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Journal of Neural Transmission

, Volume 120, Supplement 1, pp 35–41 | Cite as

Advances in the management of intracerebral hemorrhage

  • J. B. Kuramatsu
  • H. B. Huttner
  • S. Schwab
Neurology and Preclinical Neurological Studies - Review Article

Abstract

Intracerebral hemorrhage (ICH) is one of the most detrimental sub-types of stroke and accounts for 10–15 % of all strokes Qureshi et al. (Lancet 373(9675):1632–1644, 2009). ICH has an incidence of 10–30 cases per 100,000 people/year which is increasing and expected to double by the year 2050 Qureshi et al. (N Engl J Med 344 (19):1450–1460, 2001). Mortality rates still remain poor (30–50 %) and functional dependency after ICH is high (~75 %) van Asch et al. (Lancet Neurol 9 (2):167–176, 2010). Up to now, all randomized controlled trials investigating treatment approaches in ICH have failed to document improvements on clinical endpoints Mayer et al. (N Engl J Med 358 (20):2127–2137, 2008); Brouwers and Goldstein (Neurotherapeutics 9 (1):87–98, 2012). Only a specialized treatment of severely injured patients at dedicated neuro intensive care units [NICU] has been shown to be beneficial Qureshi et al. (Lancet 373(9675):1632–1644, 2009); Suarez et al. (Crit Care Med 32 (11):2311–2317, 2004). Currently, ongoing trials are investigating aggressive blood pressure lowering, hemostatic therapies, different operative strategies, intraventricular thrombolysis as well as neuroprotective approaches, and brain edema therapies. This review will summarize advanced treatment strategies and novel approaches which are currently under investigation.

Keywords

Intracerebral hemorrhage Brain edema treatment Intraventricular fibrinolysis Hypothermia 

