, 50:929 | Cite as

Perfusion-weighted MRI to evaluate cerebral autoregulation in aneurysmal subarachnoid haemorrhage

  • Elke Hattingen
  • Stella Blasel
  • Edgar Dettmann
  • Hartmut Vatter
  • Ulrich Pilatus
  • Volker Seifert
  • Friedhelm E. Zanella
  • Stefan Weidauer
Diagnostic Neuroradiology



The aim of this study was to evaluate autoregulatory mechanisms in different vascular territories within the first week after aneurysmal subarachnoid haemorrhage (SAH) by perfusion-weighted magnetic resonance imaging (PW-MRI). For this purpose, regional cerebral blood flow and volume (rCVF and rCBV) were measured in relation to different degrees of angiographically visible cerebral vasospasm (CVS).

Materials and methods

In 51 SAH patients, PW-MRI and digital subtraction angiography were performed about 5 days after onset of SAH. Regional CBF and rCBV were analysed in the territories of the anterior cerebral artery (ACA), the middle cerebral artery (MCA) and the basal ganglia of each hemisphere in relationship to the degree of CVS in the particular territory. Correlations between rCBF, rCBV and CVS were analysed.


CVS was found in 22 out of 51 patients in at least one territory. In all territories, rCBV decreased with increasing degree of CVS, correlated with a decrease of rCBF. In the ACA territories, SAH patients with severe CVS had significantly lower rCBF compared to healthy subjects and to SAH patients without CVS. In the basal ganglia, rCBF and rCBV of the control group were significantly higher compared to the patients without and with moderate vasospasms.


PW-MRI showed simultaneous decrease of rCBF and rCBV in patients with SAH. The fact that rCBV did not increase in territories with CVS to maintain rCBF reveals dysfunctional vascular autoregulation. Vasospasms in the microvasculature are most evident in the basal ganglia, showing decreased rCBV and rCBF even in SAH patients without CVS.


Subarachnoid haemorrhage Cerebral blood flow Cerebral blood volume Magnetic resonance imaging Cerebral vasospasm 



We would like to thank Hanns Ackermann for his assistance in statistics.

Conflict of interest statement

We declare that we have no conflict of interest.


