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The Bucket Test Improves Detection of Stroke in Patients With Acute Dizziness
The Journal of Emergency Medicine, Vol. -, No. -, pp. 1–10, 2020 Ó 2020 Published by Elsevier Inc. 0736-4679/$ - see front matter
https://doi.org/10.1016/j.jemermed.2020.10.052
Selected Topics: Neurological Emergencies
THE BUCKET TEST IMPROVES DETECTION OF STROKE IN PATIENTS WITH ACUTE DIZZINESS Amir Shaban, MD,* Atif Zafar, MD,* Bernadette Borte, MD,* Yasir Elhawi, MD,† Ali Maamar-Tayeb, MD,* Patrick Ten Eyck, PHD,‡ Azeemuddin Ahmed, MD, MBA,† Anne-Sophie Wattiez, PHD,§ǁ and Deema Fattal, MD*{ *Department of Neurology, The University of Iowa, Iowa City, Iowa, †Department of Emergency Medicine, The University of Iowa, Iowa City, Iowa, ‡Institute for Clinical and Translational Science, The University of Iowa, Iowa City, Iowa, §Department of Molecular Physiology and Biophysics, University of Iowa, Iowa City, Iowa, ǁCenter for the Prevention and Treatment of Visual Loss, Iowa Veterans Affairs Health Care System, Iowa City, Iowa, and {The Veteran’s Administration Medical Center, Iowa City, Iowa Corresponding Address: Deema Fattal, MD, Department of Neurology, The University of Iowa, 200 Hawkins Dr, 2007 Roy Carver Pavilion, Iowa City, IA 52242
, Abstract—Background: It is challenging to detect posterior circulation strokes in patients presenting to the emergency department (ED) with acute dizziness. The current approach uses a combinatorial head-impulse, nystagmus, and test-of-skew method and is sensitive enough to differentiate central causes from peripheral ones. However, it is difficult to perform and underused. Further, magnetic resonance imaging (MRI) of the brain is not always available and can have low sensitivity for detecting posterior circulation strokes. Objectives: We evaluated the feasibility and utility
of the bucket test (BT), which measures the difference between patient’s subjective perception of the visual vertical and the true vertical, as a screening tool for stroke in patients presenting to the ED with acute dizziness. Methods: In this work, we prospectively enrolled 81 patients that presented to our academic medical center ED with dizziness as their chief complaint. The BT was performed 3 times for every patient. Results: Seventy-one patients met the study criteria and were included in the analysis. Ten patients were excluded because of a history of drug-seeking behavior. There were no reported difficulties performing the BT. Six patients (8%) were diagnosed with ischemic stroke on MRI and 1 additional patient was diagnosed with transient ischemic attack and found to have a stroke on subsequent MRI. All 7 patients with dizziness attributed to cerebrovascular etiology had an abnormal BT, resulting in a sensitivity of 100% (95% confidence interval [CI] 59–100%). The specificity of the BT was 38% (95% CI 24–52%). The positive predictive value of the BT for detecting stroke was 18% (95% CI 15–21%). Conclusions: The BT is an easy, cheap, safe, and quick test that is feasible and sensitive to screen acutely dizzy patients for stroke in the ED. Ó 2020 Published by Elsevier Inc.
Reprints are not available from the authors. Presented as a poster at the International Stroke Conference 2016, February 17–19, Los Angeles, California. DF: conceived the study; designed the trial; obtained IRB approval; trained the rest of the authors on performing the Bucket Test; and drafted first draft of manuscript and finalized the final draft. No funding supported this work. BB, YE, AMT, AA: recruited patients and performed the Bucket Test. AZ: recruited patients and prepared data in tables. DF, AA: supervised the conduct of the trial and data collection. AS, ASW: reviewed data; prepared the final draft of manuscript; and contributed to analysis of data. PTE: provided statistical support and advice. All authors reviewed the manuscript and DF, AA, AZ contributed substantially to the revisions. DF takes responsibility for the paper as a whole.
, Keywords—acute vestibular syndrome; bucket test; dizziness; HINTS; posterior circulation stroke; subjective visual vertical
RECEIVED: 25 January 2020; FINAL SUBMISSION RECEIVED: 17 October 2020; ACCEPTED: 22 October 2020 1
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INTRODUCTION Acute dizziness represents a diagnostic challenge for neurologists and emergency department (ED) providers. Dizziness is among the most common chief complaint, accounting for approximately 3% to 4% of ED visits in the United States (1). Most causes of dizziness are related to peripheral vestibular etiologies or medical conditions, yet a small but significant percentage is central, mostly because of stroke (1). Acute vestibular syndrome (AVS) is a syndrome of dizziness of any description that is caused by acute unilateral or asymmetrical vestibular system dysfunction and that lasts for hours and is associated with nystagmus. The AVS can be related to peripheral (inner ear) or central (posterior fossa) causes; about 25% of patients with AVS have an underlying central nervous system etiology, including acute ischemic or hemorrhagic stroke (2,3). The gold standard tool for stroke diagnosis is magnetic resonance imaging (MRI) of the brain, which has good yields compared with computed tomography (CT) scans for identifying acute ischemic strokes, but has low sensitivity for posterior circulation strokes (2– 6). Furthermore, MRI of the brain is not widely available in smaller hospitals and cannot be relied upon to screen for stroke in patients with dizziness. In the absence of a standardized and feasible protocol, evaluating patients with dizziness continues to be a challenge. As a result, one third of acute ischemic strokes in the posterior circulation that present with dizziness are misdiagnosed (1). To reduce misdiagnosing stroke in patients who are acutely dizzy, the combinatorial clinical examination of head-impulse, nystagmus, and test-of-skew (HINTS) or HINTS plus (adding acute hearing loss) has been proposed by neuro-otologists as a sensitive method to differentiate central causes of acute dizziness from peripheral causes (3,7). The HINTS test performed by a trained neurologist is reported to have a sensitivity of 100% and specificity of 96% for stroke (using diffusionweighted imaging MRI as their reference standard, including repeating MRI if the initial MRI was negative) (3). However, the HINTS examination is difficult to perform and requires special training, and for these reasons remains greatly underused by emergency physicians and neurologists (7). In this work we explored the feasibility of using a cheap, readily available, and simple test, the bucket test (BT), for screening ED patients for stroke. The BT is a previously validated test that measures a patient’s subjective and visual perception of the vertical, known as the subjective visual vertical (SVV), which normally coincides with the true vertical of earth’s gravity direction (verdical vertical) (8). SVV is accomplished through the
vestibular system, and is the product of bilateral graviceptive input from the vertical semicircular canals and otolith organs to the vestibular nuclei with integration of signals from multiple other centers including rostral midbrain, cerebellum, and thalamus (9,10). The vestibular input is also integrated with somatosensory and visual information to achieve a correct perception of the vertical body position in relation to the center of gravity (9). SVV is commonly impaired in conditions that result in acute vestibular dysfunction, including stroke (9). In this study, we sought to determine the feasibility and utility of the BT in screening for acute stroke in ED patients with dizziness. The significance of this work lies in the fact that it screens patients in the acute setting of the ED. All published studies to date measured SVV in patients already known to have strokes, and did so days to months after the insult, when we know that deviation decreases during the course of the recovery. Furthermore, they measured SVV in the laboratory setting and not in the acute setting of the ED. The present study has the advantage of assessing SVV directly at the time patients present to ED with a quick, safe, easy to make, easy to use, and cheap screening tool for stroke. METHODS We prospectively enrolled 81 patients that presented to our academic medical center ED with the chief complaint of dizziness between February 2012 and February 2015. In this work, ‘‘dizziness’’ was used to encompass any sense of vertigo, lightheadedness, or any nonspecific dizziness because any type of dizziness can occur in stroke (1). Patients were identified by an emergency physician or neurology residents who contacted the research team for evaluation. We excluded 10 patients from the final analysis because of a history of drugseeking behavior resulting in new primary complaints that did not fit the inclusion criteria and were beyond the scope of our study. The final analysis included 71 patients. To measure SVV we used a simple, handheld tool, i.e., a plastic bucket (8). The bucket is equipped with a level that was fixed on the outer surface facing the examiner to measure the true vertical alignment (Figure 1). On the inner surface of the bucket facing the patient was a line of stars that glowed in the dark. Patients were given the bucket with the stars initially oriented horizontally (90 ) and were asked to place their face inside the plastic bucket to avoid visual cues, and to turn the bucket around in order to vertically align the stars on the interior surface of the bucket. The difference in degrees between the patient’s SVV and the true vertical alignment (SVV tilt) was documented for each attempt, to left or right of the
Bucket Test and Detection of Stroke
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Figure 1. Bucket test.
