sional level, males still dominate American football
while soccer may be equally distributed, with SRC
prevalence following these patterns.
1.3. Typical SRC recovery patterns
The 2016 Berlin Consensus statement cited most
severe SRC symptoms in the first 24–72 hours post-
injury, with a majority of balance, cognitive deficits
and symptoms improving in the first two weeks post-
injury. This typical SRC recovery course parallels
the animal model research of Hovda and Giza cited
above. However, further studies have shown proto-
typical but differing recovery courses based on prior
SRC status, age and gender variables. In response
to such, the Berlin Consensus acknowledged that
“a sizable minority of youth, high school and col-
legiate athletes take much longer than 10 days to
clinically recover and return to sport.” The Con-
sensus statement goes on to state: “At present it is
reasonable to conclude that the large majority of
injured athletes recover, from a clinical perspective,
within the first month of injury.” Development of sub-
acute problems including depression and migraine
headaches and pre-injury history of mental health
problems or migraines were identified in this docu-
ment as risk factors for symptom persistence of more
than a month. Finally, teenage athletes, particularly
of high school age, were identified as being most
vulnerable for a persistent symptom course, with
greater risk for female than male athletes. Consistent
with these consensus statements, Neidecker, Gealt,
Luksch & Weaver (2017) performed a retrospective
medical record analysis of 11 to 18 year-old ath-
letes who sustained first time SRC between 2011 and
2013 and found females remained symptomatic for
longer time periods when compared with male ath-
letes of similar age, regardless of sport played. Other
studies have found that female concussed athletes
generally report a higher number of symptoms than
males, although there are confounding factors noted
in these studies. Research has also examined how
post-injury athlete symptom report varies depending
on gender of the examiner, with data suggesting that
a female examiner may elicit more symptoms than a
male interviewer; whereas male athlete/male exam-
iner dyads may yield the lowest symptom reports
(Frommer, Gurka, Cross, Ingersoll, Comstock, & Sal-
iba, 2011). These athlete-examiner gender dyads may
present a confound when examining gender effects on
concussion severity and recovery.

170 A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome
Nevertheless, the usual recovery course for a sin-
gle, uncomplicated sport concussion in a collegiate or
older athlete usually follows a consistent pattern of
remission of symptoms in both frequency and sever-
ity over a time course extending from 7 to 10 days
to a few weeks. Of course, this assumes that the ath-
lete is following the current recommended treatment
guidelines, which include immediate diagnosis and
removal from sport.
1.4. Prolonged SRC recovery patterns
With regard to prolonged recovery, much research
and clinical activity has focused on examining risk
factors to explain why some athletes have prolonged
sequelae and others do not. As with many aspects of
science, the data is incomplete and sometimes contra-
dictory, but currently is being guided by better studies
on larger groups of concussed athletes (McCrea,
McAllister, Hammeke, Powell, Barr & Kelly, 2009;
Henry, Elbin, Collins, Marchetti & Kontos, 2016;
Collins, Lovell, Leddy, Kozlowski, Fung, Pendergast
& Willer, 2007). This article will examine prolonged
recovery probability across three categories: premor-
bid, comorbid, and postmorbid risk factors.
1.4.1. Premorbid risk factors for prolonged
recovery
Premorbid factors need to be investigated in any
athlete with persistent PCS, as they may add to symp-
tom burden or prolonged symptoms. Most frequently
studied and cited in the Berlin Consensus is a personal
or family history of migraine headaches, especially
in female athletes (Kuczynski et al, 2013). Pre-
existing personal and/or family history of migraines
and/or headaches has been identified as a primary
risk factor for posttraumatic migraines, which can
be especially debilitating for a student-athlete Choe
& Blume, 2016). Concern is noted that the diagnos-
tic formulations of the International Classification
of Headaches be followed and that the practitioner
does not confuse chronic daily headache, tension or
musculoskeletal headache, and migraine headache.
Zasler (2015) and Arnold (2018) should be con-
sulted as expert references for differential headache
classification. More broadly, almost any pre-existing
neurologic vulnerability should be recognized and
examined as a premorbid risk factor, given that a con-
cussion is a neurologic injury at its core. This would
include any sort of early birth complications, seizure
disorder, developmental delay or deviation, or history
of sleep pathology. A history of depression or anxiety
or other psychological disorder in the athlete or in first
degree relatives may be a premorbid risk factor for
prolonged concussion recovery (Broshek, DeMarco
& Freeman, 2015; Hou, Moss-Morris, Peveler, Mogg,
Bradley & Belli, 2012). Corollary to this, concussive
injuries may exacerbate the expression and symptom
burden of a pre-existing condition, such as ADHD,
LD, migraines, depression, anxiety or visual dysfunc-
tion (Conder, 2018). More recent resiliency studies
have identified pre-existing psychological coping
resources of the athlete and his/her family as an
important factor in mitigating the development or
maintenance of symptoms. A person with flexible
and adaptive psychological coping resources and a
family system that is supportive but not symptom-
reinforcing typically is better equipped to handle any
injury, whether neurologic or orthopedic, than is the
athlete without well-developed psychological coping
resources.
1.4.2. Comorbid risk factors for prolonged
recovery
Comorbid factors also can influence PCS severity,
course and recovery. These include active and current
modifying factors such as concurrent psychosocial
stressors within the athlete and/or his or her family
system (Broshek, DeMarco & Freeman, 2015); pres-
ence or loss of support from the athlete’s teammates
and/or peer group; impact of athlete’s injury on team
performance; financial implications; and new-onset
psychosocial responses of the athlete to changes in
their sense of resiliency or control.
1.4.3. Post-morbid risk factors for prolonged
recovery
Post-morbid factors include anything that may
inadvertently prolong the frequency, severity or
persistence of PCS symptoms or recovery. While his-
torically not a factor in the treatment of athletes, now
the specter of litigation has to be considered with
prolonged symptoms if there is a context of gain (Mil-
lis, 2015). Ponsford and Kinsella (1992) followed
Emergency Department admissions from concussion
by etiology and found that over a course of three
months, symptom presentation dropped significantly
for the sports concussion athletes, while those in liti-
gation continued to report a high symptom burden.
To a lesser extent, stressors within a psychosocial
group may prolong symptom burden. Even within
the primary family group, family dynamics in terms

A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome 171
of the meaning of symptoms and their function may
be important to evaluate. For example, a young child
evaluated by one of the authors and followed for
a period of time continued to report a high symp-
tom burden, although almost all objective measures
indicated a return to premorbid baseline. Clinical
investigation of psychosocial factors eventually led
to the child’s candid acknowledgement of worry that
“If I get better, my parents will divorce.” While dra-
matic, this emphasizes the need to look “between
the ears” to the larger nexus of the athlete’s existen-
tial situation (Conder & Conder, 2015a). The astute
clinician should carefully elucidate the above premor-
bid, comorbid, and post-morbid factors which may be
prolonging concussion symptom report or expression
(Iverson, Gardner, Terry, Ponsford, Sills, Broshek &
Solomon, 2017).
1.5. Post concussive syndrome
As discussed above, there is a poignant need for
a clear and consensus-based diagnostic schema for
delineating a syndrome which can be diagnosed reli-
ably across sports and geographic locations (Legome,
2018). Based on the PCS definition offered in a
prior section, its diagnosis de facto predicts the need
for treatment interventions beyond the passive heal-
ing effects of time and physical or cognitive rest
to address refractory PCS symptoms. Predominant
among these symptoms are migraines/headaches;
sleep disturbance (sleeping too much or too little);
mood instability such as anxiety, sadness or irritabil-
ity; balance/vestibular symptoms; oculomotor/vision
symptoms; and neurocognitive problems such as
declines in attention/concentration, memory and pro-
cessing speed. Lumba-Brown et al (2019) reviewed
the efficacy of various PCS rating scales in organiz-
ing symptoms and found a lack of consistency and
comprehensiveness among the scales. Additionally,
Iverson (2006) points out that none of these symp-
toms are unique to PCS, and many may be driven by
psychological etiologies including depression.
