vestibular - br j sports med 2013 makdissi 308 13

7/24/2019 Vestibular - Br J Sports Med 2013 Makdissi 308 13

1/8

The difcult concussion patient: what is the bestapproach to investigation and management ofpersistent (>10 days) postconcussive symptoms?

Michael Makdissi,1,2 Robert C Cantu,3 Karen M Johnston,4 Paul McCrory,1

Willem H Meeuwisse5

Additional material ispublished online only. To viewplease visit the journal online(http://dx.doi.org/10.1136/bjophthalmol-2013-092255).

1The Florey Institute ofNeuroscience and MentalHealth, Melbourne BrainCentre, Heidelberg, Victoria,Australia2Centre for Health, Exerciseand Sports Medicine, University

of Melbourne, Melbourne,Victoria, Australia3Boston University MedicalSchool, Boston, Massachusetts,USA4Division of Neurosurgery,University of Toronto, Toronto,Ontario, Canada5Sport Injury PreventionResearch Centre, Facultyof Kinesiology and HotchkissBrain Institute, Universityof Calgary, Calgary, Alberta,Canada

Correspondence toDr Michael Makdissi,

The Florey Institute ofNeuroscience and MentalHealth, Austin Campus,Melbourne Brain Centre, 245Burgundy St HeidelbergAustralia, Heidelberg, VIC3084 Australia;[email protected]

Received 26 January 2013Accepted 29 January 2013

To cite:Makdissi M,Cantu RC, Johnston KM,

et al.Br J Sports Med2013;47:308313.

ABSTRACTBackground Concussion in sport typically recoversclinically within 10 days of injury. In some cases,however, symptoms may be prolonged or complicationsmay develop. The objectives of the current paper are toreview the literature regarding the difcult concussionand to provide recommendations for an approach to theinvestigation and management of patients withpersistent symptoms.Methods A qualitative review of the literature onconcussion in sport was conducted with a focus onprolonged recovery, long-term complications andmanagement including investigation and treatmentstrategies. MEDLINE and Sports Discus databases werereviewed.Results Persistent symptoms (>10 days) are generallyreported in 1015% of concussions. This gure may behigher in certain sports (eg, ice hockey) and populations(eg, children). In general, symptoms are not specic toconcussion and it is important to consider and managecoexistent pathologies. Investigations may include formalneuropsychological testing and conventionalneuroimaging to exclude structural pathology. Currently,there is insufcient evidence to recommend routine

clinical use of advanced neuroimaging techniques orgenetics markers. Preliminary studies demonstrate thepotential benet of subsymptom threshold activity aspart of a comprehensive rehabilitation programme.Limited research is available on pharmacologicalinterventions.Conclusions Cases of concussion in sport whereclinical recovery falls outside the expected window(ie, 10 days) should be managed in a multidisciplinarymanner by healthcare providers with experience insports-related concussion. Important components ofmanagement, after the initial period of physical andcognitive rest, include associated therapies such ascognitive, vestibular, physical and psychological therapy,assessment for other causes of prolonged symptoms andconsideration of a graded exercise programme at a levelthat does not exacerbate symptoms.

INTRODUCTIONOver the past decade, recommendations for the man-agement of concussion in sport have centred on phys-ical and cognitive rest until symptoms resolve andthen a graded programme of exertion prior tomedical clearance and return to play.13 This basicapproach works well for the majority of concussionswhere clinical features resolve progressively within

10 days. In a number of cases, however, recovery canbe prolonged or complications may develop.

Persistent symptoms following concussion are a causeof signicant morbidity and frustration to the athleteand pose a management challenge to the clinician.While there has been an explosion of studies on theacute management of concussion over the pastdecade, data on the management of prolonged recov-ery remain sparse. The current managementapproach to the difcult concussion is largely basedon anecdotal evidence or extrapolation from studieson moderate-to-severe traumatic brain injury (TBI).

The objectives of the current study were toreview the literature regarding the difcult concus-sion and to provide recommendations for anapproach to the investigation and management ofpatients with persistent symptoms.

METHODSSearches of MEDLINE (ISI Web of Science,PubMed) and SportDiscus databases were under-taken using the key words concussion, mild trau-matic brain injury, head injury and sport orathlete/athletic. These terms were combined withthe following keywords to identify the literature fordifcult concussions and key aspects of investiga-

tion and management: symptoms, complex, dif-cult, prolonged, persistent, post-concussionsyndrome, investigation, imaging, biomarker,gene/genetic, treatment, medication, manage-ment, exerciseand rehabilitation.

The search was limited to the English languageand focused on original papers published in thepast 10 years. Reference lists from retrieved articleswere searched for additional articles, and theauthors own collections of articles were includedin the search strategy.

