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American Medical Society For Sports Medicine Position Statement On Concussion in Sport

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American Medical Society For Sports Medicine Position Statement On Concussion in Sport

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Position Statement

American Medical Society for Sports Medicine


Position Statement on Concussion in Sport
Kimberly G. Harmon, MD,*† James R. Clugston, MD,‡§ Katherine Dec, MD,{ Brian Hainline, MD,‖
Stanley A. Herring, MD,** Shawn Kane, MD,†† Anthony P. Kontos, PhD,‡‡ John J. Leddy, MD,§§
Michael A. McCrea, PhD,{{║║ Sourav K. Poddar, MD,*** Margot Putukian, MD,††† Julie C. Wilson, MD,‡‡‡ and
William O. Roberts, MD§§§

Abstract: Sport-related concussion (SRC) is a common injury in recreational and organized sport. Over the past 30 years, there
has been significant progress in our scientific understanding of SRC, which in turn has driven the development of clinical guidelines
for diagnosis, assessment, and management of SRC. In addition to a growing need for knowledgeable health care professionals to
provide evidence-based care for athletes with SRC, media attention and legislation have created awareness and, in some cases,
fear about many issues and unknowns surrounding SRC. The American Medical Society for Sports Medicine formed a writing group
to review the existing literature on SRC, update its previous position statement,1 and address current evidence and knowledge gaps
regarding SRC. The absence of definitive outcomes-based data is challenging and requires relying on the best available evidence
integrated with clinical experience and patient values. This statement reviews the definition, pathophysiology, and epidemiology of
SRC, the diagnosis and management of both acute and persistent concussion symptoms, the short- and long-term risks of SRC
and repetitive head impact exposure, SRC prevention strategies, and potential future directions for SRC research. The American
Medical Society for Sports Medicine is committed to best clinical practices, evidence-based research, and educational initiatives
that positively impact the health and safety of athletes.
Key Words: concussion, sport, athlete, youth
(Clin J Sport Med 2019;29:87–100)

Submitted for publication November 13, 2018; accepted November 30, 2018. BACKGROUND AND PURPOSE

From the Departments of *Family Medicine; and Orthopaedics and Sports The American Medical Society for Sports Medicine (AMSSM)
Medicine, University of Washington, Seattle, Washington; Departments of
‡ represents more than 3800 sports medicine physicians who have
Community Health; and §Family Medicine and Neurology, University of Florida,
Gainesville, Florida; {Department of Physical Medicine and Rehabilitation, and completed specialty training in sports medicine after a residency
Orthopaedic Surgery, Virginia Commonwealth University, Richmond, Virginia; program in family medicine, internal medicine, pediatrics,

National Collegiate Athletic Association, Indianapolis, Indiana; **Department of emergency medicine, or physical medicine and rehabilitation,
Rehabilitation Medicine, University of Washington, Seattle, Washington; many of whom have extensive expertise in concussion evaluation
††
Department of Family Medicine, University of North Carolina, Chapel Hill, North
Carolina; ‡‡Department of Orthopedic Surgery, University of Pittsburgh, Pittsburgh,
and management including serving as sideline team physicians at
Pennsylvania; §§UBMD Department of Orthopaedics and Sports Medicine, State all levels of sport. Sport-related concussion (SRC) is an important
University of New York at Buffalo, Buffalo, New York; Departments of {{Neurosur- topic for sports medicine physicians, and there is a rapidly
gery; and ║║Neurology, Medical College of Wisconsin, Milwaukee, Wisconsin; expanding knowledge base in this area. Sport-related concussion
***
Department of Family Medicine and Orthopedics, University of Colorado, Denver,
has become a focus of both public concern and media attention.
Colorado; †††Princeton University, University Health Services, Internal Medicine/
Sports Medicine, Rutgers—Robert Wood Johnson Medical School, New Bruns- The purpose of this statement was to provide a narrative review
wick, New Jersey, Princeton, New Jersey; ‡‡‡Department of Orthopedics, University of the existing literature and best practices to assist health care
of Colorado, Aurora, Colorado; and §§§Department of Family Medicine and providers with the evaluation and management of SRC, and to
Community Health, University of Minnesota, Minneapolis, Minnesota. establish the level of evidence, current knowledge gaps, and areas
Kimberly Harmon has research grants from Vulcan Industries and the Pac-12, requiring additional research. The first AMSSM position
outside of submitted work. Jay Clugston reports grants from Banyan Biomarkers,
statement on SRC was published in 2013, and this is an update
grants from Floriday High Tech Corridor Matching Funds Program, and grants from
NCAA-DoD CARE Consortium outside of submitted work. Stan Herring has stock to that statement.1
options in Vicis, outside of submitted work. Anthony Kontos has research contracts
with GE-NFL Head Health Initiative, Abbott Labs and ELMindA, and receives
royalties from the book “Concussion”, outside submitted work. John Leddy has
research grant from the AMSSM outside of submitted work.
WRITING GROUP SELECTION AND PROCESS
All authors have submitted disclosure forms. The AMSSM Board of Directors appointed the chair (K.G.H.)
This article has been co-published in the British Journal of Sports Medicine. to assemble a writing group that was carefully selected to
Corresponding Author: Kimberly G. Harmon, MD, Departments of Family Medicine; include a balanced panel of sports medicine physicians
and Orthopaedics and Sports Medicine, University of Washington, 3800 Montlake experienced in sideline and office evaluation and management
Blvd, Seattle, WA 98195 ([email protected]). of SRC, actively engaged in SRC research, and with
Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved. demonstrated leadership in the area of SRC. Select sub-
http://dx.doi.org/10.1097/JSM.0000000000000720 specialty experts were invited to provide diverse viewpoints.

