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26 - Imaging carotid disease: MR and CT perfusion

from Monitoring the local and distal effects of carotid interventions

Published online by Cambridge University Press:  03 December 2009

Jeroen van der Grond
Affiliation:
Leiden University Medical Center, Leiden, The Netherlands
Matthias J. P. van Osch
Affiliation:
Leiden University Medical Center, Leiden, The Netherlands
Jonathan Gillard
Affiliation:
University of Cambridge
Martin Graves
Affiliation:
University of Cambridge
Thomas Hatsukami
Affiliation:
University of Washington
Chun Yuan
Affiliation:
University of Washington
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Summary

Introduction

The presence of adequate cerebral circulation is important to maintain cerebral perfusion and brain function in patients with severe carotid artery disease (Powers, 1991; Klijn et al., 1997; Caplan and Hennerici, 1998; Derdeyn et al., 1999). The level of cerebral perfusion is influenced by many factors such as degree of ipsilateral stenosis, degree of contralateral stenosis, capacity of posterior circulation, the anatomical variants and completeness of the circle of Willis, the remaining vasomotor reactivity, which on itself is influenced by underlying pathology such as atherosclerosis or inflammatory processes, and capacity to reroute blood flow, for instance, via leptomeningeal anastomoses. Although Liebeskind correctly mentioned that the understanding of the cerebral circulation is improved by determining the extra- and intra-cranial collateral capacity (Liebeskind, 2003), the large number of confounding factors, mentioned above, makes it virtually impossible to predict which patients with carotid artery disease are at (high) risk for recurrent symptoms caused by hemodynamical factors. It has been shown that in patients with symptomatic severe internal carotid artery (ICA) stenosis carotid endarterectomy reduces the risk of recurrent stroke by removal of the atheromatous plaque (European Carotid Surgery Trialists' Collaborative Group, 1991; NASCET, 1991; Barnett et al., 2000). Although in patients with occlusive disease of the ICA, the cause of stroke is primarily thromboembolic, the presence of hemodynamic impairment is also recognized as additional risk factor (Caplan and Hennerici, 1998; Grubb et al., 1998).

Type
Chapter
Information
Carotid Disease
The Role of Imaging in Diagnosis and Management
, pp. 358 - 371
Publisher: Cambridge University Press
Print publication year: 2006

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References

Alsop, D. C. and Detre, J. A. (1996). Reduced transit-time sensitivity in noninvasive magnetic resonance imaging of human cerebral blood flow. Journal of Cerebral Blood Flow Metabolism, 16, 1236–49.CrossRefGoogle ScholarPubMed
Alsop, D. C. and Detre, J. A. (1998). Multisection cerebral blood flow Magnetic resonance imaging with continuous arterial spin labeling. Radiology, 208, 410–16.CrossRefGoogle ScholarPubMed
Alsop, D. C., Wedmid, A. and Schlaug, G. (2002). Defining a local input function for perfusion quantification with bolus contrast Magnetic resonance imaging. 659. Proceedings of the ISMagnetic resonanceM 10th annual meeting, Hawaii.Google Scholar
Axel, L. (1980). Cerebral blood flow determination by rapid sequence computed tomography. Radiology, 137, 679–86.CrossRefGoogle ScholarPubMed
Barbier, E. L., Lamalle, L. and Decorps, M. (2001). Methodology of brain perfusion imaging. Journal of Magnetic Resonance Imaging, 13, 496–520.CrossRefGoogle ScholarPubMed
