Magnetic Resonance Imaging and Cerebral Ischemia After Aneurysmal Subarachnoid Hemorrhage

HomeStrokeVol. 48, No. 1Magnetic Resonance Imaging and Cerebral Ischemia After Aneurysmal Subarachnoid Hemorrhage Free AccessResearch ArticlePDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissionsDownload Articles + Supplements ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toSupplemental MaterialFree AccessResearch ArticlePDF/EPUBMagnetic Resonance Imaging and Cerebral Ischemia After Aneurysmal Subarachnoid HemorrhageA Systematic Review and Meta-Analysis Lisa A. van der Kleij, MSc, Jill B. De Vis, MD, PhD, Jean-Marc Olivot, MD, PhD, Lionel Calviere, MD, Christophe Cognard, MD, PhD, Nicolaas P.A. Zuithoff, PhD, Gabriel J.E. Rinkel, MD, Jeroen Hendrikse, MD, PhD and Mervyn D.I. Vergouwen, MD, PhD Lisa A. van der KleijLisa A. van der Kleij From the Department of Radiology (L.A.v.d.K., J.B.D.V., J.H.), Julius Center for Health Sciences and Primary Care (N.P.A.Z.), and Department of Neurology and Neurosurgery, Brain Center Rudolf Magnus (G.J.E.R., M.D.I.V.), University Medical Center Utrecht, The Netherlands; and Department of Neurology (J.M.O., L.C.) and Department of Radiology (C.C.), University of Toulouse, France. , Jill B. De VisJill B. De Vis From the Department of Radiology (L.A.v.d.K., J.B.D.V., J.H.), Julius Center for Health Sciences and Primary Care (N.P.A.Z.), and Department of Neurology and Neurosurgery, Brain Center Rudolf Magnus (G.J.E.R., M.D.I.V.), University Medical Center Utrecht, The Netherlands; and Department of Neurology (J.M.O., L.C.) and Department of Radiology (C.C.), University of Toulouse, France. , Jean-Marc OlivotJean-Marc Olivot From the Department of Radiology (L.A.v.d.K., J.B.D.V., J.H.), Julius Center for Health Sciences and Primary Care (N.P.A.Z.), and Department of Neurology and Neurosurgery, Brain Center Rudolf Magnus (G.J.E.R., M.D.I.V.), University Medical Center Utrecht, The Netherlands; and Department of Neurology (J.M.O., L.C.) and Department of Radiology (C.C.), University of Toulouse, France. , Lionel CalviereLionel Calviere From the Department of Radiology (L.A.v.d.K., J.B.D.V., J.H.), Julius Center for Health Sciences and Primary Care (N.P.A.Z.), and Department of Neurology and Neurosurgery, Brain Center Rudolf Magnus (G.J.E.R., M.D.I.V.), University Medical Center Utrecht, The Netherlands; and Department of Neurology (J.M.O., L.C.) and Department of Radiology (C.C.), University of Toulouse, France. , Christophe CognardChristophe Cognard From the Department of Radiology (L.A.v.d.K., J.B.D.V., J.H.), Julius Center for Health Sciences and Primary Care (N.P.A.Z.), and Department of Neurology and Neurosurgery, Brain Center Rudolf Magnus (G.J.E.R., M.D.I.V.), University Medical Center Utrecht, The Netherlands; and Department of Neurology (J.M.O., L.C.) and Department of Radiology (C.C.), University of Toulouse, France. , Nicolaas P.A. ZuithoffNicolaas P.A. Zuithoff From the Department of Radiology (L.A.v.d.K., J.B.D.V., J.H.), Julius Center for Health Sciences and Primary Care (N.P.A.Z.), and Department of Neurology and Neurosurgery, Brain Center Rudolf Magnus (G.J.E.R., M.D.I.V.), University Medical Center Utrecht, The Netherlands; and Department of Neurology (J.M.O., L.C.) and Department of Radiology (C.C.), University of Toulouse, France. , Gabriel J.E. RinkelGabriel J.E. Rinkel From the Department of Radiology (L.A.v.d.K., J.B.D.V., J.H.), Julius Center for Health Sciences and Primary Care (N.P.A.Z.), and Department of Neurology and Neurosurgery, Brain Center Rudolf Magnus (G.J.E.R., M.D.I.V.), University Medical Center Utrecht, The Netherlands; and Department of Neurology (J.M.O., L.C.) and Department of Radiology (C.C.), University of Toulouse, France. , Jeroen HendrikseJeroen Hendrikse From the Department of Radiology (L.A.v.d.K., J.B.D.V., J.H.), Julius Center for Health Sciences and Primary Care (N.P.A.Z.), and Department of Neurology and Neurosurgery, Brain Center Rudolf Magnus (G.J.E.R., M.D.I.V.), University Medical Center Utrecht, The Netherlands; and Department of Neurology (J.M.O., L.C.) and Department of Radiology (C.C.), University of Toulouse, France. and Mervyn D.I. VergouwenMervyn D.I. Vergouwen From the Department of Radiology (L.A.v.d.K., J.B.D.V., J.H.), Julius Center for Health Sciences and Primary Care (N.P.A.Z.), and Department of Neurology and Neurosurgery, Brain Center Rudolf Magnus (G.J.E.R., M.D.I.V.), University Medical Center Utrecht, The Netherlands; and Department of Neurology (J.M.O., L.C.) and Department of Radiology (C.C.), University of Toulouse, France. Originally published6 Dec 2016https://doi.org/10.1161/STROKEAHA.116.011707Stroke. 