RESULTSPersistent postconcussion symptomsConcussion typically results in a range of symptomsand signs in a number of different domains.13 Theclinical features vary, but commonly reported symp-toms include headache, nausea, dizziness andbalance problems, blurred vision, confusion,memory disturbance, mental fogginess andfatigue.49 Prospective cohort studies and system-atic reviews have consistently demonstrated that themajority of cases of concussion in adult populationsresolve within 10 days of injury.6 912 A difcultconcussion can be described as one in which clin-ical recovery falls outside the expected window (ie,10 days).

The incidence of prolonged clinical recovery fol-lowing concussion varies depending on the cohort

Makdissi M,et al.Br J Sports Med2013;47:308313. doi:10.1136/bjsports-2013-092255 1 of 7

Review

group.bmj.comon November 8, 2015 - Published byhttp://bjsm.bmj.com/Downloaded from
http://group.bmj.com/http://group.bmj.com/http://bjsm.bmj.com/http://bjsm.bmj.com/http://group.bmj.com/http://bjsm.bmj.com/


2/8

being investigated (as well as the time frame used to dene pro-longed). Studies have shown that approximately 1015% ofcollegiate and professional American football players have symp-toms beyond 10 days.7 10 13 Similar gures have been demon-strated in Australian football.4 9 Higher rates of prolongedrecovery (ie, over 30% of cases) have been reported followingconcussion in ice hockey,6 and in cohorts of high schoolathletes.14 15

Common persistent symptoms include headache, depression,difculty concentrating, fatigue or low energy, difcultysleeping or feeling not quiet right, in a fog or sloweddown.4 7 9 1 0 1 3 1 6 These symptoms are non-specic and may

be reported in healthy athletic populations at baseline (table 1)and in patients with other injuries, illnesses or neuropsychiatricconditions. These same symptoms have also been reported ingeneral trauma patients, individuals with anxiety or depression,patients with chronic pain syndromes, soldiers with combatstress and individuals who are involved in litigation regardlessof the type of injury.1725

When assessing postconcussion symptoms, it is important toconsider that reporting of symptoms may be affected by anumber of factors including sex, socioeconomic factors, concur-rent illness or musculoskeletal injury and moderate-to-highintensity exercise.18 2629 Studies in patients with mild TBI havealso demonstrated that symptom reporting can be inuenced bygeneral health status,30 other medical conditions such as

migraines31 and psychological factors such as coexisting anxietyand depression.32

The method used for symptom reporting can also impact onthe results. For example, Krol and Mrazik33 performed a cross-sectional study in 117 athletes comparing self-reported symp-toms to symptoms endorsed during an interview. The authorsfound a higher number of symptoms reported and a greateroverall symptom score in the self-administered condition.33

They also found that athletes reported more symptoms whenthe interviewer was woman.33 Similarly, Iverson et al34 demon-strated a higher reporting of symptoms on a self-administeredquestionnaire when compared with a structured interview in acohort of athletes with concussion.

General health questionnaires that incorporate patient-reported outcome measures in a number of domains

(eg, depression, anxiety, etc) have been used in the study ofretired players.35 36 Given the complex nature of postconcussionsymptoms, similar questionnaires may also be benecial in theassessment of difcult concussions. Domains that should be con-sidered in this assessment include: Depression and anxiety (eg, Hospital Anxiety and

Depression Scale, Beck Depression Inventory, DepressionAnxiety Stress Scale, Prole of Moods States);

Headache and migraine (Headache Impact Test, MigraineDisability Assessment);

General health and disability (eg, Short-form 36 HealthSurvey Questionnaire, Health-Related Quality of Life);

Sleep (eg, Medical Outcomes Study Sleep Scale Survey); Drug and alcohol use/abuse (eg, Drug Abuse Screening

Test, Alcohol Use Disorders Identication Test).The advantages of a more detailed, semiquantitative assess-

ment are that it may help identify other causes or contributingfactors to the individuals symptoms and may facilitate monitor-ing over time. While specic patient-reported outcome measureshave yet to be validated in concussion, they may serve as usefulclinical and research assessment tools.

Role of investigationsThe assessment of recovery following concussion is currentlylimited by the absence of simple and reliable direct measures of

brain function. Instead, clinicians must rely on indirect measuresto inform clinical judgement, such as the symptoms and signs ofconcussion (including neurological and balance assessments), inaddition to the use of brief neuropsychological tests to estimatethe recovery of cognitive function.

Neuropsychological testingComputerised screening neuropsychological test batteries havebecome an important component of concussion assessment.13

The test batteries have been shown to be sensitive to changes incognitive function following concussion. Moreover, they havebeen shown to detect cognitive decits in a signicant propor-tion of individuals even after the symptoms have resolved.9 37

Although formal neuropsychological testing is also recom-mended in cases of concussion with persistent symptoms, there

Table 1 Summary of studies reporting symptoms at baseline

Paper Subject characteristicsScaleused Results Common symptoms reported

Covassinet al26

1209 Coll egiate ath letes PCS(ImPACT)

Mean total symptom score (SD): males: 7.3(11.5), females 7.9 (12.4)

Fatigue, headache, sleep disturbance, difficultyconcentrating

Lovell et al50 1746 High school and universitystudent athletes

PCS(ImPACT)

