Restricted accessReview articleFirst published online 2023-08
Sensitivity and Specificity of Exercise Intolerance on Graded Exertion Testing for Diagnosing Sport-Related Concussion: A Systematic Review and Exploratory Meta-Analysis
There is no single gold standard test to diagnose sport-related concussion (SRC). Concussion-related exercise intolerance, that is, inability to exercise to the individual's appropriate level due to exacerbation of concussion-like symptoms, is a frequent finding in athletes early after SRC that has not been systematically evaluated as a diagnostic test of SRC. We performed a systematic review and proportional meta-analysis of studies that evaluated graded exertion testing in athletes after SRC. We also included studies of exertion testing in healthy athletic participants without SRC to assess specificity. Pubmed and Embase were searched in January 2022 for articles published since 2000. Eligible studies included those that performed graded exercise tolerance tests in symptomatic concussed participants (> 90% of subjects had an SRC, seen within 14 days of injury), at the time of clinical recovery from SRC, in healthy athletes, or both. Study quality was assessed using the Newcastle-Ottawa Scale. Twelve articles met inclusion criteria, most of which were of poor methodological quality. The pooled estimate of incidence of exercise intolerance in participants with SRC equated to an estimated sensitivity of 94.4% (95% confidence interval [CI]: 90.8, 97.2). The pooled estimate of incidence of exercise intolerance in participants without SRC equated to an estimated specificity of 94.6% (95% CI: 91.1, 97.3). The results suggest that exercise intolerance measured on systematic testing within 2 weeks of SRC may have excellent sensitivity for helping to rule in the diagnosis of SRC and excellent specificity for helping to rule out SRC. A prospective validation study to determine the sensitivity and specificity of exercise intolerance on graded exertion testing for diagnosing SRC after head injury as the source of symptoms is warranted.
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References
1.
RoosKG, KerrZY, DjokoA, et al.Concussion incidence in US high school and collegiate basketball. Brain injury, 2016; 30(5-6):531; doi: 10.3109/02699052.2016.1162060
2.
McCroryP, MeeuwisseW, DvorakJ, et al.Consensus statement on concussion in sport—the 5th International Conference on Concussion in Sport held in Berlin, October 2016. Br J Sports Med, 2017; 51(11):838–847; doi: 10.1136/bjsports-2017-097699
3.
LangloisJA, Rutland-BrownW, WaldMM. The epidemiology and impact of traumatic brain injury: a brief overview. J Head Trauma Rehabil, 2006; 21(5):375–378
4.
GliklichRE, LeavyMB, KarlJ, et al.A framework for creating standardized outcome measures for patient registries. J Comp Eff Res, 2014; 3(5):473–480.
5.
SadyMD, VaughanCG, GioiaGA. Psychometric characteristics of the postconcussion symptom inventory in children and adolescents. Arch Clin Neuropsychol, 2014; 29(4):348–363.
6.
KontosAP, DeitrickJM, CollinsMW, et al.Review of vestibular and oculomotor screening and concussion rehabilitation. J Athl Train, 2017; 52(3):256–261; doi: 10.4085/1062-6050-51.11.05
7.
HaiderMN, LeddyJJ, DuW, et al.Practical management: brief physical examination for sport-related concussion in the outpatient setting. Clin J Sport Med, 2020; 30(5):513–517; doi: 10.1097/jsm.0000000000000687
8.
FarnsworthJL, 2nd, DargoL, RaganBG, et al.Reliability of computerized neurocognitive tests for concussion assessment: a meta-analysis. J Athl Train, 2017; 52(9):826–833; doi: 10.4085/1062-6050-52.6.03
9.
VartiainenMV, HolmA, LukanderJ, et al.A novel approach to sports concussion assessment: computerized multilimb reaction times and balance control testing. J Clin Exp Neuropsychol, 2015; 1–15; doi: 10.1080/13803395.2015.1107031
10.
HaiderMN, LeddyJJ, PavlesenS, et al.A systematic review of criteria used to define recovery from sport-related concussion in youth athletes. Br J Sports Med, 2018; 52(18):1179–1190; doi: 10.1136/bjsports-2016-096551
11.
LeddyJJ, BakerJG, MerchantA, et al.Brain or strain? Symptoms alone do not distinguish physiologic concussion from cervical/vestibular injury. Clin J Sport Med, 2015; 25(3):237–242.
12.
KozlowskiKF, GrahamJ, LeddyJJ, et al.Exercise intolerance in individuals with postconcussion syndrome. J Athl Train, 2013; 48(5):627–635.
