Abstract
The initial and exclusive use of MRI in patients with a stroke syndrome is feasible, probably cost-effective, and even time saving when considering its potential wealth of information. MRI may be the diagnostic tool of choice in patients with all stages of stroke, especially in the hyperacute assessment of ICH, and could be equivalent to CT and CTA in SAH diagnosis.
The authors’ aim is to provide a comprehensive review about the potential role of MRI in evaluating ICH and SAH. Emerging applications, such as the assessment of microbleeds as a risk factor for secondary hemorrhage after thrombolysis and perihemorrhagic ischemic changes as a potential marker for patients likely to benefit from hematoma evacuation, are reviewed.
Similar content being viewed by others
References
WHO Task Force. Stroke—1989. Recommendations on stroke prevention, diagnosis, and therapy. Report of the WHO Task Force on Stroke and Other Cerebrovascular Disorders. Stroke 1989;20:1407–1431.
Jorgensen HS, Nakayama H, Raaschou HO, Olsen TS. Intracerebral hemorrhage versus infarction: stroke severity, risk factors, and prognosis. Ann Neurol 1995;38:45–50.
Qureshi AI, Tuhrim S, Broderick JP, Batjer HH, Hondo H, Hanley DF. Spontaneous intracranial hemorrhage. N Engl J Med 2001;344:1450–1460.
Rosenow F, Hojer C, Meyer-Lohmann C, et al. Spontaneous intracerebral hemorrhage. Prognostic factors in 896 cases. Acta Neurol Scand 1997;96:174–182.
Higer HP, Pedrosa P, Schaeben W, Bielke G, Meindl S. Intracranial hemorrhage in MRT. Radiologe 1989;29:297–302.
Jansen O, Heiland S, Schellinger P. Neuroradiological diagnosis in acute ischemic stroke. Value of modern techniques. Nervenarzt 1998;69:465–471.
Hacke W, Stingele R, Steiner T, Schuchardt V, Schwab S. Critical care of acute ischemic stroke. Intens. Care Med. 1995;21:856–862.
Hayman LA, Taber KH, Ford JJ, Bryan RN. Mechanisms of MR signal alteration by acute intracerebral blood: old concepts and new theories. AJNR Am J Neuroradiol 1991;12:899–907.
Hayman LA, Pagani JJ, Kirkpatrick JB, Hinck VC. Pathophysiology of acute intracerebral and subarachnoid hemorrhage: applications to MR imaging. AJR 1989;153:135–139.
Weingarten K, Zimmerman RD, Cahill PT, Deck MD. Detection of acute intracerebral hemorrhage on MR imaging: ineffectiveness of prolonged interecho interval pulse sequences. AJNR Am J Neuroradiol 1991;12:475–479.
Bradley WG, Jr. MR appearance of hemorrhage in the brain. Radiology 1993;189:15–26.
Felber S, Auer A, Wolf C, et al. MRI characteristics of spontaneous intracerebral hemorrhage. Radiologe 1999;39:838–846.
Steinbrich W, Gross-Fengels W, Krestin GP, Heindel W, Schreier G. Intracranial hemorrhages in the magnetic resonance tomogram. Studies on sensitivity, on the development of hematomas and on the determination of the cause of the hemorrhage. Rofo Fortschr Geb Rontgenstr Neuen Bildgeb Verfahr 1990;152:534–543.
Gomori JM, Grossman RI, Yu-Ip C, Asakura T. NMR relaxation times of blood: dependence on field strength, oxidation state, and cell integrity. J Comput Assist Tomogr 1987;11:684–690.
Gomori JM, Grossman RI, Goldberg HI, Zimmerman RA, Bilaniuk LT. Intracranial hematomas: imaging by high-field MR. Radiology 1985;157:87–93.
Gomori JM, Grossman RI. Mechanisms responsible for the MR appearance and evolution of intracranial hemorrhage. Radiographics 1988;8:427–440.
Grossman RI, Gomori JM, Goldberg HI, et al. MR imaging of hemorrhagic conditions of the head and neck. Radiographics 1988;8:441–454.