Mean total symptom score (SD): males 4.6(7.7), females 7.9 (11.5)

NR

Shehataet al51

260 Univers ity athletes SCAT Mean total symptom score: males 3.52,females 6.39

Fatigue/low-energy, drowsiness, neck pain, difficultyconcentrating, difficulty remembering

Piland et al27 1065 Collegiate athletes HIS Mean total symptom score (SD): 4.72(6.07)No significant differences between males andfemales

Fatigue, drowsiness, headache, trouble falling asleep,difficulty concentrating

Schneideret al52

4193 Youth hockey players SCAT2 Median total symptom score 08(range 0108)No significant difference between males andfemales

Fatigue/low energy, headache

Jinguji et al53 214 High school athletes SCAT2 Average number of symptoms score=2.25No significant differences between males andfemales

Fatigue, trouble falling asleep, difficulty concentrating,difficulty remembering

HIS, Head Injury Scale (9 items, 7-point Likert scale); NR, not reported; PCS, Postconcussion Symptom Scale; SCAT, Sport Concussion Assessment Tool.

2 of 7 Makdissi M,et al.Br J Sports Med2013;47:308313. doi:10.1136/bjsports-2013-092255

Review



3/8

is no literature on the test properties (sensitivity, specicity, pre-dictive value, etc) in this setting.

Advanced imaging and investigation techniquesAdvanced imaging and investigation techniques have demon-strated changes in brain function, activation patterns and whitematter bre tracts in cases of concussion with prolonged symp-toms (table 2A). Often, these changes exist even when the

athlete has recovered clinically and returned to sport (table 2B).As such, the signicance of these changes remains unclear at thistime. Nevertheless, advanced imaging and investigation techni-ques (such as Diffusion Tensor Imaging, functional MRI, MRspectroscopy, quantitative EEG, etc) may hold hope for futureassessment protocols in concussion. In the short term, their usein the research setting should continue to be encouraged.

Genetic testingPreliminary research reveals a potential association between gen-etics and long-term outcome following concussion.

Apolipoprotein E (APOE) has been the most extensively studiedgene in TBI. Jordan et al38 demonstrated a relationship between

APOE4 genotype and chronic TBI score, particularly in highexposure boxers (ie, more than 12 professional bouts). Similarly,Kutner et al39 studied the potential inuence of APOE4 geno-type in a cohort of 53 active professional American footballersand found that players with at least one copy of the APOE4allele scored lower on tests of attention and information pro-cessing speed and accuracy. In a neuropathological study of ath-letes with Chronic Traumatic Encephalopathy (CTE), anincreased frequency of the APOE4 allele was noted among casesof pathologically conrmed CTE.40 Recently, however, a largecase series did not n d a d enite relationship between the

APOE genotype and CTE, especially in lesser grades of CTE.41

Other genes that have been considered include the APOE pro-

moter and Tau, with no consistent

ndings regarding an affecton outcome following concussion in sport.Despite the methodological limitations of these studies, they

provide preliminary evidence of a complex inter-relationshipbetween head injury, genetics and the risk of cumulative damage.However, more research is required in this area before genetictesting can be recommended as part of the clinical work-up ofconcussion.

Management of structural injuries masquerading asconcussion

Any athlete that sustains a head injury is at risk of having astructural brain injury (eg, brain contusion). One of the criticalroles of the initial medical assessment is to examine the playerneurologically for such injuries. There are well described andvalidated guidelines for the use of imaging in the acute stage fol-lowing head injury (eg, the Canadian CT head Rule or the NewOrleans Criteria).42 43 Furthermore, in athletes with persistentsymptoms or cognitive decits, consideration should be given toconventional neuroimaging to investigate for an underlyingstructural injury.

To date, there are no published studies evaluating treatmentstrategies in athletes who sustain structural head injuries.Consequently, decisions regarding their management, includingreturn to play, should be made by a clinician experienced instructural brain injury and based on the type of injury (eg, frac-ture and haemorrhage), relative risks associated with return to

sport and the presence of ongoing sequelae (eg, symptoms,signs, cognitive decits). Structural brain injury is not a

concussion. It requires further consideration outside of therealm of sport medicine expertise.

Treatment of persistent symptomsNon-pharmacological treatmentThe current treatment approach for difcult concussions isbased largely on an extension of the guidelines for acute injuries(ie, rest until symptoms resolve, followed by the use of com-

bined clinical measures of recovery to determine the timing ofreturn to play). While an initial brief period of rest may beimportant in the management of acute concussion, there islimited evidence that further rest is benecial in cases whereclinical features are prolonged.

Conversely, preliminary evidence suggests that an activerehabilitation programme is useful for the management of con-cussion where the symptoms are prolonged (table 3). Therehabilitation programme is started even in the presence ofsymptoms.

