Journal of Neurology

, Volume 253, Issue 8, pp 985–999 | Cite as

Update on intracerebral haemorrhage

REVIEW

Abstract

Intracerebral haemorrhage (ICH) is a common and serious disease. About 1 to 2 out of 10 patients with stroke have an ICH. The mortality of ICH is higher than that of ischaemic stroke. Only 31% are functionally independent at 3 months. Only 38% of the patients survive the 1st year. The cost of ICH is high.

Hypertension is the major risk factor, increasing the risk of ICH about 4x. Up to half of hypertensive patients who suffer a ICH are either unaware of their hypertension, non-compliant with the medication or fail to control periodically their blood pressure levels Microbleeds and white matter changes are MRI markers of the risk of ICH. ICH has 3 main pathophysiological phases: arterial rupture and haematoma formation, haematoma enlargement and peri-haematoma oedema. Up to 40% of the haematomas grow in the first hours post-rupture. ICH growth is associated with early clinical deterioration. Two randomised clinical trials (RCTs) demonstrated that treatment with rFVIIa limited haematoma growth and improved outcome, but was associated with a increase in thromboembolic complications. Ventricular drainage with thrombolytics might improve outcome for patients with intraventricular bleeding. A large RCT and meta-analysis failed to show a benefit of surgery over conservative treatment in acute ICH.

Keywords

intracerebral haemorrhage intraventricular haemorrhage amyloid angiopathy magnetic resonance imaging rFVlla 