Grossman RI, Kemp SS, Ip CY, et al. Importance of oxygenation in the appearance of acute subarachnoid hemorrhage on high field magnetic resonance imaging. Acta Radiol Suppl 1986;369:56–58.
Osborn AG. Intracranial hemorrhage. In: Osborn AG, ed. Diagnostic Neuroradiology. Mosby, Year Book Inc, 1994, pp. 154–198.
Brooks RA, Di Chiro G, Patronas N. MR imaging of cerebral hematomas at different field strengths: theory and applications. J. Comput. Assist. Tomogr. 1989;13:194–206.
Schellinger PD, Jansen O, Fiebach JB, Hacke W, Sartor K. A standardized MRI stroke protocol: comparison with CT in hyperacute intracerebral hemorrhage. Stroke 1999;30:765–768.
Zyed A, Hayman LA, Bryan RN. MR imaging of intracerebral blood: diversity in the temporal pattern at 0.5 and 1.0 T. AJNR Am. J. Neuroradiol. 1991;12:469–474.
Blackmore CC, Francis CW, Bryant, R. G., Brenner, B., Marder, V. J. Magnetic resonance imaging of blood and clots in vitro. Invest Radiol 1990;25:1316–1324.
Chin HY, Taber KH, Hayman LA. Temporal changes in red blood cell hydration: application to MRI of hemorrhage. Neuroradiology 1991;33:79–81.
Clark RA, Watanabe AT, Bradley WG, Jr, Roberts JD. Acute hematoma: effects of deoxygenation, hematocrit, and fibrin clot formation and retraction on T2 shortening. Radiology 1990;175:201–206.
Janick PA, Hackney DB, Grossman RI, Asakura T. MR imaging of various oxidation states of intracellular and extracellular hemoglobin. AJNR Am J Neuroradiol 1991;12:891–897.
Kirkpatrick JB, Hayman LA. Pathophysiology of intracranial hemorrhage. Neuroimag Clin N Amer 1992;2:11–23.
Sartor K. Diagnostic and Interventional Neuroradiology—A Multimodality Approach. Stuttgart, NY: Georg Thieme Verlag, 2002,76, 141, 160–169.
Fazekas, F., Kleinert, R., Roob, G., et al. Histopathologic analysis of foci of signal loss on gradient-echo T2*-weighted MR images in patients with spontaneous intracerebral hemorrhage: evidence of microangiopathy-related microbleeds. AJNR Am. J. Neuroradiol. 1999;20:637–642.
Hagen, T. Intracerebral hemorrhage in the context of amyloid angiopathy. Radiologe 1999;39:847–854.
Ruiz-Sandoval JL, Cantu C, Barinagarrementeria F. Intracerebral hemorrhage in young people: analysis of risk factors, location, causes, and prognosis. Stroke 1999;30:537–541.
Jansen O, Knauth M, Sartor K. Advances in clinical neuroradiology. Akt. Neurologie. 1999;26:1–7.
Powers WJ, Zivin J. Magnetic resonance imaging in acute stroke: not ready for prime time. Neurology 1998;50:842–843.
Powers WJ. Testing a test: a report card for DWI in acute stroke. Neurology 2000;54:1549–1551.
Mattle HP, Edelman RR, Schroth G, O’Reilly GV. Spontaneous and Traumatic Hemorrhage in Clinical and Magnetic Resonance Imaging. Vol. 1. Philadelphia: W B Saunders, 1996, pp. 652–702.
Gustafsson O, Rossitti S, Ericsson A, Raininko R. MR imaging of experimentally induced intracranial hemorrhage in rabbits during the first 6 hours. Acta Radiol 1999;40:360–368.
Haley EC, Jr., Brott TG, Sheppard GL, et al. Pilot randomized trial of tissue plasminogen activator in acute ischemic stroke. The TPA Bridging Study Group. Stroke 1993;24:1000–1004.
Kuker W, Thiex R, Rohde I, Rohde V, Thron A. Experimental acute intracerebral hemorrhage. Value of MR sequences for a safe diagnosis at 1.5 and 0.5 T. Acta. Radiol. 2000;41:544–552.
Linfante I, Llinas RH, Caplan LR, Warach S. MRI features of intracerebral hemorrhage within 2 hours from symptom onset. Stroke 1999;30:2263–2267.
