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Original Paper

Free Access

Stroke Mimics in a Stroke Care Pathway Based on MRI Screening

Quenardelle V.b · Lauer-Ober V.b · Zinchenko I.b · Bataillard M.b · Rouyer O.a, b · Beaujeux R.c · Pop R.c · Meyer N.d · Delplancq H.e · Kremer S.f · Marescaux C.b · Gény B.a, g · Wolff V.a, b

Author affiliations

aEA3072, Université de Strasbourg, Fédération de Médecine Translationnelle de Strasbourg, bUnité Neuro-Vasculaire, Service de Neurologie, cService de Neuroradiologie Interventionnelle, dService de Santé Publique, eSAMU, fService de Neuro-Radiologie, and gService de Physiologie et d'Explorations Fonctionnelles, Hôpitaux Universitaires de Strasbourg (HUS), Strasbourg, France

Corresponding Author

Dr. Valérie Wolff, MD, PhD

Unité Neuro-Vasculaire, Service de Neurologie

HUS, 1 Avenue Molière

FR-67098 Strasbourg (France)

E-Mail valerie.wolff@chru-strasbourg.fr

Related Articles for ""

Cerebrovasc Dis 2016;42:205-212

Abstract

Background: Since the use of tissue plasminogen activator for acute ischemic stroke (IS), stroke care pathways have been developed for patients with suspicion of acute stroke. The aim of this prospective observational study was to analyze the stroke mimic (SM) characteristics in patients who were part of our stroke care pathway. Methods: All consecutive patients admitted in the code stroke within a 1-year period were prospectively enrolled in this study. Patients with a sudden onset of neurological focal deficit in a time window less than 4H30 as indicated for intravenous thrombolysis, had been accepted in the pathway by a neurologist who was directly contactable by the prehospital emergency medical service 24 h per day. Patients arrived directly on the MRI site without passing by the emergency department. A clinical neurological evaluation and a brain MRI with tri-dimensional time-of-flight magnetic resonance angiography were performed. The FAST score was calculated a posteriori. The final discharge diagnosis was concluded either immediately after both neurological examination and cerebrovascular neuroimaging or after other relevant investigations. We classified the discharge diagnosis into neurovascular diseases (NVDs) and into SM. Results: There were 1,361 consecutive patients admitted for suspicion of acute stroke. Sixty-two percent (n = 840) had an NVD including IS (n = 529), transient ischemic attacks (n = 236), intracranial hemorrhages (n = 68), cerebral venous thrombosis (n = 3) and neurovascular medullar pathologies (n = 4). SM represented 38% of cases (n = 521) and the most frequent discharge diagnosis was defined as headaches (18.6%), psychological disorders (16.7%), peripheral vertigo (11.9%) and epilepsy (10.6%). The comparison between the characteristics of the NVD and those of the SM groups showed some significant differences: in the SM group, women were more represented, patients were younger and the NIHSS was lower than in the NVD group. All cardiovascular risk factors were more represented in the NVD group. Concerning the symptoms, motor deficit, speech disturbances, homonymous lateral hemianopia and head and gaze deviation were more represented in the NVD group, whereas vertigo, non-systematized visual trouble, headache, confusion, weakness, neuropsychological symptoms, seizure and chest pain were significantly more frequent in the SM group. The negative predictive value of the FAST score was 64% and the positive predictive value was 76%. Conclusions: A rate of SM up to 38% of the code stroke system confirms the difficulty to distinguish clinically a stroke from another diagnosis. In this study, using cerebral MRI in first intention was of special interest in patients with acute neurological symptoms to differentiate an NVD from an SM.

© 2016 S. Karger AG, Basel


Introduction

Since tissue plasminogen activator (t-PA) is used as the main thrombolytic therapy in acute ischemic stroke (IS), a real challenge lies in the proper diagnosis of IS as soon as possible and to transport patients quickly to the hospital [1]. Stroke care pathways have been developed on the basis of a pre-hospital notification [2,3,4,5] in order to refer patients as soon as possible to stroke units. In the clinical practice, manifestations of stroke can be uncommon, and that is sometimes a real challenge to distinguish clinical stroke from differential diagnosis. On the one hand, some non-vascular pathologies can simulate stroke and are called ‘stroke mimics (SMs)' [6,7], and on the other hand, unusual clinical presentations look like a non-vascular pathology while it is stroke in reality; they are called ‘stroke chameleons' [7,8,9]. In both cases, the mistake may be more frequent as believed, since most studies are based on a retrospective basis paradigm that may obscure the reality of their prevalence. Based on our own experience, since 2008, we prefer the use of cerebral MRI as a first screening method instead of a CT scan, because the sensitivity of MRI helps us to avoid SM and to confirm the presence of stroke in patients presenting with atypical symptoms. Part of the literature has recommended the use of MRI for this [6,7,8,9,10]. However, some authors have recently shown that CT could also be used as a first screening method with comparable reliability [11]. In our stroke unit, we alternatively use CT when MRI is contraindicated. The objectives of this study were (a) to determine respectively the prevalence of SM and of neurovascular diseases (NVDs) in a stroke care pathway for a suspicion of acute stroke in a time-window for thrombolysis, (b) to describe the demographic data and symptoms repartition into the 2 groups, (c) to describe the different subgroups of etiologies of SM, (d) to determine the rate of positive FAST score in each group.

