advances in sport concussion assessment

Review Articles

Advances in Sport Concussion Assessment:From Behavioral to Brain Imaging Measures

Dave Ellemberg,1 Luke C. Henry,2 Steve N. Macciocchi,3 Kevin M. Guskiewicz,4 and Steven P. Broglio5

Abstract

Given that the incidence of sports-related concussion is considered to have reached epidemic proportions, in thepast 15 years we have witnessed an explosion of research in this field. The purpose of the current review is tocompare the results provided by the different assessment tools used in the scientific literature in order to gain abetter understanding of the sequelae and recovery following a concussion. Until recently, the bulk of the hasliterature focused on the immediate outcome in the hours and days post-injury as a means to plan the safestreturn-to-play strategy. This has led to the development of several assessment batteries that are relatively easyand rapid to administer and that allow for multiple testing sessions. The main conclusion derived from thatliterature is that cognitive symptoms tend to resolve within 1 week. However, accumulating evidence indicatesthat cognitive testing should be viewed as one of several complementary tools necessary for a comprehensiveassessment of concussion. Including an objective measure of postural stability increases the sensitivity of thereturn-to-play decision-making process and minimizes the consequences of mitigating factors (e.g., practiceeffects and motivation) on neuropsychological test results. This is consistent with findings that symptom se-verity, neuropsychological function, and postural stability do not appear to be related or affected to the samedegree after a concussion. Furthermore, recent evidence from brain imaging, including event-related potentialsand functional and metabolic imaging, suggest abnormalities in the electrical responses, metabolic balance, andoxygen consumption of neurons that persist several months after the incident. We explain this apparent dis-crepancy in recovery by suggesting an initial and rapid phase of functional recovery driven by compensatorymechanisms and brain plasticity, which is followed by a prolonged neuronal recovery period during whichsubtle deficits in brain functioning are present but not apparent to standard clinical assessment tools.

Key words: assessment; balance and posture; brain imaging; cognition; concussion; sport

Introduction

Increasing attention is being paid to sport-relatedtraumatic brain injury (TBI), or concussion, by the media

and scientific community. A search of the PubMed databasefrom 1990 to 1999 for the term ‘‘concussion’’ yields 994 cita-tions. The same search from 2000 through 2008 yields 1175citations. Much of the recent literature has focused on eval-uating and improving the assessment and return-to-playdecision-making process. This is of particular importanceconsidering studies that demonstrate persistent effects ofmultiple concussions in retired professional football athletes,as well as mild cognitive impairment, self-report memoryimpairments, depression, and earlier onset of Alzheimer’s

disease when compared to the general population (Guskie-wicz et al., 2005; Guskiewicz et al., 2007a).

As more information is synthesized and the understandingof concussive injury has improved, the definition of concus-sion has changed. Most recently, the summary and agreementstatement of the First International Conference on Concussionin Sport updated the definition and stated: ‘‘Concussion isdefined as a complex pathophysiological process affecting thebrain, induced by traumatic biomechanical forces’’ (Aubryet al., 2002; McCrory et al., 2009). Injuries fitting this definitionare estimated to occur in athletic settings between 1.6 and 3.8million times annually (Langlois et al., 2006). Many injuriesare thought to go unreported, as it typically has no outwardlyvisible signs, making it difficult to recognize. Thus in many

1Department of Kinesiology, and 2Department of Psychology, University of Montreal, Montreal, Quebec, Canada.3Shepherd Center and Emory University, Atlanta, Georgia.4Department of Exercise and Sport Science, University of North Carolina, Chapel Hill, North Carolina.5Department of Kinesiology and Community Health, University of Illinois at Urbana–Champaign, Urbana, Illinois.

JOURNAL OF NEUROTRAUMA 26:2365–2382 (December 2009)ª Mary Ann Liebert, Inc.DOI: 10.1089=neu.2009.0906

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instances medical personnel rely on self-report by the athlete,but research suggests that over 50% of concussed high schoolfootball athletes failed to report their injury to medical per-sonnel (McCrea et al., 2004). An equally complex issue is es-tablishing a time course for safe return to play followinginjury. The clinician must balance athlete safety, including therisks of a second concussion (Guskiewicz et al., 2003) or cat-astrophic injury (Cantu, 1995), with the time pressures asso-ciated with athletics.

Once an athlete is suspected of sustaining a concussion,neuropsychological testing has been suggested to be the cor-nerstone of the assessment process, as it provides the clinicianwith objective data for return-to-play decision making (Aubryet al., 2002; McCrory et al., 2009). However, the role of neu-ropsychological testing as a stand-alone test in the concussionassessment protocol has been questioned (Randolph et al.,2005). As such, cognitive testing should be viewed as one ofseveral complementary tools necessary for a comprehensiveassessment of concussion. The concussion assessment proto-col should also include a systematic review of symptoms andthe evaluation of postural stability (Randolph et al., 2005).Furthermore, recent advances in imaging techniques providesensitive measures of brain injury and recovery (Boutin et al.,2008; Lovell et al., 2007). Although functional magnetic reso-nance imaging, event-related potentials, magnetic resonancespectroscopy, and diffusion tensor imaging, have been ap-plied to sport concussion research, their relative novelty hasnot yet allowed them to make their mark in clinical applica-tion. The purpose of the current review is to compare theresults provided by the different assessment tools used in thescientific literature to gain a better understanding of the se-quelae and functional recovery following a sport concussion.

Symptomatology

Use of athlete-reported symptomatology as the primarytool for concussion assessment by sports medicine profes-sionals (Notebaert and Guskiewicz, 2005) is supported by thelarge effect concussion has on physical and cognitive func-tioning immediately following injury and in the ensuing days(Broglio and Puetz, 2008). The presence of symptoms fol-lowing sport TBI is typically short lived (Aubry et al., 2002),although persistent symptoms fall under a defined syndromecalled post-concussion syndrome (PCS). This syndrome isdefined by the Diagnostic and Statistical Manual of MentalDisorders (American Psychiatric Association, 2000) as thepresence of concussion-related symptoms for a least 3 monthsfollowing injury. A discussion of PCS is beyond the scope ofthis review.

A variety of symptom forms have been proposed over theyears, with checklists used to indicate the presence or absenceof a symptom and scales to grade severity and=or duration.Commonly utilized assessments include the Post ConcussionSymptom Scale endorsed by the First International Sympo-sium for Concussion in Sport (Aubry et al., 2002), and theGraded Symptom Checklist recommended by the NationalAthletic Trainers’ Association (Guskiewicz et al., 2004b). Al-though there are subtle differences between these and otherscales, the items of blurred vision, dizziness, drowsiness, ex-cessive sleeping, fatigue, feeling ‘‘in a fog,’’ feeling ‘‘sloweddown,’’ headache, irritability, disorientation, memory prob-lems, nausea, nervousness, decreased concentration, sensi-

tivity to light, and sensitivity to noise, are commonly includedsymptoms.

The presence of post-concussive symptoms varies widelyamong individuals, although some symptoms do emergemore commonly than others. For example, headache has beenreported to occur in an average of 83% of concussed athletes,while other symptoms, such as dizziness (65% of concussedathletes) and confusion (57% of concussed athletes), are alsoprevalent, but occur less frequently (Delaney et al., 2002;Guskiewicz et al., 2003; Guskiewicz et al., 2000; McCrory et al.,2000). Notably, the heavy reliance traditionally placed on lossof consciousness (LOC) as a marker of concussion and con-cussion severity does not seem to be well founded. LOC isobserved in fewer than 10% of all injuries (Delaney et al., 2002;Guskiewicz et al., 2003), and clinical outcomes following in-jury do not appear to be tied to the presence or absence ofon-field LOC (Lovell et al., 1999). Other symptoms, such aspost-traumatic amnesia, appear to provide greater sensitiv-ity to injury severity, with longer spans of amnesia indicativeof a worse outcome (Collins et al., 2003; Erlanger et al., 2003).

