Concussion is a brain injury caused by an impulsive biomechanical force transferred from the body to the brain.
Although most patients with concussion typically achieve symptomatic recovery within 2 weeks of injury, approximately 30% of patients may experience persistent symptoms. 1 Prognostic studies outline concussion-specific checklists measured at the acute phase of injury as the strongest and most consistent prognostic factor for time to recovery. 2,3 Other risk factors for delayed recovery include a prior history of concussion, learning disability, and psychological illness. 4–6 Exercise tolerance, which can be safely assessed clinically using a graded exercise tolerance test known as the Buffalo Concussion Treadmill test (BCTT), has more recently garnered attention as a possible prognostic factor for recovery in adolescents with sports-related concussion (SRC). 7–9 In a retrospective cohort study of 130 adolescents with SRC, reduced exercise tolerance measured by the BCTT during the acute phase (<10 days after injury) was associated with delayed clinical recovery in adolescents exposed to a regimen of rest, a regimen of placebo stretching, but not in those instructed to perform aerobic exercise at 80% capacity. Little is known about this relationship when the BCTT is performed outside of the acute phase of concussion (≥10 days after injury), because most studies to date have assessed candidate prognostic factors of concussion primarily during the acute phase of injury (<10 days after injury). 10,11 In addition, a large proportion of patients may seek care and perform a first BCTT outside of this acute phase window. 4,10,11
In general, there are 4 main objectives of prognostic research: (1) description; (2) association; (3) prediction; and (4) causation.
Studies that address questions relating to description, association, and prediction model development are described as exploratory. To examine the BCTT as a candidate prognostic factor for time to recovery during the subacute phase of SRC, we performed an exploratory prognostic study using a multidisciplinary network of community concussion-trained clinics across Canada. Our objective was to assess the associations between participant, injury, and clinical process characteristics, including exercise-intolerance on a first attempt BCTT performed 10 to 21 days after injury, and days to recovery in a clinical cohort of 12 children with SRC in Canada. METHODS
Study Design, Data Source, and Setting
We conducted a historical clinical cohort study using data from a network of approximately 150 primary care clinics (chiropractor, physician, physiotherapist) offering concussion clinical services. We reported this study according to the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement.
This nationwide study for 13 children and adolescents was approved by the office of research ethics of York University in Toronto, Canada (Ethics ID#: STU 2019-104) after delegated review and determination of minimal risk. All participants (athlete or their parent/guardian) provided informed consent for their de-identified health data to be used for research purposes upon entry into the clinical network.
The database is a proprietary electronic health record system (CCMI electronic medical record system, Complete Concussion Management Inc) used by healthcare providers who undergo additional training in concussion management to document standardized patient characteristics, physical examination findings, and outcomes.
Patients with concussion access this clinical network as first point of contact or through referral. Diagnosis of SRC is provided by a regulated healthcare professional (chiropractor, physician, and physiotherapist) according to the international Concussion in Sport Group criteria.
Patients progress through a concussion management strategy, which includes guideline-adherent return to learn and play processes. 1 In instances where recovery does not progress as expected (ie, symptomatic at-rest beyond 10 days postinjury), patient-specific rehabilitation programs are initiated in accordance with the respective domain of symptoms and through shared clinical decision-making between practitioner and patient. 1 PARTICIPANTS
Our study population was
children and adolescents (≤17 years) with SRC who had a first attempt BCTT between 10-21 days after their reported date of SRC injury and received health care within the concussion clinical network between 1 January 2016 and 11 April 2019. Clinicians participating within this clinical network were advised to perform a first BCTT on patients within 10 days of injury if they reported being asymptomatic at rest, and 10 days or later after injury if symptomatic at rest at initial or follow-up assessment. The 10-21-day criterion was chosen to include participants in the subacute phase of SRC who were primarily symptomatic at rest, but not yet classified as having persistent symptoms. Participants were excluded if they presented with (1) red flag symptoms (eg, severe or worsening headache, vomiting, deficits in short term memory for over 30 minutes, seizure, physical evidence of trauma above the clavicle) ; (2) history of attention deficit disorder (ADD), attention deficit hyperactivity disorder (ADHD), learning disorder, depression, anxiety, autism, sleep disorder, or more than 3 prior concussions, as these factors have been reported to be associated with delayed recovery 15 ; or (3) scored < 7 on concussion symptom severity at initial assessment (as normally developing adolescents may present with concussion-like symptoms). 7–9 16 Participant, Injury, and Clinical Process Characteristics