Barnett, H. J. M., Gunton, R. W., Eliasziw, M, et al. (2000). Causes and severity of ischemic stroke in patients with internal carotid artery stenosis. Journal of the American Medical Association, 283, 1429–36.CrossRefGoogle ScholarPubMed
Baumgartner, R. W., Baumgartner, I., Mattle, H. P. and Schroth, G. (1997). Transcranial color-coded duplex sonography in the evaluation of collateral flow through the circle of Willis. AJNR. American Journal of Neuroradiology, 18, 127–33.Google ScholarPubMed
Blankensteijn, J. D., Grond, J., Mali, W. P. T. M., and Eikelboom, B. C. (1997). Flow volume changes in the major cerebral arteries before and after carotid endarterectomy: an Magnetic resonance angiography study. European Journal of Vascular and Endovascular Surgery, 14, 446–50.CrossRefGoogle Scholar
Boxerman, J. L., Hamberg, L. M., Rosen, B. R. and Weisskoff, R. M. (1995). Magnetic resonance contrast due to intravascular magnetic susceptibility perturbations. Magnetic Resonance in Medicine, 34, 555–66.CrossRefGoogle ScholarPubMed
Boysen, G., Ladergaard-Pedersen, H. J., Valentin, N. and Engell, H. C. (1970). Cerebral blood flow and internal carotid artery flow during carotid surgery. Stroke, 1, 253–60.CrossRefGoogle ScholarPubMed
Buxton, R. B., Frank, L. R., Wong, E. C., et al. (1998). A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magnetic Resonance in Medicine, 40, 383–96.CrossRefGoogle ScholarPubMed
Calamante, F., Gadian, D. G. and Connelly, A. (2000). Delay and dispersion effects in dynamic susceptibility contrast Magnetic resonance imaging: simulations using singular value decomposition. Magnetic Resonance in Medicine, 44, 466–73.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Calamante, F., Morup, M. and Hansen, L. K. (2004). Defining a local arterial input function for perfusion Magnetic resonance imaging using independent component analysis. Magnetic Resonance in Medicine, 52, 789–97.CrossRefGoogle Scholar
Calamante, F., Thomas, D. L., Pell, G. S., Wiersma, J. and Turner, R. (1999). Measuring cerebral blood flow using magnetic resonance imaging techniques. Journal of Cerebral Blood Flow Metabolsim, 19, 701–35.CrossRefGoogle ScholarPubMed
Calamante, F., Yim, P. J. and Cebral, J. R. (2003). Estimation of bolus dispersion effects in perfusion Magnetic resonance imaging using image-based computational fluid dynamics. Neuroimage, 19, 341–53.CrossRefGoogle ScholarPubMed
Caplan, L. R. and Hennerici, M. (1998). Impaired clearance of emboli (washout) is an important link between hypoperfusion, embolism, and ischemic stroke. Archives of Neurology, 55, 1475–82.CrossRefGoogle ScholarPubMed
Davies, N. P. and Jezzard, P. (2003). Selective arterial spin labeling (SASL): Perfusion territory mapping of selected feeding arteries tagged using two-dimensional radiofrequency pulses. Magnetic Resonance in Medicine, 49, 1133–42.CrossRefGoogle ScholarPubMed
Derdeyn, C. P., Grubb, R. L. J. and Powers, W. J. (1999). Cerebral hemodynamic impairment: methods of measurement and association with stroke risk. Neurology, 53, 251–9.CrossRefGoogle ScholarPubMed
Detre, J. A., Alsop, D. C., Vives, L. R., et al. (1998). Noninvasive Magnetic resonance imaging evaluation of cerebral blood flow in cerebrovascular disease. Neurology, 50, 633–41.CrossRefGoogle ScholarPubMed
European Carotid Surgery Trialists' Collaborative Group. (1991). Medical research council European Carotid Surgery Trial: interim results for symptomatic patients with severe (70–99%) or with mild (0–29%) carotid stenosis. Lancet, 337, 1235–43.CrossRef