The graded exercise test has also been demonstrated to havegood inter-rater and testretest reliability.44

When dizziness or disequilibrium is a prominent feature of per-sistent symptoms following concussion, vestibular rehabilitationmay be useful.45 In a cohort of individuals with blast-related mildTBI, Gottshall and colleagues demonstrated improvement insymptoms after an 8-week period of vestibular physiotherapy.46

Other treatments have been used anecdotally for the manage-ment of specic symptoms. For example, manual or physicaltherapy may be used to treat myofascial pain or neck triggerpoints contributing to headaches; cognitive therapy includingmemory tasks as well as learning coping skills may be useful forsome patients with persistent cognitive symptoms; and thosewho have problems with anxiety, panic attacks or other psycho-logical or emotional problems may benet from meditation, bio-feedback or psychological therapy. At present, however, thereare limited data on these techniques in the management of pro-

longed symptoms following concussion.

Pharmacological treatmentNumerous medications are available to treat the range of symp-toms that are observed following concussion.47 Many of thesemedications have been investigated in patients with moderate orsevere TBI, but there are few trials that have been conducted inmild TBI or concussion.

In a small cohort of volunteers diagnosed with major depres-sion following mild TBI, Fann et al48 demonstrated an improve-ment in symptoms and function with the use of sertraline.

In a recent retrospective study, Reddy et al49 examined theeffects of amantadine in 25 adolescent athletes with postconcus-sion symptoms that persisted longer than 21 days. Individualswere compared with historical controls, and all individuals wereassessed using a computerised neurocognitive test battery. Theauthors showed that the group treated with 100 mg of amanta-dine twice per day demonstrated greater improvements in theirreaction time, verbal memory and symptom reporting. 49

A number of different antimigraine treatments have beenassessed in small studies of patients with headaches following mildTBI (table 4). The studies all report moderate to good results, butthendings have not been conrmed in larger randomised controltrials, and nor have they been trialled specically in patients withpersistent symptoms following concussion in sport.

Components of a comprehensive concussion clinic

Current consensus advocates a multifaceted clinical approach tothe assessment of concussion. This is perhaps even more


Review



4/8


5/8

important in the setting of prolonged symptoms, where thediagnosis is not always clear (ie, there are other causes of pro-longed symptoms) or when superimposed factors lead to apattern of deterioration rather than the expected improvement.Some components of a comprehensive concussion clinic aresummarised in table 5, although the list is by no means com-plete and expands with time and experience. For instance,access to expertise such as sport psychology, physiatry, psych-iatry, occupational therapy, social work and educational consul-tants are now included in such a list. In addition, in the settingof the difcult concussion, access to appropriate rehabilitation

strategies, both physical and cognitive, is important and identi

-cation of programme leadership and coordination is key.Community resources may be incorporated in addition tomedical facilities.

Ideally, the concussion clinic would also have a central role inathlete and public education and health advocacy participatingin collaborative efforts. Access to academic studies, as well asparticipating in and beneting from research ndings, helps tonurture the future directions of such a programme and benetsthe injured athlete. The physical and administrative structureand support to the programme will facilitate excellence in theprovision of care.

SUMMARY AND RECOMMENDATIONSA difcult concussion can be described as one in which clinicalrecovery falls outside the expected window (ie, 10 days in theadult population).

Assessment of persistent symptomsPersistent symptoms are non-specic and may be caused by orcontributed to by other conditions (such as migraine, mentalhealth issues, concurrent injuries, etc). The assessment of per-

sistent symptoms therefore requires a careful history (includingboth past and family history) and examination (including assess-ment of the cervical spine and vestibular function). The currentpostconcussion symptom checklist on the SCAT2 alone is insuf-cient for the assessment of persistent symptoms, without adetailed history of the symptoms. The addition of patient-reported outcome measures to the assessment battery in pro-longed or difcult cases (especially in the case of the retiredplayer with ongoing cognitive issues) would provide a morecomprehensive, quantiable approach to assessment and mayallow identication of other causes or contributing factors tothe patients symptoms.

Table 3 Active rehabilitation

Paper Study type/setting Subject characteristics Inclusion criteria Outcome measures Findings/results

Gagnonet al63

Prospective cohort(tertiary referralcentre)

N=16Children and adolescents(aged 1017 years)

Postconcussion symptoms>4 weeks

Symptoms checklist,clinical examination,balance testing,coordination testing

Used a graded rehabilitation programme(beginning with submaximal aerobic trainingthat is, 15 min on a treadmill or stationary bike,then introducing sports-specific training drills for10 min)Found a significant increase in exercise toleranceand reduction in symptom score (30.020.8 atpresentation to 6.75.7 at discharge)Mean duration of intervention 4.42.6 weeks

Leddyet al64

Prospective cohort(Universityconcussion clinic)

N=12 (6 athletes, 6non-athletes)

Symptoms >6 weeksfollowing concussion (5sports related, 1 motorvehicle accident)

Graded symptomchecklist, graded exercisetreadmill test (Balkeprotocol)

Exercise at an intensity of 80% of the maximumheart rate achieved on the treadmill test beforethe exacerbation of symptoms10 of the 12reported being symptom-free at restAthletes recovered faster than non-athletesRate of symptom improvement was directlyrelated to exercise intensity achieved