13.
LeddyJJ, WilberCG, WillerBS. Active recovery from concussion. Curr Opin Neurol, 2018; 31(6):681–686; doi: 10.1097/wco.0000000000000611
14.
LeddyJJ, BakerJG, KozlowskiK, et al.Reliability of a graded exercise test for assessing recovery from concussion. Clin J Sport Med, 2011; 21(2):89–94.
15.
LeddyJJ, HaiderMN, EllisMJ, et al.Early subthreshold aerobic exercise for sport-related concussion: a randomized clinical trial. JAMA Pediatr, 2019; 173(4):319–325; doi: 10.1001/jamapediatrics.2018.4397
16.
LeddyJJ, MasterCL, MannixR, et al.Early targeted heart rate aerobic exercise versus placebo stretching for sport-related concussion in adolescents: a randomised controlled trial. Lancet Child Adolesc Health, 2021; 5(11):792–799.
17.
LeddyJJ, HindsAL, MiecznikowskiJ, et al.Safety and prognostic utility of provocative exercise testing in acutely concussed adolescents: a randomized trial. Clin J Sport Med, 2018; 28(1):13–20.
18.
OrrR, BoggT, FyffeA, et al.Graded exercise testing predicts recovery trajectory of concussion in children and adolescents. Clin J Sport Med, 2021; 31(1):23–30; doi: 10.1097/jsm.0000000000000683
19.
MoherD, LiberatiA, TetzlaffJ, et al.Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med, 2009; 151(4):264–269.
20.
ParikhR, MathaiA, ParikhS, et al.Understanding and using sensitivity, specificity and predictive values. Indian J Ophthalmol, 2008; 56(1):45.
21.
LeddyJJ, HindsAL, MiecznikowskiJ, et al.Safety and prognostic utility of provocative exercise testing in acutely concussed adolescents: a randomized trial. Clin J Sport Med, 2018; 28(1):13–20; doi: 10.1097/JSM.0000000000000431
22.
ChizukHM, WillerBS, HornEC, et al.Sex differences in the Buffalo Concussion Treadmill Test in adolescents with acute sport-related concussion. J Sci Med Sport, 2021; 24(9):876–880.
23.
CohenJ.A coefficient of agreement for nominal scales. Educ Psychol Meas, 1960; 20(1):37–46.
24.
LeddyJJ, WillerB. Use of graded exercise testing in concussion and return-to-activity management. Curr Sports Med Rep, 2013; 12(6):370–376; doi: 10.1249/jsr.0000000000000008
25.
WolthuisRA, FroelicherVFJr., FischerJ, et al.New practical treadmill protocol for clinical use. Am J Cardiol, 1977; 39(5):697–700.
26.
StangA.Critical evaluation of the Newcastle-Ottawa Scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010; 25(9):603–605.
27.
MelnykBM, Fineout-OverholtE.Evidence-Based Practice in Nursing & Healthcare: A Guide to Best Practice. Lippincott Williams & Wilkins: 2011.
28.
RossS.Chapter 6–Distributions of Sampling Statistics. In: Introduction to Probability and Statistics for Engineers and Scientists Fifth Edition. Elsevier: Los Angeles, CA; 2014; pp. 218–219.
29.
PiperC.System for the unified management, assessment, and review of information (SUMARI). J Med Library Assoc JMLA, 2019; 107(4):634.
30.
McHughML.Interrater reliability: the kappa statistic. Biochemia Medica, 2012; 22(3):276–282.
31.
HallC, HaiderM, HornE, et al.Exercise-induced headache in the concussed is associated with dysregulation of cerebral blood flow. Clin J Sport Med, 2021; 31(2):164; doi: 10.1097/JSM.0000000000000912
32.
HaiderMN, JohnsonSL, MannixR, et al.The Buffalo Concussion Bike Test for concussion assessment in adolescents. Sports Health, 2019; 1941738119870189
CordingleyD, GirardinR, ReimerK, et al.Graded aerobic treadmill testing in pediatric sports-related concussion: safety, clinical use, and patient outcomes. J Neurosurg Pediatr, 2016; 18(6):693–702.
35.
LeddyJ, LeshK, HaiderMN, et al.Derivation of a focused, brief concussion physical examination for adolescents with sport-related concussion. Clin J Sport Med, 2021; 31(1):7–14; doi: 10.1097/jsm.0000000000000686
36.