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K.G. Harmon et al. (2019) Clin J Sport Med

TABLE 1. Strength of Recommendation that have limitations when extrapolated to humans. It seems that
Taxonomy stress applied to the neuron causes changes in intracellular ion
concentrations, indiscriminate release of neurotransmitters,
Strength of
Recommendation Basis for Recommendation
mitochondrial dysfunction leading to the production of reactive
oxygen species, and increased utilization of glucose to restore
A Consistent, good-quality patient-oriented sodium and potassium balance.5 The increased glucose utiliza-
evidence
tion combined with the injury-related decrease in resting cerebral
B Inconsistent or limited-quality patient- blood flow creates an energy mismatch.6,7 Inflammatory cell
oriented evidence activation, axonal degeneration, and altered plasticity may occur
C Consensus, disease-oriented evidence, usual in the subacute and chronic stages of concussion. Animal and
practice, expert opinion, or case series for human studies support the concept of increased brain vulnera-
studies of diagnosis, treatment, prevention, or bility after an initial injury to a second brain tissue insult that can
screening
result in worsening cellular metabolic changes and more
significant deficits.8–10
Select members of the board, the publications committee, and
the writing group were surveyed to determine topics of interest
for the statement and generate an initial outline. Systematic EPIDEMIOLOGY
reviews were used as primary literature sources when avail- Concussion is common in organized scholastic and non-
able. The writing group engaged in conference calls, review of scholastic sport, nontraditional recreational activity (eg, ex-
the literature, and written communication before an in-person treme, individual), and routine activities of daily living. A recent
meeting in Chicago, IL, on February 9–10, 2018. There were report using data from emergency department visits, office
additional conference calls, emails, and iterations of the visits, and a high school injury surveillance system estimated 1.0
outline and manuscript to produce the final document. This to 1.8 million SRCs per year in the age range of 0 to 18 years and
document uses the Strength of Recommendation Taxonomy a subset of about 400 000 SRCs in high school athletes.11
to grade level of evidence2 (Table 1). Although this estimate is likely accurate, determining actual
sport- or activity-based concussion rates is difficult.
Injury surveillance systems in the United States primarily
WHO SHOULD EVALUATE AND MANAGE SPORT- study a small sample of organized college or high school sports
RELATED CONCUSSION? to estimate concussion rates. Numbers are limited or not
The clinical care, including assessment and management, of available for recreational or club sports or for activities such as
athletes with SRC is ideally performed by health care bicycling, skiing, snowboarding, skateboarding, and the
professionals with appropriate training and experience. fighting arts or for youth/early adolescent athletes. An
Sports medicine physicians are uniquely trained to provide estimate of risk requires a numerator (the number of
care along the continuum of SRC from the acute evaluation concussions) and a denominator (the amount of time
through return to learn and return to sport, and to manage participating in the activity). Numerators may vary based on
both complications of SRC and coexisting medical issues. underreporting or overreporting of concussion or inaccurate
Although most of the SRCs resolve within 1 to 4 weeks, diagnosis while denominators are difficult to accurately track.
athletes with complicated or prolonged recovery may require Most current estimates use “athlete-exposures” as the de-
a multidisciplinary team with specific expertise across the nominator, defined as an athlete participating in one practice
scope of concussion management. or game; however, estimates of risk may change dramatically
if actual hours of participation are tracked or if a seasonal or
annual risk of concussion is determined. Seasonal or annual
DEFINITION OF CONCUSSION risk may be a more readily understood concept. It is estimated
that more than 50% of concussions in high school–aged youth
Concussion is defined as a traumatically induced transient
are not related to organized sports, and only 20% are related
disturbance of brain function that involves a complex
to organized school team sports.11 Between 2% and 15% of
pathophysiologic process.1 Concussion is a subset of mild
athletes participating in organized sports will suffer a concus-
traumatic brain injury, which is classified based on acute
sion during one season12–29 (Table 2).
injury characteristics at the less severe end of the brain injury
spectrum.1 The clinical signs and symptoms of concussion
cannot be otherwise explained by drug, alcohol, medication DIAGNOSIS OF CONCUSSION
use, other injuries (such as cervical injuries or peripheral The diagnosis of concussion is challenging and based on
vestibular dysfunction), or other comorbidities (psychological clinical assessment. Concussion diagnosis is complicated by
or medical conditions).3,4 a lack of validated, objective diagnostic tests, a reliance on self-
reported symptoms, and confounding symptoms caused by
other common conditions. Nonspecific symptoms such as
PATHOPHYSIOLOGY
headaches, mood changes, “fogginess,” dizziness, visual
The pathophysiology of concussion is not completely understood changes, fatigue, and neck pain are all associated with
but has been characterized as force delivered to the brain causing concussion but can also originate from other etiologies. In
disruptive stretching of neuronal cell membranes and axons addition, symptoms may be delayed in onset or initially
resulting in a complex cascade of ionic, metabolic, and unrecognized by the athlete. Concussion remains a clinical
pathophysiologic events.5 Current understanding of the patho- diagnosis made by carefully synthesizing history and physical
physiology of concussion is primarily based on animal models examination findings as the injury evolves.

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TABLE 2. Seasonal Risk of Concussion in Sports