Ebisu T, Tanaka C, Umeda M, et al. Hemorrhagic and nonhemorrhagic stroke: diagnosis with diffusion-weighted and T2-weighted echo-planar MR imaging. Radiology 1997;203:823–828.
Patel, M. R., Edelman, R. R., Warach, S. Detection of hyperacute primary intraparenchymal hemorrhage by magnetic resonance imaging. Stroke 1996;27:2321–2324.
Rosen BR, Belliveau JW, Chien D. Perfusion imaging by nuclear magnetic resonance. Magnet Reson Q 1989;5:263–281.
Schellinger PD, Fiebach JB, Gass A, et al. Accuracy of stroke MRI in hyperacute intracerebral hemorrhage <6 hours—a prospective standardized blinded multicenter study. International Stroke Conference, Phoenix, AZ, February 13–15, 2003.
The European Stroke Initiative. Recommendations for Stroke Management. Cerebrovasc Dis 2000;10:1–34.
Kidwell CS, SAver JL, Villablanca JP, et al. Magnetic resonance imaging detection of microbleeds before thrombolysis: an emerging application. Stroke 2002;33:95–98.
Nighoghossian N, Hermier M, Adeleine P, et al. Old microbleeds are a potential risk factor for cerebral bleeding after ischemic stroke: a gradient-echo t2*-weighted brain MRI study. Stroke 2002;33:735–742.
Diringer MN. Intracerebral hemorrhage: pathophysiology and management. Crit. Care. Med. 1993;21:1591–1603.
Fernandes HM, Gregson B, Siddique S, Mendelow AD. Surgery in intracerebral hemorrhage: the uncertainty continues. Stroke 2000;31:2511–2516.
Auer LM, Deinsberger W, Niederkorn K, et al. Endoscopic surgery versus medical treatment for spontaneous intracerebral hematoma: a randomized study. J. Neurosurg. 1989;70:530–535.
Morgenstern LB, Frankowski RF, Shedden P, Pasteur W, Grotta JC. Surgical treatment for intracerebral hemorrhage (STICH). Stroke 1998;51:1359–1363.
Bullock R, Brock Utne J, van Dellen J, Blake G. Intracerebral hemorrhage in a primate model: effect on regional cerebral blood flow. Surg. Neurol. 1988;29:101–107.
Deinsberger W, Vogel J, Fuchs C, Auer LM, Kuschinsky W, Boker DK. Fibrinolysis and aspiration of experimental intracerebral hematoma reduces the volume of ischemic brain in rats. Neurol Res 1999;21:517–523.
Mun Bryce S, Kroh FO, White J, Rosenberg GA. Brain lactate and pH dissociation in edema: 1H- and 31P-NMR in collagenase-induced hemorrhage in rats. Am. J. Physiol. 1993;265:R697–702.
Ogawa T, Hatazawa J, Inugami A, et al. Carbon-11-methionine PET evaluation of intracerebral hematoma: distinguishing neoplastic from non-neoplastic hematoma. J Nucl Med 1995;36:2175–2179.
Zazulia AR, Diringer MN, Videen TO, et al. Hypoperfusion without ischemia surrounding acute intracerebral hemorrhage. J Cereb Blood Flow Metab 2001;21:804–810.
Ropper AH, Zervas NT. Cerebral blood flow after experimental basal ganglia hemorrhage. Ann. Neurol. 1982;11:266–271.
Mendelow AD, Bullock R, Nath FP, et al. Experimental intracerebral mass: time-related effects on local cerebral blood flow. In: Miller JD, Teasdale GM, Rowan JO, et al., eds. Intracranial Pressure VI. Berlin: Springer, 1986, pp. 515–520.
Castillo J, Dávalos A, Álvarez-Sabín J, et al. Molecular signatures of brain injury after intracerebral hemorrhage. Neurology 2002;58:624–629.
Qureshi AI, Wilson DA, Hanley DF, Traystman RJ. No evidence for an ischemic penumbra in massive experimental intracerebral hemorrhage. Neurology 1999;52:266–272.
