Are Divided Attention Tasks Useful in the Assessment and Management of Sport-Related Concussion?

REVIEW

Are Divided Attention Tasks Useful in the Assessment

and Management of Sport-Related Concussion?

Johna K. Register-Mihalik&Ashley C. Littleton& Kevin M. Guskiewicz

Received: 20 September 2013 / Accepted: 4 November 2013 / Published online: 17 November 2013 # Springer Science+Business Media New York 2013

Abstract This article is a systematic review of the liter-ature on divided attention assessment inclusive of a cog-nitive and motor task (balance or gait) for use in con-cussion management. The systematic review drew from published papers listed in PubMed, MEDLINE, EMBASE and CINAHL databases. The search identified 19 empirical research papers meeting the inclusion criteria. Study results were considered for the psycho-metric properties of the paradigms, the influence of di-vided attention on measures of cognition and postural control and the comparison of divided attention task outcomes between individuals with concussion and healthy controls (all samples were age 17 years or older). The review highlights that the reliability of the tasks under a divided attention paradigm presented ranges from low to high (ICC: 0.1–0.9); however, only 3/19 articles included psychometric information. Response times are greater, gait strategies are less efficient, and postural control deficits are greater in concussed partici-pants compared with healthy controls both immediately and for some period following concussive injury, specif-ically under divided attention conditions. Dual task

assessments in some cases were more reliable than single task assessments and may be better able to detect linger-ing effects followlinger-ing concussion. Few of the studies have been replicated and applied across various age groups. A key limitation of these studies is that many include laboratory and time-intensive measures. Future research is needed to refine a time and cost efficient divided attention assessment paradigm, and more work is needed in younger (pre-teens) populations where the application may be of greatest utility.

Keywords Brain injury . Postural control . Cognition . Dual-task

Introduction

Cerebral concussion is a complex injury that may be difficult to evaluate and manage given the variability in presentation and the multiple systems affected by the injury (Giza and Hovda 2001). Best practices recommended for concussion evaluation include a multimodal assessment inclusive of symptoms, cognition, balance and a detailed clinical evalua-tion. This combined approach may be over 90 % sensitive to concussive injury (Broglio et al. 2007) and is much more sensitive than using any single measure in isolation (Register-Mihalik et al. 2013). A growing body of research suggests that many of the commonly used measures of con-cussion (e.g., self-report symptoms, clinical balance assess-ments, and computerized neurocognitive assessments) may not be as sensitive to deficits further out from the injury and that other measures such as Electroencephalography (EEG) or types of analysis (e.g. Approximate Entropy) on the currently used measures may be more beneficial (Cavanaugh et al.

2005; Prichep et al.2013; Slobounov et al.2010). In addition, recent literature has suggested that gait assessments such as

J. K. Register-Mihalik (*)

Clinical Research Unit, Emergency Services Institute, WakeMed Health and Hospitals, 3000 New Bern Ave., Raleigh, NC 27610, USA

e-mail: jmihalik@wakemed.org A. C. Littleton

:

Matthew Gfeller Sport-Related Traumatic Brain Injury Research Center, The University of North Carolina at Chapel Hill, CB# 8700, Chapel Hill, NC 27599, USA

A. C. Littleton

e-mail: alittlet@live.unc.edu K. M. Guskiewicz e-mail: gus@email.unc.edu DOI 10.1007/s11065-013-9238-1

gait speed, stride length and coordination during gait may also be important assessment measures, as they are also affected post-concussion (Catena et al.2007b,2009a).

One of the recommended measures that may provide additional information in the concussion assessment pro-cess is a simultaneous assessment of motor and cognitive functions, often referred to as a dual-task or divided attention assessment. These types of assessments are functional in nature as most activities, particularly those in sport require a division of attention while still produc-ing appropriate motor and cognitive responses. Although numerous studies have examined these paradigms in con-trols and concussed individuals, they are not widely used in concussion assessment across the medical field. In addition, these types of activities may also be a way to assess changes and deficits throughout the graduated re-turn to play protocol prior to full rere-turn to sport. While single tasks require attention, divided attention tasks lead to competition for attention resources between the simul-taneous tasks. If the individual is not given specific instructions about which task to prioritize, then their brain must decide which task to unconsciously prioritize. This competition for attention, or increase in cognitive load, typically causes decreased performance in one or both tasks. Concussion leads to cognitive deficits, so divided attention tasks may be more sensitive to concus-sion than single task assessments.

As the landscape of concussion management continues to advance, understanding the key components that should be included in the assessment process is essential to developing a n a p p r o p r i a t e t r e a t m e n t a n d m a n a g e m e n t p l a n . Understanding the effects of divided attention on cognition and postural control may also allow for the use of these types of concurrent activities in the rehabilitation process in cases of prolonged recovery following concussion.

There is a need for understanding the role of divided attention tasks in assessing the interaction of multiple systems post-concussion. This review provides a systematic examina-tion of the published literature involving the use of divided attention tasks incorporating a cognitive and motor task in the assessment and management of sport-related concussion. The goal is to further our understanding of the role of divided attention tasks in the concussion management process. The review will address the following questions:

1. What are the psychometric properties of divided attention paradigms proposed in the literature concerning assess-ment of concussion?

2. Following sport-related concussion, are there greater def-icits in cognitive or motor performance when performed under a dual-task paradigm than when performed alone? 3. What differences exist in divided attention performance

between injured individuals and controls?

Methods

Search Strategy

Multiple databases including PubMed/MEDLINE (n =37), Embase (n =37) and CINAHL (n =350) were searched for relevant articles using the search terms“dual-task” OR “di-vided-attention” AND “concussion.” These article titles and abstracts were then reviewed for inclusion. Each article meet-ing the criteria after abstract review was then reviewed entirely to ensure all inclusion criteria were fully met in the study. All articles meeting relevant inclusion criteria were then hand searched for additional relevant articles to include in the review using the same inclusion criteria.

Study Selection

The search yielded a broad set of articles, not all relevant to the review with a total of 424 articles initially identified and a total of 38 articles meeting initial inclusion criteria after title and abstract review. However, after full review of each the remain-ing 38 articles by two separate reviewers, only 19 of these articles met all inclusion criteria including referencing a dual-task inclusive of a cognitive and motor dual-task and were included for the systematic review. The articles, detailed in Table1, were then hand searched for potential additional references to include in the review, with no additional articles being includ-ed. All articles were reviewed for duplication and the follow-ing inclusion criteria:

1) Published on or before July 9, 2013

2) Participants 17+ more years old (college-aged and older) 3) Dual-task (including a cognitive and motor (balance or

gait) task) assessment used

4) Discussion of application to concussion or mild TBI assessment or management

The inclusion criteria were selected to understand the body of literature surrounding sport-related concussion assessment and management. The criteria were restrictive to those studies citing or implicating direct implications for concussion assessment.

