, 50:729 | Cite as

CT perfusion mapping of hemodynamic disturbances associated to acute spontaneous intracerebral hemorrhage

  • Enrico FainardiEmail author
  • Massimo Borrelli
  • Andrea Saletti
  • Roberta Schivalocchi
  • Cristiano Azzini
  • Michele Cavallo
  • Stefano Ceruti
  • Riccardo Tamarozzi
  • Arturo Chieregato
Functional Neuroradiology



We sought to quantify perfusion changes associated to acute spontaneous intracerebral hemorrhage (SICH) by means of computed tomography perfusion (CTP) imaging.

Materials and methods

We studied 89 patients with supratentorial SICH at admission CT by using CTP scanning obtained within 24 h after symptom onset. Regional cerebral blood flow (rCBF), cerebral blood volume (rCBV) and mean transit time (rMTT) levels were measured in four different regions of interest manually outlined on CT scan: (1) hemorrhagic core; (2) perihematomal low-density area; (3) 1 cm rim of normal-appearing brain tissue surrounding the perilesional area; and (4) a mirrored area, including the clot and the perihematomal region, located in the non-lesioned contralateral hemisphere.


rCBF, rCBV, and rMTT mean levels showed a centrifugal distribution with a gradual increase from the core to the periphery (p < 0.0001). Perfusion absolute values were indicative of ischemia in hemorrhagic core, oligemia in perihematomal area, and hyperemia in normal-appearing and contralateral areas. Perihematomal rCBF and rCBV mean levels were higher in small (≤20 ml) than in large (>20 ml) hematomas (p < 0.01 and p < 0.02, respectively).


Multi-parametric CTP mapping of acute SICH indicates that perfusion values show a progressive improvement from the core to the periphery. In the first 24 h, perihemorrhagic region was hypoperfused with CTP values which were not suggestive of ischemic penumbra destined to survive but more likely indicative of edema formation. These findings also argue for a potential influence of early amounts of bleeding on perihematomal hemodynamic abnormalities.


Acute spontaneous intracerebral hemorrhage Perfusion values CT perfusion Brain edema 



This study was supported by Azienda Ospedaliera Universitaria, Ferrara. We thank Professor Julian T. Hoff of Department of Neurosurgery, University of Michigan Health System, Ann Arbor, Michigan (USA), and Doctor Howard Yonas of Department of Neurosurgery, University of New Mexico, Albuquerque, New Mexico (USA), for comments and critical review of the manuscript.

Conflict of interest statement

We declare that we have no conflict of interest.


