The Use of Magnetic Resonance for Assessing Cerebrovascular Reserve Capacity

Authors: M. Sameš 1;  A. Zolal 1;  T. Radovnický 1;  P. Vachata 1;  R. Bartoš 1;  M. Derner 2
Authors‘ workplace: Neurochirurgická klinika, UJEP a Krajská zdravotní a. s., Masarykova nemocnice v Ústí nad Labem, o. z., 2Radiodiagnostické oddělení, Krajská zdravotní a. s., Masarykova nemocnice v Ústí nad Labem, o. z. 1
Published in: Cesk Slov Neurol N 2009; 72/105(4): 323-330
Category: Review Article


The evalu ati on of cerebrovascular reserve capacity (CVRC) is the basic preconditi on required for EC‑IC bypass indicati on in pati ents with occlusive internal carotid dise ase. In additi on to the alre ady well described and established methods (PET, TCD, perfusi on CT and XeCT), in the last ye ars, a new interest in evalu ati on with the use of MRI methods has emerged. The MRI provides informati on on perfusi on in the whole volume of the brain and it does not expose pati ents to i onizing radi ati on. More over, with the use of some techniques, the examinati on can be performed witho ut the use of exogeno us contrast agent. In this revi ew, we summarize the possibiliti es of CVRC examinati on with the use of magnetic resonance methods, namely the dynamic susceptibility contrast, arteri al spin labeling and BOLD effect. The work presents the advantages and the disadvantages for e ach of these methods, provides the overvi ew of the currently available literary so urces and on their basis, the possible findings are summarized and the interpretati on is proposed.

Key words:
magnetic resonance imaging – perfusion – cerebrovascular reserve capacity – carotid artery occlusion – EC-IC bypass


1. Powers WJ, Press GA, Grubb RL jr, Gado M, Raichle ME. The effect of hemodynamically significant carotid artery dise ase on the hemodynamic status of the cerebral circulati on. Ann Intern Med 1987; 106(1): 27– 34.

2. Grubb RL jr, Derdeyn CP, Fritsch SM, Carpenter DA, Yundt KD, Videen TO et al. Importance of hemodynamic factors in the prognosis of symptomatic carotid occlusi on. JAMA 1998; 280(12): 1055– 1060.

3. Kleiser B, Widder B. Co urse of carotid artery occlusi ons with impaired cerebrovascular re activity. Stroke 1992; 23(2): 171– 174.

4. Derdeyn CP, Videen TO, Yundt KD, Fritsch SM, Carpenter DA, Grubb RL et al. Vari ability of cerebral blo od volume and oxygen extracti on: stages of cerebral haemodynamic impairment revisited. Brain 2002; 125(3): 595– 607.

5. Schumann P, To uzani O, Yo ung AR, Morello R, Baron JC, MacKenzi e ET. Evalu ati on of the rati o of cerebral blo od flow to cerebral blo od volume as an index of local cerebral perfusi on pressure. Brain 1998; 121(7): 1369– 1379.

6. Powers WJ, Derdeyn CP, Fritsch SM, Carpenter DA, Yundt KD, Videen TO et al. Benign prognosis of never- symptomatic carotid occlusi on. Ne urology 2000; 54(4): 878– 882.

7. Hennerici M, Hülsbömer HB, Ra utenberg W, Hefter H.Spontane o us history of asymptomatic internal carotid occlusi on. Stroke 1986; 17(4): 718– 722.

8. Verni eri F, Pasqu aletti P, Passarelli F, Rossini PM, Silvestrini M. Outcome of carotid artery occlusi on is predicted by cerebrovascular re activity. Stroke 1999; 30(3): 593– 598.

9. Ogasawara K, Ogawa A, Yoshimoto T. Cerebrovascular re activity to acetazolamide and o utcome in pati ents with symptomatic internal carotid or middle cerebral artery occlusi on: a xenon‑133 single‑photon emissi on computed tomography study. Stroke 2002; 33(7): 1857– 1862.

10. Schmi edek P, Pi epgras A, Leinsinger G, Kirsch CM, Einhüpl K. Improvement of cerebrovascular reserve capacity by EC‑IC arteri al bypass surgery in pati ents with ICA occlusi on and hemodynamic cerebral ischemi a. J Ne urosurg 1994; 81(2): 236– 244.

11. Derdeyn CP, Grubb RL jr, Powers WJ. Indicati ons for cerebral revascularizati on for pati ents with atherosclerotic carotid occlusi on. Skull Base 2005; 15(1): 7– 14.

12. Failure of extracrani al- intracrani al arteri al bypass to reduce the risk of ischemic stroke. Results of an internati onal randomized tri al. The EC/ IC Bypass Study Gro up. N Engl J Med 1985; 313(19): 1191– 1200.

13. Grubb RL jr, Powers WJ, Derdeyn CP, Adams HP jr,Clarke WR. The Carotid Occlusi on Surgery Study. Ne urosurg Focus 2003; 14(3): e9.