References

  1. Anderson CS, Huang Y, Wang JG, Arima H, Neal B, Peng B, Heeley E, Skulina C, Parsons MW, Kim JS, Tao QL, Li YC, Jiang JD, Tai LW, Zhang JL, Xu E, Cheng Y, Heritier S, Morgenstern LB, Chalmers J (2008) Intensive blood pressure reduction in acute cerebral haemorrhage trial (INTERACT): a randomised pilot trial. Lancet Neurol 7(5):391–399. doi: 10.1016/S1474-4422(08)70069-3 PubMedCrossRefGoogle Scholar
  2. Anderson CS, Huang Y, Arima H, Heeley E, Skulina C, Parsons MW, Peng B, Li Q, Su S, Tao QL, Li YC, Jiang JD, Tai LW, Zhang JL, Xu E, Cheng Y, Morgenstern LB, Chalmers J, Wang JG (2010) Effects of early intensive blood pressure-lowering treatment on the growth of hematoma and perihematomal edema in acute intracerebral hemorrhage: the intensive blood pressure reduction in acute cerebral haemorrhage trial (INTERACT). Stroke 41(2):307–312. doi: 10.1161/STROKEAHA.109.561795 PubMedCrossRefGoogle Scholar
  3. Arima H, Tzourio C, Anderson C, Woodward M, Bousser MG, MacMahon S, Neal B, Chalmers J (2010) Effects of perindopril-based lowering of blood pressure on intracerebral hemorrhage related to amyloid angiopathy: the PROGRESS trial. Stroke 41(2):394–396. doi: 10.1161/STROKEAHA.109.563932 PubMedCrossRefGoogle Scholar
  4. Basaldella L, Marton E, Fiorindi A, Scarpa B, Badreddine H, Longatti P (2012) External ventricular drainage alone versus endoscopic surgery for severe intraventricular hemorrhage: a comparative retrospective analysis on outcome and shunt dependency. Neurosurg Focus 32(4):E4. doi: 10.3171/2012.1.FOCUS11349 PubMedCrossRefGoogle Scholar
  5. Bhattathiri PS, Gregson B, Prasad KS, Mendelow AD (2006) Intraventricular hemorrhage and hydrocephalus after spontaneous intracerebral hemorrhage: results from the STICH trial. Acta Neurochir Suppl 96:65–68PubMedCrossRefGoogle Scholar
  6. Broderick J, Connolly S, Feldmann E, Hanley D, Kase C, Krieger D, Mayberg M, Morgenstern L, Ogilvy CS, Vespa P, Zuccarello M (2007a) 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 38(6):2001–2023. doi: 10.1161/STROKEAHA.107.183689 PubMedCrossRefGoogle Scholar
  7. Broderick JP, Diringer MN, Hill MD, Brun NC, Mayer SA, Steiner T, Skolnick BE, Davis SM (2007b) Determinants of intracerebral hemorrhage growth: an exploratory analysis. Stroke 38(3):1072–1075. doi: 10.1161/01.STR.0000258078.35316.30 PubMedCrossRefGoogle Scholar
  8. Brott T, Broderick J, Kothari R, Barsan W, Tomsick T, Sauerbeck L, Spilker J, Duldner J, Khoury J (1997) Early hemorrhage growth in patients with intracerebral hemorrhage. Stroke 28(1):1–5PubMedCrossRefGoogle Scholar
  9. Brouwers HB, Goldstein JN (2012) Therapeutic strategies in acute intracerebral hemorrhage. Neurotherapeutics 9(1):87–98. doi: 10.1007/s13311-011-0091-8 PubMedCrossRefGoogle Scholar
  10. Butcher KS, Baird T, MacGregor L, Desmond P, Tress B, Davis S (2004) Perihematomal edema in primary intracerebral hemorrhage is plasma derived. Stroke 35(8):1879–1885. doi: 10.1161/01.STR.0000131807.54742.1a PubMedCrossRefGoogle Scholar
  11. Chen CC, Liu CL, Tung YN, Lee HC, Chuang HC, Lin SZ, Cho DY (2011) Endoscopic surgery for intraventricular hemorrhage (IVH) caused by thalamic hemorrhage: comparisons of endoscopic surgery and external ventricular drainage (EVD) surgery. World Neurosurg 75(2):264–268. doi: 10.1016/j.wneu.2010.07.041S1878-8750(10)00484-5 PubMedCrossRefGoogle Scholar
