Journal of the Neurological Sciences 354 (2015) 46–50
Contents lists available at ScienceDirect
Journal of the Neurological Sciences journal homepage: www.elsevier.com/locate/jns
Is it safe to drive after acute mild stroke? A preliminary report☆ Megan A. Hird a,b, Kristin A. Vesely a,b, Leah E. Christie b,d, Melissa A. Alves b,d, Jitphapa Pongmoragot d, Gustavo Saposnik a,c,d, Tom A. Schweizer a,e,f,⁎ a
Neuroscience Research Program, Keenan Research Centre for Biomedical Science of the Li Ka Shing Knowledge Institute, St. Michael's Hospital, Toronto, Ontario, Canada University of Toronto,Toronto, Ontario, Canada Stroke Research Unit, Mobility Program, St. Michael's Hospital, Toronto, Ontario, Canada d Medicine, St. Michael's Hospital, Toronto, Ontario, Canada e Department of Surgery, Neurosurgery Division, University of Toronto, Toronto, Ontario, Canada f Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, Ontario, Canada b c
a r t i c l e
i n f o
Article history: Received 19 January 2015 Received in revised form 7 April 2015 Accepted 27 April 2015 Available online 2 May 2015 Keywords: Acute Mild stroke Ischemia Driving Driving simulation Assessment
a b s t r a c t Background: Most guidelines recommend that patients should refrain from driving for at least one month after stroke. Despite these guidelines, and the fact that patients post-stroke may be at an increased risk for driving impairment, many patients report resuming driving within the acute phase of injury. The aim of this study was to investigate the driving performance of patients with acute mild stroke. Methods: The current study compared the driving simulator performance of ten patients with acute mild ischemic stroke (N 48 h and b 7 days) to that of ten healthy, age- and education-matched controls. Results: During the City Driving and Bus Following Scenarios, patients on average committed over twice as many errors (e.g., collisions, center line crossings, speed exceedances) as controls (12.4 vs. 6.0, t(18) = 2.77, p b 0.01; and 8.2 vs. 2.1, t(17) = 2.55, p b 0.05; respectively). Although there was no difference between patients and controls in the number of errors committed during simple right and left turns, patients committed significantly more errors than controls during left turns with traffic (0.49 vs. 0.26, U = 26.5, p b 0.05). Conclusion: Results suggest that patients with acute mild ischemic stroke may be able to maintain driving performance during basic tasks (e.g., straight driving, right turns) and that deficits may become apparent during more complex tasks (e.g., left turns with traffic, bus following). The results highlight the importance of healthcare professionals providing driving advice to their patients post-stroke, particularly in the acute phase of injury. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Evaluating the driving performance of patients after a stroke is a significant challenge for health professionals [1]. Many of the impairments associated with stroke, such as visual field defects, neglect, and paralysis are fairly reliable contraindications of driving ability. However, in cases of minor stroke where impairments are more subtle, such as deficits in executive functioning [2], evaluating driving performance can be much more challenging. Physician guidelines established by prominent governing bodies including the Canadian Medical Association (CMA) [3] and the Driver and Vehicle Licensing Agency (DVLA) [4] state that patients should refrain from driving for a minimum of one month after stroke. When in place, driving guidelines typically capture the window in which stroke and transient ischemic attack (TIA) patients are at an increased risk of
☆ Drs. Saposnik and Schweizer equally contributed to qualify as senior authors. ⁎ Corresponding author at: Keenan Research Centre for Biomedical Science of the Li Ka Shing Knowledge Institute, St. Michael's Hospital, 30 Bond Street, Toronto, Ontario M5B 1W8, Canada. Tel.: +1 416 864 6060x77342. E-mail address: [email protected] (T.A. Schweizer).
http://dx.doi.org/10.1016/j.jns.2015.04.043 0022-510X/© 2015 Elsevier B.V. All rights reserved.
recurrence. Patients are often allowed to resume driving if (1) no significant motor, cognitive, or perceptual deficits are present; (2) there is no significant risk of sudden recurrence; (3) the underlying cause of the stroke has been treated; and (4) the patient did not experience a poststroke seizure [5]. Despite these guidelines, and the fact that cognitive deficits are present in the acute phase of injury and can persist several months after injury [6], approximately 35% of minor stroke and TIA patients resume driving within the one-month period [7]. Furthermore, as low as 9% of patients report receiving driving advice from a physician immediately post-stroke [7]. This number increases to 52% of patients receiving driving advice when other healthcare professionals as well as friends and family are included in addition to physicians [8]. There is a paucity of empirical research that has investigated the driving performance of patients immediately after mild stroke. Thus, it remains unclear whether driving within the acute phase of recovery after minor stroke represents a significant safety risk for the patient and the general public. The current study used driving simulator technology to characterize the driving performance of acute mild stroke patients and to compare their performance to that of age- and educationmatched, healthy adults. Given that patients presented with mild deficits, it was hypothesized that stroke patients would maintain
M.A. Hird et al. / Journal of the Neurological Sciences 354 (2015) 46–50
driving performance during more routine aspects of driving (i.e., straight driving, right and left turns without traffic), which require fewer brain resources; however, patients would exhibit more errors in general as well as during the more demanding aspects of driving (i.e., left turns with traffic), which require greater recruitment of brain resources [9]. 2. Materials and methods 2.1. Participants Twenty participants were included in the study (acute stroke, n = 10; controls, n = 10). All patients were diagnosed and consecutively recruited by members of the Stroke Assessment and Treatment Team (SATT) at St. Michael's Hospital, including stroke neurologists, a physiotherapist, and an occupational therapist. Patients sustained a stroke within one week of testing (range = 2–7 days) and presented with minimal language and motor deficits (see Table 1 and Fig. 1). Patients were required to meet the vision standards outlined by the CMA (i.e., visual acuity no less than 20/50 with both eyes open and examined together, visual field of 120° continuous along the horizontal meridian and 15° continuous above and below fixation with both eyes open and examined together, and no diplopia within the central 40° of primary gaze) [3]. Visual screening was conducted by a stroke neurologist and an occupational therapist, and if there was any indication of visual impairment, patients received a comprehensive visual assessment. Patients with a neurological deficit (e.g., moderate to severe weakness, neglect, severe visual impairment, or ataxia) or a history of dementia were excluded. AlphaFIM® scores were N 80 (mean = 109.6 ± 6.7) and the National Institutes of Health Stroke Scale (NIHSS) scores were b 5 (mean = 1.2 ± 1.4), indicating mild impairment [10]. AlphaFIM® is a standardized measure of assessing functional status and disability in
