Background: The aim of the current overview is to highlight the possibilities of magnetic resonance imaging (MRI) in the assessment of patients with obstructive arterial disease. The anatomic and hemodynamic aspects of the extra- and intracranial cerebral circulation were analyzed and show the importance of combining both aspects in studying cerebral hemodynamic changes. Results: Three levels of cerebral circulation are distinguished: blood flow to the brain (level 1); the distribution of blood flow in the brain (level 2), and finally perfusion of the brain (level 3). To investigate the anatomy of the arteries in the neck and the circle of Willis, contrast-enhanced, time-of-flight and phase contrast MR angiography (MRA) are available. To evaluate the hemodynamics at the 1st and 2nd level of the cerebral circulation two-dimensional phase contrast (volume flow and flow direction) MRA can be used. In addition, the distribution of blood via the circle of Willis can be visualized with dynamic MRA. At the 3rd level, measurements of regional brain perfusion can be obtained by injecting gadolinium, dynamic susceptibility contrast MRI, or noninvasively with arterial spin labeling (ASL) MRI. In addition, selective ASL MRI is able to evaluate the perfused territories of individual brain-feeding arteries. Conclusion: The currently available MR techniques allow evaluation of the cerebral circulation from the aortic arch upwards towards the microvasculature and brain tissue perfusion in a comprehensive 20-min protocol. The combined use of the described MR methods in patients with steno-occlusive disease will further clarify the pathophysiological relations between the vasculature, perfusion and brain function.

1.
Powers WJ: Cerebral hemodynamics in ischemic cerebrovascular disease. Ann Neurol 1991;29:231–240.
2.
Caplan LR, Hennerici M: Impaired clearance of emboli (washout) is an important link between hypoperfusion, embolism, and ischemic stroke. Arch Neurol 1998;55:1475–1482.
3.
Derdeyn CP, Grubb RLJ, Powers WJ: Cerebral hemodynamic impairment: methods of measurement and association with stroke risk. Neurology 1999;53:251–259.
4.
Klijn CJM, Kappelle LJ, Tulleken CAF, van Gijn J: Symptomatic carotid artery occlusion. A reappraisal of hemodynamic factors. Stroke 1997;28:2084–2093.
5.
Osborne A: Diagnostic Cerebral Angiography. Philadelphia, Lippincott William & Wilkins, 1999.
6.
Barnett HJM, Taylor DW, Eliasziw M, Fox AJ, Ferguson GG, Haynes RB, Rankin RN, Clagett GP, Hachinski VC, Sackett DL, Thorpe KE, Meldrum HE: Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. N Engl J Med 1998;339:1415–1425.
7.
Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of the MRC European Carotid Surgery Trial (ECST). Lancet 1998;351:1379–1387.
8.
Henderson RD, Eliasziw M, Fox AJ, Rothwell PM, Barnett HJM: Angiographically defined collateral circulation and risk of stroke in patients with severe carotid artery stenosis. Stroke 2000;31:128–132.
9.
Vernieri F, Pasqualetti P, Matteis M, Passarelli F, Troisi E, Rossini PM, Caltagirone C, Silvestrini M: Effect of collateral blood flow and cerebral vasomotor reactivity on the outcome of carotid artery occlusion. Stroke 2001;32:1552–1558.
10.
Brozici M, van der ZA, Hillen B: Anatomy and functionality of leptomeningeal anastomoses: a review. Stroke 2003;34:2750–2762.
11.
Momjian-Mayor I, Baron JC: The pathophysiology of watershed infarction in internal carotid artery disease: review of cerebral perfusion studies. Stroke 2005;36:567–577.
12.
Liebeskind DS: Collateral circulation. Stroke 2003;34:2279–2284.
13.
Parker DL, Parker DJ, Blatter DD, Du YP, Goodrich KC: The effect of image resolution on vessel signal in high-resolution magnetic resonance angiography. J Magn Reson Imaging 1996;6:632–641.
14.
Hoogeveen RM, Bakker CJ, Viergever MA: Phase-derivative analysis in MR angiography: reduced Venc dependency and improved vessel wall detection in laminar and disturbed flow. J Magn Reson Imaging 1997;7:321–330.
15.
Mustert BR, Williams DM, Prince MR: In vitro model of arterial stenosis: correlation of MR signal dephasing and trans-stenotic pressure gradients. Magn Reson Imaging 1998;16:301–310.
16.