14. Rosen BR, Bellive a u JW, Veve a JM, Brady TJ. Perfusi on imaging with NMR contrast agents. Magn Reson Med 1990; 14(2): 249– 265.

15. Mukherjee P, Kang HC, Videen TO, McKinstry RC, Powers WJ, Derdeyn CP. Me asurement of cerebral blo od flow in chronic carotid occlusive dise ase: comparison of dynamic susceptibility contrast perfusi on MR imaging with positron emissi on tomography. AJNR Am J Ne uroradi ol 2003; 24(5): 862– 871.

16. Apruzzese A, Silvestrini M, Floris R, Verni eri F, Bozzao A, Hagberg G et al. Cerebral hemodynamics in asymptomatic pati ents with internal carotid artery occlusi on: a dynamic susceptibility contrast MR and transcrani al Doppler study. AJNR Am J Ne uroradi ol 2001; 22(6): 1062– 1067.

17. Endo H, Ino ue T, Ogasawara K, Fukuda T, Kanbara Y,Ogawa A. Qu antitative assessment of cerebral hemodynamics using perfusi on- weighted MRI in pati ents with major cerebral artery occlusive dise ase: comparison with positron emissi on tomography. Stroke 2006; 37(2): 388– 392.

18. Griffiths PD, Gaines P, Cleveland T, Be ard J, Venables G, Wilkinson ID. Assessment of cerebral haemodynamics and vascular reserve in pati ents with symptomatic carotid artery occlusi on: an integrated MR method. Ne uroradi ology 2005; 47(3): 175– 182.

19. Gückel FJ, Brix G, Schmi edek P, Pi epgras Z, Becker G,Köpke J et al. Cerebrovascular reserve capacity in pati ents with occlusive cerebrovascular dise ase: assessment with dynamic susceptibility contrast- enhanced MR imaging and the acetazolamide stimulati on test. Radi ology 1996; 201(2): 405– 412.

20. Kajimoto K, Moriwaki H, Yamada N, Hayashida K, Kobayashi J, Miyashita K et al. Cerebral hemodynamic evalu ati on using perfusi on- weighted magnetic resonance imaging: comparison with positron emissi on tomography values in chronic occlusive carotid dise ase. Stroke 2003; 34(7): 1662– 1666.

21. Kikuchi K, Murase K, Miki H, Kikuchi T, Sugawara Y,Mochizuki T et al. Me asurement of cerebral hemodynamics with perfusi on- weighted MR imaging: comparison with pre‑ and post‑acetazolamide 133Xe- SPECT in occlusive carotid dise ase. AJNR Am J Ne uroradi ol 2001; 22(2): 248– 254.

22. Kim JH, Lee SJ, Shin T, Kang KH, Cho i PY, Gong JC et al. Correlative assessment of hemodynamic parameters obtained with T2*- weighted perfusi on MR imaging and SPECT in symptomatic carotid artery occlusi on. AJNR Am J Ne uroradi ol 2000; 21(8): 1450– 1456.

23. Kluytmans M, van der Grond J, Folkers PJ, Mali WP, Vi ergever MA. Differenti ati on of gray matter and white matter perfusi on in pati ents with unilateral internal carotid artery occlusi on. J Magn Reson Imaging 1998; 8(4): 767– 774.

24. Lythgoe DJ, Ostergaard L, Willi am SC, Clucki e A, Buxton- Thomas M, Simmons A et al. Qu antitative perfusi on imaging in carotid artery stenosis using dynamic susceptibility contrast- enhanced magnetic resonance imaging. Magn Reson Imaging 2000; 18(1): 1– 11.

25. Ma J, Mehrkens JH, Holtmannspoetter M, Linke R,Schmid- Elsaesser R, Steiger HJ et al. Perfusi on MRI before and after acetazolamide administrati on for assessment of cerebrovascular reserve capacity in pati ents with symptomatic internal carotid artery (ICA) occlusi on: comparison with 99mTc- ECD SPECT. Ne uroradi ology 2007; 49(4): 317– 326.

26. Maeda M, Yuh WT, Ueda T, Maley JE, Crosby DL, Zhu MW et al. Severe occlusive carotid artery dise ase: hemodynamic assessment by MR perfusi on imaging in symptomatic pati ents. AJNR Am J Ne uroradi ol 1999; 20(1): 43– 51.

27. Mihara F, Kuwabara Y, Tanaka A, Yoshi ura T, Sasaki M, Yoshida T et al. Reli ability of me an transit time obtained using perfusi on- weighted MR imaging; comparison with positron emissi on tomography. Magn Reson Imaging 2003; 21(1): 33– 39.

28. Nasel C, Azizi A, Wilfort A, Mallek R, Schindler E. Me asurement of time- to- pe ak parameter by use of a new standardizati on method in pati ents with stenotic or occlusive dise ase of the carotid artery. AJNR Am J Ne uroradi ol 2001; 22(6): 1056– 1061.