Methods

In 2011, the stroke unit of Strasbourg University Hospital was a comprehensive center including 30 beds, and 8 out of them were identified for intensive care. Patients came from the department of Bas-Rhin with a surface of 4,755 km2, which comprised 1,099,579 inhabitants. All consecutive patients admitted in our stroke care pathway between February 8, 2011 and February 7, 2012, were prospectively enrolled in this study. Patients with a sudden onset of neurological focal deficit in a time window less than 4H30, as indicated for intravenous thrombolysis, had been accepted in the pathway by a senior neurologist. The prehospital emergency medical service (SAMU-Centre 15) can call the senior neurologist directly on a dedicated phone number on a 24 h/7 days basis. Patients arrived then directly on the MRI site without passing by the emergency department (ED), and a dedicated nurse from the intensive care stroke unit joins the neurologist immediately at the MRI site with a backpack containing all the materials needed to treat the acute phase of stroke. Neurological evaluation including NIH score scale and brain MRI including diffusion-weighted imaging (DWI, b = 0-1,000 mm2/s), FLAIR and gradient echo sequences associated with a cerebral tri-dimensional time-of-flight magnetic resonance angiography were performed. MRI imaging was performed on 1.5T MRI systems (Magnetom Avanto, Siemens or Aera, Siemens) or on 3T MRI systems (Signa HDX, General Electric, or Achieva, Philips). The MRI scan protocol duration was of 15 min and this exam was interpreted by a senior neuroradiologist. In our department, a cerebral MRI is performed for all acute suspected strokes even out of the time window for thrombolysis. When there was a contraindication for MRI, a cerebral CT scan with CT-angiography was done.

Radiological indication for a thrombolysis treatment was defined by an arterial occlusion in the territory corresponding to the focal deficit and by the FLAIR vascular hyperintensities-DWI mismatch representing the ischemic penumbra [12,13]. The radiological diagnosis could have been an NVD (such as an IS with or without indication for thrombolysis, an intracranial hemorrhage (ICH), a cerebral venous thrombosis (CVT)) or a radiological differential diagnosis such as a brain tumor. If neurovascular imaging was normal, and according to the clinical context and outcome, other investigations were performed and additional specialists were called based on recommendations.

The following clinical data were collected by the neurovascular team: demographics data, past medical history and treatment, history of the present event, time of symptoms onset, arrival time to hospital and to imaging site, time when imaging begun, clinical evaluation with NIH score scale, cerebral MRI (or CT scan) results, diagnosis hypothesis after clinical and imaging evaluations, decision of thrombolysis treatment, unit where patient was addressed after cerebral imaging and final discharge diagnosis. Cerebral imaging and discharge letter were assessed on our computer system, namely, DX-CARE. The FAST score was calculated a posteriori. This score facilitates the prehospital stroke recognition and consists of 3 items (facial weakness, arm weakness and speech disturbance) [14,15]. A FAST score was defined as positive by the presence of at least one of the 3 items. The final discharge diagnosis was concluded either immediately after both neurological examination and cerebrovascular neuroimaging or after other relevant investigations. We classified the discharge diagnosis into NVD and into SM. IS, transient ischemic attack (TIA), ICH, CVT and neurovascular medullar diseases were classified as NVD. All other pathologies corresponded to SM.

Continuous data were expressed by the mean ± SEM and categorical data as frequency (%). Continuous variables were compared with the Student's t test or with the Kruskal-Wallis test depending on whether the distribution was Gaussian or not. Categorical data were compared with a chi-square test or with a Fisher exact test. Statistical analyses were performed using R 3.0.2. A p value <0.05 was considered significant.

