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Clinical Neurology and Neurosurgery 122 (2014) 59–63

Contents lists available at ScienceDirect

Clinical Neurology and Neurosurgery

jo ur nal home p age: www.elsev ier .com/ locate /c l ineuro

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review of modifying factors affecting usage of diagnostic ratingcales in concussion management

lexa Dessya,∗, Jonathan Rasouli a, Alex Gometzb, Tanvir Choudhria

Ichan School of Medicine at Mount Sinai, Department of Neurosurgery, New York, USAConcussion Management of New York, New York, USA

r t i c l e i n f o

rticle history:eceived 17 January 2014eceived in revised form 25 March 2014ccepted 9 April 2014vailable online 24 April 2014

a b s t r a c t

Sport-related concussion has gained increasing recognition as a result of recent legislation, public healthinitiatives and media coverage. Moreover, there have been substantial paradigm shifts in the managementof concussion. This article will discuss the variables that affect the use of diagnostic rating scales suchas ImPACT and SCAT in the current management of concussed individuals. Specifically, patient-specificmodifying factors affecting test interpretation, including age, gender, fitness level, psychiatric conditions,

eywords:ports-related concussioneturn-to-playild traumatic brain injury

thletes

learning disorders and other components of medical history will be addressed, as well as methodologicalconcerns with baseline testing.

Published by Elsevier B.V.

eurocognitive testing

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 602. Concussion management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 603. Test interpretation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 604. Patient-specific modifying factors affecting test interpretation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60

4.1. Age . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 604.2. Gender. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 604.3. Test setting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 614.4. Fitness level . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 614.5. Sport specific factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 614.6. Psychiatric conditions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 614.7. Learning disability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 614.8. Medical history . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61

5. Baseline testing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

∗ Corresponding author at: Department of Neurosurgery, The Mount Sinai Medical CenteSA. Tel.: +1 212 241 3313; fax: +1 212 241 9285.

E-mail address: Alexa.dessy@mountsinai.org (A. Dessy).

ttp://dx.doi.org/10.1016/j.clineuro.2014.04.003303-8467/Published by Elsevier B.V.

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. Introduction

Growing recognition of sports-related concussion throughecent legislation, public health initiatives and media coverageas resulted in a national increase in the number of concussionsvaluated in the past decade. Reports have suggested that the com-ination of these factors has led to a 5-fold increase in the numberf youth-athletes presenting for concussion at medical centers [1].mportantly, as many as 3.8 million concussions occur in the U.S.ach year during competitive sports and recreational activities [2].oreover, these values are likely underestimates, according to evi-

ence that suggests that as many as 50% of concussions may gonreported [2]. Given the mounting number of concussive injurieseceiving medical attention, the importance of effective diagnosticnd management strategies cannot be underestimated.

Consequently, the medical community faces the challenge ofeveloping guidelines, care systems and tools to evaluate athletesfficiently, follow outcomes, and understand the potential long-erm effects of concussion and repetitive head injury. These issuesave been addressed in numerous ways by respective institutionsnd disciplines, resulting in significant variation in the care andanagement of athletes with concussion. Moreover, there have

een substantial paradigm shifts in the management of concus-ion, which is moving toward an individualized, patient-centeredethod for assessment and treatment [1,3]. Physicians attending to

oncussed patients should be familiar with the myriad of changes touidelines and other current research. Furthermore, consistent andffective administration of tests and supervision of return-to-playay have significant benefits, such as prevention of repeat injury

nd reduction of institutional resource utilization [1]. This articleill elucidate the considerations that should be taken into accounthen managing concussed individuals and utilizing the currently

vailable evaluation tools, including the testing modality, patientistory and other methodological concerns.

. Concussion management

Concussion is defined by the 2012 Zurich Consensus State-ent on Concussion in Sport as “a complex pathophysiological

rocess affecting the brain, induced by biomechanical forces” [4].oncussion results in rapid onset of short-lived impairment ofeurologic function that typically resolves within 7–10 days fol-

owing injury, though certain factors, such as age, gender and prioristory of concussion, may prolong recovery. The foundation ofoncussion management involves physical and cognitive rest untilcute symptoms resolve [4,5]. Though concussive symptoms typi-ally resolve within one week of injury, return-to-play should note considered unless the athlete is completely asymptomatic [6].oreover, return-to-play should not be endorsed unless the ath-

ete has returned to baseline or normative values on neurocognitivend balance testing [7]. Once asymptomatic, a graded program ofctivity is implemented before medical clearance and return-to-lay is granted [4]. Currently, there is no evidence for an effective

ntervention to increase the rate of recovery of concussion [6].urthermore, no randomized, controlled clinical trials have beenonducted to examine the effects of rest versus exercise, or otherpecific intervention [5].

