The pathophysiology of cerebral vasospasm following aneurysmal subarachnoid hemorrhage (SAH) is complex and is not entirely understood. Mechanistic insights have been gained through advances in the capabilities of diagnostic imaging. Core techniques have focused on the assessment of vessel caliber, tissue metabolism, and/or regional perfusion parameters. Advances in imaging have provided clinicians with a multifaceted approach to assist in the detection of cerebral vasospasm and the diagnosis of delayed ischemic neurologic deficits (DIND). However, a single test or algorithm with broad efficacy remains elusive. This paper examines both anatomical and physiological imaging modalities applicable to post-SAH vasospasm and offers a historical background. We consider cerebral blood flow velocities measured by Transcranial Doppler Ultrasonography (TCD). Structural imaging techniques, including catheter-based Digital Subtraction Angiography (DSA), CT Angiography (CTA), and MR Angiography (MRA), are reviewed. We examine physiologic assessment by PET, HMPAO SPECT, 133Xe Clearance, Xenon-Enhanced CT (Xe/CT), Perfusion CT (PCT), and Diffusion-Weighted/MR Perfusion Imaging. Comparative advantages and limitations are discussed. 1. Introduction and Historical Perspective Cerebral vasospasm is a delayed complication of subarachnoid hemorrhage. It generally occurs 4–14 days after aneurysmal rupture and is associated with morbidity and mortality rates between 10 and 30% [1]. While changes are commonly observed in the large caliber conveyance arteries, effects on the smaller vessels of the microcirculation, including alterations in blood brain barrier permeability, may be equally important in determining clinical impact. Such factors may account for the higher incidence of vasospasm as defined by imaging criteria (“radiographic vasospasm”) than rates of neurological dysfunction (“clinical vasospasm”). Early diagnosis and treatment could potentially prevent and/or minimize delayed ischemic neurological deficits (DIND). Advances in clinical management of cerebral vasospasm have lagged far behind innovations in brain imaging. Given that radiographic vasospasm does not strongly associate with DIND, efforts have refocused on understanding pathophysiology through advanced correlative imaging. Technological developments have enabled accurate assessment of tissue oxygenation, metabolic uptake, and cerebral perfusion. This paper will review imaging modalities applied to the detection of cerebral vasospasm and the diagnosis of DIND. A historical background is presented, and
References
[1]
A. P. Carlson and H. Yonas, “Radiographic assessment of vasospasm after aneurysmal subarachnoid hemorrhage: the physiological perspective,” Neurological Research, vol. 31, no. 6, pp. 593–604, 2009.
[2]
A. Ecker and P. A. Riemenschneider, “Arteriographic demonstration of spasm of the intracranial arteries, with special reference to saccular arterial aneurysms,” Journal of Neurosurgery, vol. 8, no. 6, pp. 660–667, 1951.
[3]
E. G. Hoeffner, S. K. Mukherji, A. Srinivasan, and D. J. Quint, “Neuroradiology back to the future: brain imaging,” American Journal of Neuroradiology, vol. 33, no. 1, pp. 5–11, 2012.
[4]
R. Aaslid, T. M. Markwalder, and H. Nornes, “Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries,” Journal of Neurosurgery, vol. 57, no. 6, pp. 769–774, 1982.
[5]
R. Aaslid, P. Huber, and H. Nornes, “Evaluation of cerebrovascular spasm with transcranial Doppler ultrasound,” Journal of Neurosurgery, vol. 60, no. 1, pp. 37–41, 1984.
[6]
A. Rigamonti, A. Ackery, and A. J. Baker, “Transcranial Doppler monitoring in subarachnoid hemorrhage: a critical tool in critical care,” Canadian Journal of Anesthesia, vol. 55, no. 2, pp. 112–123, 2008.
[7]
H. White and B. Venkatesh, “Applications of transcranial Doppler in the ICU: a review,” Intensive Care Medicine, vol. 32, no. 7, pp. 981–994, 2006.