47
the acute care setting and contains four motor tasks (e.g., bed-to-chair transfer, walking, bowel management, toilet transfer) and two cognitive tasks (e.g., expression and memory), scored on a seven-point scale (1 = “total assistance” and 7 = “complete independence”) [11]. All healthy control participants were recruited from volunteers in the local community and had no prior history of psychiatric or neurological illness. All participants held a valid driver's license at the time of testing. Self-reported years of driving experience and number of collisions are reported in Table 2. Ethical approval for the study was obtained by the Research Ethics Board at St. Michael's Hospital in Toronto, Canada. All participants provided written informed consent prior to their inclusion in the present study. 2.2. Procedure 2.2.1. Primary outcome: driving simulation The driving performance of participants was assessed using a STISIM Drive® (version 2.08.08, Logitech G25 model) driving simulator, equipped with a fully functioning steering wheel, pedals, and signaling system. Participants first completed a training session to become familiar with the simulator environment. Two experimental driving scenarios were administered: (1) City Driving Scenario and (2) Bus Following Scenario. The City Driving Scenario involves straight driving, routine right and left turns, and left turns with traffic. In conditions with higher cognitive demands (i.e., left turns with traffic), participants need to make decisions about when it is safe to turn in order to avoid oncoming traffic and pedestrians. These decisions are associated with processes of selective attention, visual–spatial ability, and motor control [9]. In the Bus Following Scenario, participants are required to follow a bus while maintaining a safe distance from the vehicle. The vehicle is constantly changing its speed throughout the scenario. This complex task requires
Table 1 Stroke characteristics and neurological symptoms of acute stroke patients.
Patient 1
Patient 2 Patient 3 Patient 4 Patient 5
Patient 6
Patient 7
Patient 8 Patient 9
Patient 10
Infarct location
Neurological symptoms (on admission)
NIHSS score
Time between onset and driving evaluation
R MCA R corona radiata R posterior putamen R MCA R frontal cortex R MCA R lateral anterior putamen L PCA L occipital cortex L ICA L parietal cortex L frontal cortex L MCA L frontal cortex L corona radiata L posterior parietal cortex L temporal cortex L MCA L caudate L putamen L insula L parietal cortex L frontal cortex R PCA R occipital cortex R MCA R insula R corona radiata R centrum semiovale R precentral gyrus L MCA L parietal cortex
Dysarthria L sided weakness
0
5 days
Dysarthria L sided weakness Dizziness L facial droop Alexia R visual field scotomas Headache Visual changes
1
5 days
a
3
5 days
1a
4 days
0
3 days
Slowed Speech Dysarthria
0
2 days
R sided weakness Dysarthria Mild expressive aphasia
1
7 days
L lower quadrant visual field deficitb
4a
6 days
L sided weakness
2
5 days
Dysarthria R sided weakness
0
4 days
NIHSS, National Institutes of Health Stroke Scale; L, left; R, right; MCA, middle cerebral artery; ICA, internal carotid artery; PCA, posterior cerebral artery. a NIHSS scores were retrospectively calculated by a stroke neurologist. b Visual field: maintained 120° continuous along the horizontal meridian, with no defect within the central 20°. Visual field deficit subsequently resolved at retest.
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M.A. Hird et al. / Journal of the Neurological Sciences 354 (2015) 46–50
Fig. 1. Magnetic resonance imaging (MRI) showed diffusion-weighted imaging (DWI) lesions of eight patients and T2 lesions of two patients (patients 5 and 8). All hyperintense lesions on DWI were associated with a drop of apparent diffusion coefficient (ADC) values. aPatient 8 obtained an MRI at a later stage (N7 days) than all other patients.
a high degree of sustained attention, visual-motor control, and error detection [12]. Behavioral driving variables collected were: number of collisions, speed exceedances, lane deviations, road edge excursions, stop signs missed, and incorrect turns. 2.2.2. Secondary outcome: neuropsychological assessment After the driving simulation, two brief neuropsychological measures were administered: (1) the Montreal Cognitive Assessment (MoCA) and (2) the Trail Making Test (TMT). The MoCA is a screening measure of global cognitive functioning [13] and is scored on a 30-point scale. The MoCA was administered to rule out underlying cognitive impairment in healthy control participants and to determine the level of global cognitive impairment in patient participants. The TMT measures speed, attention, and mental flexibility [14]. The TMT is widely used in the driving literature [15,16] and assesses many abilities that can be impacted by stroke. Table 2 Demographics, driving habits, and neuropsychological scores of acute stroke patients and controls.
Age Years of education Gender (female), n NIHSS score AlphaFIMa Years of driving experience Number of self-reported traffic accidents MoCAb (total score) TMT-Ac time (s) TMT-A errors TMT-Bc time (s) TMT-B errors
Acute stroke (n = 10)
Control (n = 10)
p-Value
55.10 (17.32) 15.90 (2.23) 3 1.20 (1.40) 109.56 (6.73) 36.50 (20.39) 1.10 (1.20)
55.40 (16.70) 15.85 (2.43) 6
NS NS NS
36.20 (16.47) 0.90 (1.10)
NS NS
25.78 (3.15) 32.48 (17.23) 0.40 (0.52) 72.96 (35.32) 0.20 (0.42)
27.00 (1.56) 23.05 (6.13) 0.20 (0.42) 46.16 (24.70) 0.50 (0.71)
NS NS NS .035 NS
All data reported in mean (SD) format unless otherwise indicated. n, number of observations; NS, not statistically significant (p N 0.05); NIHSS, National Institutes of Health Stroke Scale; FIM, functional independence measure; TMT, Trail Making Test; MoCA, Montreal Cognitive Assessment. a AlphaFIM is a standardized measure of assessing functional status and disability in the acute care setting that contains four motor tasks (bed-to-chair transfer, walking, bowel management, toilet transfer) and two cognitive tasks (expression and memory) scored on a seven-point scale (1 = “total assistance” and 7 = “complete independence”) [8]. AlphaFIM was not reported for one patient. b One patient did not complete the MoCA. c TMT-A and TMT-B time were not recorded for one patient.
