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Neuropsychological and psychological rehabilitation interventions in refractory sport-related post-concussive syndrome

Authors:
  • Carolina Neuropsychological Service

Abstract

Background: The neuropsychological, physical, vestibular and oculomotor sequelae of sports-related concussion are extremely well documented. However, there is a paucity of interventions for these symptoms in refractory sports-related concussions. Aim: The intent of this article is to review the known and emerging neuropsychological and psychological rehabilitation interventions for reducing morbidity in refractory sports-related concussions (SRCs). Methods: The authors openly acknowledge the limited amount of empirical data available for review, as did the Zurich consensus papers, but posit a mindful and ethical approach towards rehabilitation interventions in the absence of evidence-based guidelines. Further, rehabilitation interventions proven useful with similar injuries or illnesses, particularly non-sports-related mild TBI, will be reviewed for applicability. Such interventions include Cognitive-Behavioural psychotherapy, biofeedback, cranial electrical stimulation, neurofeedback and cognitive rehabilitation. Results and conclusions: Modified approaches for rehabilitation with young children within family and school systems are provided. Recommendations for further research are offered.
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ISSN: 0269-9052 (print), 1362-301X (electronic)
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!2014 Informa UK Ltd. DOI: 10.3109/02699052.2014.965209
ORIGINAL ARTICLE
Neuropsychological and psychological rehabilitation interventions
in refractory sport-related post-concussive syndrome
Robert Conder & Alanna Adler Conder
Carolina Neuropsychological Service, Raleigh, NC, USA
Abstract
Background: The neuropsychological, physical, vestibular and oculomotor sequelae of sports-
related concussion are extremely well documented. However, there is a paucity of interventions
for these symptoms in refractory sports-related concussions.
Aim: The intent of this article is to review the known and emerging neuropsychological and
psychological rehabilitation interventions for reducing morbidity in refractory sports-related
concussions (SRCs).
Methods: The authors openly acknowledge the limited amount of empirical data available for
review, as did the Zurich consensus papers, but posit a mindful and ethical approach towards
rehabilitation interventions in the absence of evidence-based guidelines. Further, rehabilitation
interventions proven useful with similar injuries or illnesses, particularly non-sports-related mild
TBI, will be reviewed for applicability. Such interventions include Cognitive-Behavioural
psychotherapy, biofeedback, cranial electrical stimulation, neurofeedback and cognitive
rehabilitation.
Results and conclusions: Modified approaches for rehabilitation with young children within
family and school systems are provided. Recommendations for further research are offered.
Keywords
Biofeedback, biopsychosocial, cognitive
behavioural therapy, mild traumatic brain
injury, neurofeedback, sport concussion
History
Received 6 December 2013
Revised 7 May 2014
Accepted 28 May 2014
Published online 7 October 2014
Introduction
The neuropsychological, physical, vestibular and oculomotor
sequelae of sports-related concussion are extremely well
documented [1–3]. However, there is a paucity of interventions
identified to reduce these symptoms in refractory sports-
related concussions. The intent of this article is to review the
known and emerging neuropsychological and psychological
rehabilitation interventions for reducing morbidity in refrac-
tory sports-related concussions (SRCs). Operationalizing the
term ‘refractory’ is difficult because there is no established
consensus on a time-frame that constitutes intractability in a
syndrome whose diagnostic criteria itself is variable. For the
purposes of this article, ‘refractory’ is defined as post-
concussive symptoms which persist without significant
improvement beyond the expected recovery period and cause
impairment in life functions including school, work and
personal life. ‘Expected recovery periods’ vary some by age
and pre-morbid or co-morbid factors, as will be discussed. The
authors also openly acknowledge the limited amount of
empirical data available for review, as did the Zurich
Consensus Statement, but posit a mindful and ethical approach
towards rehabilitation intervention in the absence of evidence-
based guidelines. Further, rehabilitation interventions proven
useful with similar injuries or illnesses, particularly non-
sports-related mild TBI, will be reviewed for applicability.
Emerging interventions at a case study level of analysis will be
referenced.
Scope of the problem
Among the 45 million children and adolescents who partici-
pate in organized or recreational sports and exercise [4] with
positive physical, intellectual and social development oppor-
tunities [5, 6], there is also the risk of injury including
orthopaedic injury, traumatic brain injury or sports-related
concussions (SRC) [7]. An estimated 5–10% of children and
adolescents receive a SRC with an emergency room presen-
tation. Nearly a quarter million of these are hospitalized.
There are an unfortunate 900 SRC deaths per year [8]. These
figures are estimates based upon emergency room admissions
and probably under-estimate the prevalence, as many SRC
may not receive medical care, especially at the level of an
emergency room. At the college level there are 450 000
players participating in all sports and over 160 000 participat-
ing in sports identified as concussion generating [9]. At the
professional level, there are fewer but more elite athletes
participating. There are an estimated 1600 players in the
National Football League and roughly the same number in the
National Hockey League. One can conceptualize sports
participation as a pyramid, with a wide base consisting of
youth/recreational sports (YRS) participants narrowing to a
Correspondence: Robert Conder, Carolina Neuropsychological Service,
1540 Sunday Drive, Raleigh, NC 27607, USA. Tel: 919-859-9040. Fax:
919-859-9030. E-mail: bconder10@gmail.com
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peak comprised of professional, elite and Olympic athletes.
Alongside brain injury controversy at the professional level,
there is growing concern about protecting the health and
safety of K-12 and collegiate athletes who receive a concus-
sion which can impair academic, cognitive and social
development [10].
SRCs have been classified as mild TBI or MTBI [11].
Current consensus statements suggest that the prototypical
recovery pattern for an uncomplicated sports concussion may
show nearly complete improvement in the first 1–2 weeks post-
MTBI, although some symptoms may persist for several
weeks. The World Health Organization task force noted (p. 93)
that ‘the prognosis after MTBI is highly favourable, with
gradual resolution of symptoms and little evidence of residual
cognitive, behavioural or academic deficits’ [12]. McCrea et al.
[13] posit that the sequelae of a SRC in American football
players are most demonstrable within the first few hours post-
concussion and that symptoms diminish with a gradual
recovery course over the next several days. After day 7, in
some studies there are no differences between normal controls
and injured players [14]. This pattern parallels the animal
research of Hovda [15]. Hovda posits a neurometabolic
cascade with, at a minimum, a mismatch in glucose metabol-
ism and regional cerebral blood flow. For the majority of these
animal studies, the metabolic cascade restores to homeostasis
in about a 7-day period. Further, there is not irreversible
damage at a cellular level in these animal models [15].
The primary treatment advocated during this 7–10-day
window is both physical and cognitive rest [16, 17]. For an
athlete, this means not only no participation in games and
competition, but also no participation in practice and drills. For
student-athletes and gainfully employed individuals, the cog-
nitive demands of school and work also need to be reduced to
allow the normal homeostatic process to occur. There is data
showing that a precipitous return to either play or cognitive
activity, especially when symptomatic at rest, will prolong
symptoms and complicate the recovery process [18, 19].
However, much of this empirical data is in its infancy and
still emerging. The Zurich Conference in 2012 functioned as an
expert review of extant data, providing consensus in the
absence of firm empirical evidence [12]. The Zurich Return To
Play (RTP) protocol [1] is well delineated and highly useful in
professional athletes, whose only job is their sport. However,
for the injured student-athlete in grades K-12 and college,
devising an effective Returning To Learning (RTL) protocol
is much more complex. RTL guidelines for this population
must take into consideration the developmental and cognitive
level of the student, any pre-morbid or co-morbid medical
or neurologic concerns, their grade and academic level and
co-ordination between parents and multiple teachers. This
degree of variability can make RTL plans in the K-12
population more complex than for injured collegiate student-
athletes. Conder [20] has presented a working formulation for
RTL in collaboration with the North Carolina Department of
Public Instruction’s Wake County Schools TBI Task Force.
This model provides a matrix for documenting concussion-
related impairments, pairing these with needed accommoda-
tions or supports and implementing an immediate Emergency
Healthcare Plan that can be flexibly adapted with improvement
of the student’s concussion status.
A critical challenge is clinical intervention for those athletes
with SRC who fail to show the expected quick pattern of
recovery, an estimated 10–20% [21]. McCrea [11] investigated
both NCAA and high school concussed athletes. While group
differences were not statistically significant, the data from the
high school sample (Project Sideline) showed higher levels of
Grade 3 concussion using American Academy of Neurology
standards, including loss of consciousness and post-traumatic
retrograde or anterograde amnesia, than did the NCAA sample.