Participant characteristics included sex, age, and number of previous concussions. Injury characteristics included patient-reported loss of consciousness (LOC) at time of injury, presence and type of amnesia (retrograde or anterograde) at time of injury, sport mechanism of injury grouped by similarity in reported concussion incidence rates for each sport,
and symptom severity evaluation completed at initial visit. The symptom severity evaluation is a 22-item checklist, scored out of 132 points used to evaluate concussion characteristics, with lower scores representing reduced symptom severity. 17 Clinical process characteristics included days from injury to initial assessment and days from injury to first attempt BCTT. Treatment related variables included the number of clinical notes documented by the treating practitioner as a proxy for intensity of treatment, number of clinical notes that specified visual or vestibular therapy, and the total number of BCTTs performed (as targeted aerobic exercise can reduce the risk for persistent symptoms). 1 All data were collected at the time of care provision by the attending practitioner. 18 Buffalo Concussion Treadmill Test
The BCTT is a valid and reliable test used to assess exercise intolerance after SRC.
Before BCTT administration, concussion symptoms were measured on an 11-point numeric rating scale (NRS) and resting level of participant heart rate was measured. 10,19,20 The NRS asked participants to rate their overall condition on an 11-point scale from 0 to 10 (0 = feeling good, 10 = worst I have ever felt). Participants were then asked to walk on a treadmill starting at a speed of 3.2 mph at 0° incline. Treadmill incline was increased by 1° each minute for the first 15 minutes. After max incline, the treadmill speed was increased by 0.4 mph every minute. Heart rate, Borg Rating of Perceived Exertion (RPE), and symptom score on the NRS were recorded at each minute until symptom exacerbation or voluntary exhaustion. 21 Symptom exacerbation was defined as an increase of 3 or more points from the NRS taken at baseline. Maximal exertion was defined as achieving a score of ≥17 on the RPE. 21,22 Participants able to exercise to maximal exertion without concussion symptom exacerbation were deemed to be exercise-tolerant. 22 23 Main Outcome – Days from Injury to Recovery
The outcome, days from injury to recovery, was derived by calculating the difference between the patient-reported date of SRC injury and the date the patient was provided medical clearance and discharged. Recovery was defined as meeting the following 4 criteria: (1) exercise-tolerant disposition on BCTT completion; (2) successful completion of the Gapski-Goodman physical exertion test for concussion
; (3) assessment by regulated healthcare professional (chiropractor, physician, physiotherapist); and (4) completion of a stepwise return to play process. 24 1 Statistical Analysis
Participant, injury, clinical process, and treatment characteristics were summarized using descriptive statistics. Descriptive statistics were used to report participant, injury, clinical process, and treatment characteristics across BCTT disposition. Simple linear regression was used to assess the crude associations between each of the candidate prognostic factors and days to recovery (analyzed as a continuous variable). Hierarchical linear regression modelling was subsequently performed to assess the fit of 4 prespecified multivariable linear regression models based on clinical reasoning and our study objectives. Model 1 included participant characteristics only. Model 2 added injury and clinical process characteristics to model 1, with sport mechanism of injury providing information on differing recovery times by sports. Model 3 included the variables of models 1 and 2 combined, and the first attempt BCTT result (exercise-intolerant vs exercise-tolerant as the referent). Model 3 was specified a priori as the primary model of interest. Finally, model 4 included models 1, 2, and 3 variables, and treatment-related variables to further understand what management techniques patients in this cohort received. The Akaike Information Criterion was used to assess fit across the 4 multivariable models. Model 3 showed the best fit of all models without treatment-related variables included, whereas model 4 showed the best fit overall. Linearity of data was checked by inspecting residuals versus fitted values, a scale location plot was used to assess for homoscedasticity of residuals, and multicollinearity was checked by the Variance Inflation Factor. Beta coefficients, 95% confidence intervals (CIs), and R
2 values were reported for all linear regression analyses. Analyses were performed using R (Version 4.2.0). P values and 95% CIs were 2-sided and P values ≤0.05 were considered statistically significant. RESULTS
Between 1 January 2016 and 11 April 2019, 6052 candidate patient records (≤17 years) were identified in the study database as having received a concussion diagnosis after assessment at a participating clinic. After applying the study inclusion and exclusion criteria, the eligible study population consisted of 855 patients (
Figure 1). Figure 1.:
Participant inclusion flow diagram and reasons for exclusion. * May have presented with more than 1 reason for exclusion. ADD: Attention deficit disorder; ADHD: Attention deficit hyperactivity disorder; BCTT: Buffalo concussion treadmill test;
n: Number; SRC: Sport-related concussion; y: Years.