2.3. Statistical analysis Statistical analyses were run with SPSS Software (IBM SPSS Statistics for Windows, Version 20.0). The mean and standard deviation were calculated for each of the outcome variables of interest (total errors and errors during right turns, left turns, and left turns with traffic for the City Driving Scenario, and total errors for the Bus Following Scenario). Kolmogorov–Smirnov tests were used to determine normality and, based on these results, the data of patients and controls were compared using the independent-samples t-test and the Mann–Whitney U test. Differences were considered significant if p b .05 (one-tailed). All p-values are reported one-tailed because there were specific predictions regarding the direction of the results. 3. Results Demographic, clinical, and neuropsychological data of patients and controls are presented in Table 2. Despite the fact that patients performed in the cognitively impaired range, and controls performed in the cognitively normal range, there was no statistically significant difference between the two groups for the global score on the MoCA. Patients and controls performed comparably well on the TMT-A; however, patients took significantly longer to complete TMT-B compared to controls, t(17) = 1.933, p b 0.05. Driving simulator data are reported in Table 3. On average, patients committed over twice as many driving errors as controls over the entire City Driving Scenario, t(18) = 2.77, p b 0.01. As predicted, there were no significant differences between patients and controls in terms of the mean number of errors during more routine aspects of driving, such as right turns; however, a significant difference between the groups emerged during left turns with oncoming traffic (U = 26.5, p b 0.05). Patients were able to match the speed of the bus to a similar degree as controls in the bus following task. However, patients committed significantly more driving errors (e.g., center line crossings, speed exceedances) throughout the scenario compared to controls, t(17) = 2.55, p b 0.05. 4. Discussion The current study investigated the driving performance of patients with mild stroke within one-week post-ictus. To our knowledge, this study is the first to provide empirical evidence regarding the specific
M.A. Hird et al. / Journal of the Neurological Sciences 354 (2015) 46–50 Table 3 Performance on the City Driving and Bus Following Scenarios. Acute stroke (n = 10) Control (n = 10) p-value 12.40 (6.26) City Driving errors (total)a City Driving errors per turn Right turns 0.18 (0.32) Left turns 0.35 (0.47) Left turns with traffic 0.49 (0.30) b,c 8.22 (7.08) Bus Following Errors (total)
6.00 (3.77)
.007
0.12 (0.21) 0.20 (0.35) 0.26 (0.25) 2.10 (1.37)
NS NS .040 .016
n, number of observations. a Errors included: collisions (0.6 vs. 0.1), speed exceedances (4.9 vs. 2.9), center line crossings (2.6 vs. 0.9), road edge excursions (2.4 vs. 0.8), stop signs missed (1.6 vs. 1.3), and incorrect turns (0.3 vs. 0.0). b One patient did not complete the Bus Following Scenario due to fatigue. c Errors included: speed exceedances (1.8 vs. 0.6), center line crossings (1.2 vs. 0.2), road edge excursions (5.0 vs. 1.3), and collisions (0.2 vs. 0.0).
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Despite the aforementioned limitations, our study has practical implications. Guidelines typically recommend that patients should refrain from driving for a minimum of one-month post-stroke [3,4]. Despite this, it has been suggested that approximately one third of patients resume driving immediately post-stroke [7]. The results of the current study provide evidence that patients with acute mild stroke experience impairments in certain aspects of driving. This highlights the importance of physicians and other healthcare professionals in adhering to the guidelines and addressing the need for patients to refrain from driving in (at least) the acute phase of injury. In cases where patients are hesitant, have significant impairments related to driving, are at an increased risk of recurrence, or have impaired self-awareness [25], it may be in the best interest of the patient to refer them for a formal and comprehensive driving assessment. Conflict of interest
driving performance of patients within one week of an acute mild ischemic stroke. The results suggest that acute mild stroke patients may be able to maintain driving performance during more routine aspects of driving (e.g., straight driving, right and left turns without traffic). More importantly, deficits become more apparent during the more complex, attentionally demanding aspects of driving (e.g., left turns at a busy intersection, bus following). The results of studies examining the driving performance of patients post-stroke are highly variable. Some studies report less than 35% of patients passing on-road assessments [17,18], and others report over 75% of patients passing on-road assessments [19–22]. One factor contributing to this variability is the heterogeneous patient samples used across and within studies. There is a need to identify the driving behaviors that are characteristic of various subpopulations of stroke, including various stages (e.g., acute, chronic), severities, and location of stroke. Devos and colleagues [23] aimed to address this by determining whether left and right hemispheric lesions differentially impact on-road driving performance. Although there was no difference in overall score of the on-road test for right and left lesions, results suggested that the lateralization of stroke might influence the aspects of driving that contribute most to the overall driving performance score [23]. The current study represents a step in addressing a gap in the literature by characterizing the driving performance of patients with acute mild ischemic stroke. During the City Driving Scenario, patients made over twice as many errors as the control participants. This finding is supported by the results of previous driving simulator studies that investigated the performance of patients 7–14 days [24] and at least three months [25] post-stroke. The findings of the current study are also consistent with the results of Schweizer and colleagues [9], which showed that increased recruitment of various brain networks was required when driving situations increased in complexity. Taken together, the results suggest that patients with mild deficits are able to maintain driving performance during more routine driving tasks that require comparatively low levels of brain resources; however, when driving tasks increase in complexity and require greater recruitment of brain resources [9], patients with acute mild stroke demonstrate impaired driving performance. There are a few methodological limitations. The current study is a pilot study and is consequently limited by its small sample size. Although the current sample was homogeneous in terms of time since onset, severity, and type of stroke, the sample was heterogeneous in terms of other variables (i.e., location of stroke, lateralization of infarct). Replication with a larger clinical sample is required to confirm generalizability to the population as a whole and to isolate the driving behaviors that are characteristic of various subpopulations of stroke (e.g., stroke location). Second, given that the patients were tested in an inpatient setting, patients may have experienced increased fatigue and anxiety compared to controls. Although it has been stated that driving simulation is less realistic than real-traffic driving [26], it has been shown to be valid and correlated with real-world driving [27].
