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Original article
One-year prognosis of non-traumatic cortical subarachnoid haemorrhage: a prospective series of 34 patients
Pronóstico al año de la hemorragia subaracnoidea cortical no traumática: serie prospectiva de 34 pacientes
R.F. Galiano Blancarta,
Corresponding author
rafa_galiano@yahoo.es

Corresponding author.
, G. Forteab, A. Pampliega Pérezc, S. Martíc, V. Parkhutikb, A.V. Sánchez Cruzd, C. Sorianoe, D. Geffner Sclarskye, M.T. Pérez Saldañaf, N. López Hernándezc, I. Beltránc, A. Lago Martínb, on behalf of Grupo Ictus-Comunidad Valenciana
a Servicio de Neurología, Hospital Dr. Peset de Valencia, Valencia, Spain
b Servicio de Neurología, Hospital La Fe de Valencia, Valencia, Spain
c Servicio de Neurología, Hospital General de Alicante, Alicante, Spain
d Servicio de Neurología, Hospital de Sagunto, Castellón de la Plana, Spain
e Servicio de Neurología, Hospitals General de Castellón, Valencia, Spain
f Hospital de Manises, Manises, Spain
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          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Eighty-two-year-old patient presenting sudden-onset loss of strength and sensitivity in the left arm 6 days after implantation of a left carotid stent&#46; A&#41; Head CT scan showing cSAH of the left convexity&#46; B&#41; Diffusion-weighted MRI scan revealing acute infarction adjacent to the bleeding&#46; C&#41; MRI-angiography showing stent thrombosis &#40;arrow&#41;&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">The most frequent cause of non-traumatic subarachnoid haemorrhage &#40;SAH&#41; is the rupture of an intracranial aneurysm&#44; which is recorded in 85&#37; of cases&#46; These patients present familial predisposition&#44; as well as well-known risk factors such as smoking&#44; arterial hypertension&#44; or excessive alcohol consumption&#46; Prognosis is poor&#44; with a case fatality rate of approximately 50&#37;&#59; one-third of survivors remain dependent&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">The second most frequent cause is perimesencephalic haemorrhage &#40;10&#37; of all cases&#41;&#44; in which brain angiography findings are almost always normal and progression is usually satisfactory&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">The remaining 5&#37; of cases are mainly cortical SAHs &#40;cSAH&#41;&#44; which are characterised by the presence of blood in one or several sulci of the brain convexity&#46; Several causes of cSAH are reported<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a>&#58; cerebral amyloid angiopathy &#40;CAA&#41;&#44;<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3&#8211;6</span></a> vaculitis&#44;<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7&#44;8</span></a> reversible cerebral vasoconstriction syndrome &#40;RCVS&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> posterior reversible encephalopathy syndrome &#40;PRES&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> vascular malformations&#44;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> mycotic aneurysms&#44;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> ischaemic stroke&#44;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> arterial dissection or stenosis&#44;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> and cerebral venous thrombosis &#40;CVT&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0075"><span class="elsevierStyleSup">15&#8211;17</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">The prognosis of patients with cSAH is not well established&#44; with data available only from small clinical series&#46;<a class="elsevierStyleCrossRefs" href="#bib0090"><span class="elsevierStyleSup">18&#8211;23</span></a> Furthermore&#44; no prospective studies providing information on long-term progression have been published&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">The aim of this study is to describe the clinical and aetiological characteristics of patients with cSAH&#44; and to determine their progression and prognosis&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Patients and methods</span><p id="par0030" class="elsevierStylePara elsevierViewall">This is an observational&#44; prospective&#44; multi-centre study&#44; including patients from 6 hospitals from the Valencian Community &#40;Spain&#41;&#46; The study was authorised by the Research Committee at Hospital de Sagunto&#46; Informed consent forms were signed in all cases&#46; Patients were recruited between June 2011 and April 2016&#44; with follow-up consultations held at 3 months and one year&#46; Progression was assessed using the modified Rankin Scale&#44; and was considered favourable with a score &#8804;2 and unfavourable with a score &#62;2&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">All patients were admitted to their reference hospitals&#46; We excluded cases of traumatic haemorrhages and haemorrhages with associated intraparenchymal haematoma or bleeding in the interhemispheric fissure&#44; basal cisterns&#44; or ventricles&#46; Clinical&#44; demographic&#44; electrophysiological&#44; laboratory&#44; and imaging data were collected&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">All patients underwent a head CT scan&#46; Whether to