vertical 0. Each patient repeated the test 3 times, and previous results were not disclosed to the patient in between attempts as to not induce bias (11). The number of trials was chosen to balance the need for accuracy of the result and the feasibility in ED context. The bucket was considered misaligned, and the attempt abnormal, if patient’s SVV was >2 different than the true vertical (10). The BT was scored as abnormal if patient misaligned the bucket on 2 of 3 attempts and the deviation was consistently toward one side. An equivocal result was scored when patient misaligned the bucket inconsistently, sometimes to the left and other times to the right or when only 1 attempt was abnormal. The BT was considered normal when all 3 attempts showed deviation of #2 . The senior author (Dr Fattal, a neurologist specialized in balance/dizziness disorders) trained the rest of the research team clinicians to perform the test reliably (a stroke neurologist [Dr Shaban], an ED specialist [Dr Ahmed], an emergency medicine resident [Dr Elhawi], and neurology residents Drs Borte, Maamar-Tayeb, and Zafar]). Only 1 researcher conducted the test at a time for a given patient, so interrater reliability could not be calculated. Researchers performing the BT were blinded to patients’ history (except for the presence of dizziness), neurologic examination, and diagnosis. Other parts of clinical care were left to the discretion of the treating
physicians. After performing the BT, the research team extracted demographic variables, risk factors, imaging findings, and final discharge diagnoses from the patients’ medical records. We used exact (Fisher and Clopper-Pearson) methods for testing specificity and sensitivity values and the 2sample t test to compare means of continuous measures. For sample size calculations, assuming a null sensitivity of 70% as seen in the literature, where sensitivity ranges from 50% to 90%, we would need a total sample size of 17 (which should encompass 11 abnormal observations) to conclude that the true sensitivity differs with $80% power (10). This study was approved by our institutional review board (201904817) and all patients provided informed consent before participating in this study. RESULTS Of the 81 patients enrolled in the study, 71 were included in the final analysis (Figure 2). Details regarding the demographic variables and stroke risk factors in our study population are provided in Table 1. Most patients presented with isolated dizziness (n = 48) with no associated neurologic symptoms. However, 10 patients on presentation reported associated headache, 6 patients had blurred vision, 5 patients had unilateral numbness, 3 patients had unilateral weakness, and 2 patients had syncope. A total
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Number of Pa ents=81 10 excluded Number of Pa ents=71
Number of pa ents=22 BT
MRI
Normal=15
Stroke=7
Abnormal BT=40
Normal=20 Equivocal=11
Figure 2. Flow chart.
of 22 patients had brain MRIs, a decision left to the discretion of the treating emergency physicians. In our sample, benign paroxysmal positional vertigo was the most common cause and was the ultimate diagnosis in 14 cases. Other neurologic causes included 7 patients with stroke or transient ischemic attack (TIA), 4 patients with tumors, 3 patients with migraines, and 2 patients with Chiari malformation. Three cases were diagnosed with peripheral vestibulopathy. Metabolic causes of dizziness were also common in our sample, including 14 patients with dehydration or orthostatic hypotension and 3 patients with underlying cardiac issues. Hypoglycemia, anemia, and respiratory failure were among the other metabolic etiologies noted. The etiology remained unknown in 10 patients. Causes of dizziness in our sample are summarized in Table 2. All 71 patients were able to perform the 3 BTs with no reported difficulties or adverse events. The testing itself only took 1 to 2 min. Forty patients had abnormal test results, whereas 11 patients had equivocal results. The remaining 20 patients had completely normal test results. Of the 7 patients who were eventually diagnosed with a stroke or TIA, 6 patients had brain MRI on presentation Table 1. Baseline Characteristics Variable
Frequency in Total Sample (n = 71)
Mean age, years (SD) Gender, female (%) History of HTN History of DM History of HLD History of CAD Smoking Alcohol abuse Substance abuse History of prior stroke History of A-fib History of Migraines
53 (15.4) 41 (57%) 24 (34%) 13 (18%) 10 (14%) 9 (13%) 33 (46%) 5 (7%) 1 (1%) 5 (7%) 4 (6%) 6 (8%)
SD = standard deviation; HTN = hypertension; DM = diabetes mellitus; HLD = hyperlipidemia; CAD = coronary artery disease; A-fib = atrial fibrillation.
that confirmed the diagnosis of stroke. While 1 patient had a TIA with negative CT and was discharged from the ED, to return 12 days later with dizziness again, at which time the brain MRI showed a subacute ischemic stroke. Of the 7 patients with ischemic strokes or TIA, most occurred in the posterior circulation, involving the cerebellum with or without the brainstem. In 1 patient, who presented with dizziness and right hearing loss, the initial examination and diagnosis was right deafness and the initial brain MRI was read as negative; however, upon further review, the patient was found to have left beating nystagmus and upon re-examination of the brain MRI, the report was edited to reflect a subtle acute right anterior inferior cerebellar artery stroke changes that were initially read as artifact. All 7 patients with stroke or TIA had abnormal BT. Therefore, the BT sensitivity for ischemic stroke was 100% (95% confidence interval 59–100%). The specificity of the BT was 38% (95% confidence interval 24–52%). The positive predictive value of the BT for detecting stroke was 18% (95% confidence interval 15–21%). The mean SVV tilt in patients with stroke was 7.6 compared with 4.4 for patients without stroke (p = 0.006). Details regarding the BT results stratified by the etiology of dizziness are provided in Table 2. The BT was positive in 12 of 24 (50%) patients who were ultimately diagnosed with metabolic problem as a cause for their dizziness. DISCUSSION Neurologic causes of acute dizziness in the ED were common in our sample. Stroke was diagnosed in 10% of our patients, which is within the range of previously reported values of 4% to 15% (12). Benign positional vertigo and non-neurologic causes were the most common etiologies for acute dizziness in our sample population, consistent with the published literature. Our study showed that the BT was easy to perform, safe, fast, reliable, and sensitive to detect ischemic strokes in patient with acute dizziness. The BT is also easily made and is inexpensive, the analysis of the result is simple even for the nonspecialist, and as such the BT may be useful to screen for ischemic stroke in patients presenting to ED with acute dizziness. We believe that performing >1 test attempt for each patient was feasible and necessary to confirm a consistent result. Previous studies have shown that acute lesions involving the vestibular system (including stroke), can result in SVV tilt (13). Table 3 summarizes previously published studies measuring SVV tilt in pathologic conditions. The SVV tilt can remain abnormal for days after the insult (13). Several laboratory-based methods for
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Table 2. The Results of the Bucket Test per Discharge Diagnosis
Ischemic stroke/TIA BPPV Dehydration/hypovolemia Labyrinthitis Meniere’s Migraines Substance/alcohol Other CNS cause Other medical problems Unknown Total
Positive BT (Abnormal)
Negative BT (Normal)
Equivocal BT
7 8 8 1 1 1 2 2 4 6 40
0 3 5 0 0 2 0 4 4 2 20
0 3 1 2 0 0 0 1 2 2 11
BT = Bucket Test; TIA = transient ischemic attack; BPPV = Benign paroxysmal positional vertigo; CNS = central nervous system.