Concussed per
Author Type of Athletes Years of Study No. of Seasons Total No. of Athletes Concussed Player/Season (%)
Football
Barr15 High school and college football 1997-1999 2 1313 50 1.9
McCrea18 High school and college football 1998-1999 2 1325 63 2.4
McCrea17 High school and college football 1999-2001 3 2385 91 3.8
McCrea19 College football 1999-2001 2 94 3.9
Barr16 High school and college football 2008-2009 2 823 59 7.2
Seidman24 High school football 2013 1 343 9 2.6
Dompier25 Football 2012-2013 2 20 479 1178 5.8
Youth football 2012-2013 2 4092 136 3.3
High school football 2012-2013 2 11 957 767 6.4
College football 2012-2013 2 4430 275 6.7
College football 2011-2014 4 9718 518 5.3
26
Houck College football 2006-2015 9 945* 118 12.5
Bretzin14 High school football 2015-2016 1 39 520 1530 3.9
Total football 67 133 3192 4.8
All sports
Galetta27 Football, sprint football, men’s and women’s soccer, 2010-2011 1 219 10 4.6
and basketball
Marindes20 College athletes 2011-2012 1 217 30 13.8
Galetta21 Ice hockey/lacrosse youth and college 1 332 12 3.6
Leong28 Football, men’s and women’s basketball 2012-2013 1 127 11 8.7
Putukian22 College athletes 2011-2012 1 263 32 12.2
Chin23 High school and college athletes 2012-2014 3 2018 166 2.7
Kerr12 NCAA athletes 2011-2014 4 32 156 1410 4.4
Men’s baseball 2011-2014 4 1757 13 0.7
Men’s basketball 2011-2014 4 1889 74 3.9
College football 2011-2014 4 9718 518 5.3
Men’s ice hockey 2011-2014 4 3689 253 6.9
Men’s lacrosse 2011-2014 4 1768 44 2.5
Men’s soccer 2011-2014 4 1810 29 1.6
Men’s wrestling 2011-2014 4 821 65 7.9
Women’s basketball 2011-2014 4 1690 90 5.3
Women’s ice hockey 2011-2014 4 1301 94 7.2
Women’s lacrosse 2011-2014 4 1522 49 3.2
Women’s softball 2011-2014 4 1569 38 2.4
Women’s soccer 2011-2014 4 2831 93 3.3
Women’s volleyball 2011-2014 4 1791 50 2.8
Dhawan29 Youth hockey 1 141 20 14.2
Tsushima13 Athletes grade 8-12 2013-2014 1 10 334 1250 12.1
Bretzin14 High school athletes in 15 sports 2015-2016 1 193 757 3352 1.7
Total 239 564 6293 2.6
* Total number of athletes estimated using 105 athletes per year on football roster.

Preseason or a personal or family history of migraine headache disorder,


Preparation for the care of athletes begins before any practice and information on current medication use.
or competition with a preparticipation physical evaluation Several organizations recommend baseline evaluation
(PPE) and the development and practice of an emergency before sports participation to assist with diagnosis and
action plan.30 The PPE should include past concussion or return-to-play decisions in an athlete with a suspected
other traumatic brain injury history (number, recovery course, concussion.3,31,32 Several factors require consideration before
and time between injuries) as well as the presence of other implementing any test into an evaluation program for baseline
premorbid/comorbid conditions, or modifiers, which may or postinjury purposes. There is considerable normal varia-
make the diagnosis or management of concussion more tion in test performance with repeat testing in noninjured
difficult, including a history of learning disorder, attention athletes23,33,34; some tests are associated with a cost, and in
deficit disorder, motion sickness or sensitivity, mood disorders younger athletes with rapidly developing brain function, both

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K.G. Harmon et al. (2019) Clin J Sport Med

the ideal interval to repeat baseline testing and age-related differentiating SRC changes from normal variation. The
differences in test performance are unknown. Common test–retest reliability of commonly used sideline concussion
baseline evaluations include the battery of standard sideline evaluation tests is below the generally accepted threshold for
assessment tests found in the Sports Concussion Assessment clinical utility (0.75-0.90).33,39 Many concussion tests have
Tool 5th edition (SCAT 5) and/or computerized proprietary a learning effect that must be factored into analysis with
neuropsychological tests such as Cogsport, Automated repeated administration of the test. The sensitivity (ability of
Neuropsychological Assessment Metrics, Central Nervous a test to correctly identify a condition) and specificity (ability
System Vital Signs, or the Immediate Postconcussion Assess- of a test to correctly identify those without a condition) of
ment and Cognitive Testing. An initial baseline evaluation many of the individual tests used to evaluate concussion are
including a symptom checklist, cognitive evaluation, and not ideal. The area under the curve of a receiver operator
balance assessment has been considered “best practice” for all characteristic curve is another way to evaluate the usefulness
athletes by the National Collegiate Athletic Association. of a test with values greater than 0.9 considered excellent, 0.8
However, repeat annual baseline testing after an initial good, 0.7 fair, 0.6 poor, and 0.5 failing. Table 3 outlines the
baseline evaluation is no longer recommended for collegiate psychometric properties and number of subjects and con-
athletes.31 Baseline testing may be useful in some cases but is cussions studied of commonly used sideline evaluation tools.
not necessary, required, or an accepted standard of care for the There is evidence that combining tests of different functions to
appropriate management of SRC. form a multimodal assessment increases sensitivity and
specificity for diagnosis.22,33 The age of the athlete needs to
be considered when using and evaluating testing tools. Sport-
Sideline Assessment
related concussion is a heterogeneous injury, which contrib-
Observation of athletes during practice and competition by utes to the varied sensitivity of screening tools, which are often
medical personnel is valuable for potential concussion recog- domain-specific assessments. All tests should be interpreted in
nition and initial management. Reasons for immediate removal combination with relevant clinical information to arrive at the
and prompt evaluation include loss of consciousness (LOC), most accurate conclusion.
impact seizure, tonic posturing, gross motor instability, Symptoms are the most sensitive indicator of concus-
confusion, or amnesia. Any of these reported or observed signs sion.23,40 The reliability of athlete-reported symptoms
should result in removal from practice or competition for at depends on accurate reporting, which may be affected by
least the rest of the day. Concerns for more serious head injury a lack of recognition of the signs and symptoms of concussion
including prolonged LOC, severe or worsening headache, or conscious false reporting to avoid loss of playing time. An
repeated emesis, declining mental status, focal neurological athlete experiencing any increase in symptoms after a sus-
deficit, or suspicion of significant cervical spine injury should pected concussion should be held from play until further
trigger activation of the emergency action plan. evaluation can confirm or exclude SRC.
Along with directly observed signs of potential concussion, The SCAT541 and the Child SCAT542 are the evaluation
if video review demonstrates findings such as LOC, motor tools recommended by the Concussion in Sport Group (CISG)
incoordination or balance problems, or having a blank or for assessing a suspected concussion. These tests offer
vacant look, the athlete should be immediately removed from a standardized approach to sideline evaluation, which in-
participation for evaluation.35–37 A health care professional corporate multiple domains of function and are widely
familiar with the athlete is best suited to detect subtle changes available at no cost. The SCAT5 is composed of a brief
in the athlete’s personality or test performance that may neurological examination, a symptom checklist, a brief
suggest concussion. If a concussion is suspected but not cognitive assessment [the Standardized Assessment of Con-
diagnosed, removal from play and serial evaluations is cussion (SAC)], and a balance assessment (the modified-
recommended.38 Concussion assessment should be performed Balance Error Scoring System (m-BESS). The SAC in the
in a distraction-free environment with adequate time for SCAT5 offers optional 10-word lists for immediate and
examination and administration of concussion tests. If it is delayed memory and longer digit backward sequencing to
clear an athlete has an SRC, additional sideline testing can be minimize the ceiling effect, which was a weakness of the
discontinued. Sport-specific rules may not allow adequate SCAT3.43 There are currently no studies of the SCAT5 or
time for evaluation, and modifying these rules remains an area Child SCAT5’s sensitivity and specificity for SRC to determine
for improvement within the governing bodies of some sports. whether these versions are improved over the earlier versions.
When the sports medicine clinician becomes aware of The primary end point for sideline assessment is to
a potential injury, the athlete is approached and a brief history determine the probability that an athlete has sustained
of the event is obtained from the athlete and those who a concussion. If the athlete is deemed unlikely to have had
witnessed the event or athlete behavior. How the athlete a concussion, continued participation should be safe. If the
responds to the elements of orientation, memory, concentra- evaluation indicates a definite or probable concussion, the
tion, and balance is evaluated as well as speech patterns and athlete should be removed from participation with no same
how the athlete appears to be processing information. day return to play. Sport-related concussion is an evolving
Cervical palpation and range of motion (ROM) are also injury and should be serially reassessed when suspected.
typically performed to assess for other injury. If SRC is
suspected, these preliminary evaluations are followed by
Office/Subacute Assessment
a thorough and specific concussion assessment.
The psychometric properties of sideline assessment tools An office assessment should include a comprehensive history
need to be understood to accurately interpret the results.39 and neurological examination including details of injury
Knowledge of test reliability, or the stability of a test mechanism, symptom trajectory, neurocognitive functioning,
administered on more than one occasion, can assist in sleep/wake disturbance, ocular function, vestibular function,