Videen TO, Dunford-Shore JE, Diringer MN, Powers WJ. Correction for partial volume effects in regional blood flow measurements adjacent to hematomas in humans with intracerebral hemorrhage: implementation and validation. J Comput Assist Tomogr 1999;23:248–256.
Carhuapoma JR, Wang PY, Beauchamp NJ, Keyl PM, Hanley DF, Barker PB. Diffusion-weighted MRI and proton MR spectroscopic imaging in the study of secondary neuronal injury after intracerebral hemorrhage. Stroke 2000;31:726–732.
Kidwell CS, Saver JL, Mattiello J, et al. Diffusion-perfusion MR evaluation of perihematomal injury in hyperacute intracerebral hemorrhage. Neurology 2001;57:1611–1617.
Schellinger PD, Fiebach JB, Hoffmann K, et al. Stroke MRI in intracerebral hemorrhage: is there a perihemorrhagic penumbra? Stroke 2003;34:1674–1679.
Neumann-Haefelin T, Wittsack HJ, Wenserski F, et al. Diffusion-and perfusion weighted MRI. The DWI/PWI mismatch region in acute stroke. Stroke 1999;30:1591–1597.
Nath FP, Kelly PT, Jenkins A, Mendelow AD, Graham DI, Teasdale GM. Effects of experimental intracerebral hemorrhage on blood flow, capillary permeability, and histochemistry. J Neurosurg 1987;66:555–562.
Sinar EJ, Mendelow AD, Graham DL, Teasdale GM. Experimental intracerebral hemorrhage: effects of a temporary mass lesion. J Neurosurg 1987;66:568–576.
Gebel JM, Jr., Jauch EC, Brott TG, et al. Natural history of perihematomal edema in patients with hyperacute spontaneous intracerebral hemorrhage. Stroke 2002;33:2631–2635.
Gebel JM, Lauch EC, Brott TG, et al. Relative edema volume is a predictor of outcome in patients with hyperacute spontaneous intracerebral hemorrhage. Stroke 2002;33:2636–2641.
Powers WJ, Zazulia AR, Videen TO, et al. Autoregulation of cerebral blood flow surrounding acute (6 to 22 hours) intracerebral hemorrhage. Neurology 2001;57:18–24.
Hirano T, Read SJ, Abbott DF, et al. No evidence of hypoxic tissue on 18F-fluoromisonidazole PET after intracerebral hemorrhage. Neurology 1999;53:2179–2182.
Chu WJ, Mason GF, Pan JW, et al. Regional cerebral blood flow and magnetic resonance spectroscopic imaging findings in diaschisis from stroke. Stroke 2002;33:1243–1248.
Lee KR, Kawai N, Kim S, Sagher O, Hoff JT. 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 1997;86:272–278.
Rosenberg GA, Navratil M. Metalloproteinase inhibition blocks edema in intracerebral hemorrhage in the rat. Neurology 1997;48:921–926.
van Gijn J, van Dongen KJ. The time course of aneurysmal haemorrhage on computed tomograms. Neuroradiology 1982;23:153–156.
Scotti G, Ethier R, Melancon D, Terbrugge K, Tchang S. Computed tomography in the evaluation of intracranial aneurysms and subarachnoid hemorrhage. Radiology 1977;123:85–90.
Chakeres DW, Bryan RN. Acute subarachnoid hemorrhage: in vitro comparison of magnetic resonance and computed tomography. AJNR Am J Neuroradiol 1986;7:223–228.
Melhem ER, Jara H, Eustace S. Fluid-attenuated inversion recovery MR imaging: identification of protein concentration thresholds for CSF hyperintensity. AJR Am J Roentgenol 1997;169:859–862.
Noguchi K, Ogawa T, Seto H, et al. Subacute and chronic subarachnoid hemorrhage: diagnosis with fluid-attenuated inversion-recovery MR imaging. Radiology 1997;203:257–262.
Jenkins A, Hadley DM, Teasdale GM, Condon B, Macpherson P, Patterson J. Magnetic resonance imaging of acute subarachnoid hemorrhage. J Neurosurg 1988;68:731–736.
Matsumura K, Matsuda M, Handa J, Todo G. Magnetic resonance imaging with aneurysmal subarachnoid hemorrhage: comparison with computed tomography scan. Surg Neurol 1990;34:71–78.