measuring SVV were applied in previous studies, such as the hemispheric dome test, or using the virtual SVV system (14). The BT test and the laboratory-based dome test have high concordance, and the virtual SVV system yields similar results than the BT, albeit with increased precision (8). However, the virtual SVV system requires more expensive equipment (e.g., googles and a computer) and would take longer to use than the simple BT. While previous studies evaluated the BT in patients with known ischemic stroke, outpatient clinic settings, or research settings comparing healthy subjects to subjects with dizziness, our study is the first to use the BT in the real acute setting of the ED and in a nondiagnosed and diverse patient population presenting with acute dizziness (8,13,15). The association between ischemic stroke and SVV abnormalities has been shown in the published literature. In a study of 27 patients with cerebellar strokes (seen <2 weeks after onset) and using laboratorybased SVV measurements, it was noted that 56% of patients had abnormal SVV (16). Another study included 43 patients seen 1 to 12 days after cerebellar strokes, of which 84% had abnormal SVV, as measured in the laboratory (13). Piscicelli and Perennou reviewed SVV in stroke, and in that review the strokes that were called acute were evaluated on average several days to 2 weeks after the onset, a period during which SVV can start to normalize (10,13). Our stroke patients all presented the same day of the onset of dizziness, potentially explaining our higher sensitivity. The direction of the SVV tilt is either ipsilateral or contralateral to the stroke in previous studies (9,13,17). Specifically, strokes of the dorsolateral medulla, anterior inferior cerebellar artery, lateral posterior inferior cerebellar artery (PICA), and medial PICA strokes that do not involve the nodulus all give ipsilateral SVV abnormality, whereas medial PICA that involve the nodulus cause contralateral SVV (17). Similarly, in our study, all had ipsilateral SVV tilt, toward the side of the stroke, and our strokes were in PICA (without nodulus involvement), anterior inferior cerebellar artery, and dorsolateral
medulla territories. Of note, anterior circulation strokes that involve cortical/subcortical structures have also been reported to be associated with abnormal SVV, potentially explaining the abnormal BT in our patient sample where the stroke affected the anterior circulation (9). In a recent study comparing brain MRI–confirmed brainstem or cerebellar strokes to vestibular migraines in patients presenting with migraine or dizziness alone, SVV abnormalities, measured using the BT, were significantly higher in patients with strokes examined 1 day to 2 months after stroke onset (15). Furthermore, using the BT alone to differentiate strokes from migraine resulted in a sensitivity of 74% and specificity of 92% (15). In our sample, however, the specificity and the positive predictive value of the BT in detecting stroke were low, possibly because we included all patients with dizziness (including metabolic causes). For those reasons, even though the BT may be useful for screening, it should be followed by other, more specific tests that evaluate patients with acute dizziness, such as more detailed neurologic examination, neurologic consultation, HINTS, or brain MRI. The BT is currently being investigated in the EMVERT clinical trial, which is enrolling patients presenting to the emergency department with acute onset of dizziness. The SVV will be used along with other tools, including video-oculography and mobile posturography, as screening tools to detect stroke (18). Limitations This study has several limitations. First, we cannot calculate the k agreement of the BT because only 1 researcher conducted the test at a time. Small sample size and the large number of conditions that can cause dizziness limited our ability to detected potential differences in the performance of the BT to screen for these conditions. The small sample size/recruitment rate for this study depended on the ability of ED teams to contact the research team when an eligible and interested patient was
Reference
Population (#Enrolled; Diagnosis; when Evaluated Post Symptom Onset)
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Table 3. Subjective Visual Vertical (SVV) Tilts in Stroke Patients
Methods of SVV Assessment
Sensitivity (% of Patients Showing Pathological Tilts); Results in Degrees ( )
Number of Trials; Normal Range
Central Vestibular Disorders Brainstem Brandt and Dieterich, 1992 (20)
Dieterich and Brandt, 1993 (21)
Baier et al., 2012 (22) Yang et al., 2014 (23) Cnyrim et al., 2007 (24) Cerebellum Baier et al., 2008 (25)
Kim et al., 2009 (26) Baier and Dieterich, 2009 (27) Thalamus Dieterich and Brandt, 1993 (28) Cortex Brandt et al., 1994 (29)
10 trials; 6 2
53%; Mean tilt: Contravesive:4.2 ; SD,4.4 Ipsiversive:4.5 ; SD, 5.1 50%; Mean tilt: contraversive 7.04 ipsiversive 4.23 Not mentioned; Mean 9.8
7 trials; 6 2.5
N/A (chose those with abnormal SSV to start with) Tilt: Contra: 8.7 , range 3.5–15.0 Ipsi:4.8 , range 3.3–19.8 Comment: lesions in dentate gyrus lead to contraversive SVV 79%; Range from 3.11 to 24.25 in the abnormal population
7 trials; 6 2.5
Dome test
85% Median tilt: Contravesive:5.1 Ipsiversive: 5.8
7 trials; 6 2.5 (not mentioned, but assumed from ref 11)
35 patients with thalamic infarctions; seen within 5 days
Dome test
59%; Range: 4.1 to 12.7
10 trials; 6 2.5
71 patients: 52 patients in the MCA 15 patients in the PCA 4 patients in the ACA; ‘‘acute/ subacute’’ 54 stroke patients; Mean time since stroke was 5.7 days
Dome test
44% of MCA patients; Range from 6 to 15 for MCA patients, No SVV impairment for PCA or ACA 35% had tilt > 2.5 ; Tilt amount not mentioned
10 trials; 6 2.5
Laboratory based Dome test
31 patients with unilateral cerebellar infarction; Seen within 1–12 days
Dome test
14 patients with posterior inferior cerebellar artery infraction within 12 days of onset 56 unilateral cerebellar infarctions; seen within 12 days
Laboratory setup
Dome test
Dome test Laboratory setup with joystick Dome test
Special googles (AthermalÒ GSF 166 DIN)
10 trials; 6 2
10 trials; 6 3 10 trials; N/A
10 trials; 6 2
12 trials; 6 2.5
(Continued )
A. Shaban et al.
Baier et al., 2012 (30)
94% in all patients; Midbrain: 94% Pons:91% Medulla: 94% Range in Wallenberg: 2.7 to 53.3 94%; Mean of 8.1 Range: 2–26
111 vascular brainstem lesions, including 36 Wallenberg‘s syndrome; Seen range day 1 to week 9 110 healthy controls and 111 vascular brainstem lesions; time since onset is not mentioned; but suspect same patients as in ref (20) ie seen between day 1- week 9 79 patients with subacute brainstem strokes; seen mean day 6 (SD 3 days) 82 unilateral infarction of brainstem; seen within 10 days 100 patients; 50 with Wallenberg’s syndrome (seen within 1 month) 50 with vestibular neuritis
Reference
Population (#Enrolled; Diagnosis; when Evaluated Post Symptom Onset)
Methods of SVV Assessment
Sensitivity (% of Patients Showing Pathological Tilts); Results in Degrees ( )
Number of Trials; Normal Range
Central Vestibular Disorders Baier et al., 2013 (31)
10 patients with insular strokes; seen at 5 days, SD 1.4 days
Dome test
100% of patients had normal SVV
7 trials; 6 2.5
Not mentioned
100%; median of 7.3 for VN median of 7.9 for VPN
Not mentioned
Dome test (took 15 min) and Bucket test (took 5 min)
Not mentioned how many of patients were abnormal. In patients: 8.9 6 5.4
10 trials; controls: 0.9 6 0.7
Laboratory setup
94%; Mean tilt of 6.8 6 4.3
10 trials; 6 2
Laboratory setup
100% All ipsilesional Tilt: 11 6 6
5 trials; 6 2
Bucket test
Sensitivity to differentiate CVD from VM: 74.1%, specificity 91.7% Tilt: CVD 4.8 6 4.1 VM 0.7 6 1.0
3 trials; 6 2.3
Bucket test
N/A; No good cutoff points differentiated controls from patients
3 trials; N/A
Bucket test
45%; Range from 3.1 to 5.3
10 trials; 6 3
Laboratory setup
Result: SVV greater in patient group than control group
6 trials; N/A
Laboratory setup
10%; Single patient at 3.5
4 trials; 6 3
Maddox rod lenses fitted to slit lamp
62.5% patients showed statistically significant changes in their SVV from baseline to post Hallpike
3 trials; 2
Peripheral Vestibular Disorders inner ear Cnyrim et al., 2008 (32)
83 patients; 40 with vestibular neuritis 43 with vestibular pseudoneuritis; seen within 72 hours of presentation Zwergal et al., 2009 (33) 30 healthy controls and 30 patients with acute vestibular lesions; not mentioned when seen Kim et al., 2008 (34) 51 patients with acute vestibular neuritis (abnormal calorics); seen within 7 days of onset Post Vestibular Schwannoma Resection Bo¨hmer 1999 (35) 40; Seen within 2 weeks postop (assumed from (36)) Migraine Chang et al., 2019 (37) 27 subacute/chronic strokes (CVD) and 36 vestibular migraine VM); seen 3 day to 1 month post onset BPPV Cohen and Sangi-Haghpeykar, 50 healthy controls, 25 patients 2012 (38) with benign paroxysmal positional vertigo, and 25 patients with vestibular weakness Ferreira et al., 2017 (39) 20 patients with benign paroxysmal positional vertigo Faralli et al., 2011 (40) 20 healthy controls, 30 patients with benign paroxysmal positional vertigo Boles-Aguirre and Sanchez10 patients with benign Ferrandiz, 2005 (41) paroxysmal positional vertigo Gall et al., 1999 (42) 16 patients with posterior canal benign paroxysmal positional vertigo
Bucket Test and Detection of Stroke
Table 3. Continued
BPPV = Benign positional vertigo; MCA = middle cerebral artery; PCA = posterior cerebral artery; ACA = anterior cerebral artery; CVD = cardiovascular disease.