Assessment of symptom meaning and mainte-
nance is best done by an experienced clinician
undertaking a diagnostic investigation from the
Bio-Psycho-Social formulation elucidated by many
authors (Conder & Conder, 2015b; Yeates, 2010;
Engel, 1997). A BioPsychoSocial assessment is
a holistic formulation which examines symptoms
and signs at multiple levels, as well as interac-
tion among multiple systems which may prolong
symptoms. It posits that a concussion will begin
with a physiologic event (the concussive injury)
which may trigger secondary biological seque-
lae (headaches, vestibular-oculomotor dysfunction)
especially in those with premorbid vulnerabilities,
with concomitant psychological and psychosocial
factors at any stage likely to impact or mediate symp-
tom expression and maintenance.
Kontos, Sufrinko, Sandel, Emami & Collins (2019)
have postulated six rationally derived categories for
characterizing potential sub-types of post concus-
sive experience. These include: cognitive/fatigue,
oculomotor; vestibular; cervical; migraine; and anx-
iety/mood. The utility of these sub-types is that they
help group symptoms into meaningful clusters and
focus treatment interventions, depending on the pri-
mary area of symptom report. These categories are
not orthogonal and many times symptom clusters may
be overlapping. Nevertheless, this approach has util-
ity for assisting the clinician in marshaling treatment
resources. More research is needed to establish the
empirical validity of these sub-types.
2. Neurorehabilitation and treatment of SRC
2.1. Guiding principles for rehabilitation:
Regulation, resilience and mindfulness
While concussions are primarily assumed to be
a central nervous system etiology, there are parallel
Autonomic Nervous System (ANS) alterations asso-
ciated with the concussive event (Goodman, Vargas,
& Dodick, 2013, Hanna-Pladdy, Berry, Bennett &
Phillips, 2001). These may be generated by brainstem
injury but affect multiple levels of functioning. Other
physiological concussion sequelae can also impact
functioning. For example, research has identified
EEG changes (Thatcher, 2006) and cardiac correlates
including alteration in Heart Rate Variability (HRV)
following concussion (Conder & Conder, 2014; Gall,
Parkhouse & Goodman, 2004; Len, Nearly, Asmund-
son, Goodman, Bjornson & Bhambhani, 2011). All
of these psychophysiological sequelae pinpoint Reg-
ulation as a primary function disrupted by concussion
and amenable to targeted psychological, neuropsy-
chological, or psychophysiological PCS treatment
interventions and rehabilitation.
Resilience is defined as an enduring quality of
proactive adaptation to adversity (Sisto, Vicinanza,
Campanozzi, Ricci, Tartaglini, & Tambone, 2019).
The concept of resilience has been widely studied
in the field of Sport Psychology (Fletcher & Sarkar,

172 A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome
2012), focusing on factors that enhance performance
and protect against or ameliorate negative outcomes
in the face of adverse circumstances such as injury
or poor performance. Just as risk factor analysis tar-
gets athletes with higher likelihood of prolonged
PCS recovery, resilience data can identify protec-
tive factors to reduce symptom burden or promote
coping post-injury. LeUnes (2008) posits a gradient
in physiologic resilience as athletes progress from
recreational to more elite levels, with professional or
elite athletes more invulnerable to potentially career-
ending injuries. Treatment techniques which foster
resilience can be integrated with other rehabilitation
interventions to maximize recovery.
Mindfulness is a new “buzz” word with a very old
basis. Mindfulness as a meditative technique dates
back to the 14th century, emerging from monas-
tic and Buddhist traditions. Mindfulness meditation
endorses observing phenomenon without judging
or reacting. Its focus on accepting and allowing,
rather than trying to actively control, undesirable
experiences and symptoms fosters ANS regulation
by activating the parasympathetic nervous system
critical for rest and recovery functions (Criswell,
2017). In doing so, Mindfulness-based interventions
can have desirable physiological and psychologi-
cal effects which foster resilience in the face of
adversity and enhance treatment response. Currently,
mindfulness is being used not only for every day
psychological enhancement but as part of treat-
ment approaches for stress; chronic illnesses such
as cardiac disease or cancer; and chronic and post-
traumatic headaches or migraines. Inna Khazan at
Harvard Medical School (Khazan, 2013) recom-
mends combining mindfulness meditation techniques
with biofeedback or with HRV in the treatment of
PCS.
2.2. Education as PCS treatment
One of the most benign treatments offered has
been education, provided primarily by means of
hand-outs supplied by Emergency Departments and
healthcare personnel with a background in mild trau-
matic brain injury. Used in isolation, this treatment
approach traditionally has had limited efficacy, as
many concussed athletes may not present to these
facilities and not all primary care physicians were
aware of new guidelines. This challenge has been
admirably addressed over the past 15 years by
efforts from the CDC to widely disseminate free
downloadable, comprehensive educational resources
including the CDC “Heads Up!” Concussion materi-
als (www.cdc.gov/HeadsUp/) geared toward players,
coaches, sports officials, and parents. The Heads Up
materials are particularly suitable for K-12 sports par-
ticipants and are made readily available to coaches,
trainers, emergency rooms, urgent care clinics, sports
medicine centers, physicians and youth sports organi-
zations. With US state legislation mandates regarding
concussion education and management in all 50 states
and the District of Columbia, there is incentive by
schools, trainers and concussion health care providers
to document their own education and training and
that they have taken steps to educate participants and
parents. In the latest iteration, education efforts have
extended to on-line training programs that document
various stakeholders have received and understand
concussion education and/or concussion manage-
ment training.
Collegiate/NCAA and professional sports orga-
nizations have specific SRC training programs for
their healthcare personnel based on the consensus
data from the Zurich and Berlin conferences1. The
National Football League, National Hockey League,
and Major League Soccer also use a neuropsy-
chological concussion evaluation model (Lovell,
2006). Similary, many professional organizations
have developed specific concussion education and
management guidelines for their disciplines, such as
the American Medical Society for Sports Medicine,
the American Academy of Neurology and the
National Association of Athletic Trainers (NATA)
(Echemendia, Giza, & Kutcher, 2015). Of the above,
the NATA position statement is one of the most
comprehensive and pragmatic documents available,
readily implemented across medical and neuropsy-
chological disciplines (Broglio et al., 2014). Overall,
education plays a crucial first step in treatment, as
evidence-based knowledge prompts players, parents
and coaches to quickly recognize and appropriately
manage a concussive injury.
2.3. Cognitive behavior therapy and
psychotherapeutic interventions
Cognitive Behavioral Therapy (CBT) has long rec-
ognized efficacy in the treatment of depression (Beck
& Beck, 2011) and was one of the initial approaches
to be is utilized as a first line treatment for anxiety
and depressive reactions in athletes with refrac-
tory sports concussion (Hou, Moss-Morris, Peveler,
1www.ncaa.org/health-and-safetyconcussion-guidelines

A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome 173
Mogg, Bradley, & Belli, 2012). Using a modified
CBT framework, the first stage in working with the
injured athlete is to educate and alert them to iden-
tify maladaptive cognitions and distortions such as
Overgeneralization and Catastrophizing that either
result from the injury, or prolong recovery by main-
taining symptoms. For example, athletes may see
their concussion and need for supports as a sign of
weakness, may stress that protracted recovery will
transform into a career-ending event, or harbour a
catastrophic fear that they will develop CTE, the
latter not helped by distorted media attention. For
elite athletes reluctant to consider pharmacotherapy,
a modified CBT approach may have the added advan-
tage of symptom control based on procedures that
foster an internal locus of control over the recovery
process and formulation of action plans congruent
with an athlete’s natural preference for self-efficacy
(Feltz, 1984; Beauchamp, Jacksons & Morton, 2012).