perform other imaging studies during admission was considered on an individual basis&#59; these studies included CT angiography&#44; brain MRI with vascular study&#44; and conventional cerebral angiography&#46; We also collected data on the presence of superficial siderosis&#44; old haemorrhage&#44; and acute ischaemia on diffusion sequences&#46; We used the modified Boston criteria to diagnose CAA<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">24</span></a> and the Calabrese criteria for RCVS&#46;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a> During follow-up&#44; clinically stable patients did not undergo neuroimaging studies&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">A cerebrospinal fluid analysis and&#47;or electroencephalography was performed in some cases&#44; based on each centre&#8217;s criteria and the patient&#8217;s characteristics&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Results</span><p id="par0050" class="elsevierStylePara elsevierViewall">During the study period&#44; we recruited a total of 34 patients&#44; with a mean age of 68&#46;3 years &#40;range&#44; 27&#8211;89&#41;&#46; Twenty-five patients &#40;73&#46;5&#37;&#41; were older than 60&#46; Seventeen patients were women&#46; Patients&#8217; demographic and clinical data are summarised in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Clinical manifestations</span><p id="par0055" class="elsevierStylePara elsevierViewall">Several patients presented more than one symptom&#46; Onset was acute in all cases except for one patient with meningeal carcinomatosis&#44; who developed headache and progressive onset of focal neurological signs&#46; The most frequent symptom was focal neurological deficit &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>21&#44; 62&#37;&#41;&#44; with 10 patients &#40;29&#37;&#41; manifesting repetitive stereotyped behaviours and 11 patients &#40;33&#37;&#41; presenting established deficits&#46; Eleven patients &#40;33&#37;&#41; presented headache&#44; with thunderclap headache in only 4 &#40;12&#37;&#41;&#46; Three patients &#40;9&#37;&#41; presented confusion&#44; with one of these displaying symptoms resembling an episode of transient global amnesia&#46; Three patients &#40;9&#37;&#41; developed seizures as the initial symptom&#59; these were generalised in 2 cases&#46; Two patients &#40;6&#37;&#41; reported non-specific visual alterations together with other symptoms&#46; One patient displayed neck rigidity&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Radiological findings</span><p id="par0060" class="elsevierStylePara elsevierViewall">Haemorrhage was identified in the CT scan in 28 cases &#40;85&#37;&#41;&#44; and in the MRI study in the remaining patients&#46; A brain MRI scan was performed in 30 patients &#40;88&#37;&#41;&#44; and brain angiography in 12 patients &#40;35&#37;&#41;&#46; Bleeding was mostly unilateral&#44; with the most frequent locations being the parietal and frontal regions&#46; Diffusion-weighted MRI sequences showed cortical hyperintensity in 10 patients &#40;33&#37; of all patients undergoing MRI&#41;&#44; which was adjacent to the cSAH in most cases&#46; Old haemorrhages were detected in 7 cases &#40;23&#37;&#41;&#44; and superficial siderosis in another location was detected in 2 &#40;7&#37;&#41;&#46; An intra- and extracranial vascular study using CT angiography&#44; MRI angiography&#44; or conventional angiography was performed in 30 cases &#40;88&#37;&#41;&#59; this study revealed no aneurysm or arteriovenous malformation except in one patient&#44; who presented a small aneurysm measuring 1&#46;2<span class="elsevierStyleHsp" style=""></span>mm in diameter&#44; located away from the bleeding site&#46; Five patients presented carotid artery involvement ipsilateral to the bleeding &#40;2 significant stenoses&#44; 2 complete occlusions&#44; and one intrastent thrombus&#41;&#46; Multiple intracranial stenoses were detected in 2 patients&#59; one patient presented ipsilateral middle cerebral artery occlusion&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Other studies</span><p id="par0065" class="elsevierStylePara elsevierViewall">Ten patients &#40;29&#37;&#41; underwent electroencephalography studies&#44; revealing epileptiform activity in only 3 cases&#46; Fourteen patients underwent lumbar puncture&#46; Cerebrospinal fluid analysis revealed no abnormalities&#46; Xanthochromia was not detected in any case&#46; We detected lymphocytic pleocytosis in 3 patients&#44; a slightly increased protein level in 2&#44; and oligoclonal bands in one&#46; The cytological study detected malignant cells in one patient&#46; We calculated the tau&#47;Abeta42 ratio in 7 patients&#59; results were pathological in 3&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Aetiology</span><p id="par0070" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a> includes the causes of bleeding&#44; which we were able to establish in 26 patients &#40;76&#46;5&#37;&#41;&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0075" class="elsevierStylePara elsevierViewall">The most frequent diagnosis was CAA &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#44; accounting for a total of 8 cases&#46; Three patients were diagnosed during the one-year follow-up period&#58; one due