Edema Extension Distance
2015; Lippincott Williams & Wilkins; Volume: 46; Issue: 6 Linguagem: Português
10.1161/strokeaha.115.008818
ISSN1524-4628
AutoresAdrian Parry‐Jones, Xia Wang, Shoichiro Sato, W. Andrew Mould, Andy Vail, Craig S. Anderson, Daniel F. Hanley,
Tópico(s)Machine Learning in Healthcare
ResumoHomeStrokeVol. 46, No. 6Edema Extension Distance Free AccessResearch ArticlePDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessResearch ArticlePDF/EPUBEdema Extension DistanceOutcome Measure for Phase II Clinical Trials Targeting Edema After Intracerebral Hemorrhage Adrian R. Parry-Jones, MD, PhD, Xia Wang, MMed, Shoichiro Sato, MD, PhD, W. Andrew Mould, BA, Andy Vail, MSc, Craig S. Anderson, MD, PhD and Daniel F. Hanley, MD Adrian R. Parry-JonesAdrian R. Parry-Jones From the Centre for Vascular and Stroke Research, Manchester Academic Health Sciences Centre, Salford Royal NHS Foundation Trust (A.R.P.-J., A.V.) and Centre for Biostatistics (A.V.), University of Manchester, Manchester, United Kingdom; Greater Manchester Comprehensive Stroke Centre, Salford Royal NHS Foundation Trust, Salford, United Kingdom (A.R.P.-J.); Neurological and Mental Health Division, The George Institute for Global Health, University of Sydney and Royal Prince Alfred Hospital, Sydney, Australia (X.W., S.S., C.S.A.); and Division of Brain Injury Outcomes, Department of Neurology, Johns Hopkins Medical Institutions, Baltimore, MD (W.A.M., D.F.H.). , Xia WangXia Wang From the Centre for Vascular and Stroke Research, Manchester Academic Health Sciences Centre, Salford Royal NHS Foundation Trust (A.R.P.-J., A.V.) and Centre for Biostatistics (A.V.), University of Manchester, Manchester, United Kingdom; Greater Manchester Comprehensive Stroke Centre, Salford Royal NHS Foundation Trust, Salford, United Kingdom (A.R.P.-J.); Neurological and Mental Health Division, The George Institute for Global Health, University of Sydney and Royal Prince Alfred Hospital, Sydney, Australia (X.W., S.S., C.S.A.); and Division of Brain Injury Outcomes, Department of Neurology, Johns Hopkins Medical Institutions, Baltimore, MD (W.A.M., D.F.H.). , Shoichiro SatoShoichiro Sato From the Centre for Vascular and Stroke Research, Manchester Academic Health Sciences Centre, Salford Royal NHS Foundation Trust (A.R.P.-J., A.V.) and Centre for Biostatistics (A.V.), University of Manchester, Manchester, United Kingdom; Greater Manchester Comprehensive Stroke Centre, Salford Royal NHS Foundation Trust, Salford, United Kingdom (A.R.P.-J.); Neurological and Mental Health Division, The George Institute for Global Health, University of Sydney and Royal Prince Alfred Hospital, Sydney, Australia (X.W., S.S., C.S.A.); and Division of Brain Injury Outcomes, Department of Neurology, Johns Hopkins Medical Institutions, Baltimore, MD (W.A.M., D.F.H.). , W. Andrew MouldW. Andrew Mould From the Centre for Vascular and Stroke Research, Manchester Academic Health Sciences Centre, Salford Royal NHS Foundation Trust (A.R.P.-J., A.V.) and Centre for Biostatistics (A.V.), University of Manchester, Manchester, United Kingdom; Greater Manchester Comprehensive Stroke Centre, Salford Royal NHS Foundation Trust, Salford, United Kingdom (A.R.P.-J.); Neurological and Mental Health Division, The George Institute for Global Health, University of Sydney and Royal Prince Alfred Hospital, Sydney, Australia (X.W., S.S., C.S.A.); and Division of Brain Injury Outcomes, Department of Neurology, Johns Hopkins Medical Institutions, Baltimore, MD (W.A.M., D.F.H.). , Andy VailAndy Vail From the Centre for Vascular and Stroke Research, Manchester Academic Health Sciences Centre, Salford Royal NHS Foundation Trust (A.R.P.-J., A.V.) and Centre for Biostatistics (A.V.), University of Manchester, Manchester, United Kingdom; Greater Manchester Comprehensive Stroke Centre, Salford Royal NHS Foundation Trust, Salford, United Kingdom (A.R.P.