[8]
B. L. Clyde, D. K. Resnick, H. Yonas, H. A. Smith, and A. M. Kaufmann, “The relationship of blood velocity as measured by transcranial Doppler ultrasonography to cerebral blood flow as determined by stable xenon computed tomographic studies after aneurysmal subarachnoid hemorrhage,” Neurosurgery, vol. 38, no. 5, pp. 896–905, 1996.
[9]
M. A. Sloan, A. V. Alexandrov, C. H. Tegeler et al., “Assessment: transcranial Doppler ultrasonography: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology,” Neurology, vol. 62, no. 9, pp. 1468–1481, 2004.
[10]
S. P. Lad, R. Guzman, M. E. Kelly et al., “Cerebral perfusion imaging in vasospasm,” Neurosurgical Focus, vol. 21, no. 3, p. E7, 2006.
[11]
K. F. Lindegaard, H. Nornes, S. J. Bakke, W. Sorteberg, and P. Nakstad, “Cerebral vasospasm diagnosis by means of angiography and blood velocity measurements,” Acta Neurochirurgica, vol. 100, no. 1-2, pp. 12–24, 1989.
[12]
M. Jakobsen, E. Enevoldsen, and T. Dalager, “Spasm index in subarachnoid haemorrhage: consequences of vasospasm upon cerebral blood flow and oxygen extraction,” Acta Neurologica Scandinavica, vol. 82, no. 5, pp. 311–320, 1990.
[13]
N. R. Gonzalez, W. J. Boscardin, T. Glenn, F. Vinuela, and N. A. Martin, “Vasospasm probability index: a combination of transcranial Doppler velocities, cerebral blood flow, and clinical risk factors to predict cerebral vasospasm after aneurysmal subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 107, no. 6, pp. 1101–1112, 2007.
[14]
G. E. Sviri, B. Ghodke, G. W. Britz et al., “Transcranial Doppler grading criteria for basilar artery vasospasm,” Neurosurgery, vol. 59, no. 2, pp. 360–365, 2006.
[15]
R. W. Seiler, P. Grolimund, R. Aaslid, et al., “Cerebral vasospasm evaluated by transcranial ultrasound correlated with clinical grade and CT-visualized subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 64, no. 4, pp. 594–600, 1986.
[16]
G. Rordorf, W. J. Koroshetz, W. A. Copen et al., “Diffusion- and perfusion-weighted imaging in vasospasm after subarachnoid hemorrhage,” Stroke, vol. 30, no. 3, pp. 599–605, 1999.
[17]
Y. Y. Vora, M. Suarez-Almazor, D. E. Steinke, M. L. Martin, and J. M. Findlay, “Role of transcranial Doppler monitoring in the diagnosis of cerebral vasospasm after subarachnoid hemorrhage,” Neurosurgery, vol. 44, no. 6, pp. 1237–1247, 1999.
[18]
Y. Okada, T. Shima, M. Nishida et al., “Comparison of transcranial Doppler investigation of aneurysmal vasospasm with digital subtraction angiographic and clinical findings,” Neurosurgery, vol. 45, no. 3, pp. 443–449, 1999.
[19]
C. Lysakowski, B. Walder, M. C. Costanza, and M. R. Tramèr, “Transcranial Doppler versus angiography in patients with vasospasm due to a ruptured cerebral aneurysm: a systematic review,” Stroke, vol. 32, no. 10, pp. 2292–2298, 2001.
[20]
M. A. Sloan, E. C. Haley Jr., N. F. Kassel et al., “Sensitivity and specificity of transcranial Doppler ultrasonography in the diagnosis of vasospasm following subarachnoid hemorrhage,” Neurology, vol. 39, no. 11, pp. 1514–1518, 1989.
[21]
P. Creissard, F. Proust, and O. Langlois, “Vasospasm diagnosis: theoretical and real transcranial Doppler sensitivity,” Acta Neurochirurgica, vol. 136, no. 3-4, pp. 181–185, 1995.
[22]
E. Carrera, J. M. Schmidt, M. Oddo et al., “Transcranial Doppler for predicting delayed cerebral ischemia after subarachnoid hemorrhage,” Neurosurgery, vol. 65, no. 2, pp. 316–323, 2009.