2017;48:239–245Other version(s) of this articleYou are viewing the most recent version of this article. Previous versions: January 1, 2016: Previous Version 1 IntroductionThe prognosis of aneurysmal subarachnoid hemorrhage (aSAH) has improved during the past decades. However, a recent hospital-based study showed that 90-day case fatality is still 30%.1 Determinants of functional outcome after aSAH may include the severity of the initial hemorrhage, rebleeding of the aneurysm, and cerebral ischemia that can be distinguished into (1) acute ischemia at the time of bleeding when intracranial pressure rises and cerebral perfusion pressure drops, (2) procedure-related ischemia from endovascular or neurosurgical treatment of the aneurysm, and (3) delayed cerebral ischemia (DCI), which can occur between days 4 and 14 after the hemorrhage.2,3Magnetic resonance diffusion weighted imaging (MRI-DWI) is increasingly used for the evaluation of ischemia after aSAH. The aims of the present review were to (1) analyze the proportion of patients with MRI-DWI lesions within 72 hours after aSAH, both before and after aneurysm treatment; (2) study determinants of MRI-DWI lesions within 72 hours after aSAH; (3) analyze the proportion of patients with MRI-DWI lesions between 72 hours and 21 days after aSAH; (4) investigate the predictive value of MRI-DWI lesions within 72 hours for the development of DCI; and 5) investigate whether MRI-DWI can be used for the diagnosis of DCI in patients with clinical deterioration.MethodsSearch StrategyWe searched the PUBMED, EMBASE, and Web of Science databases with the following combination of variables: MRI OR magnetic resonance AND subarachnoid hemorrhage OR SAH OR DCI OR delayed cerebral ischemia OR DIND. The last search was performed in June 28, 2016. Only studies published after January 1, 2000, were included to assure a similar degree of image quality, given the technical developments in MRI hardware and sequences. Both prospective and retrospective studies were included. Eligible articles were identified according to the PICO criteria. Type of patient population (P): (1) >95% of patients had aneurysmal SAH, defined as the presence of subarachnoid blood as shown by computed tomography (CT) or lumbar puncture and the presence of an aneurysm on CT angiography, magnetic resonance angiography, or digital subtraction angiography and (2) ≥10 patients had MRI-DWI performed <72 hours or between 72 hours and 21 days after ictus. Intervention (I): MRI scan performed ≤21 days after SAH. The MRI protocol included diffusion weighted imaging (DWI). Comparator (C): N/A. Outcomes (O): MRI-DWI lesions assessed either <72 hours or between 72 hours and 21 days after ictus. Exclusion criteria were (1) article written in languages other than English, French, German, Spanish, Italian, Portuguese, or Dutch; (2) conference abstract; (3) animal study; (4) MRI was performed after elimination of the aneurysm with carotid artery occlusion and subsequent bypass surgery; (5) MRI-DWI lesions were only presented for patients with angiographic vasospasm. Two authors (J.B.D.V. and L.A.v.d.K) screened the articles by title and abstract. Disagreement was resolved by consensus. One author (L.A.v.d.K.) performed the screening of the full article. The exclusion of articles in this phase was performed in consensus with 2 other authors (J.B.D.V. and M.D.I.V.). If more than one article used the same or overlapping patient populations, we only included the report with the largest population or with the most relevant information for our review. If articles reported on MRI findings, but timing of imaging could not be categorized into image acquisition <72 hours after ictus or between 72 hours and 21 days after ictus, the corresponding authors of these articles were contacted for additional information. In case the authors did not respond, the article was excluded. References of included articles were hand searched for additional eligible articles.Data ExtractionFrom included studies, we retrieved data on age, sex, clinical condition on admission, amount of subarachnoid blood on admission CT, type of aneurysm treatment, MRI sequence, and MRI hardware information. We extracted data on MRI-DWI lesions within 72 hours after ictus, either before or after aneurysm treatment, and between 72 hours and 21 days after SAH. In studies investigating the relationship between MRI-DWI