  1. 1.
    Mayer SA, Rincon F (2005) Treatment of intracerebral haemorrhage. Lancet Neurol 4:662–672PubMedCrossRefGoogle Scholar
  2. 2.
    Xi G, Keep RF, Hoff JT (2006) Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol 5:53–63PubMedCrossRefGoogle Scholar
  3. 3.
    Heiss W-D (2000) Ischemic penumbra: evidence from functional imaging in man. J Cereb Blood Flow Metab 20:1276–1293PubMedCrossRefGoogle Scholar
  4. 4.
    Latchaw RE, Yonas H, Hunter GJ, Yuh WTC, Ueda T, Sorensen AG, Sunshine JL, Biller J, Wechsler L, Higashida R, Hademenos G (2003) Guidelines and recommendations for perfusion imaging in cerebral ischemia. A scientific statement for healthcare professionals by the Writing Group on Perfusion Imaging, from the Council on Cardiovascular Radiology of the American Heart Association. Stroke 34:1064–1104CrossRefGoogle Scholar
  5. 5.
    Miyazawa N, Mitsuka S, Asahara T, Uchida M, Fukamachi A, Fukasawa I, Sasaki H, Nukui H (1998) Clinical features of relative focal hyperperfusion in patients with intracerebral hemorrhage detected by contrast-enhanced Xenon CT. Am J Neuroradiol 19:1741–1746PubMedGoogle Scholar
  6. 6.
    Hirano T, Read SJ, Abbott DF, Sachinidis JI, Tochon-Danguy HJ, Egan GF, Bladin CF, Scott AM, McKay WJ, Donnan GA (1999) No evidence of hypoxic tissue on 18F-fluoromisonidazole PET after intracerebral hemorrhage. Neurology 53:279–2182Google Scholar
  7. 7.
    Zazulia AR, Diringer MN, Videen TO, Adams RE, Yundt K, Aiyagari V, Grubb RL, Powers WJ (2001) Hypoperfusion without ischemia surrounding acute intracerebral hemorrhage. J Cereb Blood Flow Metab 21:804–810PubMedCrossRefGoogle Scholar
  8. 8.
    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
  9. 9.
    Powers WJ, Zazulia AR, Videen TO, Adams RE, Yundt K, Aiyagari V, Grubb RL, Diringer MN (2001) Autoregulation of cerebral blood flow surrounding acute (6 to 22 hours) intracerebral hemorrhage. Neurology 57:18–24PubMedCrossRefGoogle Scholar
  10. 10.
    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 34:1674–1680PubMedCrossRefGoogle Scholar
  11. 11.
    Butcher KS, Baird T, MacGregor L, Desmond P, Tress B, Davis S (2004) Perihematomal edema in primary intracerebral hemorrhage is plasma derived. Stroke 35:1879–1885PubMedCrossRefGoogle Scholar
  12. 12.
    Pascual AM, Lopez-Mut JV, Benlloch J, Chamarro R, Soler J, Lainez MJ (2007) Perfusion-Weighted magnetic resonance imaging in acute intracerebral hemorrhage at baseline and during the 1st and the 2nd week: a longitudinal study. Cerebrovasc Dis 23:6–13PubMedCrossRefGoogle Scholar
  13. 13.
    Tayal AH, Gupta R, Yonas H, Jovin T, Uchino K, Hammer M, Wechsler L, Gebel JM (2007) Quantitative perihematomal blood flow in spontaneous intracerebral hemorrhage predicts in-hospital functional outcome. Stroke 38:319–324PubMedCrossRefGoogle Scholar
  14. 14.
    Mayer SA, Lignelli A, Fink ME, Kessler DB, Thomas CE, Swarup R, Van Heertum RL (1998) Perilesional blood flow and edema formation in acute intracerebral hemorrhage. A SPECT study. Stroke 29:1791–1798PubMedGoogle Scholar
  15. 15.
    Siddique MS, Fernandes HM, Wooldridge TD, Fenwick JD, Slomka P, Mendelow AD (2002) Reversible ischemia around intracerebral hemorrhage: a single-proton emission computerized tomography study. J Neurosurg 96:736–741PubMedCrossRefGoogle Scholar
  16. 16.
    Zhao X, Wang Y, Wang C, Li S, Wang Y, Yang Z (2006) Quantitative evaluation for secondary injury to perihematoma of hypertensive cerebral hemorrhage by functional MR and correlation analysis with ischemic factor. Neurol Res 28:66–70PubMedCrossRefGoogle Scholar
  17. 17.
    Wintermark M, Reichhart M, Thiran J-P, Maeder P, Chalaron M, Schnyder P, Bogousslavsky J, Meuli R (2002) Prognostic accuracy of cerebral blood flow measurement by perfusion computed tomography, at the time of emergency room admission, in acute stroke patients. Ann Neurol 51:417–432PubMedCrossRefGoogle Scholar
  18. 18.
    Eastwood JD, Lev MH, Azhari T, Lee T-Y, Barboriak DP, Delong DM, Fitzek C, Herzau M, Wintermark M, Meuli R, Brazier D, Provenzale JM (2002) CT perfusion with deconvolution analysis: pilot study in patients with acute middle cerebral artery stroke. Radiology 222:227–236PubMedCrossRefGoogle Scholar
  19. 19.
    Parsons MW, Pepper EM, Chan V, Siddique S, Rajaratnam S, Bateman GA, Levi CR (2005) Perfusion computed tomography: prediction of final infarct extent and stroke outcome. Ann Neurol 58:672–679PubMedCrossRefGoogle Scholar