Summary of Study Designs and Methodologies

Most studies (n =15) had a longitudinal design with at least two testing/data collection sessions (Catena et al.2007a,b,

2009a,b,2011; Chiu et al. 2013; Kleffelgaard et al. 2012;

Martini et al.2011; Okumura et al.2013; Parker et al.2005,

2006,2007, 2008; Ross et al. 2011; Teel et al. 2013). The remaining 4 had a cross sectional design (Broglio et al.2005; Cavanaugh et al. 2007; Fait et al.2013; Resch et al. 2011); however, two of these studies also included a session where tasks were practiced but not assessed. (Broglio et al. 2005;

Ta b le 1 D eta ils an d k ey find ings of ar ti cle s in clu d ed in the sys temat ic re v ie w a Study details (F ir st Auth or , Publ ica tion Y ear , Journal) Dual-task/divided attention p aradigm d escription n , S ample, sett ing S tudy design/assess ment time points Des criptive d ata h ighlig hts K ey findings Bro g lio, 2005 , Me d S ci Sport E xer -E yes open conditions of SOT w ith task switching cognitive task (bu t 10 s tr ia ls) n = 20, healthy y o ung adults , laboratory -C ross -se cti onal -S ession 1: orientation; S ession 2 (24 –72 h la te r): ass essment -F aster reaction tim e under the dual-tas k (1234.50 ms vs. 1460.01 ms ) -O verall better bala n ce under dual-task compar ed to singl e ta sk -B alance and cognitive performance improved during the dual-task -S upports posture first p rinciple Catena, 2007, Ga it and Pos ture -L evel walking w ith a continuous q u esti on and answ er task n = 28, 14 con cussed and 14 controls , young adults, laboratory -C ross -se cti onal -A cute concussion, but th e sp eci fi c time sinc e injury was not included -C oncus sed g ro up (1.007 m/s) had slower gait v elocity under the dual-ta sk compa red to co nt ro ls (1 .276 m/ s) -C oncussed g roup (0.043 m) had g reater me dial -l ate ra l displa ce me nt than controls (0.034 m) under the dual-tas k -C oncus sed g ro up (0.149 m/s) had gre ate r m edia l-l ate ra l v elo cit y than controls (0.122 m/s ) under the dual-task -U nder the dual-task, concuss ed individ u als showed a conservative gait ad apt ati on and signs of inst abil ity wit h increas ed side-to-side sway acutely following injury -G ai t v eloc ity slo w er an d p ea k forw ar d C o M in concuss ed g roup than controls ac ut ely follow ing injur y Catena, 2007, Ex p B ra in Re s -L evel walking w ith a continuous q u esti on and answ er task and level w alking with a re act ion time task (res ponding to an au dible cue ) n = 28, 14 con cussed and 14 controls , young adults, laboratory -C ross -se cti onal -C oncuss ed subjects were tested within 48 h post-inj u ry -C oncus sed individuals gait velocity slower under question and answer tas k (1. 097 m/s) th an the rea cti o n time tas k (1.245 m/s) and single task w alking (1.219 m/s) -A ll concuss ed g ai t v eloc iti es (s ee above) w ere slower than th at o f controls in the single task (1.361 m/s), re act ion ti m e task (1.3 6 9 m /s ) and the question and ans w er task (1.276 m/s ) -C oncuss ed individuals gait velocity sl ower across single and bo th dual-tasks th an controls -Q uest ion and ans w er task resul ted in a more conservative g ait strategy than the simple reaction time tas k, making the ques tion and an swer tas k a po tentially m ore u seful secondary tas k Catena, 2009, Ex p B ra in Re s -L eve l wa lking w it h obsta cle avoidance and a continuous q u esti on and answ er task n = 34, 17 con cussed and 17 controls , young adults, laboratory (subset from anoth er study) -C ross -se cti onal -C oncuss ed subjects were asse ssed ove r 1 month po st-injury -In the concus sed g roup only , within 48 h o f injury , the relations hip w ith the o ri ent ing ef fe ct of att ent ion w as signi fic ant ly cor rel ate d wit h lead foot cle ar anc e (R 2= 0 .477, p = 0 .004) and sp at ia l o ri ent ati on at te nt ion w as cor re lat ed to tr ail ing foot obst ac le cle ar anc e (R 2 = 0 .265, p = 0 .050) -W hen the dual-task was p erformed, the ab ili ty to ori ent at ten tion w as co rr el ate d ev en more w ith le ad foot cl ea ra nc e and al so cor re lat ed to tr aili ng foot cl ear anc e -B y d ay 6, thes e correlations are n o longer seen in th e concussed g roup and coincide w ith the return o f the ab ili ty to spat ial ly o ri ent at tent ion Catena, 2009, J N eur o eng and R eh ab -L evel walking w ith a continuous q u esti on and answ er task n = 30, 15 con cussed and 15 controls , young adults, laboratory -L ongitudinal, repeated measures -C oncuss ed subjects were asse ssed at appr oxi m at el y d ay s 2 , 6, 14 and 2 8 post-injury -C oncus sed individuals (1.245 m/s) have reduced anterior -po sterior velo city at 2-days post-injury compar ed to cont rol s (1 .326 m/ s) under the dual-task -C oncuss ed individuals reduce their forw ar d m ot ion ac u te ly fol lo wi ng injury when performing a dual-task -T he d ivided attention tas k w as only able to b etter d is tinguish conservative g ait adaptations immed iately following concus sion as by day 6 the groups w er e simila r