Symptom recovery appears to occur rapidly in most con-cussed athletes. In an investigation of concussed collegiatesoccer and football athletes, 87–92% reported no symptomswithin 3 days of injury, and 95% reported complete symptomresolution within 7 days of injury (Delaney et al., 2002). This isconsistent with investigations of young adults finding thatrecovery occurs within 2–10 days of injury (Broglio et al.,2007a; Collie et al., 2006; Field et al., 2003; Guskiewicz et al.,2003; Macciocchi et al., 2001). Athletes without symptomsimmediately following the injury may experience delayedonset of symptoms, and clinicians should be prepared tocheck for this during serial assessments for at least 3 days afterthe suspected injury (Guskiewicz et al., 2003). Althoughprofessional athletes exhibit notably fewer symptoms whenevaluated 1 and 3 days following injury (Pellman et al., 2006),a complete understanding the low symptom reports seen inthese athletes has not been elucidated, although job security isspeculated as a possible cause.

More notable are the differences between men and womenin reporting concussion-related symptoms following injury.In many instances women will report experiencing moresymptoms than men, with increased reports of somaticsymptoms such as headache, fatigue, and dizziness (Brosheket al., 2005; Farace and Alves, 2000). The foundation for gen-der differences in symptom reporting is not entirely clear,although cultural constructs may result in female athletesbeing more willing to express their symptoms to medicalpersonnel (Granito, 2002). This is consistent with the findingthat female athletes report a more significant number of mildbaseline symptoms than male athletes (Covassin et al., 2007,2003).

The evaluation of symptoms associated with sport con-cussion is quick, cost-efficient, and easy for medical personnelto implement in clinical practice. In many circumstances thesymptom evaluation involves asking the injured athlete toindicate the presence or absence of symptoms following asuspected injury. Despite its heavy use in concussion evalu-ation, however, this method of assessment has inherentweaknesses (Lezak et al., 2004). For example, the presence ofsymptoms alone may not be indicative of a concussion, as 20%of athletes may experience exercise-induced headaches(McCrory, 1999), and athlete willingness to report symptoms

2366 ELLEMBERG ET AL.

may not be at its highest when external pressure or a strongdesire to return to play is present (McCrea et al., 2004). Fur-thermore, some athletes report symptoms at rest, justifyingthe importance of obtaining preseason baseline symptomscores (Lovell et al., 2006; Mailer et al., 2008).

Overall, it appears that symptom recovery following con-cussion diagnosis has been used as a guide for injury recov-ery, but it is not a definitive return-to-play tool. This protocolis evidenced by the variant recovery patterns noted betweensymptoms and cognitive function (Broglio et al., 2007b; Fazioet al., 2007). In light of this evidence, symptom evaluation maynot reflect the resolution of all post-concussion decrements,and therefore should only be used in combination with otherevaluative measures and not as a sole indicator for return toplay.

The practicality of symptom reports as an indicator ofconcussion is clear, but further investigative work is needed.What is most needed is a better understanding of how toobtain accurate concussion symptom reports from injuredathletes. In addition, revision of the symptom list may be inorder. Piland and colleagues (Piland et al., 2003, 2006) notedthat nine symptoms may best characterize concussion by re-moving confounding symptoms, but this scale has not beenwidely adopted. In addition, clinical guidelines for return toplay note that no athlete should return to sport participationwhile still symptomatic (Guskiewicz et al., 2004b; Kissick andJohnston, 2005). However, recent evidence has shown a clin-ical improvement in those who participated in moderate ac-tivity while still symptomatic (Majerske et al., 2008; Willerand Leddy, 2006). A better understanding of how exercisemay increase or decrease recovery from concussive injuries isclearly warranted.

Postural Stability

Balance plays a vital role in the maintenance of fluid dy-namic movement common in sport. Balance is the process ofmaintaining the center of gravity within the body’s base ofsupport, and many factors enter into the task of controllingbalance within this designated area ( Jacobs and Horak, 2007).The system involves a complex network of neural connectionsand centers that are related by peripheral and central feedbackmechanisms. A hierarchy integrating the cerebral cortex,cerebellum, basal ganglia, brainstem, and spinal cord is pri-marily responsible for controlling voluntary movements(Guyton, 1986; Vander et al., 1990).

Postural instability has been identified in pathologicalconditions such as moderate to severe TBI (Geurts et al., 1996;Ingersoll and Armstrong, 1992; Mallinson and Longridge,1998; Wober et al., 1993), hemiplegia and craniocerebral injury(Arcan et al., 1977), cerebellar atrophy and ataxia (Mauritzet al., 1979), and whiplash (Mallinson and Longridge, 1998;Rubin et al., 1995). It has been proposed that communicationbetween sensory systems is lost in the majority of these indi-viduals, causing moderate to severe postural instability ineither the anterior-posterior direction, medial-lateral direc-tion, or both. In most cases, symptoms such as dizziness,vertigo, tinnitus, lightheadedness, blurred vision, and pho-tophobia, all having visual, vestibular, and=or somatosensoryorientation, are reported (Geurts et al., 1996; Ingersoll andArmstrong, 1992; Mallinson and Longridge, 1998; Rubin et al.,1995; Wober et al., 1993).

More recently, balance and postural stability have beenstudied as objective measures in the evaluation of athleteswith acute cerebral concussion. Concussed athletes havedemonstrated balance deficits following concussion usingboth high-tech and clinical methods of assessment. In mostcases, decreases in postural stability persisted for up to 3 daysfollowing injury in comparison to control subjects, and weremost evident when the subjects were standing either on afoam or moving (tilting) surface. Subsequent studies haveidentified decreases in postural stability for up to 3 days post-injury using the Sensory Organization Test (SOT) on theNeuroCom Smart Balance Master (Guskiewicz et al., 1997,2001). Using the SOT, Guskiewicz and associates (2001) alsofound that overall balance performance typically recoversbetween days 1 and 3 post-injury. These studies identifieddeficits between concussed and control subjects, especiallywhen visual and support surface conditions were altered.Athletes appear to have sensory interaction and decreasedpostural control until approximately 3 days following injury.The athletes gradually recover to approximately the scores ofmatched control subjects by day 10 post-injury.

It appears that this deficit is related to a sensory interactionproblem, whereby the concussed athlete fails to use their vi-sual and vestibular systems effectively. The integration ofvisual and vestibular information is essential for the mainte-nance of equilibrium under certain altered conditions similarto those performed during the SOT (Nashner and Berthoz,1978; Nashner, 1976; Nashner et al., 1982). If an athlete hasdifficulty balancing under conditions in which sensory sys-tems have been altered, it can be hypothesized that they areunable to ignore altered environmental conditions andtherefore select a motor response based on the altered envi-ronmental cues.

The SOT requires sophisticated force plate systems thatprovide a way to challenge and alter information sent to thevarious sensory systems. While the aforementioned studiessuggest that force platform sway measures provide valuableinformation in making return-to-play decisions followingconcussion, there is still a question of practicality and acces-sibility for the sports medicine clinician. In an attempt toprovide a more cost-effective, yet quantifiable method of as-sessing balance in athletes, the Balance Error Scoring System(BESS) was developed by researchers at the University ofNorth Carolina. This clinical balance test can be administeredon the sideline (Guskiewicz, 2001).

In the absence of sophisticated force plate technology, theuse of a quantifiable clinical test battery such as the BESS isrecommended. Three different stances (double, single, andtandem) are completed twice, once while on a firm surfaceand once while on piece of medium-density foam (AirexBalance Pad 81000; www.power-systems.com) for a total ofsix trials (Fig. 1). Athletes are asked to assume the requiredstance by placing their hands on the iliac crests, and that uponeye closure the 20-sec test begins. During the single leg stan-ces, subjects are asked to maintain the contralateral limb in20–308 of hip flexion and 40–508 of knee flexion. The single-limb stance tests are performed on the non-dominant foot.This same foot is placed towards the rear on the tandemstances. Subjects are told that upon losing their balance, theyare to make any necessary adjustments and return to thestarting position as quickly as possible. Performance is scoredby adding one error point for each error committed (Table 1).

ADVANCES IN SPORT CONCUSSION ASSESSMENT 2367

Trials are considered to be incomplete if the athlete is unableto sustain the stance position for longer than 5 sec during theentire 20-sec testing period. These trials are assigned a stan-dard maximum error score of 10.