None. Acknowledgments This work was supported by a Grant-in-Aid and a Personnel Award from the Heart and Stroke Foundation of Canada (G-13-0002741) and an Early Researcher Award from the Ontario Ministry of Research and Innovation to Dr. Tom Schweizer, and a Distinguished Clinician Scientists Award from the Heart and Stroke Foundation of Canada to Dr. Gustavo Saposnik. References [1] Eby DW, Molnar LJ. Driving fitness and cognitive impairment: issues for physicians. JAMA 2010;303:1642–3. [2] Tamez E, Myerson J, Morris L, White DA, Baum C, Connor LT. Assessing executive abilities following acute stroke with the trail making test and digit span. Behav Neurol 2011;24:177–85. [3] Canadian Medical Assocation. CMA driver's guide: determining medical fitness to operate motor vehicles 8th ed., 2012. [4] Driver and Vehicle Licensing Agency. DVLA's current medical guidelines for professionals. https://www.gov.uk/current-medical-guidelines-dvla-guidance-for-professionals-conditions-s-to-u. [5] Heart and Stroke Foundation of Ontario. Stroke, driving and the health care professional. http://www.integratedrehabprofessionals.com/images/Driving_Fact_Sheet0607.pdf. [6] Wolf TJ, Rognstad MC. Changes in cognition following mild stroke. Neuropsychol Rehabil 2013;23:256–66. [7] McCarron MO, Loftus AM, McCarron P. Driving after a transient ischaemic attack or minor stroke. Emerg Med J 2008;25:358–9. [8] Fisk GD, Owsley C, Pulley LV. Driving after stroke: driving exposure, advice, and evaluations. Arch Phys Med Rehabil 1997;78:1338–45. [9] Schweizer TA, Kan K, Hung Y, Tam F, Naglie G, Graham SJ. Brain activity during driving with distraction: an immersive fMRI study. Front Hum Neurosci 2013;7: 1–11. [10] Adams HP, Davis PH, Leira EC, Chang KC, Bendixen BH, Clarke WR, Woolson RF, Hansen MD. Baseline NIH Stroke Scale score strongly predicts outcome after stroke: a report of the Trail of Org 10172 in Acute Stroke Treatment (TOAST). Neurology 1999;53:126–31. [11] Ontario Hospital Association. Toolkit to support the implementation of quality-based procedures—appendix AE: stroke network — AlphaFIM® instrument for stroke. http://www.oha.com/CurrentIssues/keyinitiatives/PatientSafety/Documents/QBP/ Appendices/OHA_QBProcedurestoolkit_App_AE.pdf. [accessed 2014 July 10]. [12] Uchiyama Y, Ebe K, Kozato A, Okada T, Sadato N. The neural substrates of driving at a safe distance: a functional MRI study. Neurosci Lett 2003;352:199–202. [13] Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H. The Montreal Cognitive Assessment (MoCA): a brief screening tool for mild cognitive impairment. JAGS 2005;53:695–9. [14] Bowie CR, Harvey PD. Administration and interpretation of the Trail Making Test. Nat Protoc 2006;1:2277–81. [15] Marshall SC, Molnar F, Man-Son-Hing M, Blair R, Brosseau L, Finestone HM, Lamothe C, Korner-Bitensky N, Wilson KG. Predictors of driving ability following stroke: a systematic review. Top Stroke Rehabil 2007;14:98–114. [16] Devos H, Akinwuntan AE, Nieuwboer A, Truijen S, Tant M, De Weerdt W. Screening for fitness to drive after stroke: a systematic review and meta-analysis. Neurology 2011;76:747–56. [17] Akinwuntan AE, De Weerdt W, Feys H, Baten G, Arno P, Kiekens C. The validity of a road test after stroke. Arch Phys Med Rehabil 2005;86:421–6. [18] George S, Clark M, Crotty M. Validation of the Visual Recognition Slide Test with stroke: a component of the New South Wales occupational therapy off-road driver rehabilitation program. Aust Occup Ther J 2008;55:172–9.
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[19] George S, Crotty M. Establishing criterion validity of the Useful Field of View assessment and Stroke Drivers' Screening Assessment: comparison to the result of on-road assessment. Am J Occup Ther 2010;64:114–22. [20] Sommer M, Heidinger C, Arendasy M, Schauer S, Schmitz-Gielsdorf J, Hausler J. Cognitive and personality determinants of post-injury driving fitness. Arch Clin Neuropsychol 2010;25:99–117. [21] Stapleton T, Connolly D, O'Neill D. Exploring the relationship between selfawareness of driving efficacy and that of a proxy when determining fitness to drive after stroke. Aust Occup Ther J 2012;59:63–70. [22] Hird MA, Vetivelu A, Saposnik G, Schweizer TA. Cognitive, on-road, and simulatorbased driving assessment after stroke. J Stroke Cerebrovasc Dis 2014;23:2654–70.
[23] Devos H, Tant M, Akinwuntan AE. On-road driving impairments and associated cognitive deficits after stroke. Cerebrovasc Dis 2014;38:226–32. [24] Kotterba S, Widdig W, Brylak S, Orth M. Driving after cerebral ischemia — a driving simulator investigation. Wien Med Wochenschr 2005;155:348–53. [25] McKay C, Rapport LJ, Bryer RC, Casey J. Self-evaluation of driving simulator performance after stroke. Top Stroke Rehabil 2011;18:549–61. [26] Lundqvist A, Gerdle B, Ronnberg J. Neuropsychological aspects of driving after a stroke — in the simulator and on the road. Appl Cogn Psychol 2000;14:135–50. [27] Lee HC, Cameron D, Lee AH. Assessing the driving performance of older adult drivers: on-road versus simulated driving. Accid Anal Prev 2003;35:797–803.