Another application of CBT in concussion rehabili-
tation addresses insomnia and parasomnias, as sleep
disturbance is increasingly recognized as prominent
in refractory SRC (Kostyun, Milewski, & Hafeez,
2014). CBT for Insomnia (CBT-I) protocols (Jacobs
et al., 2004) are an alternative for those athletes
who do not like or tolerate the sedating properties
of sleep medication, or have poor sleep hygiene
impacting recovery. CBT-I also could be paired with
pharmacotherapy or relaxation training to potentiate
normalization of sleep.
2.4. Behavioral medicine approaches in SRC
rehabilitation
Behavioral Medicine approaches including train-
ing in relaxation and stress management are readily
used by athletes to optimize sports performance and
manage undesirable post-injury symptoms. In refrac-
tory concussion, athletes respond well to training in
breathing exercises, progressive relaxation, positive
imagery, autogenic phrases and mindfulness medi-
tation (Brown & Gerbang, 2009; Jacobson, 1938;
Norris, Fahrion & Oikawa, 2003) to reduce acute
stress, headaches and autonomic arousal. Many elite
and Olympic athletes know the value of breathing
for enhancing performance and self-regulation and
have worked with various breathing routines (Wil-
son & Cummings, 2011) so they respond well to
yogic or diaphragmatic breathing training. Specific
relaxation and/or hypnotic induction tapes or CDs are
commercially available or can be individually made
by a therapist for the athlete’s specific circumstances
(Schwartz, 2003). The latter tend to be more effective
due to personalization of the athlete’s situation and
needs. These audio files can be made in the office with
the athlete present, then an MP3 file can be given to
the athlete for use outside of the office. Similarly, once
trained in the relaxation response, injured athletes
can implement breathing, imagery and/or meditation
strategies in the naturalistic setting to reduce PCS
symptoms.
2.5. Cognitive rehabilitation
Cognitive rehabilitation (CR) is the use of cogni-
tive techniques to rehabilitate impaired information
processing after a neurologic event such as a concus-
sion, TBI, or CVA (Conder et al., 1988; Conder 1992).
Kreutzer, Conder, Wehman and Morrison (1989)
were early researchers examining the use of cog-
nitive rehabilitation to enhance independent living
and vocational outcome post mTBI. More recently,
Cicerone and colleagues (Cicerone et al., 2011;
Cicerone et al., 2005) have elucidated a cognitive
rehabilitation schema in association with the Ameri-
can Congress of Rehabilitation Medicine. Most often
PCS sequelae include problems with basic atten-
tion and concentration functions. Not only are these
deficits problematic in their own right, but from
an information processing view of cognition, atten-
tion/concentration are the gateways for information
to flow to higher levels of cognitive processing
including memory, problem-solving and executive
functioning. An everyday example of this com-
plex relationship is the injured student-athlete who
experiences trouble attending to detail and maintain-
ing focus upon returning to school or remembering
specific plays on the field, which in turn creates cog-
nitive fatigue and problems remembering reading
assignments, studying effectively or executing plays.
Without CR support, attempts to “gut it out” are likely
to trigger headaches and stress, which in a cyclic
manner further diminish strained attention resources.
In the initial phases of recovery, direct teaching
and practicing of strategies to remediate attention
and working memory is advocated. After the athlete
is symptom free, tolerating computer or screen-
time activities, computerized cognitive rehabilitation
programs targeting specific impaired/altered neu-
rocognitive functions can also be efficacious both in
an office setting and remotely for home use. Helmich
(2010) presents a consensus conference review of
cognitive rehabilitation for military personnel with
refractory PCS and mTBI injuries.

174 A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome
2.6. Academic and work modifications
In conjunction with the cognitive rehabilitation
interventions reviewed above, academic and work
modifications can be critical in addressing persis-
tent post-concussive functional declines in vocational
and educational settings. Most common yet complex
are the problems experienced by injured student-
athletes in the classroom, especially those enrolled in
more demanding academic pursuits such as college
students or high school students taking Advanced
Placement or International Baccalaureate courses.
At the other end of the spectrum, student-athletes
with pre-existing ADHD or learning disabilities often
experience magnified impairments that severely com-
promise post-SRC academic re-entry. Given that
concussions at a neurophysiological level affect the
information-processing capacities of the brain, any
activity dependent upon the integrity of the brain may
be attenuated. Academic settings not only primar-
ily focus on brain-based processes for new learning
consolidation (which are generally harder than post-
injury resumption of routine vocational skills), but
have the added age burden of a population where
brain development is not yet complete at the time
of injury.
Within this context, recent efforts have focused on
Return-to-Learn (RTL) needs of concussed student-
athletes (Halstead, McAvoy, Devorc, Carl, Lee, &
Logan, 2013). Cognitive re-entry is more successful
with tailored supports to address cognitive-academic
functions still recovering at the time of school
re-entry (Conder, 2011). Typical academic mod-
ifications to reduce the compromising impact of
PCS-related declines in attention, memory, pro-
cessing speed, visual tracking/accommodation, or
cognitive stamina include: provision of class notes
and Power-Points; reduced screen time and reading
activities, modified assignments and extended assign-
ment deadlines, more frequent breaks and repetition,
and test modifications (Conder, 2013; Conder, 2018).
A tailored, practical problem-solving approach is
indicated in these situations rather than uniform or
global recommendations that may actually hinder
recovery or add to academic stress. For example,
exemption from all assignments or prolonged medi-
cal leave may be detrimental in a majority of cases,
whereas successful school re-entry benefits from
analysis of which activities for what duration trigger
symptoms or require impaired resources in a particu-
lar student. A recent study by Reiger, Lewandowski,
Potts, and Shea (2019) highlighted the need for inter-
ventions to target anxiety and stress about academic
concerns as an integral part of PCS recovery.
2.7. Biofeedback interventions in SRC
rehabilitation
Biofeedback (BFB) interventions, also known as
psychophysiological intervention, have a long and
efficacious history in the behavioral medicine lit-
erature (Norris et al., 2003; Schwartz & Andrasik,
2016) and in the sports psychology literature (Wil-
son & Cummings, 2011; Blumenstein & Orbach,
2012; Conder & Conder, 2014; Wilson & Somers,
2011). They provide an adjunct treatment for somatic
complaints that have a psychophysiological compo-
nent or provide information that can improve optimal
performance in elite athletes (Beauchamp, Harvey
& Beauchamp, 2012). Traditionally, BFB methods
such as temperature biofeedback in the peripheries,
galvanic skin response/electrodermal response, and
electromyography have been used successfully with
medical conditions such as chronic headaches or
vestibular problems, and psychological conditions
including depression or anxiety. It is unsurprising,
therefore, that these techniques have applicability to
these same complaints presenting in the context of a
refractory PCS process.