  12. Chen M, Wang Q, Zhu W, Yin Q, Ma M, Fan X, Li Y, Ni G, Liu C, Liu W, Zhang R, Xu G, Liu X (2012) Stereotactic aspiration plus subsequent thrombolysis for moderate thalamic hemorrhage. World Neurosurg 77(1):122–129. doi: 10.1016/j.wneu.2011.06.036S1878-8750(11)00811-4 PubMedCrossRefGoogle Scholar
  13. Davis SM, Broderick J, Hennerici M, Brun NC, Diringer MN, Mayer SA, Begtrup K, Steiner T (2006) Hematoma growth is a determinant of mortality and poor outcome after intracerebral hemorrhage. Neurology 66(8):1175–1181. doi: 10.1212/01.wnl.0000208408.98482.99 PubMedCrossRefGoogle Scholar
  14. Finfer S, Liu B, Chittock DR, Norton R, Myburgh JA, McArthur C, Mitchell I, Foster D, Dhingra V, Henderson WR, Ronco JJ, Bellomo R, Cook D, McDonald E, Dodek P, Hebert PC, Heyland DK, Robinson BG (2012) Hypoglycemia and risk of death in critically ill patients. N Engl J Med 367(12):1108–1118. doi: 10.1056/NEJMoa1204942 PubMedCrossRefGoogle Scholar
  15. Fingas M, Clark DL, Colbourne F (2007) The effects of selective brain hypothermia on intracerebral hemorrhage in rats. Exp Neurol 208(2):277–284. doi: 10.1016/j.expneurol.2007.08.018 PubMedCrossRefGoogle Scholar
  16. Freeman BD, Morris PE (2012) Tracheostomy practice in adults with acute respiratory failure. Crit Care Med. doi: 10.1097/CCM.0b013e31825bc948 Google Scholar
  17. Gebel JM Jr, Jauch EC, Brott TG, Khoury J, Sauerbeck L, Salisbury S, Spilker J, Tomsick TA, Duldner J, Broderick JP (2002a) Natural history of perihematomal edema in patients with hyperacute spontaneous intracerebral hemorrhage. Stroke 33(11):2631–2635PubMedCrossRefGoogle Scholar
  18. Gebel JM Jr, Jauch EC, Brott TG, Khoury J, Sauerbeck L, Salisbury S, Spilker J, Tomsick TA, Duldner J, Broderick JP (2002b) Relative edema volume is a predictor of outcome in patients with hyperacute spontaneous intracerebral hemorrhage. Stroke 33(11):2636–2641PubMedCrossRefGoogle Scholar
  19. Goldstein JN, Fazen LE, Snider R, Schwab K, Greenberg SM, Smith EE, Lev MH, Rosand J (2007) Contrast extravasation on CT angiography predicts hematoma expansion in intracerebral hemorrhage. Neurology 68(12):889–894. doi: 10.1212/01.wnl.0000257087.22852.21 PubMedCrossRefGoogle Scholar
  20. Goldstein J, Brouwers H, Romero J, McNamara K, Schwab K, Greenberg S, Rosand J (2012) SCORE-IT: the Spot Sign score in restricting ICH growth horizontal line an Atach-II ancillary study. J Vasc Interv Neurol 5(supp):20–25Google Scholar
  21. Gregson BA, Murray GD, Mitchell PM, Rowan EN, Gholkar AR, Mendelow AD (2012) Update on the Surgical Trial in Lobar Intracerebral Haemorrhage (STICH II): statistical analysis plan. Trials 13:222. doi: 10.1186/1745-6215-13-2221745-6215-13-222 PubMedCrossRefGoogle Scholar
  22. Hanley DF (2009) Intraventricular hemorrhage: severity factor and treatment target in spontaneous intracerebral hemorrhage. Stroke 40(4):1533–1538. doi: 10.1161/STROKEAHA.108.535419 PubMedCrossRefGoogle Scholar
  23. Hauer EM, Stark D, Staykov D, Steigleder T, Schwab S, Bardutzky J (2011) Early continuous hypertonic saline infusion in patients with severe cerebrovascular disease. Crit Care Med 39(7):1766–1772. doi: 10.1097/CCM.0b013e318218a390 PubMedCrossRefGoogle Scholar
  24. Huttner HB, Kohrmann M, Berger C, Georgiadis D, Schwab S (2006a) Predictive factors for tracheostomy in neurocritical care patients with spontaneous supratentorial hemorrhage. Cerebrovasc Dis 21(3):159–165. doi: 10.1159/000090527 PubMedCrossRefGoogle Scholar
  25. Huttner HB, Schwab S, Bardutzky J (2006b) Lumbar drainage for communicating hydrocephalus after ICH with ventricular hemorrhage. Neurocrit Care 5(3):193–196. doi: 10.1385/NCC:5:3:193 PubMedCrossRefGoogle Scholar