Contents lists available at ScienceDirect
Journal of the Neurological Sciences journal homepage: www.elsevier.com/locate/jns
Is it safe to drive after acute mild stroke? A preliminary report☆ Megan A. Hird a,b, Kristin A. Vesely a,b, Leah E. Christie b,d, Melissa A. Alves b,d, Jitphapa Pongmoragot d, Gustavo Saposnik a,c,d, Tom A. Schweizer a,e,f,⁎ a
Neuroscience Research Program, Keenan Research Centre for Biomedical Science of the Li Ka Shing Knowledge Institute, St. Michael's Hospital, Toronto, Ontario, Canada University of Toronto,Toronto, Ontario, Canada Stroke Research Unit, Mobility Program, St. Michael's Hospital, Toronto, Ontario, Canada d Medicine, St. Michael's Hospital, Toronto, Ontario, Canada e Department of Surgery, Neurosurgery Division, University of Toronto, Toronto, Ontario, Canada f Institute of Biomaterials and Biomedical Engineering, University of Toronto, Toronto, Ontario, Canada b c
a r t i c l e
i n f o
Article history: Received 19 January 2015 Received in revised form 7 April 2015 Accepted 27 April 2015 Available online 2 May 2015 Keywords: Acute Mild stroke Ischemia Driving Driving simulation Assessment
a b s t r a c t Background: Most guidelines recommend that patients should refrain from driving for at least one month after stroke. Despite these guidelines, and the fact that patients post-stroke may be at an increased risk for driving impairment, many patients report resuming driving within the acute phase of injury. The aim of this study was to investigate the driving performance of patients with acute mild stroke. Methods: The current study compared the driving simulator performance of ten patients with acute mild ischemic stroke (N 48 h and b 7 days) to that of ten healthy, age- and education-matched controls. Results: During the City Driving and Bus Following Scenarios, patients on average committed over twice as many errors (e.g., collisions, center line crossings, speed exceedances) as controls (12.4 vs. 6.0, t(18) = 2.77, p b 0.01; and 8.2 vs. 2.1, t(17) = 2.55, p b 0.05; respectively). Although there was no difference between patients and controls in the number of errors committed during simple right and left turns, patients committed significantly more errors than controls during left turns with traffic (0.49 vs. 0.26, U = 26.5, p b 0.05). Conclusion: Results suggest that patients with acute mild ischemic stroke may be able to maintain driving performance during basic tasks (e.g., straight driving, right turns) and that deficits may become apparent during more complex tasks (e.g., left turns with traffic, bus following). The results highlight the importance of healthcare professionals providing driving advice to their patients post-stroke, particularly in the acute phase of injury. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Evaluating the driving performance of patients after a stroke is a significant challenge for health professionals [1]. Many of the impairments associated with stroke, such as visual field defects, neglect, and paralysis are fairly reliable contraindications of driving ability. However, in cases of minor stroke where impairments are more subtle, such as deficits in executive functioning [2], evaluating driving performance can be much more challenging. Physician guidelines established by prominent governing bodies including the Canadian Medical Association (CMA) [3] and the Driver and Vehicle Licensing Agency (DVLA) [4] state that patients should refrain from driving for a minimum of one month after stroke. When in place, driving guidelines typically capture the window in which stroke and transient ischemic attack (TIA) patients are at an increased risk of
☆ Drs. Saposnik and Schweizer equally contributed to qualify as senior authors. ⁎ Corresponding author at: Keenan Research Centre for Biomedical Science of the Li Ka Shing Knowledge Institute, St. Michael's Hospital, 30 Bond Street, Toronto, Ontario M5B 1W8, Canada. Tel.: +1 416 864 6060x77342. E-mail address: [email protected] (T.A. Schweizer).
http://dx.doi.org/10.1016/j.jns.2015.04.043 0022-510X/© 2015 Elsevier B.V. All rights reserved.
recurrence. Patients are often allowed to resume driving if (1) no significant motor, cognitive, or perceptual deficits are present; (2) there is no significant risk of sudden recurrence; (3) the underlying cause of the stroke has been treated; and (4) the patient did not experience a poststroke seizure [5]. Despite these guidelines, and the fact that cognitive deficits are present in the acute phase of injury and can persist several months after injury [6], approximately 35% of minor stroke and TIA patients resume driving within the one-month period [7]. Furthermore, as low as 9% of patients report receiving driving advice from a physician immediately post-stroke [7]. This number increases to 52% of patients receiving driving advice when other healthcare professionals as well as friends and family are included in addition to physicians [8]. There is a paucity of empirical research that has investigated the driving performance of patients immediately after mild stroke. Thus, it remains unclear whether driving within the acute phase of recovery after minor stroke represents a significant safety risk for the patient and the general public. The current study used driving simulator technology to characterize the driving performance of acute mild stroke patients and to compare their performance to that of age- and educationmatched, healthy adults. Given that patients presented with mild deficits, it was hypothesized that stroke patients would maintain
M.A. Hird et al. / Journal of the Neurological Sciences 354 (2015) 46–50
driving performance during more routine aspects of driving (i.e., straight driving, right and left turns without traffic), which require fewer brain resources; however, patients would exhibit more errors in general as well as during the more demanding aspects of driving (i.e., left turns with traffic), which require greater recruitment of brain resources [9]. 2. Materials and methods 2.1. Participants Twenty participants were included in the study (acute stroke, n = 10; controls, n = 10). All patients were diagnosed and consecutively recruited by members of the Stroke Assessment and Treatment Team (SATT) at St. Michael's Hospital, including stroke neurologists, a physiotherapist, and an occupational therapist. Patients sustained a stroke within one week of testing (range = 2–7 days) and presented with minimal language and motor deficits (see Table 1 and Fig. 1). Patients were required to meet the vision standards outlined by the CMA (i.e., visual acuity no less than 20/50 with both eyes open and examined together, visual field of 120° continuous along the horizontal meridian and 15° continuous above and below fixation with both eyes open and examined together, and no diplopia within the central 40° of primary gaze) [3]. Visual screening was conducted by a stroke neurologist and an occupational therapist, and if there was any indication of visual impairment, patients received a comprehensive visual assessment. Patients with a neurological deficit (e.g., moderate to severe weakness, neglect, severe visual impairment, or ataxia) or a history of dementia were excluded. AlphaFIM® scores were N 80 (mean = 109.6 ± 6.7) and the National Institutes of Health Stroke Scale (NIHSS) scores were b 5 (mean = 1.2 ± 1.4), indicating mild impairment [10]. AlphaFIM® is a standardized measure of assessing functional status and disability in