Patterns of more prolonged recovery also were seen in the high
school sample as contrasted with the NCAA sample: while the
NCAA sample substantially recovered in the Rapid to Gradual
recovery phase, 18.5% of the high school sample showed a
Prolonged recovery period (1 week–1 month), while another
almost 5% showed Persistent symptoms (41 month) [11].
These findings parallel other researchers who have shown that
high school athletes are more at risk for having significant post-
concussive symptoms and relatively longer recovery periods
[22]. This more complicated recovery process certainly has
implications for potential disruption in social development and
academic progress if concussions are not well managed. Of
particular concern is the impact on academic performance
in high-achieving student-athletes, particularly those in
Advanced Placement curricula seeking competitive college
admission.
Age and gender differences in concussion recovery also
have been studied [23]. Ten-to-fourteen year-old boys and girls
have the highest rates of sport-related TBI Emergency Room
(ER) visits. Among the 10–14 year-old group, the sport and
recreational activities producing the most concussions include
bicycling, American football and playground activities. For the
5–18 year-old group, the sports activities producing the most
concussions include bicycling, American football and soccer,
basketball and playground activities. By gender, American
football is the greatest concussion generator for males and
soccer is the greatest concussion generator for females.
Additionally, females are at higher risk for sustaining concus-
sions across all ages and sports. There are no proven reasons for
this higher risk, although hypotheses include physiologic
differences such as thinner skull thickness, smaller neck
muscles and hormonal influences [1]. There may be a higher
rate of genetic migraines with mother-to-daughter transmis-
sion. Alternatively, females simply may be more willing to
report symptoms than males. Finally, it has been shown that
more symptoms are reported by a female athlete to a female
examiner [24]. However, the most prevalent concussion
symptoms tend to be common across gender. Ninety-seven
per cent of females and 95% of males report headaches post-
concussion. Dizziness and vestibular dysfunction is noted
by 77% of both genders, while concentration difficulties
are noted by 51% of males and 47% of females. For prolonged
symptoms, however, headaches and concentration difficulties
appear to be more demonstrable for females. Given findings
suggesting more prolonged symptoms among younger ath-
letes and the adverse effects of these symptoms on psycho-
logical and academic performance in grades K-12 [25, 26],
there is great need for early rehabilitation interven-
tions effective for reducing persistent PCS symptoms in
concussed student-athletes across all levels of play and
development.
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A biopsychosocial framework for analysis
Prolonged post-concussive symptomatology does not neces-
sarily imply a sole physical aetiology for the continuation of
such symptoms. The BioPsychoSocial frameworkof analysis is
a multi-level, multi-dimensional interactive paradigm that
explains how biological, psychological and social systems
dimensions coalesce to impact symptom resolution or persist-
ence [27, 28]. By extension, the BioPsychoSocial framework
engenders diverse treatment interventions available to address
these dimensions. From this perspective, a concussion starts as
primarily a biological event, driven by external forces to the
body and brain. These physiological forces tend to be self-
limiting and the neurometabolic cascade reverts to its pre-
injury homeostasis after a finite period, without underlying
cellular damage. Often, the concussive event may trigger
secondary biological phenomena such as headaches, tinnitus,
vestibular dysfunction and oculomotor dysfunction, especially
if there are pre-morbid or co-morbid vulnerabilities. While
these biological symptoms are trauma-induced, a
BioPsychoSocial approach also examines concomitant psy-
chological factors which exacerbate or sustain the presentation
of physiologic symptoms [13]. Some concussions, of course,
will be purely physical and will be prolonged due to true
pathogenesis. With prolonged symptoms, a thorough medical
investigation by a physician versed in sports concussions is
needed [29]. Many times patients will be cleared in an
Emergency Room or Urgent Care setting when, in fact, there
can be serious pathophysiologic difficulties. These latter
problems may be shown with a brain or cervical spine MRI
which could elucidate abnormalities in the brain parenchyma,
contusions, a syrinx or Chiari malformation. On the other hand,
Iverson [30] has pointed out that PCS symptoms are not unique
to a concussive event and that some refractory PCS symptoms
may be driven by psychological or predominantly psycho-
logical aetiologies. Frequently, the most complex refractory
presentation may be an interaction of pathophysiologic and
psychological aetiologies.
Psychological analysis of injury recovery requires that the
athlete’s emotional reaction to his/her concussion be under-
stood. The emotional and psychological reactions of athletes
to orthopaedic injuries are well documented [31]. Emotional
reactions of athletes can vary and range from anger, fear, loss
of self-esteem or loss of motivation, to depression and
anxiety, among others. These reactions may play a role in the
expression or persistence of post concussive symptoms.
Conder [32] used the sports modification of Kubler-Ross’
stages of Grief and Loss to gauge professional hockey
players’ reactions to their injury. Players were rated by their
athletic trainers and sports medicine staff. In the immediate
post-injury timeframe (0–48 hours), a majority reacted
with Anger, whereas over a period of a month they progressed
to Acceptance, then Resolution. Appreciating these nuanced
emotional reactions can help the clinician tailor pro-
active interventions which can reduce prolonged symptom
expression. If post-concussive emotional dysregulation trig-
gers a psychological reaction such as depression or anxiety,
the athlete may benefit from traditional cognitive-behav-
ioural therapy approaches adapted to a sports psychology
framework.
The third systems level examined in a BioPsychoSocial
framework is the broader social context in which the injury is
occurring. Family or team dynamics, peer status and even
financial or recruiting contingencies all need to be understood
to determine possible external stressors or reinforcers for
symptom maintenance. In one vivid example, a young child
with a SRC whose parents were in the midst of an
acrimonious separation remained symptomatic for several
months because his prolonged recovery reduced parental
conflict; he finally told his neuropsychologist, ‘If I get better,
my parents will divorce’.
Investigating symptoms from these three BioPychoSocial
levels can help clinicians understand where to target their
intervention. Understanding the interaction of these three
levels also allows the clinician to differentiate physiologic and
psychosocial factors when traditional medical and pharma-
cologic interventions are not efficacious. Finally, expansion
beyond the traditional biological/medical perspective may
appeal to patients/parents who directly express reservation
about aggressive pharmacotherapy or who are indirectly non-
compliant with such treatment. In summary, a BioPsychoSo-
cial model provides a framework for differential diagnosis and
treatment intervention which goes beyond sole focus on
pathophysiologic aetiologies in accounting for prolonged
symptoms or refractory concussion recovery.
Assessment
Clinical mental status exam
A comprehensive, multi-systems level assessment forms the
basis for BioPsychoSocial concussion intervention. The first
and primary assessment tool needed for SRC athletes with
refractory or prolonged post-concussive symptoms is an
expanded psychological Clinical Mental Status Evaluation
[33] to ascertain the factors which are contributing to lack of
symptom remission.
This examination requires comprehensive history taking
and assessment of the following areas: (a) Mood and Affect;
(b) Structure and Quality of Thought; (c) Sleep: insomnia,
parasomnias, nightmares; (d) Headache Profile: types of
headache experience, location, duration, triggers, quality of
pain, identification of what exacerbates or alleviates the pain;
(e) Musculoskeletal Pain: especially cervical and trapezius
pain associated with headaches; (f) Prescribed Medication
History: pre- and post-injury medications and response or
side-effects, unusual historic responses to psychotropic
medication; (g) Pre-morbid Risk Factors: childhood medical
and developmental history including prematurity, perinatal
complications, developmental delays, early intervention
including OT/PT/ST, prolonged high fevers, meningoenceph-
alitis, seizures, migraines; (h) Family History of Psychiatric
and Neurologic Illness: particularly depression, anxiety
and migraines; (i) Substance Abuse History; and (j) History
of Self-Injurious behaviour or ideation. Essentially,
even though an athlete may be referred for a concussion, a
full and rich examination of their psychological mental status
is necessary to understand pre-morbid and co-morbid issues
and past history that may be influencing refractory SRC
recovery.
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Blending medical and sports history with the Clinical
Mental Status Exam above is important, as an athlete may feel
‘psychopathologized’ if they are subjected only to a trad-
itional mental health interview. Sports psychologists and
athletes criticize the work of traditional mental health
practitioners for their lack of knowledge and sufficient
training in sports and posit the need for a sport-specific
intake protocol to assist in an appropriate conceptualization of
the athlete’s concerns [34].
Neurocognitive test battery
A second necessary phase of the assessment process is
administration of a brief pencil-and-paper neurocognitive test
battery. Conder modified the Penn State Neuropsychological
Battery developed by Echemendia et al. [35] and the National
Hockey League Neuropsychological Battery [36] for office
assessments. This modification of the traditional sports
neuropsychological test batteries essentially included the
addition of a brief Orientation and episodic auditory memory
section, an expanded assessment of auditory and visual
Working Memory, psychological and sport-specific inven-
tories and inclusion of Symptom Validity Testing (see Table I).