Significant correlations between the BESS and force plat-form sway measures using healthy young adults have beenestablished for five static balance tests (single leg stance-firmsurface, tandem stance-firm surface, double leg stance-foamsurface, single leg stance-foam surface, and tandem stance-foam surface), with intertester reliability coefficients rangingfrom .78 to .96 (Riemann et al., 1999). Another study using theBESS identified the best test variations for eliciting posturalunsteadiness following concussion. The SOT was also ad-ministered to determine if the results of the clinical balancetests paralleled results attained with a force plate system

(Riemann and Guskiewicz, 2000). Significant group differ-ences on day 1 post-injury were revealed using the BESS withthe double leg, single leg, and tandem stances on both a firmand foam surface. The results of the SOT composite scoresparalleled the results revealed with the clinical balance tests,and were similar to recovery curves reported in previous in-vestigations (Guskiewicz et al., 1996, 1997). Resolution ofsigns and symptoms recorded across the three post-injurytesting sessions appear to coincide with the postural stabilityrecoveries demonstrated by the mild-head-injured subjects.The results revealed greater differences between injured anduninjured subjects when the balance tasks became morechallenging, such as by adding a foam surface and narrowingthe base of support (Fig. 2). Although the standard Rombergtest (double leg, firm surface) has been previously advocatedfor use in concussion assessment ( Jansen et al., 1982; Thyssenet al., 1982), it fails to objectively identify subtle balance def-icits following concussion. Moreover, studies involving theBESS have revealed similar recovery curves (within 3–5 dayspost-injury) to those seen using sophisticated force platetechnology.

Currently new assessment paradigms including posturalstability assessment in the presence of a cognitive task arebeing considered. One recent study using gait stability as ameasure of posture suggested that concussed individuals mayadopt a slower, more conservative gait strategy to maintainbalance. Under these conditions, concussed individuals con-tinued to exhibit signs of instability with large center-of-massdeviations that were greater in the presence of a cognitivetask; these deviations were significantly greater than in con-trols under both the single-task and dual-task conditions(Catena et al., 2007). Broglio and associates (2005) studiedhealthy individuals under dual-task conditions, using onlythe eyes-opened conditions of the SOT, and found that pos-tural control improved in healthy individuals with the addi-tion of the cognitive task, as healthy individuals appear to beable to divide and focus attention as needed. These studiesindicate the possibility of integration of dual tasking measuresinto the current assessment paradigm, as these measures moreclosely mimic the cognitive and postural demands of sport.

FIG. 1. Balance Error Scoring System (BESS) performed onthe firm surface (A–C) and the foam surface (D–F).

Table 1. Errors Recorded for Balance Error

Scoring System (BESS)

Hands lifted off iliac crestsOpening eyesStep, stumble, or fallMoving hip into more than 308 of flexion or abductionLifting forefoot or heelRemaining out of testing position for more than 5 secondsThe BESS score is calculated by adding one error point

for each error or any combination of errors occurringduring one movement

FIG. 2. Error score means (�standard deviation) for thethree stances on both surfaces for 16 mild-head-injured (MHI)and 16 control subjects on day 1 post-injury (DL, double legstance; SL, single leg stance; TD, tandem stance; FI, firmsurface; FO, foam surface). There were no errors committedby the control group for the DL=FI and DL=FO tests (fromRiemann and Guskiewicz, 2000, with permission).


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Postural stability assessment, whether done through theuse of a force plate or a clinical balance test such as the BESS, isuseful in identifying neurological impairment in athletes inthe acute post-concussion phase. This impairment typicallylasts up to 3–5 days post-injury, but in cases involving visualand vestibular dysfunction, the balance impairment may lastweeks or months (Guskiewicz et al., 2001; McCrea et al., 2003).Clinicians should realize that postural stability is only onesmall piece of a very large puzzle in the assessment of con-cussion, and that concussion may not necessarily affect thepostural control system in every case, nor is postural insta-bility manifest in a consistent manner in every athlete.

Paper and Pencil Neuropsychological Testing

Clinician-administered neuropsychological assessment hasbeen used to document the impact of concussive injuries forover 30 years and probably longer, as evidenced by Gronwalland Wrightson’s (1975) early work on multiple concussiveinjuries. In parallel with the initial clinical and empirical in-terest in sports concussion, which was first apparent in thelate 1970s, neuropsychological tests were being used in manyclinical research studies that focused on concussions second-ary to falls, assaults, and motor vehicle accidents (Barth et al.,1983; Dikmen et al., 1995; Levin et al., 1987). Neuropsycho-logical tests used in these studies were adapted from main-stream neuropsychological practice and typically involvedextended testing, often using fixed or flexible batteries thatindexed numerous cognitive skills such as intelligence,problem solving, and language, and attention-concentrationand memory skills (Dikmen et al., 1995).

As sports concussion research became more prevalent, theneuropsychological consequences of concussion became moreclearly defined, which resulted in truncating the extensivetesting typically used in non-sports populations and earlysports concussion studies. The emphasis in sports concussionmoved strongly toward assessment of attention, workingmemory, and information processing speed (Macciocchi et al.,1996), although some researchers continued to use more ex-tensive test batteries (Lovell et al., 1999). At that time, as wellas today, there are a large number of clinician-administeredtests that can be used to document the impact of sports con-cussion. Table 2 reviews the psychometrics of a number ofinstruments that have been used in research and clinicalpractice, but these tests by no means exhaust the optionsclinicians and researchers have at their disposal when per-forming clinical examinations or planning research investi-gations (Lezak et al., 2004; Strauss et al., 2006).

Psychometric characteristics of neuropsychologicaltests used with concussed athletes

The psychometric characteristics of most neuropsycholo-gical tests used in sports concussion assessment and researchhave been examined at length in non-sports populations, butthere are few studies that specifically address the reliability,standard error of measurement, practice effect sizes, sensi-tivity, specificity, and positive predictive value of clinician-administered neuropsychological tests used in sportspopulations. While the lack of extensive psychometric data insports populations may be a concern, clinician-administeredpencil-and paper-tests typically have more extensivelydocumented psychometrics than computerized tests (Broglio

et al., 2007c). The development of computerized tests was inpart driven by the desire to increase the reliability and sen-sitivity of clinician-administered tests, although test devel-opers’ claims of superior psychometrics and the promise ofthese instruments remains in doubt based on existing research(Broglio et al., 2007c; see below for a review of computer-based cognitive assessments). In any case, even though anumber of clinician-administered neuropsychological testshave been employed in research, there is no consensus onwhat clinician-administered tests alone or in combination arebest suited for diagnostic and return-to-play assessments.

Issues with the administration of neuropsychologicaltests to an athletic population

While clinician-administered neuropsychological tests arereadily available, several problems associated with test ap-plication deserve mention. First, clinician-administered test-ing is labor intensive and requires resources such as trainedexaminers, which was a significant factor in the move towardcomputerized test administration over the past 10 years.Second, these tests must be interpreted, which means a neu-ropsychologist must provide decision rules for test interpre-tation of clinically meaningful changes, but establishingconsistent decision rules is complicated. Changes in neu-ropsychological test scores over time may be due to factorsother than concussion, such as learning problems and fatigue;somatic symptoms such as headache, depression, anxiety,and hyposomnia; and residual effects of alcohol intoxicationand=or sub-optimal effort (Hunt et al., 2007). For instance,consider the base rate of headache immediately followingconcussion. Headache is one of the most common symptomsfollowing concussion in sports (>80%) as well as in generalclinical populations (Alves et al., 1993; Macciocchi et al., 1996).One can imagine how headache could affect sleep, which inturn could affect test performance up to several days follow-ing injury. One cannot assume that impaired performance on

Table 2. Ranges of Reliability Coefficients, Standard

Error of Measurement, and Practice Effect

Sizes for Neuropsychological Tests Commonly

Utilized in Concussion Research

Test Reliability SEMa Practice effect size

WCST .39–.72 8.0–11.9 .30–.1.0TMT .45–.72 4.7–5.6 .20–.73SDMT .72–.80 4.5–5.3 .10–.20DST .80–.91 .90–.95 .10–.45PASAT .80–.90 3.1–3.9 .40–1.3GPT .69–.78 6.9–8.1 .10–.35COWAT .70–.88 5.1–6.2 .30–.52HVLT .78 .95–2.1 .24–.30

WCST, Wisconsin Card Sort Test; TMT, Trail Making Test; SDMT,Symbol Digit Modalities Test; DST, Digit Span Test; PASAT, PacedAuditory Serial Addition Test; GPT, Grooved Pegboard Test;COWAT, Controlled Oral Word Association Test; HVLT, HopkinsVerbal Learning Test; SEM, standard error of the mean.

aRange of SEM based on lower and upper reliability coefficientsand normative data for age-, education-, and gender-appropriatecomparison groups. References used to gather data for this table:Spreen and Strauss, 1998; Mitrushina et al., 1999; Benedict et al.,1998; WAIS-III=WMS-III Technical Manual, 1997; Heaton et al., 1993;Smith, 1995; McCaffery et al., 2000.


neuropsychological tests is due to transient impairment sec-ondary to cerebral trauma when other factors such as headachemay have a significant direct or indirect effect on test perfor-mance. Currently there are no scientifically validated algo-rithms for clinician-administered test interpretation, whichmeans individual clinicians and researchers use idiosyncraticdecision rules, which can lead to variability across individualathletes and research findings (Broglio et al., 2007c).