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TABLE 3. Psychometric Properties of Sideline Assessment Tests*


# of Test and/or Sensitivity Specificity Test–Retest
Author Type of Athletes Athletes Concussed Controls Criterion (%) (%) Reliability AUC
Symptoms
McCrea19 College football 1631 94 56 89 100
22
Putukian College athletes 263 32 23 SCAT-2 84 100
Chin23 High school and college 2018 166 164 0.88
athletes
Resch120 College athletes 40 40 Revised Head 98 100
Injury Scale
Garcia40 College athletes 733 SCAT-3 93 97 0.98
Broglio33 College athletes 4360 0.40†
Total 3192 1065 283
SAC
Barr15 High school and college 1313 50 68 3 point decline 72 94 0.55‡
football
McCrea19 High school and college 1325 63 55 3 point decline 78 95 0.48§
football
McCrea17 High school and college 2385 91 ,10th percentile 79
football of normative
McCrea19 College football 1631 94 56 ? 80 91
121
Echlin Ice hockey (age 16-21) 67 21 — 1 point decline 54
Barr16 High school and college 823 59 31 ? 46 87
football
Marinides20 College athletes 217 30 2 point decline 52 82
Galetta21 Hockey/lacrosse youth/ 332 12 14 2 point decline 20 21 0.68
college
Putukian22 College athletes 263 32 23 ,10th percentile 41 91
of normative
Chin23 High school and college 2018 166 164 0.39† 0.56
athletes
Broglio33 College athletes 4874 0.39†
Total 15 284 618 411
Balance error scoring
system (BESS)
McCrea19 College football 1631 94 56 m-BESS 36 95
Broglio122 Young adults 48 BESS 0.60{
Barr16 High school and college 823 59 31 m-BESS 31 71
football
Putukian22 College athletes 263 32 23 m-BESS 25 100
Chin23 High school and college 2018 166 164 m-BESS 0.54† 0.56
athletes
Broglio33 College athletes 2894 BESS 0.41†
Total 4735 351 274
Oculomotor (King-Devick)
Galetta27 Football, m/w basketball 219 10 Worsening of KD 100
time
Leong123 Boxing Worsening of KD 100 100 0.9†
.5 s
Galetta21 Hockey/lacrosse youth/ 332 12 14 Worsening of KD 75 93 0.92
college time
Leong28 College football, m/w 127 11 Worsening of KD 89 0.95†
basketball time
King124 Amateur rugby 94 100 0.92†
20
Marinides Football, w lacrosse, 217 30 Worsening of KD 79
soccer time

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TABLE 3. Psychometric Properties of Sideline Assessment Tests* (Continued)


# of Test and/or Sensitivity Specificity Test–Retest
Author Type of Athletes Athletes Concussed Controls Criterion (%) (%) Reliability AUC
Seidman24 High school football 343 9 Worsening of KD 100 100
time
Dhawan29 Youth hockey 141 20 Worsening of KD 100 91
.5 s
Fuller125 Elite English rugby 145 Worsening of KD 60 39 0.51
time
Hecimovich126 Australian football 22 22 Worsening of KD 98 96 0.91†
time
Professional football 1223 84 63 Worsening of KD 84 62 0.88†
33
Broglio College athletes 755 0.74†
Eddy127 Recreational college 63 0.90†
athletes
Total 2041 310 99
Clinical reaction time
(dropped weighted stick)
Eckner128 College football, 102 0.65†
wrestling, and w soccer
Eckner47 High school and college 28 28 90% confidence 50 86
athletes interval
Broglio33 College athletes 261 0.32†
Total
* Study selection criteria: athletes competing in any level of sport using any sideline screening assessment or studies with test–retest reliability of included assessments. All studies were high
risk of bias as assessed using QUADAS-2 except for Fuller125 which was low risk of bias.
† Test–retest reliability: intraclass correlation coefficient.
‡ Test–retest reliability: reliable change index.
§ Test–retest reliability: Pearson’s correlation coefficient.
{ Test–retest reliability: generalizability coefficient.
AUC, area under the curve.
?, unclear what criterion/cutoff they used to develop sensitivity and specificity information.

