Abstract
Background:
The Buffalo Concussion Treadmill Test (BCTT) is a graded exertion test for assessing exercise tolerance after concussion, but its utility is limited for certain populations.
Hypothesis:
We developed the Buffalo Concussion Bike Test (BCBT) and tested its comparability with the BCTT. We hypothesize that heart rate (HR) at symptom exacerbation on the BCBT will be equivalent to the BCTT.
Study Design:
Case-control study.
Level of Evidence:
Level 3.
Methods:
Adolescents with acute concussion (AC) (n = 20; mean age, 15.9 ± 1.1 years; 60% male) presenting to a concussion clinic within 10 days of injury and age- and sex-matched healthy controls (n = 20; mean age, 15.9 ± 1.1 years; 60% male) performed the BCTT at first visit and returned within 3 days to perform the BCBT. Test duration, HR, symptom severity (measured using a visual analog scale), and exertion (measured using the Borg Rating of Perceived Exertion) were collected during each test.
Results:
Adolescents with AC who were exercise intolerant on the BCTT were also intolerant on the BCBT, with symptom exacerbation occurring at a mean 8.1 ± 2.8 minutes on the BCTT versus 14.6 ± 6.0 minutes on the BCBT (P < 0.01). Two 1-sided t tests showed that the HR at symptom exacerbation in AC patients (137 ± 28 bpm on BCTT vs 135 ± 25 bpm on BCBT; 95% CI, <0.01-0.03) and at voluntary exhaustion for controls (175 ± 13 bpm on BCTT vs 175 ± 13 bpm on BCBT; 95% CI, 0.03-0.03) on each test were statistically equivalent.
Conclusion:
The HR at symptom exacerbation on BCBT is equivalent to the BCTT for the assessment of exercise tolerance after concussion in adolescents.
Clinical Relevance:
The BCBT can be used in patients with limited mobility or for research interventions that require limited participant motion.
Keywords
The incidence of concussion, a subtype of mild traumatic brain injury, is high in contact sports and recreational activities.17,27 Concussion is the result of sudden linear and/or rotational forces applied to the brain that trigger an acute and subacute pathophysiological cerebral metabolic response in the absence of gross structural changes to the brain.1,26 Concussion diagnosis and management are based largely on patient-reported symptoms. 12 In addition to symptoms reported at rest, athletes who experience sport-related concussion (SRC) often report that symptoms become worse on physical exercise. This “symptom-limited exercise intolerance” is defined as the inability to exercise to the level of one’s physical fitness due to exacerbation of concussion symptoms. Exercise intolerance after concussion may be related to abnormal autonomic nervous system function2,16 that contributes to impairments of cerebral blood flow 5 and/or alters cardiac function during exercise. 16 Exercise intolerance has been reported in patients with persistent postconcussive symptoms 15 as well as in adolescents within days of head injury. 23 The evaluation of exercise tolerance after concussion may therefore offer a more objective and physiologically based standard to help clinicians diagnose and manage concussion better than symptoms alone. This is especially important for concussion management in athletes since they are known to under-report symptoms, 4 and many of the symptoms reported after head injury are not specific to concussion. 19
The Buffalo Concussion Treadmill Test (BCTT) is a graded exertion test that establishes the heart rate (HR) at which exercise-induced symptom exacerbation occurs after concussion. 24 It is an effective tool for diagnosing and managing concussions, as well as making the decision for return to play.21,24 A recent randomized controlled trial demonstrated that it was safe to use within the first week after concussion in adolescents, provided that the stopping criterion of symptom exacerbation was followed. 23 The BCTT, however, has limitations for certain patients and research protocols. For instance, orthopaedic injuries or significant balance problems may preclude participants from safely exercising on a treadmill, and it is difficult to do a variety of physiological tests during treadmill exercise because of excessive body movement. The purpose of this study was to introduce the Buffalo Concussion Bike Test (BCBT), developed to assess exercise tolerance in patients with concussion or participants for whom treadmill testing is difficult or contraindicated. We hypothesized that acutely concussed participants with symptom exacerbation during the BCTT would also have symptom exacerbation during the BCBT, and that the HR achieved at symptom exacerbation or voluntary exhaustion on the BCTT and BCBT would be statistically equivalent.