The study sample was primarily male, with an average age of 14 years (range 6-17 years). Most participants reported no prior concussion history and no loss of consciousness or amnesia with injury. First attempt BCTT was performed on average 14 days after the recorded date of injury. Participants took on average 32 days to achieve recovery (median, 25 days). Overall, 684 (80%) participants were rated as exercise-tolerant based on their first attempt BCTT, whereas 171 (20%) were rated as exercise-intolerant. Exercise-tolerant participants had an average resting heart rate (HR) measurement of 85.0 beats per minute (BPM) measured before their first BCTT attempt and had an average maximal HR of 164.1 BPM during the BCTT. In contrast, exercise-intolerant participants had an average resting HR of 85.3 BPM, with an average maximal HR of 146.9 BPM during the BCTT.
Table 1 provides participant characteristics.
TABLE 1. -
Characteristics of Study Population by First-Attempt BCTT Result (
All Participants (
n = 855) BCTT Exercise- Tolerant (
n = 684) BCTT Exercise- Intolerant (
n = 171)
Age in yr, median (IQR)
14.0 (13, 16)
14.0 (13, 16)
14 (13, 15)
n (%) 480 (56.1)
n (%) 375 (43.9)
Prior concussion history
Number of previous concussions, mean (SD)
n (%) 475 (55.6)
n (%) 380 (44.4)
Loss of consciousness with injury
n (%) 804 (94.0)
n (%) 51 (6.0)
Amnesia with injury
n (%) 710 (83.0)
n (%) 75 (8.8)
n (%) 70 (8.2)
Sport mechanism of injury
n (%) 394 (46.1)
n (%) 128 (15.0)
n (%) 152 (17.8)
n (%) 54 (6.3)
n (%) 127 (14.8)
Symptom severity score, median (IQR)
27.0 (16, 40)
27 (16, 40)
30 (19, 40)
Clinical process characteristics
Days from injury to assessment, median (IQR)
4.0 (3, 7)
4.0 (2, 7)
5.0 (3, 9)
Days from injury to 1st BCTT attempt, median (IQR)
13.0 (11, 17)
13.0 (11, 17)
14 (12, 17)
Number of clinical notes on record, mean (SD)
Number of clinical notes with visual or vestibular therapy specified, mean (SD)
Number of BCTT's performed, mean (SD)
Heart rate measurements
Resting heart rate in BPM, mean (SD)
Maximal heart rate during BCTT in BPM, mean (SD)
First BCTT result
n (%) 684 (80.0)
n (%) 171 (20.0)
Time to clinical recovery, mean (SD)
Time to clinical recovery, median (IQR)
25 (19, 33)
24.0 (19, 31)
33.0 (26, 49)
BCTT: Buffalo concussion treadmill test; n: number; y: yr.
Prognostic Factors Analysis
Table 2 provides results of the hierarchical linear regression analysis (see supplementary table 1, for unadjusted estimates of participant, injury, and clinical process characteristics, and the BCTT result as candidate prognostic factors and their crude associations with days to recovery). Model 1, which included only participant characteristics, explained 2.5% of the variation in days to recovery after SRC (R https://links.lww.com/JSM/A368 2 = 0.025). Model 2, including participant, injury, and clinical process characteristics, explained 7.3% of the variation in days to recovery (R 2 = 0.073). Model 3, which added the first attempt BCTT result to model 2, explained a total of 11.3% of the variability in days to recovery (R 2 = 0.113, R 2 change between models 2 and 3 = 0.04). After adjusting for participant, injury and clinical process characteristics, exercise-intolerance, as measured by a first attempt BCTT, was associated with an increased 13 days to recovery (95% CI = 9.1-17.5 days) compared with exercise-tolerance. Each additional concussion was associated with an increase of 3 days to recovery (95% CI = 0.8-4.9). Each additional day between SRC injury and first attempt BCTT was associated with a prolongation of recovery by 1 additional day (95% CI, 0.07-1.9 days).