References

  1. 1.
    Abilleira S, Montaner J, Molina CA, Monasterio J, Castillo J, Alvarez-Sabin J (2003) Matrix metalloproteinase-9 concentration after spontaneous intracerebral hemorrhage. J Neurosurg 99:65–70PubMedGoogle Scholar
  2. 2.
    Al-Shahi R, Bhattacharya JJ, Currie DG, Papanasta ssiou V, Ritchie V, Roberts RC, Sellar RJ, Warlow CP for the SIVMS Collaborators (2003) Prospective, population-based detection of intracranial vascular malformations in adults. The Scottish Intracranial Vascular Malformation Study (SIVMS). Stroke 34:1163–1169PubMedGoogle Scholar
  3. 3.
    Al-Shahi R, Warlow C (2001) A systematic review of the frequency and prognosis of arteriovenous malformations of the brain in adults. Brain 124:1900–1926PubMedGoogle Scholar
  4. 4.
    Alvarez-Sabin J, Delgado P, Abilleira S, Molina CA, Arenillas J, Ribo M, Santamarina E, Quintana M, Monasterio J, Montaner J (2004) Temporal profile of matrix metalloproteinases and their inhibitors after spontaneous intracerebral hemorrhage: relationship to clinical and radiological outcome. Stroke 35:1316–1322PubMedGoogle Scholar
  5. 5.
    Ariesen MJ, Claus SP, Rinkel GJE, Algra A (2003) Risk factors for intracerebral hemorrhage in the general population. A systematic review. Stroke 34:2060–2066PubMedGoogle Scholar
  6. 6.
    Auer LM, Deinsberger W, Niederkorn K, Gell G, Kleinert R, Schneider G, Holzer P, Bone G, Mokry M, Körner E, Kleinert G, Hanusch S (1989) Endoscopic surgery versus medical treatment for spontaneous intracerebral hematoma: a randomized study. J Neurosurg 70:530–535PubMedCrossRefGoogle Scholar
  7. 7.
    Bailey RD, Hart RG, Benavente O, Pearce LA (2001) Recurrent brain hemorrhage is more frequent than ischemic stroke after intracranial hemorrhage. Neurology 56:773–777PubMedGoogle Scholar
  8. 8.
    Bak S, Andersen M, Tsiropoulos I, Garcia Rodriguez LA, Hallas J, Christensen K, Gaist D (2003) Risk of stroke associated with nonsteroidal anti-inflammatory drugs: a nested case-control study. Stroke 4:379–386Google Scholar
  9. 9.
    Bereczki D, Liu M, do Prado GF, Fekete I (2000) Cochrane report: A systematic review of mannitol therapy for acute ischemic stroke and cerebral parenchymal hemorrhage. Stroke 31:2719–2722PubMedGoogle Scholar
  10. 10.
    Bertananffy H, Benes L, Miyazawa T, Alberti O, Siegel AM, Sure U (2002) Cerebral cavernomas in the adult. Review of the literature and analysis of 72 surgically treated patients. Neurosurg Rev 25:1–53Google Scholar
  11. 11.
    Broderick JP, Adams HP Jr, Barsan W, Feinberg W, Feldmann E, Grotta J, Kase C, Krieger D, Mayberg M, Tilley B, Zabramski JM, Zuccarello M (1999) Guidelines for the management of spontaneous intracerebral hemorrhage: A statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 30:905–915PubMedGoogle Scholar
  12. 12.
    Butcher KS, Baird T, MacGregor L, Desmond P, Tress B, Davis S (2004) Perihematomal edema in primary intracerebral hemorrhage is plasma derived. Stroke 35:1879–1885PubMedGoogle Scholar
  13. 13.
    Cantu C, Arauz A, Murillo-Bonilla LM, López M, Barinagarrementeria F (2003) Stroke associated with sympathomimetics container in over-the counter cough and cold drugs. Stroke 34:1667–1673PubMedGoogle Scholar
  14. 14.
    Castillo J Dávalos A, Álvarez-Sabin J, Pumar JM, Leira R, Silva Y, Montaner J, Kase CS (2002) Molecular signatures of brain injury after intracerebral hemorrhage. Neurology 58:624–629Google Scholar
  15. 15.
    Cheng KM, Chan CM, Fu YT, Ho LC, Cheung FC, Law CK (2001) Acute hemorrhage in late radiation necrosis of the temporal lobe: report of five cases and review of the literature. J Neurooncol 51:143–150PubMedGoogle Scholar
  16. 16.