. Test interpretation

Currently, there is overwhelming evidence that assessment

nd management of sport-related concussion should involve aultifaceted approach. Indeed, the consequences of concussion,

ncluding symptom severity, changes in neuropsychological func-ion and postural instability often appear to be unrelated and

Neurosurgery 122 (2014) 59–63

are affected to different degrees after injury [8]. Therefore, theevaluation should include a clinical exam, self-reported symp-tom checklist, postural assessment and neurocognitive testing[9–11]. In particular, evaluation of cognitive functioning shouldinclude intellectual functioning, academic skills, attention and con-centration, processing speed and learning, memory, psychomotorfunction and emotional functioning [12]. To facilitate objectiveand comprehensive evaluation of concussed individuals, the mostcommonly used assessment tools include the PCSS, SAC, SCAT2and ImPACT [5]. However, the sensitivity, specificity, validityand reliability of these standardized tests remain largely unde-fined, particularly among different age groups, cultural groupsand settings. Moreover, no single test has demonstrated sufficientsensitivity to warrant standalone use, though the combination ofmultiple assessment tools may increase sensitivity and specificityof diagnosis [2,13]. Therefore, the sports-medicine practitionermust not rely on any one tool in managing concussion, and mustbe aware of the advantages and drawbacks of whichever methodis incorporated into the evaluation and management plan [11].These considerations are of critical importance for reducing therisk of additional injury [13]. Additionally, test interpreters mustrecognize that the reliable change difference scores serve as a sup-plement, rather than a substitute to clinical expertise in this area[14].

4. Patient-specific modifying factors affecting testinterpretation

Due to the complexity of brain function, concussion is a highlyindividualized injury, with significant variability in the type andseverity of concussion presentations in the acute setting [6,14,15].The specific symptoms reported by patients are modulated to somedegree by the particular regions of the brain affected, as well as thesocial, educational, occupational and medical histories of the indi-vidual [12,16]. In fact, numerous factors have been identified thatmodify the risk of sustaining a concussion or alter the progression ofrecovery. Such factors include history of prior concussion, impactlocation and magnitude, severity or duration of symptoms afterconcussion, age, gender, genetic predisposition, history of learn-ing disorder, Attention Deficit Disorder (ADD), migraines, mooddisorder, fitness, and engaging in sports positions that could poten-tially involve repeated head trauma (boxer, lineman, hockey, etc.)[8,11,17–19].

4.1. Age

Age has been proposed as the most important factor in recoverytime [8]. Evidence indicates that children appear to be more sus-ceptible to concussion from the same amount of force than adultsand that they require a longer recovery period [6]. Prolonged recov-ery on verbal memory, visual memory and reaction time has beenobserved among younger concussed athletes compared to olderconcussed athletes [7]. Specifically, athletes aged 13–16 take longerto return to their neurocognitive and symptom baseline than ath-letes aged 18–22 years [20]. Similarly, Valovich McLeod et al. foundthat 9th graders scored significantly lower on SCAT2 total scorethan 11th and 12th graders [21]. The development of Child SCAT3and the Pediatric ImPACT test reflects the growing recognition ofthis elevated risk among young athletes and the specific needs ofthis population.

4.2. Gender

Studies have suggested that the incidence of concussion ishigher in male athletes compared to female athletes [5]. This may beattributed to greater male participation in sports in which there is

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nherently a higher risk of concussion, such as football or ice hockey5]. In addition to the higher incidence of sports-related concus-ions, male athletes were also found to score significantly lowerhan their female counterparts on a number of baseline measures,ncluding balance, immediate memory, concentration scores andhe total SCAT2 score [11,21,22]. Therefore, gender may need to beonsidered in the interpretation of post-concussion test results andn the use of normative data as comparison.