gait, balance, and a cervical spine examination. The utility of be used in athletes aged older than 10 years.46 It is a no-cost
sideline neurocognitive and balance assessments to identify evaluation of symptom provocation with smooth pursuits,
concussion decreases as early as 3 days after injury.41 saccades, vestibular ocular reflex, vestibular motion sensitiv-
Symptom checklists can be useful to track symptom trajectory. ity, and convergence distance.46
To confirm the diagnosis of SRC, there should typically be
a clear mechanism consistent with concussion; characteristic
signs, symptoms, and time course of concussion; and no other Other Considerations in the Assessment of Concussion
cause for the constellation of clinical findings. It is not unusual
There is a need for definitive, objective, and clinically useful
for symptoms, signs, and testing to normalize by the time an
tools for the diagnosis of concussion. This interest has led to
office visit occurs,44 in which case the visit should focus on
innovation and fast-paced changes with the ongoing need for
recommendations for safe return to school and sport. If
refinement and validation of these efforts.
computerized neurocognitive tests were performed before
injury, they are often repeated during this assessment period.
If an athlete has ongoing symptoms at the time of the first
office visit, the visit should focus on excluding other Emerging Sideline Concussion Evaluation Tools
pathologies and providing anticipatory guidance. Other Other sideline evaluation tools have been developed, in-
pathologies such as cervicogenic pain, headache/migraine cluding tests of vestibular–ocular function and reaction time.
disorder, mood disorders, and peripheral vestibular condi- Physical examination components of the VOMS are becoming
tions may either be the cause of symptoms or may represent more frequently used in the office setting, but the role of
previous pathology worsened or unmasked by concussion. A formal VOMS testing on the sideline has not yet been studied.
complete cervical spine evaluation, screenings for psychoso- The King-Devick (KD) Test is a proprietary, timed saccadic
cial or mental health disorders, and additional tests evaluating eye movement test requiring individuals to quickly read
the vestibular and oculomotor system may be helpful in the numbers aloud.28 The KD requires a baseline test as well as an
office setting to determine the etiology of symptoms. understanding of potential learning and practice effects to be
Vestibular symptoms occur in 67% to 77%, and ocular useful. Simple reaction time as a sideline screen has also been
impairment occurs in approximately 45% of SRC.45,46 The studied using a dropped weighted stick.47 Further research
vestibular/ocular motor screening (VOMS) tool offers a brief, including larger numbers and control subjects is needed for
standardized way to assess vestibular–ocular function that can these tests.

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Other technologies such as app-based measures of reaction There is currently no scientific support for genetic testing in
time, eye trackers, postural stability, speech pattern, quanti- the evaluation and management of athletes with SRC, and
tative electroencephalography, and various abbreviated neu- additional research is needed to determine how genetic factors
rocognitive tests are being developed. Some are available on influence risk of injury and recovery after SRC.50
portable electronic platforms with the ability to share
information with multiple users. These newer technologies
do not have sufficient research to establish their utility. The Clinical Profiles
mention of all of these sideline tools does not imply AMSSM The recognition of heterogeneity among concussion presenta-
endorsement. tions has led to the concept of “clinical profiles” or “clinical
domains” with the potential for more specific prognostic value
Helmeted and Nonhelmeted Impact Monitors and targeted treatment.51–53 It must be stressed that this is an
emerging concept and does not represent clinical standards or
Current impact sensor systems indirectly monitor linear and norms but may serve to facilitate individualized patient
angular acceleration forces to the brain; however, they may not management. Although SRC may present with symptoms
consistently record head impacts or forces transmitted to the representing only one clinical profile, it is more often that SRC
brain. Neither a device nor a specific threshold measure of force presents with symptoms and impairment supporting multiple
or angular acceleration can be used to diagnose concus- profiles. It is currently unknown at what postinjury time point
sion.38,48 Some athletes experience high forces with no clinical these profiles become clinically important as most SRCs resolve
symptoms of concussion, and some athletes sustain a concus- with time. Thus, clinical profiles may be more applicable to
sion at much lower impact forces, making current impact athletes with persistent symptoms. More research in this area is
measures a poor predictor of SRC.49 The number, location, needed. The diverse symptoms and functional impairments of
density, and individual thresholds of head impacts may be SRC are variously categorized with overlapping symptom
important parameters. At this time, impact monitors are clinical profiles that may include cognitive, affective (anxiety/
a research tool requiring additional study and are not validated mood), fatigue, migraine/headache, vestibular, and ocular52–54
for clinical use in the diagnosis or management of SRC. (Figure 1). How clinical profiles fit into the clinical care of SRC
warrants additional research.
Biomarkers of Concussion
Head computerized tomography (CT) is rarely necessary in Management of Concussion
the evaluation of SRC but should be used when clinical
suspicion for intracranial bleeding or macrostructural injury Sport-related concussion clinical symptoms typically resolve
exists. Intracranial bleeds are rare in the context of SRC, but spontaneously with 80% to 90% of concussed older
can occur, and CT is the standard evaluation tool for these and adolescents and adults returning to preinjury levels of clinical
other suspected neurosurgical emergencies in acute and function within 2 weeks.55 In younger athletes, clinical
critical care. Conventional brain magnetic resonance imaging recovery may take longer, with return to preinjury levels of
(MRI) is not commonly used in the evaluation of concussion function within 4 weeks.56 It is important to communicate the
but may have value in cases with atypical or prolonged usual time course and outcome to patients and families to
recovery. Newer, advanced multimodal MRI technologies (eg, relieve the anxiety that often accompanies this injury.
diffusion tensor imaging, resting state functional MRI, Symptom checklists are useful for tracking symptomatic
quantitative susceptibility imaging, magnetic resonance spec- recovery. Clinical recovery based on our current evaluation
trography, and arterial spin labeling) are being studied in methods and SRC testing may not coincide with complete
research protocols aimed at understanding the neurobiolog- physiological recovery, although the functional, clinical, and
ical effects and recovery after SRC.50 Additional research will long-term significance of persistent imaging findings and
be required to determine the clinical utility of advanced subtle neuropsychological deficits on tests used in research
neuroimaging in the setting of SRC. settings is unknown.44
The role of fluid biomarkers (blood, saliva, and cerebro-
spinal fluid) in the diagnosis of SRC is also under active
Predicting Recovery
investigation.50 Proteomic markers of injury and recovery in
more severe forms of civilian neurotrauma and traumatic The most consistent predictor of recovery from concussion is
brain injury have shown some promise; however, in recent the number and severity of acute and subacute symptoms.57
systematic reviews, the overall level of evidence is low for Subacute headache or depression after injury are risk factors
using fluid biomarkers for diagnosis of SRC.50 Fluid for symptoms persisting for .1 month.57 A preinjury history
biomarkers have potential for informing the pathophysiology of mental health problems, particularly depression, seems to
of concussion and neurobiological recovery, but more re- increase the risk of prolonged symptoms.56 Athletes with
search is required to determine their clinical utility.50 Recent learning disabilities or attention deficit/hyperactivity disorder
Federal Drug Administration (FDA) approval of a two- do not seem to be at risk of prolonged recovery.57 More
protein brain trauma indicator with glial fibrillary acidic research is needed to address other SRC modifiers, including
protein and ubiquitin carboxy-terminal hydrolase L1 age and sex, although some studies demonstrate a longer
(UCHL1), and clinical use of S100 calcium-binding protein period of reported symptoms in females compared to males
b (s100b) in Europe, show promise for ruling out intracranial and for adolescent athletes.57 Newer research suggests that
bleeds and structural damage to reduce utilization of head CTs a lower symptom-limited heart rate threshold during graded
in the emergency department setting. At this time, none of exercise testing within a week of SRC in adolescents predicts
these tests has a role in the diagnosis or management of SRC. a longer recovery time.58