47
the acute care setting and contains four motor tasks (e.g., bed-to-chair transfer, walking, bowel management, toilet transfer) and two cognitive tasks (e.g., expression and memory), scored on a seven-point scale (1 = “total assistance” and 7 = “complete independence”) [11]. All healthy control participants were recruited from volunteers in the local community and had no prior history of psychiatric or neurological illness. All participants held a valid driver's license at the time of testing. Self-reported years of driving experience and number of collisions are reported in Table 2. Ethical approval for the study was obtained by the Research Ethics Board at St. Michael's Hospital in Toronto, Canada. All participants provided written informed consent prior to their inclusion in the present study. 2.2. Procedure 2.2.1. Primary outcome: driving simulation The driving performance of participants was assessed using a STISIM Drive® (version 2.08.08, Logitech G25 model) driving simulator, equipped with a fully functioning steering wheel, pedals, and signaling system. Participants first completed a training session to become familiar with the simulator environment. Two experimental driving scenarios were administered: (1) City Driving Scenario and (2) Bus Following Scenario. The City Driving Scenario involves straight driving, routine right and left turns, and left turns with traffic. In conditions with higher cognitive demands (i.e., left turns with traffic), participants need to make decisions about when it is safe to turn in order to avoid oncoming traffic and pedestrians. These decisions are associated with processes of selective attention, visual–spatial ability, and motor control [9]. In the Bus Following Scenario, participants are required to follow a bus while maintaining a safe distance from the vehicle. The vehicle is constantly changing its speed throughout the scenario. This complex task requires
Table 1 Stroke characteristics and neurological symptoms of acute stroke patients.
Patient 1
Patient 2 Patient 3 Patient 4 Patient 5
Patient 6
Patient 7
Patient 8 Patient 9
Patient 10
Infarct location
Neurological symptoms (on admission)
NIHSS score
Time between onset and driving evaluation
R MCA R corona radiata R posterior putamen R MCA R frontal cortex R MCA R lateral anterior putamen L PCA L occipital cortex L ICA L parietal cortex L frontal cortex L MCA L frontal cortex L corona radiata L posterior parietal cortex L temporal cortex L MCA L caudate L putamen L insula L parietal cortex L frontal cortex R PCA R occipital cortex R MCA R insula R corona radiata R centrum semiovale R precentral gyrus L MCA L parietal cortex
Dysarthria L sided weakness
0
5 days
Dysarthria L sided weakness Dizziness L facial droop Alexia R visual field scotomas Headache Visual changes
1
5 days
a
3
5 days
1a
4 days
0
3 days
Slowed Speech Dysarthria
0
2 days
R sided weakness Dysarthria Mild expressive aphasia
1
7 days
L lower quadrant visual field deficitb
4a
6 days
L sided weakness
2
5 days
Dysarthria R sided weakness
0
4 days
NIHSS, National Institutes of Health Stroke Scale; L, left; R, right; MCA, middle cerebral artery; ICA, internal carotid artery; PCA, posterior cerebral artery. a NIHSS scores were retrospectively calculated by a stroke neurologist. b Visual field: maintained 120° continuous along the horizontal meridian, with no defect within the central 20°. Visual field deficit subsequently resolved at retest.
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Fig. 1. Magnetic resonance imaging (MRI) showed diffusion-weighted imaging (DWI) lesions of eight patients and T2 lesions of two patients (patients 5 and 8). All hyperintense lesions on DWI were associated with a drop of apparent diffusion coefficient (ADC) values. aPatient 8 obtained an MRI at a later stage (N7 days) than all other patients.
a high degree of sustained attention, visual-motor control, and error detection [12]. Behavioral driving variables collected were: number of collisions, speed exceedances, lane deviations, road edge excursions, stop signs missed, and incorrect turns. 2.2.2. Secondary outcome: neuropsychological assessment After the driving simulation, two brief neuropsychological measures were administered: (1) the Montreal Cognitive Assessment (MoCA) and (2) the Trail Making Test (TMT). The MoCA is a screening measure of global cognitive functioning [13] and is scored on a 30-point scale. The MoCA was administered to rule out underlying cognitive impairment in healthy control participants and to determine the level of global cognitive impairment in patient participants. The TMT measures speed, attention, and mental flexibility [14]. The TMT is widely used in the driving literature [15,16] and assesses many abilities that can be impacted by stroke. Table 2 Demographics, driving habits, and neuropsychological scores of acute stroke patients and controls.
Age Years of education Gender (female), n NIHSS score AlphaFIMa Years of driving experience Number of self-reported traffic accidents MoCAb (total score) TMT-Ac time (s) TMT-A errors TMT-Bc time (s) TMT-B errors
Acute stroke (n = 10)
Control (n = 10)
p-Value
55.10 (17.32) 15.90 (2.23) 3 1.20 (1.40) 109.56 (6.73) 36.50 (20.39) 1.10 (1.20)
55.40 (16.70) 15.85 (2.43) 6
NS NS NS
36.20 (16.47) 0.90 (1.10)
NS NS
25.78 (3.15) 32.48 (17.23) 0.40 (0.52) 72.96 (35.32) 0.20 (0.42)
27.00 (1.56) 23.05 (6.13) 0.20 (0.42) 46.16 (24.70) 0.50 (0.71)
NS NS NS .035 NS
All data reported in mean (SD) format unless otherwise indicated. n, number of observations; NS, not statistically significant (p N 0.05); NIHSS, National Institutes of Health Stroke Scale; FIM, functional independence measure; TMT, Trail Making Test; MoCA, Montreal Cognitive Assessment. a AlphaFIM is a standardized measure of assessing functional status and disability in the acute care setting that contains four motor tasks (bed-to-chair transfer, walking, bowel management, toilet transfer) and two cognitive tasks (expression and memory) scored on a seven-point scale (1 = “total assistance” and 7 = “complete independence”) [8]. AlphaFIM was not reported for one patient. b One patient did not complete the MoCA. c TMT-A and TMT-B time were not recorded for one patient.