A primary advantage of psychophysiological BFB
protocols in post-concussion treatment is their provi-
sion of sensitive, objective physiologic measures of
interest, which can provide data independent of sub-
jective symptom report. There are no true biomarkers
for concussion that are generally accepted. How-
ever, the Institute of Medicine report notes alteration
on numerous neurophysiologic parameters post-
concussion, such as fMRI, DTI, MEG, and Evoked
Potentials. BFB data can be instrumental in objectify-
ing athlete symptom report, identifying dysregulated
systems, and identifying targets for BFB and
psychotherapeutic treatment intervention, with the
ultimate goal of teaching self-regulation. After a
concussion, post-traumatic headaches and cardiovas-
cular changes may cause vasoconstriction leading to
significant alterations in temperature regulation in the
extremities, which can be assessed and intervened
with traditional thermal biofeedback. Muscle con-
traction headaches can be treated effectively with
electromyography BFB measuring tension at the
frontalis and masseter muscle sites. Finally, electro-
dermal response (GSR) is very sensitive to negative
thinking, making it possible to objectively measure
changes in GSR within seconds of a maladaptive

A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome 175
thought or awareness of a stressor (Mann & Janelle,
2012).
2.8. Heart rate variability biofeedback (HRV-B)
An evidence-based form of psychophysiological
biofeedback for sports performance and SRC reha-
bilitation is heart rate variability (HRV) training,
discussed in detail by Conder and Conder, 2014; Tan,
Fink, Dao, Hebert, Farmer, Sanders, A.,. . . Gevirtz,
2009. As noted above, there are cardiac consequences
of a concussion. These most often include reduced
cerebral perfusion with exertion post-concussion
(needed by athletes attempting to perform at their
normal strenuous competitive level). Essentially, the
healthy heart has variability in heart rate, measured by
the R-wave intervals, which may reflect an alteration
between input from the sympathetic and parasym-
pathetic branches of the ANS (Strack & Gevertz,
2011). In cardiopathology, there is reduced vari-
ability between R-waves which reflects illness and
which can predict serious cardiac events. Multi-
ple studies have shown that an athlete’s heart rate
variability is reduced post-concussion (Gall, Park-
house & Goodman, 2004), reflecting ANS changes
driven by the vagus nerve, both at rest and more
importantly at exertion. Post-concussive changes in
cardiac inter-beat variability can be measured with
the traditional biofeedback protocol in the labora-
tory, such as using the protocol of Leddy with the
Buffalo Treadmill Test (Leddy, Haider, & Willer,
2018). This reduction in heart rate variability post-
concussion may have implications for changes in
cardiac demand while performing sports, as well as
reduced cerebrovascular perfusion. Lagos, Thomp-
son, and Vaschillo (2013) modified Lehrer’s heart
rate variability training successfully with concussed
adolescents. In HRV-B training, an athlete learns to
increase variability through respiratory sinus arrhyth-
mia resonant frequency breathing. While the resonant
frequency varies by individual physiology, gender
and age, it is usually between four to seven breaths
per minute (BPM), with six BPM as the modal
rate. Cognitive correlates of heart rate variability
training, especially in the low frequency band, have
shown improvement in complex neurocognitive per-
formance including executive functioning. There are
portable instruments to assess and treat not only heart
rate variability but also temperature and EDR that the
athletes can use in everyday life, including during ath-
letic practice. HRV-B treatment provides an objective
measure of heart-brain connectivity impacting per-
sistent SRC, and preliminary studies by the military
and clinical researchers suggest promising efficacy in
promoting a quicker return to pre-injury status.
3. Conclusions
As noted above, there is a need for reliable and
valid diagnostic schema for identifying concussions
and diagnosing Persisting Post Concussive Syndrome
that can be adopted by all practitioners for all sports
in all geographic regions. This reliable diagnos-
tic formulation would help with understanding and
studying the phenomenon of PCS, perhaps leading
to more effective and focussed treatment. As also
noted and discussed, PCS is not an entity unto itself
and its symptoms are shared with other disorders,
particularly depression and anxiety. Consequently,
a comprehensive differential diagnostic approach
from the Bio-Psycho-Social formulation is needed to
understand not only the degree of biological injury,
but the syndrome’s manifestation based on premorbid
and comorbid psychological factors occurring within
a psychosocial context. These phenomena should be
examined for their role in prolonging presentation of
symptom degree and frequency. Not only is analysis
of secondary gain needed, but also analysis of pri-
mary gain to better understand intrapsychic, social
and family systems factors impacting the PCS pre-
sentation. Unfortunately, the specter of litigation also
must be factored in as a component that can pro-
long symptom presentation. Further, a fundamental
misunderstanding of PCS and concussions, in gen-
eral, is promulgated by the popular media and/or by
persons who may have an interest in prolonging the
symptoms, and are not cognizant of relevant, rapidly
evolving neuroscience literature. Appreciation and
attention to all of these factors can improve concus-
sion management and protect the health and safety of
student-athletes.
Future directions should include further investiga-
tion of objective biomarkers. Evoked Potentials have
been shown to be altered for up to a year in con-
cussed collegiate athletes and may serve as a viable
biomarker (Broglio, 2009). However, not all prac-
titioners may have the availability of equipment to
measure this. A discussion of computerized testing
is out of the scope of this paper but other studies
should be consulted which elucidate the problems
with reliability and validity of such forms of adminis-
tration (Schatz & Maelender, 2013; Maelender et al,
2013; Malerlender et al, 2010). The authors would

176 A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome
generally advocate that computerized testing results
in and of themselves be interpreted cautiously, due
to general problems with reliability. From a philos-
ophy of science perspective, they provide one level
of data to be considered within an overall clinical
formulation undertaken and synthesized by a quali-
fied practitioner in their diagnostic decision-making.
Ultimately, the diagnosis of Persistent Sports Related
Concussion is the burden of a skilled diagnostician,
as inappropriate diagnosis of this syndrome can lead
to symptom burden and morbidity, when not neces-
sary. Going forward and guided by better research
studies, it is hoped that clinicians will be more
inclined to rely on a variety of assessment modalities,
including objective physiological and psychophysio-
logical data in addition to the clinical examination
and neurocognitive assessment, assist in diagnostic
formulation and treatment intervention development
for concussed athletes. While concussive injury is
a physiologic and neurophysiologic entity, persis-
tent sport related concussion should be recognized
as a psychophysiological entity best elucidated using
a BioPsychoSocial diagnostic formulation to guide
diagnostic accuracy and formulate treatment and neu-
rorehabilitation interventions to maximize symptom
remission.
Conflict of interest
All of the authors declare they have no conflict of
interest. No sources of funding nor outside support
was received for this project.
References
Ahn, S., & Fedewa, A. (2011). A meta-analysis of the rela-
tionship between children’s physical activity and mental
health. Journal of Pediatric Psychology, 36(4), 385-97. doi:
10.1093/jpepsy/jsq107
Baillargeon, A., Lassonde, M., Leclerc, S., & Ellemberg,
D. (2012). Neuropsychological and neurophysiological
assessment of sport concussion in children, adoles-
cents and adults. Brain Injury, 26(3), 211-20. doi:
10.3109/02699052.2012.654590
Barr, W. B., Prichep, L. S., Chabot, R., Powell, M. R., & McCrea,
M. (2012). Measuring brain electrical activity to track recovery
from sport-related concussion. Brain Injury, 26(1), 8-66. doi:
10.3109/02699052.2011.608216
Beauchamp, M. K., Harvey, R. H., & Beauchamp, P. H. (2012).
An integrated biofeedback and psychological skills train-
ing program for Canada’s Olympic short-track speedskating
team. Journal of Clinical Sport Psychology, 6(1), 67-84. doi:
10.1123/jcsp.6.1.67
Beck, J. S. (2011). Cognitive Behavior Therapy: Basics and
Beyond (2nd ed). New York, NY: Guilford Press.