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K.G. Harmon et al. (2019) Clin J Sport Med

Figure 1. Overlapping clinical profiles: An emerging concept to facilitate individualized management after SRC. Most patients have features of multiple
profiles.

Treatment of Sport-Related Concussion symptom-exacerbation thresholds.3 Further research is needed


In this section the role of rest, physical activity and to define the role of prescribed rest in recovery.
nutraceuticals are discussed.
Activity and Exercise
Prescribed Rest Exercise intolerance is an objective physiological sign of acute
Prescribed cognitive and physical rest has been the mainstay of concussion that seems to reflect impaired autonomic function and
treatment for the past several decades despite insufficient evidence control of cerebral blood flow.67,68 Exercise improves autonomic
nervous system balance and CO2 sensitivity, cerebral blood flow
to support this approach.59,60 Earlier animal data suggested that
regulation, brain-derived neurotropic factor gene upregulation,
uncontrolled or forced early exercise is detrimental to
and both mood and sleep.69,70 Emerging data suggest that
recovery61–63; however, recent data in aerobically trained animals
symptom-limited activity, including activities of daily living and
given early access to exercise showed improved outcomes noncontact aerobic exercise, may begin as soon as tolerated after
compared with no or delayed exercise or to social isolation.64 an initial brief period (24-48 hours) of cognitive and physical
In human studies, strict rest after SRC slowed recovery and led to relative rest.3 There is some preliminary evidence that subsymp-
an increased chance of prolonged symptoms.65,66 Total rest, that tom threshold exercise improves recovery in acute concus-
is, “the dark room” or “cocoon therapy,” may have detrimental sion,71,72 and early symptom-limited graded exercise testing
effects similar to social isolation effects seen in animal studies and seems to be safe in athletes.58 Understanding for whom and when
is no longer recommended.3,51 Consensus guidelines endorse 24 to begin early exercise after SRC remains an ongoing area of
to 48 hours of symptom-limited cognitive and physical rest exploration. Early activity and exercise do not take the place of
followed by a gradual increase in activity, staying below a graded return to sport.

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Role of Nutraceuticals deficits identified and use an “expose-recover” model