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identified, and does not reflect the percentage of patients presenting to the ED with acute dizziness. Second, not all AVS patients were assessed by the HINTS-plus, so we could not compare data from the BT with that obtained from the HINTS-plus. We excluded patients with drug-seeking behavior, which makes our results inapplicable to this population. The rationale for excluding those patients is that dizziness was no longer their primary symptom after examination, and therefore they no longer fit the enrollment criteria. In addition, discharge diagnoses were taken from the charts, which at times had incomplete information. For example, some patients diagnosed with AVS had no documentation of nystagmus. This is why we used brain MRI as the gold standard against which BT was compared. Third, brain MRI was not required in all and was left to the decision of the treating team, leaving open the possibility that we missed some strokes or other central nervous system pathologies. Concerning the equivocal findings, even if we added those to the abnormal results, the sensitivity would still remain at 100% and specificity would still remain low (31%). Furthermore, we chose to perform 3 attempts for each patient to facilitate feasibility in ED setting, and cannot rule out that more attempts may improve the accuracy of the test. We did not limit our study to patients with the AVS because nystagmus might be missed in the ED (19). CONCLUSION The bucket test is a simple, cheap, safe, quick, and feasible test that could be used in the acute setting to screen dizzy patients for stroke in EDs. REFERENCES 1. Kerber KA, Brown DL, Lisabeth LD, Smith MA, Morgenstern LB. Stroke among patients with dizziness, vertigo, and imbalance in the emergency department: a population-based study. Stroke 2006;37: 2484–7. 2. Choi JH, Park MG, Choi SY, et al. Acute Transient Vestibular Syndrome: Prevalence of Stroke and Efficacy of Bedside Evaluation. Stroke 2017;48:556–62. 3. Kattah JC, Talkad AV, Wang DZ, Hsieh YH, Newman-Toker DE. HINTS to diagnose stroke in the acute vestibular syndrome: three-step bedside oculomotor examination more sensitive than early MRI diffusion-weighted imaging. Stroke 2009;40:3504–10. 4. Kerber KA, Meurer WJ, Brown DL, et al. Stroke risk stratification in acute dizziness presentations: A prospective imaging-based study. Neurology 2015;85:1869–78. 5. Newman-Toker DE, Kattah JC, Alvernia JE, Wang DZ. Normal head impulse test differentiates acute cerebellar strokes from vestibular neuritis. Neurology 2008;70:2378–85. 6. Oppenheim C, Stanescu R, Dormont D, et al. False-negative diffusion-weighted MR findings in acute ischemic stroke. AJNR Am J Neuroradiol 2000;21:1434–40. 7. Dumitrascu OM, Torbati S, Tighiouart M, Newman-Toker DE, Song SS. Pitfalls and Rewards for Implementing Ocular Motor Testing in Acute Vestibular Syndrome: A Pilot Project. Neurologist 2017;22:44–7.
8. Zwergal A, Rettinger N, Frenzel C, Dieterich M, Brandt T, Strupp M. A bucket of static vestibular function. Neurology 2009;72:1689–92. 9. Dieterich M, Brandt T. Perception of Verticality and Vestibular Disorders of Balance and Falls. Front Neurol 2019;10:172. 10. Piscicelli C, Perennou D. Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization. Ann Phys Rehabil Med 2017;60:208–16. 11. Bjasch D, Bockisch CJ, Straumann D, Tarnutzer AA. Differential effects of visual feedback on subjective visual vertical accuracy and precision. PLoS One 2012;7:e49311. 12. Zwergal A, Dieterich M. Vertigo and dizziness in the emergency room. Curr Opin Neurol 2020;33:117–25. 13. Baier B, Dieterich M. Ocular tilt reaction: a clinical sign of cerebellar infarctions? Neurology 2009;72:572–3. 14. Michelson PL, McCaslin DL, Jacobson GP, Petrak M, English L, Hatton K. Assessment of Subjective Visual Vertical (SVV) Using the "Bucket Test" and the Virtual SVV System. Am J Audiol 2018;27:249–59. 15. Chang TP, Winnick AA, Hsu YC, Sung PY, Schubert MC. The bucket test differentiates patients with MRI confirmed brainstem/ cerebellar lesions from patients having migraine and dizziness alone. BMC Neurol 2019;19:219. 16. Choi SY, Lee SH, Kim HJ, Kim JS. Impaired modulation of the otolithic function in acute unilateral cerebellar infarction. Cerebellum 2014;13:362–71. 17. Kim HA, Lee H, Yi HA, Lee SR, Lee SY, Baloh RW. Pattern of otolith dysfunction in posterior inferior cerebellar artery territory cerebellar infarction. J Neurol Sci 2009;280:65–70. 18. Mohwald K, Bardins S, Muller HH, Jahn K, Zwergal A. Protocol for a prospective interventional trial to develop a diagnostic index test for stroke as a cause of vertigo, dizziness and imbalance in the emergency room (EMVERT study). BMJ Open 2017;7:e019073. 19. Kerber KA, Morgenstern LB, Meurer WJ, et al. Nystagmus assessments documented by emergency physicians in acute dizziness presentations: a target for decision support? Acad Emerg Med 2011;18:619–26. 20. Brandt T, Dieterich M. Cyclorotation of the eyes and subjective visual vertical in vestibular brain stem lesions. Ann N Y Acad Sci 1992;656:537–49. 21. Dieterich M, Brandt T. Ocular torsion and tilt of subjective visual vertical are sensitive brainstem signs. Ann Neurol 1993;33:292–9. 22. Baier B, Thomke F, Wilting J, Heinze C, Geber C, Dieterich M. A pathway in the brainstem for roll-tilt of the subjective visual vertical: evidence from a lesion-behavior mapping study. J Neurosci 2012;32:14854–8. 23. Yang TH, Oh SY, Kwak K, Lee JM, Shin BS, Jeong SK. Topology of brainstem lesions associated with subjective visual vertical tilt. Neurology 2014;82:1968–75. 24. Cnyrim CD, Rettinger N, Mansmann U, Brandt T, Strupp M. Central compensation of deviated subjective visual vertical in Wallenberg’s syndrome. J Neurol Neurosurg Psychiatry 2007;78:527–8. 25. Baier B, Bense S, Dieterich M. Are signs of ocular tilt reaction in patients with cerebellar lesions mediated by the dentate nucleus? Brain 2008;131:1445–54. 26. Kim HA, Lee H, Yi HA, Lee SR, Lee SY, Baloh RW. Pattern of otolith dysfunction in posterior inferior cerebellar artery territory cerebellar infarction. J Neurol Sci 2009;280:65–70. 27. Baier B, Dieterich M. Ocular tilt reaction: a clinical sign of cerebellar infarctions? Neurology 2009;72:572–3. 28. Dieterich M, Brandt T. Thalamic infarctions: differential effects on vestibular function in the roll plane (35 patients). Neurology 1993; 43:1732–40. 29. Brandt T, Dieterich M, Danek A. Vestibular cortex lesions affect the perception of verticality. Ann Neurol 1994;35:403–12. 30. Baier B, Suchan J, Karnath HO, Dieterich M. Neural correlates of disturbed perception of verticality. Neurology 2012;78:728–35. 31. Baier B, Conrad J, Zu Eulenburg P, et al. Insular strokes cause no vestibular deficits. Stroke 2013;44:2604–6. 32. Cnyrim CD, Newman-Toker D, Karch C, Brandt T, Strupp M. Bedside differentiation of vestibular neuritis from central "vestibular pseudoneuritis. J Neurol Neurosurg Psychiatry 2008;79:458–60.
Bucket Test and Detection of Stroke 33. Zwergal A, Rettinger N, Frenzel C, Dieterich M, Brandt T, Strupp M. A bucket of static vestibular function. Neurology 2009; 72:1689–92. 34. Kim HA, Hong JH, Lee H, et al. Otolith dysfunction in vestibular neuritis: recovery pattern and a predictor of symptom recovery. Neurology 2008;70:449–53. 35. Bohmer A, Mast F. Assessing otolith function by the subjective visual vertical. Ann N Y Acad Sci 1999;871:221–31. 36. Bohmer A, Mast F, Jarchow T. Can a unilateral loss of otolithic function be clinically detected by assessment of the subjective visual vertical? Brain Res Bull 1996;40:423–7. 37. Chang TP, Winnick AA, Hsu YC, Sung PY, Schubert MC. The bucket test differentiates patients with MRI confirmed brainstem/ cerebellar lesions from patients having migraine and dizziness alone. BMC Neurol 2019;19:219.
9 38. Cohen HS, Sangi-Haghpeykar H. Subjective visual vertical in vestibular disorders measured with the bucket test. Acta Otolaryngol 2012;132:850–4. 39. Ferreira MM, Gananca MM, Caovilla HH. Subjective visual vertical after treatment of benign paroxysmal positional vertigo. Braz J Otorhinolaryngol 2017;83:659–64. 40. Faralli M, Manzari L, Panichi R, et al. Subjective visual vertical before and after treatment of a BPPV episode. Auris Nasus Larynx 2011;38:307–11. 41. Boleas-Aguirre FM, Sanchez-Ferrandiz N, Perez N. The subjective visual vertical in benign paroxysmal positional vertigo. A preliminary study. Rev Laryngol Otol Rhinol (Bord) 2005;126:253–5. 42. Gall RM, Ireland DJ, Robertson DD. Subjective visual vertical in patients with benign paroxysmal positional vertigo. J Otolaryngol 1999;28:162–5.