-J.); Neurological and Mental Health Division, The George Institute for Global Health, University of Sydney and Royal Prince Alfred Hospital, Sydney, Australia (X.W., S.S., C.S.A.); and Division of Brain Injury Outcomes, Department of Neurology, Johns Hopkins Medical Institutions, Baltimore, MD (W.A.M., D.F.H.). , Craig S. AndersonCraig S. Anderson From the Centre for Vascular and Stroke Research, Manchester Academic Health Sciences Centre, Salford Royal NHS Foundation Trust (A.R.P.-J., A.V.) and Centre for Biostatistics (A.V.), University of Manchester, Manchester, United Kingdom; Greater Manchester Comprehensive Stroke Centre, Salford Royal NHS Foundation Trust, Salford, United Kingdom (A.R.P.-J.); Neurological and Mental Health Division, The George Institute for Global Health, University of Sydney and Royal Prince Alfred Hospital, Sydney, Australia (X.W., S.S., C.S.A.); and Division of Brain Injury Outcomes, Department of Neurology, Johns Hopkins Medical Institutions, Baltimore, MD (W.A.M., D.F.H.). and Daniel F. HanleyDaniel F. Hanley From the Centre for Vascular and Stroke Research, Manchester Academic Health Sciences Centre, Salford Royal NHS Foundation Trust (A.R.P.-J., A.V.) and Centre for Biostatistics (A.V.), University of Manchester, Manchester, United Kingdom; Greater Manchester Comprehensive Stroke Centre, Salford Royal NHS Foundation Trust, Salford, United Kingdom (A.R.P.-J.); Neurological and Mental Health Division, The George Institute for Global Health, University of Sydney and Royal Prince Alfred Hospital, Sydney, Australia (X.W., S.S., C.S.A.); and Division of Brain Injury Outcomes, Department of Neurology, Johns Hopkins Medical Institutions, Baltimore, MD (W.A.M., D.F.H.). Originally published5 May 2015https://doi.org/10.1161/STROKEAHA.115.008818Stroke. 2015;46:e137–e140Other version(s) of this articleYou are viewing the most recent version of this article. Previous versions: January 1, 2015: Previous Version 1 Perihematomal edema (PHE) complicates acute spontaneous intracerebral hemorrhage (ICH) and can increase mass effect, contributing to early neurological deterioration and poor outcome.1,2 The innate immune response within the brain is a key driver of PHE and is characterized by the activation of resident microglia by damage-associated molecular patterns, infiltration of peripheral immune cells, and the production of inflammatory mediators, all of which increase tissue damage and promote blood–brain barrier breakdown.3 Following the well-documented failure to translate treatments for ischemic stroke from experimental studies to clinical use, early-phase clinical trials to demonstrate proof-of-concept in clinical stroke have been recommended before definitive phase III trials.4 Edema has been widely used as the main outcome to test interventions in preclinical ICH,5 so has considerable appeal as an outcome measure for such early-phase clinical trials. PHE can be reliably and objectively measured using noncontrast computed tomography,6,7 so can be collected easily and cheaply from almost all patients with ICH. However, ICH and PHE volumes are closely correlated,2,6,8 so variation in hematoma volume introduces variation in PHE volume. Unlike experimental ICH (where hematoma volume is tightly controlled by the investigator), hematoma volumes in clinical ICH are highly variable, introducing variability in PHE volumes and increasing the sample size required to demonstrate a given treatment effect. The use of relative PHE volume (PHE volume÷ICH volume) has been suggested as a solution to this, but tends to be disproportionately high for smaller hematomas and has thus been advised against.6 Here, we present a solution to this problem that will allow researchers to demonstrate a reduction in PHE with a much smaller sample size, thus potentially accelerating translational ICH research with reduced