Figueiredo, P. M., Clare, S. and Jezzard, P. (2005). Quantitative perfusion measurements using pulsed arterial spin labeling: effects of large region-of-interest analysis. Journal of Magnetic Resonance Imaging, 21, 676–82.CrossRefGoogle ScholarPubMed
Golay, X., Hendrikse, J. and Lim, T. C. (2004). Perfusion imaging using arterial spin labeling. Topics in Magnetic Resonance Imaging, 15, 10–27.CrossRefGoogle ScholarPubMed
Gordon, I. L, Stemmer, E. A. and Wilson, S. E. (1995). Redistribution of blood flow after carotid endarterectomy. Journal of Vascular Surgery, 22, 349–58.CrossRefGoogle ScholarPubMed
Grubb, R. L. Jr., Derdeyn, C. P., Fritsch, S. M., et al. (1998). Importance of hemodynamic factors in the prognosis of symptomatic carotid occlusion. Journal of the American Medical Association, 280, 1055–60.CrossRefGoogle ScholarPubMed
Gunther, M., Bock, M. and Schad, L. R. (2001). Arterial spin labeling in combination with a look-locker sampling strategy: inflow turbo-sampling EPI-FAIR (ITS-FAIR). Magnetic Resonance in Medicine, 46, 974–84.CrossRefGoogle Scholar
Hartl, W. H., Janssen, I. and Fürst, H. (1994). Effect of carotid endarterectomy on patterns of cerebrovascular reactivity in patients with unilateral carotid artery stenosis. Stroke, 25, 1952–7.CrossRefGoogle ScholarPubMed
Henderson, R. D., Eliasziw, M., Fox, A. J., Rothwell, P. M. and Barnett, H. J. M. (2000). Angiographically defined collateral circulation and risk of stroke in patients with severe carotid artery stenosis. Stroke, 31, 128–32.CrossRefGoogle ScholarPubMed
Hendrikse, J., Lu, H., Grond, J., Zijl, P. C. and Golay, X. (2003). Measurements of cerebral perfusion and arterial hemodynamics during visual stimulation using TURBO-TILT. Magnetic Resonance in Medicine, 50, 429–33.CrossRefGoogle ScholarPubMed
Hendrikse, J., Eikelboom, B. C. and Grond, J. (2002). Magnetic resonance angiography of collateral compensation in asymptomatic and symptomatic internal carotid artery stenosis. Journal of Vascular Surgery, 36, 799–805.CrossRefGoogle ScholarPubMed
Hendrikse, J., Grond, J., Lu, H., Zijl, P. C. and Golay, X. (2004). Flow territory mapping of the cerebral arteries with regional perfusion Magnetic resonance imaging. Stroke, 35, 882–7.CrossRefGoogle Scholar
Hirata, M., Murase, K., Sugawara, Y., Nanjo, T. and Mochizuki, T. (2005). A method for reducing radiation dose in cerebral Computerized tomography perfusion study with variable scan schedule. Radiation Medicine, 23, 162–9.Google ScholarPubMed
Kiselev, V. G. (2001). On the theoretical basis of perfusion measurements by dynamic susceptibility contrast Magnetic resonance imaging. Magnetic Resonance in Medicine, 46, 1113–22.CrossRefGoogle Scholar
Klijn, C. J. M., Kappelle, L. J., Tulleken, C. A. F. and Gijn, J. (1997). Symptomatic carotid artery occlusion. A reappraisal of hemodynamic factors. Stroke, 28, 2084–93.CrossRefGoogle ScholarPubMed
Kluytmans, M., Grond, J., Eikelboom, B. C. and Viergever, M. A. (1998). Long-term hemodynamic effects of carotid endarterectomy. Stroke, 29, 1567–72.CrossRefGoogle ScholarPubMed
Knutsson, L., Stahlberg, F. and Wirestam, R. (2004). Aspects on the accuracy of cerebral perfusion parameters obtained by dynamic susceptibility contrast Magnetic resonance imaging,: a simulation study. Magnetic Resonance Imaging, 22, 789–98.CrossRefGoogle ScholarPubMed
Ko, N. U., Achrol, A. S., Chopra, M., et al. (2005). Cerebral blood flow changes after endovascular treatment of cerebrovascular stenoses. AJNR. American Journal of Neuroradiology, 26, 538–42.Google ScholarPubMed
Kwong, K. K., Chesler, D. A., Weisskoff, R. M., et al. (1995). Magnetic resonance perfusion studies with T1-weighted echo planar imaging. Magnetic Resonance in Medicine, 34, 878–87.CrossRefGoogle Scholar