2.3. Statistical analysis Statistical analyses were run with SPSS Software (IBM SPSS Statistics for Windows, Version 20.0). The mean and standard deviation were calculated for each of the outcome variables of interest (total errors and errors during right turns, left turns, and left turns with traffic for the City Driving Scenario, and total errors for the Bus Following Scenario). Kolmogorov–Smirnov tests were used to determine normality and, based on these results, the data of patients and controls were compared using the independent-samples t-test and the Mann–Whitney U test. Differences were considered significant if p b .05 (one-tailed). All p-values are reported one-tailed because there were specific predictions regarding the direction of the results. 3. Results Demographic, clinical, and neuropsychological data of patients and controls are presented in Table 2. Despite the fact that patients performed in the cognitively impaired range, and controls performed in the cognitively normal range, there was no statistically significant difference between the two groups for the global score on the MoCA. Patients and controls performed comparably well on the TMT-A; however, patients took significantly longer to complete TMT-B compared to controls, t(17) = 1.933, p b 0.05. Driving simulator data are reported in Table 3. On average, patients committed over twice as many driving errors as controls over the entire City Driving Scenario, t(18) = 2.77, p b 0.01. As predicted, there were no significant differences between patients and controls in terms of the mean number of errors during more routine aspects of driving, such as right turns; however, a significant difference between the groups emerged during left turns with oncoming traffic (U = 26.5, p b 0.05). Patients were able to match the speed of the bus to a similar degree as controls in the bus following task. However, patients committed significantly more driving errors (e.g., center line crossings, speed exceedances) throughout the scenario compared to controls, t(17) = 2.55, p b 0.05. 4. Discussion The current study investigated the driving performance of patients with mild stroke within one-week post-ictus. To our knowledge, this study is the first to provide empirical evidence regarding the specific
M.A. Hird et al. / Journal of the Neurological Sciences 354 (2015) 46–50 Table 3 Performance on the City Driving and Bus Following Scenarios. Acute stroke (n = 10) Control (n = 10) p-value 12.40 (6.26) City Driving errors (total)a City Driving errors per turn Right turns 0.18 (0.32) Left turns 0.35 (0.47) Left turns with traffic 0.49 (0.30) b,c 8.22 (7.08) Bus Following Errors (total)
6.00 (3.77)
.007
0.12 (0.21) 0.20 (0.35) 0.26 (0.25) 2.10 (1.37)
NS NS .040 .016
n, number of observations. a Errors included: collisions (0.6 vs. 0.1), speed exceedances (4.9 vs. 2.9), center line crossings (2.6 vs. 0.9), road edge excursions (2.4 vs. 0.8), stop signs missed (1.6 vs. 1.3), and incorrect turns (0.3 vs. 0.0). b One patient did not complete the Bus Following Scenario due to fatigue. c Errors included: speed exceedances (1.8 vs. 0.6), center line crossings (1.2 vs. 0.2), road edge excursions (5.0 vs. 1.3), and collisions (0.2 vs. 0.0).
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Despite the aforementioned limitations, our study has practical implications. Guidelines typically recommend that patients should refrain from driving for a minimum of one-month post-stroke [3,4]. Despite this, it has been suggested that approximately one third of patients resume driving immediately post-stroke [7]. The results of the current study provide evidence that patients with acute mild stroke experience impairments in certain aspects of driving. This highlights the importance of physicians and other healthcare professionals in adhering to the guidelines and addressing the need for patients to refrain from driving in (at least) the acute phase of injury. In cases where patients are hesitant, have significant impairments related to driving, are at an increased risk of recurrence, or have impaired self-awareness [25], it may be in the best interest of the patient to refer them for a formal and comprehensive driving assessment. Conflict of interest
driving performance of patients within one week of an acute mild ischemic stroke. The results suggest that acute mild stroke patients may be able to maintain driving performance during more routine aspects of driving (e.g., straight driving, right and left turns without traffic). More importantly, deficits become more apparent during the more complex, attentionally demanding aspects of driving (e.g., left turns at a busy intersection, bus following). The results of studies examining the driving performance of patients post-stroke are highly variable. Some studies report less than 35% of patients passing on-road assessments [17,18], and others report over 75% of patients passing on-road assessments [19–22]. One factor contributing to this variability is the heterogeneous patient samples used across and within studies. There is a need to identify the driving behaviors that are characteristic of various subpopulations of stroke, including various stages (e.g., acute, chronic), severities, and location of stroke. Devos and colleagues [23] aimed to address this by determining whether left and right hemispheric lesions differentially impact on-road driving performance. Although there was no difference in overall score of the on-road test for right and left lesions, results suggested that the lateralization of stroke might influence the aspects of driving that contribute most to the overall driving performance score [23]. The current study represents a step in addressing a gap in the literature by characterizing the driving performance of patients with acute mild ischemic stroke. During the City Driving Scenario, patients made over twice as many errors as the control participants. This finding is supported by the results of previous driving simulator studies that investigated the performance of patients 7–14 days [24] and at least three months [25] post-stroke. The findings of the current study are also consistent with the results of Schweizer and colleagues [9], which showed that increased recruitment of various brain networks was required when driving situations increased in complexity. Taken together, the results suggest that patients with mild deficits are able to maintain driving performance during more routine driving tasks that require comparatively low levels of brain resources; however, when driving tasks increase in complexity and require greater recruitment of brain resources [9], patients with acute mild stroke demonstrate impaired driving performance. There are a few methodological limitations. The current study is a pilot study and is consequently limited by its small sample size. Although the current sample was homogeneous in terms of time since onset, severity, and type of stroke, the sample was heterogeneous in terms of other variables (i.e., location of stroke, lateralization of infarct). Replication with a larger clinical sample is required to confirm generalizability to the population as a whole and to isolate the driving behaviors that are characteristic of various subpopulations of stroke (e.g., stroke location). Second, given that the patients were tested in an inpatient setting, patients may have experienced increased fatigue and anxiety compared to controls. Although it has been stated that driving simulation is less realistic than real-traffic driving [26], it has been shown to be valid and correlated with real-world driving [27].