Psychological assessment
Psychometric measures of mood and personality are useful,
especially if they have validity indicators. Clinical depression
is a common sequelae of SRC. Studies with the Beck
Depression Inventory [37] have shown a clinical presentation
for days post-injury that usually does not progress to the level
of a Major Depression [38]. Establishing baseline levels of
depression is necessary, as this may exacerbate post-injury
cognitive changes [39]. The modified Beck Depression
Inventory for medical patients may be useful, as it removes
the somatic section which can result in a false positive
diagnosis of depression due to actual physical problems in
injured athletes [40].
A broadband personality instrument such as the MMPI-II
or the MMPI-A, depending on age level, is useful given the
multiple validity indices, especially for ascertaining symp-
tom denial in athletes or symptom exaggeration in other
populations. These inventories also assess multiple factors
which can establish co-morbid or pre-morbid psychological
factors that interfere with symptom remediation. In K-12
students, a parent rating scale that also has validity
indicators, such as the Clinical Assessment of Attention
Deficit-Child (CAT-C) [41] can be useful in differentiating
pre- and post-injury attention weakness. For competitive
athletes of 16 years and older, traditional Sports Psychology
instruments can be added to ascertain specific sports
motivation and coping abilities seen in competitive or elite
athletes. Measures such as Smith et al.’s [42] Athletic
Coping Skills Inventory (ACSI) and Meyer et al.’s [43]
Sports Inventory for Pain (SIP-15) assess the psychological
coping and pain management abilities of an athlete. These
instruments have clear relevance not only for exploring
susceptibility to injury and factors influencing injury
recovery, but also probable adherence to prescribed medical
treatment. In fact, the sport psychology literature has
identified a relationship between an athlete’s susceptibility
to musculoskeletal and orthopaedic injuries such as ACL
tears and pre-injury personal and psychosocial stressors or
Table I. Suggested assessment instruments for older adolescent and adult athletes.
Functional area Specific tests Comments
Attention/Concentration Digits Forward Longest span
Digits Backward Longest Span
Brief Test of Attention
PSU Symbol Cancellation Task 5 Forms
CPT/VIGIL
Learning/Memory Hopkins Verbal Learning T-Rev 5 Forms
Brief Visual Memory T-Rev 5 Forms
Symbol Digit Modalities Test
Paragraph Memory Various episodic memory stories
-Imm, Delayed & Recog
Executive & Fluency Color Trails A 3 Forms
Color Trails B 3 Forms
Controlled Oral Word Assoc. 2 forms of original task
Symptoms Concussion Symptom Rating Scale Multiple scales with same four factors: Physical,
Cognitive, Emotional & Sleep—Scores not inter-
changeable. Both before & after testing is reported to
assess symptom change from cognitive effort
Psychological, if needed BSI; MMPI-2 or A; Adolescent Psychopathology
Scale; POMS
If BDI, use one for Medical patients, without somatic
scale
Sports Specific Tests Athletic Coping Skills Inventory;
Tests of Performance Strategies
Sports Inventory for Pain
See Sports Psych lit for sports specific tests
Symptom Validity, if needed RDS; Word Choice; Rey 15; CARB Athletes tend to have positive motivational set
Sub-tests of the Brief Neuropsychological Cognitive Exam (WPS) can be useful as a quick warm-up: Orientation; Naming; Comprehension (Left-Right
orientation in personal and extra-personal space); and Reciprocal Motor Function (Go–No Go paradigm).
For Symptom Validity, clinically, one should first develop an Index of Suspicion for lower motivation during the Clinical Exam. More formal
assessment such as the TOMM or CARB or Dot Counting may be useful. Many athletes have a positive motivational set, as opposed to litigants. Don’t
overload testing with symptom validity tests.
Assessment strategy based on Echemendia et al. [35].
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inadequate pre-injury stress coping abilities [44]. Among
collegiate sports, the strongest stress–injury relationship has
been documented in American football, while other diverse
sports such as soccer, gymnastics and figure skating have
shown a similar relationship [45, 46]. Additionally, quicker
recovery from orthopaedic injuries was noted in athletes
with positive psychological characteristics such as a positive
attitude, use of positive self-talk and positive mental
imagery during the recovery phase [47]. While this
relationship has not been documented in SRC, one can
posit a similar association, especially in athletes with less
adequate stress coping abilities (resilience). By extension,
utilizing or augmenting personal psychological strengths
may enhance coping during a SRC, possibly speeding
recovery.
Psychophysiological evaluation
Finally, in this rehabilitation framework, a psychophysio-
logical evaluation is extremely useful to assess the non-
cognitive aspects of concussion that may be prolonging PCS,
such as changes in Autonomic Nervous System reactivity,
Heart Rate Variability and excess slow wave (theta) activity,
as measured by EEG [48]. Many commercial and FDA-
approved hardware and software devices for performing such
an evaluation are available. A simple entry level device is a
two channel encoder which measures hand temperature and
GSR (Thought Technology; Montreal, Canada). The same
Canadian company manufactures a more complex eight
channel encoder which measures EMG (1–2 channels),
heart rate variability, blood volume pulse or EKG, tempera-
ture, skin conductance, respiration and EEG (1–2 channels).
The assessment paradigm with each encoder is similar:
baseline measures, followed by alternating tasks that induce
cognitive stress, then relaxation periods, to measure recovery
(a very useful concept in sports). Both programs use a Stroop
paradigm that begins with slow presentation, then progresses
to a failure level. Each program also uses a mental math
count-down from a 4-digit number. During each exercise, the
clinician is providing corrective feedback and prompts the
athlete to go faster, thereby increasing physical and cognitive
stress. When this psychophysiological and electrophysio-
logical evaluation is integrated with the Mental Status Exam,
the focused Neurocognitive Exam and the psychological
instruments, a clinically rich and nearly complete portrait of
the athlete with refractory SRC can be achieved.
Rehabilitation and treatment interventions
for refractory PCS
Overview
This section will highlight the rationale and history of various
treatment approaches with sports-related concussion (SRC) or
MTBI. When there is not sufficient empirical evidence and
background using these interventions with SRC, better
established MTBI treatment approaches will be reviewed, as
they can be applied to a sports population. Limited case study
reports that appear promising also will be presented. Keep in
mind, however, the possible differences in response to injury
between the traditional MTBI population studies, primarily
involving motor vehicle accidents and the possibility of
litigation, and the generally positive motivational set of
competitive athletes, not to mention the latter population’s
enhanced cardiovascular and musculoskeletal conditioning.
Ponsford and Kinsella [49] followed consecutive ER admis-
sions for MTBI and found that, at 3 months, the motor vehicle
crash group of patients was significantly more symptomatic
than the sports group.
Mediating factors determining intervention efficacy
include the number of concussions sustained, the time
period between concussions, the morbidity of symptoms and
the level of play of the athlete (recreational, high school,
varsity, collegiate, professional or Olympic). Using the
pyramid metaphor presented earlier, LeUnes [46] posits a
gradient in physiologic resilience as athletes progress from
recreational to collegiate and elite levels, with the elite
athletes more ‘immune’ to season-limiting or career-ending
injuries. Paralleling this is the degree of musculoskeletal and
cardiovascular fitness in elite athletes that may mediate
concussive type injury or reduce prolonged symptom presen-
tation. However, as seen in the case of the famous NHL player
Sidney Crosby, even the best player can unfortunately have a
prolonged symptom presentation.
Paralleling behavioural medicine, it is well known that a
patient’s pre-morbid or co-morbid psychological status can
affect both adherence to medical treatment and symptom
maintenance or resolution [31]. As stated elsewhere in this
article, co-morbid depression and anxiety are typical psycho-
logical responses to a concussion which, if prolonged or left
untreated, can mimic the neurocognitive symptoms of con-
cussion. Hou et al. [50] undertook a prospective study of
MTBI patients who presented at an Emergency Department to
investigate cognitive, social, behavioural and emotional risk
factors to predict PCS at 3 and 6 months post-injury. The
authors identified all-or-nothing behaviour (over activity
when feeling well, followed by extensive rest periods while
symptomatic) as the key predictor at 3 months and negative
head injury perceptions as best predicting PCS at 6 months.
Stress, anxiety and depression were also potent predictors of
PCS at 6 months post-injury. Notably, age, gender, GCS
score, LOC and amnesia did not predict PCS. As such,
cognitive and behavioural factors emerged as potent risk
predictors, validating the usefulness of cognitive-behavioural
approaches for early post-injury treatment intervention [50].