Interest in nutraceuticals for prevention and treatment of performed by clinicians with expertise in vestibular rehabil-
concussion is high. There is emerging evidence in animal models itation.51,82 There is preliminary evidence that addressing
of concussion that some supplements may protect or speed cervical spine and/or vestibular dysfunction with a targeted
recovery from concussion; specifically focused on certain B physical therapy program improves outcomes in those with
vitamins, omega-3 fatty acids, vitamin D, progesterone, N- PPCS.83,84 Cognitive work should be modified or limited to
methyl-D-aspartate, exogenous ketones, and dietary manipula- that which does not exacerbate symptoms.60 In athletes with
tions (eg ketogenic diet).73–75 There is a gap, however, between sleep disturbances after an SRC, sleep hygiene should be
experimentally produced injury in an animal model and the addressed, sleep monitored, and treated with nonpharmaco-
heterogeneous mechanisms that cause human concussion during logic or pharmacologic strategies.85 Individuals experiencing
sports activities. There is no human evidence that nutraceuticals psychological symptoms such as irritability, sadness, and
prevent or ameliorate concussion in athletes.76 Supplements are anxiety should be evaluated and offered appropriate treat-
not FDA regulated, and potential for harm or contamination ment. A collaborative care model including cognitive behav-
should be considered. This is an area that requires significantly ioral therapy can improve outcomes in those with PPCS.86
more research to guide future recommendations.
Return to Learn
Sport-related concussions can induce changes in attention,
Persistent Postconcussive Symptoms
cognitive processing speed, learning, short-term memory, and
Postconcussion syndrome or disorder are terms that have been executive function that make learning difficult.87 Return to learn
frequently used to describe patients with lingering symptoms is the process of transitioning back to the classroom after
after a sport- or recreation-related concussion, but often those concussion using individualized academic adjustments87,88
patients do not meet diagnostic criteria for these diagnoses. A (Table 4). School personnel should be informed of the injury
preferred term is persistent postconcussive symptoms (PPCS), and implement an initial school support plan without delay.89
defined as symptoms that persist beyond the expected recovery Many concussed athletes recover quickly enough to return to the
time frame (.2 weeks in adults, .4 weeks in children).44 classroom with no or very brief adjustment of academic activities,
Persistent symptoms do not necessarily represent ongoing but schools should be prepared to provide additional support in
concussive injury to the brain. It is not unusual for common the event that recovery takes longer. Athletes with persisting
symptoms to be inappropriately or mistakenly attributed to symptoms should be provided an individualized return-to-learn
concussion; therefore, it is critical to understand pre-existing or accommodation plan that allows for symptom-limited learning
coexisting symptoms and conditions in the evaluation of PPCS. activity similar to return to physical activity protocols. Early
introduction of symptom-limited physical activity is appropriate;
however, return to sport training activities should follow
Targeted Treatments
a successful return to the classroom for student-athletes.
Recent systematic reviews have advocated including vestibu-
lar, oculomotor, psychological, sleep, cervical and autonomic
nervous system evaluations in the assessment to facilitate Return to Sport
individualized and targeted management of PPCS.77 Concussion-related symptoms and signs should be resolved
before returning to sport. A return-to-play progression
Exercise for Persistent Postconcussive Symptom
involves a gradual, stepwise increase in physical demands
and sport-specific activities without return of symptoms
Activity and exercise that does not exacerbate symptoms are before the final introduction of exposure to contact
recommended for those with PPCS. A formal symptom- (Table 5). The athlete should also demonstrate psychological
limited aerobic exercise program has been shown to be safe readiness for returning to play. The return-to-sport pro-
and improve resolution of persistent symptoms compared gression is individualized and is a function of the injury, the
with controls and should be considered in athletes with athlete’s age, history of SRC and level of play, and the ability
symptoms lasting longer than expected.78–80 The Buffalo to provide close supervision during the return to activity. The
Concussion Exercise Treatment Protocol, a progressive sub- return-to-sport progression presented by the CISG is widely
symptom threshold aerobic exercise program based on accepted but empiric, without evidence to support either the
systematically establishing the level of exercise tolerance on progression sequence or the time spent in each stage. In
the Buffalo Concussion Treadmill Test, is the most studied general, for young athletes, each stage of the progression
controlled exercise program.81 It is ideal for those with PPCS should be at least 24 hours without return of symptoms before
to be evaluated by a provider or multidisciplinary team with progressing to the next stage.
expertise in complicated concussion management.
Return to Driving
Physical Therapy, Vestibular Therapy, and Collaborative In addition to return to learning and sporting environments,
Care
older athletes may need to return to driving, where subtle
Athletes with migraine/headache should be evaluated for deficits could compromise safety. Most sports medicine
underlying headache disorders, cervical dysfunction causing physicians do not counsel athletes with SRC about driving.90
headache, and other possible contributors, and treated Driving is a complex process involving coordination of
appropriately with nonpharmacologic and pharmacologic cognitive, visual, and motor skills as well as concentration,
treatments.77 Vestibular therapy should focus on specific attention, visual perception, insight, and memory that can all

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K.G. Harmon et al. (2019) Clin J Sport Med

TABLE 4. Return to Learn


Facilitate communication and transition back to school
• Notify school personnel after injury to prepare for return to school
Obtain consent for communication between medical and school teams
• Designate point person to monitor student’s status related to academics, recovery, and coping with injury and communicate with medical team
School health professional, guidance counselor, administrator, and athletic trainer
• Develop plan for missed assignments and examinations
• Adjust schedule to accommodate reduced or modified attendance if needed

Classroom adjustments School environment adjustments


• Breaks as needed during school day • Allow the use of headphones/ear plugs to
reduce noise sensitivity
• Reduce in-class assignments and homework • Allow the use of sunglasses/hat to reduce light
sensitivity
• Allow increased time for completion of • Limit the use of electronic screens or adjust
assignments and testing screen settings, including font size, as needed
• Delay exams until student is adequately • Allow student to leave class early to avoid
prepared and symptoms do not interfere with crowded hallways
testing
• Allow testing in a separate, distraction-free • Avoid busy, crowded, or noisy
environment environments—music room, hallways, lunch
room, vocational classes, and assemblies
• Modify due dates or requirements for major
projects
• Provide preprinted notes or allow peer
notetaker
• Avoid high risk or strenuous physical activity
Clinicians should individualize adjustments based on patient-specific symptoms, symptom severity, academic demands, and pre-existing conditions, such as mood disorder, learning
disability, or attention deficit/hyperactivity disorder.87,88
Athletes with complicated or prolonged recovery may require a multidisciplinary team with specific expertise across the scope of concussion management.

be affected by SRC.90 Little is known about the risk of driving Short-Term Risks of Continued Exposure After Concussion
after SRC, but preliminary data suggest some impairment or Premature Return to Play
exists when concussion patients report they are asymptom- Continuing to play immediately after a concussion is a risk
atic.91 Currently, no widely accepted return to driving of increased symptom burden, worsening of the injury, and
protocols exist; however, in athletes who drive, discussing prolonged recovery.92–95 Athletes who return to sport
the potential risks and harms is appropriate. before full recovery are at increased risk of repeat
concussion.96 Some research has demonstrated that ath-
letes who return to sport after SRC following standard
return to sport protocols had an increased rate of
RISKS RELATED TO CONCUSSION musculoskeletal injury.97,98 The “Second Impact Syn-
Short and long-term risks of concussion are an area of drome” is both rare and controversial. It is considered by
growing concern. some to be a potentially life-threatening complication of