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ARTICLE SUMMARY 1. Why is the topic important? Dizzy patients due to posterior circulation strokes continue to be missed. There is need to improve detection of stroke in the acutely dizzy patient. 2. What does this study attempt to show? This study is a feasibility and utility study of a screening tool for stroke in the acutely dizzy patient. 3. What are the key findings? The key finding is that the Bucket test, which is a safe, quick, cheap and easy to use test, might be useful as a screening tool for stroke in the acutely dizzy patient. 4. How is patient care impacted? Currently, one third of the acutely dizzy patients due to posterior circulation strokes are missed. Using the bucket test as a screening tool in emergency departments may help improve detection of stroke in the acutely dizzy patient.
https://doi.org/10.1016/j.jemermed.2020.10.052
Selected Topics: Neurological Emergencies
THE BUCKET TEST IMPROVES DETECTION OF STROKE IN PATIENTS WITH ACUTE DIZZINESS Amir Shaban, MD,* Atif Zafar, MD,* Bernadette Borte, MD,* Yasir Elhawi, MD,† Ali Maamar-Tayeb, MD,* Patrick Ten Eyck, PHD,‡ Azeemuddin Ahmed, MD, MBA,† Anne-Sophie Wattiez, PHD,§ǁ and Deema Fattal, MD*{ *Department of Neurology, The University of Iowa, Iowa City, Iowa, †Department of Emergency Medicine, The University of Iowa, Iowa City, Iowa, ‡Institute for Clinical and Translational Science, The University of Iowa, Iowa City, Iowa, §Department of Molecular Physiology and Biophysics, University of Iowa, Iowa City, Iowa, ǁCenter for the Prevention and Treatment of Visual Loss, Iowa Veterans Affairs Health Care System, Iowa City, Iowa, and {The Veteran’s Administration Medical Center, Iowa City, Iowa Corresponding Address: Deema Fattal, MD, Department of Neurology, The University of Iowa, 200 Hawkins Dr, 2007 Roy Carver Pavilion, Iowa City, IA 52242
, Abstract—Background: It is challenging to detect posterior circulation strokes in patients presenting to the emergency department (ED) with acute dizziness. The current approach uses a combinatorial head-impulse, nystagmus, and test-of-skew method and is sensitive enough to differentiate central causes from peripheral ones. However, it is difficult to perform and underused. Further, magnetic resonance imaging (MRI) of the brain is not always available and can have low sensitivity for detecting posterior circulation strokes. Objectives: We evaluated the feasibility and utility
of the bucket test (BT), which measures the difference between patient’s subjective perception of the visual vertical and the true vertical, as a screening tool for stroke in patients presenting to the ED with acute dizziness. Methods: In this work, we prospectively enrolled 81 patients that presented to our academic medical center ED with dizziness as their chief complaint. The BT was performed 3 times for every patient. Results: Seventy-one patients met the study criteria and were included in the analysis. Ten patients were excluded because of a history of drug-seeking behavior. There were no reported difficulties performing the BT. Six patients (8%) were diagnosed with ischemic stroke on MRI and 1 additional patient was diagnosed with transient ischemic attack and found to have a stroke on subsequent MRI. All 7 patients with dizziness attributed to cerebrovascular etiology had an abnormal BT, resulting in a sensitivity of 100% (95% confidence interval [CI] 59–100%). The specificity of the BT was 38% (95% CI 24–52%). The positive predictive value of the BT for detecting stroke was 18% (95% CI 15–21%). Conclusions: The BT is an easy, cheap, safe, and quick test that is feasible and sensitive to screen acutely dizzy patients for stroke in the ED. Ó 2020 Published by Elsevier Inc.
Reprints are not available from the authors. Presented as a poster at the International Stroke Conference 2016, February 17–19, Los Angeles, California. DF: conceived the study; designed the trial; obtained IRB approval; trained the rest of the authors on performing the Bucket Test; and drafted first draft of manuscript and finalized the final draft. No funding supported this work. BB, YE, AMT, AA: recruited patients and performed the Bucket Test. AZ: recruited patients and prepared data in tables. DF, AA: supervised the conduct of the trial and data collection. AS, ASW: reviewed data; prepared the final draft of manuscript; and contributed to analysis of data. PTE: provided statistical support and advice. All authors reviewed the manuscript and DF, AA, AZ contributed substantially to the revisions. DF takes responsibility for the paper as a whole.
, Keywords—acute vestibular syndrome; bucket test; dizziness; HINTS; posterior circulation stroke; subjective visual vertical
RECEIVED: 25 January 2020; FINAL SUBMISSION RECEIVED: 17 October 2020; ACCEPTED: 22 October 2020 1
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INTRODUCTION Acute dizziness represents a diagnostic challenge for neurologists and emergency department (ED) providers. Dizziness is among the most common chief complaint, accounting for approximately 3% to 4% of ED visits in the United States (1). Most causes of dizziness are related to peripheral vestibular etiologies or medical conditions, yet a small but significant percentage is central, mostly because of stroke (1). Acute vestibular syndrome (AVS) is a syndrome of dizziness of any description that is caused by acute unilateral or asymmetrical vestibular system dysfunction and that lasts for hours and is associated with nystagmus. The AVS can be related to peripheral (inner ear) or central (posterior fossa) causes; about 25% of patients with AVS have an underlying central nervous system etiology, including acute ischemic or hemorrhagic stroke (2,3). The gold standard tool for stroke diagnosis is magnetic resonance imaging (MRI) of the brain, which has good yields compared with computed tomography (CT) scans for identifying acute ischemic strokes, but has low sensitivity for posterior circulation strokes (2– 6). Furthermore, MRI of the brain is not widely available in smaller hospitals and cannot be relied upon to screen for stroke in patients with dizziness. In the absence of a standardized and feasible protocol, evaluating patients with dizziness continues to be a challenge. As a result, one third of acute ischemic strokes in the posterior circulation that present with dizziness are misdiagnosed (1). To reduce misdiagnosing stroke in patients who are acutely dizzy, the combinatorial clinical examination of head-impulse, nystagmus, and test-of-skew (HINTS) or HINTS plus (adding acute hearing loss) has been proposed by neuro-otologists as a sensitive method to differentiate central causes of acute dizziness from peripheral causes (3,7). The HINTS test performed by a trained neurologist is reported to have a sensitivity of 100% and specificity of 96% for stroke (using diffusionweighted imaging MRI as their reference standard, including repeating MRI if the initial MRI was negative) (3). However, the HINTS examination is difficult to perform and requires special training, and for these reasons remains greatly underused by emergency physicians and neurologists (7). In this work we explored the feasibility of using a cheap, readily available, and simple test, the bucket test (BT), for screening ED patients for stroke. The BT is a previously validated test that measures a patient’s subjective and visual perception of the vertical, known as the subjective visual vertical (SVV), which normally coincides with the true vertical of earth’s gravity direction (verdical vertical) (8). SVV is accomplished through the
vestibular system, and is the product of bilateral graviceptive input from the vertical semicircular canals and otolith organs to the vestibular nuclei with integration of signals from multiple other centers including rostral midbrain, cerebellum, and thalamus (9,10). The vestibular input is also integrated with somatosensory and visual information to achieve a correct perception of the vertical body position in relation to the center of gravity (9). SVV is commonly impaired in conditions that result in acute vestibular dysfunction, including stroke (9). In this study, we sought to determine the feasibility and utility of the BT in screening for acute stroke in ED patients with dizziness. The significance of this work lies in the fact that it screens patients in the acute setting of the ED. All published studies to date measured SVV in patients already known to have strokes, and did so days to months after the insult, when we know that deviation decreases during the course of the recovery. Furthermore, they measured SVV in the laboratory setting and not in the acute setting of the ED. The present study has the advantage of assessing SVV directly at the time patients present to ED with a quick, safe, easy to make, easy to use, and cheap screening tool for stroke. METHODS We prospectively enrolled 81 patients that presented to our academic medical center ED with the chief complaint of dizziness between February 2012 and February 2015. In this work, ‘‘dizziness’’ was used to encompass any sense of vertigo, lightheadedness, or any nonspecific dizziness because any type of dizziness can occur in stroke (1). Patients were identified by an emergency physician or neurology residents who contacted the research team for evaluation. We excluded 10 patients from the final analysis because of a history of drugseeking behavior resulting in new primary complaints that did not fit the inclusion criteria and were beyond the scope of our study. The final analysis included 71 patients. To measure SVV we used a simple, handheld tool, i.e., a plastic bucket (8). The bucket is equipped with a level that was fixed on the outer surface facing the examiner to measure the true vertical alignment (Figure 1). On the inner surface of the bucket facing the patient was a line of stars that glowed in the dark. Patients were given the bucket with the stars initially oriented horizontally (90 ) and were asked to place their face inside the plastic bucket to avoid visual cues, and to turn the bucket around in order to vertically align the stars on the interior surface of the bucket. The difference in degrees between the patient’s SVV and the true vertical alignment (SVV tilt) was documented for each attempt, to left or right of the
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Figure 1. Bucket test.