As is increasingly recognized, concussion does not solely
affect the central nervous system. Bigler [51] effectively
pointed out that concussions can impact many organ systems
in the body. There is increasing recognition that vestibular
and oculomotor dysfunction constitute prominent physical
PCS sequelae which, left untreated, prolong recovery.
Remediation techniques delineated below address these
symptoms, as well as other prominent PCS symptoms
including headache, concentration and working memory
decline and sleep disturbance. From a psychophysiological
perspective, concussions are known to alter the autonomic
nervous system, especially the sympathetic branch [52, 53].
Further, there are important cardiac correlates of a concussion
including alteration in heart rate variability [54, 55]. All of
these aetiologies can be amenable to psychological, neuro-
psychological or psychophysiological intervention.
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Education
One of the most benign treatments offered has been education,
provided primarily by means of presumably reassuring
information from medical staff and hand-outs at the emer-
gency room [56, 57]. This treatment traditionally has had
limited efficacy, since most sports-related concussions do not
present to an ER or a healthcare facility with a background in
traumatic brain injury and sometimes not even to a primary
care physician. More recently, a series of ‘Heads Up’
concussion management hand-outs developed by the Centers
for Disease Control has become available for free download
[58]. These excellent hand-outs are available for easy dissem-
ination to coaches, trainers, emergency rooms, urgent care
clinics, sports medicine centres, paediatric offices and youth
sports organizations. Education is a first step in treatment
when knowledge prompts players, parents and coaches to
quickly recognize and manage the concussion appropriately.
Cognitive behavioural therapy (CBT)
Cognitive Behavioural Therapy (CBT) is recommended as a
first line treatment for anxiety and depressive reactions in
athletes with refractory sports concussion. As noted earlier,
anger, anxiety and depression are typical reactions of an
injured athlete. For those elite athletes reluctant to elect
pharmacotherapy, a modified CBT approach may not only be
effective, but also can provide an internal locus of control
over the recovery process and formulation of an action plan,
congruent with an athlete’s natural preference for self-
efficacy [59, 60]. Using a modified CBT framework, injured
athletes should be alerted to cognitive distortions of
Overgeneralization and Catastrophizing [61, 62]. For exam-
ple, players may feel that their concussion is a sign of
weakness, may stress that their injury is a career-ending event
or harbour a catastrophic fear that they will develop Chronic
Traumatic Encephalopathy. The first stage in working with
the athlete is to identify the maladaptive cognitions or
distortions that either result from the injury or prolong
recovery by maintaining symptoms. The traditional thought
record systems [62] are useful here to identify and interrupt
negative cycles and can be expanded over the course of
treatment to incorporate positive cognitive mindsets which
enhance performance. Consonant with traditional CBT is the
development of rational, realistic alternatives to distorted
cognitions and formation of a realistic action plan.
Another application of CBT in concussion rehabilitation
addresses insomnia and parasomnias, as sleep disturbance is
increasingly recognized as prominent in refractory SRC. CBT
sleep protocols are an option for those athletes who do not
like the sedating properties of sleep medication, do not
respond well to their use or who have poor sleep hygiene [63].
CBT also could be paired with pharmacotherapy to potentiate
normalization of sleep.
Relaxation training
Behavioural Medicine approaches including training in
relaxation and stress management are readily used by athletes
with sports performance concerns and are easily extended to
the concussion population. In refractory concussion, athletes
are well served by training in breathing exercises, positive
imagery and relaxation [64] for acute stress, headaches and
autonomic arousal. Many elite and Olympic athletes know the
value of breathing for enhancing performance and have
worked with various breathing routines [65], so they respond
well to yogic or diaphragmatic breathing training. Less elite
athletes of all ages can also benefit from training in these
techniques. Specific relaxation and/or hypnotic induction
tapes, CDs or MP3 files are commercially available or can be
individually made for the athlete’s specific circumstances.
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,
including before a game [66].
Traditional relaxation approaches can be taught in the
office or locker room in a manner of minutes to athletes of all
ages and across all levels of play. This involves teaching the
athlete to relax and engage in slow diaphragmatic breathing,
while thinking positive thoughts and visualizing relaxing
imagery suggested by the clinician. Jacobsonian muscle
relaxation [67] is appealing to athletes, given the protocol
of tensing, then relaxing, the major muscle groups. In an
extension of the study of athletes with rapidly healing
orthopaedic injuries [47], positive self-talk and positive
imagery would be posited to assist in recovery from refractory
SRC, due to an enhanced sense of self-regulation and self-
efficacy.
Biofeedback
Biofeedback (BFB) interventions, also known as psycho-
physiological intervention, have a long and efficacious history
in the behavioural medicine literature [68] and in the sports
psychology literature [65]. They provide an alternative or
adjunct treatment for somatic features that may have a
psychophysiological component or as a means to address non-
malignant pathophysiology. Traditionally, biofeedback meth-
ods such as temperature biofeedback in the peripheries,
galvanic skin response/electrodermal response and electro-
myography have been used successfully with conditions such
as chronic headaches, depression, arthritis and other illnesses
[69]. At a basic level, biofeedback involves placing a sensor
on the body part of interest (e.g. a thermistor to measure
temperature of the fingers, an EMG sensor for muscle tension
from the frontalis or trapezius muscles or a photoplethysmo-
graph or 3-lead EKG for heart rate and heart rate variability).
The stimuli from that body part are fed into an analogue-
to-digital convertor/amplifier, then to a computer with
appropriate software to display the stimulus level. The
athlete’s stimuli can be fed back to them in the form of a
visual display or auditory signal. Through operant condition-
ing, the athlete can learn to change the signal in a desired
direction, to help reduce symptoms, remediate an injury or
optimize athletic performance [70].
It is well established that headaches are one of the most
common sequelae of SRC and may occur in up to 86% of
concussed athletes [71]. In addition to post-traumatic muscle
contraction headaches, a sub-set of injured athletes experi-
ence post-traumatic migraines, defined as a headache with
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nausea and either phono- or photo-sensitivity. Both types of
headache can compromise concentration, neurocognitive
efficiency, memory, balance and reaction time [72, 73]. A
traditional intervention for refractory tension headaches is
Electromyography (EMG) biofeedback. In a meta-analytic
review of treatment of headaches, Nestoriuc et al. [74] found
that EMG treatment was the most often used modality and the
most efficacious. The second most efficacious was a
combination of EMG and Thermal BFB, whereas EEG
treatment was not superior to relaxation therapies. For
migraine headaches, all types of biofeedback intervention
showed significant effect sizes. The highest treatment gains
for migraines occurred with Blood-Volume Pulse (BVP)
biofeedback, followed by Temperature biofeedback paired
with relaxation therapies [74]. Both of these approaches alter
vascular regulation and blood flow in what is hypothesized as
a neurovascular event. A comprehensive intervention pro-
gramme for post-traumatic headaches from motor-vehicles
accidents used Thermal and EMG biofeedback, progressive
muscle relaxation and CBT and resulted in more headache-
free days, a significant reduction in headache frequency and
intensity and minor reduction in anxiety [75]. A separate
review of paediatric migraines posited treatment success
using Thermal biofeedback alone [76]. Mixed EMG and
Thermal biofeedback is considered Level 4: Efficacious for
Adult Headaches and Level 3: Probably Efficacious for
Paediatric Headaches [69, 77, 78].
After a concussion, there can be an autonomic dysregula-
tion [78, 79] altering the metabolic and physiologic homeo-
static processes. Physiology amenable to BFB intervention is
due to sympathetic arousal in the autonomic nervous system.
Most commonly this results in vasoconstriction and lowered
temperature in the fingers and toes, as well as an increase in
the electrodermal response. Traditional thermal biofeedback
intervention involves measurement of finger-tip temperature
by placing a thermistor on the distal phalange of the index or
second finger of the non-dominant hand. Again, the actual
temperature of this extremity is measured and reflected on a
computer monitor or similar display. The athlete is taught
relaxation exercises and mental imagery that increase finger
temperature, paralleling relaxation of skeletal muscles, as
well as relaxation (dilatation) of the smooth muscles in the
arterial walls. Using an operant conditioning paradigm,
the athlete is rewarded for successive approximations
toward the target temperature by auditory tones and/or
visual displays. While core body temperature is 98.6F,
ideal finger temperature to remediate headaches is 92Ffor
men and 89F for women.