Ta b le 1 (continued ) Study details (F ir st Auth or , Publ ica tion Y ear , Journal) Dual-task/divided attention p aradigm d escription n , S ample, sett ing S tudy design/assess ment time points Des criptive d ata h ighlig hts K ey findings Catena, 201 1, J of Neuroeng and R eh ab -L ev el w al k in gw it ha na u d it o ry S troop task n = 20, 10 con cussed and 10 controls , young adults, laboratory -L ongitudinal, repeated measures -C oncuss ed subjects were asse ssed at appr oxi m at el y d ay s 2 , 6, 14 and 2 8 post-injury -N o d if ferences on Stroop tasks across groups or conditions -In concussed individu als (not controls ) mode ra te co rr ela tion b et we en sagi tta l plan e m otion and Stroop performance during g ait at 4 8 h post-injury (R 2 = 0.41 1, p = 0 .046) -C oncussed individuals had m ore frontal plane m otion during g ait, but even more so durin g the cognitive task at day 1 4 post-injury compared to days 7 and 2 8 -C oncuss ed individuals S troo p performan ce correlated w ith g ait measures within 2 d ays o f injury Cavanaugh, 2007, J NeuroEngi- neer Rehab -M odified SOT (only 2 trials of each condition) with a d igit span (pre-d etermined length b y single tas k) n = 30, healthy y o ung adults , laboratory -C ross se cti onal -S ingle testing sess ion -M ore random center of pressu re A/P time se rie s duri n g dua l-task performance (p = 0 .004) -U sed approx imate entrop y -M ore ran dom A/P C OP data under the du al-tas k -P oten tial for ApEn to detect subtle changes in postural contro l and be us ed in dual -ta sk asse ssment Chiu, 2 013, Ga it and Pos ture -L evel walking w ith continuous que st ion/ ans w er ta sk n = 46, 23 con cussed and 23 controls , young adults, laboratory -R epea te d m ea sure s -C oncuss ed subjects were asse ssed w it hin 4 8 h po st-injury -C oncus sed p atients showed greater deviatio n p hase va lues (approximately 20°) during the dual-task than the control g roup (approximately 18°) -D uring the dual-task concussed p atients (18.2°) h ad greater root mean square dif ferences for the h ip-knee continuous relative phase (C RP) patterns durin g the dual-task compared to controls (16.5°) -D uring the dual-task concussed p atients (30.9°) h ad greater root mean square dif ferences for the knee C RP patterns during the dual-task compared to controls (22.8°) -C ompared to level walking, co ncussed individ u als h ad greater p attern changes in h ip-knee and knee-angle inter -joint coordination during the ob stacle or concur re nt ta sk com p ar ed to the contr o ls Fait, 2013, J He ad Tr au m a Rehabil -L ev el wa lking w it h m odif ied visua l S troop task -L eve l wa lking, w ith obst acl e avoidance and modified visual S troop task n = 12, 6 concussed and 6 controls , college aged athletes, laboratory -C ross -se cti onal -O n average concus sed subjec ts we re asses sed 37 .33 d ay s (SD = 4 .8) po st-injury -C oncus sed h ad more mean errors on the Stroop task than controls (15 v s. 5) -C oncus sed individuals (no obstacle-173.94 ms; left p assage-147 .60 m s; right passage 131.8 1 ms ; m oving obstacle left to rig ht-224.24; moving obstacle right to left-184.09) had a greater dual-task cost d u ring all wal k ing ta sks than contro ls (no obstacle-68.5 8 ms ; left p assage-71.51 ms; right passage 7 3 .29 m s; moving o b stacle left to right-68.36; moving o b stacle right to left-151.19 ) -In this p reliminary , small st udy , concus sed athletes h ad higher dual-ta sk cos t to gait va ri able s and mor e ov erall errors o n the cognitive Stroop task when they were asymptomatic com p ar ed to cont rol s

Ta b le 1 (continued ) Study details (F ir st Auth or , Publ ica tion Y ear , Journal) Dual-task/divided attention p aradigm d escription n , S ample, sett ing S tudy design/assess ment time points Des criptive d ata h ighlig hts K ey findings K lef fe lg aa rd, 2012, Disabil and Rehabil -N ormal dou ble leg st ance with arithmetic tas k of 8 double d igit addition and subtraction tasks n = 2 9 in d ividuals part of a lar ger study who consented to a 1 and a 4 y ear pos t-mild brain injury follow-up, young adult to middle ag e individuals , laboratory -L ongitudinal -1 year and 4 years pos t-inj u ry -S igni fi cant corr ela tio n w ith per ce ived bala nce abili tie s (ρ = 0 .4 3), phys ical symptom sc o re (ρ = 0 .49) and psychological symptom sc ore (ρ = 0.37) and b alance performance during the dua l-t ask -B al anc e pr oblems, sp eci fi cal ly wi th the addition of a cognitive task p ersist for po tentially y ears after concu ssive in jur y and the se de fi cit s ar e as socia te d with perception of symptoms Martini, 201 1, Arch Phys Me d Rehabil -L evel walking w ith B rooks ’Spa tia l Me mor y T ask and le v el w alki n g with obstacle avoidance and B rooks ’ Spat ial M emory T as k n = 68, 28 previous ly concussed and 4 0 non-concuss ed, college students, laboratory -C ross -se cti onal -C oncuss ed subjects were asse ssed at an average of 6.32 y ears post-inj u ry -C oncus sed g ro up sh owed greater double-suppo rt percent in the obstacle with cognitive task (21.63 %) compared to controls (19.00 %) -C oncus sed g ro up sh owed significantly shorter single leg stance time (39.54 %) co mpared to controls (40.79 %) -S ignificant cor re la tio ns be tw een previous number o f concu ssions and percen tage of single leg stance time for walking and cognitive task (ρ = − 0.45) and obstacle and cognitive task (ρ = − 0.42) as wells as double leg stance time fo r wal k ing and co gniti ve tas k (ρ = 0 .34) and the obstacle and cognitive task (ρ = 0 .44) -Individuals with a p reviou s concus sion history (av g. of 6 y ears prior) continued to show dif ferences in g ait patterns compared to h eal th contr o ls Okumura, 2013, Med Sci S port Ex er -H arvard S tep T es t with Global S w itch T ask (3 0, 40 and 6 0 trials) n = 59, healthy y o ung adults , laboratory -R epea te d m ea sure s -A sse ssments oc curred at baseline, 1 week later and approximately 7 m onths later -G lobal S witch reliability at 7 d ays: 0.64 30 trial test, 0.86 40-trial test, and 0 .8 3 for the 60-tra ils te st -G loba l S w itch R elia bili ty at 7 m onths : could not calculate 3 0 trial test, 0 .32 40-trial tes t, and 0 .59 for the 60-trial tes t -T he average g lobal cos t w as greater in the dual-task (209.37 ms) than in the single-task (89.96 ms) -R eli abil ity of th e swit ch ta sk w as moderate to high -S witch index m ay provide researchers an d cli nici ans w it h a common metr ic to assess cognitive pertu rbation Parker , 2005, Cli n Bio m ec h -L eve l wa lking w it h simple m enta l ta sks (spel ling 5 let ter w or ds in revers e, subtractio n b y 7 s and reciting the m on ths o f the year in re ve rs e o rde r) n = 20, 10 con cussed and 10 controls , college-aged, laboratory -C ross se cti onal -C oncuss ed subjects were asse ssed w it hin 4 8 h of their injury -U nder the dual-task (within 2 days of injur y ) m edi al/l ate ra l CoM R O M wa s greater in the con cussed g roup (0 .043) than th e control g roup (0.037) -U nder the dual-task (within 2 days of injur y ) th e CoM ant er ior/ poste ri or velo city was slower in the concussed group (1.207 m/s ) than th e control group (1.352) -Illustrates ef fects o f concussion on atte ntio nal ca p ac ity -D if ferences betwee n g roups greater in the dual-task conditions, h ighlight the atte ntio nal ca p ac ity ma y not be adequate to resp ond to multiple inputs wi th in the fir st 48 h fol low ing concus sion