costs.Description of the SolutionAs the factors driving edema (eg, damage-associated molecular patterns) are derived from the hematoma and will passively diffuse into the brain parenchyma, they will tend to exert their proinflammatory effects along a similar distance from the hematoma border regardless of ICH volume. We thus hypothesized that for the same intensity of inflammatory response, edema will extend a fairly consistent mean linear distance from the hematoma border (which we have termed the edema extension distance [EED]) across a wide range of hematoma volumes. If this hypothesis is correct, EED would be largely influenced by the intensity of the inflammatory response and not the hematoma volume, thus representing an ideal measure for proof-of-concept trials of immune modulating treatments. We initially tested this hypothesis using a simple theoretical model and compared this with published data sets. Using individual patient data from the conservative arms of the Minimally Invasive Surgery Plus rt-PA for ICH Evacuation Phase II trial (MISTIE II) and the pilot phase Intensive Blood Pressure Reduction in Acute Cerebral Hemorrhage Trial (INTERACT1), we then tested how EED compares with conventional measures (absolute PHE volume, relative PHE volume), in terms of the number of patients required to detect a treatment effect in a clinical trial.Results of Pilot TestingIn developing our theoretical model, we assumed that PHE is contained within an ellipsoid which fully encapsulates a smaller ellipsoid representing the hematoma. We then calculated PHE volume and relative PHE volume across a range of hematoma volumes using 3 fixed EEDs of 0.5, 0.75, and 1.0 cm (Figure 1).9 Our model demonstrates a similar relationship between ICH and PHE volume as observed in previous clinical studies, with a clear tendency for relative PHE volume to increase with smaller ICH volumes, suggesting that EED may indeed be fairly consistent across a wide range of hematoma volumes in clinical ICH. To investigate this further, we pooled individual patient data describing PHE and hematoma volume in 39 patients from the conservative treatment arm of the MISTIE II trial7 and 139 patients from the conservative treatment arm of the INTERACT1 trial.10 For MISTIE II patients, a previously described, semiautomated, threshold-based approach6 was applied using computed tomographic scans to measure ICH and PHE volumes using an open source DICOM viewer (OsiriX v. 4.1, Pixmeo; Geneva, Switzerland). To define edema, a fixed lower Hounsfield unit (HU) value of 5 was used with the upper value adjusted by the reader to obtain the best delineation of edema and avoid artifact introduced by leukoaraiosis, with an absolute maximum of 33 HU allowed. For INTERACT1 patients, ICH and PHE volumes were calculated independently by 2 trained neurologists blind to clinical data, treatment, and date and sequence of scan, using computer-assisted multislice planimetric and voxel threshold techniques in MIStar software, version 3.2 (Apollo Medical Imaging Technology, Melbourne, Australia).8 Although a threshold-based method was also used for the INTERACT1 analysis, unlike the MISTIE II analysis, there was no prespecified upper and lower threshold limit. EED (Figure 2) was calculated for each patient using the following formula:Download figureDownload PowerPointFigure 1. Relationship between perihematomal edema (PHE) volume (A) and relative PHE volume (B) and hematoma volume when edema extension distance (EED) is assumed to be constant at 0.5, 0.75, or 1.0 cm within a theoretical model. The relationships demonstrated approximate well to published patient data from intracerebral hemorrhage patients at 3 to 7 days post onset (C and D). Reprinted from Venkatasubramanian et al9 with permission of the publisher. Copyright ©2011, American Heart Association, Inc.Download figureDownload PowerPointFigure 