Intracerebral hemorrhage: an update on diagnosis and treatment

References

• Poon MT, Fonville AF, Al-Shahi Salman R. Long-term prognosis after intracerebral haemorrhage: systematic review and meta-analysis. J Neurol Neurosurg Psychiatry. 2014 Jun;85(6):660-7. doi: 10.1136/jnnp-2013-306476. Epub 2013 Nov 21.
   Google Scholar
• Bamford J, Sandercock P, Dennis M, et al. A prospective study of acute cerebrovascular disease in the community: the oxfordshire community stroke project–1981-86. 2. Incidence, case fatality rates and overall outcome at one year of cerebral infarction, primary intracerebral and subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry. 1990;53(1):16–22.
   PubMed Web of Science ®Google Scholar
• Naj AC, Jun G, Reitz C, et al. Effects of multiple genetic loci on age at onset in late-onset Alzheimer disease: a genome-wide association study. JAMA Neurol. 2014;71(11):1394–1404.
   PubMed Web of Science ®Google Scholar
• Sudlow CL, Warlow CP. Comparable studies of the incidence of stroke and its pathological types: results from an international collaboration. international stroke incidence collaboration. Stroke. 1997;28(3):491–499.
   PubMed Web of Science ®Google Scholar
• van Asch CJ, Luitse MJ, Rinkel GJ, et al. Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: a systematic review and meta-analysis. Lancet Neurol. 2010;9(2):167–176.
   PubMed Web of Science ®Google Scholar
• Woo D, Sauerbeck LR, Kissela BM, et al. Genetic and environmental risk factors for intracerebral hemorrhage: preliminary results of a population-based study. Stroke. 2002;33(5):1190–1195.
   PubMed Web of Science ®Google Scholar
• Hong KS, Bang OY, Kang DW, et al. Stroke statistics in Korea: part I. Epidemiology and risk factors: a report from the korean stroke society and clinical research center for stroke. J Stroke. 2013;15(1):2–20.
   PubMed Web of Science ®Google Scholar
• Toyoda K. Epidemiology and registry studies of stroke in Japan. J Stroke. 2013;15(1):21–26.
   PubMed Web of Science ®Google Scholar
• Tatlisumak T, Cucchiara B, Kuroda S, et al. Nontraumatic intracerebral haemorrhage in young adults. Nat Rev Neurol. 2018;14(4):237–250.
   PubMed Web of Science ®Google Scholar
• Moulin S, Labreuche J, Bombois S, et al. Dementia risk after spontaneous intracerebral haemorrhage: a prospective cohort study. Lancet Neurol. 2016;15(8):820–829.
   PubMed Web of Science ®Google Scholar
• Xiong L, Reijmer YD, Charidimou A, et al. Intracerebral hemorrhage and cognitive impairment. Biochim Biophys Acta. 2016;1862(5):939–944.
   PubMed Web of Science ®Google Scholar
• Bejot Y, Cordonnier C, Durier J, et al. Intracerebral haemorrhage profiles are changing: results from the Dijon population-based study. Brain. 2013;136(Pt 2):658–664.
   PubMed Web of Science ®Google Scholar
• Flaherty ML, Kissela B, Woo D, et al. The increasing incidence of anticoagulant-associated intracerebral hemorrhage. Neurology. 2007;68(2):116–121.
   PubMed Web of Science ®Google Scholar
• Lovelock CE, Molyneux AJ, Rothwell PM, et al. Change in incidence and aetiology of intracerebral haemorrhage in Oxfordshire, UK, between 1981 and 2006: a population-based study. Lancet Neurol. 2007;6(6):487–493.
   PubMed Web of Science ®Google Scholar
• Mayo NE, Nadeau L, Daskalopoulou SS, et al. The evolution of stroke in Quebec: a 15-year perspective. Neurology. 2007;68(14):1122–1127.
   PubMed Web of Science ®Google Scholar
• Roger VL, Go AS, Lloyd-Jones DM, et al. Heart disease and stroke statistics–2011 update: a report from the American Heart Association. Circulation. 2011;123(4):e18–e209.
   PubMed Web of Science ®Google Scholar
• Parry-Jones AR, Paley L, Bray BD, et al. Care-limiting decisions in acute stroke and association with survival: analyses of UK national quality register data. Int J Stroke. 2016;11(3):321–331.
   PubMed Web of Science ®Google Scholar
• Fisher CM. Pathological observations in hypertensive cerebral hemorrhage. J Neuropathol Exp Neurol. 1971;30(3):536–550.
   PubMed Web of Science ®Google Scholar
• Vinters HV. Cerebral amyloid angiopathy. A critical review. Stroke. 1987;18(2):311–324.
   PubMed Web of Science ®Google Scholar
• Wilson D, Charidimou A, Werring DJ. Advances in understanding spontaneous intracerebral hemorrhage: insights from neuroimaging. Expert Rev Neurother. 2014;14(6):661–678.
   PubMed Web of Science ®Google Scholar
• Banerjee G, Carare R, Cordonnier C, et al. The increasing impact of cerebral amyloid angiopathy: essential new insights for clinical practice. J Neurol Neurosurg Psychiatry. 2017;88(11):982–994.
   PubMed Web of Science ®Google Scholar
• Hilkens NA, van Asch CJJ, Werring DJ, et al. Predicting the presence of macrovascular causes in non-traumatic intracerebral haemorrhage: the DIAGRAM prediction score. J Neurol Neurosurg Psychiatry. 2018;89(7):674–679.
   PubMed Web of Science ®Google Scholar
• Walsh KB, Woo D, Sekar P, et al. Untreated hypertension: A powerful risk factor for lobar and nonlobar intracerebral hemorrhage in whites, blacks, and hispanics. Circulation. 2016;134(19):1444–1452.
   PubMed Web of Science ®Google Scholar
• Van Dorpe J, Smeijers L, Dewachter I, et al. Prominent cerebral amyloid angiopathy in transgenic mice overexpressing the london mutant of human APP in neurons. Am J Pathol. 2000;157(4):1283–1298.