Ta b le 1 (continued ) Study details (F ir st Auth or , Publ ica tion Y ear , Journal) Dual-task/divided attention p aradigm d escription n , S ample, sett ing S tudy design/assess ment time points Des criptive d ata h ighlig hts K ey findings Parker , 2006, Me d S ci Sport E xer -L eve l wa lking w it h simple m enta l ta sks (spel ling 5 let ter w or ds in revers e, subtractio n b y 7 s and reciting the m on ths o f the year in re ve rs e o rde r) n = 30, 15 con cussed and 15 controls , college aged, laboratory -L ongitudinal, repeated measures -C oncuss ed subjects were asse ssed at d ays 2 , 5 , 1 4 an d 2 8 p o st-i n jur y -C oncus sed individuals walked significantly slower than the norm group at 4 8 h post-injur y in dual-ta sk conditions (single task: 1 .200 m/s v s. 1.275 m/s ; dual task: 1.05 0 vs.1.175 m/s) -S tride length w as longer during the single tas k compared to the dual-task at days 2 (1.326 m v s 1 .224 m) and 5 (1.403 vs. 1 .342) post-injury in the concussion group -D ual-task slowed gait in concus sed individ u als at all ti me po ints -V ar ia bi li ty in ef fe ct s o f tas k and ti m e o n ga it ve loci ty and st rid e leng th b etw ee n concus sed and con trol g roups -M ost d if ferences occurred during the du al-tas k condition highlighting the need for m ore complex assessment po st-concus sion Parker , 2007, Br J S p o rts Me d -W alking on 10-m w alkway at p ref er re d spee d w ith simple ment al ta sks (s p ell ing 5 lett er words in reverse, subtraction b y 7 s and reciting the months of the y ear in reve rs e o rde r) n = 58, 29 con cussed and 29 controls , college aged, laboratory -L ongitudinal, repeated measures -C oncuss ed subjects were asse ssed at d ays 2 , 5 , 1 4 an d 2 8 p o st-i n jur y -L ow to moderate corr elations between R T an d dua l-tas k medi al-lat er al sw ay (r = 0 .401, p = 0 .003) and reaction time an ds w ayv el o ci ty (r = 0 .317, p = 0.022) on the first day o f testing 48 h after injury – No other correlation s observed -R ecov ery of gait patterns and neuro p sychological p erformance were independent -D ual-task produced more sway and displacemen t for both g roups, w ith th is inc re ase d sw ay dur ing dual-ta sk lasting longer in the concussed g roup Parker , 2008, Me d En gineer and P h y s -L eve l wa lking w it h simple m enta l ta sks (spel ling 5 let ter w or ds in revers e, subtractio n b y 7 s and reciting the m on ths o f the year in re ve rs e o rde r) n = 56, 2 8 concuss ed (14 athletes 14 n on-athletes) and 28 controls (14 athletes 1 4 non-athletes), young adults, laboratory -R epea te d m ea sure s -C oncuss ed subjects were asse ssed at d ays 2 , 5 , 1 4 an d 2 8 p o st-i n jur y -T he gait velocity of athlete g roups (concuss ed athletes: 1.225 m/s, non-concussed athletes: 1.175 m/s) was slower th an non-athlete g roups (concuss ed non-athletes : 1 .275 m/s, non-concus sed non-athletes: 1 .350 m/ s) under the dual-task -A thletes, whether concu ssed o r not, maintain their b alance through re duc ed sa gitta l p la ne move me nt to po tentially control fo r increased cor o na l p la ne sw ay -A thle te s h av e an ove ra ll slow er gai t velocity than the non-athletes Res ch, 201 1, J At hl T ra in -S OT wit h auditor y swi tch ta sk n = 20, healthy college-aged students, laboratory -R epea te d m ea sure s -T wo se ssi ons sepa rat ed by 2 d ays: one se ssi on in clu d ed singl e tas k asse ssment and oth er se ssion inclu d ed a dual ta sk as sess me nt -B alance improved during S OT condition 1 and condition 3 in the dual-task (C1: 91.6 v s. 89.5; C 3 : 89.7 vs. 84.1) -R eaction time longer and more errors made during switch trials u n d er th e dual-task -R eaction times longer for sw itch trials than non-switch trials in dual and si ngle task -R eaction time longer for dual-task conditions during switch trials -P oten tia l u se for dual-ta sk asse ssment fo ll owing co n cussi on -S upports posture first p rinciple Ross, 2 0 1 1 , J Sport R ehab -B ESS w ith aud itor y mat h ta sk -S OT eyes open conditions with vi su al ma th ta sk n = 30, healthy college aged participants, laboratory -R epea te d m ea sure s -T wo se ssi ons sepa rat ed by 14 days -D ual-ta sk re li abi lity : S OT 0.318 , B ESS 0.662, procedural re action time 0.501, procedural auditory accuracy (S O T) 0.142, procedural auditory accuracy (BESS) 0.513 -L ow re li abil ity of the S OT composit e sc ore, but hig h er reliability of BESS un der dual-task -B etter S OT perfo rmance under dual-task, b u t not on the B ES S -Improved p rocedural reaction time un der th e dual-task (SOT)

Resch et al. 2011) Of the 19 studies, 13 compared concussed patients to controls (Catena et al. 2007a, b,

2009a, b, 2011; Chiu et al. 2013; Fait et al. 2013;

Kleffelgaard et al. 2012; Martini et al.2011; Parker et al.

2005, 2006, 2007, 2008), whereas 6 used only healthy participants to examine potential paradigms (Broglio et al.

2005; Cavanaugh et al.2007; Okumura et al.2013; Resch et al.2011; Ross et al.2011; Teel et al.2013). Only 3 out of the 19 studies examined psychometrics of the paradigms and these articles only included healthy participants (Okumura et al.2013; Resch et al.2011; Teel et al.2013). All studies included both male and female participants; however, no study controlled for gender as a potential covariate. The mean sample size for the included studies was (35.05±15.51 participants). Age range for the studies ranged from college aged participants through middle age. Not all studies included age range specifications for inclu-sion, but all included descriptors around the age of partici-pants included in the study.

The definition of concussion or mild TBI was not con-sistent across studies. Most commonly, the definition of the American Academy of Neurology’s Grade II concussion (Neurology Quality Standards Subcommittee1997) requir-ing transient confusion, no loss of consciousness, concus-sion symptoms of mental status abnormalities on examina-tion that last more than 15 min (Catena et al. 2007a, b,

2009a,b,2011; Chiu et al.2013; Parker et al.2005,2006,

2007). No studies included in the final review were inclu-sive of a dual-task rehabilitation paradigm encompassing balance and cognitive activities. A dual-task rehabilitation case-study was identified in the search but was excluded due to the task only consisting of dual cognitive task and not being an empirical research article.