[23]
J. M. K. Lam, P. Smielewski, M. Czosnyka, J. D. Pickard, and P. J. Kirkpatrick, “Predicting delayed ischemic deficits after aneurysmal subarachnoid hemorrhage using a transient hyperemic response test of cerebral autoregulation,” Neurosurgery, vol. 47, no. 4, pp. 819–825, 2000.
[24]
E. A. Perez-Arjona, Z. DelProposto, V. Sehgal, and R. D. Fessler, “New techniques in cerebral imaging,” Neurological Research, vol. 24, supplement 1, pp. S17–S26, 2002.
[25]
N. Janjua and S. A. Mayer, “Cerebral vasospasm after subarachnoid hemorrhage,” Current Opinion in Critical Care, vol. 9, no. 2, pp. 113–119, 2003.
[26]
G.-E. Yao, Q. Li, X.-J. Jiang et al., “Vasospasm after subarachnoid hemorrhage: a 3D rotational angiography study,” Acta Neurochirurgica Supplements, vol. 110, part 2, pp. 221–225, 2011.
[27]
S. A. Marshall, S. Kathuria, P. Nyquist, and D. Gandhi, “Noninvasive imaging techniques in the diagnosis and management of aneurysmal subarachnoid hemorrhage,” Neurosurgery Clinics of North America, vol. 21, no. 2, pp. 305–323, 2010.
[28]
R. P. Ochi, P. T. Vieco, and C. E. Gross, “CT angiography of cerebral vasospasm with conventional angiographic comparison,” American Journal of Neuroradiology, vol. 18, no. 2, pp. 265–269, 1997.
[29]
Y. Otawara, K. Ogasawara, A. Ogawa et al., “Evaluation of vasospasm after subarachnoid hemorrhage by use of multislice computed tomographic angiography,” Neurosurgery, vol. 51, no. 4, pp. 939–942, 2002.
[30]
B. Andrews, Intensive Care in Neurosurgery, Thieme, 2002.
[31]
B. L. Dolmatch, “The History of CT Angiography,” Endovascular Today, 2005, http://bmctoday.net/evtoday/2005/07/article.asp?f=EVT0705_vu_Dolmatch.html.
[32]
A. J. Moore and D. W. Newell, Neurosurgery: Principles and Practice, Springer, 2005.
[33]
R. Takagi, H. Hayashi, H. Kobayashi et al., “Three-dimensional CT angiography of intracranial vasospasm following subarachnoid haemorrhage,” Neuroradiology, vol. 40, no. 10, pp. 631–635, 1998.
[34]
A. Aralasmak, M. Akyuz, C. Ozkaynak, T. Sindel, and R. Tuncer, “CT angiography and perfusion imaging in patients with subarachnoid hemorrhage: correlation of vasospasm to perfusion abnormality,” Neuroradiology, vol. 51, no. 2, pp. 85–93, 2009.
[35]
F. Chen, X. Wang, and B. Wu, “Neuroimaging research on cerebrovascular spasm and its current progress,” Acta Neurochirurgica Supplements, vol. 110, part 2, pp. 233–237, 2011.
[36]
G. B. Anderson, R. Ashforth, D. E. Steinke, and J. M. Findlay, “CT angiography for the detection of cerebral vasospasm in patients with acute subarachnoid hemorrhage,” American Journal of Neuroradiology, vol. 21, no. 6, pp. 1011–1015, 2000.
[37]
S. Binaghi, M. L. Colleoni, P. Maeder et al., “CT angiography and perfusion CT in cerebral vasospasm after subarachnoid hemorrhage,” American Journal of Neuroradiology, vol. 28, no. 4, pp. 750–758, 2007.
[38]
J. J. S. Shankar, I. Y. L. Tan, T. Krings, K. Terbrugge, and R. Agid, “CT angiography for evaluation of cerebral vasospasm following acute subarachnoid haemorrhage,” Neuroradiology, vol. 54, no. 3, pp. 197–203, 2012.