    Correia M, Silva MR, Matos I, Magalhães R, Castro Lopes J, Ferro JM, Silva MC (2004) Prospective community-based study of stroke in Northern Portugal Incidence and case fatality in rural and urban populations. Stroke 35:2048–2053PubMedGoogle Scholar
  17. 17.
    Costa J, Ferro JM, Matias-Guiu J, Alvarez-Sabin J, Torres F, (2005) Triflusal for preventing serious vascular events in people at high risk. Cochrane Database Syst Rev (accepted for publication)Google Scholar
  18. 18.
    Denier C, Labauge P, Brunereau L, Cave-Riant F, Marchelli F, Arnoult M, Cecillon M, Maciazek J, Joutel A, Tournier-Lasserve E, Societe Francaise de Neurochirurgie, Societe de Neurochirurgie de Langue Francaise (2004) Clinical features of cerebral cavernous malformations patients with KRIT1 mutations. Ann Neurol 55:213–220PubMedGoogle Scholar
  19. 19.
    Dennis MS (2003) Outcome after brain haemorrhage. Cerebrovasc Dis 16(suppl 1):9–13PubMedGoogle Scholar
  20. 20.
    Derex L, Nighoghossian N, Hermier M, Adeleine P, Philippeau F, Honnorat J, Yilmaz H, Dardel P, Froment JC, Trouillas P (2004) Thrombolysis for ischemic stroke in patients with old microbleeds on pretreatment MRI. Cerebrovasc Dis 17:238–241PubMedGoogle Scholar
  21. 21.
    Dziedzic T, Szczudlik A, Klimkowicz A, Rog TM, Slowik A (2003) Is mannitol safe for patients with intracerebral hemorrhages? Renal considerations. Clin Neurol Neurosurg 105:87–89PubMedGoogle Scholar
  22. 22.
    Eckman MH, Rosand J, Knudsen KA, Singer DE, Greenberg SM (2003) Can patients be anticoagulated after intracerebral hemorrhage? A decision analysis. Stroke 34:1710–1716PubMedGoogle Scholar
  23. 23.
    Engelhard HH, Andrews CO, Slavin KV, Charbel FT (2003) Current management of intraventricular hemorrhage. Surg Neurol 60:15–22PubMedGoogle Scholar
  24. 24.
    Fan YH, Zhang L, Lam WW, Mok VC, Wong KS (2003) Cerebral microbleeds as a risk factor for subsequent intracerebral hemorrhages among patients with acute ischemic stroke. Stroke 34:2459–6242PubMedGoogle Scholar
  25. 25.
    Fernandes H, Gregson BA, Siddigue MS, Mendelow AD (2002) Testing the ICH score: letter to the editor. Stroke 33:1455–1456PubMedGoogle Scholar
  26. 26.
    Fernandes HM, Gregson B, Siddique S, Mendelow AD (2000) Surgery in intracerebral haemorrhage: the uncertainity continues. Stroke 31:2511–2516PubMedGoogle Scholar
  27. 27.
    Ferro JM, Mendes M, Guimarães LC, Pimentel J, Cravino J, Lima R (1993) Intracerebral hemorrhage following cardiac transplant. Cerebrovasc Dis 3:375–376Google Scholar
  28. 28.
    Ferro JM, Pinto F (2004) Poststroke epilepsy. Epidemiology, pathophysiology and management. Drugs Aging 21:639–653PubMedGoogle Scholar
  29. 29.
    Fewel ME, Thompson G, Hoff JT (2003) Spontaneous intracerebral hemorrhage: a review. Neurosurg Focus 15(article 1):1–16CrossRefGoogle Scholar
  30. 30.
    Fiebach JB, Schellinger PD, Gass A, Kucinski T, Siebler M, Villringer A, Ölkers P, Hirsch JG, Heiland S, Wilde P, Jansen O, Röther J, Hacke W, Sartor K for the Komptenznetzwerk Schlaganfall B5 (2004) Stroke magnetic resonance imaging is accurate in hyperacute intracerebral hemorrhage. A multicenter study on the validity of stroke imaging. Stroke 35:502–507PubMedGoogle Scholar
  31. 31.
    Fleetwood IG, Steinberg GK (2002) Arteriovenous malformation. Lancet 359:863–873PubMedGoogle Scholar
  32. 32.
    Freeman WD, Brott TG, Barrett KM, Castillo PR, Deen HG Jr, Czervionke LF, Meschia JF (2004) Recombinant factor VIIa for rapid reversal of warfarin anticoagulation in acute intracranial hemorrhage. Mayo Clin Proc 79:1495–500PubMedGoogle Scholar
  33. 33.
    Friedman JA, Ecker RD, Piepgras DG, Duke DA (2002) Cerebellar hemorrhage after spinal surgery: report of two cases and literature review. Neurosurgery 50:1361–1363PubMedGoogle Scholar
  34. 34.
    Garcia C, Melo TP, Rocha L, Lechner MC (1999) Cerebral hemorrhage and apoE. J Neurol 246:830–834PubMedGoogle Scholar