to recurrence of cSAH and presence of superficial siderosis on MRI&#44; and the other 2 due to lobar haemorrhage&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0080" class="elsevierStylePara elsevierViewall">The second most frequent cause was ischaemic stroke &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>5&#41;&#58; 2 cardioembolic strokes&#44; one atherothrombotic infarction&#44; one stroke secondary to carotid artery occlusion&#44; and one case of carotid stent thrombosis &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0085" class="elsevierStylePara elsevierViewall">The third most frequent cause was vasculitis &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>4&#41;&#46; Three cases were secondary &#40;Sj&#246;gren syndrome&#44; Churg-Strauss syndrome&#44; neurosyphilis&#41;&#44; with the fourth patient presenting primary angiitis of the central nervous system&#46; The remaining aetiologies included&#58; PRES &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#41;&#44; CVT &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#41;&#44; RCVS &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#41;&#44; carotid artery occlusion with no associated infarction &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41;&#44; Marfan syndome &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41;&#44; and meningeal carcinomatosis &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41;&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Progression</span><p id="par0090" class="elsevierStylePara elsevierViewall">One patient diagnosed with CVT and prostate cancer died during admission due to a massive cerebral haematoma&#46; Two other patients died during the follow-up period&#44; one due to meningeal carcinomatosis originated by cSAH&#44; and another who was diagnosed with CAA due to an unrelated cause&#46; Overall mortality amounted to 9&#37; &#40;<a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0015"></elsevierMultimedia><p id="par0095" class="elsevierStylePara elsevierViewall">We were able to follow up 32 of 33 patients &#40;97&#37;&#41;&#46; One-year outcomes were favourable in 24 patients &#40;73&#37;&#41; and unfavourable in 9 &#40;27&#37;&#41;&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">Twelve percent of patients presented rebleeding within one year of follow-up &#40;3 lobar haematomas and one new cSAH&#41;&#46; Three patients developed dementia&#46;</p></span></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Discussion</span><p id="par0105" class="elsevierStylePara elsevierViewall">In addition to presenting one of the largest series of patients with cSAH &#40;34 cases&#41;&#44; this study is to our knowledge the first prognostic study with prospective follow-up and data progression at one year&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">Our results show several differences between cSAH and aneurysmal SAH&#46; Firstly&#44; the most frequent initial manifestation was not headache but focal neurological signs&#44; which manifested in approximately two-thirds of patients in our series&#46; Seventeen patients &#40;50&#37;&#41; presented recurrent&#44; stereotyped &#40;especially paresthesia affecting one side of the body&#41;&#44; short-lasting transient neurological deficits&#59; in these cases&#44; CAA was the most frequent underlying cause&#46; One-third of patients presented headache as the initial symptom&#44; with thunderclap headache in some cases&#46; Neck rigidity&#44; a typical sign of aneurysmal SAH&#44; was exceptional&#46; We should also underscore that there was no case of bleeding due to aneurysmal rupture&#44; that patients had no family history of SAH or intracranial aneurysm&#44; and that the percentage of smokers and alcohol users &#40;well-established risk factors for aneurysmal SAH&#41; was low&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">Our findings show that cSAH may be due to various causes&#44; going beyond other authors&#8217; dichotomy of RCVS in young patients and CAA in elderly patients&#46;<a class="elsevierStyleCrossRefs" href="#bib0095"><span class="elsevierStyleSup">19&#44;23</span></a> The 3 most frequently diagnosed causes were CAA&#44; ischaemic stroke&#44; and vasculitis&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">A possible explanation for CAA being the most frequent cause of cSAH is that most of patients were older than 60 years&#44; as is reported in previous studies&#46;<a class="elsevierStyleCrossRefs" href="#bib0100"><span class="elsevierStyleSup">20&#44;22&#44;26</span></a> Almost all patients presented recurrent&#44; stereotyped transient neurological deficits&#44; also known as amyloid spells&#46; It has been suggested that cSAH may precede the appearance of a lobar haematoma by several weeks&#46;<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3&#44;4&#44;27</span></a> In fact&#44; 4 of our patients presented rebleeding in the months following admission&#46; Therefore&#44; antithrombotics should be prescribed with caution&#46; When initial diagnosis is uncertain&#44; a deferred brain MRI study may help to establish a diagnosis of CAA if rebleeding or superficial siderosis are observed&#46;<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4&#44;5&#44;24</span></a></p><p id="par0125" class="elsevierStylePara