  26. Huttner HB, Nagel S, Tognoni E, Kohrmann M, Juttler E, Orakcioglu B, Schellinger PD, Schwab S, Bardutzky J (2007) Intracerebral hemorrhage with severe ventricular involvement: lumbar drainage for communicating hydrocephalus. Stroke 38(1):183–187. doi: 10.1161/01.STR.0000251795.02560.62 PubMedCrossRefGoogle Scholar
  27. Inaji M, Tomita H, Tone O, Tamaki M, Suzuki R, Ohno K (2003) Chronological changes of perihematomal edema of human intracerebral hematoma. Acta Neurochir Suppl 86:445–448PubMedGoogle Scholar
  28. Kawanishi M, Kawai N, Nakamura T, Luo C, Tamiya T, Nagao S (2008) Effect of delayed mild brain hypothermia on edema formation after intracerebral hemorrhage in rats. J Stroke Cerebrovasc Dis 17(4):187–195. doi: 10.1016/j.jstrokecerebrovasdis.2008.01.003 PubMedCrossRefGoogle Scholar
  29. Kazui S, Minematsu K, Yamamoto H, Sawada T, Yamaguchi T (1997) Predisposing factors to enlargement of spontaneous intracerebral hematoma. Stroke 28(12):2370–2375PubMedCrossRefGoogle Scholar
  30. Kimura K, Iguchi Y, Inoue T, Shibazaki K, Matsumoto N, Kobayashi K, Yamashita S (2007) Hyperglycemia independently increases the risk of early death in acute spontaneous intracerebral hemorrhage. J Neurol Sci 255(1–2):90–94. doi: 10.1016/j.jns.2007.02.005 PubMedCrossRefGoogle Scholar
  31. Kiphuth IC, Staykov D, Kohrmann M, Struffert T, Richter G, Bardutzky J, Kollmar R, Maurer M, Schellinger PD, Hilz MJ, Doerfler A, Schwab S, Huttner HB (2009) Early administration of low molecular weight heparin after spontaneous intracerebral hemorrhage. A safety analysis. Cerebrovasc Dis 27(2):146–150. doi: 10.1159/000177923 CrossRefGoogle Scholar
  32. Kollmar R, Staykov D, Dorfler A, Schellinger PD, Schwab S, Bardutzky J (2010) Hypothermia reduces perihemorrhagic edema after intracerebral hemorrhage. Stroke 41(8):1684–1689. doi: 10.1161/STROKEAHA.110.587758 PubMedCrossRefGoogle Scholar
  33. Kurtz P, Fitts V, Sumer Z, Jalon H, Cooke J, Kvetan V, Mayer SA (2011) How does care differ for neurological patients admitted to a neurocritical care unit versus a general ICU? Neurocrit Care 15(3):477–480. doi: 10.1007/s12028-011-9539-2 PubMedCrossRefGoogle Scholar
  34. Lee KR, Kawai N, Kim S, Sagher O, Hoff JT (1997) Mechanisms of edema formation after intracerebral hemorrhage: effects of thrombin on cerebral blood flow, blood-brain barrier permeability, and cell survival in a rat model. J Neurosurg 86(2):272–278. doi: 10.3171/jns.1997.86.2.0272 PubMedCrossRefGoogle Scholar
  35. Longatti PL, Martinuzzi A, Fiorindi A, Maistrello L, Carteri A (2004) Neuroendoscopic management of intraventricular hemorrhage. Stroke 35(2):e35–e38. doi: 10.1161/01.STR.0000113736.73632.F6 PubMedCrossRefGoogle Scholar
  36. Mayer SA (2003) Ultra-early hemostatic therapy for intracerebral hemorrhage. Stroke 34(1):224–229PubMedCrossRefGoogle Scholar
  37. Mayer SA, Sacco RL, Shi T, Mohr JP (1994) Neurologic deterioration in noncomatose patients with supratentorial intracerebral hemorrhage. Neurology 44(8):1379–1384PubMedCrossRefGoogle Scholar
  38. Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, Skolnick BE, Steiner T (2005) Recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med 352(8):777–785. doi: 10.1056/NEJMoa042991 PubMedCrossRefGoogle Scholar
  39. Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, Skolnick BE, Steiner T (2008) Efficacy and safety of recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med 358(20):2127–2137. doi: 10.1056/NEJMoa0707534 PubMedCrossRefGoogle Scholar