Bakeret al65

Retrospective caseseries

N=91 (63 had follow-upphone assessment473 months postinjury)

Symptoms >3 weeks Subjective symptomreporting, gradedexercise treadmill test(Balke protocol)

41/57 Who completed the exercise programmereturned to full daily functioning

Table 4 Pharmacotherapy for persistent post-traumatic headache

PaperStudy type/setting Subject characteristics Treatment Findings/results

Weisset al66 Case series 14 Mild TBI and 7 whiplash injurypatients diagnosed with migrainespostinjury

Propranolol and/oramitriptyline

Dramatic reductionin the frequency and severity ofheadaches in 70%

McBeath andNanda67

Case series 34 Patients referred to headache clinicwith headache as part of apostconcussion syndrome

Repeat intravenousdihydroergotamine andmetoclopramide

Reported a good-to-excellent response in 29 of 34 patients.Also noted improvement in memory symptoms, sleepdisturbance and dizziness

Packard68 Retrospectivecohort

100 Patients with chronic dailyheadache of between 2 and 6 monthsduration following mild TBI

Valproate 60% Reported mild- to-moderate improvement after 1 monthof treatment. The remaining 40% either showed no response(26%) or stopped treatment because of side effects

TBI, traumatic brain injury.


Review



6/8

Role of investigationsNeuropsychological testing remains as an important componentof assessment following concussion. Formal neuropsychologicaltesting should be encouraged in the difcult concussion,although there are limited data to support its recommendationat present.

Conventional imaging should be considered in any athletewith persistent symptoms or cognitive decits to investigate foran underlying structural injury.

Advanced imaging and investigation techniques have demon-

strated changes in small cohorts of patients with persistentsymptoms, as well as in individuals after clinical recovery fol-lowing concussion. At present, the clinical signicance of thesechanges remains unclear. The current literature does notsupport the use of these investigation tools in the routine clin-ical management of athletes with concussion. Advanced imagingand investigation techniques do, however, contribute to ourunderstanding of the pathophysiology of concussion, andongoing use should be encouraged in the research setting.

TreatmentCurrently, there is no evidence that prolonged rest is benecialfor patients with persistent symptoms. Preliminary studies dem-onstrate that an active rehabilitation programme may be usefulfor the management of cases where symptoms are prolonged.

The important components of an active rehabilitation pro-gramme include: Commencement even in the absence of complete symptom

resolution; Prescriptive advice regarding the intensity, duration and

timing of exercise; Working to a level that does not aggravate the symptoms

(subsymptom threshold exercise); Slow progression of rehabilitation with monitoring of clin-

ical outcome.Currently, there is limited evidence for the use of pharmaco-

therapy in concussion. Medications should be limited to casesthat do not resolve with a conservative approach, or those with

severe symptoms at rest that preclude the start of a gradedrehabilitation programme. Medications generally should berestricted to the management of related syndromes (eg,migraine, sleep disturbance, etc).

Difcult concussions should be managed in a multidisciplin-ary manner. Ideally, this is in the setting of a concussion clinicwith access to expertise in a wide range of areas.

Contributors MM, RCC, KMJ, PMC and WHM all made substantial contributionsto conception and design, acquisition and interpretation of data; drafting andrevising the article and nal approval of the version to be published.

Competing interests See the supplementary online data for competing interests(http://dx.doi.org/10.1136/bjsports-2013-092255).

Provenance and peer review Commissioned; internally peer reviewed.

REFERENCES1 Aubry M, Cantu R, Dvorak J,et al. Summary and agreement statement of the 1st

International Symposium on Concussion in Sport, Vienna 2001. Clin J Sport Med2002;12:611.

2 McCrory P, Meeuwisse W, Johnston K,et al. Consensus statement on concussion insport: the 3rd International Conference on Concussion in Sport held in Zurich,

November 2008.Br J Sports Med2009;43:I76

84.3 McCrory P, Johnston K, Meeuwisse W, et al. Summary and agreement statement ofthe 2nd International Conference on Concussion in Sport, Prague 2004. Br J SportsMed2005;39:196204.

4 McCrory PR, Ariens M, Berkovic SF. The nature and duration of acute concussivesymptoms in Australian football. Clin J Sport Med2000;10:2358.

5 Erlanger D, Kaushik T, Cantu R,et al. Symptom-based assessment of the severity ofa concussion. J Neurosurg 2003;98:47784.

6 Benson BW, Meeuwisse WH, Rizos J,et al. A prospective study of concussionsamong National Hockey League players during regular season games: theNHL-NHLPA Concussion Program. Can Med Assoc J 2011;183:90511.

7 McCrea M, Guskiewicz KM, Marshall SW, et al. Acute effects and recovery timefollowing concussion in collegiate football playersthe NCAA Concussion Study.JAMA2003;290:255663.