lesions and DCI, we decided a priori to include the following terms as an outcome measure reflecting DCI: delayed ischemic neurological deficit, delayed ischemic deficit, delayed neurological deficit, secondary cerebral ischemia, clinical vasospasm, symptomatic vasospasm, symptomatic ischemia, and cerebral infarction. The definition of DCI or a similar term needed to include clinical deterioration or cerebral infarction. Studies with vasospasm as an outcome measure were only included if it was defined as any kind of clinical deterioration.Quality Assessment and Risk of Bias AssessmentQuality assessment of the included articles was based on a previously used scoring system,4,5 which was adapted to fit the studies within the scope of this review (Table I in the online-only Data Supplement). Two authors (L.A.v.d.K. and J.B.D.V.) performed the assessment independently. Disagreement was solved in a consensus reading between both authors. The score ranged from 0 to 14, and a high-quality article was predefined as having a score of 9 to 14. Risk of bias was assessed by L.A.v.d.K. and J.B.D.V. through a consensus reading using a tool developed to assess risk of bias in prevalence studies.6AnalysesFirst, we analyzed the proportion of patients with MRI-DWI lesions within 72 hours after aSAH, both before and after aneurysm treatment. Second, we studied whether the following variables were determinants of MRI-DWI lesions before aneurysm treatment within 72 hours after ictus: age, sex, clinical condition on admission, and amount of subarachnoid blood on CT classified by the (modified) Fisher scale. Third, we examined the proportion of patients with MRI-DWI lesions between 72 hours and 21 days after ictus. Fourth, we analyzed the proportion of patients with and without MRI-DWI lesions within 72 hours who later on developed DCI and calculated positive and negative predictive values. And fifth, we analyzed the proportion of patients with clinical deterioration because of DCI with compatible MRI-DWI lesions. For the analyses in which the proportion of patients with MRI-DWI lesions was investigated within 72 hours or between 72 hours and 21 days, a separate sensitivity analysis was performed for lesions with both a high signal on DWI and low signal on apparent diffusion coefficient (ADC). Statistical analyses were performed in R (version 3.2.3) with the lme4 package.7,8 We pooled proportions across studies using a generalized linear mixed-effects model for dichotomous outcomes, allowing for between-study heterogeneity. Besides the pooled proportion estimates, we report prediction intervals for the evaluation of between-study heterogeneity.9 Subsequently, risk ratios with 95% confidence intervals were calculated where appropriate using the epitools package.10 If zero events occurred in one group of a study, ½ was added to each cell of the table.11 We included clinical grade on admission into the model to evaluate its impact on the prevalence of MRI-DWI lesions within 72 hours. For MRI-DWI lesions between 72 hours and 21 days, we included clinical grade on admission, aneurysm treatment, and day of scanning after ictus into the model (Metaregression section in the online-only Data Supplement). Inter-rater agreement was assessed with Cohen κ.ResultsOur search strategy yielded a total of 7299 articles, of which 13 were included with 522 SAH patients (Figure 1; Table II in the online-only Data Supplement).12–24 Additional data were obtained on request from 2 studies.17,23 Characteristics of the included studies are shown in the Table III in the online-only Data Supplement. The median number of patients per study was 32 (range: 11–100). Five studies provided data on MRI within 72 hours after ictus,12,14,17,19,23 and 6 studies on MRI between 72 hours and 21 days after SAH.15,16,18,21,22,24 Two studies performed sequential imaging within both time categories.13,20 Six studies fulfilled the criteria for high-quality studies.12–14,16,20,24 Two out of 13 studies had a low risk of bias (Table IV in the online-only Data Supplement).Download figureDownload PowerPointFigure 1. Flowchart. aSAH indicates aneurysmal subarachnoid hemorrhage; DWI, diffusion weighted imaging; and MRI, magnetic resonance imaging.MRI-DWI Lesions Within 72 HoursDiffusion weighted imaging was performed within 72 hours after ictus in 302 patients from 7 studies.12–14,17,19,20,23 Four studies were considered a high-quality study.12–14,20 The median number of patients per study was 38 (range: 15–85). MRI was performed before aneurysm treatment