elsevierViewall">Regarding ischaemic stroke&#44; a retrospective review of almost 5000 patients with acute stroke or transient ischaemic attack showed low incidence of cSAH &#40;8 cases&#59; 0&#46;14&#37;&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> We believe copresence of CAA to be the most probable underlying mechanism&#46; However&#44; another study reports an unusually high incidence of cSAH associated with brain ischaemia among patients with heart disease and implanted left ventricular assist devices&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a> It should be noted that the mean age in that study was 39 years&#44; making CAA highly improbable&#46; In these cases&#44; the most probable mechanism is haemorrhagic transformation of a cardioembolic stroke&#44; which is also favoured by the fact that many patients were receiving anticoagulants&#46; Some cases have been reported of cSAH associated with carotid artery occlusion or stenosis&#46; The mechanism could again be haemorrhagic transformation of a small ischaemic stroke or rupture of fragile collateral vessels&#44; even in the absence of infarction&#44;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> as occurred in one of our patients&#46; Carotid artery stenosis may be underdiagnosed&#44; as the extracranial carotid artery is frequently not explored&#46;</p><p id="par0130" class="elsevierStylePara elsevierViewall">Cortical SAH is a frequent manifestation of primary cerebral vasculitis or vasculitis secondary to autoimmune systemic diseases&#46;<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7&#44;29&#44;30</span></a> A study by Boulouis et al&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> including 60 patients diagnosed with primary angiitis of the central nervous system&#44; reported vasculitis in 26&#37; of cases&#46; In our series&#44; vasculitis was suspected due to the patient&#8217;s history in 3 of the 4 cases&#59; diagnosis was supported by the presence of multiple arterial stenoses in the vascular study&#46; Meningeal enhancement in the MRI study helped to establish a differential diagnosis with RCVS&#46; Changes in the cerebrospinal fluid and response to immunosuppressant treatment supported diagnosis&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">It is important to identify the underlying cause of bleeding&#44; not only to orient treatment but also to establish prognosis&#46; Diagnostic yield increases with an extensive initial aetiological study and with follow-up of the patient&#46; Brain MRI is the most useful complementary test&#46; FLAIR sequences are more sensitive than head CT in identifying acute bleeding&#44; whereas echo-gradient MRI helps to identify old haemorrhages&#44; superficial siderosis&#44; and cortical CVT&#46;<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3&#44;17&#44;31&#44;32</span></a> An intra- and extracranial vascular study should be performed in every patient&#46; Cerebral angiography would be reserved for those cases in which diagnosis is not established after performing these studies&#44; or in which vasculitis or RCVS is suspected&#46;</p><p id="par0140" class="elsevierStylePara elsevierViewall">It was possible to establish a diagnosis during admission in 23 patients &#40;68&#37;&#41;&#46; We should highlight the importance of follow-up after discharge&#44; which enabled us to increase this number to 26 &#40;76&#46;5&#37;&#41;&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">Prognosis of patients with cSAH differs between series&#46; Studies reporting good progression usually include younger patients diagnosed with PRES&#44; CVT&#44; or RCVS&#46;<a class="elsevierStyleCrossRefs" href="#bib0045"><span class="elsevierStyleSup">9&#44;15&#44;16&#44;18</span></a> Other studies report poor progression&#44; associated especially with age&#46;<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4&#44;19&#44;22&#44;26</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">33</span></a> Only the study by Mart&#237;nez-Lizana et al&#46;<span class="elsevierStyleSup">4</span> included patients diagnosed with CAA and ambispective follow-up&#46; Our study is the first to include prospective follow-up&#44; which was possible in more than 95&#37; of cases&#46; All patients with a modified Rankin Scale score &#62;2 at one year &#40;27&#37; of patients&#41; were older than 65&#46; Furthermore&#44; both cognitive impairment and all episodes of rebleeding were recorded in patients diagnosed with CAA&#46; Therefore&#44; prognosis will depend on age and aetiology&#44; and is poorer in older patients with CAA&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">Our study has several limitations&#46; Not all the available diagnostic tests were performed on all patients&#44; especially very elderly patients with a very poor situation at baseline&#46; Specifically&#44; brain MRI and extracranial carotid artery exploration were not performed in all cases&#46; Cerebral angiography was not performed in all cases of uncertain diagnosis&#46;</p><p id="par0155" class="elsevierStylePara elsevierViewall">In conclusion&#44; cSAH is a rare cerebrovascular disease with numerous possible aetiologies&#46; In our series&#44; the most frequent causes were amyloid angiopathy&#44; ischaemic stroke&#44; and vasculitis&#46; Prognosis is poorer than in other non-aneurysmal SAHs&#46; In elderly patients&#44; risk of intracranial haemorrhage and cognitive impairment is greater due to the frequent association with CAA&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Conflicts of interest</span><p id="par0160" class="elsevierStylePara elsevierViewall">This study has received no funding of any kind&#46; The authors have no conflicts of interest to declare&#46;</p></span></span>"