8 Lovell MR, Collins MW, Iverson GL,et al. Recovery from mild concussion in highschool athletes. J Neurosurg 2003;98:296301.

9 Makdissi M, Darby D, Maruff P, et al. Natural history of concussion in sport markers

of severity and implications for management. Am J Sports Med2010;38:46471.10 Guskiewicz KM, McCrea M, Marshall SW,et al. Cumulative effects associated with

recurrent concussion in collegiate football playersthe NCAA Concussion Study.JAMA2003;290:254955.

11 Belanger HG, Vanderploeg RD. The neuropsychological impact of sports-relatedconcussion: a meta-analysis. J Int Neuropsychol Soc2005;11:34557.

12 Broglio SP, Puetz TW. The effect of sport concussion on neurocognitive function,self-report symptoms and postural controla meta-analysis.Sports Med2008;38:5367.

13 Pellman EJ, Viano DC, Casson IR,et al. Concussion in professional football: injuriesinvolving 7 or more days outpart 5. Neurosurgery2004;55:110016.

14 Iverson G. Predicting slow recovery from sport-related concussion: the newsimple-complex distinction. Clin J Sport Med2007;17:317.

15 Lau BC, Kontos AP, Collins MW, et al. Which on-eld signs/symptoms predictprotracted recovery from sport-related concussion among high school footballplayers?Am J Sports Med2011;39:231118.

16 Cantu RC, Guskiewicz K, Register-Mihalik JK. A retrospective clinical analysis ofmoderate to severe athletic concussions. PM R2010;2:108893.17 Lees-Haley PR, Fox DD, Courtney JC. A comparison of complaints by mild brain

injury claimants and other claimants describing subjective experiences immediatelyfollowing their injury. Arch Clin Neuropsychol2001;16:689915.

18 Mickeviciene D, Schrader H, Obelieniene D,et al. A controlled prospective inceptioncohort study on the post-concussion syndrome outside the medicolegal context. EurJ Neurol2004;11:41119.

19 Alla S, Sullivan SJ, McCrory P. Dening asymptomatic status following sportsconcussion: fact or fallacy?Br J Sports Med2012;46:5629.

20 Meares S, Shores EA, Batchelor J,et al. The relationship of psychological andcognitive factors and opioids in the development of the postconcussion syndrome ingeneral trauma patients with mild traumatic brain injury. J Int Neuropsychol Soc2006;12:792801.

21 Meares S, Shores EA, Taylor AJ,et al. Mild traumatic brain injury does not predictacute postconcussion syndrome. J Neurol Neurosurg Psychiatry2008;79:3006.

22 Meares S, Shores EA, Taylor AJ,et al. The prospective course of postconcussion

syndrome: the role of mild traumatic brain injury. Neuropsychology2011;25:45465.

Table 5 Components of a comprehensive concussion clinic

Component Purpose/role

Personnel

Sports medicine physician,neurologist, neurosurgeon

NeuropsychologistCertified athletic trainer/exercise

physiologistPhysical therapistPsychologistPsychiatristNeuroradiologistResearch coordinatorAccess to subspecialtiesSocial workerEducation specialist/consultant

Detailed assessment andtreatment outline for patient

Comprehensive neuropsychologicalassessment

Coordination of subsymptomthreshold programmeVestibular rehabilitationManagement of expectation/

educationPerform and interpret imagingCoordinate research programmes

Equipment

CT/MRI scannerTreadmill/heart-rate monitorBalance testingReaction timeOthers: bloods, genetic marker

kits

Access to research protocols

ImagingExercise stress testingOther investigations

6 of 7 Makdissi M,et al.Br J Sports Med2013;47:308313. doi:10.1136/bjsports-2013-092255

Review



7/8

23 Cooper DB, Kennedy JE, Cullen MA,et al. Association between combat stress andpost-concussive symptom reporting in OEF/OIF service members with mild traumaticbrain injuries. Brain Inj2011;25:17.

24 Iverson GL. Misdiagnosis of the persistent postconcussion syndrome in patients withdepression. Arch Clin Neuropsychol2006;21:30310.

25 Iverson GL, McCracken LM. Postconcussive symptoms in persons with chronic pain.Brain Inj1997;11:78390.

26 Covassin T, Swanik CB, Sachs M,et al. Sex differences in baselineneuropsychological function and concussion symptoms of collegiate athletes.Br JSports Med2006;40:9237.

27 Piland SG, Ferrara MS, Macciocchi SN,et al. Investigation of baseline relf-reportconcussion symptom scores. J Athl Train 2010;45:2738.

28 Gaetz MB, Iverson GL. Sex differences in self-reported symptoms after aerobicexercise in non-injured athletes: implications for concussion managementprogrammes.Br J Sports Med2009;43:50813.

29 Alla S, Sullivan SJ, McCrory P,et al. Does exercise evoke neurological symptoms inhealthy subjects?J Sci Med Sport2010;13:246.

30 McLean SA, Kirsch NL, Tan-Schriner CU,et al. Health status, not head injury,predicts concussion symptoms after minor injury. Am J Emerg Med2009;27:18290.