Increased electrodermal response (EDR) in the peripheries
is very reflective of sympathetic ANS arousal due to stress
and pain. EDR technology measures changes in electrical
resistance across sweat glands in the fingers. While an ideal
resting value for EDR is between 0–5 microSiemens (mS),
concussed individuals can have values between 10–20 mS or
greater and show extreme lability in response to external or
internal stressors. The EDR measurement is very sensitive to
negative thoughts and can reflect distressing ideation in less
than 2 seconds. As such, it is an ideal measure for teenage and
adult men who are symptom deniers and prefer not to discuss
problems, functioning as a de facto ‘lie detector’. Biofeedback
through auditory or visual feedback, relaxation and positive
imagery are intervention techniques for sympathetic arousal.
Heart rate variability training
A newer and popular form of psychophysiological biofeed-
back for sports performance and injuries is training in heart
rate variability (HRV) [80]. 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 parasympathetic branches of the ANS [81].
In cardiopathology, there is reduced variability between R-
waves which reflects illness and which can predict serious
cardiac events. Multiple studies have shown that an athlete’s
heart rate variability is reduced post-concussion [54, 55],
reflecting changes perhaps in the autonomic nervous system
driven by the vagus nerve [82, 83], both at rest and more
importantly at exertion. This reduction in heart rate variability
post-concussion may have implications for changes in cardiac
demand while performing sports, as well as reduced cerebro-
vascular perfusion. Lehrer et al. [84] developed a protocol for
heart rate variability training in medical conditions, particu-
larly asthma. Lagos et al. [85, 86] modified Lehrer et al.’s
heart rate variability training successfully with concussed
adolescents. They used a biofeedback protocol taught in the
office but then practiced at home. Number of office visits
varied from 5–10 sessions. This non-invasive HRV interven-
tion involves placement of a photoplethysmograph on the
finger or earlobe; a hand-held portable device (HeartMath,
Boulder Creek, CA) or computer monitor display to visually
guide respiration; and training to increase variability of
respiratory sinus arrhythmia resonant frequency breathing.
The hand-held device is portable and suitable for home use.
The resonant frequency varies by individual, gender and age,
but is usually between four-to-six breaths per minute.
Cognitive correlates of heart rate variability training, espe-
cially in the low frequency band, include better performance
on executive functioning tasks [87].
From a psychological perspective, these biofeedback
therapies enhance the athlete’s sense of self-efficacy, self-
regulation and control, all emotional factors appreciated by
athletes. Additionally, serious athletes are sensitive to their
own physiology, so biofeedback technologies which provide
accurate and external measurement of physical processes such
as temperature, muscle tension, nerve conduction velocity,
HRVand reaction time naturally help them to enhance athletic
performance. Not surprisingly, such techniques are widely
used by Olympic teams and trainers, especially the Canadian
Olympic teams [88].
Vestibular dysfunction intervention
Vestibular problems are one of the most common complaints
seen following SRC. They can present as problems with
balance, dizziness, nausea with visual tracking or classic
vertigo. Vestibular symptoms can manifest as part of the
traditional post-concussive triad of neurocognitive dysfunc-
tion, vestibular dysfunction and oculomotor dysfunction or
can present independently from neurocognitive impairment.
Traditional treatment is referral to a physical therapist with
specialized vestibular training. However, it is well known that
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psychological factors such as depression and anxiety can
exacerbate vestibular symptoms or interfere with their treat-
ment. Recognizing this relationship, some academic
Rehabilitation Medicine programmes now have a rehabilita-
tion psychologist who can provide education and treatment
for the psychological component of vestibulitis. Meholik [89]
at NYU Langone Medical Centre provides training in
cognitive behaviour therapy, mindfulness meditation and
relaxation training as components of their physical therapy
rehabilitation for vestibular dysfunction. This intervention has
been shown to improve emotional and physical domains of
patients and may improve selected cognitive domains.
Gilewski at Loma Linda Medical Centre (personal com-
munications by email) adds biofeedback to the above
approaches. He monitors increases in skin conductance as a
precursor measure of autonomic distress during movements
which trigger the vestibular symptoms (e.g. head turning,
visual tracking, bending over). As the athlete becomes aware
of autonomic arousal through biofeedback, they begin paced
breathing, which also helps attain optimal heart rate variabil-
ity. Bender et al. [90] uses a similar approach to vestibular
dysfunction, but adds a graded exposure component. Finally,
the Defense Centers of Excellence for Psychological Health
and Traumatic Brain Injury [91] produced a clinical recom-
mendation document for assessment and management of
dizziness associated with mild TBI. While there are no RCTs
for this intervention with vertigo, both paced breathing and
skin conductance represent psychological interventions for
this common but distressing and disabling sequelae of
refractory SRC. Similar training has been used with astro-
nauts to control symptoms of motion-induced sickness in
space travel and microgravity. Typical autonomic precursors
of motion sickness include a rise in skin conductance, drop in
skin temperature and higher heart rate. Psychophysiological
training involves learning GSR control first, then pairing this
with simulated exposure or actual motion by an athlete or
astronaut. Biofeedback treatment for motion sickness is
considered Level 4: Efficacious [92].
Neurofeedback
Perhaps the biofeedback intervention for concussions with the
least empirical data but touted as having great potential is
Neurofeedback. Neurofeedback involves measurement of the
electrical activity of the brain and its association with
cognitive states and processes. The patient learns through
operant conditioning to increase the amplitude of a desired
EEG frequency, usually while simultaneously decreasing the
amplitude of an undesired EEG frequency. Barr et al. [93] and
McCrea et al. [94] conducted two innovative studies
measuring the EEG correlates of frontal brain activity in
concussed athletes and found decreased left–right hemi-
spheric coherence and decreased Beta power (reflecting
decreased concentration abilities). Further, these electro-
physiological abnormalities lasted longer than impairment
noted on computerized neurocognitive testing, showed an
increase in abnormalities through Day 8 post-injury and were
present in some athletes at Day 45 post-injury. This interest-
ing protocol did not utilize the full 19-channel quantitative
EEG that is performed clinically. Other clinical protocols have
found abnormal EEG functioning post-concussion in posterior
areas, such as parietal and occipital areas, as well as problems
with coherence between adjacent and distant brain sites
measured by the 10–20 mapping system [95]. Thatcher [96]
notes that a Quantitative EEG with comparison to a normative
database is needed due to the idiosyncratic nature of changes
in neuroelectrical activity post-concussion and absence of a
specific electrical pattern post-concussion (as there usually is
in ADHD). He further notes that Coherence needs to be
measured over the entire brain, as this may be the most
sensitive measure of TBI in general. Coherence changes can
be noted with either higher levels of association (known as
hypercoherence) or lower levels of coherence (known as
hypocoherence) when comparing inter-hemispheric homolo-
gous brain sites. Either hyper- or hypo-coherence represents
an abnormal electrical activity shift from the default brain
network [97, 98]. Generally, optimal performance involves
production of higher Alpha range frequencies (10–12 Hz.)
paired with suppression of Theta waves (4–7 Hz). However,
the specific EEG pattern can be sport-specific for frequency
and specific location over the cortex, as identified by the
10–20 system.
A similar electrophysiological measure of brain electrical
activity post-concussion is the measurement of Event Related
Potentials (ERPs), especially the P300 wave, reflecting
attentional processes needed for working memory. While
Baillargeon et al. [99] hypothesized that younger athletes
would show greater reduction in P3b amplitude, their study
found that both children and adults post-sports concussion had
this P3b amplitude reduction and that it was detectible up to 1
year post-injury. Further, the P3b amplitude reduction
correlated with reduced working memory abilities during
that time period. Broglio et al. [100] found N2 and P3b
anomalies up to 3 years post-mild TBI in young adult athletes.
Ostensibly, the P3b abnormality can be addressed through
EEG biofeedback.
Linden [101] reported using neurofeedback successfully
with concussed athletes, although this is only at the case study
level and was not case controlled research. Tinius and Tinius
[102] treated young adults with MTBI (aetiology unstated)
with neurofeedback and successfully improved sustained
attention. Further, the EEG correlates of successful vs.
unsuccessful competitive athletes have been identified as a
reduction in high alpha frequencies and a greater feeling of
confidence [103]. For neurofeedback treatment, the electrical
signals are acquired exactly as with the clinical neurology 10–
20 19-channel clinical diagnostic EEG, but with a differential
amplifier that can feed back the EEG signal to the patient as
visual or auditory stimuli (Brain Master Technologies,
Bedford, OH). Through operant conditioning, the patient/
athlete is rewarded when they are in a target state (e.g. above
an amplitude threshold for a desired frequency and below an
amplitude threshold for an undesired frequency). It is beyond
the scope of this article to fully describe the hardware and
software programs available for psychophysiological and
neurophysiologic biofeedback, but the Schwartz and Andrasik
[104] text has excellent descriptions of both types of
equipment.