Li, T. Q., Guang, C. Z., Ostergaard, L., Hindmarsh, T. and Moseley, M. E. (2000). Quantification of cerebral blood flow by bolus tracking and artery spin tagging methods. Magnetic Resonance Imaging, 18, 503–12.CrossRefGoogle Scholar
Liebeskind, D S. (2003). Collateral circulation. Stroke, 34, 2279–84.CrossRefGoogle ScholarPubMed
Lin, W., Celik, A., Derdeyn, C., et al. (2001). Quantitative measurements of cerebral blood flow in patients with unilateral carotid artery occlusion: a PET and Magnetic resonance study. Journal of Magnetic Resonance Imaging, 14, 659–67.CrossRefGoogle Scholar
Lythgoe, D. J., Ostergaard, L., William, S. C., et al. (2000). Quantitative perfusion imaging in carotid artery stenosis using dynamic susceptibility contrast-enhanced magnetic resonance imaging. Magnetic Resonance Imaging, 18, 1–11.CrossRefGoogle ScholarPubMed
Markus, H. S, Clifton, A., Buckenham, T., Taylor, R. and Brown, M. M. (1996). Improvement in cerebral hemodynamics after carotid angioplasty. Stroke, 27, 612–16.CrossRefGoogle ScholarPubMed
Markus, H. and Cullinane, M. (2001). Severely impaired cerebrovascular reactivity predicts stroke and Transient ischemic attack risk in patients with carotid artery stenosis and occlusion. Brain, 124(Pt. 3), 457–67.CrossRefGoogle ScholarPubMed
Miyazawa, N., Arbab, A., Umeda, T. and Akiyama, I. (2005). Perfusion Computerized tomography investigation of chronic internal carotid artery occlusion: comparison with SPEComputerized tomography. Clinical Neurology and Neurosurgery, 108, 11–17.CrossRefGoogle Scholar
Mount, L. A. and Taveras, J. M. (1957). Arteriographic demonstration of the collateral circulation of the cerebral hemispheres. AMA. Archives of Neurology and Psychiatry, 78, 235–53.CrossRefGoogle ScholarPubMed
Muller, M., Hermes, M., Bruckmann, H. and Schimrigk, K. (1995). Transcranial Doppler ultrasound in the evaluation of collateral blood flow in patients with internal carotid artery occlusion: correlation with cerebral angiography. AJNR. American Journal of Neuroradiology, 16, 195–202.Google ScholarPubMed
Nabavi, D. G., Cenic, A., Craen, R. A., et al. (1999). Computerized tomography assessment of cerebral perfusion: experimental validation and initial clinical experience. Radiology, 213, 141–9.CrossRefGoogle ScholarPubMed
North American symptomatic carotid endarterectomy trial North American Symptomatic Carotid Endarterectomy Trial Steering Committee. (1991). North American Symptomatic Carotid Endarterectomy Trial. Methods, patient characteristics, and progress. Stroke, 22, 711–20.CrossRef
Niesen, W. D., Rosenkranz, M., Eckert, B., et al. (2004). Hemodynamic changes of the cerebral circulation after stent-protected carotid angioplasty. AJNR. American Journal of Neuroradiology, 25, 1162–7.Google ScholarPubMed
Nighoghossian, N., Trouillas, P., Philippon, B., Itti, R. and Adeleine, P. (1994). Cerebral blood flow reserve assessment in symptomatic versus asymptomatic high-grade internal carotid artery stenosis. Stroke, 25, 1010–13.CrossRefGoogle ScholarPubMed
Norris, J. W., Krajewski, A. and Bornstein, N. M. (1990). The clinical role of the cerebral collateral circulation in carotid occlusion. Journal of Vascular Surgery, 12, 113–18.CrossRefGoogle ScholarPubMed
Ogasawara, K., Yukawa, H., Kobayashi, M., et al. (2003). Prediction and monitoring of cerebral hyperperfusion after carotid endarterectomy by using single-photon emission computerized tomography scanning. Journal of Neurosurgery, 99, 504–10.CrossRefGoogle ScholarPubMed