31 Gunstad J, Suhr JA. Expectation as etiologyversus the good old days:postconcussion syndrome symptom reporting in athletes, headache sufferers, anddepressed individuals. J Int Neuropsychol Soc2001;7:32333.

32 Lange RT, Iverson GL, Rose A. Depression strongly inuences postconcussionsymptom reporting following mild traumatic brain injury. J Head Trauma Rehabil2011;26:12737.

33 Krol AL, Mrazik M. Self-report of concussion symptoms in collegiate athletes. ArchClin Neuropsychol2009;24:5066.34 Iverson GL, Brooks BL, Ashton VL,et al. Interview versus questionnaire symptom

reporting in people with the postconcussion syndrome. J Head Trauma Rehabil2010;25:2330.

35 Guskiewicz KM, Marshall SW, Bailes J,et al. Association between recurrentconcussion and late-life cognitive impairment in retired professional football players.Neurosurgery2005;57:71924.

36 Guskiewicz KM, Marshall SW, Bailes J,et al. Recurrent concussion and risk ofdepression in retired professional football players. Med Sci Sports Exerc2007;39:9039.

37 Broglio SP, Macciocchi SN, Ferrara MS. Neurocognitive performance of concussedathletes when symptom free. J Athl Train 2007;42:5048.

38 Jordan BD, Relkin NR, Ravdin LD,et al. Apolipoprotein E epsilon4 associated withchronic traumatic brain injury in boxing. JAMA1997;278:13640.

39 Kutner KC, Erlanger DM, Tsai J,et al. Lower cognitive performance of older footballplayers possessing apolipoprotein E epsilon 4. Neurosurgery2000;47:6517.

40 McKee AC, Cantu RC, Nowinski CJ,et al. Chronic traumatic encephalopathy inathletes: progressive tauopathy after repetitive head injury.J Neuropathol ExpNeurol2009;68:70935.

41 McKee A, Stein TD, Nowinski C, et al. The spectrum of disease in chronic truamaticencephalopathy.Brain2013;136:4364.

42 Papa L, Stiell IG, Clement CM,et al. Performance of the Canadian CT Head Rule andthe New Orleans Criteria for predicting any traumatic intracranial injury on computedtomography in a United States Level I trauma center.Acad Emerg Med2012;19:210.

43 Stiell IG, Wells GA, Vandemheen K, et al. The Canadian CT Head Rule for patientswith minor head injury. Lancet2001;357:13916.

44 Leddy JJ, Baker JG, Kozlowski K,et al. Reliability of a graded exercise test forassessing recovery from concussion. Clin J Sport Med2011;21:8994.

45 Gottshall K. Vestibular rehabilitation after mild traumatic brain injury with vestibularpathology.Neurorehabilitation2011;29:16771.

46 Gottshall KR, Hoffer ME. Tracking recovery of vestibular function in individuals withblast-induced head trauma using vestibular-visual-cognitive interaction tests.

J Neurol Phys Ther2010;34:947.

47 Petraglia AL, Maroon JC, Bailes JE. From theeld of play to the eld of combat: areview of the pharmacological management of concussion. Neurosurgery2012;70:152033.

48 Fann JR, Uomoto JM, Katon WJ. Sertraline in the treatment of major depressionfollowing mild traumatic brain injury. J Neuropsychiatry Clin Neurosci2000;12:22632.

49 Reddy CC, Collins M, Lovell M,et al. Efcacy of amantadine treatment onsymptoms and neurocognitive performance among adolescents followingsports-related concussion. J Head Trauma Rehabil (in press).

50 Lovell MR, Iverson GL, Collins MW,et al. Measurement of symptoms following

sports-related concussion: reliability and normative data for the Post-ConcussionScale.Appl Neuropsychol2006;13:16674.

51 Shehata N, Wiley JP, Richea S,et al. Sport concussion assessment tool: baselinevalues for varsity collision sport athletes. Br J Sports Med2009;43:7304.

52 Schneider KJ, Emery CA, Kang JA,et al. Examining Sport Concussion AssessmentTool ratings for male and female youth hockey players with and without a history ofconcussion. Br J Sports Med2010;44:111217.

53 Jinguji TM, Bompadre V, Harmon KG,et al. Sport Concussion Assessment Tool-2:baseline values for high school athletes.Br J Sports Med2012;46:36570.

54 Chen JK, Johnston KM, Petrides M,et al. Recovery from mild head injury in sports:evidence from serial functional magnetic resonance imaging studies in maleathletes. Clin J Sport Med2008;18:2417.

55 Cubon VA, Putukian M, Boyer C,et al. A Diffusion Tensor Imaging Study on thewhite matter skeleton in individuals with sports-related concussion. J Neurotrauma2011;28:189201.