Bender, M. C., Martelli, M. F., & Zasler, N. D. (2003). A graduated
exposure protocol for post traumatic sensory disorders. Pre-
sented at the WilliamsburgTraumatic Brain Injury Conference,
27th Annual Meeting, Williamsburg VA.
Bigler, E. D. (2008). Neuropsychology and clinical neuro-
science of persistent post-concussive syndrome. Journal of
the International Neuropsychological Society, 14(1), 1-22.
doi:10.1017/S135561770808017X
Blumenstein, B., & Orbach, I. (2012). The road to Olympic medal.
In Edmonds, W. A, & Tenenbaum, G., (Eds.). Case studies
in applied psychophysiology: Neurofeedback &Biofeedback
treatments for advances in human performance (pp. 120–133).
West Sussex, UK: Wiley-Blackwell.
Broglio, S. P., Cantu, R. C., Gioia, G. A., Guskiewicz, K. M.,
Kutcher, J., Palm, M., & Valovich McLeod, T. C. (2014).
National athletic trainers’ association position statement: Man-
agement of sport concussion. Journal of Athletic Training,
49(2), 245-265. doi: 10.4085/1062-6050-49.1.07
Broglio, S. P., Pontifex, M. B., O’Connor, P., & Hillman, C. H.
(2009). The persistent effects of concussion on neuroelectric
indices of attention. Journal of Neurotrauma, 26(9), 1463-70.
doi:10.1089/neu.2008-0766
Broshek, D. K., De Marco, A. P., & Freeman, J. R. (2015). A
review of post-concussion syndrome and psychological factors
associated with concussion. Brain Injury, 29(2), 228-37. doi:
10.3109/02699052.2014.974674
Broshek, D. K., Kaushik, T., Freeman, J. R., Erlanger, D., Webbe,
F., & Barth, J. T. Sex differences in outcome following sports-
related concussion. Journal of Neurosurgery, 102(5), 856-63.
doi: 10.3171/jns.2005.102.5.0856
Brown, R. P., & Gerbang, P. L. (2009). Yogic breathing and med-
itation: When the thalamus quiets the cortex and rouses the
limbic system. Annals of the New York Academy of Science,
1172, 11-19.
Carroll, L. J., Cassidy, J. D., Peloso, P. M., Borg, J., von Holst,
H., & Holm, L....P´
epin, M. (2004). Prognosis for mild
traumatic brain injury: Results of the WHO Collaborating
Centre Task Force on Mild Traumatic Brain Injury. Jour-
nal of Rehabilitation Medicine. (Suppl. 43), 84-105. doi:
10.1080/16501960410023859
Centers for Disease Control and Prevention. (2011). Nonfatal
traumatic brain injuries related to sports and recre-
ational activities among persons aged<19 years – United
States, 2001–2009. Morbidity and Mortality Weekly Report,
60(39), 1337-42. Retrieved from https://www.cdc.gov/mmwr/
preview/mmwrhtml/mm6039a1.htm
Centers for Disease Control and Prevention. (2013). Injury pre-
vention and control: Traumatic brain injury: Mild traumatic
brain injury/concussion. Retrieved December 14, 2015, from
http://www.cdc.gov/concussion/signs symptoms.html
Choe, M. C., Babikian, T., DiFiori, J., Hovda, D. A., & Giza,
C. C. (2012). A pediatric perspective on concussion patho-
physiology. Current Opinion in Pediatrics, 24(6), 689-95. doi:
10.1097/MOP.0b013e32835a1a44
Choe, M. C., & Blume, H. K. (2016). Pediatric posttraumatic
headache: A review. Journal of Child Neurology, 31(1), 76-85.
doi.org/10.1177/0883073814568152

A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome 177
Cicerone, K. D., Dahlberg, C., Malec, J. F., Langenbahn,
D. M., Felicetti, T., & Kneipp, S.,.. . Catanese, J. (2002).
Evidence-based cognitive rehabilitation: Updated review of
the literature from 1988 through 2002. Archives of Phys-
ical Medicine and Rehabilitation, 86(8), 1681-92. Doi:
10.1016/j.apmr.2005.03.024
Cicerone, K. D., Langenbahn, D. M., Braden, C., Malec,
J. F., Kalmar, K., & Fraas, M.,. . . Ashman, T. (2011).
Evidence-based cognitive rehabilitation: Updated review
of the literature from 2003 through 2008. Archives of
Physical Medicine and Rehabilitation, 92(4), 519-30. doi:
10.1016/j.apmr.2010.11.015
Conder, A. (2013). Academic accommodations for the concussed
student athlete. Paper presented at the Second Matthew Gfeller
Sport-Related Neurotrauma Symposium, University of North
Carolina, Chapel Hill, NC.
Conder, A. A. (2011). The Gfeller-Waller Sport Concussion
Awareness Act: new legislation on traumatic brain injury.
Presentation to the North Carolina Department of Public
Instruction, 61st Conference on Exceptional Children. Greens-
boro, NC.
Conder, R. (1992). A pragmatic theory of cognitive rehabilitation.
In: Conder R, Allen LM, Cox D, editors. Neurorehabilitative
software guide. Durham, NC.: Cognisyst 1992. p 7-12.
Conder, R., & Conder, A. A. (2015). Neuropsychological and
psychological rehabilitation interventions in refractory sport-
related post-concussive syndrome. Brain Injury, 29(2), 249-62.
doi: 10.3109/02699052.2014.965209
Conder, R., & Conder, A. A. (2018). Assessment and management
of sport-related concussions. In Taylor, J. (Ed.) Assessment in
applied sport psychology. Champagne, Il: Human Kinetics.
Conder, R., Evans, D., Faulkner, P., Henley, K., Kreutzer, J. S.,
Lent, B.,. . . Stith, F. (1988). An interdisciplinary programme
for cognitive rehabilitation. Brain Injury, 2, 365-85. doi:
10.3109/02699058809150909
Conder, R. L., & Conder, A. A. (2014). Heart rate variability
interventions for concussion and rehabilitation. Frontiers in
Psychology, 5, 890. doi: 10.3389/fpsyg.2014.00890
Conder, R. L., & Conder, A. A. (2015). Sports-related concus-
sions. North Carolina Medical Journal, 76(2), 89-95. doi:
10.18043/ncm.76.2.89
Conder, R. L., Conder, A. A., Register-Mihalik, J., Conder, L.
H., & Newton, S. (2015). Preliminary normative data on the
Penn State University Symbol Cancellation Task with non-
concussed adolescents. Applied Neuropsychology: Child, 4(3),
141-47. doi: 10.1080/21622965.2013.816849
Covassin, T., Crutcher, B., Bleecker, A., Heiden, E. O., Daily, A.,
& Yang, J. Z. (2014). Postinjury anxiety and social support
among collegiate athletes: A comparison between orthopedic
injuries and concussions. Journal of Athletic Training, 49(4),
462-68. doi: 0.4085/1062-6059-49.2.03
Covassin, T., Elbin, R. J., Larson, E., & Kontos, A. P.
(2012). Sex and age differences in depression and base-
line sport-related concussion neurocognitive performance and
symptoms. Clinical Journal of Sports Medicine, 22(2), 98-104.
doi: 10.1097/JSM.0b013e31823403d2
Criswell, J. D. (2017). Mindfulness interventions. Annual Review
of Psychology, 68, 491-16.
Echemendia, R. J., Giza, C. C., & Kutcher, J. S. (2015).