[39]
E. D. Greenberg, R. Gold, M. Reichman et al., “Diagnostic accuracy of CT angiography and CT perfusion for cerebral vasospasm: a meta-analysis,” American Journal of Neuroradiology, vol. 31, no. 10, pp. 1853–1860, 2010.
[40]
D. Y. Yoon, C. S. Choi, K. H. Kim, and B.-M. Cho, “Multidetector-row CT angiography of cerebral vasospasm after aneurysmal subarachnoid hemorrhage: comparison of volume-rendered images and digital subtraction angiography,” American Journal of Neuroradiology, vol. 27, no. 2, pp. 370–377, 2006.
[41]
S. D. Ferguson, D. S. Rosen, D. Bardo, and R. L. Macdonald, “Arterial diameters on catheter and computed tomographic angiography,” World Neurosurgery, vol. 73, no. 3, pp. 165–173, 2010.
[42]
C. W. Washington and G. J. Zipfel, “Detection and monitoring of vasospasm and delayed cerebral ischemia: a review and assessment of the literature,” Neurocritical Care, vol. 15, no. 2, pp. 312–317, 2011.
[43]
S. R. Chaudhary, N. Ko, W. P. Dillon et al., “Prospective evaluation of multidetector-row CT angiography for the diagnosis of vasospasm following subarachnoid hemorrhage: a comparison with digital subtraction angiography,” Cerebrovascular Diseases, vol. 25, no. 1-2, pp. 144–150, 2008.
[44]
C. L. Dumoulin and H. R. Hart Jr., “Magnetic resonance angiography,” Radiology, vol. 161, no. 3, pp. 717–720, 1986.
[45]
T. Horikoshi, A. Fukamachi, H. Nishi, S. I. Yagi, and I. Fukasawa, “Observation of vasospasm after subarachnoid hemorrhage by magnetic resonance angiography—a preliminary study,” Neurologia Medico-Chirurgica, vol. 35, no. 5, pp. 298–304, 1995.
[46]
C. B. Grandin, G. Cosnard, F. Hammer, T. P. Duprez, G. Stroobandt, and P. Mathurin, “Vasospasm after subarachnoid hemorrhage: diagnosis with MR angiography,” American Journal of Neuroradiology, vol. 21, no. 9, pp. 1611–1617, 2000.
[47]
S. Tamatani, O. Sasaki, S. Takeuchi, Y. Fujii, T. Koike, and R. Tanaka, “Detection of delayed cerebral vasospasm, after rupture of intracranial aneurysms, by magnetic resonance angiography,” Neurosurgery, vol. 40, no. 4, pp. 748–753, 1997.
[48]
M. Oelerich, M. G. Lentschig, P. Zunker, P. Reimer, E. J. Rummeny, and G. Schuierer, “Intracranial vascular stenosis and occlusion: comparison of 3D time-of-flight and 3D phase-contrast MR angiography,” Neuroradiology, vol. 40, no. 9, pp. 567–573, 1998.
[49]
P. M. Ruggieri, T. J. Masaryk, J. S. Ross, and M. T. Modic, “Intracranial magnetic resonance angiography,” CardioVascular and Intervenlional Radiology, vol. 15, no. 1, pp. 71–81, 1992.
[50]
R. L. Grubb Jr., M. E. Raichle, J. O. Eichling, and M. H. Gado, “Effects of subarachnoid hemorrhage on cerebral blood volume, blood flow and oxygen utilization in humans,” Journal of Neurosurgery, vol. 46, no. 4, pp. 446–453, 1977.
[51]
W. J. Powers, R. L. Grubb Jr., R. P. Baker, M. A. Mintun, and M. E. Raichle, “Regional cerebral blood flow and metabolism in reversible ischemia due to vasospasm. Determination by positron emission tomography,” Journal of Neurosurgery, vol. 62, no. 4, pp. 539–546, 1985.
[52]
R. L. MacDonald and B. Weir, Cerebral Vasospasm, Academic Press, 2001.
[53]
A. S. Sarrafzadeh, D. Haux, L. Lüdemann et al., “Cerebral ischemia in aneurysmal subarachnoid hemorrhage: a correlative microdialysis-PET study,” Stroke, vol. 35, no. 3, pp. 638–643, 2004.