vertical 0. Each patient repeated the test 3 times, and previous results were not disclosed to the patient in between attempts as to not induce bias (11). The number of trials was chosen to balance the need for accuracy of the result and the feasibility in ED context. The bucket was considered misaligned, and the attempt abnormal, if patient’s SVV was >2 different than the true vertical (10). The BT was scored as abnormal if patient misaligned the bucket on 2 of 3 attempts and the deviation was consistently toward one side. An equivocal result was scored when patient misaligned the bucket inconsistently, sometimes to the left and other times to the right or when only 1 attempt was abnormal. The BT was considered normal when all 3 attempts showed deviation of #2 . The senior author (Dr Fattal, a neurologist specialized in balance/dizziness disorders) trained the rest of the research team clinicians to perform the test reliably (a stroke neurologist [Dr Shaban], an ED specialist [Dr Ahmed], an emergency medicine resident [Dr Elhawi], and neurology residents Drs Borte, Maamar-Tayeb, and Zafar]). Only 1 researcher conducted the test at a time for a given patient, so interrater reliability could not be calculated. Researchers performing the BT were blinded to patients’ history (except for the presence of dizziness), neurologic examination, and diagnosis. Other parts of clinical care were left to the discretion of the treating
physicians. After performing the BT, the research team extracted demographic variables, risk factors, imaging findings, and final discharge diagnoses from the patients’ medical records. We used exact (Fisher and Clopper-Pearson) methods for testing specificity and sensitivity values and the 2sample t test to compare means of continuous measures. For sample size calculations, assuming a null sensitivity of 70% as seen in the literature, where sensitivity ranges from 50% to 90%, we would need a total sample size of 17 (which should encompass 11 abnormal observations) to conclude that the true sensitivity differs with $80% power (10). This study was approved by our institutional review board (201904817) and all patients provided informed consent before participating in this study. RESULTS Of the 81 patients enrolled in the study, 71 were included in the final analysis (Figure 2). Details regarding the demographic variables and stroke risk factors in our study population are provided in Table 1. Most patients presented with isolated dizziness (n = 48) with no associated neurologic symptoms. However, 10 patients on presentation reported associated headache, 6 patients had blurred vision, 5 patients had unilateral numbness, 3 patients had unilateral weakness, and 2 patients had syncope. A total
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Number of Pa ents=81 10 excluded Number of Pa ents=71
Number of pa ents=22 BT
MRI
Normal=15
Stroke=7
Abnormal BT=40
Normal=20 Equivocal=11
Figure 2. Flow chart.
of 22 patients had brain MRIs, a decision left to the discretion of the treating emergency physicians. In our sample, benign paroxysmal positional vertigo was the most common cause and was the ultimate diagnosis in 14 cases. Other neurologic causes included 7 patients with stroke or transient ischemic attack (TIA), 4 patients with tumors, 3 patients with migraines, and 2 patients with Chiari malformation. Three cases were diagnosed with peripheral vestibulopathy. Metabolic causes of dizziness were also common in our sample, including 14 patients with dehydration or orthostatic hypotension and 3 patients with underlying cardiac issues. Hypoglycemia, anemia, and respiratory failure were among the other metabolic etiologies noted. The etiology remained unknown in 10 patients. Causes of dizziness in our sample are summarized in Table 2. All 71 patients were able to perform the 3 BTs with no reported difficulties or adverse events. The testing itself only took 1 to 2 min. Forty patients had abnormal test results, whereas 11 patients had equivocal results. The remaining 20 patients had completely normal test results. Of the 7 patients who were eventually diagnosed with a stroke or TIA, 6 patients had brain MRI on presentation Table 1. Baseline Characteristics Variable
Frequency in Total Sample (n = 71)
Mean age, years (SD) Gender, female (%) History of HTN History of DM History of HLD History of CAD Smoking Alcohol abuse Substance abuse History of prior stroke History of A-fib History of Migraines
53 (15.4) 41 (57%) 24 (34%) 13 (18%) 10 (14%) 9 (13%) 33 (46%) 5 (7%) 1 (1%) 5 (7%) 4 (6%) 6 (8%)
SD = standard deviation; HTN = hypertension; DM = diabetes mellitus; HLD = hyperlipidemia; CAD = coronary artery disease; A-fib = atrial fibrillation.
that confirmed the diagnosis of stroke. While 1 patient had a TIA with negative CT and was discharged from the ED, to return 12 days later with dizziness again, at which time the brain MRI showed a subacute ischemic stroke. Of the 7 patients with ischemic strokes or TIA, most occurred in the posterior circulation, involving the cerebellum with or without the brainstem. In 1 patient, who presented with dizziness and right hearing loss, the initial examination and diagnosis was right deafness and the initial brain MRI was read as negative; however, upon further review, the patient was found to have left beating nystagmus and upon re-examination of the brain MRI, the report was edited to reflect a subtle acute right anterior inferior cerebellar artery stroke changes that were initially read as artifact. All 7 patients with stroke or TIA had abnormal BT. Therefore, the BT sensitivity for ischemic stroke was 100% (95% confidence interval 59–100%). The specificity of the BT was 38% (95% confidence interval 24–52%). The positive predictive value of the BT for detecting stroke was 18% (95% confidence interval 15–21%). The mean SVV tilt in patients with stroke was 7.6 compared with 4.4 for patients without stroke (p = 0.006). Details regarding the BT results stratified by the etiology of dizziness are provided in Table 2. The BT was positive in 12 of 24 (50%) patients who were ultimately diagnosed with metabolic problem as a cause for their dizziness. DISCUSSION Neurologic causes of acute dizziness in the ED were common in our sample. Stroke was diagnosed in 10% of our patients, which is within the range of previously reported values of 4% to 15% (12). Benign positional vertigo and non-neurologic causes were the most common etiologies for acute dizziness in our sample population, consistent with the published literature. Our study showed that the BT was easy to perform, safe, fast, reliable, and sensitive to detect ischemic strokes in patient with acute dizziness. The BT is also easily made and is inexpensive, the analysis of the result is simple even for the nonspecialist, and as such the BT may be useful to screen for ischemic stroke in patients presenting to ED with acute dizziness. We believe that performing >1 test attempt for each patient was feasible and necessary to confirm a consistent result. Previous studies have shown that acute lesions involving the vestibular system (including stroke), can result in SVV tilt (13). Table 3 summarizes previously published studies measuring SVV tilt in pathologic conditions. The SVV tilt can remain abnormal for days after the insult (13). Several laboratory-based methods for
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Table 2. The Results of the Bucket Test per Discharge Diagnosis
Ischemic stroke/TIA BPPV Dehydration/hypovolemia Labyrinthitis Meniere’s Migraines Substance/alcohol Other CNS cause Other medical problems Unknown Total
Positive BT (Abnormal)
Negative BT (Normal)
Equivocal BT
7 8 8 1 1 1 2 2 4 6 40
0 3 5 0 0 2 0 4 4 2 20
0 3 1 2 0 0 0 1 2 2 11
BT = Bucket Test; TIA = transient ischemic attack; BPPV = Benign paroxysmal positional vertigo; CNS = central nervous system.