  40. Mendelow AD, Gregson BA, Fernandes HM, Murray GD, Teasdale GM, Hope DT, Karimi A, Shaw MD, Barer DH (2005) 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 365(9457):387–397. doi: 10.1016/S0140-6736(05)17826-X PubMedGoogle Scholar
  41. Mendelow AD, Gregson BA, Mitchell PM, Murray GD, Rowan EN, Gholkar AR (2011) Surgical trial in lobar intracerebral haemorrhage (STICH II) protocol. Trials 12:124. doi: 10.1186/1745-6215-12-1241745-6215-12-124 PubMedCrossRefGoogle Scholar
  42. Menon RS, Burgess RE, Wing JJ, Gibbons MC, Shara NM, Fernandez S, Jayam-Trouth A, German L, Sobotka I, Edwards D, Kidwell CS (2012) Predictors of highly prevalent brain ischemia in intracerebral hemorrhage. Ann Neurol 71(2):199–205. doi: 10.1002/ana.22668 PubMedCrossRefGoogle Scholar
  43. Morgan T, Awad I, Keyl P, Lane K, Hanley D (2008a) Preliminary report of the clot lysis evaluating accelerated resolution of intraventricular hemorrhage (CLEAR-IVH) clinical trial. Acta Neurochir Suppl 105:217–220PubMedCrossRefGoogle Scholar
  44. Morgan T, Zuccarello M, Narayan R, Keyl P, Lane K, Hanley D (2008b) Preliminary findings of the minimally-invasive surgery plus rtPA for intracerebral hemorrhage evacuation (MISTIE) clinical trial. Acta Neurochir Suppl 105:147–151PubMedCrossRefGoogle Scholar
  45. Morgenstern LB, Hemphill JC 3rd, Anderson C, Becker K, Broderick JP, Connolly ES Jr, Greenberg SM, Huang JN, MacDonald RL, Messe SR, Mitchell PH, Selim M, Tamargo RJ (2010) Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 41(9):2108–2129. doi: 10.1161/STR.0b013e3181ec611b PubMedCrossRefGoogle Scholar
  46. Naff N, Williams MA, Keyl PM, Tuhrim S, Bullock MR, Mayer SA, Coplin W, Narayan R, Haines S, Cruz-Flores S, Zuccarello M, Brock D, Awad I, Ziai WC, Marmarou A, Rhoney D, McBee N, Lane K, Hanley DF Jr (2011) Low-dose recombinant tissue-type plasminogen activator enhances clot resolution in brain hemorrhage: the intraventricular hemorrhage thrombolysis trial. Stroke 42(11):3009–3016. doi: 10.1161/STROKEAHA.110.610949 PubMedCrossRefGoogle Scholar
  47. Naidech AM, Bernstein RA, Levasseur K, Bassin SL, Bendok BR, Batjer HH, Bleck TP, Alberts MJ (2009) Platelet activity and outcome after intracerebral hemorrhage. Ann Neurol 65(3):352–356. doi: 10.1002/ana.21618 PubMedCrossRefGoogle Scholar
  48. Navalesi P, Frigerio P, Moretti MP, Sommariva M, Vesconi S, Baiardi P, Levati A (2008) Rate of reintubation in mechanically ventilated neurosurgical and neurologic patients: evaluation of a systematic approach to weaning and extubation. Crit Care Med 36(11):2986–2992. doi: 10.1097/CCM.0b013e31818b35f2 PubMedCrossRefGoogle Scholar
  49. O’Donnell HC, Rosand J, Knudsen KA, Furie KL, Segal AZ, Chiu RI, Ikeda D, Greenberg SM (2000) Apolipoprotein E genotype and the risk of recurrent lobar intracerebral hemorrhage. N Engl J Med 342(4):240–245PubMedCrossRefGoogle Scholar
  50. O’Donnell MJ, Xavier D, Liu L, Zhang H, Chin SL, Rao-Melacini P, Rangarajan S, Islam S, Pais P, McQueen MJ, Mondo C, Damasceno A, Lopez-Jaramillo P, Hankey GJ, Dans AL, Yusoff K, Truelsen T, Diener HC, Sacco RL, Ryglewicz D, Czlonkowska A, Weimar C, Wang X, Yusuf S (2010) Risk factors for ischaemic and intracerebral haemorrhagic stroke in 22 countries (the INTERSTROKE study): a case-control study. Lancet 376(9735):112–123. doi: 10.1016/S0140-6736(10)60834-3 PubMedCrossRefGoogle Scholar
  51. Qureshi AI (2007) Antihypertensive Treatment of Acute Cerebral Hemorrhage (ATACH): rationale and design. Neurocrit Care 6(1):56–66. doi: NCC:6:1:56 PubMedCrossRefGoogle Scholar