[54]
S. H. Yeh, R. S. Liu, H. H. Hu et al., “Brain SPECT imaging with 99Tcm-hexamethylpropyleneamine oxime in the early detection of cerebral infarction: comparison with transmission computed tomography,” Nuclear Medicine Communications, vol. 7, no. 12, pp. 873–878, 1986.
[55]
D. Rawluk, F. W. Smith, H. E. Deans, H. G. Gemmell, and A. F. MacDonald, “Technetium 99m HMPAO scanning in patients with subarachnoid haemorrhage: a preliminary study,” British Journal of Radiology, vol. 61, no. 721, pp. 26–29, 1988.
[56]
J. G. Rajendran, D. H. Lewis, D. W. Newell, and H. R. Winn, “Brain SPECT used to evaluate vasospasm after subarachnoid hemorrhage: correlation with angiography and transcranial Doppler,” Clinical Nuclear Medicine, vol. 26, no. 2, pp. 125–130, 2001.
[57]
D. H. Lewis, J. M. Eskridge, D. W. Newell et al., “Brain SPECT and the effect of cerebral angioplasty in delayed ischemia due to vasospasm,” Journal of Nuclear Medicine, vol. 33, no. 10, pp. 1789–1796, 1992.
[58]
S. Davis, J. Andrews, M. Lichtenstein et al., “A single-photon emission computed tomography study of hypoperfusion after subarachnoid hemorrhage,” Stroke, vol. 21, no. 2, pp. 252–259, 1990.
[59]
S. Naderi, M. A. Ozgüven, H. Bayhan, H. G？kalp, A. Erdo？an, and N. Egemen, “Evaluation of cerebral vasospasm in patients with subarachnoid hemorrhage using single photon emission computed tomography,” Neurosurgical Review, vol. 17, no. 4, pp. 261–265, 1994.
[60]
D. Hasan, J. van Peski, I. Loeve, E. P. Krenning, and M. Vermeulen, “Single photon emission computed tomography in patients with acute hydrocephalus or with cerebral ischaemia after subarachnoid haemorrhage,” Journal of Neurology, Neurosurgery & Psychiatry, vol. 54, no. 6, pp. 490–493, 1991.
[61]
R. A. Powsner, L. A. O'Tuama, A. Jabre, and E. R. Melhem, “SPECT imaging in cerebral vasospasm following subarachnoid hemorrhage,” Journal of Nuclear Medicine, vol. 39, no. 5, pp. 765–769, 1998.
[62]
A. Egge, H. Sj？holm, K. Waterloo, T. Solberg, T. Ingebrigtsen, and B. Romner, “Serial single-photon emission computed tomographic and transcranial Doppler measurements for evaluation of vasospasm after aneurysmal subarachnoid hemorrhage,” Neurosurgery, vol. 57, no. 2, pp. 237–242, 2005.
[63]
J. M. Rosen, A. V. Butala, J. M. Oropello et al., “Postoperative changes on brain SPECT imaging after aneurysmal subarachnoid hemorrhage. A potential pitfall in the evaluation of vasospasm,” Clinical Nuclear Medicine, vol. 19, no. 7, pp. 595–597, 1994.
[64]
H. Yonas, R. R. Pindzola, C. C. Meltzer, and H. Sasser, “Qualitative versus quantitative assessment of cerebrovascular reserves,” Neurosurgery, vol. 42, no. 5, pp. 1005–1010, 1998.
[65]
K. Hoedt-Rasmussen, E. Sveinsdottir, and N. A. Lassen, “Regional cerebral blood flow in man determined by intra-arterial injection of radioactive inert gas,” Circulation Research, vol. 18, no. 3, pp. 237–247, 1966.
[66]
M. P. Heilbrun, J. Olesen, and N. A. Lassen, “Regional cerebral blood flow studies in subarachnoid hemorrhage,” Journal of Neurosurgery, vol. 37, no. 1, pp. 36–44, 1972.