Methods
Approval for this study was obtained from the State University of New York at Buffalo Institutional Review Board. We estimated the oxygen consumption (VO2) achieved during each stage of the BCTT using the American College of Sports Medicine (ACSM) metabolic equations. 10 We then calculated the power output on a cycle ergometer that would be required to elicit 90% of the estimated VO2 for each stage of the BCTT. This was done because graded exercise tests performed on a cycle ergometer typically elicit maximum VO2 values that are lower than those achieved on a treadmill yet elicit similar HR at maximal exercise.7,13 We compared (1) HR, (2) concussion symptom severity using a visual analog scale (VAS), and (3) perceived exertion using the Borg Rating of Perceived Exertion (RPE) 3 between the BCTT and BCBT.
Study Design
This matched case-control study is part of a larger study on the physiology of concussion. Participants with acute concussion (AC) were sequentially recruited from the Concussion Management Clinic at the initial visit after injury. A sports medicine physician diagnosed the concussion based on history (including a cognitive and behavioral screen), 11 a concussion-specific symptom checklist, 14 a concussion-relevant physical examination, 18 and exertion testing on the BCTT. Once a potential participant was diagnosed with concussion, the research team explained the study, determined eligibility, and obtained consent/assent. Participants were asked to return to the clinic within 3 days to perform the BCBT. We chose this time frame because our goal was to test patients using the BCBT while they were still symptomatic. Since the BCTT is done as part of our routine clinical practice, the order of the exercise tests was not randomized. AC patients were instructed not to perform any physical activity/sport as part of their concussion management during the 3 days after injury.
Age- and sex-matched healthy controls were recruited from the same source population as those with AC, that is, local high schools and sports teams. The study was explained, and consent/assent was obtained. Control subjects came to the research center for a physical examination and performed the BCTT at their first visit, and then returned to perform the BCBT within 3 days. Controls were instructed not to perform any intense physical activity and/or play sports on the days of their study visits. Study participants and research personnel were not blinded to the results of the tests.
Participants
Inclusion criteria for AC patients were (1) physician-diagnosed SRC, (2) 13 to 18 years old, (3) ability to perform both tests within 14 days of injury, and (4) ability to perform the BCBT within 3 days of the BCTT. Exclusion criteria for AC patients were (1) unwilling to exercise; (2) currently on medications that would affect HR, for example, mood disorder and/or learning disorder medications or beta blockers; (3) focal neurologic deficit on physical examination or imaging; and (4) orthopaedic injury that would represent a significant risk on the treadmill or bike. Inclusion criteria for control subjects consisted of (1) no history of concussion within the past 1 year, (2) age 13 to 18 years, (3) ability to perform all tests within 3 days, and (4) participation in at least 1 organized sport (to control for cardiovascular fitness). Exclusion criteria for controls were identical to AC patients.
Calculation of Gross VO2
Using the ACSM walking equation, 10 we estimated VO2 for each stage of the BCTT:
where VO2 is the gross oxygen consumption in mL·kg−1·min−1, S is the speed in m·min−1, and G is the percentage elevation grade on the treadmill expressed as a fraction.
To calculate the power output needed to elicit 90% of the estimated VO2 from each stage of the BCTT, we used the ACSM leg cycling equation. 10 First, we used the following equation to determine the work rate in kg·m·min−1 at each stage that would elicit the equivalent estimated VO2 during the same stage of the BCTT.
where VO2 is the estimated gross oxygen consumption in mL·kg−1·min−1 from the corresponding stage of the BCTT and BM is the body mass (kg).
We then converted work rate to watts by multiplying by 0.164. 10 Finally, we multiplied this value by 90% because graded exercise tests performed using cycle ergometers elicit maximal VO2 values that are lower than exercise tests performed on a treadmill. 7 Importantly, however, graded exercise tests performed on cycle ergometers elicit maximal HRs that are not different than those achieved during treadmill exercise tests. 13
Exercise Test Protocols
Buffalo Concussion Treadmill Test
Participants walked on a level treadmill at 3.2 mph at 0° incline (3.6 mph if participant was 5 ft 10 in and taller). 24 Each stage on the treadmill was 1 minute. The incline was increased by 1 degree after each minute for the first 15 minutes, and then the speed was increased by 0.4 mph every minute thereafter. HR (assessed using a Polar HR monitor, Model #FIT N2965), VAS, and RPE were recorded at the end of each stage until symptom exacerbation or voluntary exhaustion, followed by a cooldown period at 2 mph for 2 minutes. Symptom exacerbation was defined as an increase of 3 points or more from the pre-exercise VAS value (a point or more for an increase in symptoms and a point for appearance of a new symptom). Voluntary exhaustion was defined as a value of ≥17 on the RPE scale. Participants were instructed to report symptoms and not to push through them. An examiner also observed for visible signs of distress, which may prompt test cessation.