  52. Qureshi AI, Palesch YY (2011) Antihypertensive Treatment of Acute Cerebral Hemorrhage (ATACH) II: design, methods, and rationale. Neurocrit Care 15(3):559–576. doi: 10.1007/s12028-011-9538-3 PubMedCrossRefGoogle Scholar
  53. Qureshi AI, Tuhrim S, Broderick JP, Batjer HH, Hondo H, Hanley DF (2001) Spontaneous intracerebral hemorrhage. N Engl J Med 344(19):1450–1460PubMedCrossRefGoogle Scholar
  54. Qureshi AI, Mendelow AD, Hanley DF (2009) Intracerebral haemorrhage. Lancet 373(9675):1632–1644. doi: 10.1016/S0140-6736(09)60371-8 PubMedCrossRefGoogle Scholar
  55. Rincon F, Mayer SA (2004) Novel therapies for intracerebral hemorrhage. Curr Opin Crit Care 10(2):94–100 [pii:00075198-200404000-00003]PubMedCrossRefGoogle Scholar
  56. Rincon F, Mayer SA (2007) Neurocritical care: a distinct discipline? Curr Opin Crit Care 13(2):115–121. doi: 10.1097/MCC.0b013e32808255 PubMedCrossRefGoogle Scholar
  57. Schwarz S, Hafner K, Aschoff A, Schwab S (2000) Incidence and prognostic significance of fever following intracerebral hemorrhage. Neurology 54(2):354–361PubMedCrossRefGoogle Scholar
  58. Simard PF, Tosun C, Melnichenko L, Ivanova S, Gerzanich V, Simard JM (2011) Inflammation of the Choroid Plexus and Ependymal Layer of the Ventricle Following Intraventricular Hemorrhage. Transl Stroke Res 2(2):227–231. doi: 10.1007/s12975-011-0070-8 PubMedCrossRefGoogle Scholar
  59. Staykov D, Schwab S (2013) Clearing bloody cerebrospinal fluid: clot lysis, neuroendoscopy and lumbar drainage. Curr Opin Crit Care 19(2):92–100. doi: 10.1097/MCC.0b013e32835cae5e PubMedCrossRefGoogle Scholar
  60. Staykov D, Huttner HB, Struffert T, Ganslandt O, Doerfler A, Schwab S, Bardutzky J (2009) Intraventricular Fibrinolysis and Lumbar Drainage for Ventricular Hemorrhage. Stroke. doi: 10.1161/STROKEAHA.109.551945 PubMedGoogle Scholar
  61. Staykov D, Huttner HB, Lunkenheimer J, Volbers B, Struffert T, Doerfler A, Ganslandt O, Juettler E, Schwab S, Bardutzky J (2010) Single versus bilateral external ventricular drainage for intraventricular fibrinolysis in severe ventricular haemorrhage. J Neurol Neurosurg Psychiatry 81(1):105–108. doi: 10.1136/jnnp.2008.168427 PubMedCrossRefGoogle Scholar
  62. Staykov D, Volbers B, Wagner I, Huttner HB, Doerfler A, Schwab S, Bardutzky J (2011) Prognostic significance of third ventricle blood volume in intracerebral haemorrhage with severe ventricular involvement. J Neurol Neurosurg Psychiatry 82(11):1260–1263. doi: 10.1136/jnnp.2010.234542jnnp.2010.234542 PubMedCrossRefGoogle Scholar
  63. Staykov D, Wagner I, Volbers B, Doerfler A, Schwab S, Kollmar R (2012) Mild Prolonged Hypothermia for Large Intracerebral Hemorrhage. Neurocrit Care. doi: 10.1007/s12028-012-9762-5 PubMedGoogle Scholar
  64. Steiner T, Diringer MN, Schneider D, Mayer SA, Begtrup K, Broderick J, Skolnick BE, Davis SM (2006) Dynamics of intraventricular hemorrhage in patients with spontaneous intracerebral hemorrhage: risk factors, clinical impact, and effect of hemostatic therapy with recombinant activated factor VII. Neurosurgery 59(4):767–773. doi: 10.1227/01.NEU.0000232837.34992.32 (discussion 773–764)PubMedCrossRefGoogle Scholar
  65. Suarez JI, Zaidat OO, Suri MF, Feen ES, Lynch G, Hickman J, Georgiadis A, Selman WR (2004) Length of stay and mortality in neurocritically ill patients: impact of a specialized neurocritical care team. Crit Care Med 32(11):2311–2317. doi: 00003246-200411000-00020 PubMedGoogle Scholar