None. Acknowledgments This work was supported by a Grant-in-Aid and a Personnel Award from the Heart and Stroke Foundation of Canada (G-13-0002741) and an Early Researcher Award from the Ontario Ministry of Research and Innovation to Dr. Tom Schweizer, and a Distinguished Clinician Scientists Award from the Heart and Stroke Foundation of Canada to Dr. Gustavo Saposnik. References [1] Eby DW, Molnar LJ. Driving fitness and cognitive impairment: issues for physicians. JAMA 2010;303:1642–3. [2] Tamez E, Myerson J, Morris L, White DA, Baum C, Connor LT. Assessing executive abilities following acute stroke with the trail making test and digit span. Behav Neurol 2011;24:177–85. [3] Canadian Medical Assocation. CMA driver's guide: determining medical fitness to operate motor vehicles 8th ed., 2012. [4] Driver and Vehicle Licensing Agency. DVLA's current medical guidelines for professionals. https://www.gov.uk/current-medical-guidelines-dvla-guidance-for-professionals-conditions-s-to-u. [5] Heart and Stroke Foundation of Ontario. Stroke, driving and the health care professional. http://www.integratedrehabprofessionals.com/images/Driving_Fact_Sheet0607.pdf. [6] Wolf TJ, Rognstad MC. Changes in cognition following mild stroke. Neuropsychol Rehabil 2013;23:256–66. [7] McCarron MO, Loftus AM, McCarron P. Driving after a transient ischaemic attack or minor stroke. Emerg Med J 2008;25:358–9. [8] Fisk GD, Owsley C, Pulley LV. Driving after stroke: driving exposure, advice, and evaluations. Arch Phys Med Rehabil 1997;78:1338–45. [9] Schweizer TA, Kan K, Hung Y, Tam F, Naglie G, Graham SJ. Brain activity during driving with distraction: an immersive fMRI study. Front Hum Neurosci 2013;7: 1–11. [10] Adams HP, Davis PH, Leira EC, Chang KC, Bendixen BH, Clarke WR, Woolson RF, Hansen MD. Baseline NIH Stroke Scale score strongly predicts outcome after stroke: a report of the Trail of Org 10172 in Acute Stroke Treatment (TOAST). Neurology 1999;53:126–31. [11] Ontario Hospital Association. Toolkit to support the implementation of quality-based procedures—appendix AE: stroke network — AlphaFIM® instrument for stroke. http://www.oha.com/CurrentIssues/keyinitiatives/PatientSafety/Documents/QBP/ Appendices/OHA_QBProcedurestoolkit_App_AE.pdf. [accessed 2014 July 10]. [12] Uchiyama Y, Ebe K, Kozato A, Okada T, Sadato N. The neural substrates of driving at a safe distance: a functional MRI study. Neurosci Lett 2003;352:199–202. [13] Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H. The Montreal Cognitive Assessment (MoCA): a brief screening tool for mild cognitive impairment. JAGS 2005;53:695–9. [14] Bowie CR, Harvey PD. Administration and interpretation of the Trail Making Test. Nat Protoc 2006;1:2277–81. [15] Marshall SC, Molnar F, Man-Son-Hing M, Blair R, Brosseau L, Finestone HM, Lamothe C, Korner-Bitensky N, Wilson KG. Predictors of driving ability following stroke: a systematic review. Top Stroke Rehabil 2007;14:98–114. [16] Devos H, Akinwuntan AE, Nieuwboer A, Truijen S, Tant M, De Weerdt W. Screening for fitness to drive after stroke: a systematic review and meta-analysis. Neurology 2011;76:747–56. [17] Akinwuntan AE, De Weerdt W, Feys H, Baten G, Arno P, Kiekens C. The validity of a road test after stroke. Arch Phys Med Rehabil 2005;86:421–6. [18] George S, Clark M, Crotty M. Validation of the Visual Recognition Slide Test with stroke: a component of the New South Wales occupational therapy off-road driver rehabilitation program. Aust Occup Ther J 2008;55:172–9.
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M.A. Hird et al. / Journal of the Neurological Sciences 354 (2015) 46–50
[19] George S, Crotty M. Establishing criterion validity of the Useful Field of View assessment and Stroke Drivers' Screening Assessment: comparison to the result of on-road assessment. Am J Occup Ther 2010;64:114–22. [20] Sommer M, Heidinger C, Arendasy M, Schauer S, Schmitz-Gielsdorf J, Hausler J. Cognitive and personality determinants of post-injury driving fitness. Arch Clin Neuropsychol 2010;25:99–117. [21] Stapleton T, Connolly D, O'Neill D. Exploring the relationship between selfawareness of driving efficacy and that of a proxy when determining fitness to drive after stroke. Aust Occup Ther J 2012;59:63–70. [22] Hird MA, Vetivelu A, Saposnik G, Schweizer TA. Cognitive, on-road, and simulatorbased driving assessment after stroke. J Stroke Cerebrovasc Dis 2014;23:2654–70.
[23] Devos H, Tant M, Akinwuntan AE. On-road driving impairments and associated cognitive deficits after stroke. Cerebrovasc Dis 2014;38:226–32. [24] Kotterba S, Widdig W, Brylak S, Orth M. Driving after cerebral ischemia — a driving simulator investigation. Wien Med Wochenschr 2005;155:348–53. [25] McKay C, Rapport LJ, Bryer RC, Casey J. Self-evaluation of driving simulator performance after stroke. Top Stroke Rehabil 2011;18:549–61. [26] Lundqvist A, Gerdle B, Ronnberg J. Neuropsychological aspects of driving after a stroke — in the simulator and on the road. Appl Cogn Psychol 2000;14:135–50. [27] Lee HC, Cameron D, Lee AH. Assessing the driving performance of older adult drivers: on-road versus simulated driving. Accid Anal Prev 2003;35:797–803.