2. Example of a computed tomographic scan demonstrating delineation of the region of perihematomal edema (PHE; outlined in green) and intracerebral hemorrhage (ICH; outlined in red). The edema extension distance (EED) is the difference between the radius (re) of a sphere (shown in green) equal to the combined volume of PHE and ICH and the radius of a sphere (shown in red) equal to the volume of the ICH alone (rh).Download figureEED was found to be relatively independent of ICH volume (Figure 3), with a mean of 0.32 cm (SD=0.16 cm) at baseline and 0.51 cm (SD=0.23 cm) at day 3 to 4. We then used these data to calculate the sample size required for a trial using PHE at day 3 to 4 as the primary outcome and compared the 3 different edema measures (PHE volume, relative PHE, and EED) across a range of treatment effects (Table). Treatment effects ranging from 5% reduction to 30% reduction were considered for our analysis. Table demonstrates that using relative PHE as the outcome measure leads to a negligible reduction in sample size when compared with PHE volume, so relative PHE has no advantage as a clinical trial outcome measure. However, using EED instead of PHE volume reduces the required sample size by ≈75% across the range of treatment effects examined. As a diagnostic computed tomographic scan is readily available, sample sizes can be reduced even further by also adjusting for PHE at baseline. This adjustment brings sample sizes down to a similar extent for all 3 PHE measures, thus maintaining relative performance.Table. Clinical Trial Sample Size Calculations Using PHE as the Primary OutcomeReduction in Measure, %80% Power90% PowerPHE VolumeRelative PHEEEDPHE VolumeRelative PHEEED5502047751230672163921646101266121032116951619429155625361427527171892031830481425406108252041945227226069301421363718918149Number of patients required in each arm of a clinical trial with PHE at day 3 to 4 as the primary outcome, assuming α=0.05 and either 80% or 90% power to detect a range of reductions in each measure. Calculations based on data from conservative arms of INTERACT 1 and MISTIE II. Mean (SD) for each measure were PHE volume, 25.12 mL (22.53 mL); relative PHE, 1.63 (1.43); EED, 0.51 cm (0.23 cm). EED indicates edema extension distance; INTERACT1, Intensive Blood Pressure Reduction in Acute Cerebral Hemorrhage Trial; MISTIE II, Minimally Invasive Surgery Plus rt-PA for ICH Evacuation Phase II trial; and PHE, perihematomal edema.Download figureDownload PowerPointFigure 3. Relationships between intracerebral hemorrhage volume (ICH) and perihematomal edema (PHE) volume in patients recruited to the conservative arms of the Minimally Invasive Surgery Plus rt-PA for ICH Evacuation phase II trial and Intensive Blood Pressure Reduction in Acute Cerebral Hemorrhage Trial at baseline (A) and day 3 to 4 (C). The relationship between ICH volume and both the relative PHE volume and edema extension distance (EED) are demonstrated at baseline (B) and at day 3 to 4 (D).We tested whether EED was associated with death or dependency at 90 days (according to scores 3–6 on the modified Rankin Scale) using the INTERACT1 data set (n=286), adjusting for age, log ICH volume at 72 hours, and randomized treatment in a multifactorial logistic regression model. EED was not associated with death or dependency at 90 days (odds ratio, 1.03; 95% confidence interval CI, 0.31–3.36; P=0.968). Limiting our analysis to patients with smaller ICH volume ( 500 patients in each arm using PHE volume or relative PHE as the primary outcome.In developing the EED, we made the assumption that ICH and PHE volumes approximate to an ellipsoid shape, but in a significant minority of ICH patients, this is not the case. A previous study of unselected ICH patients found that 70% had a round/ellipsoid hematoma and 24% had an irregular hematoma shape.12 Hematoma shape was not available in