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            1 => "Non-traumatic subarachnoid haemorrhage"
            2 => "Cerebral amyloid angiopathy"
            3 => "Prognosis"
            4 => "Ischaemic stroke"
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          "palabras" => array:6 [
            0 => "Hemorragia subaracnoidea cortical"
            1 => "Hemorragia subaracnoidea atraum&#225;tica"
            2 => "Angiopat&#237;a amiloide"
            3 => "Pron&#243;stico"
            4 => "Ictus isqu&#233;mico"
            5 => "Etiolog&#237;a"
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    "resumen" => array:2 [
      "en" => array:3 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Introduction</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Cortical subarachnoid haemorrhage &#40;cSAH&#41; has multiple aetiologies&#46; No prospective study has reported the long-term progression of the condition&#46; The objective of this study is to describe the clinical and aetiological characteristics of patients with cSAH and to gain insight into prognosis&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">We performed a prospective&#44; observational&#44; multi-centre study&#46; Data on clinical and radiological variables were collected&#59; during a one-year follow-up period&#44; we recorded data on mortality&#44; dependence&#44; rebleeding&#44; and the appearance of dementia&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">The study included 34 patients &#40;mean age&#44; 68&#46;3 years&#59; range&#44; 27&#8211;89&#41;&#46; The most frequent symptoms were headache and focal neurological deficits&#44; which were frequently transient and recurrent&#46; CT scans returned pathological findings in 28 patients &#40;85&#37;&#41;&#46; Brain MRI scans were performed in 30 patients &#40;88&#37;&#41;&#44; revealing acute ischaemia in 10 &#40;29&#37;&#41;&#44; old haemorrhage in 7 &#40;21&#37;&#41;&#44; and superficial siderosis in 2 &#40;6&#37;&#41;&#46; Aetiology was identified in 26 patients &#40;76&#46;5&#37;&#41;&#58; causes were cerebral amyloid angiopathy in 8&#44; ischaemic stroke in 5&#44; vasculitis in 4&#44; reversible posterior encephalopathy in 2&#44; venous thrombosis in 2&#44; reversible cerebral vasoconstriction syndrome in 2&#44; carotid occlusion in 1&#44; Marfan syndrome in 1&#44; and meningeal carcinomatosis in 1&#46; Three patients died during follow-up &#40;2 due to causes related to the cause of cSAH&#41;&#46; Three patients developed dementia&#44; 3 had lobar haemorrhages&#44; and one had a second cSAH&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusions</span><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">The most frequent causes of cSAH in our series were cerebral amyloid angiopathy&#44; ischaemic stroke&#44; and vasculitis&#46; This type of haemorrhage has a worse prognosis than other non-aneurysmal cSAH&#46; There are numerous possible causes&#44; and prognosis depends on the aetiology&#46; In elderly patients&#44; intracranial haemorrhage is frequently associated with cognitive impairment&#46;</p></span>"
        "secciones" => array:4 [
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            "identificador" => "abst0005"
            "titulo" => "Introduction"
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            "titulo" => "Methods"
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            "identificador" => "abst0015"
            "titulo" => "Results"
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            "identificador" => "abst0020"
            "titulo" => "Conclusions"
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      "es" => array:3 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducci&#243;n</span><p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Las hemorragias subaracnoideas corticales &#40;HSAc&#41; tienen numerosas etiolog&#237;as&#46; No hay estudios prospectivos que indiquen su evoluci&#243;n a largo plazo&#46; El objetivo de este trabajo es describir las caracter&#237;sticas cl&#237;nicas y etiol&#243;gicas de los pacientes con HSAc y conocer su pron&#243;stico&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">M&#233;todos</span><p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">Estudio observacional&#44; prospectivo y multic&#233;ntrico&#46; Se recogieron variables cl&#237;nicas y radiol&#243;gicas&#44; y se sigui&#243; la evoluci&#243;n al a&#241;o&#44; observando la mortalidad&#44; dependencia&#44; tasa de resangrado y aparici&#243;n de demencia&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">Se incluyeron 34 pacientes &#40;edad media 68&#46;3 a&#241;os&#44; rango 27&#8211;89&#41;&#46; Los s&#237;ntomas m&#225;s frecuentes fueron el d&#233;ficit neurol&#243;gico focal&#44; con