  1. 1.
    Ohkuma H, Manabe H, Tanaka M, Suzuki S (2000) Impact of cerebral microcirculatory changes on cerebral blood flow during cerebral vasospasm after aneurysmal subarachnoid hemorrhage. Stroke 31:1621–1627PubMedGoogle Scholar
  2. 2.
    Géraud G, Tremoulet M, Guell A, Bes A (1984) The prognostic value of noninvasive CBF measurement in subarachnoid hemorrhage. Stroke 5:301–305Google Scholar
  3. 3.
    Powsner RA, O'Tuama LA, Jabre A, Melhem ER (1998) SPECT imaging in cerebral vasospasm following subarachnoid hemorrhage. J Nucl Med 39:765–769PubMedGoogle Scholar
  4. 4.
    Jakobsen M, Enevoldsen E, Bjerre P (1990) Cerebral blood flow and metabolism following subarachnoid haemorrhage: cerebral oxygen uptake and global blood flow during the acute period in patients with SAH. Acta Neurol Scand 82:174–182PubMedGoogle Scholar
  5. 5.
    Kawamura S, Sayama I, Yasui N, Uemura K (1992) Sequential changes in cerebral blood flow and metabolism in patients with subarachnoid haemorrhage. Acta Neurochir 114:12–15CrossRefGoogle Scholar
  6. 6.
    Ishii R (1979) Regional cerebral blood flow in patients with ruptured intracranial aneurysms. J Neurosurg 50:587–594PubMedGoogle Scholar
  7. 7.
    Voldby B, Enevoldsen EM, Jensen FT (1985) Cerebrovascular reactivity in patients with ruptured intracranial aneurysms. J Neurosurg 62:59–67PubMedCrossRefGoogle Scholar
  8. 8.
    Hassler W, Chioffi F (1989) CO2 reactivity of cerebral vasospasm after aneurysmal subarachnoid haemorrhage. Acta Neurochir 98:167–175CrossRefGoogle Scholar
  9. 9.
    Shinoda J, Kimura T, Funakoshi T, Araki Y, Imao Y (1991) Acetazolamide reactivity on cerebral blood flow in patients with subarachnoid haemorrhage. Acta Neurochir 109:102–108CrossRefGoogle Scholar
  10. 10.
    Lam JM, Smielewski P, Czosnyka M Pickard JD, Kirkpatrick PJ (2000) Predicting delayed ischemic deficits after aneurysmal subarachnoid hemorrhage using a transient hyperemic response test of cerebral autoregulation. Neurosurgery 47:819–825PubMedCrossRefGoogle Scholar
  11. 11.
    Rätsep T, Asser T (2001) Cerebral hemodynamic impairment after aneurysmal subarachnoid hemorrhage as evaluated using transcranial Doppler ultrasonography: relationship to delayed cerebral ischemia and clinical outcome. J Neurosurg 95:393–401PubMedGoogle Scholar
  12. 12.
    Grubb RL Jr, Raichle ME, Eichling JO, Gado MH (1977) Effects of subarachnoid hemorrhage on cerebral blood volume, blood flow, and oxygen utilization in humans. J Neurosurg 46:446–453PubMedGoogle Scholar
  13. 13.
    Martin WR, Baker RP, Grubb RL, Raichle ME (1984) Cerebral blood volume, blood flow, and oxygen metabolism in cerebral ischaemia and subarachnoid haemorrhage: an in-vivo study using positron emission tomography. Acta Neurochir 70:3–9CrossRefGoogle Scholar
  14. 14.
    Hino A, Mizukawa N, Tenjin H, Imahori Y, Taketomo S, Yano I, Nakahashi H, Hirakawa K (1989) Postoperative hemodynamic and metabolic changes in patients with subarachnoid hemorrhage. Stroke 20:1504–1510PubMedGoogle Scholar
  15. 15.
    Carpenter DA, Grubb RL Jr, Tempel LW, Powers WJ (1991) Cerebral oxygen metabolism after aneurysmal subarachnoid hemorrhage. J Cereb Blood Flow Metab 11:837–844PubMedGoogle Scholar
  16. 16.
    Yundt KD, Grubb RL Jr, Diringer MN, Powers WJ (1998) Autoregulatory vasodilation of parenchymal vessels is impaired during cerebral vasospasm. J Cereb Blood Flow Metab 18:419–424PubMedCrossRefGoogle Scholar
  17. 17.
    Weidauer S, Lanfermann H, Raabe A, Zanella F, Seifert V, Beck J (2007) Impairment of cerebral perfusion and infarct patterns attributable to vasospasm after aneurysmal subarachnoid hemorrhage: a prospective MRI and DSA study. Stroke 38:1831–1836PubMedCrossRefGoogle Scholar
  18. 18.
    Origitano TC, Wascher TM, Reichman OH, Anderson DE (1990) Sustained increased cerebral blood flow with prophylactic hypertensive hypervolemic hemodilution (“triple-H” therapy) after subarachnoid hemorrhage. Neurosurgery 27:729–739PubMedCrossRefGoogle Scholar
  19. 19.
    Wittsack HJ, Ritzl A, Mödder U (2002) User friendly analysis of MR investigations of the cerebral perfusion: Windows(R)-based image processing. Rofo 174:742–746 [Article in German]PubMedGoogle Scholar