Developing guidelines for return to play: Consensus and
evidence-based approaches. Brain Injury, 29(2), 185-94.
doi:10.3109/02699052.2014.96521
Engel, G. L. (1977). The need for a new medical model: A
challenge for biomedicine. Science, 196(4286), 129-36. doi:
10.1126/science.847460
Ewing, M. E., & Seefeldt, V. D. (2002). Patterns of participation in
American agency-sponsored sports. In: Smoll, F.L., & Smith,
R.E., (Eds.). Children and youth in sport: A biopsychosocial
perspective (2nd ed, pp. 39-56). Dubuque, Iowa:Kendall/Hunt.
Field, M., Collins, M. W.,Lovell, M. R., & Maroon, J. (2003). Does
age play a role in recovery from sports-related concussion? A
comparison of high school and collegiate athletics. Journal of
Pediatrics, 142(5), 546-53. doi: 10.1067/mpd.2003.190
Fletcher, D., & Sarkar, M. (2012). A grounded theory of
psychological resilience in olympic champions. Psychol-
ogy of Sport and Exercise, 13(5), 669-78. doi:10.1016/j.
psychsport.2012.04.007
Frommer, L. J., Gurka, K. K., Cross, K. M., Ingersoll, C. D.,
Comstock, R. D., & Saliba, S. A. (2011). Sex differences in
concussion symptoms in high school athletes. Journal of Ath-
letic Training, 46(1), 76-84. doi: 10.4085/1062-6050-46.1.76
Gall, B., Parkhouse, W., & Goodman, D. (2004). Heart rate vari-
ability of recently concussed athletes at rest and exercise.
Medicine &Science in Sports &Exercise, 36(8), 1269-74. doi:
10.1249/01.MSS.0000135787.73757.4D
Gilchrist, J., Thomas, K. E., Xu, L., McGuire, L. C., & Coronado,
V. G. (2011). Nonfatal sports and recreation related traumatic
brain injuries among children and adolescents treated in emer-
gency departments in the United States, 2001–2009. Morbidity
and Mortality Weekly Review, 60(39), 1337-42.
Gioia, G. A., Vaughn, C. G., & Sady, M. D. Developmental consid-
erations in pediatric concussion evaluation and management.
In Apps, J. N., & Walter, K. D., (Eds.). Pediatric and adoles-
cent concussion: Diagnosis, management and outcomes (pp.
687–695). NY: Springer.
Gioia, G., & Collins, M. Heads up in sports. Center for Dis-
ease Control and Prevention [Internet]. Atlanta, GA: CDC;
2006 Jan 6- [cited 2019 Jun 06]; Available from HEADS UP :
https://www.cdc.gov/headsup/index.html
Giza, C. C., & Hovda, D. A. (2001). The neurometabolic cascade
of concussion. Journal of Athletic Training, 36(3), 228-35. doi:
10.1227/NEU.0000000000000505
Goodman, B., Vargas, B., & Dodick, D. (2013). Autonomic
nervous system dysfunction in concussion. Neurology, 80(7
suppl), p01-265.
Guskiewicz, K. M. (2015). Sport-related concussions: Paranoia or
legitimate concerns? North Carolina Medical Journal, 76(2),
93-94. doi: 10.18043/ncm.76.2.93
Halstead, M. E., McAvoy, K., Devorc, C. D., Carl, R., Lee, M.,
& Logan, K. (2013). Returning to learning following a con-
cussion. Pediatrics, 132(5), 948-57. doi: 10.1542/peds.2013-
2867
Hanna-Pladdy, B., Berry, Z., Bennett, T., & Phillips, H. (2001).
Stress as a diagnostic challenge for postconcussive symp-
toms: Sequelae of mild traumatic brain injury or physiological
stress response. Clinical Neuropsychologist, 15(3), 289-304.
doi: 10.1076/clin.15.3.289.10272
Harmon, K. G., Drezner, J. A., Gammons, M., Guskiewicz, K.
M., Halstead, M., Herring, & S. A.,. . .Roberts, W. O. (2013).
American Medical Society for Sports Medicine position state-
ment; concussion in sport. British Journal of Sports Medicine,
47(1), 15-26. doi: 10.1136/bjsports-2012-091941
Harvey, D. J., Freeman J., Broshek, D. K., & Barth, J. T. (2011).
Sports injuries. In Silver, J. M., McAllister, T. W., & Yudofsky,

178 A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome
S. C. (Eds.). Textbook of traumatic brain injury (2nd ed, pp.
453–476). New York: American Psychiatric Publishing.
Headache Classification Committee of the International Headache
Society (IHS). (2018). The International Classification of
Headache Disorders, 3rd edition. Cephalalgia, 38(1), 1-211.
doi: 10.1177/0333102417738202
Helmick, K. (2010). Cognitive rehabilitation for military per-
sonnel with mild traumatic brain injury and chronic
post-concussional disorder: Results of April 2009 consen-
sus conference. NeuroRehabilitation, 26(3), 239-55. doi:
10.3233/NRE-2010-0560
Henry, L. C., Elbin, R. J., Collins, M. W., Marchetti, G.,
& Kontos, A. P. (2016). Examining recovery trajectories
after sport-related concussion with a multimodal clinical
assessment approach. Neurosurgery, 78(2), 232-41. doi:
10.1227/NEU.0000000000001041
Hou, R., Moss-Morris, R., Peveler, R., Mogg, K., Bradley, B. P.,
& Belli A. (2012). When a minor head injury results in endur-
ing symptoms: A prospective investigation of risk factors for
postconcussional syndrome after mild traumatic brain injury.
Journal of Neurology, Neurosurgery &Psychiatry, 83(2), 217-
23. doi: 10.1136/jnnp-2011-300767
Institute of Medicine and National Research Council. (2013).
Sports-related concussions in youth: Improving the sci-
ence, changing the culture. Washington, DC: The National
Academies Press.
Iverson, G. L. (2006). Misdiagnosis of the persistent post-
concussion syndrome in patients with depression. Archives
of Clinical Neuropsychology, 21(4), 303-310. doi: 10.1016/
j.acn.2005.12.008
Iverson, G. L, Gardner, A. J., Terry, D. P., Ponsford, J. L.,
Sills, A. K., Broshek, D. K., & Solomon, G. S. (2017). Pre-
dictors of clinical recovery from concussion: A systematic
review. British Journal of Sports Medicine, 51(12), 941-48.
doi: 10.1136/bjsports-2017-097729
Jacobs, G. D., Pace-Schott, E. F., Stickgold, R., & Otto, M. W.
(2004). Cognitive behavior therapy and pharmacotherapy for
insomnia: A randomized controlled trial and direct compar-
ison. Archives of Internal Medicine, 164(17), 1888-96. doi:
10.1001/archinte.164.17.1888
Jacobson, E. (1938). Progressive Relaxation. (2nd ed). Chicago:
University of Chicago Press.
Janicak, P. G., & Dokucu, M. E. (2015). Transcranial magnetic
stimulation for the treatment of major depression. Neuropsy-
chiatric Disease and Treatment, 11, 1549–1560. Published
online 2015 Jun 26. doi: 10.2147/NDT.S67477
Khazan, I. Z. (2013). The clinical handbook of biofeedback: A
step by step guide for training and practice with mindfulness.
Chichester, West Sussex, UK: John Wiley & Sons Inc.
Kirk, J. W., Slomine, B., Dise-Lewis, J. E. (2012). School-based
management. In: Kirkwood, M. W., Yeates, K. O., (Eds.). Mild
traumatic brain injury in children and adolescents (pp. 321–
337). New York: Guilford.
Kirkwood, M. W., Yeates, K. D., & Wilson, P. E. (2006). Pediatric
sport-related concussion: A review of the clinical management
of an oft-neglected population. Pediatrics, 117(4), 1359-71.
doi: 10.1542/peds.2005-0994
Kontos, A. P., Covassin, T., Elbin, R. J., & Parker, T. (2012).