Common Divided Attention Measures

The most common measures of divided attention used in the reviewed studies were gait and walking tasks with a cogni-tive task or an obstacle to avoid task (n =13) (Catena et al.

2007a,b,2009a,b,2011; Chiu et al.2013; Fait et al.2013;

Martini et al.2011; Okumura et al.2013; Parker et al.2005,

2006,2007,2008) and clinical balance tasks in the pres-ence of a cognitive task (n = 6) (Broglio et al. 2005; Cavanaugh et al. 2007; Kleffelgaard et al. 2012; Resch et al.2011; Ross et al.2011; Teel et al.2013). The cognitive tasks included in the reviewed paradigms were simple ques-tion and answer tasks with basic mental status quesques-tions (Catena et al.2007a,b,2009a,b; Parker et al.2005,2006,

2007, 2008), complex attention tasks with incongruent Stroop task (Teel et al.2013), global task switching visual (Broglio et al. 2005) and auditory task (Okumura et al.

2013; Resch et al.2011), modified visual Stroop task (Fait et al.2013), auditory Stroop task (Catena et al.2011), the

Ta b le 1 (continued ) Study details (F ir st Auth or , Publ ica tion Y ear , Journal) Dual-task/divided attention p aradigm d escription n , S ample, sett ing S tudy design/assess ment time points Des criptive d ata h ighlig hts K ey findings T eel, 2013, J Sc i M ed Sport -S OT eyes ope n w it h a vi sual incongruent S troo p task n = 23, healthy college-aged participants, laboratory -R epea te d m ea sure s -T wo se ssi ons appr oxi m at el y 1 4 d ay s apa rt -Incongruent Stroop dual-task re lia bili ty = 0 .745 -Incongruent Stroop single-task re lia bili ty = 0 .649 -S OT conditions dual-task reliability: condition 1 0 .613, condition 3 0 .714, condition 4 0 .801, condition 6 0 .745 -S OT conditions single task reliability: condi tion 1 0 .61 1 , con ditio n 3 0.3 45, condition 4 0 .845, condition 6 0 .745 -R eaction time longer under d ual-tas k (5625.898 ms vs. 6161.470 ms) -R eliability of in congruent Stroop and S O T conditions moderate to high and higher than in o ther stud ies (pote n tia lly due to pr ac tic ing the ta sk in ful l) -R eaction time longer u nder dual-task -O nly condition 4 equilibrium sc ore better under dual-task (dif feren t from other studies) a Abbr eviation Key : SOT se nsor y o rg aniz ati o n test , BE SS balance error sc oring system, Co M ce nter of ma ss, CO P ce n te ro fp re ss u re , ApE n approximate en tropy ,ρ spea rman cor re la tion coe ff ic ie nt

Attentional Network Test (Chiu et al.2013), basic arithmetic (Kleffelgaard et al.2012), digit span task (Cavanaugh et al.

2007), spatial memory task (Martini et al.2011), and visual and auditory choice reaction time tasks (response indicated if the sum of addition problem was greater than 5 or less than 5 via right and left mouse clicks for the visual task with the Sensory Organization Test and orally with the auditory task performed with the Balance Error Scoring System) (Ross et al.

2011). The clinical balance assessments included the Balance Error Scoring System and the NeuroCom Sensory Organization Test. The main outcome measures for the clini-cal balance assessments included number of errors on the Balance Error Scoring System (Ross et al. 2011) and the Sensory Organization Test Equilibrium Scores, which is a measure of general postural sway across balance conditions (Broglio et al.2005; Cavanaugh et al.2007; Resch et al.2011; Ross et al.2011; Teel et al.2013). The Harvard Step Test was used in one of the reviewed studies (Okumura et al.2013). For the forceplate and gait assessments, center of mass displace-ment in the anterior and medial/lateral directions and peak velocity in those directions, maximum horizontal separation between the center of mass and center of pressure and range of motion in the sagittal and coronal planes, gait velocity, stride length, step width and stride time were the most common outcome measures (Catena et al.2007a,b,2009a,b,2011; Chiu et al.2013; Parker et al.2005,2006,2007,2008). When obstacle avoidance was included with a gait task, the primary variable of interest was the clearance height of a marker placed on the toe for the lead foot and the trailing foot (Fait et al.

2013; Chiu et al.2013; Catena et al.2009a,2009b). A few studies also assessed coordination among segments during gait tasks (Chiu et al.2013) and percent time in double and single leg stance (Martini et al.2011). Accuracy and reaction time were two common outcomes used in the cognitive assessments.

Results

Reliability and Validity of Measures

Only three of the articles included psychometric information on the dual-task paradigms incorporated in the studies. Although these three studies examined healthy subjects only, each also examined test reliability across time (Okumura et al.

2013; Ross et al.2011; Teel et al.2013). Because the tasks were inherently different, the psychometrics for each set of tasks are presented. Teel et al. (Teel et al.2013), using the eyes open conditions of the Sensory Organization Test and a in-congruent Stroop cognitive task, found that the reaction time correct (average) for each condition (ICC2, k =0.745) and the average equilibrium scores of conditions three (ICC2, k = 0.714) and four (ICC2, k =0.801) were highly reliable under

the dual-task paradigm and higher than in the other two studies presenting Sensory Organization Test stability and reliability measures. Conditions 1 (ICC2, k =0.611) and 6 (ICC2, k =0.514) average equilibrium scores and average reaction time (ICC2, k =0.649) were moderately reliable un-der the single task conditions. Reliability improved unun-der the dual-task condition for all measures except for condition 4 of the Sensory Organization Test (Table1).

Another reliability study (Ross et al.2011) examined two separate dual-task paradigms and found low reliability for the Sensory Organization Test composite score under both the dual-task (ICC2, 1=0.318) and single-task (ICC2, 1=0.245) conditions, whereas the Balance Error Scoring System had moderate reliability under both conditions (dual: ICC2, 1= 0.662; single: ICC2, 1=0.676). The cognitive task used in this study was a procedural (choice) reaction time task. The single task visual choice reaction time task throughput score reliabil-ity was moderate under the dual-task (ICC2, k =0.501) when performed with the Sensory Organization Test and low for the single-task (ICC2, k =−0.038). The accuracy score yielded low reliability scores for the single task (ICC2, k =0.279) and the dual-task Sensory Organization Test (ICC2, 1 = 0.142) but the auditory choice reaction time task yielded moderate reliability when performed with the Balance Error Scoring System (ICC2, 1=0.513).