  35. 35.
    Garcia FP, Molina C, Sabin JA (2002) Spontaneous cerebellar haemorrhage associated with Ginko biloba ingestion. Med Clin (Barc) 119:596–597Google Scholar
  36. 36.
    Greenberg SM, Eng JA, Ning M, Smith EE, Rosand J (2004) Hemorrhage burden predicts recurrent intracerebral hemorrhage after lobar hemorrhage. Stroke 35:1415–1420PubMedGoogle Scholar
  37. 37.
    Greenberg SM, Gurol ME, Rosand J, Smith EE (2004) Amyloid angiopathy-related vascular cognitive impairment. Stroke 35(suppl I):2616–2619PubMedGoogle Scholar
  38. 38.
    Greenberg SM, Rebeck GW, Vonsattel JPG, Gomes-Isla T, Hyman BT (1995) Apolipoprotein E ε4 and cerebral hemorrhage associated with amyloid angiopathy. Ann Neurol 38:254–259PubMedGoogle Scholar
  39. 39.
    Gregson BA, Mendelow AD for the STICH Investigators (2003) International variations in surgical practice for spontaneous intracerebral hemorrhage. Stroke 34:2593–2598PubMedGoogle Scholar
  40. 40.
    Hanel RA, Xavier AR, Mohammad Y, Kirmani JF, Yahia AM, Qureshi AI (2002) Outcome following intracerebral hemorrhage and subarachnoid hemorrhage. Neurol Res 24:S58–S62PubMedGoogle Scholar
  41. 41.
    Hankey GJ (2003) Evacuation of intracerebral haematoma is likely to be of benefit- against. Stroke 34:1568–1569PubMedGoogle Scholar
  42. 42.
    Hankey GJ, Hon C (1997) Surgery for primary intracerebral haemorrhage: is it safe and effective? A systematic review of case series and randomised trials. Stroke 28:2126–2132PubMedGoogle Scholar
  43. 43.
    Hardie K, Jamrozik K, Hankey GJ, Broadhurst RJ, Anderson C (2005) Trends in five-year survival and risk of recurrent stroke after first-ever stroke in the Perth Community Stroke Study. Cerebrovasc Dis 19:179–185PubMedGoogle Scholar
  44. 44.
    Hattori N, Katayama Y, Maya Y, Gatherer A (2004) Impact of stereotactic hematoma evacuation on activities of daily living during the chronic period following spontaneous putaminal hemorrhage: a randomized study. J Neurosurg 101:417–420PubMedGoogle Scholar
  45. 45.
    Hemphill JC (2004) Hospital usage of early do-not-resuscitate orders and outcome after intracerebral hemorrhage. Stroke 35:1130–1134PubMedGoogle Scholar
  46. 46.
    Hemphill JC, Bonovich DC, Besmertis L, Manley GT, Johnston SC (2001) The ICH score: a simple, reliable grading scale for intracerebral hemorrhage. Stroke 32:891–897PubMedGoogle Scholar
  47. 47.
    Iso H, Baba S, Mannami T, Sasaki S, Okada K, Konishi M, Tsugane S; JPHC Study Group (2004) Alcohol consumption and risk of stroke among middle -age men: the JPHC Study Cohort I. Stroke 35:1124–1129PubMedGoogle Scholar
  48. 48.
    Jamora RDG, Kishi-Generao EM, Bitanga ES, Gan RN, Apaga NEP, San Jose MCZ (2003) The ICH Store: predicting mortality and functional outcome in an Asian population. Stroke 34:6–7PubMedGoogle Scholar
  49. 49.
    Jeong SW, Jung KH, Chu K, Bae HJ, Lee SH, Roh JK (2004) Clinical and radiologic differences between primary intracerebral hemorrhage with and without microbleeds on gradient-echo magnetic resonance images. Arch Neurol 2004; 61:905–909Google Scholar
  50. 50.
    Johnsen SP, Pedersen L, Friis S, Blot WJ, McLaughlin JK, Olsen JH, Sorensen HT (2003) Nonaspirin nonsteroidal anti-inflammatory drugs and risk of hospitalization for intracerebral hemorrhage: a population-based case-control study. Stroke 34:387–391PubMedGoogle Scholar
  51. 51.
    Kalita J, Misra UK, Ranjan P, Pradhan PK Das BK (2004) Effect of mannitol on regional cerebral blood flow in patients with intracerebral hemorrhage. J Neurol Sci 224:19–22PubMedGoogle Scholar
  52. 52.
    Karapanayiotides T, Meuli R, Devuyst G, Piechowski-Jozwiak B, Dewarrat A, Ruchat P, Von Segesser L, Bogousslavsky J (2005) Postcarotid endarterectomy hyperperfusion or reperfusion syndrome. Stroke 36:21–26PubMedGoogle Scholar