measuring SVV were applied in previous studies, such as the hemispheric dome test, or using the virtual SVV system (14). The BT test and the laboratory-based dome test have high concordance, and the virtual SVV system yields similar results than the BT, albeit with increased precision (8). However, the virtual SVV system requires more expensive equipment (e.g., googles and a computer) and would take longer to use than the simple BT. While previous studies evaluated the BT in patients with known ischemic stroke, outpatient clinic settings, or research settings comparing healthy subjects to subjects with dizziness, our study is the first to use the BT in the real acute setting of the ED and in a nondiagnosed and diverse patient population presenting with acute dizziness (8,13,15). The association between ischemic stroke and SVV abnormalities has been shown in the published literature. In a study of 27 patients with cerebellar strokes (seen <2 weeks after onset) and using laboratorybased SVV measurements, it was noted that 56% of patients had abnormal SVV (16). Another study included 43 patients seen 1 to 12 days after cerebellar strokes, of which 84% had abnormal SVV, as measured in the laboratory (13). Piscicelli and Perennou reviewed SVV in stroke, and in that review the strokes that were called acute were evaluated on average several days to 2 weeks after the onset, a period during which SVV can start to normalize (10,13). Our stroke patients all presented the same day of the onset of dizziness, potentially explaining our higher sensitivity. The direction of the SVV tilt is either ipsilateral or contralateral to the stroke in previous studies (9,13,17). Specifically, strokes of the dorsolateral medulla, anterior inferior cerebellar artery, lateral posterior inferior cerebellar artery (PICA), and medial PICA strokes that do not involve the nodulus all give ipsilateral SVV abnormality, whereas medial PICA that involve the nodulus cause contralateral SVV (17). Similarly, in our study, all had ipsilateral SVV tilt, toward the side of the stroke, and our strokes were in PICA (without nodulus involvement), anterior inferior cerebellar artery, and dorsolateral
medulla territories. Of note, anterior circulation strokes that involve cortical/subcortical structures have also been reported to be associated with abnormal SVV, potentially explaining the abnormal BT in our patient sample where the stroke affected the anterior circulation (9). In a recent study comparing brain MRI–confirmed brainstem or cerebellar strokes to vestibular migraines in patients presenting with migraine or dizziness alone, SVV abnormalities, measured using the BT, were significantly higher in patients with strokes examined 1 day to 2 months after stroke onset (15). Furthermore, using the BT alone to differentiate strokes from migraine resulted in a sensitivity of 74% and specificity of 92% (15). In our sample, however, the specificity and the positive predictive value of the BT in detecting stroke were low, possibly because we included all patients with dizziness (including metabolic causes). For those reasons, even though the BT may be useful for screening, it should be followed by other, more specific tests that evaluate patients with acute dizziness, such as more detailed neurologic examination, neurologic consultation, HINTS, or brain MRI. The BT is currently being investigated in the EMVERT clinical trial, which is enrolling patients presenting to the emergency department with acute onset of dizziness. The SVV will be used along with other tools, including video-oculography and mobile posturography, as screening tools to detect stroke (18). Limitations This study has several limitations. First, we cannot calculate the k agreement of the BT because only 1 researcher conducted the test at a time. Small sample size and the large number of conditions that can cause dizziness limited our ability to detected potential differences in the performance of the BT to screen for these conditions. The small sample size/recruitment rate for this study depended on the ability of ED teams to contact the research team when an eligible and interested patient was
Reference
Population (#Enrolled; Diagnosis; when Evaluated Post Symptom Onset)
6
Table 3. Subjective Visual Vertical (SVV) Tilts in Stroke Patients
Methods of SVV Assessment
Sensitivity (% of Patients Showing Pathological Tilts); Results in Degrees ( )
Number of Trials; Normal Range
Central Vestibular Disorders Brainstem Brandt and Dieterich, 1992 (20)
Dieterich and Brandt, 1993 (21)
Baier et al., 2012 (22) Yang et al., 2014 (23) Cnyrim et al., 2007 (24) Cerebellum Baier et al., 2008 (25)
Kim et al., 2009 (26) Baier and Dieterich, 2009 (27) Thalamus Dieterich and Brandt, 1993 (28) Cortex Brandt et al., 1994 (29)
10 trials; 6 2
53%; Mean tilt: Contravesive:4.2 ; SD,4.4 Ipsiversive:4.5 ; SD, 5.1 50%; Mean tilt: contraversive 7.04 ipsiversive 4.23 Not mentioned; Mean 9.8
7 trials; 6 2.5
N/A (chose those with abnormal SSV to start with) Tilt: Contra: 8.7 , range 3.5–15.0 Ipsi:4.8 , range 3.3–19.8 Comment: lesions in dentate gyrus lead to contraversive SVV 79%; Range from 3.11 to 24.25 in the abnormal population
7 trials; 6 2.5
Dome test
85% Median tilt: Contravesive:5.1 Ipsiversive: 5.8
7 trials; 6 2.5 (not mentioned, but assumed from ref 11)
35 patients with thalamic infarctions; seen within 5 days
Dome test
59%; Range: 4.1 to 12.7
10 trials; 6 2.5
71 patients: 52 patients in the MCA 15 patients in the PCA 4 patients in the ACA; ‘‘acute/ subacute’’ 54 stroke patients; Mean time since stroke was 5.7 days
Dome test
44% of MCA patients; Range from 6 to 15 for MCA patients, No SVV impairment for PCA or ACA 35% had tilt > 2.5 ; Tilt amount not mentioned
10 trials; 6 2.5
Laboratory based Dome test
31 patients with unilateral cerebellar infarction; Seen within 1–12 days
Dome test
14 patients with posterior inferior cerebellar artery infraction within 12 days of onset 56 unilateral cerebellar infarctions; seen within 12 days
Laboratory setup
Dome test
Dome test Laboratory setup with joystick Dome test
Special googles (AthermalÒ GSF 166 DIN)
10 trials; 6 2
10 trials; 6 3 10 trials; N/A
10 trials; 6 2
12 trials; 6 2.5
(Continued )
A. Shaban et al.
Baier et al., 2012 (30)
94% in all patients; Midbrain: 94% Pons:91% Medulla: 94% Range in Wallenberg: 2.7 to 53.3 94%; Mean of 8.1 Range: 2–26
111 vascular brainstem lesions, including 36 Wallenberg‘s syndrome; Seen range day 1 to week 9 110 healthy controls and 111 vascular brainstem lesions; time since onset is not mentioned; but suspect same patients as in ref (20) ie seen between day 1- week 9 79 patients with subacute brainstem strokes; seen mean day 6 (SD 3 days) 82 unilateral infarction of brainstem; seen within 10 days 100 patients; 50 with Wallenberg’s syndrome (seen within 1 month) 50 with vestibular neuritis
Reference
Population (#Enrolled; Diagnosis; when Evaluated Post Symptom Onset)
Methods of SVV Assessment
Sensitivity (% of Patients Showing Pathological Tilts); Results in Degrees ( )
Number of Trials; Normal Range
Central Vestibular Disorders Baier et al., 2013 (31)
10 patients with insular strokes; seen at 5 days, SD 1.4 days
Dome test
100% of patients had normal SVV
7 trials; 6 2.5
Not mentioned
100%; median of 7.3 for VN median of 7.9 for VPN
Not mentioned
Dome test (took 15 min) and Bucket test (took 5 min)
Not mentioned how many of patients were abnormal. In patients: 8.9 6 5.4
10 trials; controls: 0.9 6 0.7
Laboratory setup
94%; Mean tilt of 6.8 6 4.3
10 trials; 6 2
Laboratory setup
100% All ipsilesional Tilt: 11 6 6
5 trials; 6 2
Bucket test
Sensitivity to differentiate CVD from VM: 74.1%, specificity 91.7% Tilt: CVD 4.8 6 4.1 VM 0.7 6 1.0
3 trials; 6 2.3
Bucket test
N/A; No good cutoff points differentiated controls from patients
3 trials; N/A
Bucket test
45%; Range from 3.1 to 5.3
10 trials; 6 3
Laboratory setup
Result: SVV greater in patient group than control group
6 trials; N/A
Laboratory setup
10%; Single patient at 3.5
4 trials; 6 3
Maddox rod lenses fitted to slit lamp
62.5% patients showed statistically significant changes in their SVV from baseline to post Hallpike
3 trials; 2
Peripheral Vestibular Disorders inner ear Cnyrim et al., 2008 (32)
83 patients; 40 with vestibular neuritis 43 with vestibular pseudoneuritis; seen within 72 hours of presentation Zwergal et al., 2009 (33) 30 healthy controls and 30 patients with acute vestibular lesions; not mentioned when seen Kim et al., 2008 (34) 51 patients with acute vestibular neuritis (abnormal calorics); seen within 7 days of onset Post Vestibular Schwannoma Resection Bo¨hmer 1999 (35) 40; Seen within 2 weeks postop (assumed from (36)) Migraine Chang et al., 2019 (37) 27 subacute/chronic strokes (CVD) and 36 vestibular migraine VM); seen 3 day to 1 month post onset BPPV Cohen and Sangi-Haghpeykar, 50 healthy controls, 25 patients 2012 (38) with benign paroxysmal positional vertigo, and 25 patients with vestibular weakness Ferreira et al., 2017 (39) 20 patients with benign paroxysmal positional vertigo Faralli et al., 2011 (40) 20 healthy controls, 30 patients with benign paroxysmal positional vertigo Boles-Aguirre and Sanchez10 patients with benign Ferrandiz, 2005 (41) paroxysmal positional vertigo Gall et al., 1999 (42) 16 patients with posterior canal benign paroxysmal positional vertigo
Bucket Test and Detection of Stroke
Table 3. Continued
BPPV = Benign positional vertigo; MCA = middle cerebral artery; PCA = posterior cerebral artery; ACA = anterior cerebral artery; CVD = cardiovascular disease.