Only the reliability of the global switch cost was presented in the third study at a 7-day interval and a 7-month interval (Okumura et al.2013). Chronbach’s alpha was used to calcu-late the stability reliability of the 30, 40 and 60 trial test at each time point. At the 7-day interval, the test-retest reliability was 0.64 for the 30, 0.86 for the 40, and 0.83. for the 60 trial test. At the 7-month interval, only the 40 and 60 trail tests reliabil-ity scores are presented, because the 30 trial test could not be calculated because of a negative average covariance. These scores were 0.32 for the 40 and 0.59 for 60 trial tests (Table1).

Neurocognitive and Postural Control Findings– The Influence of Dual-Task

The studies that only included healthy participants (no concussed participants) and examined potential dual-task par-adigms found mixed results concerning the influence of com-bining tasks on the performance of the specified cognitive and balance tasks. Table1highlights the findings of each study. Each of the four studies utilizing the various Sensory Organization Test condition equilibrium scores illustrate some balance improvements under the dual-task but for various conditions. Two of the studies found slowed response or reaction times (Teel et al. 2013; Resch et al. 2011), where one found response times to be faster under the dual-task (Broglio et al. 2005). Another study (Broglio et al.2005) found significant improvements in 3 out of 4 conditions (1, 3 and 4) balance tasks tested and 3 out of 4 cognitive tasks

assessed during the visual global switch task. However, when using all six Sensory Organization Test conditions and an auditory global switch task, one of these studies (Resch et al.

2011) only found significant improvements on two of the conditions (1 and 3) and significantly faster response times under the dual-task. A separate study including the eyes open conditions of the dual-task, but using the incongruent Stroop task, only found improvements on condition 4 of the Sensory Organization Test and found significantly slowed reaction time on the Stroop task under the dual-task (Teel et al.

2013). Ross et al. found the overall Sensory Organization Test composite equilibrium score to be significantly improved under the dual-task and significant improvement in the throughput score of a choice reaction time task when attention was divided (Ross et al.2011). The additional study incorpo-rating the various versions of the global switch task found longer response times and greater errors in all three versions of the task. No assessment of the motor control task was per-formed (Okumura et al.2013). One study that used various calculations from the Sensory Organization Test to obtain Approximate Entropy values, found changes in the random-ness of the center of pressure oscillations with the center of pressure time series values becoming more random (less pre-scribed or rigid) during a dual-task (digit forward task with predetermined string length) (Cavanaugh et al.2007).

The studies involving concussed and control participants found a greater cost to balance and gait performance (more sway, more errors and more conservative gait strategies) (Catena et al.2007a,b,2009a,2011; Chiu et al. 2013; Fait et al.2013; Parker et al.2005,2006,2007,2008) under the dual-task in concussed individuals compared to healthy con-trols, immediately after concussion (Table 1). Overall, re-sponse times are greater and gait strategies are overall more conservative under the dual-task vs. the single task, with this being magnified in concussed participants. However, these results may differ based on time frame of assessment as well as difficulty of the task employed. Effect sizes ranged from moderate to high when comparing dual vs. single tasks (Table2), with greater effect sizes for composite measures (Table2).

Divided Attention Differences Between Injured Individuals and Controls

Of the 13 studies including concussed participants (Catena et al.2007a,b,2009a,b,2011; Chiu et al.2013; Fait et al.

2013; Kleffelgaard et al.2012; Martini et al.2011; Parker et al.

2005,2006,2007,2008), 12 studies (Catena et al.2007a,b,

2009a,b,2011; Chiu et al.2013; Fait et al.2013; Martini et al.

2011; Parker et al.2005,2006,2007,2008) evaluated postural parameters of gait in conjunction with a cognitive task in both concussed and healthy individuals. Postural control and gait measures are less efficient (slower, less coordinated) in injured

individuals than controls and overall, and there is a greater cost to balance and gait efficiency (more sway, more errors and more conservative gait strategies) among concussed indi-viduals under the dual-task parameters. However, these changes and differences vary across the various assessment points included across the various studies. The article summa-ry table (Table1) outlines the various assessment time points and results for these studies. Many of the gait-focused studies have also illustrated that initially there are more deficits concerning gait performance. However over time, many of the single task and level walking gait parameters return to that of healthy normal controls within the first 6–7 days of injury (Catena et al. 2007a, b, 2009a,b, 2011; Chiu et al. 2013; Parker et al.2005,2006,2007,2008). However, the dual-task, specifically when obstacle avoidance is also includ-ed, requiring further division of attention, further sepa-rates the concussed participants from that of healthy con-trols at later time points (Catena et al.2009a,2009b; Chiu et al. 2013; Fait et al. 2013). Furthermore, the three studies that examined individuals further out from con-cussion (30 days to an average of 6 years post-injury) still found existing divided attention deficits concerning some gait parameters between the concussed individuals and control groups.(Fait et al.2013; Kleffelgaard et al. 2012; Martini et al. 2011) Table 1 highlights the findings from these studies. The paradigms included in the gait-focused studies include a cognitive task to divide attention, but many do not report the accuracy or response time of these tasks as outcomes in the studies. Another study reported no differences in auditory Stroop performance but did report a relationship between Stroop performance and sagittal plane motion at 48 h post-injury, where concussed individuals who had shorter sagittal plane center of mass/ center of pressure angles had longer reaction times in the Stroop task (Catena et al.2011). In addition, (Catena et al.

2009b) correlated spatial attention task performance with

obstacle clearance abilities under the dual- and single-task in concussed individuals (not healthy controls).

The additional study (Kleffelgaard et al.2012) including an injured population (4-years after injury) used a static double leg balance task while performing an arithmetic task with eight single- and double-digit additions and subtractions. The dual-task cognitive data was not recorded or scored in the study. There was a significant correlation between body sway (change in the center of pressure beneath the feet in the medial-lateral and anterior-posterior directions and in the ve-locity of the movement) and self-reported balance problems (p =0.020), physical symptoms (p =0.007), and psychological symptoms (p =0.05) at 4-years post-injury (Table1). Effect sizes varied from low to high when comparing findings be-tween concussed and control individuals on various dual-task measures. The effect size was typically larger immediately post-injury; however, moderate to high effect sizes were