Clinically, it has been found that, in the early stages post-
concussion, athletes may become symptomatic during
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neurofeedback training, as there is extensive computer work
involved with the complex visual displays. For this reason,
basic relaxation paradigms with breathing exercises and
temperature biofeedback may be better suited to early
intervention and home practice. An option for the clinician
wishing to do early neurofeedback would be substitution of
auditory feedback providing soothing acoustic stimuli.
Sophisticated biofeedback software can use auditory feedback
chosen by the patient, including their preferred environmen-
tal/nature sounds or favourite music. More recently, novel
technologies have been marketed with appeal to young kids
and the middle school population; in these programs
neurofeedback is linked with sports-related games on a
computer screen (NeuroSports; BrainTrain, Richmond, VA).
Wearing a wireless EEG headset, the concussed child athlete
who obtains target brainwave criteria (individually set) can
mentally make free throws or kick field goals in computer
simulation.
Neurofeedback rehabilitation with concussed athletes is
still in its infancy and lacks a research base. It is ideally
guided by a full quantitative brain map (QEEG 19 channel
analysis) done post-concussion to understand the neuroelec-
trophysiologic correlates of concussion. It is interesting that
the clinical EEG performed by Neurology is now digitized
and has information needed to understand functional
neuroelectrophysiologic integrity, but neurologists focus
more on pathological processes such as spike and wave
discharges and abnormal slowing. However, the potential is
certainly there for a clinician to obtain the digital EEG output
file and analyse it through one of the commercial EEG
analytic programs used with functional brain mapping to
assess the integrity of electrophysiological functioning of the
human brain.
Cranial electrical stimulation
While electrical stimulation for musculoskeletal athletic
injuries is well documented, micro-current cranial electrical
stimulation (CES) of the brain in anxiety, depression and
insomnia is less well known. Rather than just monitoring
psychophysiological processes, CES involves administering
extremely low amplitude and low frequency current to an
athlete’s brain. While electrotherapy has been used for almost
100 years, more recently it is an exciting treatment being used
with soldiers diagnosed with PCS from IED blasts who have
accompanying PTSD. Theoretically, the stimulation (applied
with clip-on electrodes on each earlobe) increases levels of
serotonin and acetylcholine through brainstem activation,
thereby increasing alpha EEG, associated with greater
alertness and relaxation [105, 106]. Successful randomized
controlled trials of CES for pain and insomnia have been
conducted, but the majority of TBI studies are case studies,
except for a blinded study of severe TBI patients in a group
home [107]. While cognitive improvement with CES is not
well documented, improvement in headaches, anxiety
and insomnia, core symptoms in PCS, is well documented.
This symptom improvement may indirectly improve concen-
tration. With the use of CES for TBI/PCS/PTSD in the
military, there are on-going studies that may show efficacy in
these areas.
Cognitive rehabilitation
Cognitive rehabilitation (CR) has a long history as an
intervention for cognitive impairment after significant TBI,
CVA and other neurologic disorders. It is widely used in
Rehabilitation Medicine programmes. Evidence-based
reviews by Cicerone et al. [108, 109] and Rohling et al.
[110] have established the efficacy of cognitive rehabilitation
in both civilian and military populations. As working memory
and executive dysfunction are commonly seen in PCS, CR
interventions are most appropriate for these impairments.
Attention remediation through Attention Processing Training
typically involves exposure to both auditory and visual
stimuli, with increasing levels of difficulty and distracting
stimuli. This can be administered either through direct
training with a CR therapist or via a computer. However,
the earlier cautions about the adverse effects of computer
interaction with symptomatic patients during biofeedback
training also hold with this intervention. In fact, Cicerone
et al. specifically recommend against computerized cognitive
rehabilitation as a sole method of intervention. The Brain
Injury Interdisciplinary Special Interest Group of the
American Congress of Rehabilitation Medicine [109] has
published an evidence-based Cognitive Rehabilitation Manual
that provides exercises and strategies for direct intervention.
While direct intervention to address a specific cognitive
dysfunction can be a starting point, development of internal
strategies to enhance performance is usually more effective in
a patient with MTBI. Additional external cognitive prosthetic
devices, such as smartphones, can function as cueing and
memory devices, in addition to using lists for organization
and prioritization and portable voice recorders. Of course, low
tech devices such as 3 5 note cards, Post It Notes (tm) and
pocket wirebound notebooks can serve a similar purpose.
Additionally, Attention Process Training (APT) has been
found to have positive effects on other cognitive functions, as
attention is a basic gateway for cognitive processing [111].
In addition to face-to-face cognitive rehabilitation and
workbooks, there also is a large body of computer-assisted
cognitive rehabilitation programmes (CACR) [112, 113]. As
noted, for athletes in the early stages of recovery or those
prone to become symptomatic with computer usage, use of
these programmes should be delayed. However, in later stages
of recovery and as an adjunct to traditional CR, these
programmes can provide effective home practice [114].
Special considerations for paediatric
concussed patients
There is growing consensus that younger athletes are at higher
risk of slower recovery and, therefore, require more cautious
RTP decision-making [115–118]. This is particularly the case
in the paediatric population, where brain growth and devel-
opment is rapidly advancing. Unfortunately, the mechanism of
injury in paediatric sports concussion is least often studied
and based on theory more than empirical evidence [99, 118].
Early assumptions about the protective effects of neuroplas-
ticity [119, 120] have been challenged by newer brain models
suggesting that the developing brain may be more sensitive to
concussion [121–125]. Problematically, neither model has
been stringently tested with large paediatric samples using
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standardized and sensitive baseline or post-injury measures.
Heterogeneity in the infrastructure of YRS programmes,
reliance on volunteer coaches without concussion training and
infrequent presence of Certified Athletic Trainers at YRS
games impede data collection on the incidence, severity and
recovery of paediatric sports concussions [118]. Assessment
of the paediatric concussed athlete requires awareness and
training in stages of child development and modification of
language and questionnaire items to fit the child’s develop-
mental level [126]. Neurocognitive measures must be appro-
priate to young children and have age-based norms. With a
few notable exceptions, few of these measures have both age
norms and multiple equivalent forms for tracking recovery
[99, 127, 128].
Post-concussion treatment intervention with a paediatric
population requires a constant interface with parents and
school personnel. Elementary aged students have one
primary teacher, which simplifies the Returning to
Learning (RTL) process. Cognitive and physical rest is
most readily achieved by school absence, modified day
scheduling and modified classwork and homework assign-
ments. Parent resistance to these school-based interventions
tends to be low for elementary aged students. Early on,
parents are coached on play activities that minimize attention
and memory in favour of relaxing social and family
activities. If neurocognitive PCS continue, game-like activ-
ities or structured intervention can be used to build attention
and working memory. Younger athletes are generally more
open to biofeedback interventions, as children like the
physical and game-like approach of these programmes and
also experience positive placebo effects [129]. Relaxation
training long used with paediatric populations [130] can be
readily transferred to the concussed elementary aged athlete
and used in a home programme.
Middle and high school injured student-athletes require
more documentation to implement academic modifications
and this aspect of treatment is essential to the recovery
process [131]. Meehan et al. [118] posits that the job of this
age student is to rapidly acquire large amounts of new
learning and to be prepared for frequent evaluations to
demonstrate such proficiency. Medical and neurocognitive
testing data provide a critical role in the documentation phase
needed to access appropriate Returning to Learning supports.
Parent and teacher education and support is critical,
emphasizing the need for reduced short-term cognitive
exertion in the interests of long-term recovery [132]. The
just-released American Academy of Paediatrics (AAP)
Position Statement on Returning to Learning Guidelines
[133] produced for paediatricians emphasizes the need for an
integrated team approach that includes parents, teachers,
athletic staff, the school nurse and guidance counsellor and
the SRC trained physician or neuropsychologist. This level of
co-ordination is particularly critical in refractory concussion
management, where more extended support is needed [131].
Since the academic role is primary for this population, failure
to adapt school demands during cognitive recovery will
trigger anxiety or non-compliance that attenuates the efficacy
of formal concussion rehabilitation treatments implemented.
RTL guidelines in the Healthcare Plan must be flexibly
adapted as recovery progresses.