   PubMed Web of Science ®Google Scholar
• Weller RO, Massey A, Kuo YM, et al. Cerebral amyloid angiopathy: accumulation of A beta in interstitial fluid drainage pathways in Alzheimer’s disease. Ann N Y Acad Sci. 2000;903:110–117.
   PubMed Web of Science ®Google Scholar
• Weller RO, Massey A, Newman TA, et al. Cerebral amyloid angiopathy: amyloid beta accumulates in putative interstitial fluid drainage pathways in Alzheimer’s disease. Am J Pathol. 1998;153(3):725–733.
   PubMed Web of Science ®Google Scholar
• Rodrigues MA, Samarasekera N, Lerpiniere C, et al. The Edinburgh CT and genetic diagnostic criteria for lobar intracerebral haemorrhage associated with cerebral amyloid angiopathy: model development and diagnostic test accuracy study. Lancet Neurol. 2018 Mar;17(3):232-240. doi: 10.1016/S1474-4422(18)30006-1. Epub 2018 Jan 10.
   Google Scholar
• Charidimou A, Gang Q, Werring DJ. Sporadic cerebral amyloid angiopathy revisited: recent insights into pathophysiology and clinical spectrum. J Neurol Neurosurg Psychiatry. 2012;83(2):124–137.
   PubMed Web of Science ®Google Scholar
• Jellinger KA Alzheimer disease and cerebrovascular pathology: an update. J Neural Transm, 109(5–6), 813–836 (2002).
   PubMed Web of Science ®Google Scholar
• Ellis RJ, Olichney JM, Thal LJ, et al. Cerebral amyloid angiopathy in the brains of patients with Alzheimer’s disease: the CERAD experience, Part XV. Neurology. 1996;46(6):1592–1596.
   PubMed Web of Science ®Google Scholar
• Yamada M, Tsukagoshi H, Otomo E, et al. Cerebral amyloid angiopathy in the aged. J Neurol. 1987;234(6):371–376.
   PubMed Web of Science ®Google Scholar
• Linn J, Halpin A, Demaerel P, et al. Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology. 2010;74(17):1346–1350.
   PubMed Web of Science ®Google Scholar
• Greenberg SM, Rebeck GW, Vonsattel JP, et al. Apolipoprotein E epsilon 4 and cerebral hemorrhage associated with amyloid angiopathy. Ann Neurol. 1995;38(2):254–259.
   PubMed Web of Science ®Google Scholar
• Rodrigues MA, Samarasekera N, Lerpiniere C, et al. The Edinburgh CT and genetic diagnostic criteria for lobar intracerebral haemorrhage associated with cerebral amyloid angiopathy: model development and diagnostic test accuracy study. Lancet Neurol. 2018;17(3):232–240.
   PubMed Web of Science ®Google Scholar
• Adams HP Jr., Bendixen BH, Kappelle LJ, et al. Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. trial of org 10172 in acute stroke treatment. Stroke. 1993;24(1):35–41.
   PubMed Web of Science ®Google Scholar
• Amarenco P, Bogousslavsky J, Caplan LR, et al. Classification of stroke subtypes. Cerebrovasc Dis. 2009;27(5):493–501.
   PubMed Web of Science ®Google Scholar
• Amarenco P, Bogousslavsky J, Caplan LR, et al. The ASCOD phenotyping of ischemic stroke (Updated ASCO Phenotyping). Cerebrovasc Dis. 2013;36(1):1–5.
   PubMed Web of Science ®Google Scholar
• Arsava EM, Ballabio E, Benner T, et al. The causative classification of stroke system: an international reliability and optimization study. Neurology. 2010;75(14):1277–1284.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Schmitt A, Wilson D, et al. The cerebral haemorrhage anatomical rating instrument (CHARTS): development and assessment of reliability. J Neurol Sci. 2017;372:178–183.
   PubMed Web of Science ®Google Scholar
• Rannikmae K, Woodfield R, Anderson CS, et al. Reliability of intracerebral hemorrhage classification systems: A systematic review. Int J Stroke. 2016;11(6):626–636.
   PubMed Web of Science ®Google Scholar
• Marti-Fabregas J, Prats-Sanchez L, Martinez-Domeno A, et al. The H-ATOMIC criteria for the etiologic classification of patients with intracerebral hemorrhage. PloS One. 2016;11(6):e0156992.
   PubMed Web of Science ®Google Scholar
• Meretoja A, Strbian D, Putaala J, et al. SMASH-U: a proposal for etiologic classification of intracerebral hemorrhage. Stroke. 2012;43(10):2592–2597.
   PubMed Web of Science ®Google Scholar
• Palm F, Henschke N, Wolf J, et al. Intracerebral haemorrhage in a population-based stroke registry (LuSSt): incidence, aetiology, functional outcome and mortality. J Neurol. 2013;260(10):2541–2550.
   PubMed Web of Science ®Google Scholar
• Garcia-Rodriguez LA, Gaist D, Morton J, et al. Antithrombotic drugs and risk of hemorrhagic stroke in the general population. Neurology. 2013;81(6):566–574.
   PubMed Web of Science ®Google Scholar
• Hart RG. What causes intracerebral hemorrhage during warfarin therapy? Neurology. 2000;55(7):907–908.
   PubMed Web of Science ®Google Scholar
• O’Donnell MJ, Chin SL, Rangarajan S, et al. Global and regional effects of potentially modifiable risk factors associated with acute stroke in 32 countries (INTERSTROKE): a case-control study. Lancet. 2016;388(10046):761–775.
   PubMed Web of Science ®Google Scholar
• Biffi A, Anderson CD, Jagiella JM, et al. APOE genotype and extent of bleeding and outcome in lobar intracerebral haemorrhage: a genetic association study. Lancet Neurol. 2011;10(8):702–709.
   PubMed Web of Science ®Google Scholar
• Palsdottir A, Abrahamson M, Thorsteinsson L, et al. Mutation in cystatin C gene causes hereditary brain haemorrhage. Lancet. 1988;2(8611):603–604.
   PubMed Web of Science ®Google Scholar
• Vidal R, Frangione B, Rostagno A, et al. A stop-codon mutation in the BRI gene associated with familial British dementia. Nature. 1999;399(6738):776–781.