Ta b le 2 E ffe ct si zes fo r se lec t v ar iabl es and assess ment time points from the reviewed st udies St udy de ta ils (F ir st Auth or , Publication Y ear , Journal) Co mpa ris ons used in ef fe ct siz e cal cula tion T y p e o f ef fec t siz e cal cula tio n u se d/ reported E ffe ct si ze a Bro g lio, 2005 , M ed S ci S port E xer D ual v s. single-task balance under a gl o b al switch dual-task (c al cu la te d) C ohen ’s d (d) S OT condition 6 w ith global switch task:-0.06 Catena, 2007, Gait and P os ture Gait veloci ty under a dual-task of obstacle avoidance in concuss ed v s. co ntrols (calculated) C ohen ’s d (d) G ait v elocity w ith o bstacle avoidance: -1.17 Catena, 2007, Exp B rain Res G ait v elocity unde r a reaction time dual-task and a ques tion answer dual-task in concussed v s contro ls acu tel y pos t-i n jur y (c al cu la te d) C ohen ’s d (d ) G ait v el oci ty w it h rea cti o n time tas k:-0 .88 G ait ve loci ty wit h q u esti on/a n swe r tas k :-1 .23 Catena, 2009, Exp B rain Res O bs tacle clearance of lead foot under a dual-task in concus sed vs . controls at 14 and 2 8 d ays post-injury (calculated) C ohen ’s d (d) 1 4 d ays post-injury obstacl e clearance of lead foot: -0.3 6 28 days post-injury obstacle clearance of lead foot: -0.3 9 Catena, 2009, J N euroeng and R ehab A nterior/Post erior (A/P ) and M edial/L ateral (M/L) v elocity during g ait under a dual-task in concus sed in concussed vs . controls at 14 and 2 8 d ays post-injury (calculated) C ohen ’s d (d) 1 4 d ays post-injury A/P v elocity:-0.05 28 days post-injury A/P v elocity:-0.05 14 days post-injury M/L v elocity:-0.16 28 days post-injury M/L v elocity:-0.1 1 Catena, 201 1, J o f N euroen g and Re hab Strength o f correlatio n b etween sagittal p lane m otion and Stroop performance during g ai t( re p o rt edi np ap er ) P earson C orrelation Coef fi ci ent (r) Stroop performance during g ait task: 0.6 4 Cavanaugh, 2007, J N euroEngineer Re hab D u al vs. si ngle ta sk b al ance pe rforman ce in h ealth y individuals (c al cu la te d) C ohen ’s d (d ) C ond ition 6 A ppr oximat e Ent ropy val u e for SOT condition 6 anterior/poster center o f p ress ure ti me se ri es : 0 .3 5 Cond ition 6 A ppr oximat e Ent ropy val u e for SOT condition 6 m edial/lateral center o f p ressure time se ries: -0.07 Chiu, 2 013, Gait and P osture Dual-tas k root mean square dif ferences for h ip –k n ee an d knee –ankle continuous relativ e p atterns (a co n tinuous me as ur em ent o f the in te ra ct io n between joints o r segments throughout the g ait cycle us ing jo int angl e-veloc ity pha se por tra its ) over a gait cycle under a cognitive task in con cussed v s. controls at 48 h post-inju ry (c alc u lat ed) C ohen ’s d (d) H ip-k nee root mean square dif ferences: 0.25 Knee ankle ro o t m ean square dif ferences: 0.29 Fait, 2013, J H ead T rauma Rehabil C ognitive d ual-ta sk cost (ef fect o f task o n p erformance) in concuss ed v s. co ntrol at appr oximately 30-days post-injury (c al cu la te d) C ohen ’s d (d) C os t durin g m oving obstacle left to right: 1 .75 Cos t durin g m oving obstacle right to left: 0 .29 Maximum g ait speed durin g m oving obs tacle left to right: -0.54 Maximum g ait speed during m oving obs tacle right to left: -0.73 Klef felgaard, 2012, Disabil and Rehabil D u al-tas k b al an ce per fo rmanc e am ong individ u als w ith concussion history correlation st rength w it h self-reported b alance problems at approximately 4-years post-injur y (r epor ted in p ap er ) S p ea rman ’sR an k Corr el ati ons Sway during normal standing w ith dua l task co rr ela ted w ith se lf-re por ted b alance problems: 0.43 Martini, 201 1, Arch Ph ys Med Rehabil Dual-tas k concuss ion history (avg. 6.3 y ear post-inju ry) v s. controls (c al cu la te d) C ohen ’s d (d) % time in double leg stance during g ait w ith cognitive task and obstacle: 0.89 % time in double leg stance during g ait w ith cognitive ta sk an d obs ta cl e: -0 .9 4

Ta b le 2 (continued ) St udy de ta ils (F ir st Auth or , Publication Y ear , Journal) Co mpa ris ons used in ef fe ct siz e cal cula tion T y p e o f ef fec t siz e cal cula tio n u se d/ reported E ffe ct si ze a Okumura, 2013, Med S ci Sp ort E xer D ual v s. single tas k cognitive p erformance in healthy in d ividuals (r ep o rt edi np ap er ) P ar tia l E ta S quar ed (p η 2) G lobal switch costs = 0 .44 Pe rc ent age er ro r scor es = 0. 54 Parker , 2005, Clin B iomech Dual-tas k concuss ed v s. co ntrol g ait m easures at 4 8 h post-injury (c al cu la te d) C ohen ’s d (d) 4 8 h pos t-injury gait velocity: -1.15 Parker , 2006, Med S ci S port E xer D ual-tas k concus se d v s. co ntrol g ait m easures at 1 4 and 28 days pos t-i n jur y (c al cul ate d) C ohen ’s d (d) 1 4 d ays post-injury stride length: -0.63 28 days post-injury stride length: -0.28 Parker , 2007, Br J S p o rts M ed Strength o f corre lation b etween reaction time and dual-task medi al/ lat er al swa y at 2 d ay s post-injur y (r epor ted in p ap er) P earson C orrelation Coef fi ci ent (r) 2 d ays post-inj u ry cor re lat ion b et wee n sw ay an d rea cti o n ti me : 0 .4 0 Parker , 2008, Med E ngineer and Phys Dual task concus sed v s. control g ait m ea sure s at 4 8 h post -in jury (c al cu la te d) C ohen ’s d (d ) 1 4 d ays post-inj u ry gai t veloc ity: 0 .4 4 28 days post-injury gait velocity: 0 .16 Res ch, 201 1, J A thl T rain T rial b y type intera ction in h ealth individuals for co gnitive performance (reported in p aper) P ar tia l E ta S quar ed (p η 2 ) G lobal switch costs: = 0.32 Ross, 2 0 1 1 , J S port R ehab Dual vs. single task b alance and cognitive performance in healthy individuals (r ep o rt edi np ap er ) P ar tia l E ta S quar ed (p η 2 ) S O T co mpo site = 0 .58 BESS to ta l error sc o re = 0 .26 Choice (procedural) react ion time (PR T) through put (on S OT) = 0.51 PR T A ccuracy (on SOT) = 0 .03 PR T A cc ura cy (on BE SS) = 0 .28 T eel, 2013, J S ci Med S p o rt Dual vs. single task b alance and cognitive performance in healthy individuals (calculated) C ohen ’s d (d) S OT condition 6 w ith Stroop: 0.08 Incongruent S troo p = 0 .25 a T h e ef fec t siz es lis ted ar e fo r sel ect , cli nic all y impor tan t v ari able s for m the reviewed studies, as each studi es emp loyed numerous comparisons acr os s a vary ing number o f outcomes

observed in studies examining differences among individuals with a concussion history, up to 6 years post-injury (Table2).