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identified, and does not reflect the percentage of patients presenting to the ED with acute dizziness. Second, not all AVS patients were assessed by the HINTS-plus, so we could not compare data from the BT with that obtained from the HINTS-plus. We excluded patients with drug-seeking behavior, which makes our results inapplicable to this population. The rationale for excluding those patients is that dizziness was no longer their primary symptom after examination, and therefore they no longer fit the enrollment criteria. In addition, discharge diagnoses were taken from the charts, which at times had incomplete information. For example, some patients diagnosed with AVS had no documentation of nystagmus. This is why we used brain MRI as the gold standard against which BT was compared. Third, brain MRI was not required in all and was left to the decision of the treating team, leaving open the possibility that we missed some strokes or other central nervous system pathologies. Concerning the equivocal findings, even if we added those to the abnormal results, the sensitivity would still remain at 100% and specificity would still remain low (31%). Furthermore, we chose to perform 3 attempts for each patient to facilitate feasibility in ED setting, and cannot rule out that more attempts may improve the accuracy of the test. We did not limit our study to patients with the AVS because nystagmus might be missed in the ED (19). CONCLUSION The bucket test is a simple, cheap, safe, quick, and feasible test that could be used in the acute setting to screen dizzy patients for stroke in EDs. REFERENCES 1. Kerber KA, Brown DL, Lisabeth LD, Smith MA, Morgenstern LB. Stroke among patients with dizziness, vertigo, and imbalance in the emergency department: a population-based study. Stroke 2006;37: 2484–7. 2. Choi JH, Park MG, Choi SY, et al. Acute Transient Vestibular Syndrome: Prevalence of Stroke and Efficacy of Bedside Evaluation. Stroke 2017;48:556–62. 3. Kattah JC, Talkad AV, Wang DZ, Hsieh YH, Newman-Toker DE. HINTS to diagnose stroke in the acute vestibular syndrome: three-step bedside oculomotor examination more sensitive than early MRI diffusion-weighted imaging. Stroke 2009;40:3504–10. 4. Kerber KA, Meurer WJ, Brown DL, et al. Stroke risk stratification in acute dizziness presentations: A prospective imaging-based study. Neurology 2015;85:1869–78. 5. Newman-Toker DE, Kattah JC, Alvernia JE, Wang DZ. Normal head impulse test differentiates acute cerebellar strokes from vestibular neuritis. Neurology 2008;70:2378–85. 6. Oppenheim C, Stanescu R, Dormont D, et al. False-negative diffusion-weighted MR findings in acute ischemic stroke. AJNR Am J Neuroradiol 2000;21:1434–40. 7. Dumitrascu OM, Torbati S, Tighiouart M, Newman-Toker DE, Song SS. Pitfalls and Rewards for Implementing Ocular Motor Testing in Acute Vestibular Syndrome: A Pilot Project. Neurologist 2017;22:44–7.
8. Zwergal A, Rettinger N, Frenzel C, Dieterich M, Brandt T, Strupp M. A bucket of static vestibular function. Neurology 2009;72:1689–92. 9. Dieterich M, Brandt T. Perception of Verticality and Vestibular Disorders of Balance and Falls. Front Neurol 2019;10:172. 10. Piscicelli C, Perennou D. Visual verticality perception after stroke: A systematic review of methodological approaches and suggestions for standardization. Ann Phys Rehabil Med 2017;60:208–16. 11. Bjasch D, Bockisch CJ, Straumann D, Tarnutzer AA. Differential effects of visual feedback on subjective visual vertical accuracy and precision. PLoS One 2012;7:e49311. 12. Zwergal A, Dieterich M. Vertigo and dizziness in the emergency room. Curr Opin Neurol 2020;33:117–25. 13. Baier B, Dieterich M. Ocular tilt reaction: a clinical sign of cerebellar infarctions? Neurology 2009;72:572–3. 14. Michelson PL, McCaslin DL, Jacobson GP, Petrak M, English L, Hatton K. Assessment of Subjective Visual Vertical (SVV) Using the "Bucket Test" and the Virtual SVV System. Am J Audiol 2018;27:249–59. 15. Chang TP, Winnick AA, Hsu YC, Sung PY, Schubert MC. The bucket test differentiates patients with MRI confirmed brainstem/ cerebellar lesions from patients having migraine and dizziness alone. BMC Neurol 2019;19:219. 16. Choi SY, Lee SH, Kim HJ, Kim JS. Impaired modulation of the otolithic function in acute unilateral cerebellar infarction. Cerebellum 2014;13:362–71. 17. Kim HA, Lee H, Yi HA, Lee SR, Lee SY, Baloh RW. Pattern of otolith dysfunction in posterior inferior cerebellar artery territory cerebellar infarction. J Neurol Sci 2009;280:65–70. 18. Mohwald K, Bardins S, Muller HH, Jahn K, Zwergal A. Protocol for a prospective interventional trial to develop a diagnostic index test for stroke as a cause of vertigo, dizziness and imbalance in the emergency room (EMVERT study). BMJ Open 2017;7:e019073. 19. Kerber KA, Morgenstern LB, Meurer WJ, et al. Nystagmus assessments documented by emergency physicians in acute dizziness presentations: a target for decision support? Acad Emerg Med 2011;18:619–26. 20. Brandt T, Dieterich M. Cyclorotation of the eyes and subjective visual vertical in vestibular brain stem lesions. Ann N Y Acad Sci 1992;656:537–49. 21. Dieterich M, Brandt T. Ocular torsion and tilt of subjective visual vertical are sensitive brainstem signs. Ann Neurol 1993;33:292–9. 22. Baier B, Thomke F, Wilting J, Heinze C, Geber C, Dieterich M. A pathway in the brainstem for roll-tilt of the subjective visual vertical: evidence from a lesion-behavior mapping study. J Neurosci 2012;32:14854–8. 23. Yang TH, Oh SY, Kwak K, Lee JM, Shin BS, Jeong SK. Topology of brainstem lesions associated with subjective visual vertical tilt. Neurology 2014;82:1968–75. 24. Cnyrim CD, Rettinger N, Mansmann U, Brandt T, Strupp M. Central compensation of deviated subjective visual vertical in Wallenberg’s syndrome. J Neurol Neurosurg Psychiatry 2007;78:527–8. 25. Baier B, Bense S, Dieterich M. Are signs of ocular tilt reaction in patients with cerebellar lesions mediated by the dentate nucleus? Brain 2008;131:1445–54. 26. Kim HA, Lee H, Yi HA, Lee SR, Lee SY, Baloh RW. Pattern of otolith dysfunction in posterior inferior cerebellar artery territory cerebellar infarction. J Neurol Sci 2009;280:65–70. 27. Baier B, Dieterich M. Ocular tilt reaction: a clinical sign of cerebellar infarctions? Neurology 2009;72:572–3. 28. Dieterich M, Brandt T. Thalamic infarctions: differential effects on vestibular function in the roll plane (35 patients). Neurology 1993; 43:1732–40. 29. Brandt T, Dieterich M, Danek A. Vestibular cortex lesions affect the perception of verticality. Ann Neurol 1994;35:403–12. 30. Baier B, Suchan J, Karnath HO, Dieterich M. Neural correlates of disturbed perception of verticality. Neurology 2012;78:728–35. 31. Baier B, Conrad J, Zu Eulenburg P, et al. Insular strokes cause no vestibular deficits. Stroke 2013;44:2604–6. 32. Cnyrim CD, Newman-Toker D, Karch C, Brandt T, Strupp M. Bedside differentiation of vestibular neuritis from central "vestibular pseudoneuritis. J Neurol Neurosurg Psychiatry 2008;79:458–60.
Bucket Test and Detection of Stroke 33. Zwergal A, Rettinger N, Frenzel C, Dieterich M, Brandt T, Strupp M. A bucket of static vestibular function. Neurology 2009; 72:1689–92. 34. Kim HA, Hong JH, Lee H, et al. Otolith dysfunction in vestibular neuritis: recovery pattern and a predictor of symptom recovery. Neurology 2008;70:449–53. 35. Bohmer A, Mast F. Assessing otolith function by the subjective visual vertical. Ann N Y Acad Sci 1999;871:221–31. 36. Bohmer A, Mast F, Jarchow T. Can a unilateral loss of otolithic function be clinically detected by assessment of the subjective visual vertical? Brain Res Bull 1996;40:423–7. 37. Chang TP, Winnick AA, Hsu YC, Sung PY, Schubert MC. The bucket test differentiates patients with MRI confirmed brainstem/ cerebellar lesions from patients having migraine and dizziness alone. BMC Neurol 2019;19:219.
9 38. Cohen HS, Sangi-Haghpeykar H. Subjective visual vertical in vestibular disorders measured with the bucket test. Acta Otolaryngol 2012;132:850–4. 39. Ferreira MM, Gananca MM, Caovilla HH. Subjective visual vertical after treatment of benign paroxysmal positional vertigo. Braz J Otorhinolaryngol 2017;83:659–64. 40. Faralli M, Manzari L, Panichi R, et al. Subjective visual vertical before and after treatment of a BPPV episode. Auris Nasus Larynx 2011;38:307–11. 41. Boleas-Aguirre FM, Sanchez-Ferrandiz N, Perez N. The subjective visual vertical in benign paroxysmal positional vertigo. A preliminary study. Rev Laryngol Otol Rhinol (Bord) 2005;126:253–5. 42. Gall RM, Ireland DJ, Robertson DD. Subjective visual vertical in patients with benign paroxysmal positional vertigo. J Otolaryngol 1999;28:162–5.
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ARTICLE SUMMARY 1. Why is the topic important? Dizzy patients due to posterior circulation strokes continue to be missed. There is need to improve detection of stroke in the acutely dizzy patient. 2. What does this study attempt to show? This study is a feasibility and utility study of a screening tool for stroke in the acutely dizzy patient. 3. What are the key findings? The key finding is that the Bucket test, which is a safe, quick, cheap and easy to use test, might be useful as a screening tool for stroke in the acutely dizzy patient. 4. How is patient care impacted? Currently, one third of the acutely dizzy patients due to posterior circulation strokes are missed. Using the bucket test as a screening tool in emergency departments may help improve detection of stroke in the acutely dizzy patient.