[67]
R. Ishii, “Regional cerebral blood flow in patients with ruptured intracranial aneurysms,” Journal of Neurosurgery, vol. 50, no. 5, pp. 587–594, 1979.
[68]
I. Yamakami, K. Isobe, A. Yamaura, et al., “Vasospasm and regional cerebral blood flow (rCBF) in patients with ruptured intracranial aneurysm: serial rCBF studies with the xenon-133 inhalation method,” Neurosurgery, vol. 13, no. 4, pp. 394–401, 1983.
[69]
B. Mickey, S. Vorstrup, B. Voldby, et al., “Serial measurement of regional cerebral blood flow in patients with SAH using 133Xe inhalation and emission computerized tomography,” Journal of Neurosurgery, vol. 60, no. 5, pp. 916–922, 1984.
[70]
B. Voldby, E. M. Enevoldsen, and F. T. Jensen, “Regional CBF, intraventricular pressure, and cerebral metabolism in patients with ruptured intracranial aneurysms,” Journal of Neurosurgery, vol. 62, no. 1, pp. 48–58, 1985.
[71]
B. P. Drayer, S. K. Wolfson, O. M. Reinmuth, M. Dujovny, M. Boehnke, and E. E. Cook, “Xenon enhanced CT for analysis of cerebral integrity, perfusion, and blood flow,” Stroke, vol. 9, no. 2, pp. 123–130, 1978.
[72]
H. Yonas, J. M. Darby, E. C. Marks, S. R. Durham, and C. Maxwell, “CBF measured by Xe-CT: approach to analysis and normal values,” Journal of Cerebral Blood Flow & Metabolism, vol. 11, no. 5, pp. 716–725, 1991.
[73]
D. Gur, W. F. Good, S. K. Wolfson Jr., et al., “In vivo mapping of local cerebral blood flow by xenon-enhanced computed tomography,” Science, vol. 215, no. 4537, pp. 1267–1268, 1982.
[74]
P. R. Kishore, G. U. Rao, R. E. Fernandez et al., “Regional cerebral blood flow measurements using stable xenon enhanced computed tomography: a theoretical and experimental evaluation,” Journal of Computer Assisted Tomography, vol. 8, no. 4, pp. 619–630, 1984.
[75]
H. Yonas, L. Sekhar, D. W. Johnson, and D. Gur, “Determination of irreversible ischemia by xenon-enhanced computed tomographic monitoring of cerebral blood flow in patients with symptomatic vasospasm,” Neurosurgery, vol. 24, no. 3, pp. 368–372, 1989.
[76]
M. B. Fukui, D. W. Johnson, H. Yonas, L. Sekhar, R. E. Latchaw, and S. Pentheny, “Xe/CT cerebral blood flow evaluation of delayed symptomatic cerebral ischemia after subarachnoid hemorrhage,” American Journal of Neuroradiology, vol. 13, no. 1, pp. 265–270, 1992.
[77]
J. Hillman, P. Sturnegk, H. Yonas et al., “Bedside monitoring of CBF with xenon-CT and a mobile scanner: a novel method in neurointensive care,” British Journal of Neurosurgery, vol. 19, no. 5, pp. 395–401, 2005.
[78]
N. W. Knuckey, R. A. Fox, I. Surveyor, and B. A. R. Stokes, “Early cerebral blood flow and computerized tomography in predicting ischemia after cerebral aneurysm rupture,” Journal of Neurosurgery, vol. 62, no. 6, pp. 850–855, 1985.
[79]
D. G. Nabavi, L. M. LeBlanc, B. Baxter et al., “Monitoring cerebral perfusion after subarachnoid hemorrhage using CT,” Neuroradiology, vol. 43, no. 1, pp. 7–16, 2001.
[80]
M. R. Harrigan, C. R. Magnano, L. R. Guterman, and L. N. Hopkins, “Computed tomographic perfusion in the management of aneurysmal subarachnoid hemorrhage: new application of an existent technique,” Neurosurgery, vol. 56, no. 2, pp. 304–317, 2005.