  53. 53.
    Keir SL, Wardlaw JM, Sandercock PAG, Chen Z (2002) Antithrombotic therapy in patients with any form of intracranial haemorrhage: a systematic review of the available controlled studies. Cerebrovasc Dis 14:197–206PubMedGoogle Scholar
  54. 54.
    Keir SL, Wardlaw JM, Warlow CP (2002) Stroke epidemiology studies have underestimated the frequency of intracerebral haemorrhage A systematic review of imaging in epidemiological studies. J Neurol 249:1226–1231PubMedGoogle Scholar
  55. 55.
    Kelly J, Hunt BJ, Lewis RR, Rudd A (2003) Anticoagulation or inferior vena cava placement for patients with primary intracerebral haemorrhage developing venous thromboembolism?. Stroke 34:2999–3005PubMedGoogle Scholar
  56. 56.
    Kidwell CS, Chalela JA, Saver JL, Starkman S, Hill MD, Demchuk AM, Butman JA, Patronas N, Alger JR, Latour LL, Luby ML, Baird AE, Leary MC, Tremwel M, Ovbiagele B, Fredieu A, Suzuki S, Villablanca JP, Davis S, Dunn B, Todd JW, Ezzeddine MA, Haymore J, Lynch JK, Davis L, Warach S (2004) Comparison of MRI and CT for detection of acute intracerebral hemorrhage. JAMA 292:1823–1830PubMedGoogle Scholar
  57. 57.
    Kidwell CS, Saver JL, Mattiello J, Warach S, Liebeskind DS, Starkman S, Vespa PM, Villablanca JP, Martin NA, Frazee J, Alger JR (2001) Diffusion-perfusion MR evaluation of perihematomal injury in hyperacute intracerebral hemorrhage. Neurology 57:1611–1617PubMedGoogle Scholar
  58. 58.
    Kobayashi E, Saeki N, Oishi H, Hiral S, Yamaura A (2000) Long-term natural history of hemorrhagic moyamoya disease in 42 patients. J Neurosurg 93:976–980PubMedGoogle Scholar
  59. 59.
    Kupersmith MJ, Kalish H, Epstein F, Yu G, Berenstein A, Woo H, Jafar J, Mandel G, De Lara F (2001) Natural history of brainstem cavernous malformations. Neurosurgery 48:47–54PubMedGoogle Scholar
  60. 60.
    Labovitz DL, Sacco RL (2001) Intracerebral hemorrhage: update. Curr Opin Neurol 14:103–108PubMedGoogle Scholar
  61. 61.
    Lee SH, Kwon SJ, Kim KS, Yoon BW, Roh JK (2004) Cerebral microbleeds in patients with hypertensive stroke Topographical distribution in the supratentorial area. J Neurol 251:1183–1189PubMedGoogle Scholar
  62. 62.
    Lee SH, Park JM, Kwon SJ, Kim H, Kim YH, Roh JK, Yoon BW (2004) Left ventricular hypertrophy is associated with cerebral microbleeds in hypertensive patients. Neurology 13; 63:16–21Google Scholar
  63. 63.
    Leira R, Davalos A, Silva Y, Gil-Peralta A Tejada J, Garcia M, Castillo J (2004) Early neurologic deterioration in intracerebral hemorrhage: predictors and associated factors. Neurology 63:461–467PubMedGoogle Scholar
  64. 64.
    Licata B, Turazzi S (2003) Bleeding cerebral neoplasms with symptomatic hematoma. J Neurosurg Sci 47:201–210PubMedGoogle Scholar
  65. 65.
    Major ongoing stroke trials (2005) Stroke 36 e7–e16Google Scholar
  66. 66.
    Marquardt G, Setzer M, Schick U, Seifert V (2002) Cerebellar hemorrhage after supratentorial craniotomy. Surg Neurol 57:241–252PubMedGoogle Scholar
  67. 67.
    Martí-Fàbregas J, Martí-Vilalta JL (2000) Hemorragia intraventricular primaria. Rev Neurol (Barc) 31:187–191Google Scholar
  68. 68.
    Matsuoka H, Hamada R (2002) Role of thrombin in CNS damage associated with intracerebral haemorrhage Opportunity for pharmachological intervention? CNS Drugs 16:509–516PubMedGoogle Scholar
  69. 69.
    Mayer SA (2002) Intracerebral hemorrhage: natural history and rationale of ultra-early hemostatic therapy. Intensive Care Med 28:S235–S240PubMedGoogle Scholar
  70. 70.
    Mayer SA (2003) Ultra-early hemostatic therapy for intracerebral hemorrhage. Stroke 34:224–229PubMedGoogle Scholar
  71. 71.
    Mayer SA, Brun NC, Begtrup K, Broderick J, Davis S, Diringer MN, Skolnick BE, Steiner T for the Recombinat Activated Factor VII Intracerebral Hemorrhage Trial Investigators (2005) N Engl J Med 352:777–785PubMedGoogle Scholar