the trial data sets used for our analysis, but the participants in the MISTIE II and INTERACT1 trials would be expected to include some with irregularly shaped hematomas. However, even with the inclusion of such patients, we have found that using EED as the primary edema outcome measure leads to reduced sample size requirements to assessments of variable sized treatment effects, suggesting that hematoma shape is unlikely to have an important impact on EED variability. We recognize, however, that this requires confirmation in further analysis.Accurate calculation of the EED is dependent on the robust and accurate measurement of the absolute PHE and ICH volumes. To define PHE volume, we recommend the semiautomated threshold-based approach described by Volbers et al,6 using a HU range of 5 to 33. This technique has been validated against T2-weighted magnetic resonance imaging and shows an excellent intraclass correlation coefficient for interobserver reliability of 0.96 (95% CI, 0.93–0.99).6 Early phase trials would be well advised to use this or similarly robust methods with equivalent interobserver reliability.In agreement with previous work, testing for associations between conventional measures of edema and clinical outcomes in INTERACT1 patients,8 we have found that EED was not an independent predictor of poor outcome. However, edema is only one component of the pathophysiology of the inflammatory response to ICH, and inflammation worsens injury via multiple parallel mechanisms.13 Thus, EED seems to provide a useful surrogate parameter in early phase proof-of-concept clinical trials of anti-inflammatory treatments. Although reduction in edema alone is unlikely to be the only factor that could improve clinical outcomes, it does provide an indication that a treatment can reduce the inflammatory response within the brain. This approach could allow early selection of the most promising treatments to take forward to larger and more expensive trials that test clinical efficacy. It is important to distinguish this approach from that of using reduction of edema (as measured by EED) as a surrogate measure for functional outcome, an approach that is dependent on an association of EED with clinical outcomes, which our findings do not support.Regardless of its association with clinical outcomes, PHE is an ideal primary target for early-phase proof-of-concept clinical trials. Using EED as the preferred PHE measure could allow the necessary data to be acquired with around a quarter of the patients needed for assessments with conventional PHE measures, and thereby serve to accelerate translation of novel findings from the laboratory to the clinic.Sources of FundingThis work did not receive specific funding. The first Intensive Blood Pressure Reduction in Acute Cerebral Hemorrhage Trial study was supported by a Program Grant (571281) from the National Health and Medical Research Council of Australia. The Minimally Invasive Surgery Plus rt-PA for ICH Evacuation phase II trial was supported by the National Institute of Health/National Institute of Neurological Disorders and Stroke with grants number R01Ns046309 and 5U01NS062851. The study was designed, conducted, analyzed, and interpreted by the investigators independent of sponsors.DisclosuresDr Anderson is employed by the George Institute for Global Health, holds a Senior Principal Research Fellowship of the National Health and Medical Research Council of Australia, and has received advisory board fees from Pfizer and The Medicines Company and speaker fees and travel paid by Takeda China and Covidien. The other authors report no conflicts.FootnotesGuest Editor for this article was Bo Norrving, MD, PhD.Correspondence to Adrian R. Parry-Jones, MD, PhD, Brain Injury Research Group Clinical Sciences Bldg Stott Ln, Salford M6 8HD, United Kingdom. E-mail [email protected]References1. Zazulia AR, Diringer MN, Derdeyn CP, Powers WJProgression of mass effect after intracerebral hemorrhage. Stroke. 