[81]
M. Wintermark, N. U. Ko, W. S. Smith, S. Liu, R. T. Higashida, and W. P. Dillon, “Vasospasm after subarachnoid hemorrhage: utility of perfusion CT and CT angiography on diagnosis and management,” American Journal of Neuroradiology, vol. 27, no. 1, pp. 26–34, 2006.
[82]
R. Kanazawa, M. Kato, K. Ishikawa, T. Eguchi, and A. Teramoto, “Convenience of the computed tomography perfusion method for cerebral vasospasm detection after subarachnoid hemorrhage,” Surgical Neurology, vol. 67, no. 6, pp. 604–611, 2007.
[83]
A. M. Laslo, J. D. Eastwood, F.-X. Chen, and T.-Y. Lee, “Dynamic CT perfusion imaging in subarachnoid hemorrhage-related vasospasm,” American Journal of Neuroradiology, vol. 27, no. 3, pp. 624–631, 2006.
[84]
E. G. Hoeffner, I. Case, R. Jain et al., “Cerebral perfusion CT: technique and clinical applications,” Radiology, vol. 231, no. 3, pp. 632–644, 2004.
[85]
J. W. Dankbaar, M. Rijsdijk, I. C. van der Schaaf, B. K. Velthuis, M. J. H. Wermer, and G. J. E. Rinkel, “Relationship between vasospasm, cerebral perfusion, and delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage,” Neuroradiology, vol. 51, no. 12, pp. 813–819, 2009.
[86]
A. G. Sorensen, F. S. Buonanno, R. G. Gonzalez et al., “Hyperacute stroke: evaluation with combined multisection diffusion-weighted and hemodynamically weighted echo-planar MR imaging,” Radiology, vol. 199, no. 2, pp. 391–401, 1996.
[87]
K. O. L？vblad, M. El-Koussy, R. Guzman et al., “Diffusion-weighted and perfusion-weighted MR of cerebral vasospasm,” Acta Neurochirurgica Supplements, vol. 77, pp. 121–126, 2001.
[88]
P. D. Griffiths, I. D. Wilkinson, P. Mitchell et al., “Multimodality MR imaging depiction of hemodynamic changes and cerebral ischemia in subarachnoid hemorrhage,” American Journal of Neuroradiology, vol. 22, no. 9, pp. 1690–1697, 2001.
[89]
S. Condette-Auliac, S. Bracard, R. Anxionnat et al., “Vasospasm after subarachnoid hemorrhage interest in diffusion-weighted MR imaging,” Stroke, vol. 32, no. 8, pp. 1818–1824, 2001.
[90]
A. A. Wani, R. V. Phadke, S. Behari, R. N. Sahu, A. Jaiswal, and V. K. Jain, “Role of diffusion-weighted MRG in predicting outcome in subarachnoid hemorrhage due to anterior communicating artery aneurysms,” Turkish Neurosurgery, vol. 18, no. 1, pp. 10–16, 2008.
[91]
E. Hattingen, S. Blasel, E. Dettmann et al., “Perfusion-weighted MRI to evaluate cerebral autoregulation in aneurysmal subarachnoid haemorrhage,” Neuroradiology, vol. 50, no. 11, pp. 929–938, 2008.
[92]
F. Hertel, C. Walter, M. Bettag, and M. M？rsdorf, “Perfusion-weighted magnetic resonance imaging in patients with vasospasm: a useful new tool in the management of patients with subarachnoid hemorrhage,” Neurosurgery, vol. 56, no. 1, pp. 28–35, 2005.
[93]
T. Ohtonari, K. Kakinuma, T. Kito, I. Ezuka, and T. Kanazawa, “Diffusion-perfusion mismatch in symptomatic vasospasm after subarachnoid hemorrhage,” Neurologia Medico-Chirurgica, vol. 48, no. 8, pp. 331–336, 2008.
[94]
H. Vatter, E. Güresir, J. Berkefeld et al., “Perfusion-diffusion mismatch in MRI to indicate endovascular treatment of cerebral vasospasm after subarachnoid haemorrhage,” Journal of Neurology, Neurosurgery & Psychiatry, vol. 82, no. 8, pp. 876–883, 2011.