Reliability issues also complicate one’s ability to assess theimpact of sports concussion. On the one hand, tests need to besufficiently reliable, while at the same time they are not soreliable that they are insensitive to the effects of concussion.For instance, tests with high reliability coefficients such as theDigit Span Test typically have low sensitivity. In contrast, theTrail Making Test (TMT) has relatively high sensitivity andhas been widely used in clinical settings as well as in researchinvestigations of sports concussion (Collins et al., 2002; Mac-ciocchi et al., 1996; Matser et al., 1999). Unfortunately, the TMThas been shown to have test-retest reliability in the question-able range in some studies (.50–.60), and significant practiceeffects in others (Macciocchi et al., 1992; Spreen and Strauss,1998). Reliability problems would be expected to impact sen-sitivity, specificity, and positive predictive value, all of whichare important when using neuropsychological tests to identifyand monitor post-concussive changes in cognition.

An additional concern involves the susceptibility of neuro-psychological instruments to practice effects. Although thereis limited literature regarding practice effects, many measuresused in studies of concussion have been found to have pro-minent practice effects (Macciocchi et al., 1992; Spreen andStrauss, 1998). In fact, some tests have practice effect sizes thatequal or exceed effects of concussions on those same instru-ments (McCaffrey et al., 2000). In clinical practice, one solu-tion for large practice effect sizes is the use of alternate formsof the same test, but the extent to which this strategy effec-tively reduces practice effects is questionable, particularlywhen tests are administered numerous times over a briefperiod (Macciocchi et al., 1996, 2001). An alternative approachemployed by Hinton-Bayre and colleagues (1999) utilizesmultiple pre-injury assessments in order to obtain maximalperformance prior to injury, while limiting practice in subse-quent post-injury assessments. In this approach, athletes areadministered dependent measures several times prior to en-tering a study. Consequently, athletes’ optimal level of per-formance is reached prior to injury, and a decrement inperformance following injury would reflect change from thisoptimal level. This methodology has considerable promisebecause changes in performance would theoretically reflectgenuine impairment in neuropsychological functioning post-injury and not psychometric variability. However, a draw-back that can limit the application of this strategy is thenotable time allotment needed to gain an acceptable baselineassessment.

Neuropsychological markers of post-concussionsequelae and recovery

Given the documented pathophysiological response tosports concussion (Giza and Hovda, 2001; Jantzen et al., 2004),tests focused on sustained and divided attention, reactiontime, visual and auditory processing speed, and workingmemory are most likely to be sensitive to the effects of con-

cussion. In fact, the neuropsychological tests administered byclinicians that have been shown to be most sensitive to con-cussive injuries include the TMT, the Symbol Digit ModalitiesTest, and the Paced Auditory Serial Addition Test (Broglioet al., 2007c; Collins et al., 1999, 2002; Hinton-Bayre andGeffen, 2002; Pellman et al., 2004). However, the sensitivityand specificity of these instruments varies across studies andseems to some extent to be population-dependent.

While many studies reveal a cognitive decrement in thehours and days following even a first concussion, there is noagreement on the duration of cognitive symptoms and thetime course of recovery. A series of studies using paper-and-pencil tests report that cognitive sequelae rarely persist be-yond 2 weeks after a concussion (Echemendia et al., 2001;Guskiewicz, 2001; Macciocchi et al., 2001, 1998; Peterson et al.,2003). In addition to a pre-season baseline test, most protocolstested athletes up to five times during that short period. Asnoted earlier, despite the use of alternate versions, practiceeffects likely underestimate impairments caused by the con-cussion. In fact, some athletes actually perform significantlybetter during the last testing session than they did on theirpre-concussion baseline (Belanger et al., 2005; Echemendiaet al., 2001). In addition to a practice effect, some athletesmight also have been motivated to perform exceptionally wellgiven that in most protocols return-to-play decisions de-pended on their test results. When athletes (high school, col-lege, and professional) are tested only once, even up to severalmonths after a first concussion, persistent cognitive deficitsare revealed (Downs and Abwender, 2002; Ellemberg et al.,2007; Matser et al., 1999, 1998; Witol and Webbe, 1994). Forexample, a recent study comparing intercollegiate femaleathletes suffering their first concussion to a group of age-matched non-concussed teammates demonstrated enduringcognitive deficits at least up to 9 months following injury(Ellemberg et al., 2007). Cognitive deficits were apparent ontests that appraised high-level executive functions, such asplanning, anticipating, and complex decision making. Thissuggests that the effects of sport-related concussion may bemore enduring than once thought.

Overall, clinician-administered tests have psychometricstrengths and limitations. Despite 20 years of research onsports concussion, there is no consensus or guidelines onwhich tests provide clinicians and researchers with the mostreliable, sensitive, and specific neuropsychological metrics.The advent of computerized tests has to some extent hinderedthe development of appropriate clinical decision rules forclinician-administered tests, but clinician-administered testshave been shown to be sensitive to the effects of sports con-cussion in a large number of studies. Whether these instru-ments will continue to be used and developed for sportsconcussion clinical practice and research remains to be seen.

Computer Platform Neuropsychological Testing

Presently, four computer-based neuropsychological as-sessments are available for sport concussion assessment: Im-PACT (Pittsburgh, PA), Headminder Concussion ResolutionIndex (CRI) (New York, NY), CogSport (CogState, Mel-bourne, Australia), and the Automated NeuropsychologicalAssessment Metric (ANAM) (Center for the Study of HumanOperator Performance, The University of Oklahoma, Nor-man, OK). The length of this review does not permit a detailed


description of each test’s methodology, which have beenprovided elsewhere (Bleiberg et al., 2000; Erlanger et al., 2002;Iverson et al., 2005; Makdissi et al., 2001). Many of these testswere developed to alleviate problems associated withtraditional pen-and-paper based testing, such as baselineadministration time, learning effects associated with multiplepost-injury assessments, and the need for specialized per-sonnel to interpret results. These computer-based batteriesemploy multiple sub-tests that evaluate a range of cognitivedomains, such as information processing, planning, memory,and switching mental set. Many also include an evaluation ofsymptoms associated with sport concussion, a review ofwhich has been addressed in a different section of this article.The computer tests can be rapidly administered (20–25 min) tomultiple athletes simultaneously, and several forms areavailable for post-morbid assessments to reduce learning ef-fects, and interpretation of results is commonly automated forthe clinical sports medicine staff. These improvements overpencil-and-paper tests have led to their adoption by sportsmedicine professionals as part of their assessment protocols atall levels of sports, from the intramural athlete through theprofessional (Ferrara et al., 2001; Notebaert and Guskiewicz,2005).

The computer-based assessments of cognitive performancehave been evaluated for their ability to detect post-morbiddecrements. For example, when a group of high school ath-letes was assessed within 3 days of injury, the ImPACT testcorrectly identified 81.9% of the concussed athletes as havingsome cognitive impairment or elevated symptom reports(Schatz et al., 2006). This level of sensitivity is slightly higherthan that reported in a group of concussed collegiate athleteson the ImPACT (62.5% sensitivity) and the Headminder CRI(78.6% sensitivity), although concussion-related symptomswere not included in the evaluation process (Broglio et al.,2007c). Investigations of ANAM and CogSport sensitivity couldnot be found. The moderate sensitivity to post-concussiondecrements is encouraging, but all athletes should be evaluatedon a case-by-case basis. Variables such as previous history,psychological factors, genetics, and methodology appear toplay a role in testing outcomes (McCrory et al., 2005b), butin general, computer-based testing shows declines in cogni-tive performance following injury, with a steady return tobaseline in the subsequent days and weeks. Perhaps the mostimportant factor in recovery time is the age of the athlete(Field et al., 2003).