in 264 patients12–14,17,19,20,23 and after treatment in 38 patients.13,23 For 1 study with 15 patients, the corresponding author supplied additional data so that distinction could be made between pre- and post-treatment lesions.23 Four studies defined a lesion as a hyperintense b1000 signal on DWI with a corresponding low ADC signal.12,13,20,23 Two studies defined lesions as high-intensity areas on DWI17,19 and 1 study defined a lesion as an abnormal signal intensity on DWI.14 In 1 study, a comparison of DWI with CT was made to differentiate a lesion signal from a subarachnoid clot.19Pretreatment DWI lesions were reported in 105 of 264 patients (pooled proportion 51%; 95% confidence interval [CI], 24%–77%; Figure 2). The 95% prediction interval was 4% to 96% (Figure 2). The 2 studies with the highest proportion of patients with pretreatment DWI lesions only included patients with a poor clinical condition on admission (Hunt&Hess [H&H]/Hunt&Kosnik IV–V).19,23 In a sensitivity analysis with 4 studies and 150 patients in which lesions were defined as a hyperintense b1000 signal on DWI with a corresponding low ADC signal, the pooled proportion of lesions was 57% (95% CI, 19%–88%; 95% prediction interval, 3%–98%).12,13,20,23 Post-treatment DWI lesions were investigated in 2 studies and found in 26 of 38 patients (pooled proportion 68%; 95% CI, 52%–81%; 95% prediction interval, 52%–81%).13,23Download figureDownload PowerPointFigure 2. Forest plot of pretreatment diffusion weighted imaging lesions <72 h after ictus. CI indicates confidence interval.Determinants of Pretreatment MRI-DWI Lesions Within 72 HoursThree studies investigated determinants of pretreatment MRI-DWI lesions within 72 hours after aSAH.14,19,20AgeTwo studies with a total of 123 patients investigated the relationship between age and DWI lesions.19,20 In a high-quality study with 85 patients, the mean age of patients with DWI lesions was 62 (±14) years versus 58 (±13) years in those without lesions.20 In a low-quality study with 38 patients, the median age in patients with lesions >10 mm was 63 (interquartile range, 54–73) years, and in patients with lesions <10 mm, the median age was 67 (interquartile range, 55–76) years, compared with 60 (interquartile range, 52–73) years in patients without lesions.19 Because no individual patient data were available, data on age could not be pooled, and therefore, a potential relationship between age and presence of DWI lesions remains unclear.SexOne high-quality study and a low-quality study with a total of 123 patients investigated the relationship between sex and DWI lesions.19,20 DWI lesions were observed in 9 of 45 male patients and in 29 of 78 female patients (risk ratio, 0.54; 95% CI, 0.28–1.03).Clinical Condition on AdmissionOne high-quality study investigated the relationship between clinical condition on admission and presence of pretreatment DWI lesions.14 DWI lesions were observed in 5 out of 7 patients with H&H grade IV–V on admission compared with 0 out of 25 patients with H&H grade I–III (RR, 35.8; 95% CI, 2.2–578.9).14 Clinical grade on admission was associated with lesion prevalence before aneurysm treatment (Metaregression section in the online-only Data Supplement). In a cohort with 75% of patients presenting with a good clinical grade (WFNS or H&H grade I–III) on admission, 30% (95% CI, 10%–62%) of patients are expected to present with pretreatment DWI lesions <72 hours. In a cohort with 75% of patients presenting with a poor clinical grade (WFNS or H&H grade IV–V) on admission, 73% (95% CI, 42%–91%) of patients are expected to have MRI-DWI lesions before aneurysm treatment.Amount of Subarachnoid BloodOne high-quality study studied the relationship between the amount of subarachnoid blood, as measured with the modified Fisher score, and pretreatment DWI lesions.20 A median Fisher score of 3 (range, 1–4) was reported in both in the 7 patients with lesions and in the 78 patients without pretreatment lesions.20DWI Lesions Between 72 Hours and 21 DaysEight studies with 346 patients reported on DWI-MRI between 72 hours to 21 days after ictus.13,15,16,18,21–24 Four studies were high-quality studies.13,16,20,24 The median number of patients per study was 34 (range, 11–100).DWI lesions were assessed in 8 studies and reported in 173 out of 346 patients (47%; 95% CI, 35%–59%; Figure 3).13,15,16,18,20–22,24 The 95% prediction interval was 20% to 76% (Figure 3). The study with the lowest proportion of DWI lesions only included patients with a good clinical condition on admission (H&H I–II).15 In none of the studies was a lesion defined as a hyperintense b1000-signal on DWI with a corresponding low ADC signal.Download figureDownload PowerPointFigure 3. Forest plot of diffusion weighted imaging lesions between 72 h and 21 d after ictus. CI indicates confidence interval.A high-quality study with 61 patients performed MRI within 72 hours and at a median follow-up time of 7 days from ictus.13 Twelve patients were lost to follow-up. New DWI lesions were observed in 25 of 49 patients (51%; 95% CI, 31% to 71%).Determinants of DWI Lesions Between 72 Hours and 21 DaysClinical grade on admission did not influence the prevalence of MRI-DWI lesions between 72 hours and 21 days after ictus (Metaregression section in the online-only Data Supplement). The modality of aneurysm treatment slightly impacted the pooled prevalence. If 75% of patients underwent endovascular coiling, the expected lesion prevalence was 50% (95% CI, 30%–69%). If 25% underwent endovascular coiling, the expected lesion prevalence was 45% (95% CI, 30%–61%). In addition, the pooled lesion prevalence was slightly affected by including day of scanning as a dichotomous determinant. The pooled lesion prevalence was 48% (95% CI, 34%–63%) in a model with studies that on average scanned before day 14, compared with 44% (95% CI, 26%–64%) in a model in which all patients were scanned on day 14 post-ictus.Predictive Value of MRI-DWI Lesions Within 72 Hours for the Development of DCIIn a high-quality study with 85 patients, clinical deterioration because of DCI developed in 6 out of 7 patients with DWI lesions within 72 hours and in 8 out of 78 patients without DWI lesions within 72 hours.20 The positive predictive value of pretreatment DWI lesions within 72 hours for developing clinical deterioration because of DCI was 86% (95% CI, 17%–100%) and the negative predictive value was 90% (95% CI, 69%–100%).MRI-DWI in Patients With Clinical Deterioration Because of DCINo studies were performed that investigated the proportion of patients with clinical deterioration because of DCI with compatible MRI-DWI lesions.DiscussionIn this systematic review, we found that the proportion of patients with MRI-DWI lesions, both pretreatment within 72 hours and between 72 hours and 21 days after ictus, differed widely between studies. This heterogeneity was somewhat wider in the analysis on MRI-DWI lesions pre-treatment within 72 hours compared with the analysis on lesions between 72 hours and 21 days. The wide 95% prediction intervals indicate that for a new, individual study the estimate of the proportion of patients with lesions carries a high level of uncertainty. Metaregression analyses identified clinical condition on admission as a determinant for pretreatment lesions with 72 hours and aneurysm treatment modality and day of MRI as determinants for lesions between 72 hours and 21 days.One high-quality study showed that MRI-DWI lesions within 72 hours predict the later development of DCI. This supports the concept that processes involved in early brain injury after aSAH, such as increased intracranial pressure, microvascular alterations, platelet aggregation, acute vasospasm, and reperfusion injury, induce the development of DCI.25–28No studies are available that directly compare CT and MRI for the evaluation of cerebral ischemia after SAH. Nevertheless, it is plausible that MRI is the preferred method for the detection of cerebral ischemia after SAH because MRI is more sensitive for the detection of small cortical lesions, which have an important effect on outcome after SAH according to autopsy studies.29,30Interestingly, clinical grade on admission only affected lesion prevalence in the model for DWI lesions with 72 hours. Between 72 hours and 21 days, no such effect was found. The reason for this contrasting finding remains unclear. The model that included the day of MRI indicated that lesion prevalence is slightly lower in studies that assessed MRI-DWI lesions on day 14 compared with imaging between 72 hours and 14 days. This finding is in accordance with the observation from human and animal studies that DWI hyperintensities may partially or fully reverse.31–33 It has been found that even lesions with markedly decreased ADC normalize between day 1 and day 7 after stroke.34A limitation of our study is that not all studies specified the evaluation of DWI lesions, which complicates interpretation of the results. The ADC value and DWI signal intensity at different b-levels are the most important features to distinguish