TABLE 2. -
Associations Between Participant, Injury, Clinical Process, and Treatment Characteristics and Days to Recovery in
With SRC (
Model 1. Participant Characteristics
Model 2. Model 1 + Injury + Clinical Process
Model 3. Model 2 + BCTT Result
Model 4. Model 3 + Treatment
Unstandardized ß (SE)
Unstandardized ß (SE)
Unstandardized ß (SE)
Unstandardized ß (SE)
0.2 to 1.9
−0.1 to 1.6
−0.1 to 1.5
−0.3 to 1.3
0.5 to 7.5
−2.4 to 5.2
−2.7 to 4.8
−3.3 to 3.8
Number of previous concussions
1.0 to 5.3
1.2 to 5.4
0.8 to 4.9
0.8 to 4.8
Loss of consciousness with injury
−12.7 to 2.1
−12.7 to 1.8
−12.9 to 1.1
Amnesia with injury
−3.9 to 8.3
−3.5 to 8.5
−2.5 to 9.0
−3.0 to 9.8
−2.9 to 9.6
−1.3 to 10.8
Sport mechanism of injury
−5.1 to 5.0
−5.3 to 4.7
−4.7 to 4.9
−2.6 to 7.1
−4.0 to 5.6
−3.7 to 5.5
1.2 to 16.2
−1.2 to 13.7
−2.0 to 12.3
−1.6 to 8.7
−2.3 to 7.8
−1.9 to 7.9
Symptom severity score
0.1 to 0.2
0.0 to 0.2
0.0 to 0.1
Days from injury to initial assessment
−0.4 to 0.6
−0.5 to 0.4
−0.2 to 0.8
Days from injury to 1
st BCTT attempt
0.7 to 1.8
0.7 to 1.9
0.2 to 1.3
First BCTT result
9.1 to 17.5
1.3 to 12.0
Number of clinical notes on record
2.3 to 4.1
Number of clinical notes with visual or vestibular therapy specified
−0.9 to 1.8
Number of BCTT's performed
−2.5 to 6.3
*Model specifications for the impact of candidate prognostic factors for days to recovery in children with SRC with adjustment.
Numbers in bold indicate estimates found to be statistically significant with a
P value < 0.05.
BCTT, Buffalo concussion treadmill test; ref, reference; y, yr
Model 4 added treatment characteristics to model 3. This model explained 18% of the variation in days to recovery (R
2 = 0.177). In this model, first attempt BCTT exercise-intolerance was associated with an increase of 7 days to recovery (95% CI = 1.3-12.0) when compared with those deemed to be exercise-tolerant as measured by the BCTT. DISCUSSION
In this exploratory prognostic study of 855
children with SRC, we found that prior history of concussion, exercise intolerance on a first attempt BCTT (preformed 10-21 days after injury), and increased time from injury to first BCTT attempt were associated with prolonged recovery. However, the result of a first attempt BCTT at 10 to 21 days postinjury alone was not a remarkably strong prognostic factor for time to recovery. First Attempt BCTT as a Candidate Prognostic Factor during the Subacute Phase
Previous work has primarily focused on the BCTT as a candidate prognostic factor of recovery when performed during the acute phase of concussion.