Osch, M. J. P., Vonken, E. J., Bakker, C. J. G. and Viergever, M. A. (2001). Correcting partial volume artifacts of the arterial input function in quantitative cerebral perfusion Magnetic resonance imaging. Magnetic Resonance in Medicine, 45, 477–85.3.0.CO;2-4>CrossRefGoogle Scholar
Ostergaard, L., Sorensen, A. G., Kwong, K. K., et al. (1996a). High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part II: Experimental comparison and preliminary results. Magnetic Resonace in Medicine, 36, 726–36.CrossRefGoogle Scholar
Ostergaard, L., Weisskoff, R. M., Chesler, D. A., Gyldensted, C. and Rosen, B. R. (1996b). High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis. Magnetic Resonance in Medicine, 36, 715–25.CrossRefGoogle Scholar
Powers, W. J. (1991). Cerebral hemodynamics in ischemic cerebrovascular disease. Annals of Neurology, 29, 231–40.CrossRefGoogle ScholarPubMed
Powers, W. J., Press, G. A. and Grubb, R. L Jr. (1987). The effect of hemodynamically significant carotid artery disease on the hemodynamic status of the cerebral circulation. Annals of Internal Medicine, 106, 27–35.CrossRefGoogle ScholarPubMed
Rempp, K. A., Brix, G., Wenz, F., et al. (1994). Quantification of regional cerebral bloodflow and volume with dynamic susceptibility contrast-enhanced Magnetic resonance imaging. Radiology, 193, 637–41.CrossRefGoogle Scholar
Sakoh, M., Rohl, L., Gyldensted, C., Gjedde, A. and Ostergaard, L. (2000). Cerebral blood flow and blood volume measured by magnetic resonance imaging bolus tracking after acute stroke in pigs. Comparison with 15O H2O positron emission tomography. Stroke, 31, 1958–64.CrossRefGoogle Scholar
Schomer, D. F., Marks, M. P., Steinberg, G. K., et al. (1994). The anatomy of the posterior communicating artery as a risk factor for ischemic cerebral infarction. New England Journal of Medicine, 330, 1565–70.CrossRefGoogle ScholarPubMed
Schroeder, T., Sillesen, H., Sorensen, O. and Engell, H. C. (1987). Cerebral hyperperfusion following carotid endarterectomy. Journal of Neurosurgery, 66, 824–9.CrossRefGoogle ScholarPubMed
Silvestrini, M., Troisi, E., Matteis, M., Cupini, L. M. and Caltagirone, C. (1996). Transcranial Doppler assessment of cerebrovascular reactivity in symptomatic and asymptomatic severe carotid stenosis. Stroke, 27, 1970–3.CrossRefGoogle ScholarPubMed
Smith, M. R., Lu, H., Trochet, S. and Frayne, R. (2004). Removing the effect of SVD algorithmic artifacts present in quantitative Magnetic resonance perfusion studies. Magnetic Resonance in Medicine, 51, 631–4.CrossRefGoogle Scholar
Taoka, T., Iwasaki, S., Nakagawa, H., et al. (2004). Distinguishing between anterior cerebral artery and middle cerebral artery perfusion by color-coded perfusion direction mapping with arterial spin labeling. AJNR. American Journal of Neuroradiology, 25, 248–51.Google ScholarPubMed
Thomas, D. L., Lythgoe, M. F., Pell, G. S., Calamante, F. and Ordidge, R. J. (2000). The measurement of diffusion and perfusion in biological systems using magnetic resonance imaging. Physics in Medicine and Biology, 45, R97–138.CrossRefGoogle ScholarPubMed
Trampel, R., Mildner, T., Goerke, U., et al. (2002). Continuous arterial spin labeling using a local magnetic field gradient coil. Magnetic Resonance in Medicine, 48, 543–6.CrossRefGoogle ScholarPubMed
Zwan, A., Hillen, B., Tulleken, C. A. F., et al. (1992). Variability of the territories of the major cerebral arteries. Journal of Neurosurgery, 77, 927–40.CrossRefGoogle ScholarPubMed
Laar, P. J., Hendrikse, J. and Golay, X., et al. (2005). In vivo flow territory mapping of major brain feeding arteries. Neuroimage, 29, 136–44.CrossRefGoogle ScholarPubMed