Interestingly, despite the greater incidence of concussions inale athletes, several studies have suggested that female athletes

xperience worse outcomes than males after concussive injury5,8]. In particular, female concussed athletes were found to be

ore cognitively impaired and have more concussion symptomshan male concussed athletes [35]. However, this discrepancy

ay be the result of greater willingness among females to reportymptoms than males [8]. Indeed, women frequently report moreomatic symptoms than men, such as headache, fatigue and dizzi-ess [5,8,35]. In addition, several factors specific to women haveeen investigated [24]. Specifically, in a sample of 36 healthyollege-aged females, no effect of menstrual cycle phase on con-ussion symptom scores was found [11]. Additionally, fewerymptoms were reported by oral contraceptive users than eumen-rrheic females, both in terms of total symptom severity score andumber of symptoms endorsed [11]. These considerations high-

ight the importance of understanding the individual factors thatay affect concussion assessment and test interpretation.

.3. Test setting

The sport setting contributes certain challenges to test admin-stration and interpretation. For example, when the symptom scales being completed after exercise, evaluation must be completed

hile the athlete is in the resting state, at least 10 min post-exercise,o mitigate the effects of fatigue on symptom reporting [4]. In addi-ion, test administrators must be aware that athletes are often lessilling to report symptoms when there is external pressure or a

trong desire to return-to-play [8]. Therefore, the test should bedministered in an area removed from the sideline and away fromoaches, teammates and parents, if possible.

In addition, Mihalik et al. observed that subjects with lowleep quantity the night before baseline reported a greater num-er of symptoms and higher total symptom severity score [25].eanwhile, no clinically significant effects for sleep quality were

bserved. The authors conclude that sleep deprived athletes repor-ing for baseline testing should be rescheduled for testing after

normal night’s sleep [25]. Additionally, Giza et al. observedhat athlete-specific characteristics, including body mass index ofreater than 27 kg/m2 and training time less than 3 h weekly, likelyncreases the risk of concussion [24].

.4. Fitness level

Fitness level also appears to influence athlete performance ononcussion assessments. Mrazik et al. evaluated the effect of phys-cal fitness on self-report of baseline concussion symptoms inollegiate athletes and students and found that fitness accountedor a significant amount of variance in SCAT2 symptoms at base-ine [17]. Indeed, fitter individuals reported fewer symptoms athree time intervals. In addition, exercise seemed to induce con-ussion symptom reporting [17]. Similarly, in a study in which

0 healthy participants engaged in 15 min bursts exercise, symp-oms increased significantly after intense exercise and somewhatncreased after moderate intensity exercise [11]. These results high-ight the importance of timing and setting when administering

Neurosurgery 122 (2014) 59–63 61

concussion assessments and confirm the need for the athlete toreturn to resting state prior to testing.

4.5. Sport specific factors

The risk of concussive injury may also vary by sport setting. Forexample, the risk of concussion appears to be greatest in Americanfootball and Australian rugby, while the risk is lowest in baseball,softball, volleyball and gymnastics [24]. Similarly, an athlete’s par-ticular position may affect their risk of concussion. In Americanfootball, it has been suggested that linebackers, offensive linemenand defensive backs are at greater risk of concussion than receivers[24]. Quarterbacks appear to be more vulnerable to recurrent con-cussion and are more likely to have a prolonged period beforereturn-to-play [24]. In soccer, it has been reported that goalkeep-ers sustain significantly more concussions than forwards [36]. Thus,the sport and position may need to be considered in the interpre-tation of baseline and post-concussion test results.

4.6. Psychiatric conditions

Psychiatric conditions may play an important role in the con-cussion management process. In a study by Bailey et al., theauthors obtained several significant correlations of moderate tolarge effect between baseline neurocognitive performance and anx-iety, depression, substance abuse and suicidal ideation [26]. Asubstantial portion of the athlete participants endorsed symptomsof psychological distress, and the results suggest that psychologicaldistress has a moderate to large effect on baseline concussion test-ing, diminishing performance among individuals experiencing suchdistress. Indeed, participants with suicidal ideation showed signif-icantly slower simple reaction time and complex reaction time onthe CRI, with a similar trend of processing speed [26]. These resultsunderscore the importance of screening for psychological distressduring baseline and post-injury concussion evaluations.