PrimJH, DavilaMI, McCullochKL. A pilot study on exertional tasks with physiological measures designed for the assessment of military concussion. Concussion, 2021; 6(1); doi: 10.2217/cnc-2020-0018
37.
PowierzaCS, ClarkMD, HughesJM, et al.Validation of a self-monitoring tool for use in exercise therapy. PM R, 2017; 9(11):1077–1084; doi: 10.1016/j.pmrj.2017.03.012
38.
GaetzMB, IversonGL. Sex differences in self-reported symptoms after aerobic exercise in non-injured athletes: implications for concussion management programmes. Br J Sports Med, 2009; 43(7):508–13; doi: 10.1136/bjsm.2008.051748
39.
MiutzLN, BlackAM, JordanMJ, et al.Feasibility, reliability, and concurrent validity of a field test of exertion in high school students. Clin J Sport Med, 2020; 30(3):e91; doi: 10.1097/JSM.0000000000000844
40.
ReschJE, BrownCN, SchmidtJ, et al.The sensitivity and specificity of clinical measures of sport concussion: three tests are better than one. BMJ Open Sport Exerc Med, 2016; 2(1):e000012; doi: 10.1136/bmjsem-2015-000012
41.
SchatzP, SandelN. Sensitivity and specificity of the online version of ImPACT in high school and collegiate athletes. Am J Sports Med, 2013; 41(2):321–326.
42.
ArcaKN, StarlingAJ, AciernoMD, et al.Is King-Devick testing, compared with other sideline screening tests, superior for the assessment of sports-related concussion?: a critically appraised topic. Neurologist, 2020; 25(2):33–37.
43.
GalettaKM, LiuM, LeongDF, et al.The King-Devick test of rapid number naming for concussion detection: meta-analysis and systematic review of the literature. Concussion, 2016; 1(2):CNC8.
44.
FullerG, TuckerR, StarlingL, et al.The performance of the world rugby head injury assessment screening tool: a diagnostic accuracy study. Sports Med Open, 2020; 6(1):1–12.
45.
DowneyRI, HutchisonMG, ComperP. Determining sensitivity and specificity of the Sport Concussion Assessment Tool 3 (SCAT3) components in university athletes. Brain Inj, 2018; 32(11):1345–1352.
46.
ClausenM, PendergastDR, WilierB, et al.Cerebral blood flow during treadmill exercise is a marker of physiological postconcussion syndrome in female athletes. J Head Trauma Rehabil, 2016; 31(3):215–224.
47.
LeddyJ, CoxJ, BakerJ, et al.Exercise treatment for post concussion syndrome: a placebo controlled pilot study of changes in fMRIBlood flow and symptoms. Brain Inj, 2012; 26(4-5):388–389; doi: 10.3109/02699052.2012.660091
48.
BroglioSP, FerraraMS, MacciocchiSN, et al.Test-retest reliability of computerized concussion assessment programs. J Athl Train, 2007; 42(4):509–514.
49.
LeddyJJ, KozlowskiK, DonnellyJP, et al.A preliminary study of subsymptom threshold exercise training for refractory post-concussion syndrome. Clin J Sport Med, 2010; 20(1):21–27.
50.
WillerB, LeddyJ, PendergastD, et al.Use of low-level exercise to improve the physiologic condition of individuals with post concussion syndrome. J Head Trauma Rehabil, 2009; 24(5):397; doi: 10.1097/HTR.0b013e3181bd6769
51.
ChrismanSPD, WhitlockKB, MendozaJA, et al.Pilot randomized controlled trial of an exercise program requiring minimal in-person visits for youth with persistent sport-related concussion. Front Neurol 019;10:623; doi: 10.3389/fneur.2019.00623
52.
KurowskiBG, HugentoblerJ, Quatman-YatesC, et al.Aerobic exercise for adolescents with prolonged symptoms after mild traumatic brain injury: an exploratory randomized clinical trial. J Head Trauma Rehabil, 2017; 32(2):79–89; doi: 10.1097/HTR.0000000000000238
53.
ChanC, IversonGL, PurtzkiJ, et al.Safety of active rehabilitation for persistent symptoms after pediatric sport-related concussion: a randomized controlled trial. Arch Phys Med Rehabil, 2018; 99(2):242–249; doi: 10.1016/j.apmr.2017.09.108
54.
SlobogeanGP, VermaA, GiustiniD, et al.MEDLINE, EMBASE, and Cochrane index most primary studies but not abstracts included in orthopedic meta-analyses. J Clin Epidemiology, 2009; 62(12):1261–1267.
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