Establishing the functional recovery of cognition followingconcussion in the high school athlete is difficult because ofdevelopmental issues occurring in adolescents. Concussedathletes evaluated on the ANAM battery returned to normalfunctioning on all aspects of the test 1 week post-injury, exceptfor memory, which resolved by day 10 (Sim et al., 2008). Aseries of investigations implementing the ImPACT test dem-onstrated impairment on verbal memory and reaction timerelative to baseline in high school athletes when tested anaverage of 5 days post-concussion (Pellman et al., 2006).However, those with grade 1 injuries took a day longer todemonstrate full recovery on the same assessment battery(Lovell et al., 2004a), and a separate investigation found thatconcussed high school athletes continued to have compositememory impairments at 7 days post-injury (Lovell et al.,2003). Full recovery from sport concussion was apparent 35days following concussion when concussed and control sub-

jects performed comparably on a cognitive assessment (Lovellet al., 2007).

Cognitive functioning in post-morbid young adults showsa similar recovery pattern as their younger counterparts.Evaluations completed within 48 h of sport concussion diag-nosis revealed a decrease in the ANAM composite score in55% of the sample (Guskiewicz et al., 2007c). Follow-up test-ing was not reported, although concussed military recruitsreturned to their baseline level of performance on all ANAMvariables within 4 days of injury, with the exception of simplereaction time (Warden et al., 2001) Similar trends have beennoted when the ImPACT test was implemented in the eval-uation of concussed young adults. For example, cognitionreturned to baseline levels in those without a history of con-cussion within 5 days post-injury, while those with two ormore previous injuries continued to show impaired perfor-mance on reaction time and verbal memory (Covassin et al.,2008). Further follow-up assessments were not completed, butseparate investigations show prolonged impairment on thesame variables when evaluated up to 10 days following di-agnosis (Broglio et al., 2007b; Covassin et al., 2008). In allinstances, additional test administrations were not given todetermine if there was complete restoration of functionalcognition.

Only one investigation examining the functional recoveryon computer-based neuropsychological assessments follow-ing sport concussion has been conducted with professionalathletes. As part of the National Football League’s investiga-tion of concussion, concussed professional athletes wereevaluated the day following injury and again 3 days post-injury. When evaluated on the ImPACT test, the NFL athletesshowed declines in verbal and visual memory, reaction time,and processing speed at the initial post-injury assessment, butscores returned to baseline levels by day 3 (Pellman et al.,2006). Figure 3 summarizes the recovery trends indicated bycomputer-based neuropsychological exams in some of theavailable studies.

Some experts have suggested that the cognitive evaluationshould serve as the cornerstone of the concussion assessmentprocess (Aubry et al., 2002), and the rapid adoption andpresence of computer-based cognitive evaluations suggeststhat they have become a key component of the concussionassessment battery. Regardless, surprisingly few studies havebeen carried out that track recovery in concussed athletes viacomputer-based assessments. While these tests provide

FIG. 3. Minimum days to recovery as indicated by com-puter-based neurocognitive assessment. The dotted line in-dicates the mean minimum recovery (5.9 days) for all settings.



valuable information on the cognitive performance of theconcussed athlete, they do not appear to accurately reflect themetabolic recovery of the injured brain. In the investigationsreviewed here, athlete age appears to influence recovery, butmost high school and collegiate athletes displayed functionalcognitive recovery approximately 6 days following a sport-related concussion, while the professional athlete displayedrecovery within 3 days. This falls shy of the 14–28 days ofimpaired glucose metabolism (Giza and Hovda, 2001) andmetabolic imbalance (Vagnozzi et al., 2008) reported in hu-mans. This discrepancy may account for the increased con-cussion incidence seen when athletes are returned within thefirst 7–10 days of injury (Guskiewicz et al., 2003). Further-more, many assessment paradigms call for multiple test ad-ministrations in the days following the concussion diagnosis.In one investigation concussed athletes were evaluated onseven occasions within a week of injury, with two assess-ments occurring within the first 3 h post-diagnosis (McCreaet al., 2003). Improvements on some computer paradigmshave been noted in healthy athletes (Bleiberg et al., 2004),leading one to speculate that improvements in concussedathletes may be partially associated with learning effects andnot with injury recovery. As such, unless mitigating circum-stances are present, clinicians should consider delaying theadministration of neuropsychological assessments for thepurpose of determining return-to-play status until the athleteis symptom-free (Guskiewicz et al., 2004b).

This review does not encompass all of the available litera-ture on cognitive functioning in the concussed athlete. Ad-ditional investigations have been completed on the groups ofinterest examined here, but intramural and collegiate athleteswere commonly pooled, thus preventing a separate evalua-tion of the two groups. It is clear, however, that the use ofcomputer-based assessment for the clinical evaluation ofcognitive functioning is well founded at all levels of sport.Some investigators have speculated that their use in the as-sessment process should be limited (Randolph et al., 2005),and others have shown that they may show state functioning,rather than trait cognitive performance (Broglio et al., 2007a).Regardless, the recovery patterns presented here are repre-sentative of group performance, necessitating an individual-ized approach to each athlete.

Electrophysiological Measures

The recording of electroencephalograms (EEGs) synchro-nized with a cognitive or perceptual task is a common re-search and clinical tool for the diagnosis and management ofvarious brain pathologies, including epilepsy, multiple scle-rosis, and the effects of premature birth and concussion(Magnano et al., 2006; Viggiano, 1996; Walls-Esquivel et al.,2007). These electrophysiological techniques assess the in-tegrity of specific brain processes during the performance ofcognitive tasks for which behavioral impairments are ob-served. The main feature of event-related potentials (ERPs) isthat they reveal ongoing and covert processing that cannot befully assessed by behavioral measures. In fact, it is the objec-tivity, reliability, and relative low cost of ERPs that nowmakes them a common clinical tool to assess brain injury.

The potential benefits of ERPs for the investigation of sport-related concussion has only been recently explored. Althoughyoung, this modality has already made a significant contri-

bution to our understanding of sport-related concussion. Thepresent section provides the first comparative analysis of thisliterature in order to highlight its main conclusions and pro-vide a better understanding of its limits. We will systemati-cally review evidence that ERPs are a sensitive measure ofsymptomatology, the cumulative effects of repeated concus-sions, and recovery.

Post-concussion symptoms

ERPs provide a sensitive measure of subtle functionalneuronal damage when no clinical symptoms are reported byconcussed athletes, and when the results on classical neu-ropsychological tests are normal. The strongest evidence forthis comes from a study by Gosselin and colleagues (2006)that compared results from paper-and-pencil neuropsycho-logical tests (a modified NFL battery; Lovell and Collins,1998) to those of cognitive evoked potentials in a group ofsymptomatic concussed athletes, a group of asymptomaticconcussed athletes, and a third group of athletes from a non-contact sport without a history of concussion. The concussedathletes were a mixed bag of football, soccer, and hockeyplayers, and the majority of athletes in this group had sufferedtwo or more concussions. The non-concussed athletes wereeither volleyball or tennis players. This is the only study inthe ERP sports literature to include a control group consistingof athletes without a history of concussion that came from anon-contact sport. This is particularly important, as a signif-icant portion of soccer and football players fail to recognizethat they suffered symptoms associated with a concussion(Delaney et al., 2002).

Compared to the two other groups, the self-reportedsymptomatic athletes had significantly higher scores on apost-concussion symptom scale. However, no difference wasfound between the symptomatic and asymptomatic athleteswith regard to the total number of concussions sustained (i.e.,three to five concussions), the severity of the last concussion,the time elapsed between testing and the last concussion (i.e.,5–15 weeks), and the number of episodes of LOC. Overall, thethree groups of athletes had comparable results on the paper-and-pencil neuropsychological tests as they did for the reac-tion time component of the computerized choice reaction timetask associated with the ERP paradigm. In contrast, the con-cussed athletes had significantly lower amplitudes and longerlatencies for the P3 component of the ERP compared to thecontrol group, with no difference between the symptomaticand the asymptomatic athletes. In addition to finding abnor-mal ERPs in asymptomatic concussed athletes, Gosselin andassociates (2006), as well as other researchers (Dupuis et al.,2000; Gaetz et al., 2000; Lavoie et al., 2004), found that theseverity of self-reported clinical symptoms in the symptom-atic athletes were negatively correlated with the amplitude ofthe P3 component.