frecuencia transitorio y de repetici&#243;n&#44; y la cefalea&#46; El TAC fue patol&#243;gico en 28 pacientes &#40;85&#37;&#41;&#46; Se realiz&#243; RM cerebral en 30 pacientes &#40;88&#37;&#41;&#44; con isquemia aguda en 10 &#40;29&#37;&#41;&#44; sangrados antiguos en 7 &#40;21&#37;&#41; y siderosis superficial en otros 2 &#40;6&#37;&#41;&#46; Se encontr&#243; etiolog&#237;a en 26 pacientes &#40;76&#46;5&#37;&#41;&#58; angiopat&#237;a amiloide &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>8&#41;&#44; ictus isqu&#233;mico &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>5&#41;&#44; vasculitis &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>4&#41;&#44; encefalopat&#237;a posterior reversible &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#41;&#44; trombosis venosa &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#41;&#44; s&#237;ndrome de vasoconstricci&#243;n cerebral reversible &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#41;&#44; oclusi&#243;n carotidea &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41;&#44; s&#237;ndrome de Marfan &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41; y carcinomatosis men&#237;ngea &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#41;&#46; Durante el seguimiento fallecieron tres pacientes &#40;en dos de ellos relacionado con la causa de la HSAc&#41;&#46; Tres pacientes desarrollaron una demencia&#44; tres presentaron un hematoma lobar y otro una nueva HSAc&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusiones</span><p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">En nuestra serie las causas m&#225;s frecuentes de HSAc fueron la angiopat&#237;a amiloide&#44; el ictus isqu&#233;mico y la vasculitis&#46; La HSAc tiene peor pron&#243;stico que otras HSA no aneurism&#225;ticas&#46; Puede tener numerosas causas y su pron&#243;stico depende de la etiolog&#237;a subyacente&#46; En el anciano existe una frecuente asociaci&#243;n con hemorragia intracraneal y deterioro cognitivo&#46;</p></span>"
        "secciones" => array:4 [
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            "titulo" => "Introducci&#243;n"
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            "identificador" => "abst0030"
            "titulo" => "M&#233;todos"
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            "identificador" => "abst0035"
            "titulo" => "Resultados"
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          3 => array:2 [
            "identificador" => "abst0040"
            "titulo" => "Conclusiones"
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    "NotaPie" => array:2 [
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        "etiqueta" => "&#9734;"
        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; Galiano Blancart RF&#44; et al&#46; Pron&#243;stico al a&#241;o de la hemorragia subaracnoidea cortical no traum&#225;tica&#58; serie prospectiva de 34 pacientes&#46; Neurolog&#237;a&#46; 2021&#59;36&#58;215&#8211;221&#46;</p>"
      ]
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        "etiqueta" => "&#9734;&#9734;"
        "nota" => "<p class="elsevierStyleNotepara" id="npar0010">This study was presented at the 68th Annual Meeting of the Spanish Society of Neurology&#46;</p>"
      ]
    ]
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        "etiqueta" => "Figure 1"
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        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr1.jpeg"
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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Eighty-year-old patient with CAA&#46; A&#41; Head CT scan showing hyperintensity in a sulcus of the right frontal convexity&#46; B&#41; Echo-gradient MRI sequence showing extensive&#44; bilateral superficial siderosis&#46;</p>"
        ]
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        "etiqueta" => "Figure 2"
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        "mostrarFloat" => true
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        "figura" => array:1 [
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            "imagen" => "gr2.jpeg"
            "Alto" => 825
            "Ancho" => 2000
            "Tamanyo" => 132383
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        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at0250"
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          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Eighty-two-year-old patient presenting sudden-onset loss of strength and sensitivity in the left arm 6 days after implantation of a left carotid stent&#46; A&#41; Head CT scan showing cSAH of the left convexity&#46; B&#41; Diffusion-weighted MRI scan revealing acute infarction adjacent to the bleeding&#46; C&#41; MRI-angiography showing stent thrombosis &#40;arrow&#41;&#46;</p>"