4.7. Learning disability

Similarly, recent investigations are now examining existingdiagnosis learning disabilities as risk factors for concussion [5].Individuals with learning disorders may exhibit common symp-toms of concussion prior to injury, such as difficulty in learning,concentration, attention and memory. Therefore, such traits maybe exacerbated following concussion (Borich et al. [5]). Up to16% of children in the U.S. between the ages of 3 and 17 haveeither Attention Deficit Spectrum Disorder or a learning disabil-ity [27]. Zuckerman et al. observed that participants with attentiondeficit hyperactivity disorder (ADHD) administered the ImPACTassessment battery had significantly lower verbal memory, visualmemory, visual motor processing speed scores, along with signif-icantly higher reaction time, impulse control and symptom scorescompared without learning disorders or ADHD [27]. Participantswith learning disorders had similar results to those with ADHD, butdid not differ in their impulse control score compared to those with-out learning disorders or ADHD. These authors provide preliminarynormative neurocognitive data for these special populations [27].Similarly, Maerlender et al. found that increased symptoms of cur-rent anxiety were associated with poorer scores on the processingspeed composite of the ImPACT battery [28].

4.8. Medical history

Evidently, the medical history of the patient is an essential fac-tor that must be considered in the management of concussion.Concussion history is of critical importance. Indeed, it has beenobserved that those who have sustained multiple concussions are

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t increased risk for long term cognitive impairment and have areater probability of suffering a subsequent concussion [5]. In atudy conducted by Meehan et al., 30.5% of patients diagnosedith sports-related concussion reported previously undiagnosed

oncussions [29]. These patients were more likely to have lost con-ciousness with their current injury and had a higher mean PCSScore than patients without previously undiagnosed concussions29]. In addition, history of migraines may be relevant in evaluatingoncussed individuals. Indeed, studies have shown that concussedndividuals with post-traumatic migraine require prolonged recov-ry compared to those who do not experience headaches after thenjury [30]. However, the causal relationship between migrainesnd concussions has not yet been established.

. Baseline testing

The principal paradigm for management of sports-related con-ussion includes acquisition of pre-injury or baseline performanceevel for comparison in the event of later concussive injury [12].iven that individuals exhibit a range of cognitive performance

n attention, memory, concentration, information processing andeaction time, baseline neurocognitive testing is purported torovide the most accurate representation of an athlete’s pre-injuryognitive status [9]. Knowledge of an individual’s baseline perfor-ance allows detection of relative deficits, and reduces potential

alse positive errors and the risk of misdiagnosis [29,31,32]. Inact, it has been reported that baseline neurocognitive testing hasesulted in an increased detection of post-concussion neurocogni-ive impairments [9].

However, concerns regarding the psychometric and method-logical properties of current test approaches have called intouestion the effectiveness of the baseline model [2,12]. Whilere-injury baselines help to reduce the error due to individualifferences, they also introduce additional complexity in the inter-retation of test data because of measurement error associatedith a second test administration [18]. Moreover, it has been

uggested that administering baseline neurocognitive testing tothletes in a group setting in their school, rather than individu-lly in a private neurological clinic, may introduce error whicheakens test performance [33]. Preseason testing also functionsnder the assumption that the athlete has made an honest effort2]. Moreover, baseline evaluations on one measure should not besed as the basis for post-concussion assessment using anothereasure. Indeed, Schatz and Putz (2006) revealed modest corre-

ations between ImPACT and CogSport (0.65) and between ImPACTnd HeadMinder (0.41), and no correlation between CogSport andeadMinder [34].

Valovich McLeod et al. examined baseline performance onCAT2 and observed variability among healthy adolescents, indi-ating that the assumption of a perfect baseline score of 100 is notppropriate in the adolescent athlete population [21]. Similarly, Jin-ui et al. found the average SCAT2 score for high school athletes toe 89 of a possible 100, with a standard deviation of 6 units [22].n general, non-concussed high school athletes score near the totalossible in most domains of SCAT2, with the exception of concen-ration testing and balance testing [22].

. Conclusions

The vast and increasing number of individuals presenting withoncussion has created a growing need for effective and efficient

iagnostic and management strategies. There are many clinical andon-clinical factors that must be considered in the evaluation ofoncussion. Greater understanding and integration of these con-iderations into medical practice will likely improve patient care

[

Neurosurgery 122 (2014) 59–63

and prevent premature return-to-play, and repeat injuries that mayoccur as a consequence.

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