Noguchi K, Ogawa T, Inugami A, et al. Acute subarachnoid hemorrhage: MR imaging with fluid-attenuated inversion recovery pulse sequences. Radiology 1995;196:773–777.
Chrysikopoulos H, Papanikolaou N, Pappas J, et al. Acute subarachnoid haemorrhage: detection with magnetic resonance imaging. Br J Radiol 1996;69:601–609.
Noguchi K, Seto H, Kamisaki Y, Tomizawa G, Toyoshima S, Watanabe N. Comparison of fluid-attenuated inversion-recovery MR imaging with CT in a simulated model of acute subarachnoid hemorrhage. AJNR Am J Neuroradiol 2000;21:923–927.
Ogawa T, Inugami A, Shimosegawa E, et al. Subarachnoid hemorrhage: evaluation with MR imaging. Radiology 1993;186:345–351.
Satoh S, Kadoya S. Magnetic resonance imaging of subarachnoid hemorrhage. Neuroradiology 1988;30:361–366.
Atlas SW. MR imaging is highly sensitive for acute subarachnoid hemorrhage ... not! Radiology 1993;186:319–322; discussion 323.
Atlas SW, Thulborn KR. MR Detection of hyperacute parenchymal hemorrhage of the brain. AJNR Am J Neuroradiol 1998;19:1471–1477.
Wiesmann M, Mayer TE, Medele R, Bruckmann H. Diagnosis of acute subarachnoid hemorrhage at 1.5 Tesla using proton-density weighted FSE and MRI sequences. Radiologe 1999;39:860–865.
Noguchi K, Ogawa T, Inugami A, Toyoshima H, Okudera T, Uemura K. MR of acute subarachnoid hemorrhage: a preliminary report of fluid-attenuated inversion-recovery pulse sequences. AJNR Am J Neuroradiol 1994;15:1940–1943.
Busch E, Beaulieu C, de Crespigny A, Moseley ME. Diffusion MR imaging during acute subarachnoid hemorrhage in rats. Stroke 1998;29:2155–2161.
Jäger HR, Mansmann U, Hausmann O, Partzsch U, Moseley IF, Taylor WJ. MRA versus digital subtraction angiography in acute subarachnoid haemorrhage: a blinded multireader study of prospectively recruited patients. Neuroradiology 2000;42:313–326.
Fiebach JB, Schellinger PD, Geletneky K, et al. Stroke MRI in hyperacute subarachnoid hemorrhage in humans. Neuroradiology 2004; in press.
Imaizumi T, Chiba M, Honma T, Niwa J. Detection of hemosiderin deposition by T2*-weighted MRI after subarachnoid hemorrhage. Stroke 2003;34:1693–1698.
Rordorf G, Koroshetz WJ, Copen WA, et al. Diffusion-and perfusion-weighted imaging in vasospasm after subarachnoid hemorrhage. Stroke 1999;30:599–605.
Condette-Auliac S, Bracard S, Anxionnat R, et al. Vasospasm after subarachnoid hemorrhage: interest in diffusion-weighted MR imaging. Stroke 2001;32:1818–1824.
Hadeishi H, Suzuki A, Yasui N, Hatazawa J, Shimosegawa E. Diffusion-weighted magnetic resonance imaging in patients with subarachnoid hemorrhage. Neurosurgery 2002;50:741–747.
Griffiths PD, Wilkinson ID, Mitchell P, et al. Multimodality MR imaging depiction of hemodynamic changes and cerebral ischemia in subarachnoid hemorrhage. AJNR Am J Neuroradiol 2001;22:1690–1697.
Schellinger PD, Fiebach JB. Stroke MRI and Intracranial Hemorrhage. In: Fiebach JB, Schellinger PD, eds. Stroke MRI. Darmstadt: Steinkopff Verlag, 2003, pp. 35–44.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Schellinger, P.D., Fiebach, J.B. Intracranial hemorrhage. Neurocrit Care 1, 31–45 (2004). https://doi.org/10.1385/NCC:1:1:31
Issue Date:
DOI: https://doi.org/10.1385/NCC:1:1:31