  20. 20.
    Schaefer PW, Roccatagliata L, Ledezma C, Hoh B, Schwamm LH, Koroshetz W, Gonzales RG, Lev MH (2006) First-pass quantitative CT perfusion identifies threshold for salvageable penumbra in acute stroke patients treated with intra-arterial therapy. AJNR Am J Neuroradiol 27:20–25PubMedGoogle Scholar
  21. 21.
    Rosand J, Eskey C, Chang Y, Gonzalez RG, Greenberg SM, Koroshetz WJ (2002) Dynamic single-section CT demonstrates reduced cerebral blood flow in acute intracerebral hemorrhage. Cerebrovasc Dis 14:214–220PubMedCrossRefGoogle Scholar
  22. 22.
    Herweh C, Jüttler E, Schellinger PD, Klotz E, Jenetzky E, Orakcioglu B, Sartor K, Schramm P (2007) Evidence against a perihemorrhagic penumbra provided by perfusion computed tomography. Stroke 38:2941–2947PubMedCrossRefGoogle Scholar
  23. 23.
    Fainardi E, Borrelli M, Saletti A, Schivalocchi R, Russo M, Azzini C, Cavallo M, Ceruti S, Chieregato A, Tamarozzi R (2005) Assessment of acute spontaneous intracerebral hematoma by CT perfusion imaging. J Neuroradiol 32:333–336PubMedCrossRefGoogle Scholar
  24. 24.
    Brott T, Adams HP, Olinger CP Marler JR, Barsan WG, Biller J, Spilker J, Holleran R, Eberle R, Hertzberg V, Rorick M, Moomaw CJ, Walker M (1989) Measurements of acute cerebral infarction: a clinical examination scale. Stroke 20:864–870PubMedGoogle Scholar
  25. 25.
    Kothari RU, Brott T, Broderick JP, Barsan WG, Sauerbeck LR, Zuccarello M, Khoury J (1996) The ABCs of measuring intracerebral hemorrhage volume. Stroke 27:1034–1035Google Scholar
  26. 26.
    Furlan M, Marchal G, Viader F, Derlon J-M, Baron J-C (1996) Spontaneous neurological recovery after stroke and fate of ischemic penumbra. Ann Neurol 40:216–226PubMedCrossRefGoogle Scholar
  27. 27.
    Calamante F, Gadian DG, Connelly A (2000) Delay and dispersion effects in dynamic susceptibility contrast MRI: simulations using singular value decomposition. Magn Reson Med 44:466–473PubMedCrossRefGoogle Scholar
  28. 28.
    Leira R, Dávalos A, Silva Y, Gil-Peralta A, Tejada J, Garcia M, Castillo J, for the Stroke Project, Cerebrovascular Diseases Group of the Spanish Neurological Society (2004) Early neurologic deterioration in intracerebral hemorrhage. Predictors and associated factors. Neurology 63:461–467PubMedGoogle Scholar
  29. 29.
    Chieregato A, Fainardi E, Servadei F Tanfani A, Pugliese G, Pascarella R, Targa L (2004) Centrifugal distribution of regional cerebral blood flow and its time course in traumatic intracerebral hematomas. J Neurotrauma 21:655–666PubMedCrossRefGoogle Scholar
  30. 30.
    Muizelaar JP, Fatouros PP, Schröder ML (1997) A new method for quantitative regional cerebral blood volume measurements using computed tomography. Stroke 28:1998–2005PubMedGoogle Scholar
  31. 31.
    Kealey SM, Loving VA, Delong DM, Eastwood JD (2004) User defined vascular input function curves: influence on mean perfusion parameter values and signal-to-noise ratio. Radiology 231:587–593PubMedCrossRefGoogle Scholar
  32. 32.
    Sanelli PC, Lev MH, Eastwood JD, Gonzalez G, Lee TY (2004) The effect of varying user-selected input parameters on quantitative values in CT perfusion maps. Acad Radiol 11:1085–1092PubMedCrossRefGoogle Scholar
  33. 33.
    Kudo K, Terae S, Katoh C, Oka M, Shiga T, Tamaki N, Myasaka K (2003) Quantitative cerebral blood flow measurement with dynamic perfusion CT using the vascular pixel elimination method: comparison with H215O positron emission tomography. Am J Neuroradiol 24:419–426PubMedGoogle Scholar
  34. 34.
    Bandera E, Botteri M, Minelli C, Sutton A, Abrams KR, Latronico N (2006) Cerebral blood flow threshold of ischemic penumbra and infarct core in acute ischemic stroke. A systematic review. Stroke 37:1334–1339PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Enrico Fainardi
    • 1
    Email author
  • Massimo Borrelli
    • 1
  • Andrea Saletti
    • 1
  • Roberta Schivalocchi
    • 2
  • Cristiano Azzini
    • 3
  • Michele Cavallo
    • 2
  • Stefano Ceruti
    • 1
  • Riccardo Tamarozzi
    • 1
  • Arturo Chieregato
    • 4
  1. 1.Neuroradiology Unit, Department of NeuroscienceAzienda Ospedaliera UniversitariaFerraraItaly
  2. 2.Neurosurgery Unit, Department of NeuroscienceAzienda Ospedaliera UniversitariaFerraraItaly
  3. 3.Neurology Unit, Department of NeuroscienceAzienda Ospedaliera UniversitariaFerraraItaly
  4. 4.Neurocritical Care UnitOspedale M. BufaliniCesenaItaly

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