Kent KC, Kuntz KM, Patel MR, Kim D, Klufas RA, Whittemore AD, Polak JF, Skillman JJ, Edelman RR: Perioperative imaging strategies for carotid endarterectomy. An analysis of morbidity and cost-effectiveness in symptomatic patients. JAMA 1995;274:888–893.
17.
Nederkoorn PJ, van der Graaf Y, Hunink MG: Duplex ultrasound and magnetic resonance angiography compared with digital subtraction angiography in carotid artery stenosis: a systematic review. Stroke 2003;34:1324–1332.
18.
Willinek WA, Gieseke J, Conrad R, Strunk H, Hoogeveen R, von Falkenhausen M, Keller E, Urbach H, Kuhl CK, Schild HH: Randomly segmented central k-space ordering in high-spatial-resolution contrast-enhanced MR angiography of the supraaortic arteries: initial experience. Radiology 2002;225:583–588.
19.
Buskens E, Nederkoorn PJ, Buijs-Van Der Woude T, Mali WP, Kappelle LJ, Eikelboom BC, van der Graaf Y, Hunink MG: Imaging of carotid arteries in symptomatic patients: cost-effectiveness of diagnostic strategies. Radiology 2004;233:101–112.
20.
Nederkoorn PJ, Elgersma OE, van der Graaf Y, Eikelboom BC, Kappelle LJ, Mali WP: Carotid artery stenosis: accuracy of contrast-enhanced MR angiography for diagnosis. Radiology 2003;228:677–682.
21.
Willinek WA, von Falkenhausen M, Born M, Gieseke J, Holler T, Klockgether T, Textor HJ, Schild HH, Urbach H: Noninvasive detection of steno-occlusive disease of the supra-aortic arteries with three-dimensional contrast-enhanced magnetic resonance angiography: a prospective, intra-individual comparative analysis with digital subtraction angiography. Stroke 2005;36:38–43.
22.
Saito K, Kimura K, Nagatsuka K, Nagano K, Minematsu K, Ueno S, Naritomi H: Vertebral artery occlusion in duplex color-coded ultrasonography. Stroke 2004;35:1068–1072.
23.
Amin-Hanjani S, Du X, Zhao M, Walsh K, Malisch TW, Charbel FT: Use of quantitative magnetic resonance angiography to stratify stroke risk in symptomatic vertebrobasilar disease. Stroke 2005;36:1140–1145.
24.
Firmin DN, Nayler GL, Klipstein RH, Underwood SR, Rees RSO, Longmore DB: In vivo validation of MR velocity imaging. J Comput Assist Tomogr 1987;11:751–756.
25.
Bendel P, Buonocore E, Bockisch A, Besozzi MC: Blood flow in the carotid arteries: quantification by using phase-sensitive MR imaging. AJR Am J Roentgenol 1989;152:1307–1310.
26.
Enzmann DR, Marks MP, Pelc NJ: Comparison of cerebral artery blood flow measurements with gated cine and ungated phase-contrast techniques. J Magn Reson Imaging 1993;3:705–712.
27.
Bakker CJG, Kouwenhoven M, Hartkamp MJ, Hoogeveen RM, Mali WPTM: Accuracy and precision of time-averaged flow as measured by non-triggered 2D phase-contrast MR angiography: a phantom evaluation. Magn Reson Imaging 1995;13:959–965.
28.
Bakker CJG, Hartkamp MJ, Mali WPTM: Measuring blood flow by nontriggered 2D phase contrast MR angiography. Magn Reson Imaging 1996;14:609–614.
29.
Spilt A, Box FM, van der Geest RJ, Reiber JH, Kunz P, Kamper AM, Blauw GJ, van Buchem MA: Reproducibility of total cerebral blood flow measurements using phase contrast magnetic resonance imaging. J Magn Reson Imaging 2002;16:1–5.
30.
van Everdingen KJ, Klijn CJM, Kappelle LJ, Mali WPTM, Van der Grond J: MRA flow quantification in patients with a symptomatic internal carotid artery occlusion. Stroke 1997;28:1595–1600.
31.
Hendrikse J, van Raamt AF, van der Graaf Y, Mali WP, van der Grond J: Distribution of cerebral blood flow in the circle of Willis. Radiology 2005;235:184–189.
32.
Krabbe Hartkamp MJ, Van der Grond J, de Leeuw FE, de Groot JC, Algra A, Hillen B, Breteler MM, Mali WPTM: Circle of Willis: morphologic variation on three-dimensional time-of-flight MR angiograms. Radiology 1998;207:103–111.