Regarding treatment intervention, the middle through
high school population is especially amenable to training in
relaxation, guided imagery, biofeedback and record keeping
for headache logs to identify triggers [129]. By this age,
student-athletes are developmentally able to understand and
follow the step-wise and logical process needed to effect-
ively use CBT interventions [61, 62, 74, 134]. The inherent
reward provided by enhancing self-efficacy and internal
locus of control discussed earlier [60] also applies to Junior
Varsity and Varsity athletes. Cognitive rehabilitation inter-
vention, including computer and smart phone applications, is
readily available and enjoyed by this age group. Awareness
of family and peer social systems dynamics in this age
population is essential. For example, the athlete side-lined
from play may retain group identity by being a scorekeeper
or an assistant-manager and practicing in-session role-
playing about explaining the concussion to peers may
reduce social anxiety. Access to peers who have experienced
and recovered from a concussion reduces the sense of
isolation and anxiety about recovery in the Junior Varsity or
Varsity athlete [135]. Parent education about irritability and
executive PCS sequelae including reduced awareness of
deficits can do much to prevent parent–child conflict during
the recovery process. Finally, family systems interventions
that target parental reactions to their child/adolescent’s
injury can be pivotal in assisting refractory concussion
recovery. In the case of a child or adolescent with pre-
existing risk factors including prematurity, ADHD/LD,
seizures, migraines or prior concussions, referral to a child
and adolescent neuropsychologist should be strongly con-
sidered, as there is greater risk of a protracted recovery
process [136].
Summary
Overall, the authors have tried to extend the
BioPsychoSocial framework to the evaluation and treatment
of the cardinal symptoms of refractory sports-related con-
cussion. Paramount to this approach is a multi-level, multi-
dimensional interactive paradigm for establishing aetiology,
factors that are prolonging the symptoms and inhibiting
recovery and suggestions for targeting interventions. Non-
pharmacologic interventions include Cognitive-Behavioural
Therapy, Psychophysiological and Neurophysiologic bio-
feedback therapies and cognitive rehabilitation. While some
of these interventions have limited empirical data with sports
concussions, they have been used successfully with other
similar populations or illnesses. A common factor is that
athletes prefer techniques which are active, parallel their
positive motivational set and enhance their self-efficacy.
Much more research needs to be performed to extend the
clinical results. While recent studies and media attention
have exponentially increased awareness about the incidence
and complexity of sports-related Post-Concussion Syndrome,
the focus has primarily been on symptoms and prevention.
This article has instead tried to focus on treatment
and rehabilitation interventions with tested or potential
efficacy for the growing population of athletes across the
lifespan experiencing refractory or prolonged Post-
Concussion Syndrome.
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Acknowledgements
We wish to sincerely thank Ms. Lauren Conder for her
diligent research assistance through The University of North
Carolina at Chapel Hill Library.
Declaration of interest
The authors report no conflicts of interest. The authors alone
are responsible for the content and writing of the paper.
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... Postconcussion symptom inventories are employed by diverse healthcare providers, including physicians, psychologists, and certified athletic trainers, and can be used as an initial screening for mood/emotional symptomology and can help determine if more comprehensive evaluation is warranted. Researchers and clinicians have recommended utiltizing standardized self-report inventories for anxiety, depression, and mood states, such as the modified Beck Depression Inventory (Beck et al., 2000), to help the clinician identify an anxiety/mood clinical profile and athletes at risk for protracted recovery following SRC (Conder & Conder, 2015). These tools, which are easy to administer with minimal necessary qualifications, help to decrease the likelihood of a false positive diagnosis of depression due to actual physical symptoms of injury. ...
... For example, if anxiety is revolving around pressure to return to sport or sadness regarding loss of skill set, then the athlete may benefit from therapy with a psychologist or counseling from a sport psychology professional. If anxiety is more generalized (e.g., academics, social stressors) or the athlete lacks adequate coping skills, referral to a mental health professional who provides supportive and cognitive-behavioral therapy may be the first line of treatment (Conder & Conder, 2015). Although there is limited empirical support for the effectiveness of specific psychological approaches with athletes following concussion, a variety of approaches have been recommended, including biofeedback, relaxation training, and mindfulness meditation (Conder & Conder, 2015;Seguin & Durand-Bush, 2019). ...
... If anxiety is more generalized (e.g., academics, social stressors) or the athlete lacks adequate coping skills, referral to a mental health professional who provides supportive and cognitive-behavioral therapy may be the first line of treatment (Conder & Conder, 2015). Although there is limited empirical support for the effectiveness of specific psychological approaches with athletes following concussion, a variety of approaches have been recommended, including biofeedback, relaxation training, and mindfulness meditation (Conder & Conder, 2015;Seguin & Durand-Bush, 2019). In addition to cognitive and behavioral approaches to treatment, prescribed medications may be employed by physicians or psychologists (in states where prescription rights exist) when more conservative approaches are ineffective. ...
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The field of sport-related concussion (SRC) is evolving quickly, and psychological aspects affecting athletes’ recovery and well-being are now recognized as an important component for research and clinical practice. There has been considerable recent emphasis on empirical research into the psychological implications of SRC. This emphasis reflects trends from clinical research that indicate anxiety and mood-related issues may represent the primary symptoms in nearly 30% of concussions. In short, SRC and its psychological aspects is a major issue that influences not only athletes’ performance, but also their physical and mental health. The purpose of this position paper is to provide a concise yet comprehensive review of the current state of research and evidence-based practice as it relates to the psychological aspects of SRC. More specifically, we present five postulates that are intended to stimulate discussion among researchers and allied health professionals who are interested in psychological aspects of SRC. Our intent in writing this position paper is to advance this subdiscipline within the area of SRC by discussing areas for growth in theory, research, and practice. Lay Summary: Sport-related concussions (SRC) have become a public health issue, however little research has focused on the the psychological aspects of this injury. This position paper identifies five postulates that are intended to stimulate research and practice on psychological aspects of SRC. • Implications for Practice • Multidisciplinary concussion care teams should include a sport psychology professional to assist with psychosocial recovery and well-being. • Identify psychological factors that detract athletes from feeling ready to return to sport following a concussion (e.g., confidence, fear), and work with them to develop coping strategies to assist their return. • Appropriately trained sport psychology professionals could deliver effective concussion education interventions that involve behavior change techniques.
... Concussion can exacerbate preexisting mental health conditions and new psychological issues can be caused by both the injury itself and the recovery process. 38,39 Ellis et al 40 found that 11.5% of youth with sports-related concussions endorsed psychological symptoms, and that a higher PCSS score predicted the presence of a mental health disorder. However, many patients with low PCSS scores also had preexisting or new mental health disorders. ...
... 41,42 Evidence-based psychological interventions for PCS symptoms, including headaches and dizziness, include Cognitive-Behavioral Therapy (CBT) and biofeedback. 38,40 A previous study found that pediatric PCS patients receiving a collaborative intervention that included CBT showed significant improvements compared with adolescents who received standard care from sports medicine providers and neuropsychologists. 43 Early evaluation by a mental health provider may help to facilitate screening of a greater proportion of PCS patients for contributing psychological factors, yielding more consistent initiation of such therapies for those who need them. ...
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Objective: To describe the collaborative findings across a broad array of subspecialties in children and adolescents with postconcussion syndrome (PCS) in a pediatric multidisciplinary concussion clinic (MDCC) setting. Design: Retrospective analysis. Setting: Multidisciplinary concussion clinic at a pediatric tertiary-level hospital. Patients: Fifty-seven patients seen in MDCC for evaluation and management of PCS between June 2014 and January 2016. Interventions: Clinical evaluation by neurology, sports medicine, otolaryngology, optometry, ophthalmology, physical therapy, and psychology. Main outcome measures: Specialty-specific clinical findings and specific, treatable diagnoses relevant to PCS symptoms. Results: A wide variety of treatable, specialty-specific diagnoses were identified as potential contributing factors to patients' postconcussion symptoms. The most common treatable diagnoses included binocular vision dysfunction (76%), anxiety, (57.7%), depression (44.2%), new or change in refractive error (21.7%), myofascial pain syndrome (19.2%), and benign paroxysmal positional vertigo (17.5%). Conclusions: Patients seen in a MDCC setting receive a high number of treatable diagnoses that are potentially related to patients' PCS symptoms. The MDCC approach may (1) increase access to interventions for PCS-related impairments, such as visual rehabilitation, physical therapy, and psychological counseling; (2) provide patients with coordinated medical care across specialties; and (3) hasten recovery from PCS.
... Concussion can exacerbate preexisting mental health conditions and new psychological issues can be caused by both the injury itself and the recovery process. 38,39 Ellis et al 40 found that 11.5% of youth with sports-related concussions endorsed psychological symptoms, and that a higher PCSS score predicted the presence of a mental health disorder. However, many patients with low PCSS scores also had preexisting or new mental health disorders. ...