  72. 72.
    Mayer SA, Brun NC, Broderick J, Davis S, Diringer MN, Skolnick BE, Steiner T for the Europe/Austral Asia NovoSeven ICH Trial Investigators (2005) Safety and feasibility of recombinant factor VIIa for acute intracerebral hemorrhage. Stroke 36:74–79PubMedGoogle Scholar
  73. 73.
    McCarron MO, Nicoll JAR (2004) Cerebral amyloid angiopathy and thrombolysis-related intracerebral haemorrhage. Lancet Neurol 3:484–492PubMedGoogle Scholar
  74. 74.
    Melo TP, Pinto AN, Guerreiro S, Ferro JM (1996) Early and long-term prognosis of intracerebral hematoma. Cerebrovas Dis 6(supp 2):108Google Scholar
  75. 75.
    Mendelow AD, Gregson BA, Fernandes HM, Murray GD, Teasdale GM, Hope DT, Karimi A, Shaw MDM, Barer DH for the STICH investigators (2005) Early surgery versus initial conservative treatment in patients with spontaneous supratentorial intracerebral haematomas in the International Surgical Trial in Intracerebral Haemorrhage (STICH): a randomized trial. Lancet 365:387–397PubMedGoogle Scholar
  76. 76.
    Montes JM, Wong JH, Fayad PB, Awad IA (2000) Stereotactic computed tomographic-guided aspiration and thrombolysis of intracerebral hematoma. Protocol and preliminary experience. Stroke 31:834–840PubMedGoogle Scholar
  77. 77.
    Naff NJ, Carhuapoma JR, Williams MA, Bhardwaj A, Ulatowski JA, Bederson J, Bullock R, Schmutzhard E, Pfausler B, Keyl PM, Tuhrim S, Hanley DF (2000) Treatment of intraventricular hemorrhage with urokinase. Effect on 30-day survival. Stroke 31:841–847PubMedGoogle Scholar
  78. 78.
    Naff NJ, Hanley DF, Keyl PM, Tuhrim S, Kraut M, Bederson J, Bullock R, Mayer SA, Schmutzhard E (2004) Intraventricular thrombolysis speeds blood clot resolution: results of a pilot, prospective, randomized, double-blind, controlled trial. Neurosurgery 54:577–584PubMedGoogle Scholar
  79. 79.
    Nieuwkamp DJ, de Gans K, Rinkel GJE, Algra A (2000) Treatment and outcome of severe intraventicular extension in patients with subarachnoid or intracerebral hemorrhage: a systematic review of the literature. J Neurol 247:117–121PubMedGoogle Scholar
  80. 80.
    NINDS ICH workshop participants (2005) Priorities for clinical research in intracerebral hemorrhage. Report from a National Institute of Neurological Disorders and Stroke Workshop. Stroke 36:e23–e41Google Scholar
  81. 81.
    Ohwaki K, Yano E, Nagashima H, Hirata M, Nakagomi T Tamura A (2004) Blood pressure management in acute intracerebral hemorrhage: relationship between elevated blood pressure and hematoma enlargement. Stroke 35:1364–1367PubMedGoogle Scholar
  82. 82.
    Passero S, Rocchi R, Rossi S, Ulivelli M, Vatti G (2002) Seizures after spontaneous supratentorial intracerebral hemorrhage. Epilepsia 43:1175–1180PubMedGoogle Scholar
  83. 83.
    Phan TG, Koh M, Wijdicks EFM (2000) Safety of discontinuation of anticoagulation in patients with intracranial hemorrhage at high thromboembolic risk. Arch Neurol 57:1710–1713PubMedGoogle Scholar
  84. 84.
    Pimentel J, Fernandes AC, Silva R, Ferro J, Cattoni B (2001) Brain metastases of a malignant fibrous histiocytoma presenting as an acute cerebral hemorrhage. Clin Neuropathol 20:64–69PubMedGoogle Scholar
  85. 85.
    Pouratian N, Kassell NF, Dumont AS (2003)Update on management of intracerebral hemorrhage. Neurosurg Focus 15(article 2):1–6Google Scholar
  86. 86.
    Prasad K, Shrivastava A (2000) Surgery for primary supratentorial intracerebral haemorrhage. Cochrane Database Syst Rev 2:CD000200PubMedGoogle Scholar
  87. 87.
    Quinones-Hinojosa A, Gulati M, Singh V, Lawton MT (2003) Spontaneous intracerebral hemorrhage due to coagulation disorders. Neurosurg Focus 15(article 3):1–17Google Scholar
  88. 88.