  66. Tuhrim S, Horowitz DR, Sacher M, Godbold JH (1999) Volume of ventricular blood is an important determinant of outcome in supratentorial intracerebral hemorrhage. Crit Care Med 27(3):617–621PubMedCrossRefGoogle Scholar
  67. Vahedi K, Hofmeijer J, Juettler E, Vicaut E, George B, Algra A, Amelink GJ, Schmiedeck P, Schwab S, Rothwell PM, Bousser MG, van der Worp HB, Hacke W (2007) Early decompressive surgery in malignant infarction of the middle cerebral artery: a pooled analysis of three randomised controlled trials. Lancet Neurol 6(3):215–222. doi: 10.1016/S1474-4422(07)70036-4 PubMedCrossRefGoogle Scholar
  68. van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, Klijn CJ (2010) 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 9(2):167–176. doi: 10.1016/S1474-4422(09)70340-0 PubMedCrossRefGoogle Scholar
  69. Wada R, Aviv RI, Fox AJ, Sahlas DJ, Gladstone DJ, Tomlinson G, Symons SP (2007) CT angiography “spot sign” predicts hematoma expansion in acute intracerebral hemorrhage. Stroke 38(4):1257–1262. doi: 10.1161/01.STR.0000259633.59404.f3 PubMedCrossRefGoogle Scholar
  70. Wagner KR, Sharp FR, Ardizzone TD, Lu A, Clark JF (2003) Heme and iron metabolism: role in cerebral hemorrhage. J Cereb Blood Flow Metab 23(6):629–652. doi: 10.1097/01.WCB.0000073905.87928.6D PubMedCrossRefGoogle Scholar
  71. Wagner I, Hauer EM, Staykov D, Volbers B, Dorfler A, Schwab S, Bardutzky J (2011) Effects of continuous hypertonic saline infusion on perihemorrhagic edema evolution. Stroke 42(6):1540–1545. doi: 10.1161/STROKEAHA.110.609479 PubMedCrossRefGoogle Scholar
  72. Wang F, Wu Y, Bo L, Lou J, Zhu J, Chen F, Li J, Deng X (2011) The timing of tracheotomy in critically ill patients undergoing mechanical ventilation: a systematic review and meta-analysis of randomized controlled trials. Chest 140(6):1456–1465. doi: 10.1378/chest.11-2024 PubMedCrossRefGoogle Scholar
  73. Wasserman JK, Zhu X, Schlichter LC (2007) Evolution of the inflammatory response in the brain following intracerebral hemorrhage and effects of delayed minocycline treatment. Brain Res 1180:140–154. doi: 10.1016/j.brainres.2007.08.058 PubMedCrossRefGoogle Scholar
  74. Webb AJ, Ullman NL, Mann S, Muschelli J, Awad IA, Hanley DF (2012) Resolution of Intraventricular Hemorrhage Varies by Ventricular Region and Dose of Intraventricular Thrombolytic: the Clot Lysis: Evaluating Accelerated Resolution of IVH (CLEAR IVH) Program. Stroke. doi: 10.1161/STROKEAHA.112.650523 Google Scholar
  75. Xi G, Keep RF, Hoff JT (2006) Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol 5(1):53–63. doi: 10.1016/S1474-4422(05)70283-0 PubMedCrossRefGoogle Scholar
  76. Zazulia AR, Diringer MN, Derdeyn CP, Powers WJ (1999) Progression of mass effect after intracerebral hemorrhage. Stroke 30(6):1167–1173PubMedCrossRefGoogle Scholar
  77. Zhang Z, Li X, Liu Y, Shao Y, Xu S, Yang Y (2007) Application of neuroendoscopy in the treatment of intraventricular hemorrhage. Cerebrovasc Dis 24(1):91–96. doi: 10.1159/000103122 PubMedCrossRefGoogle Scholar
  78. Ziai WC, Muschelli J, Thompson CB, Keyl PM, Lane K, Shao S, Hanley DF (2012) Factors affecting clot lysis rates in patients with spontaneous intraventricular hemorrhage. Stroke 43(5):1234–1239. doi: 10.1161/STROKEAHA.111.641050 PubMedCrossRefGoogle Scholar

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© Springer-Verlag Wien 2013

Authors and Affiliations

  1. 1.Department of NeurologyUniversity of Erlangen-NurembergErlangenGermany

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