... 41,42 Evidence-based psychological interventions for PCS symptoms, including headaches and dizziness, include Cognitive-Behavioral Therapy (CBT) and biofeedback. 38,40 A previous study found that pediatric PCS patients receiving a collaborative intervention that included CBT showed significant improvements compared with adolescents who received standard care from sports medicine providers and neuropsychologists. 43 Early evaluation by a mental health provider may help to facilitate screening of a greater proportion of PCS patients for contributing psychological factors, yielding more consistent initiation of such therapies for those who need them. ...
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Absence of the pericardium is a rare congenital disease in which the fibroserum membrane covering the heart is partially or totally absent. It is characterized by few echocardiography (ECG) and imaging features that can mislead the diagnosis to an inherited cardiac disease, such as arrhythmogenic right ventricular cardiomyopathy. Although it has often a benign course, this congenital defect should be identified as in some cases herniation and strangulation can be life-threatening and cause sudden cardiac death. Red flags on ECG (sinus bradycardia, variable T-wave inversion), chest x-ray (Snoopy sign, absence of tracheal deviation, and esophagus impression), and transthoracic echocardiogram (unusual windows, teardrop left ventricle, and elongated atria) should rise the suspicion of pericardium absence. The correct diagnosis, confirmed by cardiac magnetic resonance, is mandatory as the consequences on the sport activity certification, the management, and the treatment are extremely different.
... Such clinical symptoms are generally resolved within an acute phase of 10 to 14 days following the trauma [1]. However, for 10-15% of athletes, symptoms persist beyond this acute phase [10], causing significant emotional distress, functional limitations, and delayed return to daily activities [11,12]. Previous research found that psychological reactions, such as stress and anxiety, were associated with developing and maintaining symptoms that persisted beyond the expected 10-14 day recovery period, suggesting a failure of normal clinical recovery [1,[13][14][15]. ...
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Sport-related concussion is a serious public health issue affecting millions of individuals each year. Among the many negative side effects, emotional symptoms, such as stress, are some of the most common. Stress management is repeatedly cited by expert groups as an important intervention for this population. It was shown that music has relaxing effects, reducing stress through the activation of brain areas involved in emotions and pleasure. The objective of this study was to explore the effects of a music-listening intervention compared with silence on experimentally induced stress in concussed and non-concussed athletes. To this aim, four groups of athletes (non-concussed music, non-concussed silence, concussed music, and concussed silence) performed the Trier Social Stress Test, for which both physiological (skin conductance level) and self-reported stress measurements were taken. No significant difference was found in the pattern of stress recovery for self-reported measurements. However, the skin conductance results showed greater and faster post-stress recovery after listening to music compared with silence for concussed athletes only. Taken together, these results suggest that music could be an efficient stress management tool to implement in the everyday life of concussed athletes to help them prevent stress accumulation.
... 11 Studies with adults suggest that CBT interventions that include these elements may relieve symptoms after traumatic brain injury. [12][13][14] Yet, the literature is more scant for pediatric populations. One pre-post pilot study of CBT for adolescents with PPCS found that a brief 4-session treatment delivered weekly was associated with decreases in symptoms and improvements in quality of life. ...
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Importance Despite the high level of impairment for adolescents with persistent postconcussive symptoms, few studies have tested whether such problems can be remediated. Objective To examine whether collaborative care treatment is associated with improvements in postconcussive, quality of life, anxiety, and depressive symptoms over 1 year, compared with usual care. Design, Setting, and Participants The Collaborative Care Model for Treatment of Persistent Symptoms After Concussion Among Youth II Trial was a randomized clinical trial conducted from March 2017 to May 2020 with follow-up assessments at 3, 6, and 12 months. Participants were recruited from pediatric primary care, sports medicine, neurology, and rehabilitation clinics in western Washington. Adolescents aged 11 to 18 years with a diagnosed sports-related or recreational-related concussion within the past 9 months and with at least 3 symptoms persisting at least 1 month after injury were eligible. Data analysis was performed from June to September 2020. Interventions The collaborative care intervention included cognitive behavioral therapy and care management, delivered mostly through telehealth, throughout the 6-month treatment period, with enhanced medication consultation when warranted. The comparator group was usual care provided in specialty clinics. Main Outcomes and Measures Primary outcomes were adolescents’ reports of postconcussive, quality of life, anxiety, and depressive symptoms. Secondary outcomes were parent-reported symptoms. Results Of the 390 eligible adolescents, 201 (51.5%) agreed to participate, and 200 were enrolled (mean [SD] age, 14.7 [1.7] years; 124 girls [62.0%]), with 96% to 98% 3- to 12-month retention. Ninety-nine participants were randomized to usual care, and 101 were randomized to collaborative care. Adolescents who received collaborative care reported significant improvements in Health Behavior Inventory scores compared with usual care at 3 months (3.4 point decrease; 95% CI, −6.6 to −0.1 point decrease) and 12 months (4.1 point decrease; 95% CI, −7.7 to −0.4 point decrease). In addition, youth-reported Pediatric Quality of Life Inventory scores at 12 months improved by a mean of 4.7 points (95% CI, 0.05 to 9.3 points) in the intervention group compared with the control group. No differences emerged by group over time for adolescent depressive or anxiety symptoms or for parent-reported outcomes. Conclusions and Relevance Although both groups improved over time, youth receiving the collaborative care intervention had fewer symptoms and better quality of life over 1 year. Intervention delivery through telehealth broadens the reach of this treatment. Trial Registration ClinicalTrials.gov Identifier: NCT03034720
... Considering evidence that repeated subconcussive head impacts can have similar cumulative effects to those of SRC (Adler et al., 2018), some portion of our false-positive classifications may have included individuals who possess a similar risk profile without having sustained a past diagnosis of SRC. A biopsychosocial approach to performance optimization requires a comprehensive assessment of physical, mental, and social well-being to guide possible delivery of interventions other than those typically administered by a traditional pathophysiological approach (Conder & Conder, 2015), which the 82-item OWI response profile might facilitate. Further research involving a larger number of athletes will be needed to establish symptom profiles that may help guide an individualized approach to clinical management. ...
Article
Recent research findings have strongly suggested that sport-related concussion (SRC) increases risk for subsequent injury of any type, as well as a potential for long-term adverse effects on neurological and psychological well-being. The primary purpose of this study was to explore the reliability and discriminatory power of clinical testing procedures for detecting persisting effects of SRC. We used a cross-sectional study design to assess both self-reported symptoms commonly associated with post-concussion syndrome, and the effects of mental or physical activity on metrics derived from a smartphone app designed to test perceptual-motor responses. Among 30 physically active college students, 15 participants reported a SRC occurrence prior to testing ( M time-since-injury = 4.0 years, SD = 3.1, range = 5 months to 11 years). We found good test-retest reliability for key metrics derived from the smartphone app (ICC ≥ .70); and the internal consistency for the Overall Wellness Index (OWI) for 10 categories of 82 post-concussion symptoms was ideal (Cronbach’s α ≥ .80). Moderate intensity treadmill running demonstrated the strongest differential effect on perceptual-motor responses between participants with a history of SRC (HxSRC) and those with no such history (No SRC), which was best represented by the speed-accuracy trade-off quantified by the inverse efficiency index (IEI: group X trial interaction p = .055). Self-reported OWI symptoms ≥4 and post-physical activity IEI ≥ 568 ms provided the strongest discrimination between HxSRC and NoSRC participants (≥1 versus 0: OR = 9.75). Our findings suggest that persisting effects from a remote SRC occurrence can be detected by easily administered screening procedures that have the potential to identify individual athletes who might derive benefit from interventions to restore their optimal function and well-being.
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A complexity of biological, psychological, environmental and systemic factors influences a child's adaption after acquired brain injury (ABI), all of which transform as the child matures. Multidisciplinary rehabilitation teams are challenged by balancing family system needs and the child's needs, whilst promoting the child's functional skills in difficult or unappealing tasks. This paper presents the conceptual basis for a model for use in childhood ABI neurorehabilitation to address these challenges. A non-systematic narrative review of literature pertinent to integrated neurorehabilitation of pediatric ABI was conducted. Contemporary models of adult and pediatric psychosocial adaptation involving identity following ABI were reviewed. Key findings were then synthesized with models of pediatric resilience and self-concept development. The resulting model describes a cyclical adaptation process whereby the child learns experientially about their self and their world after ABI. Processes of identity development play a central role - particularly emotive processes of self-evaluation - by influencing the child's motivation for participation, tolerance for challenge, self-regulation and emerging self-awareness. The model directs clinicians to use the psychosocial processes of identity development to enhance the child's willingness and capacity to engage in the daily challenges of rehabilitation. Further systematic development and evaluation of the model is needed.
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