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                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">n &#40;&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Age &#40;years&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">68&#46;3 &#40;74&#37; older than 60&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Sex &#40;men&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">17 &#40;50&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Arterial hypertension&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">21 &#40;62&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Dyslipidaemia&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10 &#40;29&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Diabetes mellitus&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">5 &#40;15&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Atrial fibrillation&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2 &#40;6&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Cognitive impairment&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4 &#40;12&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Prior ischaemic stroke&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">5 &#40;15&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Smoker or former smoker&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10 &#40;30&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Alcohol use&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">2 &#40;6&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Drug use&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">2 &#40;6&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Anti-platelet agents&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">6 &#40;18&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Anticoagulants&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">4 &#40;12&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
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          "leyenda" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">cSAH&#58; cortical subarachnoid haemorrhage&#59; CVT&#58; cerebral venous thrombosis&#59; PRES&#58; posterior reversible encephalopathy syndrome&#59; RCVS&#58; reversible cerebral vasoconstriction syndrome&#46;</p>"
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">8 &#40;23&#46;5&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">5 &#40;15&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>RCVS&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t"><span class="elsevierStyleHsp" style=""></span>Carotid artery occlusion without infarct&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">1 &#40;3&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">1 &#40;3&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">8 &#40;23&#46;5&#37;&#41;&nbsp;\t\t\t\t\t\t\n
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                0 => array:2 [
                  "contribucion" => array:1 [
                    0 => array:2 [
                      "titulo" => "Subarachnoid haemorrhage&#58; diagnosis&#44; causes and management"
                      "autores" => array:1 [
                        0 => array:2 [
                          "etal" => false
                          "autores" => array:2 [
                            0 => "J&#46; Van Gijn"
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                    0 => array:2 [
                      "doi" => "10.1093/brain/124.2.249"
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                          "etal" => false
                          "autores" => array:5 [
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                            2 => "J&#46; Alamst"
                            3 => "M&#46; Mangla"
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                      "Revista" => array:5 [
                        "tituloSerie" => "Emerg Radiol"
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                      "titulo" => "Cortical superficial siderosis&#58; detection and clinical significance in cerebral amyloid angiopathy and related conditions"
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                          "etal" => true
                          "autores" => array:6 [
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                            4 => "S&#46; Akoudad"
                            5 => "J&#46;C&#46; Baron"
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                            3 => "A&#46; Faury"
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                      "titulo" => "Spontaneous convexity subarachnoid haemorrhage&#58; Clinical series of 3 patients with associated cerebral amyloid angiopathy"
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                          "etal" => false
                          "autores" => array:5 [
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                      "titulo" => "Isolated angiitis of the CNS presenting as subarachnoid haemorrhage"
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                    0 => array:2 [
                      "titulo" => "Reversible cerebral vasoconstriction syndromes&#58; analysis of 139 cases"
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                          "etal" => true
                          "autores" => array:6 [
                            0 => "A&#46;B&#46; Singhal"
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                            3 => "J&#46; Fok"
                            4 => "J&#46; Bena"
                            5 => "D&#46; Yang"
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