33.
Hoksbergen AW, Majoie CB, Hulsmans FJ, Legemate DA: Assessment of the collateral function of the circle of Willis: three-dimensional time-of-flight MR angiography compared with transcranial color-coded duplex sonography. AJNR Am J Neuroradiol 2003;24:456–462.
34.
Hendrikse J, Eikelboom BC, Van der Grond J: Magnetic resonance angiography of collateral compensation in asymptomatic and symptomatic internal carotid artery stenosis. J Vasc Surg 2002;36:799–805.
35.
Schomer DF, Marks MP, Steinberg GK, Johnstone IM, Boothroyd DB, Ross MR, Pelc NJ, Enzmann DR: The anatomy of the posterior communicating artery as a risk factor for ischemic cerebral infarction. N Engl J Med 1994;330:1565–1570.
36.
Hartkamp MJ, Van der Grond J, van Everdingen KJ, Hillen B, Mali WPTM: Circle of willis collateral flow investigated by magnetic resonance angiography. Stroke 1999;30:2671–2678.
37.
Hoogeveen RM, Bakker CJ, Viergever MA: Limits to the accuracy of vessel diameter measurement in MR angiography. J Magn Reson Imaging 1998;8:1228–1235.
38.
Pernicone JR, Siebert JE, Laird TA, Rosenbaum TL, Potchen EJ: Determination of blood flow direction using velocity-phase image display with 3-D phase-contrast MR angiography. AJNR Am J Neuroradiol 1992;13:1435–1438.
39.
Ross MR, Pelc NJ, Enzmann DR: Qualitative phase contrast MRA in the normal and abnormal circle of Willis. AJNR Am J Neuroradiol 1993;14:19–25.
40.
Miralles M, Dolz JL, Cotillas J, Aldoma J, Santiso MA, Gimenez A, Capdevila A, Cairols MA: The role of the circle of Willis in carotid occlusion: assessment with phase contrast MR angiography and transcranial duplex. Eur J Vasc Endovasc Surg 1995;10:424–430.
41.
Rutgers DR, Klijn CJM, Kappelle LJ, van Huffelen AC, Van der Grond J: A longitudinal study of collateral flow patterns in the circle of Willis and the ophthalmic artery in patients with a symptomatic internal carotid artery occlusion. Stroke 2000;31:1913–1920.
42.
Hendrikse J, Rutgers DR, Klijn CJ, Eikelboom BC, Van der Grond J: Effect of carotid endarterectomy on primary collateral blood flow in patients with severe carotid artery lesions. Stroke 2003;34:1650–1654.
43.
Enzmann DR, Ross MR, Marks MP, Pelc NJ: Bloodflow in major cerebral arteries measured by phase contrast cine MR. AJNR Am J Neuroradiol 1994;15:123–129.
44.
van Osch MJ, Hendrikse J, Golay X, Bakker CJ, van der Grond J: Non-invasive visualization of collateral blood flow patterns of the circle of Willis by dynamic MR angiography. Med Image Anal 2006;10:59–70.
45.
Gauvrit JY, Leclerc X, Oppenheim C, Munier T, Trystram D, Rachdi H, Nataf F, Pruvo JP, Meder JF: Three-dimensional dynamic MR digital subtraction angiography using sensitivity encoding for the evaluation of intracranial arteriovenous malformations: a preliminary study. AJNR Am J Neuroradiol 2005;26:1525–1531.
46.
Warren DJ, Hoggard N, Walton L, Radatz MW, Kemeny AA, Forster DM, Wilkinson ID, Griffiths PD: Cerebral arteriovenous malformations: comparison of novel magnetic resonance angiographic techniques and conventional catheter angiography. Neurosurgery 2001;48:973–982.
47.
Edelman RR, Mattle HP, O’Reilly GV, Wentz KU, Liu C, Zhao B: Magnetic Resonance Imaging of flow dynamics in the circle of Willis. Stroke 1990;21:56–65.
48.
Warmuth C, Ruping M, Forschler A, Koennecke HC, Valdueza JM, Kauert A, Schreiber SJ, Siekmann R, Zimmer C: Dynamic spin labeling angiography in extracranial carotid artery stenosis. AJNR Am J Neuroradiol 2005;26:1035–1043.
49.
Hendrikse J, van der Grond J, Lu H, van Zijl PC, Golay X: Flow territory mapping of the cerebral arteries with regional perfusion MRI. Stroke 2004;35:882–887.