  20. 20.
    Østergaard L, Weisskoff R, Chesler D, Gyldensted C, Rosen B (1996) High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. I. Mathematical approach and statistical analysis. Magn Reson Med 36:715–725PubMedCrossRefGoogle Scholar
  21. 21.
    Rordorf G, Koroshetz WJ, Copen WA, Gonzalez G, Yamada K, Schaefer PW, Schwamm LH, Ogilvy CS, Sorensen AG (1999) Diffusion- and perfusion weighted imaging in vasospasm after subarachnoid hemorrhage. Stroke 30:599–605PubMedGoogle Scholar
  22. 22.
    Shimoda M, Takeuchi M, Tominaga J, Oda S, Kumasaka A, Tsugane R (2001) Asymptomatic versus symptomatic infarcts from vasospasm in patients with subarachnoid hemorrhage: serial magnetic resonance imaging. Neurosurgery 49:1341–1350PubMedCrossRefGoogle Scholar
  23. 23.
    Leclerc X, Fichten A, Gauvrit JY, Riegel B, Steinling M, Lejeune JP, Pruvo JP (2002) Symptomatic vasospasm after subarachnoid hemorrhage: assessment of brain damage by diffusion and perfusion-weighted MRI and single-photon emission computed tomography. Neuroradiology 44:610–616PubMedCrossRefGoogle Scholar
  24. 24.
    Cronqvist M, Wirestam R, Ramgren B, Brandt L, Nilsson O, Säveland H, Holtås S, Larsson EM (2005) Diffusion and perfusion MRI in patients with ruptured and unruptured intracranial aneurysms treated by endovascular coiling: complications, procedural results, MR findings and clinical outcome. Neuroradiology 47:855–873PubMedCrossRefGoogle Scholar
  25. 25.
    Hertel F, Walter C, Bettag M, Mörsdorf M (2005) Perfusion-weighted magnetic resonance imaging in patients with vasospasm: a useful new tool in the management of patients with subarachnoid hemorrhage. Neurosurgery 56:28–35PubMedGoogle Scholar
  26. 26.
    Soustiel JF, Levy E, Bibi R, Lukaschuk S, Manor D (2001) Hemodynamic consequences of cerebral vasospasm on perforating arteries: a phantom model study. Stroke 32:629–635PubMedGoogle Scholar
  27. 27.
    Weidauer S, Vatter H, Beck J, Raabe A, Lanfermann H, Seifert V, Zanella F (2008) Focal laminar cortical infarcts following aneurysmal subarachnoid haemorrhage. Neuroradiology 50:1–8PubMedCrossRefGoogle Scholar
  28. 28.
    Ohkuma H, Itoh K, Shibata S, Suzuki S (1997) Morphological changes of intraparenchymal arterioles after experimental subarachnoid hemorrhage in dogs. Neurosurgery 41:230–235PubMedCrossRefGoogle Scholar
  29. 29.
    Ohkuma H, Suzuki S (1999) Histological dissociation between intra- and extraparenchymal portion of perforating small arteries after experimental subarachnoid hemorrhage in dogs. Acta Neuropathol 98:374–382PubMedCrossRefGoogle Scholar
  30. 30.
    Uhl E, Lehmberg J, Steiger HJ, Messmer K (2003) Intraoperative detection of early microvasospasm in patients with subarachnoid hemorrhage by using orthogonal polarization spectral imaging. Neurosurgery 52:1307–1315PubMedCrossRefGoogle Scholar
  31. 31.
    Dreier JP, Woitzik J, Fabricius M, Bhatia R, Major S, Drenckhahn C, Lehmann TN, Sarrafzadeh A, Willumsen L, Hartings JA, Sakowitz OW, Seemann JH, Thieme A, Lauritzen M, Strong AJ (2006) Delayed ischemic neurological deficits after subarachnoid hemorrhage are associated with clusters of spreading depolarizations. Brain 129:3224–3237PubMedCrossRefGoogle Scholar
  32. 32.
    Dreier JP, Sakowitz OW, Harder A, Zimmer C, Dirnagl U, Valdueza JM, Unterberg AW (2002) Focal laminar cortical MR signal abnormalities after subarachnoid hemorrhage. Ann Neurol 52:825–829PubMedCrossRefGoogle Scholar
  33. 33.
    Østergaard L (2005) Principles of cerebral perfusion imaging by bolus tracking. J Magn Reson Imaging 22:710–717PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Elke Hattingen
    • 1
  • Stella Blasel
    • 1
  • Edgar Dettmann
    • 1
  • Hartmut Vatter
    • 2
  • Ulrich Pilatus
    • 1
  • Volker Seifert
    • 2
  • Friedhelm E. Zanella
    • 1
  • Stefan Weidauer
    • 1
    • 3
  1. 1.Institute of NeuroradiologyUniversity of FrankfurtFrankfurtGermany
  2. 2.Department of NeurosurgeryUniversity of FrankfurtFrankfurtGermany
  3. 3.Department of NeurologySankt Katharinen Hospital FrankfurtFrankfurtGermany

Personalised recommendations