   PubMed Web of Science ®Google Scholar
• Vidal R, Revesz T, Rostagno A, et al. A decamer duplication in the 3ʹ region of the BRI gene originates an amyloid peptide that is associated with dementia in a Danish kindred. Proc Natl Acad Sci U S A. 2000;97(9):4920–4925.
   PubMed Web of Science ®Google Scholar
• Devan WJ, Falcone GJ, Anderson CD, et al. Heritability estimates identify a substantial genetic contribution to risk and outcome of intracerebral hemorrhage. Stroke. 2013;44(6):1578–1583.
   PubMed Web of Science ®Google Scholar
• Biffi A, Sonni A, Anderson CD, et al. Variants at APOE influence risk of deep and lobar intracerebral hemorrhage. Ann Neurol. 2010;68(6):934–943.
   PubMed Web of Science ®Google Scholar
• Domingues-Montanari S, Hernandez-Guillamon M, Fernandez-Cadenas I, et al. ACE variants and risk of intracerebral hemorrhage recurrence in amyloid angiopathy. Neurobiol Aging. 2011;32(3):551 e513–522.
   Web of Science ®Google Scholar
• Nalls MA, Pankratz N, Lill CM, et al. Large-scale meta-analysis of genome-wide association data identifies six new risk loci for Parkinson’s disease. Nat Genet. 2014;46(9):989–993.
   PubMed Web of Science ®Google Scholar
• Radmanesh F, Falcone GJ, Anderson CD, et al. Rare coding variation and risk of intracerebral hemorrhage. Stroke. 2015;46(8):2299–2301.
   PubMed Web of Science ®Google Scholar
• Rannikmae K, Davies G, Thomson PA, et al. Common variation in COL4A1/COL4A2 is associated with sporadic cerebral small vessel disease. Neurology. 2015;84(9):918–926.
   PubMed Web of Science ®Google Scholar
• Nicoll JA, Burnett C, Love S, et al. High frequency of apolipoprotein E epsilon 2 allele in hemorrhage due to cerebral amyloid angiopathy. Ann Neurol. 1997;41(6):716–721.
   PubMed Web of Science ®Google Scholar
• Peck G, Smeeth L, Whittaker J, et al. The genetics of primary haemorrhagic stroke, subarachnoid haemorrhage and ruptured intracranial aneurysms in adults. PLoS One. 2008;3(11):e3691.
   PubMed Web of Science ®Google Scholar
• Sudlow C, Martinez Gonzalez NA, Kim J, et al. Does apolipoprotein E genotype influence the risk of ischemic stroke, intracerebral hemorrhage, or subarachnoid hemorrhage? Systematic review and meta-analyses of 31 studies among 5961 cases and 17,965 controls. Stroke. 2006;37(2):364–370.
   PubMed Web of Science ®Google Scholar
• Broderick JP, Brott TG, Duldner JE, et al. Volume of intracerebral hemorrhage. A powerful and easy-to-use predictor of 30-day mortality. Stroke. 1993;24(7):987–993.
   PubMed Web of Science ®Google Scholar
• Marini S, Devan WJ, Radmanesh F, et al. 17p12 influences hematoma volume and outcome in spontaneous intracerebral hemorrhage. Stroke. 2018 Jul;49(7):1618-1625. doi: 10.1161/STROKEAHA.117.020091. Epub 2018 Jun 18.
   Google Scholar
• Biffi A, Shulman JM, Jagiella JM, et al. Genetic variation at CR1 increases risk of cerebral amyloid angiopathy. Neurology. 2012;78(5):334–341.
   PubMed Web of Science ®Google Scholar
• Falcone GJ, Woo D. Genetics of spontaneous intracerebral hemorrhage. Stroke. 2017;48(12):3420–3424.
   PubMed Web of Science ®Google Scholar
• Josephson CB, White PM, Krishan A, et al. Computed tomography angiography or magnetic resonance angiography for detection of intracranial vascular malformations in patients with intracerebral haemorrhage. Cochrane Database Syst Rev. 2014;9:CD009372.
   Google Scholar
• van Asch CJ, Velthuis BK, Rinkel GJ, et al. Diagnostic yield and accuracy of CT angiography, MR angiography, and digital subtraction angiography for detection of macrovascular causes of intracerebral haemorrhage: prospective, multicentre cohort study. BMJ. 2015;351:h5762.
   PubMed Web of Science ®Google Scholar
• Cordonnier C, Klijn CJ, van Beijnum J, et al. Radiological investigation of spontaneous intracerebral hemorrhage: systematic review and trinational survey. Stroke. 2010;41(4):685–690.
   PubMed Web of Science ®Google Scholar
• Wilson D, Ogungbemi A, Ambler G, et al. Developing an algorithm to identify patients with intracerebral haemorrhage secondary to a macrovascular cause. Eur Stroke J. 2017;2(4):369–376.
   PubMed Web of Science ®Google Scholar
• Boulouis G, Morotti A, Charidimou A, et al. Noncontrast Computed tomography markers of intracerebral hemorrhage expansion. Stroke. 2017;48(4):1120–1125.
   PubMed Web of Science ®Google Scholar
• Demchuk AM, Dowlatshahi D, Rodriguez-Luna D, et al. Prediction of haematoma growth and outcome in patients with intracerebral haemorrhage using the CT-angiography spot sign (PREDICT): a prospective observational study. Lancet Neurol. 2012;11(4):307–314.
   PubMed Web of Science ®Google Scholar
• Biffi A, Anderson CD, Battey TW, et al. Association between blood pressure control and risk of recurrent intracerebral hemorrhage. Jama. 2015;314(9):904–912.
   PubMed Web of Science ®Google Scholar
• Wardlaw JM, Smith EE, Biessels GJ, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol. 2013;12(8):822–838.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Imaizumi T, Moulin S, et al. Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: A meta-analysis. Neurology. 2017;89(8):820–829.
   PubMed Web of Science ®Google Scholar
• Staals J, Makin SD, Doubal FN, et al. Stroke subtype, vascular risk factors, and total MRI brain small-vessel disease burden. Neurology. 2014;83(14):1228–1234.