Depression and neurocognitive performance after concussion
among male and female high school and collegiate athletes.
Archives of Physical Medicine and Rehabilitation, 93(10),
1751-56. doi: 10.1016/j.apmr.2012.03.032
Kontos, A. P., Elbin, R. J., Lau, B., Simensky, S., Freund, B.,
French, J., & Collins, M. W. (2013). Posttraumatic migraine as
a predictor of recovery and cognitive impairment after sport-
related concussion. American Journal of Sports Medicine,
41(7), 1497-1504. doi: 10.1177/036354651348875
Kontos, A. P., Sufrinko, A., Sandel, N., Emami, K., & Collins,
M. (2019). Sport-related concussion clinical profiles: Clinical
characteristics, targeted treatments, and preliminary evidence.
Current Sport Medicine Reports, 18(30), 82-92.
Kostyun, R. O., Milewski, M. D., & Hafeez, I. (2014). Sleep distur-
bance and neurocognitive function during the recovery from a
sport-related concussion in adolescents. American Journal of
Sports Medicine, doi.org/10.1177/0363546514560727
Kreutzer, J. S., Conder, R., Wehman, P., & Morrison, K. (1989).
Compensatory strategies for enhancing independent living and
vocational outcome following traumatic brain injury. Cognitive
Rehabilitation, 7(1), 30-35.
Kuczynski, A., Crawford, S., Bodell, L., Dewey, D., & Barlow. K.
M. (2013). Characteristics of post-traumatic headaches in chil-
dren following mild traumatic brain injury and their response
to treatment: A prospective cohort. Developmental Medicine &
Child Neurology, 55(7), 636-41. doi.org/10.1111/dmcn.12152
Lagos, L., Bottiglieri, T., Vaschillo, B., & Vaschillo, E. (2012).
Heart rate variability biofeedback for postconcussion syn-
drome: Implications for treatment. Biofeedback, 40(4), 150-53.
doi: 10.5298/1081-5937-40.4.05
Lagos, L., Thompson, J., & Vaschillo, E. (2013). A prelimi-
nary study: Heart rate variability biofeedback for treatment
of postconcussion syndrome. Biofeedback, 41(3), 136-43. doi:
10.5298/1081-5937-41.3.02
Leddy, J. L., Kozlowski, K., Fung, M., Pendergast, D. R., & Willer
B. (2007). Regulatory and autoregulatory physiologic dysfunc-
tion as a primary characteristic of post-concussion syndrome:
Implications for treatment. NeuroRehabilitation, 22(3), 199-
205.
Leddy, J. J., Haider, M. N., Ellis, M., & Willer, B. S. (2018).
Exercise is medicine for concussion. Current Sports Medicine
Reports, 17(8), 262-70. doi:10.1249/JSR.0000000000000505
Legome, E. L. (2018). Postconcussion syndrome. Accessed
June 7, 2019. Retrieved from: https://emedicine.medscape.
com/article/828904-print
Len, T., Nearly, J., Asmundson, G., Goodman, D., Bjornson,
B., & Bhambhani, Y. (2011). Cerebrovascular reactivity
impairment after sport-induced concussion. Medicine & Sci-
ence in Sports &Exercise,43(12), 2241-48. doi: 10.1249/
MSS.0b013e3182249539
LeUnes, A. (2008). Sports Psychology (4th ed). New York: Psy-
chology Press.
Lovell, M. R. (2006). Neuropsychological assessment of the
professional athlete. In Echemendia, R. J. (Ed.). Sports neu-
ropsychology: Assessment and managementof traumatic brain
injury (pp. 176-192). New York, NY: Guilford.
Lumba-Brown, A., Ghajar, J., Cornwell, J., Bloom, O. J., Chesnutt,
J., Clugston, J. R., Kolluri, R., Leddy, J., Teramoto, M., &
Gioia, G. (2019). Representation of concussion subtypes in
common post-concussion symptom rating scales. Concussion
1;4(3), CNC65. doi: 10.2217/cnc-2019-0005.
Majerske, C. W., Mihalik, J. P., Ren, D., Collins, M. W., Reddy,
C. C., Lovell, M. R., & Wagner, A. K. (2008). Concussion
in sports: Postconcussive activity levels, symptoms and neu-
rocognitive performance. Journal of Athletic Training, 43(3),
265-74. doi: 10.4085/1062-6050-43.3.265

A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome 179
Maerlender, A., Flashman, L., Kessler, A., Kumbhani, S., Green-
wald, R., Tosteson, T., & McAllister, T. (2010). Examination
of construct validity of ImPACT computerized test, traditional
and experimental neuropsychological measures. The Clinical
Neuropsychologist, 24, 1309-25.
Maerlender, A., Flashman, L., Kessler, A., Kumbhani, S.,
Greenwald, R., Tosteson, T., & McAllister, T. (2010). The dis-
criminant construct validity of ImPACT: A companion study.
The Clinical Neuropsychologist, 27, 290-99.
Mann, D. T. Y., & Janelle, C. M. (2012). Psychophysiology:
Equipment in research and practice. Case studies in applied
psychophysiology: Neurofeedback &Biofeedback treatments
for advances in human performance (pp. 257–274). West Sus-
sex, UK: Wiley-Blackwell.
McCrea, M. (2008). Mild traumatic brain injury and postconcus-
sion syndrome. New York: Oxford.
McCrea, M., Iverson, G. L., McAllister, T. W., Hammeke, T. A.,
Powell, M. R., Barr, W. B., & Kelly, J. P. (2009). An integrated
review of recovery after mild traumatic brain injury (MTBI):
Implications for clinical management. The Clinical Neuropsy-
chologist, 23(8), 1368-90. doi: 10.1080/13854040903074652
McCrea, M., Prichep, L., Powell, M. R., Chabot, R., & Barr, W. B.
(2010). Acute effects and recovery after sport-related concus-
sion: A neurocognitive and quantitativebrain electrical activity
study. Journal of Head Trauma Rehabilitation, 25(4), 283-92.
doi: 10.1097/HTR.0b013e3181e67923
McCrory, P., Meeuwisse, W. H., Aubry, M., Cantu, B., Dvo-
rak, J., Echemendia, & R. J.,...Turner, M. (2013). Consensus
statement on concussion in sport: The 4th International Con-
ference on Concussion in Sport held in Zurich, November
2012. British Journal of Sport Medicine, 23(2), 89-117. doi:
10.1136/bjsports-2013-092313.
McCrory, P., Meeuwisse, W., Dvorak, J., Aubry, M., Bailes, J.,
& Broglio, S....Vos, P. E. (2017). Consensus statement on
concussion in sport: The 5th International Conference on Con-
cussion in Sport held in Berlin, October 2016. British Journal
of Sport Medicine, 51(11), 838-47. doi: 10.1136/bjsports-
2017-097699
McGrath, N. (2010). Supporting the student-athlete’s return to the
classroom after a sport-related concussion. Journal of Athletic
Training, 45(5), 492-98. doi: 10.4085/1062-6050-45.5.492
Meehan, W., Mannix, R., Straccioloni, A., Elbin, R., & Collins,
M. (2013). Symptom severity predicts prolonged recov-
ery after sport-related concussion, but age and amnesia do
not. Journal of Pediatrics, 163(3), 721-25. doi: 10.1016/
j.jpeds.2013.03.012
Meehan, W. P., Taylor, A. M., & Proctor, M. (2012). The
pediatric athlete: Younger athletes with sport-related con-
cussion. Clinical Sports Medicine, 30(1), 133-44. doi:
10.1016/j.csm.2010.08.004
Millis, S. (2015). What clinicians really need to know about
symptom exaggeration, insufficient effort and malingering:
Statistical and measurement matters. In J. E. Morgan & J.