1999; 30:1167–1173.LinkGoogle Scholar2. Appelboom G, Bruce SS, Hickman ZL, Zacharia BE, Carpenter AM, Vaughan KA, et al. Volume-dependent effect of perihaematomal oedema on outcome for spontaneous intracerebral haemorrhages. J Neurol Neurosurg Psychiatry. 2013; 84:488–493. doi: 10.1136/jnnp-2012-303160.CrossrefMedlineGoogle Scholar3. Keep RF, Hua Y, Xi GIntracerebral haemorrhage: mechanisms of injury and therapeutic targets. Lancet Neurol. 2012; 11:720–731. doi: 10.1016/S1474-4422(12)70104-7.CrossrefMedlineGoogle Scholar4. Fisher M, Feuerstein G, Howells DW, Hurn PD, Kent TA, Savitz SI, et al; STAIR Group. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke. 2009; 40:2244–2250. doi: 10.1161/STROKEAHA.108.541128.LinkGoogle Scholar5. Frantzias J, Sena ES, Macleod MR, Al-Shahi Salman RTreatment of intracerebral hemorrhage in animal models: meta-analysis. Ann Neurol. 2011; 69:389–399. doi: 10.1002/ana.22243.CrossrefMedlineGoogle Scholar6. Volbers B, Staykov D, Wagner I, Dörfler A, Saake M, Schwab S, et al. Semi-automatic volumetric assessment of perihemorrhagic edema with computed tomography. Eur J Neurol. 2011; 18:1323–1328. doi: 10.1111/j.1468-1331.2011.03395.x.CrossrefMedlineGoogle Scholar7. Mould WA, Carhuapoma JR, Muschelli J, Lane K, Morgan TC, McBee NA, et al; MISTIE Investigators. Minimally invasive surgery plus recombinant tissue-type plasminogen activator for intracerebral hemorrhage evacuation decreases perihematomal edema. Stroke. 2013; 44:627–634. doi: 10.1161/STROKEAHA.111.000411.LinkGoogle Scholar8. Arima H, Wang JG, Huang Y, Heeley E, Skulina C, Parsons MW, et al; INTERACT Investigators. Significance of perihematomal edema in acute intracerebral hemorrhage: the INTERACT trial. Neurology. 2009; 73:1963–1968. doi: 10.1212/WNL.0b013e3181c55ed3.CrossrefMedlineGoogle Scholar9. Venkatasubramanian C, Mlynash M, Finley-Caulfield A, Eyngorn I, Kalimuthu R, Snider RW, et al. Natural history of perihematomal edema after intracerebral hemorrhage measured by serial magnetic resonance imaging. Stroke. 2011; 42:73–80. doi: 10.1161/STROKEAHA.110.590646.LinkGoogle Scholar10. Anderson CS, Huang Y, Wang JG, Arima H, Neal B, Peng B, et al; INTERACT Investigators. Intensive blood pressure reduction in acute cerebral haemorrhage trial (INTERACT): a randomised pilot trial. Lancet Neurol. 2008; 7:391–399. doi: 10.1016/S1474-4422(08)70069-3.CrossrefMedlineGoogle Scholar11. Fu Y, Hao J, Zhang N, Ren L, Sun N, Li YJ, et al. Fingolimod for the treatment of intracerebral hemorrhage: a 2-arm proof-of-concept study. JAMA Neurol. 2014; 71:1092–1101. doi: 10.1001/jamaneurol.2014.1065.CrossrefMedlineGoogle Scholar12. Fujii Y, Tanaka R, Takeuchi S, Koike T, Minakawa T, Sasaki OHematoma enlargement in spontaneous intracerebral hemorrhage. J Neurosurg. 1994; 80:51–57. doi: 10.3171/jns.1994.80.1.0051.CrossrefMedlineGoogle Scholar13. Wang J, Doré SInflammation after intracerebral hemorrhage. J Cereb Blood Flow Metab. 2007; 27:894–908. doi: 10.1038/sj.jcbfm.9600403.CrossrefMedlineGoogle Scholar Previous Back to top Next FiguresReferencesRelatedDetailsCited By Marchina S, Trevino-Calderon J, Hassani S, Massaro J, Lioutas V, Carvalho F and Selim M (2022) Perihematomal Edema and Clinical Outcome After Intracerebral Hemorrhage: A Systematic Review and Meta-Analysis, Neurocritical Care, 10.1007/s12028-022-01512-4, 37:1, (351-362), Online publication date: 1-Aug-2022. Wiegertjes K, Voigt S, Jolink W, Koemans E, Schreuder F, van Walderveen M, Wermer M, Meijer F, Duering M, de Leeuw F and Klijn C (2022) Diffusion-Weighted Lesions After Intracerebral Hemorrhage: Associated MRI Findings, Frontiers in Neurology, 10.3389/fneur.2022.882070, 13 Huang X, Wang D, Li S, Zhou Q and Zhou J (2022) Advances in computed tomography-based prognostic methods for intracerebral