   PubMed Web of Science ®Google Scholar
• Steiner T, Al-Shahi Salman R, Beer R, et al. European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage. Int J Stroke. 2014 Oct;9(7):840-55. doi: 10.1111/ijs.12309. Epub 2014 Aug 24.
   Google Scholar
• Hemphill JC 3rd, Greenberg SM, Anderson CS, et al. Guidelines for the management of spontaneous intracerebral hemorrhage: A guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2015;46(7):2032–2060.
   PubMed Web of Science ®Google Scholar
• Claude Hemphill J 3rd, Lam A. Emergency neurological life support: intracerebral hemorrhage. Neurocrit Care. 2017;27(Suppl 1):89–101.
   PubMed Web of Science ®Google Scholar
• Leira R, Davalos A, Silva Y, et al. Early neurologic deterioration in intracerebral hemorrhage: predictors and associated factors. Neurology. 2004;63(3):461–467.
   PubMed Web of Science ®Google Scholar
• Specogna AV, Turin TC, Patten SB, et al. Factors associated with early deterioration after spontaneous intracerebral hemorrhage: a systematic review and meta-analysis. PloS One. 2014;9(5):e96743.
   PubMed Web of Science ®Google Scholar
• Fan JS, Huang HH, Chen YC, et al. Emergency department neurologic deterioration in patients with spontaneous intracerebral hemorrhage: incidence, predictors, and prognostic significance. Acad Emerg Med. 2012;19(2):133–138.
   PubMed Web of Science ®Google Scholar
• Brott T, Broderick J, Kothari R, et al. Early hemorrhage growth in patients with intracerebral hemorrhage. Stroke. 1997;28(1):1–5.
   PubMed Web of Science ®Google Scholar
• Lord AS, Gilmore E, Choi HA, et al. Collaboration V-I.Time course and predictors of neurological deterioration after intracerebral hemorrhage. Stroke. 2015;46(3): 647–652.
   PubMed Web of Science ®Google Scholar
• Davis SM, Broderick J, Hennerici M, et al. Hematoma growth is a determinant of mortality and poor outcome after intracerebral hemorrhage. Neurology. 2006;66(8):1175–1181.
   PubMed Web of Science ®Google Scholar
• Sreekrishnan A, Dearborn JL, Greer DM, et al. Intracerebral hemorrhage location and functional outcomes of patients: A systematic literature review and meta-analysis. Neurocrit Care. 2016;25(3):384–391.
   PubMed Web of Science ®Google Scholar
• Murthy SB, Levy AP, Duckworth J, et al. Presence of haptoglobin-2 allele is associated with worse functional outcomes after spontaneous intracerebral hemorrhage. World Neurosurg. 2015;83(4):583–587.
   PubMed Web of Science ®Google Scholar
• Szepesi R, Szell IK, Hortobagyi T, et al. New prognostic score for the prediction of 30-day outcome in spontaneous supratentorial cerebral haemorrhage. Biomed Res Int. 2015;961085:2015.
   Google Scholar
• Tetri S, Juvela S, Saloheimo P, et al. Hypertension and diabetes as predictors of early death after spontaneous intracerebral hemorrhage. J Neurosurg. 2009;110(3):411–417.
   PubMed Web of Science ®Google Scholar
• Tetri S, Mantymaki L, Juvela S, et al. Impact of ischemic heart disease and atrial fibrillation on survival after spontaneous intracerebral hemorrhage. J Neurosurg. 2008;108(6):1172–1177.
   PubMed Web of Science ®Google Scholar
• Al-Shahi Salman R, Frantzias J, Lee RJ, et al. Absolute risk and predictors of the growth of acute spontaneous intracerebral haemorrhage: a systematic review and meta-analysis of individual patient data. Lancet Neurol. 2018;17(10):885–894.
   PubMed Web of Science ®Google Scholar
• Flibotte JJ, Hagan N, O’Donnell J, et al. Warfarin, hematoma expansion, and outcome of intracerebral hemorrhage. Neurology. 2004;63(6):1059–1064.
   PubMed Web of Science ®Google Scholar
• Langhorne P, Fearon P, Ronning OM, et al. Stroke unit care benefits patients with intracerebral hemorrhage: systematic review and meta-analysis. Stroke. 2013;44(11):3044–3049.
   PubMed Web of Science ®Google Scholar
• Kurtz P, Fitts V, Sumer Z, et al. How does care differ for neurological patients admitted to a neurocritical care unit versus a general ICU? Neurocrit Care. 2011;15(3):477–480.
   PubMed Web of Science ®Google Scholar
• Knopf L, Staff I, Gomes J, et al. Impact of a neurointensivist on outcomes in critically ill stroke patients. Neurocrit Care. 2012;16(1):63–71.
   PubMed Web of Science ®Google Scholar
• Diringer MN, Edwards DF. Admission to a neurologic/neurosurgical intensive care unit is associated with reduced mortality rate after intracerebral hemorrhage. Crit Care Med. 2001;29(3):635–640.
   PubMed Web of Science ®Google Scholar
• Evans A, Perez I, Harraf F, et al. Can differences in management processes explain different outcomes between stroke unit and stroke-team care? Lancet. 2001;358(9293):1586–1592.
   PubMed Web of Science ®Google Scholar
• Fischer U, Cooney MT, Bull LM, et al. Acute post-stroke blood pressure relative to premorbid levels in intracerebral haemorrhage versus major ischaemic stroke: a population-based study. Lancet Neurol. 2014;13(4):374–384.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Luna D, Pineiro S, Rubiera M, et al. Impact of blood pressure changes and course on hematoma growth in acute intracerebral hemorrhage. Eur J Neurol. 2013;20(9):1277–1283.
   PubMed Web of Science ®Google Scholar
• Sakamoto Y, Koga M, Todo K, et al. Relative systolic blood pressure reduction and clinical outcomes in hyperacute intracerebral hemorrhage: the SAMURAI-ICH observational study. J Hypertens. 2015;33(5):1069–1073.