    Qureshi AI (2003) Nonsteroidal anti-Inflammatory drugs and the risk of intracerebral hemorrhage. Stroke 23:1–2Google Scholar
  89. 89.
    Qureshi AI, Tuhrim S, Broderick JP, Batjer HH, Hondo H, Hanley DF (2001) Spontaneous intracerebral hemorrhage. N Engl J Med 344:1450–1460PubMedGoogle Scholar
  90. 90.
    Remes-Troche JM, Tellez-Zenteno JF, Rojas-Serrano J, Senties-Madrid H, Vega-Boada F, Garcia-Ramos G (2003) Thalamic and mesencephalic hemorrhages after multiple honeybee stings: a life-threatening apitherapy complication. Eur Neurol 49:188–189PubMedGoogle Scholar
  91. 91.
    Renner C, Hegenbarth U, Schneider JP, Meixensberger J (2004) Fatal bihemispheric intracerebral hemorrhage after burrhold evacuation of chronic subdural hematoma in a bone marrow-transplanted patient : case report and review of the literature. Surg Neurol 62:260–263PubMedGoogle Scholar
  92. 92.
    Revesz T, Holton JL, Lashley T, Plant G, Rostagno A, Ghiso J, Frangione B (2002) Sporadic and familial cerebral amyloid angiopathies. Brain Pathol 12:343–357PubMedCrossRefGoogle Scholar
  93. 93.
    Rincon F, Mayer SA (2004) Novel therapies for intracerebral hemorrhage. Curr Opin Crit Care 10:94–100PubMedGoogle Scholar
  94. 94.
    Roch A, Michelet P, Jullien AC, Thirion X, Bregeon F, Papazian L, Roche P, Pellet W, Auffray JP (2004) Long-term outcome in intensive care unit survivors after mechanical ventilation for intracerebral hemorrhage. Crit Care Med 31:2651–2656Google Scholar
  95. 95.
    Roob G, Fazekas F (2000) Magnetic resonance imaging of cerebral microbleeds. Curr Opin Neurol 13:69–73PubMedGoogle Scholar
  96. 96.
    Rosand J, Eckman MH, Knudsen KA, Singer DE, Greenberger SM (2004) The effect of warfarin and intensity of anticoagulation on outcome of intracerebral hemorrhage. Arch Intern Med 164:880–884PubMedGoogle Scholar
  97. 97.
    Rothwell PM, Coull AJ, Giles MF, Howard SC, Silver LE, Bull LM, Gutnikov SA, Edwards P, Mant D, Sackley CM, Farmer A, Sandercock PA, Dennis MS, Warlow CP, Bamford JM, Anslow P; Oxford Vascular Study (2004) Change in stroke incidence, mortality, case-fatality, severity, and risk factors in Oxfordshire, UK from 1981 to 2004 (Oxford Vascular Study). Lancet 363:1925–1933PubMedGoogle Scholar
  98. 98.
    Russell DA, Gough MJ. (2004) Intracerebral haemorrhage following carotid endarterectomy. Eur J Endovasc Surg 28:115–123Google Scholar
  99. 99.
    Saloheimo P, Juvela S, Hillbom M (2001) Use of aspirin, epistaxis, and untreated hypertension as risk factors for primary intracerebral hemorrhage in middle-aged and elderly people. Stroke 32:399–404PubMedGoogle Scholar
  100. 100.
    Schellinger PD, Fiebach JB, Hoffmann K, Becker K, Orakcioglu B, Kollmar R, Jüttler E, Schramm P, Schwab S, Sartor K, Hacke W (2003) Stroke MRI in intracerebral hemorrhage. Is there a perihemorrhagic penumbra? Stroke 34:1674–1680PubMedGoogle Scholar
  101. 101.
    Silva Y, Leiria R, Tejada J, Lainez JM, Castillo J, Davalos A; Stroke Project Cerebrovascular Diseases Group of the Spanish Neurological Society (2005) Molecular signatures of vascular injury are associated with early growth of intracerebral hemorrhage. Stroke 36:86–91PubMedGoogle Scholar
  102. 102.
    Smith EE, Gurol ME, Eng JA, Engel CR, Nguyen TN, Rosand J, Greenberg SM (2004) White matter lesions, cognition, and recurrent hemorrhage in lobar intracerebral hemorrhage. Neurology 2004 63:1606–1612Google Scholar
  103. 103.
    Söderman M, Andersson T, Karlsson B, Wallace MC, Edner G (2003) Management of patients with brain arteriovenous malformations. Eur J Radiol 46:195–205PubMedGoogle Scholar
  104. 104.
    Song YM, Sung J, Lawlor DA, Smith GD, Shin Y, Ebrahim S (2004) Blood pressure, haemorrhagic stroke, and ischaemic stroke: the Korean national prospective occupational cohort study. BMJ 328:324–325PubMedGoogle Scholar