various types of brain injury on DWI-MRI. Areas with a hyperintense signal on DWI in combination with a low ADC indicate cytotoxic edema in the acute stage, which typically progress to infarction over time.35 On the other hand, either a hyperintense signal on DWI with a normal ADC, or a DWI lesion which decreases in signal intensity when going from b0 to b1000 images indicates vasogenic edema. Because the ADC value returns to normal around 1 to 4 weeks after ictus, vasogenic edema and ischemia because of cytotoxic edema cannot be distinguished after normalization of the ADC value.35 Second, in the subacute stage, blood products may complicate the characterization of DWI lesions.35,36 Finally, the number of patients available for analysis was low, both in individual studies and in total. Accordingly, outliers in an individual study may strongly impact its results and subsequently the results of the meta-analysis. In addition, only 2 out of 13 studies had a low risk of bias. This limits the ability to identify determinants of DWI lesions and complicates the estimation of the true heterogeneity in lesion prevalence among studies.Conclusion and Future DirectionsDuring the past 15 years, experience has been gained with the use of MRI in patients with aSAH. MRI is an imaging modality that can be used for diagnosing cerebral ischemia at different stages after SAH (Figure 4). More studies are needed to investigate whether MRI is a useful diagnostic tool for the diagnosis of DCI in patients who have clinical deterioration between days 4 and 14 after ictus. Moreover, future MRI studies might challenge the current DCI definition.2 Future research questions may include (1) Does imaging performed within hours after DCI onset confirm the ischemic mechanism of clinical deterioration?; (2) What is the additional value of arterial spin labeling and perfusion weighted imaging besides DWI?; (3) Are MRI-DWI lesions on admission risk factors for developing procedure-related ischemia from endovascular or neurosurgical treatment of the aneurysm?; and (4) Are MRI-DWI lesions on admission associated with functional outcome in SAH patients who do not develop complications in the first 3 weeks after the hemorrhage? We suggest well-designed prospective, longitudinal studies in unselected patient cohorts with large numbers of patients, detailed descriptions of the results, and MRI at predefined days to establish the proportion of patients with DWI lesions, study determinants of lesions, and investigate the evolution of cerebral ischemia and the impact of complications and interventions on cerebral ischemia after aSAH.Download figureDownload PowerPointFigure 4. Magnetic resonance imaging for diagnosing cerebral ischemia at different stages after aneurysmal subarachnoid hemorrhage.Sources of FundingThis work was supported by the Netherlands Organization for Scientific Research under grant no. 91712322 (J. Hendrikse) and by the European Research Council under grant agreement no. 637024 (J. Hendrikse).DisclosuresNone.FootnotesThe online-only Data Supplement is available with this article at http://stroke.ahajournals.org/lookup/suppl/doi:10.1161/STROKEAHA.116.011707/-/DC1.Correspondence to Mervyn D.I. 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Osborn A and Grigoryev M (2019) Subarachnoidalblutung und Aneurysmen Osborn's Brain, 10.1016/B978-3-437-21041-9.00006-6, (113-141), . Nelson S, Sair H and Stevens R (2018) Magnetic Resonance Imaging in Aneurysmal Subarachnoid Hemorrhage: Current Evidence and Future Directions, Neurocritical Care, 10.1007/s12028-018-0534-8, 29:2, (241-252), Online publication date: 1-Oct-2018. Gonçalves B, Turon R, Mendes A, Melo N, Lacerda P, Brasil P, Bozza F, Kurtz P and Righy C (2018) Effect of Early Brain Infarction After Subarachnoid Hemorrhage: A Systematic Review and Meta-Analysis, World Neurosurgery, 10.1016/j.wneu.2018.04.037, 115, (e292-e298), Online publication date: 1-Jul-2018. Knipe H and Gaillard F (2008) Subarachnoid haemorrhage Radiopaedia.org, 10.53347/rID-2119 January 2017Vol 48, Issue 1 Advertisement Article InformationMetrics © 2016 American Heart Association, Inc.https://doi.org/10.1161/STROKEAHA.116.011707PMID: 27924052 Manuscript receivedApril 30, 2016Manuscript acceptedNovember 15, 2016Originally publishedDecember 6, 2016Manuscript revisedApril 30, 2016 Keywordssubarachnoid hemorrhageaneurysmischemiamagnetic resonance imagingPDF download Advertisement SubjectsCerebral AneurysmCerebrovascular Disease/StrokeImagingMagnetic Resonance Imaging (MRI)Meta Analysis