   PubMed Web of Science ®Google Scholar
• Sakamoto Y, Koga M, Yamagami H, et al. Systolic blood pressure after intravenous antihypertensive treatment and clinical outcomes in hyperacute intracerebral hemorrhage: the stroke acute management with urgent risk-factor assessment and improvement-intracerebral hemorrhage study. Stroke. 2013;44(7):1846–1851.
   PubMed Web of Science ®Google Scholar
• Anderson CS, Heeley E, Huang Y, et al. Rapid blood-pressure lowering in patients with acute intracerebral hemorrhage. N Engl J Med. 2013;368(25):2355–2365.
   PubMed Web of Science ®Google Scholar
• Qureshi AI, Palesch YY, Barsan WG, et al. Intensive blood-pressure lowering in patients with acute cerebral hemorrhage. N Engl J Med. 2016;375(11):1033–1043.
   PubMed Web of Science ®Google Scholar
• Boulouis G, Morotti A, Goldstein JN, et al. Intensive blood pressure lowering in patients with acute intracerebral haemorrhage: clinical outcomes and haemorrhage expansion. Systematic review and meta-analysis of randomised trials. J Neurol Neurosurg Psychiatry. 2017;88(4):339–345.
   PubMed Web of Science ®Google Scholar
• Lattanzi S, Cagnetti C, Provinciali L, et al. How should we lower blood pressure after cerebral hemorrhage? A systematic review and meta-analysis. Cerebrovascular Dis. 2017;43(5–6):207–213.
   PubMed Web of Science ®Google Scholar
• Toyoda K, Koga M, Yamamoto H, et al. Clinical outcomes depending on acute blood pressure after cerebral hemorrhage. Ann Neurol. 2019;85(1):105–113.
   PubMed Web of Science ®Google Scholar
• Kidwell CS, Rosand J, Norato G, et al. Ischemic lesions, blood pressure dysregulation, and poor outcomes in intracerebral hemorrhage. Neurology. 2017 Feb 21;88(8):782-788. doi: 10.1212/WNL.0000000000003630. Epub 2017 Jan 25.
   Web of Science ®Google Scholar
• Al-Shahi Salman R, Law ZK, Bath PM, et al. Haemostatic therapies for acute spontaneous intracerebral haemorrhage. Cochrane Database Syst Rev. 2018;4:CD005951.
   PubMed Web of Science ®Google Scholar
• Sprigg N, Flaherty K, Appleton JP, et al. Tranexamic acid for hyperacute primary IntraCerebral Haemorrhage (TICH-2): an international randomised, placebo-controlled, phase 3 superiority trial. Lancet. 2018;391(10135):2107–2115.
   PubMed Web of Science ®Google Scholar
• Thompson BB, Bejot Y, Caso V, et al. Prior antiplatelet therapy and outcome following intracerebral hemorrhage: a systematic review. Neurology. 2010;75(15):1333–1342.
   PubMed Web of Science ®Google Scholar
• Flaherty ML, Haverbusch M, Sekar P, et al. Location and outcome of anticoagulant-associated intracerebral hemorrhage. Neurocrit Care. 2006;5(3):197–201.
   PubMed Web of Science ®Google Scholar
• Baharoglu MI, Cordonnier C, Al-Shahi Salman R, et al. Platelet transfusion versus standard care after acute stroke due to spontaneous cerebral haemorrhage associated with antiplatelet therapy (PATCH): a randomised, open-label, phase 3 trial. Lancet. 2016;387(10038):2605–2613.
   PubMed Web of Science ®Google Scholar
• Kuramatsu JB, Gerner ST, Schellinger PD, et al. Anticoagulant reversal, blood pressure levels, and anticoagulant resumption in patients with anticoagulation-related intracerebral hemorrhage. Jama. 2015;313(8):824–836.
   PubMed Web of Science ®Google Scholar
• Steiner T, Poli S, Griebe M, et al. Fresh frozen plasma versus prothrombin complex concentrate in patients with intracranial haemorrhage related to vitamin K antagonists (INCH): a randomised trial. Lancet Neurol. 2016;15(6):566–573.
   PubMed Web of Science ®Google Scholar
• Steiner T, Weitz JI, Veltkamp R. anticoagulant-associated intracranial hemorrhage in the era of reversal agents. Stroke. 2017;48(5):1432–1437.
   PubMed Web of Science ®Google Scholar
• Ruff CT, Giugliano RP, Braunwald E, et al. Comparison of the efficacy and safety of new oral anticoagulants with warfarin in patients with atrial fibrillation: a meta-analysis of randomised trials. Lancet. 2014;383(9921):955–962.
   PubMed Web of Science ®Google Scholar
• Wilson D, Seiffge DJ, Traenka C, et al. Outcome of intracerebral hemorrhage associated with different oral anticoagulants. Neurology. 2017;88(18):1693–1700.
   PubMed Web of Science ®Google Scholar
• Tsivgoulis G, Lioutas VA, Varelas P, et al. Direct oral anticoagulant- vs vitamin K antagonist-related nontraumatic intracerebral hemorrhage. Neurology. 2017;89:1142–1151.
   Web of Science ®Google Scholar
• Tsivgoulis G, Wilson D, Katsanos AH, et al. Neuroimaging and clinical outcomes of oral anticoagulant associated ICH. Ann Neurol. 2018 Nov;84(5):694-704. doi: 10.1002/ana.25342. Epub 2018 Oct 25.
   Web of Science ®Google Scholar
• Gerner ST, Kuramatsu JB, Sembill JA, et al. Association of prothrombin complex concentrate administration and hematoma enlargement in non-vitamin K antagonist oral anticoagulant-related intracerebral hemorrhage. Ann Neurol. 2018;83(1):186–196.
   PubMed Web of Science ®Google Scholar
• Pollack CV Jr., Reilly PA, Eikelboom J, et al. Idarucizumab for dabigatran reversal. N Engl J Med. 2015;373(6):511–520.
   PubMed Web of Science ®Google Scholar
• Pollack CV Jr., Reilly PA, van Ryn J, et al. Idarucizumab for dabigatran reversal - Full Cohort Analysis. N Engl J Med. 2017;377(5):431–441.
   PubMed Web of Science ®Google Scholar
• Connolly SJ, Milling TJ Jr., Eikelboom JW, et al. Andexanet Alfa for acute major bleeding associated with factor Xa inhibitors. N Engl J Med. 2016.