Results

In this 1-year period, 1,361 patients were included in the stroke care pathway, with an average of 4 ± 1.58 patients per day (range 0-10). During this period there were 754 patients admitted to our hospital with a final diagnosis of acute NVD but not included into the stroke care pathway because of the missed time window of 4H30. Cerebral MRI or CT scan was performed in respectively 96 and 4% of cases (because of the presence of pace-maker or claustrophobia). Sixty-two percent of cases had an NVD and 38% of cases displayed an SM (fig. 1). Demographic data of the whole cohort of patients addressed for a suspicion of acute stroke are presented in table 1. The NVD group represented 840 patients; 63% of cases had IS, 28% had ITA, 8% had ICH, 0.5% had CVT and 0.5% had neurovascular medullar pathologies. Cerebral reperfusion therapies (intra-venous thrombolysis and/or endovascular procedures) were performed in 29% of cases of IS, 18% of cases of NVD and 11% of all the patients involved in the pathway. The door-to-needle time in patients treated by thrombolysis was 53 ± 20 min (range 15-120) and the door-to-imaging time was 18 ± 11 min (range 1-120). Table 2 detailed the discharge diagnosis of the SM group. The most frequent diagnosis included migraine with aura in 17.3%, psychological disorder in 16.7%, peripheral vertigo in 11.9% or focal epilepsy in 10.6% of cases.

Table 1

Demographic characteristics of the 1,361 patients addressed for a suspicion of acute stroke

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Table 2

Description of the discharge diagnosis in the SM group

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Fig. 1

Repartition of the patients in the NVD and SM groups in the whole cohort of 1,361 code strokes. MP = Medullar pathology.

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The comparison between the characteristics of the NVD and those of the SM groups showed some significant demographic and clinical differences (table 1). In the SM group, women were more represented, patients were younger and the NIHSS was lower than in the NVD group. All cardiovascular risk factors were more represented in the NVD group. Concerning the symptoms, motor deficit, speech disturbances, homonymous lateral hemianopia and head and gaze deviation were more represented in the NVD group, whereas vertigo, non-systematized visual trouble, headache, confusion, weakness, neuropsychological symptoms, seizure and chest pain were significantly more frequent in the SM group (table 3). The FAST score was positive in 80% for the NVD group and positive in 41% for the SM group (p < 0.001). The negative predictive value of the FAST score was 64% and the positive predictive value was 76%.

Table 3

Types of symptoms in the NVD group and in the SM group

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Discussion

During a 1-year period, 1,361 patients were enrolled prospectively in our stroke care pathway. To our knowledge, this is the most important prospective study about the functioning of a single stroke care pathway [16,17,18,19]. An SM was found in 38% and the type of SM was similar to previous reports associating more frequently with migraine with aura, psychological symptoms, peripheral vertigo or epilepsy [17,18,20]. The SM rate of 38% seems similar or higher to the expressed by literature data [16,17,18,19,21,22,23]. Comparison between the different studies in the literature is difficult because the SM definition varies from study to study, and this phenomenon is consequently reflected by heterogeneous results. Thus, in several other studies, the rate of SM comprised between 14.6 and 31% of cases [7,16,17,21,22]. Another prospective study, however, was performed in California in similar conditions as ours; this study evaluated suspected strokes within a 5 h window. There were 1,360 patients included in this study and 32.6% out of them were SM, quite similar to our 38% of SM [18]. As in this study, we have chosen to classify the discharge diagnosis in NVD when patients displayed IS, TIA and ICH, but we added CVT and neurovascular medullar pathologies. Our high rate of patients with an SM can be due to several factors. From our point of view, it is difficult and sometimes impossible to clinically distinguish patients with an SM from patients with stroke. Hopefully imaging, such as MRI, helps clinicians to disambiguate the heterogeneity of clinical presentation of strokes [24]. MRI is more sensitive than CT scan to confirm IS during the first hours after the symptoms [6,10]. Diffusion sequence allows objectifying the presence of a cytotoxic edema related to a recent ischemia [6,10]. Some of the other advantages of MRI compared to CT scan are the explorations of the cerebellum, the trunk and the possibility to explore some SM unseen on CT-scan such as brain tumor, posterior reversible encephalopathy, encephalitis, drug toxicity and metabolic disturbances [6,25,26]. An MRI was performed in a majority of cases in our series and we show that it revealed several different diagnoses, which belong to the SM group. In others studies, a CT scan was performed in first intention with a lower rate of SM. Consequently, it may be suggested that SM rate was minimized leading to give thrombolysis treatment to SM patients [20,27,28]. Although thrombolysis treatment in SM patients did not lead to harmful complications, there is still a potential risk of cerebral hemorrhage [27]. Whatever the type of imaging was used in patients with acute neurological deficit, there is a need to identify the ischemic penumbra in order to better select the patient indicated for a thrombolysis treatment [29].