Discussion

Overall, the current literature suggests that divided attention tasks, specifically involving a concurrent cognitive and pos-tural control task would be useful in the assessment and management of concussion. Response times are greater, gait strategies are less efficient, and postural control deficits are greater in concussed participants compared with healthy con-trols both immediately and for some period following concus-sive injury, specifically under divided attention conditions. Dual task assessments in some cases were more reliable than single task assessments and they may be better able to detect lingering effects following concussion. Effect sizes vary de-pending on timing of assessment and the measures used. Future research is needed to refine a time and cost efficient divided attention assessment paradigm and to expand findings to younger populations.

Psychometrics

Overall, the reliability of the dual-tasks measures ranged from low to high in the paradigms where these values were pre-sented. The higher reliability values presented were on the Balance Error Scoring System (Ross et al.2011) and in the study where a complete practice session was allowed when performing the eyes open conditions of the Sensory Organization Test (Teel et al. 2013) Previous studies have reported the Balance Error Scoring System in singular form to be a reliable measure of balance (Valovich McLeod et al.

2004; Bell et al.2011), while one recent study reported lower reliability values (Finnoff et al.2009). Previous studies report lower reliability values overall on the Sensory Organization Test (Dickin and Clark2007; Broglio et al.2008; Register-Mihalik et al.2013). Some of this variability may perhaps be due to task familiarization with the task, as when this variation was removed by allowing the practice trials on the Sensory Organization Test in the study by (Teel et al.2013) reliability values were much higher. The stability of the global switch task over the various trials was good. The Sensory Organization Test eyes open measures, when oriented to them, the Balance Error Scoring System (Ross et al.2011), the global switch cost (Okumura et al.2013) and the incongruent Stroop task (Teel et al.2013) measures may be beneficial in the assessment of divided attention deficits following concus-sion from a reliability standpoint; however, research on these measures in concussed participants is needed. Furthermore, the other paradigms discussed did not include psychometric information for the balance or cognitive task. Given the serial nature of concussion assessment, future studies should include

reliability and validity measures when possible for the tasks and paradigms used.

Effects of the Dual-Task on Performance

The summary of study findings are consistent with previous divided attention literature in that under the divided attention paradigm there are differences that emerge, depending on the difficulty of the secondary cognitive task. In addition, these findings are also consistent in that depending on the paradigm, results and effects on divided attention may be varied. In studies with a relatively simple cognitive task, balance perfor-mance seems to improve under the dual- compared to the single-task conditions (Broglio et al.2005). However, with a more difficult cognitive task, balance often remains un-changed in healthy individuals (Teel et al.2013). Few studies use the same paradigm to compare outcomes, which makes interpretation as a whole difficult. In addition, not all studies evaluate cognitive performance and division of attentional resources, which would also add value to interpretation of study findings. Even among injured individuals, these same problems exist; however, overall gait strategies seem to be more conservative under the dual-task. Future studies should examine assessment of dual-task measures inclusive of the more traditional balance and gait tasks, in order to refine the most effective and efficient way to use the dual-task assess-ments. Since most tasks in everyday life involve carrying out both a cognitive task and balance task at the same time, it is important that we establish the effect of concurrent cognitive and balance tasks on performance, so that we can use dual-task paradigms as a more functional assessment and rehabil-itation strategy following concussion.

Divided Attention Effects in Concussed Individuals vs. Healthy Controls

Overall, the current review suggests that the divided attention gait tasks can differentiate concussed individuals from con-trols and that there is some resolution and change in attention-al capacity throughout the recovery process (Catena et attention-al.

2007a,b,2009a,b,2011; Chiu et al.2013; Fait et al.2013;

Parker et al. 2005,2006,2007, 2008). In addition, beyond 6 days post-injury, the articles reviewed here suggest that concussed individuals resemble healthy controls when the gait and cognitive tasks are performed in the typical single task paradigm. However, when the tasks are combined, concussed individuals illustrate a more conservative gait strategy under the dual-task (Catena et al. 2009a, 2007). These findings illustrate the need for this type of more complex assessment to be included in the acute assessment and return to play decision-making process following concussive injury as dif-ferent processes are assessed through these measures. Furthermore, two of the studies inclusive of individuals with

a previous history of concussion or brain injury, illustrate that these types of tasks may still differentiate these individuals from healthy controls, further highlighting the more long-term effects that may exist following a concussive injury (Kleffelgaard et al.2012; Martini et al.2011). Many of the studied tasks and outcomes are laboratory intensive and few studies have attempted to transfer how these types of tasks and what potential outcomes may be used in more traditional clinical settings, where the majority of concussions are eval-uated and managed. However, many of the gait tasks as well as the Harvard Step Test could be evaluated in a more sim-plistic way and provide valuable information in the clinical setting. Future studies should examine the use of dual-task assessments comprised of well-established clinical measures of cognition and balance and should explore new possibilities of incorporating divided attention tasks in the assessment and management of concussion.

Potential Role in Rehabilitation

No studies that met the inclusion criteria for the review in-cluded rehabilitation paradigms or interventions inclusive of divided attention tasks for post-concussion rehabilitation. To our knowledge, there have been no published empirical stud-ies on this topic. However, logically incorporating directed divided attention tasks into the return to play process may help improve performance. Participation in sport requires divided attention, because it involves rapid simultaneous processing of cognitive, motor and sensory information in order to carry out specified tasks. Because divided attention is required for sport, it is imperative that the role of divided attention tasks in the return to play progression following sport-related concussion be identified.

Conclusions and Limitations

Overall, divided attention tasks involving cognition and pos-tural control tasks may refine the assessment of concussion and identify compromised processes requiring healing and rehabilitation. Assessment of divided attention may give time-ly and relevant information to clinicians, as all aspects of sport require adequate and precise motor control in the presence of numerous cognitive demands. The current concussion evalu-ation paradigm does not include objective assessments in this capacity. Psychometric properties of the available paradigms need to be better established. Divided attention paradigms used in other settings and for other conditions should also be examined for their psychometric properties and potential fit in a concussion assessment model. In addition, more streamlined study of these paradigms, defining the most clinically useful and feasible paradigm, including specified motor and cogni-tive outcomes, in an injured population is needed before large-scale implementation is employed. Future research should

also address the role of divided attention activities in rehabil-itation following concussive injury.

Acknowledgments None. No funding sources contributed to the cur-rent paper. The authors have no disclosures related to the curcur-rent paper.

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