   Web of Science ®Google Scholar
• Buchheit J, Reddy P, Connors JM. Idarucizumab (Praxbind) formulary review. Crit Pathw Cardiol. 2016;15(3):77–81.
   PubMedGoogle Scholar
• Hutcherson TC, Cieri-Hutcherson NE, Bhatt R. Evidence for Idarucizumab (Praxbind) in the Reversal of the direct thrombin inhibitor dabigatran: review following the RE-VERSE AD full cohort analysis. P T. 2017;42(11):692–698.
   PubMedGoogle Scholar
• Andexxa–an antidote for apixaban and rivaroxaban. Med Lett Drugs Ther. 2018;60(1549):99–101.
   PubMed Web of Science ®Google Scholar
• Mendelow AD, Gregson BA, Fernandes HM, et al. Early surgery versus initial conservative treatment in patients with spontaneous supratentorial intracerebral haematomas in the international surgical trial in intracerebral haemorrhage (STICH): a randomised trial. Lancet. 2005;365(9457):387–397.
   PubMed Web of Science ®Google Scholar
• Mendelow AD, Gregson BA, Rowan EN, et al. Early surgery versus initial conservative treatment in patients with spontaneous supratentorial lobar intracerebral haematomas (STICH II): a randomised trial. Lancet. 2013;382(9890):397–408.
   PubMed Web of Science ®Google Scholar
• Hanley DF, Lane K, McBee N, et al. Thrombolytic removal of intraventricular haemorrhage in treatment of severe stroke: results of the randomised, multicentre, multiregion, placebo-controlled CLEAR III trial. Lancet. 2017;389(10069):603–611.
   PubMed Web of Science ®Google Scholar
• Mould WA, Carhuapoma JR, Muschelli J, et al. Minimally invasive surgery plus recombinant tissue-type plasminogen activator for intracerebral hemorrhage evacuation decreases perihematomal edema. Stroke. 2013;44(3):627–634.
   PubMed Web of Science ®Google Scholar
• Hanley DF, Thompson RE, Rosenblum M, et al. Efficacy and safety of minimally invasive surgery with thrombolysis in intracerebral haemorrhage evacuation (MISTIE III): a randomised, controlled, open-label, blinded endpoint phase 3 trial. Lancet. 2019;393(10175):1021–1032.
   PubMed Web of Science ®Google Scholar
• Kellner CP, Chartrain AG, Nistal DA, et al. The stereotactic intracerebral hemorrhage underwater blood aspiration (SCUBA) technique for minimally invasive endoscopic intracerebral hemorrhage evacuation. J Neurointerv Surg. 2018;10(8):771–776.
   PubMed Web of Science ®Google Scholar
• Hanley DF, Thompson RE, Muschelli J, et al. Safety and efficacy of minimally invasive surgery plus alteplase in intracerebral haemorrhage evacuation (MISTIE): a randomised, controlled, open-label, phase 2 trial. Lancet Neurol. 2016;15(12):1228–1237.
   PubMed Web of Science ®Google Scholar
• Werring DJ. Outlook for intracerebral haemorrhage after a MISTIE spell. Lancet Neurol. 2016;15(12):1197–1199.
   PubMed Web of Science ®Google Scholar
• Fung C, Murek M, Klinger-Gratz PP, et al. Effect of decompressive craniectomy on perihematomal edema in patients with intracerebral hemorrhage. PLoS One. 2016;11(2):e0149169.
   PubMed Web of Science ®Google Scholar
• Fung C, Murek M, Z’Graggen WJ, et al. Decompressive hemicraniectomy in patients with supratentorial intracerebral hemorrhage. Stroke. 2012;43(12):3207–3211.
   PubMed Web of Science ®Google Scholar
• Flaherty ML, Woo D, Haverbusch M, et al. Racial variations in location and risk of intracerebral hemorrhage. Stroke. 2005;36(5):934–937.
   PubMed Web of Science ®Google Scholar
• Gujjar AR, Deibert E, Manno EM, et al. Mechanical ventilation for ischemic stroke and intracerebral hemorrhage: indications, timing, and outcome. Neurology. 1998;51(2):447–451.
   PubMed Web of Science ®Google Scholar
• Kirollos RW, Tyagi AK, Ross SA, et al. Management of spontaneous cerebellar hematomas: a prospective treatment protocol. Neurosurgery. 2001;49(6): 1378–1386. discussion 1386-1377.
   PubMed Web of Science ®Google Scholar
• van Loon J, Van Calenbergh F, Goffin J, et al. Controversies in the management of spontaneous cerebellar haemorrhage. A consecutive series of 49 cases and review of the literature. Acta Neurochir (Wien). 1993;122(3–4):187–193.
   PubMed Web of Science ®Google Scholar
• European Stroke Initiative Writing C, Writing Committee for the EEC, Steiner T, et al. Recommendations for the management of intracranial haemorrhage - part I: spontaneous intracerebral haemorrhage. the European stroke initiative writing committee and the writing committee for the EUSI executive committee. Cerebrovascular Dis. 2006;22(4):294–316.
   PubMed Web of Science ®Google Scholar
• Broderick J, Connolly S, Feldmann E, et al. Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Association Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisciplinary Working Group. Stroke. 2007;38(6):2001–2023.
   PubMed Web of Science ®Google Scholar
• Wang CX, Shuaib A. Neuroprotective effects of free radical scavengers in stroke. Drugs Aging. 2007;24(7):537–546.
   PubMed Web of Science ®Google Scholar
• Satopaa J, Meretoja A, Koivunen RJ, et al. Treatment of intracerebellar haemorrhage: poor outcome and high long-term mortality. Surg Neurol Int. 2017;8:272.
   PubMedGoogle Scholar
• Luney MS, English SW, Longworth A, et al. Acute posterior cranial fossa hemorrhage-is surgical decompression better than expectant medical management? Neurocrit Care. 2016;25(3):365–370.