56 Gosselin N, Bottari C, Chen JK,et al. Electrophysiology and functional MRI in

post-acute mild traumatic brain injury. J Neurotrauma2011;28:329

41.57 Tallus J, Lioumis P, Hamalainen H, et al. Long-lasting TMS motor thresholdelevation in mild traumatic brain injury. Acta Neurologica Scandinavica2012;126:17882.

58 Vagnozzi R, Signoretti S, Cristofori L,et al. Assessment of metabolic brain damageand recovery following mild traumatic brain injury: a multicentre, proton magneticresonance spectroscopic study in concussed patients. Brain2010;133:323242.

59 Henry LC, Tremblay S, Leclerc S,et al. Metabolic changes in concussed Americanfootball players during the acute and chronic post-injury phases.BMC Neurol2011;11:105.

60 Slobounov SM, Gay M, Zhang K,et al. Alteration of brain functional network at restand in response to YMCA physical stress test in concussed athletes: RsFMRI study.Neuroimage2011;55:171627.

61 Baillargeon A, Lassonde M, Leclerc S, et al. Neuropsychological andneurophysiological assessment of sport concussion in children, adolescents andadults. Brain Injury2012;26:21120.

62 Johnson B, Zhang K, Gay M,et al. Alteration of brain default network in subacutephase of injury in concussed individuals: resting-state fMRI study. Neuroimage2012;59:51118.

63 Gagnon I, Galli C, Friedman D,et al. Active rehabilitation for children who are slowto recover following sport-related concussion. Brain Injury2009;23:95664.

64 Leddy JJ, Kozlowski K, Donnelly JP,et al. A preliminary study of subsymptomthreshold exercise training for refractory post-concussion syndrome. Clin J Sport Med2010;20:217.

65 Baker JG, Freitas MS, Leddy JJ,et al. Return to full functioning after graded exerciseassessment and progressive exercise treatment of postconcussion syndrome. RehabilRes Pract 2012;2012:705309.

66 Weiss HD, Stern BJ, Goldberg J. Post-traumatic migraine: chronic migraineprecipitated by minor head or neck trauma. Headache1991;31:4516.

67 McBeath JG, Nanda A. Use of dihydroergotamine in patients with postconcussionsyndrome.Headache1994;34:14851.

68 Packard RC. Treatment of chronic daily posttraumatic headache with divalproexsodium.

Headache2000;40:7369.


Review



8/8

postconcussive symptoms?days)management of persistent (>10

best approach to investigation andThe difficult concussion patient: what is the

Willem H MeeuwisseMichael Makdissi, Robert C Cantu, Karen M Johnston, Paul McCrory and

doi: 10.1136/bjsports-2013-0922552013 47: 308-313Br J Sports Med

http://bjsm.bmj.com/content/47/5/308Updated information and services can be found at:

These include:

MaterialSupplementary

http://bjsm.bmj.com/content/suppl/2013/03/11/47.5.308.DC1.htmlSupplementary material can be found at:

References #BIBLhttp://bjsm.bmj.com/content/47/5/308This article cites 67 articles, 15 of whichyou can access for free at:

serviceEmail alerting

box at the top right corner of the online article.Receive free email alerts when new articles cite this article. Sign up in the

CollectionsTopic Articles on similar topics can be found in the following collections

(55)Ice hockey

Notes

http://group.bmj.com/group/rights-licensing/permissionsTo request permissions go to:

http://journals.bmj.com/cgi/reprintformTo order reprints go to:

http://group.bmj.com/subscribe/To subscribe to BMJ go to:

http://bjsm.bmj.com/content/47/5/308http://bjsm.bmj.com/content/47/5/308http://bjsm.bmj.com/content/suppl/2013/03/11/47.5.308.DC1.htmlhttp://bjsm.bmj.com/content/suppl/2013/03/11/47.5.308.DC1.htmlhttp://bjsm.bmj.com/content/suppl/2013/03/11/47.5.308.DC1.htmlhttp://bjsm.bmj.com/content/47/5/308#BIBLhttp://bjsm.bmj.com/content/47/5/308#BIBLhttp://bjsm.bmj.com//cgi/collection/ice_hockeyhttp://group.bmj.com/group/rights-licensing/permissionshttp://group.bmj.com/group/rights-licensing/permissionshttp://journals.bmj.com/cgi/reprintformhttp://journals.bmj.com/cgi/reprintformhttp://group.bmj.com/subscribe/http://group.bmj.com/subscribe/http://group.bmj.com/http://group.bmj.com/http://bjsm.bmj.com/http://bjsm.bmj.com/http://group.bmj.com/http://bjsm.bmj.com/http://group.bmj.com/subscribe/http://journals.bmj.com/cgi/reprintformhttp://group.bmj.com/group/rights-licensing/permissionshttp://bjsm.bmj.com//cgi/collection/ice_hockeyhttp://bjsm.bmj.com/content/47/5/308#BIBLhttp://bjsm.bmj.com/content/suppl/2013/03/11/47.5.308.DC1.htmlhttp://bjsm.bmj.com/content/47/5/308

vestibular - br j sports med 2013 makdissi 308 13

Documents