hemorrhage, Neurosurgical Review, 10.1007/s10143-022-01760-0, 45:3, (2041-2050), Online publication date: 1-Jun-2022. Crilly S, Parry-Jones A, Wang X, Selley J, Cook J, Tapia V, Anderson C, Allan S and Kasher P (2022) Zebrafish drug screening identifies candidate therapies for neuroprotection after spontaneous intracerebral haemorrhage, Disease Models & Mechanisms, 10.1242/dmm.049227, 15:3, Online publication date: 1-Mar-2022. Chen Y, Chen S, Chang J, Wei J, Feng M and Wang R (2021) Perihematomal Edema After Intracerebral Hemorrhage: An Update on Pathogenesis, Risk Factors, and Therapeutic Advances, Frontiers in Immunology, 10.3389/fimmu.2021.740632, 12 Loan J, Gane A, Middleton L, Sargent B, Moullaali T, Rodrigues M, Cunningham L, Wardlaw J, Al-Shahi Salman R, Samarasekera N, Addison A, Ahmad K, Alhadad S, Andrews P, Bisset E, Bodkin P, Bouhaidar R, Brennan P, Campbell B, Chandran S, Cook H, Davenport R, Dennis M, Derry C, Dodds K, Doubal F, Duncan S, Elder A, Fitzpatrick M, Foley P, Fouyas I, Ghosh S, Gibson R, Gordon C, Grant R, Hewett R, Hughes F, Hughes M, Hunt D, Hunter N, Ironside J, Liaquat I, Josephson C, Kamat A, Kealley S, Keir S, Kerr G, Kerrigan S, Keston P, King M, Knight R, Macdonald E, Mackay G, Macleod D, Macleod M, Maguire C, Makin S, Mathews A, Maxwell F, McClellan S, Millar T, Morris Z, Morse T, Mumford C, Murray K, Myles L, Nimmo G, Ng Y, Pal S, Rannikmae K, Rhodes J, Ross J, Russell T, Sandercock P, Sellar R, Shanmuganathan M, Shekhar H, Simms H, Sittampalam M, Smith C, Soleiman H, Spiers H, Statham P, Stavrinos N, Stone J, Stuart J, Sudlow C, Summers D, Taylor P, Torgersen A, van Dijke M, Walker R, Weller B, Whiteley W, Whittle I, Will R, Young W, Anderson J, Broadbent S, Butler L, Caesar D, Cantley P, Carter J, Clegg G, Coull A, Crosswaite A, Dear J, Dummer S, Duncan F, Elder-Gracie T, Enright K, Fitzgerald T, Fothergill J, Frier B, Grant D, Gray A, Hart S, Henderson R, Jaap A, Leigh-Smith S, Jones M, Masson M, McCallum L, McKechnie M, McKillop G, Mead G, Morley W, Morrow B, Morrow F, Murchison J, Murphy R, Ng J, Ogundipe O, Patel D, Pollock A, Reed M, Roberts G, Selvarajah J, Smith R, Stirling C, Turner N, Wilson M, Yordanov S, Bell N, Chambers S, Dewar S, Farquhar D, Harmouche A, Jacob A, Jackson K, Knox A, McCafferty J, Moultrie S, Munang L, Noble D, Ramsay S, Spence L, Threlfall B, Williams A, Wilson J, Fitzgerald A, Jamieson A, Lange P, McIntosh A, Morrison L and Todd I (2020) Association of baseline hematoma and edema volumes with one-year outcome and long-term survival after spontaneous intracerebral hemorrhage: A community-based inception cohort study, International Journal of Stroke, 10.1177/1747493020974282, 16:7, (828-839), Online publication date: 1-Oct-2021. Haider S, Qureshi A, Jain A, Tharmaseelan H, Berson E, Zeevi T, Majidi S, Filippi C, Iseke S, Gross M, Acosta J, Malhotra A, Kim J, Sansing L, Falcone G, Sheth K and Payabvash S (2021) Admission computed tomography radiomic signatures outperform hematoma volume in predicting baseline clinical severity and functional outcome in the ATACH‐2 trial intracerebral hemorrhage population, European Journal of Neurology, 10.1111/ene.15000, 28:9, (2989-3000), Online publication date: 1-Sep-2021. Nawabi J, Elsayed S, Morotti A, Speth A, Liu M, Kniep H, McDonough R, Broocks G, Faizy T, Can E, Sporns P, Fiehler J, Hamm B, Penzkofer T, Bohner G, Schlunk F and Hanning U (2021) Perihematomal Edema and Clinical Outcome in Intracerebral Hemorrhage Related to Different Oral Anticoagulants, Journal of Clinical Medicine, 10.3390/jcm10112234, 10:11, (2234) Tan Y, Gu Y, Zhao Y, Lu Y, Liu X and Zhao Y (2021) Effects of Hemodialysis on Prognosis in Individuals with Comorbid ERSD and ICH: A Retrospective Single-Center Study, Journal of Stroke and Cerebrovascular Diseases, 10.1016/j.jstrokecerebrovasdis.2021.105686, 30:5, (105686), Online publication date: 1-May-2021. Best J