   PubMed Web of Science ®Google Scholar
• Pantazis G, Tsitsopoulos P, Mihas C, et al. Early surgical treatment vs conservative management for spontaneous supratentorial intracerebral hematomas: A prospective randomized study. Surg Neurol. 2006;66(5): 492–501. discussion 501-492.
   PubMedGoogle Scholar
• Zuccarello M, Brott T, Derex L, et al. Early surgical treatment for supratentorial intracerebral hemorrhage: a randomized feasibility study. Stroke. 1999;30(9):1833–1839.
   PubMed Web of Science ®Google Scholar
• Gregson BA, Broderick JP, Auer LM, et al. Individual patient data subgroup meta-analysis of surgery for spontaneous supratentorial intracerebral hemorrhage. Stroke. 2012;43(6):1496–1504.
   PubMed Web of Science ®Google Scholar
• Morgenstern LB, Demchuk AM, Kim DH, et al. Rebleeding leads to poor outcome in ultra-early craniotomy for intracerebral hemorrhage. Neurology. 2001;56(10):1294–1299.
   PubMed Web of Science ®Google Scholar
• Steiner T, Al-Shahi Salman R, Beer R, et al. European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage. Int J Stroke. 2014;9(7):840–855.
   PubMed Web of Science ®Google Scholar
• Bhattathiri PS, Gregson B, Prasad KS, et al. Intraventricular hemorrhage and hydrocephalus after spontaneous intracerebral hemorrhage: results from the STICH trial. Acta Neurochir Suppl. 2006;96:65–68.
   PubMedGoogle Scholar
• Gaberel T, Magheru C, Emery E. Management of non-traumatic intraventricular hemorrhage. Neurosurg Rev. 2012;35(4): 485–494. discussion 494-485.
   PubMed Web of Science ®Google Scholar
• Lovasik BP, McCracken DJ, McCracken CE, et al. The effect of external ventricular drain use in intracerebral hemorrhage. World Neurosurg. 2016;94:309–318.
   PubMed Web of Science ®Google Scholar
• Herrick DB, Ullman N, Nekoovaght-Tak S, et al. Determinants of external ventricular drain placement and associated outcomes in patients with spontaneous intraventricular hemorrhage. Neurocrit Care. 2014;21(3):426–434.
   PubMed Web of Science ®Google Scholar
• Gaberel T, Magheru C, Parienti JJ, et al. Intraventricular fibrinolysis versus external ventricular drainage alone in intraventricular hemorrhage: a meta-analysis. Stroke. 2011;42(10):2776–2781.
   PubMed Web of Science ®Google Scholar
• Moradiya Y, Murthy SB, Newman-Toker DE, et al. Intraventricular thrombolysis in intracerebral hemorrhage requiring ventriculostomy: a decade-long real-world experience. Stroke. 2014;45(9):2629–2635.
   PubMed Web of Science ®Google Scholar
• Naff N, Williams MA, Keyl PM, et al. Low-dose recombinant tissue-type plasminogen activator enhances clot resolution in brain hemorrhage: the intraventricular hemorrhage thrombolysis trial. Stroke. 2011;42(11):3009–3016.
   PubMed Web of Science ®Google Scholar
• Maas MB, Rosenberg NF, Kosteva AR, et al. Surveillance neuroimaging and neurologic examinations affect care for intracerebral hemorrhage. Neurology. 2013;81(2):107–112.
   PubMed Web of Science ®Google Scholar
• Biffi A, Kuramatsu JB, Leasure A, et al. Oral Anticoagulation and functional outcome after intracerebral hemorrhage. Ann Neurol. 2017 Nov;82(5):755-765. doi: 10.1002/ana.25079. Epub 2017 Oct 31.
   Web of Science ®Google Scholar
• Korompoki E, Filippidis FT, Nielsen PB, et al. Long-term antithrombotic treatment in intracranial hemorrhage survivors with atrial fibrillation. Neurology. 2017;89(7):687–696.
   PubMed Web of Science ®Google Scholar
• Horstmann S, Zugck C, Krumsdorf U, et al. Left atrial appendage occlusion in atrial fibrillation after intracranial hemorrhage. Neurology. 2014;82(2):135–138.
   PubMed Web of Science ®Google Scholar
• Kuramatsu JB, Sembill JA, Gerner ST, et al. Management of therapeutic anticoagulation in patients with intracerebral haemorrhage and mechanical heart valves. Eur Heart J. 2018;39(19):1709–1723.
   PubMed Web of Science ®Google Scholar
• Goldstein LB, Amarenco P, Lamonte M, et al. Relative effects of statin therapy on stroke and cardiovascular events in men and women: secondary analysis of the Stroke Prevention by Aggressive Reduction in Cholesterol Levels (SPARCL) Study. Stroke. 2008;39(9):2444–2448.
   PubMed Web of Science ®Google Scholar
• Tai SY, Lin FC, Lee CY, et al. Statin use after intracerebral hemorrhage: a 10-year nationwide cohort study. Brain Behav. 2016;6(8):e00487.
   PubMed Web of Science ®Google Scholar
• Jhuo SJ, Tsai WC, Lin TH, et al. statin dose and the risk of intracerebral hemorrhage: A population-based longitudinal study in taiwan. Acta Cardiol Sin. 2016;32(1):23–30.
   PubMed Web of Science ®Google Scholar
• Wang X, Dong Y, Qi X, et al. Cholesterol levels and risk of hemorrhagic stroke: a systematic review and meta-analysis. Stroke. 2013;44(7):1833–1839.
   PubMed Web of Science ®Google Scholar
• Lei C, Chen T, Chen C, et al. Pre-Intracerebral hemorrhage and in-hospital statin use in intracerebral hemorrhage: A systematic review and meta-analysis. World Neurosurg. 2018;111:47–54.
   PubMed Web of Science ®Google Scholar
• Siddiqui FM, Langefeld CD, Moomaw CJ, et al. Use of statins and outcomes in intracerebral hemorrhage patients. Stroke. 2017;48(8):2098–2104.
   PubMed Web of Science ®Google Scholar
• Ziff OJ, Banerjee G, Ambler G, et al. Statins and the risk of intracerebral haemorrhage in patients with stroke: systematic review and meta-analysis. J Neurol Neurosurg Psychiatry. 2019 Jan;90(1):75-83. doi: 10.1136/jnnp-2018-318483. Epub 2018 Aug 27.
