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

  • Diagnostic Neuroradiology
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Abstract

Introduction

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.

Results

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.

Conclusion

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.

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References

  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 31:1621–1627

    PubMed  CAS  Google Scholar 

  2. Géraud G, Tremoulet M, Guell A, Bes A (1984) The prognostic value of noninvasive CBF measurement in subarachnoid hemorrhage. Stroke 5:301–305

    Google Scholar 

  3. Powsner RA, O'Tuama LA, Jabre A, Melhem ER (1998) SPECT imaging in cerebral vasospasm following subarachnoid hemorrhage. J Nucl Med 39:765–769

    PubMed  CAS  Google Scholar 

  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 82:174–182

    PubMed  CAS  Google Scholar 

  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 114:12–15

    Article  CAS  Google Scholar 

  6. Ishii R (1979) Regional cerebral blood flow in patients with ruptured intracranial aneurysms. J Neurosurg 50:587–594

    PubMed  CAS  Google Scholar 

  7. Voldby B, Enevoldsen EM, Jensen FT (1985) Cerebrovascular reactivity in patients with ruptured intracranial aneurysms. J Neurosurg 62:59–67

    Article  PubMed  CAS  Google Scholar 

  8. Hassler W, Chioffi F (1989) CO2 reactivity of cerebral vasospasm after aneurysmal subarachnoid haemorrhage. Acta Neurochir 98:167–175

    Article  CAS  Google Scholar 

  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 109:102–108

    Article  CAS  Google Scholar 

  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 47:819–825

    Article  PubMed  CAS  Google Scholar 

  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 95:393–401

    PubMed  Google Scholar 

  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 46:446–453

    PubMed  Google Scholar 

  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 70:3–9

    Article  CAS  Google Scholar 

  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 20:1504–1510

    PubMed  CAS  Google Scholar 

  15. Carpenter DA, Grubb RL Jr, Tempel LW, Powers WJ (1991) Cerebral oxygen metabolism after aneurysmal subarachnoid hemorrhage. J Cereb Blood Flow Metab 11:837–844

    PubMed  CAS  Google Scholar 

  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 18:419–424

    Article  PubMed  CAS  Google Scholar 

  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 38:1831–1836

    Article  PubMed  Google Scholar 

  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 27:729–739

    Article  PubMed  CAS  Google Scholar 

  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]

    PubMed  CAS  Google Scholar 

  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 36:715–725

    Article  PubMed  Google Scholar 

  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 30:599–605

    PubMed  CAS  Google Scholar 

  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 49:1341–1350

    Article  PubMed  CAS  Google Scholar 

  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 44:610–616

    Article  PubMed  CAS  Google Scholar 

  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 47:855–873

    Article  PubMed  CAS  Google Scholar 

  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 56:28–35

    PubMed  Google Scholar 

  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 32:629–635

    PubMed  CAS  Google Scholar 

  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 50:1–8

    Article  PubMed  Google Scholar 

  28. Ohkuma H, Itoh K, Shibata S, Suzuki S (1997) Morphological changes of intraparenchymal arterioles after experimental subarachnoid hemorrhage in dogs. Neurosurgery 41:230–235

    Article  PubMed  CAS  Google Scholar 

  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 98:374–382

    Article  PubMed  CAS  Google Scholar 

  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 52:1307–1315

    Article  PubMed  Google Scholar 

  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 129:3224–3237

    Article  PubMed  Google Scholar 

  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 52:825–829

    Article  PubMed  Google Scholar 

  33. Østergaard L (2005) Principles of cerebral perfusion imaging by bolus tracking. J Magn Reson Imaging 22:710–717

    Article  PubMed  Google Scholar 

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Acknowledgement

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.

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Correspondence to Elke Hattingen.

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Hattingen, E., Blasel, S., Dettmann, E. et al. Perfusion-weighted MRI to evaluate cerebral autoregulation in aneurysmal subarachnoid haemorrhage. Neuroradiology 50, 929–938 (2008). https://doi.org/10.1007/s00234-008-0424-4

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  • DOI: https://doi.org/10.1007/s00234-008-0424-4

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