50.
Davies NP, Jezzard P: Selective arterial spin labeling (SASL): perfusion territory mapping of selected feeding arteries tagged using two-dimensional radiofrequency pulses. Magn Reson Med 2003;49:1133–1142.
51.
Taoka T, Iwasaki S, Nakagawa H, Fukusumi A, Hirohashi S, Sakamoto M, Kichikawa K, Murata K: Distinguishing between anterior cerebral artery and middle cerebral artery perfusion by color-coded perfusion direction mapping with arterial spin labeling. AJNR Am J Neuroradiol 2004;25:248–251.
52.
Werner R, Norris DG, Alfke K, Mehdorn HM, Jansen O: Continuous artery-selective spin labeling (CASSL). Magn Reson Med 2005;53:1006–1012.
53.
Trampel R, Mildner T, Goerke U, Schaefer A, Driesel W, Norris DG: Continuous arterial spin labeling using a local magnetic field gradient coil. Magn Reson Med 2002;48:543–546.
54.
Zaharchuk G, Ledden PJ, Kwong KK, Reese TG, Rosen BR, Wald LL: Multislice perfusion and perfusion territory imaging in humans with separate label and image coils. Magn Reson Med 1999;41:1093–1098.
55.
Werner R, Alfke K, Schaeffter T, Nabavi A, Mehdorn HM, Jansen O: Brain perfusion territory imaging applying oblique-plane arterial spin labeling with a standard send/receive head coil. Magn Reson Med 2004;52:1443–1447.
56.
van der Zwan A, Hillen B, Tulleken CAF, Dujovny M, Dragovic L: Variability of the territories of the major cerebral arteries. J Neurosurg 1992;77:927–940.
57.
Van Laar PJ, Hendrikse J, Golay X, Lu H, van Osch MJP, Van der Grond J: In vivo flow territory mapping of major brain feeding arteries. Neuroimage 2006;1:136–144.
58.
Detre JA, Alsop DC: Perfusion magnetic resonance imaging with continuous arterial spin labeling: methods and clinical applications in the central nervous system. Eur J Radiol 1999;30:115–124.
59.
Calamante F, Thomas DL, Pell GS, Wiersma J, Turner R: Measuring cerebral blood flow using magnetic resonance imaging techniques. J Cereb Blood Flow Metab 1999;19:701–735.
60.
Barbier EL, Lamalle L, Decorps M: Methodology of brain perfusion imaging. J Magn Reson Imaging 2001;13:496–520.
61.
Rempp KA, Brix G, Wenz F, Becker CR, Gückel F, Lorenz WJ: Quantification of regional cerebral bloodflow and volume with dynamic susceptibility contrast-enhanced MR Imaging. Radiology 1994;193:637–641.
62.
Ostergaard L, Weisskoff RM, Chesler DA, Gyldensted C, Rosen BR: High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis. Magn Reson Med 1996;36:715–725.
63.
Vonken EJ, van Osch MJ, Bakker CJ, Viergever MA: Measurement of cerebral perfusion with dual-echo multi-slice quantitative dynamic susceptibility contrast MRI. J Magn Reson Imaging 1999;10:109–117.
64.
Weisskoff RM, Chesler D, Boxerman JL, Rosen BR: Pitfalls in MR measurement of tissue blood flow with intravascular tracers: which mean transit time? Magn Reson Med 1993;29:553–558.
65.
Perthen JE, Calamante F, Gadian DG, Connelly A: Is quantification of bolus tracking MRI reliable without deconvolution? Magn Reson Med 2002;47:61–67.
66.
Calamante F, Williams SR, van Bruggen N, Kwong KK, Turner R: A model for quantification of perfusion in pulsed labelling techniques. NMR Biomed 1996;9:79–83.
67.
Buxton RB, Frank LR, Wong EC, Siewert B, Warach S, Edelman RR: A general kinetic model for quantitative perfusion imaging with arterial spin labeling. Magn Reson Med 1998;40:383–396.
68.
Gonzalez-At JB, Alsop DC, Detre JA: Cerebral perfusion and arterial transit time changes during task activation determined with continuous arterial spin labeling. Magn Reson Med 2000;43:739–746.
69.
Hendrikse J, van Osch MJ, Rutgers DR, Bakker CJ, Kappelle LJ, Golay X, van der Grond J: Internal carotid artery occlusion assessed at pulsed arterial spin-labeling perfusion MR imaging at multiple delay times. Radiology 2004;233:899–904.
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