J. Sweet (Eds.), Neuropsychology of malingering casebook
(pp. 21–38). New York, NY: Psychology Press.
National Collegiate Athletic Association [Internet]. Indianapo-
lis, IN: NCAA; 2012 September 19 – [cited 2013 Oct 19];
Retrieved from http://www.ncaa.org
National Collegiate Athletic Association. (2014). Concus-
sion: return-to-learn guidelines. Retrieved December 8,
2015 from http://www.ncaa.org/health-and-safety/medical-
conditions/concussion-return-learn-guidelines
Neidecker, J., Gealt, D. B., Luksch, J. R., & Weaver, M. D. (2017).
First-time sports-related concussion recovery: The role of sex,
age, and sport. Journal of the American Osteopathic Associa-
tion, 117(10), 635-42. doi: 10.7556/jaoa.2017.120
Nelson, L. D., Janecek, J. K., & McCrea, M. A. (2013). Acute clin-
ical recovery from sport-related concussion. Neuropsychology
Review, 23(4), 285-299.
Norris, P. A., Fahrion, S. L., & Oikawa, L. O. (2003). Autogenic
biofeedback training in psychophysiological therapy and stress
management. In Schwartz, M.S., Andrasik, F. (Eds.). Biofeed-
back: A practitioner’s guide (3rd ed., pp. 175-205). New York:
Guilford.
Pertab, J. L., Merkley, T. I., Cramond, A. J., Cramond, K., Pax-
ton, H., & Wu, T. (2018). Concussion and the autonomic
nervous system: An introduction to the field and the results
of a systematic review. NeuroRehabilitation, 42(4), 397-427.
doi:10.3233/NRE-172298
Ponsford, J., & Kinsella, G. (1992). Attentional deficits
following closed-head injury. Journal of Clinical and Exper-
imental Neuropsychology, 14(5), 822-38. doi: 10.1080/
01688639208402865
Register-Mihalik, J., Guskiewicz, K. M., Mann, J. D., & Shields, E.
W.(2007). The effects of headache on clinical measures of neu-
rocognitive functioning. Clinical Journal of Sports Medicine,
17(4), 282-88. doi:10.1097/JSM.0b013e31804ca68a
Rieck, T., Jackson, A., Martin, S. B., Petrie, T., & Green-
leaf, C. (2013). Health-related fitness, body mass index,
and risk for depression among adolescents. Medicine &
Science in Sports &Exercise, 45(6), 1083-1088. doi:
10.1249/MSS.0b013e3182831db1
Rieger, B., Lewandowski, L., Potts, H., & Shea, N. (2019). Effects
of concussion in adolescent students: perceptions and per-
formance. Journal of the International Neuropsychological
Society, 1-10. doi:10.1017/S1355617719000468
Schatz, P., & Maerlender, A. (2013). A two-factor theory of con-
cussion assessment using ImPACT:Memory & speed. Archives
of Clinical Neuropsychology, 28, 791-97.
Schneider, K. J., Iverson, G. L., Emery, C. A., McCrory, P., Her-
ring, S. A., & Meeuwisse, W. H. (2013). The effects of rest
and treatment following sport-related concussion: A system-
atic review of the literature. British Journalof Sports Medicine,
47(5), 304-307. doi: 10.1136/bjsports-2013-092190
Schwartz, M. S. (2003). The use of audiotapes for patient educa-
tion and relaxation. In Schwartz, M.S., & Andrasik, F. (Eds.).
Biofeedback: A practitioner’s guide (3rd ed, pp. 265–274).
New York: Guilford.
Sisto, A., Vicinanza, F., Campanozzi, L. L., Ricci, G., Tartaglini,
D., & Tambone, V. (2019). Towards a transversal definition
of psychological resilience: A literature review. Medicina,
16;55(11), pii: E745. doi: 10.3390/medicina55110745
Strack, B., & Gevirtz, R. N. (2011). Getting to the heart of the
matter: Heart rate variability biofeedback for enhanced perfor-
mance, In Biofeedback &Neurofeedback Applications in Sport
Psychology, (Eds.) B. W. Strack, M. K. Linden, V. S. Wilson.
Wheat Ridge, CO: AAPB Press.
Tan, G., Fink, B., Dao, T. K., Hebert, R., Farmer, L. S., Sanders,
A....Gevirtz, R. (2009). Associations between pain, PTSD,
mTBI, and heart rate variability in veterans of Operation Endur-
ing and Iraqi Freedom: A pilot study. Pain Medicine, 10(7),
1237-45. doi: 10.1111/j.1526-4637.2009.00712.x
Tan, G., Shaffer, F., Lyle, R., & Teo, I. (2016). Evidence-based
practice in biofeedback and neurofeedback (3rd ed). Wheat

180 A. Conder et al. / Neurorehabilitation of Persistent Sport-Related Post-Concussion Syndrome
Ridge, CO: Association for Applied Psychophysiology and
Biofeedback.
Taylor, H. G., Dietrich, A., Nuss, K., Wright, M., Rusin, J., Bangert,
B....Yeates, K. O. (2010). Post concussive symptoms in chil-
dren with mild traumatic brain injury. Neuropsychology, 24(2),
148-159. doi: 10.1037/a0018112.
Thatcher, R. (2006). Electroencephalography and mild traumatic
brain injury. In Slobounov, S., Sebastianelli, W., (Eds.). Foun-
dations of sport-related brain injuries (pp. 241–265). New
York, NY: Springer.
Valovich-McLeod, T. C., & Gioia, G. A. (2010). Cognitive rest:
The often neglected aspect of concussion management. Human
Kinetics, 15(2), 1-3. https://doi.org/10.1123/att.15.2.1
Weiss, M. R., Kipp, L. E., & Bolter, N. D. (2012). Training for
life: Optimizing positive youth development through sport and
physical activity. In Murphy, S. M. (Ed.). The Oxford hand-
book of sport and performance psychology (pp. 448–475). New
York: Oxford.
Werthner, P., Christie, S., & Dupee, M. (2013). Neurofeedback
and biofeedback training with Olympic athletes. Neurocon-
nections, 2, 32-38.
Wilson, V. E., & Cummings, M. S. (2011). Mind/body control in
sport: Learned self-regulation. In Strack, B.W., Linden, M.K.,
& Wilson, V.S., (Eds.). Biofeedback and neurofeedback appli-
cations in sport psychology (pp 107-144). Wheat Ridge, CO:
AAPB Publishers.
Wilson, V. E., & Somers, K. Psychophysiological assessment and
training with athletes. In Strack, B.W., Linden, M.K., & Wil-
son, V.S., (Eds.). Biofeedback and neurofeedback applications
in sport psychology (pp. 145-188). Wheat Ridge, CO: AAPB
Publishers.
Yeates, K. O. (2010). Mild traumatic brain injury and postcon-
cussive symptoms in children and adolescents. Journal of the
International NeuropsychologicalSociety, 16(6), 953-960. doi:
10.1017/S1355617710000986
Yucha, C., & Montgomery, D. (2008). Evidence-based prac-
tice in biofeedback and neurofeedback. Faculty Publications
(N). Paper 1. Retrieved from http://digitalcommons.library.
unlv.edu/nursing fac articles/1
Zasler, N. (2015). Sports concussion headache. Brain Injury, 29(2),
207-220. doi: 10.3109/02699052.2014.965213