Osch, M. J., Grond, J. and Bakker, C. J. (2005). Partial volume effects on arterial input functions: Shape and amplitude distortions and their correction. Journal of Magnetic Resonance Imaging, 22, 704–9.CrossRefGoogle ScholarPubMed
Osch, M. J., Vonken, E. J., Wu, O., et al. (2003). Model of the human vasculature for studying the influence of contrast injection speed on cerebral perfusion Magnetic resonance imaging. Magnetic Resonance in Medicine, 50, 614–22.CrossRefGoogle Scholar
Vanninen, R., Koivisto, K., Tulla, H., Manninen, H. and Partanen, K. (1995). Hemodynamic effects of carotid endarterectomy by magnetic resonance flow quantification. Stroke, 26, 84–9.CrossRefGoogle ScholarPubMed
Vonken, E. P. A., Beekman, F. J., Bakker, C. J. G. and Viergever, M. A. (1999). Maximum likelihood estimation of cerebral blood flow in dynamic susceptibility contrast Magnetic resonance imaging. Magnetic Resonance in Medicine, 41, 343–50.3.0.CO;2-T>CrossRefGoogle Scholar
Werner, R., Norris, D. G., Alfke, K., Mehdorn, H. M. and Jansen, O. (2005a). Continuous artery-selective spin labeling (CASSL). Magnetic Resonance in Medicine, 53, 1006–12.CrossRefGoogle Scholar
Werner, R., Norris, D. G., Alfke, K., Mehdorn, H. M. and Jansen, O. (2005b). Improving the amplitude-modulated control experiment for multislice continuous arterial spin labeling. Magnetic Resonance in Medicine, 53, 1096–102.CrossRefGoogle Scholar
Wiart, M., Berthezène, Y., Adeleine, P., et al. (2000). Vasodilatory response of border zones to acetazolamide before and after endarterectomy. An echo planar imaging-dynamic susceptibility contrast-enhanced Magnetic resonance imaging study in patients with high-grade unilateral internal carotid artery stenosis. Stroke, 31, 1561–5.CrossRefGoogle ScholarPubMed
Wintermark, M., Maeder, P., Thiran, J. P., Schnyder, P. and Meuli, R. (2001). Quantitative assessment of regional cerebral blood flows by perfusion Computerized tomography studies at low injection rates: a critical review of the underlying theoretical models. European Radiology, 11, 1220–30.CrossRefGoogle ScholarPubMed
Wirestam, R., Ryding, E., Lindgren, A., et al. (2000). Absolute cerebral blood flow measured by dynamic susceptibility contrast Magnetic resonance imaging: a direct comparison with Xe-133 SPEComputerized tomography. Magma, 11, 96–103.CrossRefGoogle Scholar
Wu, O., Ostergaard, L., Koroshetz, W. J., et al. (2003). Effects of tracer arrival time on flow estimates in Magnetic resonance perfusion-weighted imaging. Magnetic Resonance in Medicine, 50, 856–64.CrossRefGoogle Scholar
Wu, O., Ostergaard, L., Weisskoff, R. M., et al. (2003). Tracer arrival timing-insensitive technique for estimating flow in Magnetic resonance perfusion-weighted imaging using singular value decomposition with a block-circulant deconvolution matrix. Magnetic Resonance in Medicine, 50, 164–74.CrossRefGoogle Scholar
Wong, E. C., Buxton, R. B. and Frank, L. R. (1998). Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSS II). Magnetic Resonance in Medicine, 39, 702–8.CrossRefGoogle Scholar
Zaharchuk, G., Ledden, P. J., Kwong, K. K., et al. (1999). Multislice perfusion and perfusion territory imaging in humans with separate label and image coils. Magnetic Resonance in Medicine, 41, 1093–8.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Zierler, K. L. (1962). Theoretical basis of indicator-dilution methods for measuring flow and volume. Circulation Research, 10, 393–407.CrossRefGoogle Scholar

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