The ERP task used by Gosselin and colleagues was amodified version of the classical auditory oddball paradigmthat was designed to have greater attentional requirements(2006). The oddball paradigm is the most widely used in theERP literature. In its simplest form, it consists of a choice re-action time task during which the subject is asked to respondto an infrequent stimulus (presented in 10–25% of trials), andto ignore a frequent stimulus. The neurophysiological re-sponse associated with each stimulus is a waveform that ap-


pears anytime between 250 and 600 msec after the presenta-tion of the stimulus. This is known as the P3 component. Theamplitude of the P3 is said to reflect the amount of attentionallocated to the stimulus, while its latency reflects the pro-cessing speed associated with stimulus categorization (i.e.,frequent versus infrequent stimulus).

Two other sets of researchers also found a reduction in theamplitude of the P3 component in concussed athletes withotherwise normal results on neuropsychological tests (Dupuiset al., 2000; Lavoie et al., 2004). However in these cases, onlythe self-reported symptomatic athletes had abnormal ERPs.The ERPs of the asymptomatic concussed athletes were nodifferent than those of non-concussed athletes who partici-pated in the same contact sport (e.g., football). This differentpattern of results could likely be explained by the lack of acontrol group from a non-contact sport, or because the odd-ball choice reaction time tasks used in those studies were vi-sual rather than auditory and they had a weaker attentionalload.

Cumulative effects of multiple concussions

ERPs have been used to investigate the possibility of cu-mulative damage that could result from a history of multipleconcussions. The first study to use ERPs as a measure of braindamage in sport-related concussion (Gaetz et al., 2000) com-pared four groups of junior hockey players: athletes with nohistory of concussion; athletes who experienced one concus-sion; athletes who experienced two concussions; and athleteswho experienced three or more concussions. The athletes fromthe injured groups had concussions of comparable severity,corresponding to a grade three concussion, and were tested atleast 6 months post-injury. By means of a classical visualoddball task, a significant difference in the latency of the P3component was found between the no-concussion group andthe three-or-more-concussions group. Although not signifi-cant, the one- and two-concussions groups had longer P3 la-tencies than the non-concussion group, but shorter than thoseof the three-or-more-concussions group. Unfortunately, it isimpossible to attribute the findings only to the cumulativeeffects of the concussions, as clinical symptoms and the timeelapsed since the last concussion could also explain part ofthe results. First, it was reported that the three-or-more-concussions group had significantly more clinical symptomsthan the non-concussion group, while nothing is mentionedabout the possibility of clinical symptoms in the one- and two-concussions groups. Second, we do not know whether thetime elapsed since the last concussion was comparable amongthe three injured groups. The authors only indicate that allparticipants were tested at least 6 months post-injury, andthat the average post-injury period for the three-or-more-concussions group was 13.2 months.

A second study of the cumulative effects of concussions onERPs controlled for the effect of symptomatology by includ-ing only concussed athletes who where asymptomatic (DeBeaumont et al., 2007). Specifically, a group of asymptomaticathletes who suffered one concussion, a second group ofasymptomatic athletes who experienced two or more con-cussions, and a third group who never experienced a con-cussion were tested with a modified visual oddball paradigmcombined with a visual search task. The P3 component wassignificantly reduced for the multiple-concussion group com-

pared to the single-concussion and non-concussed groups.However, this result could be explained at least in part by theimportant difference in the mean time elapsed between thelast concussion and the testing, which was nearly twice aslong for the single-concussed group than for the multiple-concussed group. In fact, no correlation between the reduc-tion in P3 amplitude and the number of concussions wasfound, while there was a nearly significant correlation be-tween time since the last concussion and the attenuation of theP3 component.

Post-concussion recovery

Although ERP studies provide evidence of neurofunctionaldeficits that persist at least up to 3 years post-concussion inasymptomatic athletes that suffered from multiple concus-sions (Broglio et al., 2009), no study has compared the acuteand post-acute periods. The only ERP study to investigate theeffect of the passage of time since injury is a single case reportof an 8-year-old girl (Boutin et al., 2008). Specifically, thelongitudinal assessment of the athlete, who suffered a con-cussion playing soccer, revealed neuropsychological impair-ments associated with attention at 24 h post-injury thatresolved within 22 weeks. In contrast, visual evoked poten-tials and quantitative EEGs recorded 7 weeks pre-injury, andat 24 h and 7, 22, 32, and 55 weeks post-injury confirmed thepresence of cortical impairments up to 1 year post-injury.

The results from the spectral analysis of quantitative EEGsindicated an important increase in delta power and a reduc-tion in beta and gamma power at 24 h post-injury. The greaterdelta activity suggests a reduction in the level of arousal im-mediately after the concussion, which resolves within 22weeks. In contrast, the reduction in beta and gamma activitythat persisted at 1 year after the concussion suggests that thecortical mechanisms underlying attention and informationprocessing were impaired in this 8-year-old girl. These resultsare consistent with those of Gosselin and associates (2009),who reported an increase in delta and a reduction in alphapower in a group of concussed athletes who had other-wise normal results on a computerized neuropsychologicalbattery.

Taken together, the literature indicates that ERPs are ahighly sensitive measure of subtle neurofunctional deficits notdetectable by other behavioral methods. It is a non-invasivetechnique present in most clinical settings that can be rapidlyadministered. Some protocols can be completed in as little as15–20 min. Another advantage of this measure is that it is notinfluenced by internal factors (i.e., downplaying or minimiz-ing cognitive symptoms in order to remain in the game). It isalso less affected by motivation and practice than paper-and-pencil or computerized neuropsychological tests.

Further research is needed to identify the most sensitiveERP paradigm and to create a standardized procedure forclinical testing. Different behavioral tasks have been associ-ated with the online measurement of EEGs to study sports-related concussion. Specifically, a visual search paradigm (DeBeaumont et al., 2007), a visual stimulus paring paradigm(Gaetz et al., 2000), visual oddball paradigms of varying dif-ficulty (Broglio et al., 2009; Dupuis et al., 2000; Gaetz et al.,2000; Lavoie et al., 2004), and a difficult auditory oddballparadigm (Gosselin et al., 2006) have all been used. Despiteimportant differences in the subject characteristics among the


different studies, there is evidence that tasks with the highestcognitive load are most sensitive to the effects of sport-relatedconcussion. Of the four tasks used to assess asymptomaticathletes, the two with the highest level of difficulty founddeficits in these athletes (Broglio et al., 2009; Gosselin et al.,2006), while those with the easier tasks did not detect anyproblems (Dupuis et al., 2000; Lavoie et al., 2004).

Future studies will also need to investigate recovery fromsport-related concussion by obtaining a pre-season baselineand repeat measurements up to several years post-injury.Although ERPs are not as perturbed by practice effects as areneuropsychological tests, ERP amplitude is known to be re-duced by repeated experience with the same task (Guillaumeet al., 2009; Prinzel et al., 2003; Sambeth et al., 2004). The mainadvantage of the spectral analysis of EEG activity for studyingrecovery after a sport-related concussion is that because it isnot paired with a cognitive task, it is not affected by thepractice effects associated with repeated testing. This proce-dure, which takes as little as 2 min, can easily be added to theERP paradigm.

Neuroimaging Techniques

Neuroimaging represents a unique means of discoveringthe pathophysiological mechanisms and biomarkers thatcharacterize sport concussion. To date, however, the contri-bution of neuroimaging to the understanding of sports con-cussion are inconsistent, owing mostly to rapid changes inimaging technology, heterogenous research populations, anda lack of information about the acute post-concussion phase.The following section details the major imaging techniquesused in clinical and research practice and their contributionsto understanding sport concussion.

Anatomical imaging

Computed tomography (CT) and magnetic resonance im-aging (MRI) can provide information about anatomical andgross structural changes following a concussion. CT is anx-ray-dependent technique that constructs a 3-D image ofthe brain. Clinically, CT scans can reveal brain lesions, con-tusions, fractures, and intracranial hemorrhaging. They arewidely used in the management of closed-head injuries, par-ticularly within the first 24 h post-injury, though it is generallyonly specified in cases for which there has been LOC (Li-vingston et al., 2000; Stein and Ross, 1992; Warren and Bailes,1998), or persistent symptomatology (Rimal et al., 2007).