Buffalo Concussion Bike Test
Participants exercised on a cycle ergometer (LODE Corival Recumbent stationary bike) at 60 rpm (±5) at a specific resistance based on body mass. Each stage on the cycle ergometer was 2 minutes. The participant was told to maintain 60 rpm while the resistance was increased every 2 minutes based on the above formula. HR, VAS, and RPE were recorded at the end of each stage until voluntary exhaustion or symptom exacerbation, followed by a 2-minute cooldown at the first stage resistance at 30 rpm. Test stopping criteria were identical to the BCTT. A complete manual for the BCBT is provided in a supplementary file (Appendix 1, available in the online version of this article).
Statistical Analysis
Analysis of variance was used for group differences in age and body mass index; a Kruskal-Wallis test (nonparametric) was used for differences in days between exercise tests; and a chi-square test was used for group differences in sex, prior concussions, and number of stages achieved in each test. Mean HR with 95% CI was calculated at each stage for AC patients and controls. Mean VAS with 95% CI was calculated at each stage for AC patients. Upper and lower confidence limits and 2 one-sided t tests (TOSTs) using 90% CI (1 − 2α) were used to test for equivalence in HR and VAS in AC patients for each exercise test at symptom exacerbation or voluntary exhaustion. Only maximum HR was compared in controls at voluntary exhaustion. A P value of <0.05 was considered statistically significant. Statistical analysis was performed using SPSS v24 (SPSS).
Results
Twenty-four acutely concussed patients consented to the study and performed the BCTT at their initial clinic visit, but 4 participants could not return to perform the BCBT within 3 days so they were excluded. Hence, 20 participants comprised the AC group. Mean time since injury and the BCTT visit was 5.6 ± 2.8 days. Twenty age- and sex-matched athletic, healthy subjects comprised the control group. There were no dropouts in the control group. AC patients and controls did not statistically differ in age, sex, body mass index, or prior number of concussions (Table 1). AC patients performed the cycle ergometer test 1.9 ± 0.9 days after the treadmill test, and controls performed it 3.1 ± 1.3 days after, which was significantly different than those with AC (P < 0.01).
Participant demographics a
—, not applicable.
Data presented as mean ± SD unless otherwise indicated.
AC Group
AC patients exercised a mean of 8.1 ± 2.8 stages (8.1 ± 2.8 minutes) on the treadmill and 7.3 ± 3.0 stages (14.6 ± 6.0 minutes; P < 0.01) on the cycle ergometer. All except 1 AC patient ended the BCTT due to symptom exacerbation. The participant who did not have symptom exacerbation on the treadmill also did not have symptom exacerbation on the cycle ergometer. TOST showed that both tests exacerbated concussion symptoms at a statistically equivalent HR (137 ± 28 bpm on BCTT vs 135 ± 25 bpm on BCBT; 95% CI, <0.01-0.03). Symptom severity at symptom exacerbation was not statistically equivalent (4.5 ± 1.7 on BCTT vs 4.4 ± 1.8 on BCBT; 95% CI, 0.02-0.06). Maximal exertion RPE was not equivalent on the treadmill and cycle ergometer (13.6 ± 1.8 vs 12.3 ± 2.5; 95% CI, <0.01-0.77). Figures 1 and 2 present mean HR and VAS values over the first 10 stages for each test. Mean values for subsequent stages are not presented because the majority of participants did not reach them.
Mean heart rate (HR) in patients with acute concussion (AC) at each stage of Buffalo Concussion Treadmill Test and Buffalo Concussion Bike Test with 95% CIs. No significant differences were found at each stage.
Mean symptom severity (visual analog scale [VAS; range, 0-10]) in patients with acute concussion (AC) at each stage of Buffalo Concussion Treadmill Test and Buffalo Concussion Bike Test (BCBT) with 95% CI. **95% CI for BCBT on stage 10 is −5.39 to 12.06 (n = 3). No significant differences were found at each stage.