  105. 105.
    Song YM, Sung J, Smith GD, Ebrahim S (2004) Body mass index and ischemic and hemorrhagic stroke: a prospective study in Korean men. Stroke 35:831–836PubMedGoogle Scholar
  106. 106.
    Teernstra OP, Evers SM, Lodder J, Leffers P, Franke CL, Blaauw G; Multicenter randomized controlled trial (SICHPA) (2003) Stereotactic treatment of intracerebral hematoma by means of a plasminogen activator: a multicenter randomized controlled trial (SICHPA). Stroke 34:968–974PubMedGoogle Scholar
  107. 107.
    Thrift AG, McNeil JJ, Forbes A, for Melbourne Risk Factor Study Group (1998) Three important subgroups of hypertensive persons at greater risk of intracerebral haemorrhage. Hypertension 31:1223–1229PubMedGoogle Scholar
  108. 108.
    Vega-Basulto SD, Mosqueda-Betancourt G, Gutiérrez-Muñoz FG, Vega-Trenado SA, Rivero-García C (2004) Hematoma intracerebral postoperatorio. Una complicación poco frecuente del hematoma subdural crónico. Rev Neurol (Barc) 38:497–499Google Scholar
  109. 109.
    Vespa PM, O’Phelan K, Shah M, Mirabelli J, Starkman S, Kidwell C, Saver J, Nuwer MR, Frazee JG, McArthur DA, Martin NA (2003). Acute seizures after intracerebral hemorrhage: a factor in progressive midline shift and outcome. Neurology 60:1441–1446PubMedGoogle Scholar
  110. 110.
    Weimar C, Weber C, Wagner M, Busse O, Haberl RL, Lauterbach KW, Diener HC on behalf of the German Stroke Data Bank Collaborators (2003) Management patterns and health care use after intracerebral hemorrhage. Cerebrovasc Dis 15:29–36PubMedGoogle Scholar
  111. 111.
    Willmot M, Leonardi-Bee J, Bath PMW (2004) High blood pressure in acute stroke and subsequent outcome. A systematic review. Hypertension 43:18–24Google Scholar
  112. 112.
    Wong KS, Chan YL, Liu JY, Gao S, Lam WW (2003) Asymptomatic microbleeds as a risk factor for aspirin-associated intracerebral hemorrhages. Neurology 60:511–513PubMedGoogle Scholar
  113. 113.
    Woo D, Sauerbeck LR, Kissela BM, Khoury JC, Szaflarski JP, Gebel J, Shukla R, Pancioli AM, Jauch EC, Menon AG, Deka R, Carrozzella JA, Moomaw CJ, Fontaine RN, Broderick JP (2002) Genetic and environmental risk factors for intracerebral hemorrhage Preliminary results of a population-based study. Stroke 33:1190–1196PubMedGoogle Scholar
  114. 114.
    Woo D, Haverbusch M, Sekar P, Kissela B, Khoury J, Schneider A, Kleindorfer D, Szaflarski J, Pancioli A, Jauch E, Moomaw C, Sauerbeck L, Gebel J, Broderick J (2004) Effect of untreated hypertension on hemorrhagic stroke. Stroke 35:1703–1708PubMedGoogle Scholar
  115. 115.
    Woo D, Kissela BM, Khoury JC, Sauerbeck LR, Haverbusch MA, Szaflarski JP, Gebel JM, Pancioli AM, Jauch EC, Schneider A, Kleindorfer D, Broderick JP (2004) Hypercholesterolemia, HMG-CoA reductase inhibitors, and risk of intracerebral hemorrhage: a case-control study. Stroke 35:1360–1364PubMedGoogle Scholar
  116. 116.
    Yang QD, Niu Q, Zhou YH, Xu HW, Gu WP, Tian FF, Xie YQ, Zhang L, Xia J (2004) Incidence of cerebral hemorrhage in the Ghangsha community. A prospective study from 1986 to 2000. Cerebrovasc Dis 17:303–313PubMedGoogle Scholar
  117. 117.
    Yasaka M, Minematsu K, Naritomi H, Sakata T, Yamaguchi T (2003) Predisposing factors for enlargement of intracerebral hemorrhage in patients treated with warfarin. Thromb Haemost 89:278–839PubMedGoogle Scholar
  118. 118.
    Zazulia AR, Diringer MN, Videen TO, Adams RE, Yundt K, Aiyagari V, Grubb RL Jr, Powers WJ (2001) Hypoperfusion without ischemia surrounding acute intracerebral hemorrhage. J Cereb Blood Flow Metab 21:804—810PubMedGoogle Scholar

Copyright information

© Steinkopff Verlag Darmstadt 2006

Authors and Affiliations

  1. 1.Centro de Estudos Egas MonizHospital de Santa MariaLisboaPortugal

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