Research on the utility of CT in sports concussion man-agement is limited, as the only studies available focus onboxers. Though there are instances where lesions are detected,the majority of concussed athletes have negative CT findingswith weak predictable outcome validity ( Jordan et al., 1992;Jordan and Zimmerman, 1988; Ross et al., 1987). The lack ofconsistent CT findings is quite common in the concussionliterature as well (Gentry et al., 1988; Groswasser et al., 1987;Han et al., 1984; Newton et al., 1992; Zimmerman et al., 1986).A large study investigating the prevalence of lesions in con-cussion found that approximately only 16% of scans arepositive (Iverson et al., 2000); moreover, patients with positivescans share some common characteristics, chief among thembeing the presence of intracranial abnormalities, LOC, skullfractures, and lower Glasgow Coma Scale (GCS) and Gal-veston Orientation and Amnesia Test scores. Though they are

still used in clinical and emergency settings because of theirrelative cost effectiveness and wide availability (Toga andMazziotta, 2002), CT scans have fallen out of favor, particu-larly in research, because of their limited ability to detect finitelesions and contusions, especially relative to MRI ( Jordan andZimmerman, 1990; Newton et al., 1992; Snow et al., 1986).

MRI is a more sensitive technique for investigating ana-tomical changes due to its higher resolution, its capacity toimage different planes, and because it provides better dis-tinction between tissue types: gray matter, white matter, andcerebrospinal fluid. Typical injuries detected by MRI resultingfrom sport concussion include small cortical contusions orsubdural hematomas, and small white matter hemorrhages(Toga and Mazziotta, 2002), that are generally interpreted tobe reflective of diffuse axonal injury (DAI) (Bazarian et al.,2006). Though more effective at detecting abnormalities thanCT ( Jordan and Zimmerman, 1990; Newton et al., 1992), MRIhas proven inconsistent with only moderate predictive va-lidity in sports concussion ( Jordan and Zimmerman, 1990;Newton et al., 1992), and concussion in general (Barr, 2005;Bazarian et al., 2006; Toga and Mazziotta, 2002). Though itsresolution is vastly improved over CT, MRI is still not able todetect lesions in all concussed athletes ( Jordan et al., 1992;Jordan and Zimmerman, 1990), limiting its clinical applica-bility. Moreover, CT and MRI are unable to provide infor-mation about functional alterations in brain function resultingfrom sports concussion.

Diffusion tensor imaging (DTI) exploits differences inwater movement through grey and white matter to create animage of the white matter neural pathways and their direc-tionality. DTI’s main utility in neurology is detecting thepresence of axonal injury (Toga and Mazziotta, 2002). There isincreasing evidence to suggest that DAI is present in TBI andthat the extent of the damage is related to the severity of theinjury as defined by initial GCS score (Huisman et al., 2004).Similarly, Kraus and associates (2007) investigated TBI acrossthe severity spectrum using DTI and found the degree of DAIto be related to the severity of the injury, with severe TBIpatients exhibiting the greatest extent of damage. One of thefew studies to focus on concussion found changes in whitematter in the corpus callosum up to 5 years post-injury (Ing-lese et al., 2005). While it is important to note the persistence ofinjury after such a long period of time, there are very fewstudies documenting DAI in the acute post-injury phase inconcussion; however, studies suggest that damage can bedetected within the first week of injury (Miles et al., 2008;Wilde et al., 2008). Understanding DAI in the early phase iscrucial to our understanding of how white matter changesover time after a concussion and could provide insight intorehabilitation and recovery.

Functional imaging

Functional MRI (fMRI) relies on the same principles asMRI, though instead of providing an anatomical picturebased on hydrogen protons, it takes advantage of the mag-netic properties of hemoglobin. While fMRI can track bloodperfusion, the more common paradigm tracks blood oxy-genation changes, for which the blood oxygenation level-dependent (BOLD) signal is detected (Toga and Mazziotta,2002). It is assumed that increased blood flow to a given brainarea is related to the cognitive processing inherent to the task


and the subsequent increased metabolic demand. Followinginjury, decreases in blood flow are therefore speculated torepresent an impaired functional capacity.

Few studies have specifically targeted sports concussionusing fMRI, but each reports dysfunction in concussed ath-letes (Chen et al., 2007, 2004, 2008b; Jantzen et al., 2004; Lovellet al., 2007). Chen and colleagues (2007, 2004, 2008b) reportedfunctional deficits in working memory in concussed athletesthat manifest as reduced activation in the dorsolateral pre-frontal cortex, while Jantzen and colleagues (2004) noted anatypical BOLD response on a finger-tapping sequence in pa-rietal and lateral frontal cortical areas. Furthermore, Chen andassociates (2007, 2004, 2008b) found that the detectability ofan atypical BOLD signal is directly related to the symptom-atology experienced by the athlete. Though useful in under-standing persistent symptomatology and its covariates(athletes were tested 1–14 months post-concussion), the focusof the studies by Chen and colleagues did not address theacute phase during which deficits, transient though they maybe, are most commonly seen in concussed athletes. Lovell andcolleagues (2007) scanned concussed athletes in the acutepost-concussion phase (1 week post-concussion), and ap-proximately 1 month after injury. Briefly, athletes who dis-played hyperactivation on a cognitive task in the acute phasehad prolonged recovery times relative to those athletes whodemonstrated typical activation in the acute phase. The im-plication of the findings from Lovell and associates (2007), inconcert with those of Chen and colleagues (2007, 2004, 2008b),is that atypical activation in the acute phase is related to re-covery time. Though small in scope, the limited fMRI findingsin sports concussion are in agreement with those of the otherconcussion literature (McAllister et al., 1999, 2001a, 2001b),underscoring the link between symptomatology and corre-sponding changes in functional brain activation.

Positron emission tomography (PET) constructs a highlysensitive functional 3-D image of the brain from the emissionsof a radio isotope and can directly detect blood flow as well asglucose and oxygen metabolism in the brain. The majority ofPET studies have focused on non-sports-related concussionpatients with persistent symptomatology, and found thatfrontotemporal areas are the most consistently impaired re-gions (Chen et al., 2003; Gross et al., 1996; Ruff et al., 1994;Umile et al., 2002; Varney et al., 2001). Unfortunately, all ofthese studies were conducted with patients well after theacute injury phase. PET appears to offer reasonable correla-tion with neuropsychological deficits, but it is difficult to ex-trapolate these findings to what is seen in the acute phase insports concussion. Those people who remain diagnosticallysymptomatic well after suffering an concussion represent avery small portion of the population (3–5%) (McCrea, 2008),and as such may not be the best group upon whom to baseconclusions. To our knowledge there have been no PETstudies that have focused on sports concussion. This generalabsence of data makes it difficult to assess the efficacy ofPET in concussion diagnosis and management in general,let alone how it pertains to sports concussion research inparticular.

Metabolic imaging

Single-photon emission computed tomography (SPECT)provides information about changes in cerebral blood perfu-

sion following a concussion. SPECT works similarly to PET, asan intravenously injected radioactive ligand accumulates indifferent brain areas in proportion to the delivery of nutrientsto provide an overall picture of regional cerebral blood flow(rCBF) (Toga and Mazziotta, 2002). With respect to concus-sion, changes in rCBF are moderately correlated with clinicaloutcome (Bonne et al., 2003; Hofman et al., 2001; Umile et al.,1998), but many of the SPECT studies suffer from the samelimitations as the PET research. Most of the studies are carriedout in patients with persistent symptomatology at varioustime points after injury, with a wide range in cause of injury.Despite the variability in participant populations, mostSPECT studies find focal hypoperfusion in frontal and tem-poral cortical areas, as well as in thalamic-basal ganglia areas(Abdel-Dayem et al., 1998, 2000, 1999; Bergsneider et al., 1997;Bonne et al., 2003; Korn et al., 2005; Umile et al., 1998).