Haider et al, assigned 130 adolescents <10 days after concussion to a regimen of rest, light stretching, or aerobic activity for 4 weeks. Participant BCTT result in each group was measured as the difference between resting HR and the average HR over the final minute of the BCTT (Δ HR). Participant Δ HR was shown to explain 22.8% variation in clinical recovery within the rest group, 12.6% variation in the light stretch group, and 5.9% variation within the aerobic activity group. 10,11 Participant Δ HR on the BCTT was shown to be associated with duration of clinical recovery in participants randomized to the rest and light stretching groups. Leddy et al 11 showed similar results in 27 adolescents who performed the BCTT 1 to 10 days after SRC. Participants with a higher average heart rate during the last minute of the BCTT were associated with shorter recovery time. Our study expands on these findings by (1) use of a dichotomous BCTT prognostic factor measurement (exercise-tolerant vs intolerant), rather than Δ HR; (2) use of a nonacute concussion sample performing the BCTT (10-21 days after injury, compared with <10 days); (3) recovery definition which includes the ability to exercise to maximal exertion without symptom exacerbation, assessment by a regulated healthcare professional, and completion of a stepwise return to play process 10 ; and (4) expanding to a study population outside of specialized sports medicine settings by including a diverse group of primary care practice clinicians and patients across Canada. However, a more diverse study population likely introduces additional unexplained variance and can strongly influence R 1 2 estimates, making it more difficult to assess predictive capacity of the candidate prognostic factors on outcome because of imprecision. 25 Participant, Injury, and Clinical Process Characteristics
The literature surrounding previous concussion history as a prognostic factor for delayed recovery remains mixed. A 2017 systematic review on predictors of clinical recovery after concussion reported most included studies did not show a relationship between prior history and clinical outcome.
However, quality assessment on included studies was not performed. In comparison, a 2014 systematic review of prognosis and return to play after SRC reported delayed recovery time was more likely in participants with a history of previous concussion. 4 In this review, only 46% of eligible articles were included in the evidence synthesis after quality assessment, none of which were described as phase 3 (hypothesis confirmatory) studies (only phase 1 and phase 2 exploratory studies were identified). 26 These differing results highlight the large amount of heterogeneity and a lack of high-quality confirmatory prognostic studies within the field of SRC. Nonetheless, previous concussion history is an important candidate prognostic factor because it is associated with increased symptom reporting in athletes and is a risk factor for sustaining a subsequent concussion. 26 In a child and adolescent population returning to sport, it is likely that such factors result in more conservative clinician decision-making, thereby delaying final recovery date. 27,28
Exercise has been found to have a dose-dependant relationship in patients with concussion because excessive exercise and exercise restriction may lead to poor clinical outcomes.
In 2 randomized trials, early (<10 days after injury) targeted subsymptomatic aerobic exercise was reported to reduce the risk of developing persistent postconcussion symptoms in adolescents when compared with stretching programs. 29 In light of such results, our findings of delayed recovery in 18,30 children with a greater duration between injury and initiation of targeted aerobic exercise (first attempt BCTT) may be an indicator of late therapeutic exercise prescription. STRENGTHS AND LIMITATIONS
This study has several strengths. First, a large number participants were recruited from diverse primary care settings across Canada which enhances generalizability of findings. To our knowledge, this is the largest study examining the prognostic value of the BCTT on recovery time after SRC. Second, clinicians participating in this network had additional training to help standardize methods and diagnostic criteria. Third, we were able to adjust for a large number of clinically relevant prognostic factors in a stepwise fashion.
Our study has several limitations. First, participants lost to follow-up or without complete recovery were excluded from this study. It is possible that the profile of these individuals may have differed from those who fully completed their treatment plan, and this may have led to selection bias. Second, participants in our study received concussion care, which may have had an effect on exercise tolerance/intolerance at the time of first attempt BCTT, and time to recovery. This may have been a possible source of confounding, mediation, or both, that is difficult to disentangle. Third, we acknowledge the possibility of detection bias, as clinicians were not masked to the first BCTT result in our highly pragmatic study. Clinician knowledge may have affected subsequent treatment recommendations, speeding up or slowing down participant progression toward recovered status. Fourth, practitioners included in the primary-care clinical network come from a variety of disciplines (chiropractor, physician, physiotherapist). This may affect the generalizability of our results because patients with access to these clinicians are more likely to be included in this study.
This study found that exercise-intolerant
children and adolescents, identified by a first attempt BCTT performed 10 to 21 days after injury, showed increased days to recovery when compared with those who were exercise-tolerant. Previous history of concussion and longer delay between injury and first BCTT attempt were also associated with delayed recovery. These candidate prognostic factors should be examined in future confirmatory prognostic studies which may lead to greater clinical utility during assessment of SRC. References
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