   Google Scholar
• Hilkens NA, Greving JP, Algra A, et al. Blood pressure levels and the risk of intracerebral hemorrhage after ischemic stroke. Neurology. 2017;88(2):177–181.
   PubMed Web of Science ®Google Scholar
• Benavente OR, Coffey CS, Conwit R, et al. Blood-pressure targets in patients with recent lacunar stroke: the SPS3 randomised trial. Lancet. 2013;382(9891):507–515.
   PubMed Web of Science ®Google Scholar
• Group PC. Randomised trial of a perindopril-based blood-pressure-lowering regimen among 6,105 individuals with previous stroke or transient ischaemic attack. Lancet. 2001;358(9287):1033–1041.
   PubMed Web of Science ®Google Scholar
• Arima H, Anderson C, Omae T, et al. Effects of blood pressure lowering on intracranial and extracranial bleeding in patients on antithrombotic therapy: the PROGRESS trial. Stroke. 2012;43(6):1675–1677.
   PubMed Web of Science ®Google Scholar
• Arima H, Tzourio C, Anderson C, et al. Effects of perindopril-based lowering of blood pressure on intracerebral hemorrhage related to amyloid angiopathy: the PROGRESS trial. Stroke. 2010;41(2):394–396.
   PubMed Web of Science ®Google Scholar
• Aronowski J, Zhao X. Molecular pathophysiology of cerebral hemorrhage: secondary brain injury. Stroke. 2011;42(6):1781–1786.
   PubMed Web of Science ®Google Scholar
• Selim M, Foster LD, Moy CS, et al. Deferoxamine mesylate in patients with intracerebral haemorrhage (i-DEF): a multicentre, randomised, placebo-controlled, double-blind phase 2 trial. Lancet Neurol. 2019;18(5):428–438.
   PubMed Web of Science ®Google Scholar
• Mracsko E, Veltkamp R. Neuroinflammation after intracerebral hemorrhage. Front Cell Neurosci. 2014;8:388.
   PubMed Web of Science ®Google Scholar
• Fu Y, Hao J, Zhang N, et al. Fingolimod for the treatment of intracerebral hemorrhage: a 2-arm proof-of-concept study. JAMA Neurol. 2014;71(9):1092–1101.
   PubMed Web of Science ®Google Scholar
• Galea J, Brough D. The role of inflammation and interleukin-1 in acute cerebrovascular disease. J Inflamm Res. 2013;6:121–128.
   PubMedGoogle Scholar
• Galea J, Ogungbenro K, Hulme S, et al. Reduction of inflammation after administration of interleukin-1 receptor antagonist following aneurysmal subarachnoid hemorrhage: results of the Subcutaneous Interleukin-1Ra in SAH (SCIL-SAH) study. J Neurosurg. 2018;128(2):515–523.
   PubMed Web of Science ®Google Scholar
• Smith CJ, Hulme S, Vail A, et al. SCIL-STROKE (Subcutaneous Interleukin-1 Receptor Antagonist in Ischemic Stroke): A randomized controlled phase 2 trial. Stroke. 2018;49(5):1210–1216.
   PubMed Web of Science ®Google Scholar
• Morotti A, Phuah CL, Anderson CD, et al. Leukocyte count and intracerebral hemorrhage expansion. Stroke. 2016;47(6):1473–1478.
   PubMed Web of Science ®Google Scholar
• Morotti A, Marini S, Jessel MJ, et al. Lymphopenia, infectious complications, and outcome in spontaneous intracerebral hemorrhage. Neurocrit Care. 2017;26(2):160–166.
   PubMed Web of Science ®Google Scholar
• Andersen CB, Torvund-Jensen M, Nielsen MJ, et al. Structure of the haptoglobin-haemoglobin complex. Nature. 2012;489(7416):456–459.
   PubMed Web of Science ®Google Scholar
• Bulters D, Gaastra B, Zolnourian A, et al. Haemoglobin scavenging in intracranial bleeding: biology and clinical implications. Nat Rev Neurol. 2018 Jul;14(7):416-432. doi: 10.1038/s41582-018-0020-0.
   Google Scholar
• Cooper CE, Schaer DJ, Buehler PW, et al. Haptoglobin binding stabilizes hemoglobin ferryl iron and the globin radical on tyrosine beta145. Antioxid Redox Signal. 2013;18(17):2264–2273.
   PubMed Web of Science ®Google Scholar
• Huang FP, Xi G, Keep RF, et al. Brain edema after experimental intracerebral hemorrhage: role of hemoglobin degradation products. J Neurosurg. 2002;96(2):287–293.
   PubMed Web of Science ®Google Scholar
• Morotti A, Dowlatshahi D, Boulouis G, et al. Predicting intracerebral hemorrhage expansion with noncontrast computed tomography: the BAT score. Stroke. 2018;49(5):1163–1169.
   PubMed Web of Science ®Google Scholar
• Chilamkurthy S, Ghosh R, Tanamala S, et al. Deep learning algorithms for detection of critical findings in head CT scans: a retrospective study. Lancet. 2018;392(10162):2388–2396.
   PubMed Web of Science ®Google Scholar
• Hemphill JC 3rd, Bonovich DC, Besmertis L, et al. The ICH score: a simple, reliable grading scale for intracerebral hemorrhage. Stroke. 2001;32(4):891–897.
   PubMed Web of Science ®Google Scholar
• Wilson D, Ambler G, Shakeshaft C, et al. Cerebral microbleeds and intracranial haemorrhage risk in patients anticoagulated for atrial fibrillation after acute ischaemic stroke or transient ischaemic attack (CROMIS-2): a multicentre observational cohort study. Lancet Neurol. 2018;17(6):539–547.
   PubMed Web of Science ®Google Scholar
• Charidimou A, Peeters AP, Jäger R, et al. Cortical superficial siderosis and intracerebral hemorrhage risk in cerebral amyloid angiopathy. Neurology. 2013 Nov 5;81(19):1666–1673.
   PubMed Web of Science ®Google Scholar