Magnetic resonance spectroscopy (MRS) images the che-mical composition of living tissue. Several compounds can beimaged with MRS, chief among them being creatine, a generalenergy marker; choline, a marker of neuronal damage andmembrane turnover; and N-acetyl aspartate (NAA), a markerof neuronal integrity. MRS is thus able to detect neuronaldamage and changes in the chemical make-up of neurons. It isparticularly useful in corroborating evidence of DAI as de-tected using DTI, because damage-related changes to neuronsare manifest not only in their physical structure, but also intheir composition (Toga and Mazziotta, 2002). In the only twosports-concussion studies, a decrease in NAA was reported,suggesting that there is indeed structural damage in sportsconcussions despite the negative findings of more traditionalimaging techniques (Cimatti, 2006; Vagnozzi et al., 2008).Studies outside of the sports literature have also demon-strated abnormalities in individuals with concussion withotherwise normal-appearing MR scans (Babikian et al., 2006;Govindaraju et al., 2004; Holshouser et al., 2006; Kirov et al.,2007; Shutter et al., 2006). Significantly depressed concentra-tions of NAA have been measured in concussion despitenormal findings on conventional MRI (Cecil et al., 1998;Garnett et al., 2000b), with the greatest reductions seen ininjury-prone brain tissues, which typically include frontalareas and grey-white matter junctions. In contrast, levels ofmyo-inositol were shown to be augmented in concussion(Garnett et al., 2000a). This provides yet another indication ofcellular injury, as higher concentrations of this intracellularcompound are associated with glial proliferation (Friedmanet al., 1998). Though the MRS research is burgeoning andencouraging, more studies in which sports concussion is thefocus must be conducted before any conclusions can be maderegarding the athlete population.

In summary, though neuroimaging has grown in impor-tance in understanding sports concussion, there are certainlymore questions than answers at this point. This knowledgegap should not be seen as a weakness of the tools, but rather atestament to the difficulties associated with understandingsports concussion and its sequelae. Questions that lie beyondthe anatomical and rest at a cellular level are crucial to ourunderstanding of sports concussions, and as neuroimaging’sprecision improves, those questions will be elucidated. In-deed, even as CT and MRI do not detect anatomical changes,other functional techniques including fMRI, PET, and SPECT,are yielding modest results, whereas newer techniques likeDTI and MRS have yet to display their full potential in aiding


our understanding of the changes in the concussed athlete’sbrain.

Discussion

There is no dispute that sport-related concussion has im-mediate consequences for brain function. In the hours anddays following injury, concussed athletes have marked dec-rements in certain aspects of cognitive functioning and pos-tural stability, and they report associated symptoms ofheadache, dizziness, and confusion. Most studies suggest thatathletes return to normal within 1–2 weeks post-injury, asperformance on neuropsychological tests returns to baselinewithin 5–10 days (Lovell et al., 2004b; Sim et al., 2008), deficitsin postural stability resolve within 3–5 days (Guskiewicz,2001), and symptoms dissipate within 3–10 days (Broglioet al., 2007b; Collie et al., 2006; Macciocchi et al., 2001). Incontrast, recent evidence from brain imaging studies showsabnormalities in the electrical responses (Gaetz et al., 2000;Gosselin et al., 2006), metabolic balance (Cimatti, 2006; Vag-nozzi et al., 2008), and oxygen consumption (Chen et al., 2004;Jantzen et al., 2004) of neurons that persist for several monthsafter the injury. These results are not all that surprising, con-sidering the evidence found of persisting neuropsychologicaldeficits for high-level executive functions in athletes withoutprior experience with cognitive testing (Downs and Abwen-der, 2002; Ellemberg et al., 2007), and given the evidence ofcognitive impairment in retired professional athletes with ahistory of sport concussion (Guskiewicz et al., 2005, 2007a).

There are possibly two explanations for the discrepancyregarding the findings of post-concussion recovery. As notedpreviously, the sensitivity of neuropsychological tests is likelyreduced by repeated testing within a short period of time(Bleiberg et al., 2004). It is also possible that the pressure as-sociated with athletic performance motivates some individ-uals to minimize their symptoms or altogether deny theirpresence (McCrea et al., 2004). Including an objective measureof postural stability increases the sensitivity of the return-to-play decision-making process, and minimizes the consequencesof mitigating factors (e.g., practice effects and motivation) onneuropsychological test results. This is consistent with find-ings indicating that symptom severity, cognitive function,and postural stability do not appear to be related or affected tothe same degree after a concussion (Broglio et al., 2007c; Rosset al., 2000). A second possibility, although more speculative,is that recovery takes place in two phases. First, a rapidfunctional recovery occurs, in which compensatory mecha-nisms such as the adoption of new strategies and=or func-tional reorganization via brain plasticity allows the athlete toperform normally on standard clinical assessments. Thiscould be followed by a more prolonged neuronal recoveryperiod, during which subtle deficits in cognitive functioningare present, but are not apparent using standard clinicalconcussion assessment tools.

Athletic trainers and other clinicians need readily accessi-ble, inexpensive, and rapidly administered tests to allow themto make return-to-play decisions that are sensitive enough toprotect both the short- and long-term health of the athlete.However, the various assessment tools presented in this ar-ticle are certainly complementary, as each contributes a dif-ferent piece of the concussion assessment puzzle. Symptomreporting should first be privileged. Although computerized

neuropsychological tests have been especially designed formultiple testing during the acute post-concussive phase, it isadvantageous to preserve their sensitivity by using themparsimoniously, when other measures are no longer infor-mative. As noted earlier, symptoms like headache, hypo-somnia, and depression, which are known to be associatedwith concussion, can disrupt cognitive performance (Chenet al., 2008a; Guskiewicz et al., 2007b; Hunt et al., 2007). If nosymptoms are reported, or when they are no longer reported,athletic trainers and clinicians could turn to the assessment ofpostural stability using the BESS. The computerized neu-ropsychological assessment should be considered only whenathletes do not report symptoms at rest and under stress, andwhen they have normal results on the BESS (Guskiewicz et al.,2004a). When used in combination, symptom assessment,balance assessment, and neuropsychological testing provide asensitivity of over 90% for the identification of concussion(Broglio et al., 2007c).

Although there are currently several published sets ofreturn-to-play guidelines, none has been validated, and notall are supported by clinical assessment data (McCrory et al.,2005a). Furthermore, there are no guidelines or recommen-dations regarding when an athlete should retire from sports.It should also be noted that no universal diagnostic or return-to-play protocol can be applied to all athletes or under allcircumstances. For instance, recent work suggests that im-mediate outcome is worse and recovery longer followingconcussion in younger athletes (Boutin et al., 2008; Lovellet al., 2003), and in female compared to male athletes (Brosheket al., 2005; Covassin et al., 2007; Ellemberg et al., 2007). Also,although more research is required, it appears likely that thenature of the biomechanical forces exerted during impact in-fluences the severity of the concussion (Ommaya and Gen-narelli, 1974; Pellman et al., 2003). Factors like diet, exercise,metabolic dysfunction, and individual characteristics alsoappear to influence recovery (Fox et al., 2008; Makdissi et al.,2009; Slobounov et al., 2007; Vagnozzi et al., 2008). To datemost of the concussion work has focused on adult athletes,and more research is required to determine factors and pop-ulation characteristics that influence concussion severity andrecovery, as well as the sensitivity of the assessment protocoland return-to-play guidelines.

Although tremendous strides have been made in concus-sion assessment in the last two decades, there remain manyquestions left unanswered. Future research efforts usingmetabolic and functional brain imaging, as well as humanelectrophysiology, are needed to clarify the time course ofacute functional recovery and of neuronal recovery. Futureresearch using these measures should also be done underconditions of cognitive (e.g., dual-task performance) orphysical effort. The consequences of multiple concussions andthe effect of timing between subsequent concussions also needto be documented. Furthermore, it will be important to verifyif there is a relationship between changes in functional neu-rochemistry and neuroelectric responses, and symptom re-porting, postural stability, and cognitive function in theimmediate post-concussion phase. Brain imaging could alsobe used to compare the effectiveness of various return-to-playprotocols. Finally, a better understanding of the neurophysi-ological and neurometabolic changes associated with sportconcussion and their mechanisms of recovery could eventu-ally guide research on potential pharmacological treatments.


Author Disclosure Statement

No conflicting financial interests exist.

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Address correspondence to:Dave Ellemberg, Ph.D.University of Montreal

Department of Kinesiology2100 Edouard Montpetit

Montreal, Quebec H3T 1J4

E-mail: [email protected]


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