TABLE 5. Return to Sport


Stage Description Objective
1 Symptom-limited activity Reintroduction of normal activities of daily living. Symptoms should not
worsen with activity.
2 Light aerobic exercise Walking, stationary biking, and controlled activities that increase heart rate.
3 Sport-specific exercise Running, skating, or other sport-specific aerobic exercise avoiding risk of
head impact.
4 Noncontact training drills Sport-specific noncontact training drills that involve increased coordination
and thinking. Progressive introduction of resistance training.
5 Full-contact practice Return to normal training activities. Assess psychological readiness.
6 Return to sport
RTS progressions should be individualized based on the injury, athlete’s age, history, and level of play, and the ability to provide close supervision during the return to activity and progressions
may vary between athletes. Each stage is generally 24 hours without return of concussion symptoms. Consider written clearance from a health care professional before RTS as directed by
local laws and regulations.3

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reinjury during the initial postinjury period that is not fully impacts are defined as transfer of mechanical energy to the brain
understood and seems primarily limited to pediatric and causing presumed axonal or neuronal injury in the absence of
adolescent athletes.99 clinical signs or symptoms.112 It is unclear whether a biomechan-
ical threshold or other factors lead to injury or whether this entity
qualifies as injury, as it does not seem to be associated with
Long-Term Risks After Concussion neuropsychological changes.113 Although subconcussive impacts
have been associated with CTE, the short- and long-term effects of
Mental Health Problems and Depression
repetitive head impacts, similar to SRC, cannot be accurately
Sport and exercise are protective against depression.100 Most characterized using current technology. Future research will
studies examining the relationship of contact sports to mental depend on developing technologies that can assess brain changes
health problems or depression later in life have low methodolog- after repetitive asymptomatic head trauma in living subjects.
ical quality, high risk of bias, or both.101–103 Several studies have
reported that National Football League (NFL) and college
football athletes with a history of concussion are more likely to DISQUALIFICATION FROM SPORT
experience depression, although the risk of mental health issues,
There are no evidence-based guidelines for disqualifying or
including suicide, among former NFL players is lower than age-
retiring an athlete from sport after concussion; therefore, each
matched controls.101–103 Former high school football players
athlete should be carefully and individually assessed to
show no difference in cognitive function testing and have lower
determine the safety and potential long-term health conse-
depression scores when compared with noncontact sport
quences of continued participation. There is no “set” number
controls.104 Mental health issues are common, multifactorial,
of concussions or repetitive head impact exposures that
and often present independent of participation in contact or
should force retirement from a season or from sport, and it is
collision sport. Longitudinal research on contact sport athletes,
likely that athletes with higher numbers of diagnosed
which addresses multiple variables, is needed to understand the
concussions will be seen in clinical settings as the recognition
long-term risks.
and awareness of concussion is improved.
Considerations for retirement from sport include the length
Chronic Traumatic Encephalopathy of concussion recovery (progressively longer time intervals for
symptom resolution), patterns of developing concussion with
Chronic traumatic encephalopathy (CTE) and other neurode-
less force, or increasing severity of concussions, as well as the
generative diseases have been described in former athletes with
athlete’s readiness or apprehension regarding to return to
a history of concussion or repetitive head impact exposure,
sport. Additional contraindications for continued participa-
typically accompanied by behavioral change. The incidence and
tion may include behavioral changes, post-traumatic seizures,
prevalence of CTE in the general population, in former athletes,
persistent neurological deficit, or imaging findings suggesting
or in former athletes with a history of concussion or repetitive
additional/other pathology. Individual and family tolerance of
head impact exposure is unknown. A cause and effect
risk and perception of the benefit of sport participation (eg,
relationship between postmortem CTE changes and antemor-
personal identify and financial motivation) should be consid-
tem behavioral and cognitive manifestations has not been
ered and explored in a process of shared decision-making.114
demonstrated, and, asymptomatic players have had confirmed
CTE pathology at autopsy.105,106 It is also unknown whether
CTE is a progressive disease and whether tau deposition is the
cause of CTE or a byproduct or marker of a disease.107 PREVENTION
The expression of CTE-associated symptoms may be related Prevention of SRC is ultimately more effective in reducing the
to impact load and type, duration of career, underlying genetic burden of this condition than any treatment, and although
factors, or other lifestyle behaviors including alcohol, drug and primary prevention of all SRC is not possible, measures to
anabolic steroid use, general health, psychiatric disease, and decrease the number and severity of concussions are of value.
other factors. Some retrospective studies have reported in- Rule changes, enforcement of existing rules, technique changes,
creased risk of neurodegenerative disease in former professional neck strengthening, and equipment modifications have been the
football players; however, former high school football players primary focus of prevention. There is moderate evidence that
do not show a higher prevalence of neurodegenerative disease delaying the introduction of body checking in youth hockey
when compared with nonfootball peers.108,109 The most widely reduces concussion rates.115–117 The effectiveness of rule changes
described risk factor to date is extensive exposure to both in youth soccer and football to reduce concussion incidence is not
multiple concussions and repetitive head impacts, but the clear; however, there is initial evidence that practice modification
degree of necessary exposure is likely specific to the individual and changes in tackling technique may reduce injury.118,119 There
and subject to multiple modifying risk factors.110 Athletes and is conflicting evidence regarding mouthguards and concussion
former athletes who present with neuropsychiatric symptoms reduction, and mouthguards should primarily be used for
and signs that have been ascribed to CTE should be evaluated preventing dental trauma.117 Helmets prevent skull trauma and
for potentially treatable comorbid conditions that share intracranial bleeding, but their protective effects for concussion
symptoms and not be assumed to have CTE.111 are less pronounced. Some football helmet designs have improved
the ability to absorb force, but it is unknown whether this will
reduce concussion incidence. Studies of headgear in other sports
Repetitive Head Impacts
have produced mixed results. Player behavior can change when
Subconcussive or nonconcussive head impacts have been athletes wear new or “improved” protective equipment, encour-
discussed as an entity apart from concussion history that may aging a more aggressive style of play, potentially increasing the
create risk of long-term neurologic sequelae. Subconcussive risk of injury.

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K.G. Harmon et al. (2019) Clin J Sport Med

FUTURE RESEARCH DIRECTIONS American Medical Society for Sports Medicine supports
continued research in the area of SRC to enhance safe
The panel has identified these key areas for further study:
participation in sport.
1. High-quality epidemiologic studies in younger athletes,
recreational activities, nontraditional sports, and non-
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