Control Group
Control subjects exercised a mean of 15.8 ± 2.1 stages (15.8 ± 2.1 minutes) on the treadmill and 13.6 ± 2.6 stages (27.2 ± 5.2 minutes; P < 0.01) on the cycle ergometer. TOST showed that both tests were statistically equivalent in HR achieved on the treadmill and cycle ergometer at maximal exertion (175 ± 13 vs 175 ± 13 bpm, UCL = 0.03, LCL = 0.03). Control subjects did not report any concussion symptoms during either test (VAS, 0). Figure 3 presents mean HR values over the first 15 stages for both tests. Mean values for subsequent stages are not presented because the majority of participants did not reach them.
Mean heart rate in healthy control subjects (HC) at each stage of Buffalo Concussion Treadmill Test and Buffalo Concussion Bike Test with 95% CIs. No significant differences were found at each stage.
Discussion
Our findings confirm that the HR at symptom exacerbation achieved on the BCBT is equivalent to the BCTT, making it a comparable tool for the assessment of exercise tolerance in adolescents in the acute stage after concussion. All the concussed participants who were symptomatic on the treadmill were also symptomatic on the cycle ergometer. The data show that symptom exacerbation on the BCBT in recently injured adolescent athletes was reached at an equivalent HR to the BCTT. This is important because 80% to 90% of HR at symptom exacerbation is used to prescribe a subsymptom threshold aerobic exercise treatment program to help patients recover from concussion and perhaps prevent protracted recovery.20,22 It was important to demonstrate that the BCBT can be a clinically useful tool to assess exercise intolerance after concussion since some patients have limited mobility as a result of premorbid conditions or orthopaedic injuries, or they may have significant vestibular dysfunction, preventing safe usage of the treadmill. Moreover, for research purposes, many cardiovascular and cerebrovascular measurements are typically easier to obtain on a cycle ergometer because of the relative stability of the head and torso when compared with treadmill exercise. The maximal HR achieved by control participants on the BCBT was almost identical to the BCTT, indicating that the BCBT can also be used to determine whether a patient is exercise tolerant after recovery, thus effectively performing the first 2 stages of the standard return-to-play strategy recommended by the most recent international Concussion in Sport group consensus conference. 25
The BCBT differs from the BCTT in several aspects. It takes almost twice as long to perform the bike test because each stage on the bike is 2 minutes versus 1 minute on the treadmill. This modification was required because it takes longer to reach a physiological steady state on a cycle ergometer versus a treadmill.8,9 We reduced the absolute workload for each bike stage by 10% from the treadmill because pilot participants reached leg muscle exhaustion well before their age-predicted maximal HR, which has been reported in another study of stationary cycling versus treadmill running in 300 healthy males. 6 Graded exercise tests performed on a cycle ergometer typically elicit maximum VO2 values that are lower than those achieved on a treadmill yet elicit similar HR at maximal exercise.7,13 The BCBT may be a safer test of exercise tolerance after concussion than the BCTT because cycling does not stimulate the vestibular system as much as running and the patient is less likely to fall while seated.
The primary limitation to our study is that the order of the tests was not randomized. The BCTT is used as part of our clinical management so it was performed first. There was also a 2-day interval between the tests during which the autonomic nervous system in concussed participants could have partially recovered. Nevertheless, the BCBT was a robust enough test to exacerbate symptoms at a statistically equivalent HR to the BCTT. Finally, the HR response to exercise may be affected by a variety of factors, such as mood, food intake, time of day, and environment. These factors were not controlled for.
Conclusion
The BCBT, when performed on a cycle ergometer with adjustable resistance, takes longer to perform than the BCTT but elicits symptom exacerbation at a statistically equivalent HR to the BCTT. The BCBT appears to be a valid physiological test for the clinical evaluation of exercise tolerance after acute concussions and may be especially useful for patients with limited mobility.
Supplemental Material
Buffalo_Concussion_Bike_Test_Manual – Supplemental material for The Buffalo Concussion Bike Test for Concussion Assessment in Adolescents
Supplemental material, Buffalo_Concussion_Bike_Test_Manual for The Buffalo Concussion Bike Test for Concussion Assessment in Adolescents by Mohammad N. Haider, Samantha L. Johnson, Rebekah Mannix, Alexander J. Macfarlane, Dylan Constantino, Blair D. Johnson, Barry Willer and John Leddy in Sports Health: A Multidisciplinary Approach
Footnotes
Acknowledgements
We thank Dr Andrea Hinds, PhD, for her assistance with participant recruitment and data collection.
The authors declared the following potential conflicts of interest: The University at Buffalo received support for this study from the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under award number 1R01NS094444 and from the National Center for Advancing Translational Sciences of the National Institutes of Health under award number UL1TR001412.
References
Supplementary Material
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