and Werring D (2021) Intracerebral Haemorrhage Precision Medicine in Stroke, 10.1007/978-3-030-70761-3_7, (127-159), . Chen J, Li G, Chen M, Jin G, Zhao S, Bai Z, Yang J, Liang H, Xu J, Sun J and Qin M (2020) A noninvasive flexible conformal sensor for accurate real-time monitoring of local cerebral edema based on electromagnetic induction, PeerJ, 10.7717/peerj.10079, 8, (e10079) Wang Q, Huang G, Chen F, Hu P, Ren W, Luan X, Zhou C and He J (2020) Prediabetes is associated with poor functional outcome in patients with intracerebral hemorrhage, Brain and Behavior, 10.1002/brb3.1530, 10:4, Online publication date: 1-Apr-2020. Hostettler I, Morton M, Ambler G, Kazmi N, Gaunt T, Wilson D, Shakeshaft C, Jäger H, Cohen H, Yousry T, Al-Shahi Salman R, Lip G, Brown M, Muir K, Houlden H, Bulters D, Galea I and Werring D (2020) Haptoglobin genotype and outcome after spontaneous intracerebral haemorrhage, Journal of Neurology, Neurosurgery & Psychiatry, 10.1136/jnnp-2019-321774, 91:3, (298-304), Online publication date: 1-Mar-2020. Selim M and Norton C (2018) Perihematomal edema: Implications for intracerebral hemorrhage research and therapeutic advances, Journal of Neuroscience Research, 10.1002/jnr.24372, 98:1, (212-218), Online publication date: 1-Jan-2020. Hurford R, Vail A, Heal C, Ziai W, Dawson J, Murthy S, Wang X, Anderson C, Hanley D and Parry-Jones A (2019) Oedema extension distance in intracerebral haemorrhage: Association with baseline characteristics and long-term outcome, European Stroke Journal, 10.1177/2396987319848203, 4:3, (263-270), Online publication date: 1-Sep-2019. Ironside N, Chen C, Ding D, Mayer S and Connolly E (2019) Perihematomal Edema After Spontaneous Intracerebral Hemorrhage, Stroke, 50:6, (1626-1633), Online publication date: 1-Jun-2019. Volbers B, Fischer U and Huttner H (2018) Inflammation, edema, hematoma and etiology – a rectangular relationship?, European Journal of Neurology, 10.1111/ene.13829, 26:1, Online publication date: 1-Jan-2019. Wu T, Putaala J, Sharma G, Strbian D, Tatlisumak T, Davis S and Meretoja A (2017) Persistent Hyperglycemia Is Associated With Increased Mortality After Intracerebral Hemorrhage, Journal of the American Heart Association, 6:8, Online publication date: 2-Aug-2017.Wu T, Sharma G, Strbian D, Putaala J, Desmond P, Tatlisumak T, Davis S and Meretoja A (2017) Natural History of Perihematomal Edema and Impact on Outcome After Intracerebral Hemorrhage, Stroke, 48:4, (873-879), Online publication date: 1-Apr-2017. Grunwald Z, Beslow L, Urday S, Vashkevich A, Ayres A, Greenberg S, Goldstein J, Leasure A, Shi F, Kahle K, Battey T, Simard J, Rosand J, Kimberly W and Sheth K (2016) Perihematomal Edema Expansion Rates and Patient Outcomes in Deep and Lobar Intracerebral Hemorrhage, Neurocritical Care, 10.1007/s12028-016-0321-3, 26:2, (205-212), Online publication date: 1-Apr-2017. Murthy S, Urday S, Beslow L, Dawson J, Lees K, Kimberly W, Iadecola C, Kamel H, Hanley D, Sheth K and Ziai W (2016) Rate of perihaematomal oedema expansion is associated with poor clinical outcomes in intracerebral haemorrhage, Journal of Neurology, Neurosurgery & Psychiatry, 10.1136/jnnp-2016-313653, 87:11, (1169-1173), Online publication date: 1-Nov-2016. Leasure A, Kimberly W, Sansing L, Kahle K, Kronenberg G, Kunte H, Simard J and Sheth K (2016) Treatment of Edema Associated With Intracerebral Hemorrhage, Current Treatment Options in Neurology, 10.1007/s11940-015-0392-z, 18:2, Online publication date: 1-Feb-2016. June 2015Vol 46, Issue 6 Advertisement Article InformationMetrics © 2015 American Heart Association, Inc.https://doi.org/10.1161/STROKEAHA.115.008818PMID: 25944323 Originally publishedMay 5, 2015 Keywordsclinical trialsbrain edemacerebral hemorrhagePDF download Advertisement SubjectsComputerized Tomography (CT)Intracranial HemorrhageTreatment
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