Some authors suggested that MRI-based thrombolysis was related to an improved safety compared to CT-based treatment [30,31], whereas others argued that using CT-scan allows limiting the delays between the onset of symptoms and the thrombolysis [32,33]. Indeed, ultrafast door-to-needle time (less than 25 min) has been reported by selective centers using CT [34,35]. Other authors showed, however, that using multimodal MRI as the first-line imaging does not lead to loss of time [36]. In our series, the door-to-needle was less than 60 min as recommended [37]. It is possible to further reduce this delay. It was recently suggested that this reduction of delay may be achieved by dedicating a stroke unit team on a 24 h/7 days basis, improving on-site imaging facilities [34] and by the implementation of a rapid treatment protocol [38]. The selection of patients with MRI criteria stressed the need to have access to cerebral MRI as a matter of priority 24 h/24, every day when an abrupt onset of neurological deficit is encountered [19,39]. Of course, this recommendation may lead to a reorganization of hospital departments that is not easy to set.

Another hypothesis may argue that the high SM rate in our study be related to the selection of the patients, which was done according to the data collected by prehospital health professionals who are not systematically trained in the emergency clinical pathways [40]. Indeed, Moulin et al. [41] underlined the need of neurological expertise in the recognition of neurological pathologies, especially neurovascular, in the ED. In our program, however, we have included training courses for health professionals and we urged them to appreciate the use of FAST score. Using a pre-hospital stroke scale as the FAST score in pre-hospital selection can be helpful to identify NVD [42,43]. According to Goldstein and Simel [43], the presence of acute facial palsy, arm drift, or abnormal speech increased the likelihood of stroke. These data are akin to our results showing a positive predictive value of the FAST score of 76% and a negative predictive value of 64%.

As in other studies, patients of the SM group in our study were younger, more frequently women, and had less cardiovascular risk factors in comparison with the NVD group [7]. The literature about ‘SM risk factor' reports dissonant results [21,27,28,30,40], that underlies the difficulty of clinical diagnosis in this domain. The results from this literature only show that diagnostic accuracy of stroke is lower among subgroups with mild, nonspecific, or transient symptoms and with past-medical history of epilepsy or migraine or also psychiatric disturbance [44]. Moreover, factors associated with stroke under-diagnosis include young age, posterior circulation, sensory symptoms and a lake of lateralizing weakness [45,46]. We should not select patients based on the probability to have or not have an SM; it could represent a source of misdiagnosis and a lost opportunity for thrombolysis. The abruptness of symptoms onset is probably the most important point in clinical stroke diagnosis [47]. Our study underlines that performing MRI is useful for all acute deficits suspected to be a stroke, before concluding wrongly on an SM because there is no reliable clinical data that can exclude the stroke diagnosis. As Merino et al. [7] suggested that a low rate of SM is due to the fact that the stroke team is not calling for all potential stroke patients, whereas a higher rate is linked to the consideration that all patients with neurological symptoms may have a stroke.

The name of our stroke code initially called ‘thrombolysis stroke care pathway' switched naturally to ‘acute neurological deficit care pathway', in which patients presenting with acute neurological symptoms can be evaluated for stroke diagnosis and considered for t-PA eligibility. Therefore, recanalization therapies were realized in 29% of the IS seen in our pathway, which is a superior rate comparing to those between 2 and 22% in a systematic review [48]. Our study has several strengths: the sample size is large and the recruitment of patients was prospective, cerebral MRI was performed in a majority of patients and the final diagnosis of the patients with SM was done appropriately. The main limitations of our study were its monocentric recruitment for the cohort and the preselection of the patients who had onset of symptoms within the thrombolysis time window. These are however the limitations of a majority of studies, but reducing the number of factors to be considered may be a strength compared to the difficulty in analyzing heterogeneous results that originate from different stroke care pathways.

Conclusion

The challenge of distinguishing between stroke and SM is more critical as thought since the latter may represent 38% of patients with suspected stroke. The patients with SM show symptoms from a large variety of etiologies that do not require the use of thrombolytic drugs. Our ‘acute neurological deficit care pathway' enables to optimize the management of acute stroke suspicion by a systematic MRI assessment, a fast evaluation and management of patients with NVD and neurovascular mimics pathologies. The challenge for the future will be to increase the number of IS patients having a recanalization treatment. The objectives are to shorten the delays between symptoms and call emergency medical services, improve number of patients recognizing symptoms of stroke by the information of the public, and provide appropriate training to prehospital and emergency personnel.

Acknowledgments

The authors would like to acknowledge all the physicians who participated in this study, especially all the neurology team of Strasbourg University Hospital.

The authors would like to thank Rodrigue Galani, PhD for writing assistance.

Disclosure Statement

None declared.

Sources of Funding

None.


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Author Contacts

Dr. Valérie Wolff, MD, PhD

Unité Neuro-Vasculaire, Service de Neurologie

HUS, 1 Avenue Molière

FR-67098 Strasbourg (France)

E-Mail valerie.wolff@chru-strasbourg.fr


Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: September 16, 2015
Accepted: March 18, 2016
Published online: April 26, 2016
Issue release date: July 2016

Number of Print Pages: 8
Number of Figures: 1
Number of Tables: 3

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