29. Nighoghossi an N, Berthezene Y, Philippon B, Adeleine P, Froment JC, Tro uillas P. Hemodynamic parameter assessment with dynamic susceptibility contrast magnetic resonance imaging in unilateral symptomatic internal carotid artery occlusi on. Stroke 1996; 27(3): 474– 479.

30. Schreiber WG, Gückel F, Stritzke P, Schmi edek P, Schwartz A, Brix G. Cerebral blo od flow and cerebrovascular reserve capacity: estimati on by dynamic magnetic resonance imaging. J Cereb Blo od Flow Metab 1998; 18(10): 1143– 1156.

31. Schubert GA, Weinmann C, Seiz M, Gerigk L, Weiss C,Horn P et al. Cerebrovascular insuffici ency as the criteri on for revascularizati on procedures in selected pati ents: a correlati on study of xenon contrast‑enhanced CT and PWI. Ne urosurg Rev 2009; 32(1): 29– 35.

32. van Osch MJ, Rutgers DR, Vonken EP, van Huffelen AC, Klijn CJ, Bakker CJ et al. Qu antitative cerebral perfusi on MRI and CO2 re activity me asurements in pati ents with symptomatic internal carotid artery occlusi on. Ne uro image 2002; 17(1): 469– 478.

33. Golay X, Hendrikse J, Lim TC. Perfusi on imaging using arteri al spin labeling. Top Magn Reson Imaging 2004; 15(1): 10– 27.

34. Wintermark M, Sesay M, Barbi er E, Borbely K, Dillon WP, Eastwo od JD et al. Comparative overvi ew of brain perfusi on imaging techniques. Stroke 2005; 36(9): e83– e99.

35. Parkes LM, Rashid W, Chard DT, Tofts PS. Normal cerebral perfusi on me asurements using arteri al spin labeling: Reproducibility, stability, and age and gender effects. Magn Reson Med 2004; 51(4): 736– 743.

36. Golay X, Hendrikse J, Van Der Grond J. Applicati on of regi onal perfusi on imaging to extra- intracrani al bypass surgery and severe stenoses. J Ne uroradi ol 2005; 32(5): 321– 324.

37. Detre JA, Samuels OB, Alsop DC, Gonzalez- At JB, Kasner SE, Raps EC. Noninvasive magnetic resonance imaging evalu ati on of cerebral blo od flow with acetazolamide challenge in pati ents with cerebrovascular stenosis. J Magn Reson Imaging 1999; 10(5): 870– 875.

38. Hendrikse J, van Osch MJ, Rutgers DR, Bakker CJ,Kappelle LJ, Golay X et al. Internal carotid artery occlu-si on assessed at pulsed arteri al spin‑labeling perfusi on MR imaging at multiple delay times. Radi ology 2004; 233(3): 899– 904.

39. Yoneda K, Harada M, Morita N, Nishitani H, Uno M,Matsuda T. Comparison of FAIR technique with different inversi on times and post contrast dynamic perfusi on MRI in chronic occlusive cerebrovascular dise ase. Magn Reson Imaging 2003; 21(7): 701– 705.

40. Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blo od oxygenati on. Proc Natl Acad Sci U S A 1990; 87(24): 9868– 9872.

41. Roc AC, Wang J, Ances BM, Li ebeskind DS, Kasner SE, Detre JA. Altered hemodynamics and regi onal cerebral blo od flow in pati ents with hemodynamically significant stenoses. Stroke 2006; 37(2): 382– 387.

42. Herzig R, Hlustik P, Skolo udik D, Sanak D, Vlachova I,Herman M et al. Assessment of the cerebral vasomotor re activity in internal carotid artery occlusi on using a transcrani al Doppler sonography and functi onal MRI. J Ne uro imaging 2008; 18(1): 38– 45.

43. Kazumata K, Tanaka N, Ishikawa T, Kuroda S, Ho ukin K, Mitsumori K. Dissoci ati on of vasore activity to acetazolamide and hypercapni a. Comparative study in pati ents with chronic occlusive major cerebral artery dise ase. Stroke 1996; 27(11): 2052– 2058.

44. Kleinschmidt A, Steinmetz H, Sitzer M, Merboldt KD, Frahm J. Magnetic resonance imaging of regi onal cerebral blo od oxygenati on changes under acetazolamide in carotid occlusive dise ase. Stroke 1995; 26(1): 106– 110.

45. Lythgoe DJ, Willi ams SC, Cullinane M, Markus HS. Mapping of cerebrovascular re activity using BOLD magnetic resonance imaging. Magn Reson Imaging 1999; 17(4): 495– 502.

46. Mandell DM, Han JS, Po ublanc J, Crawley AP, Stainsby JA, Fisher JA et al. Mapping cerebrovascular re activity using blo od oxygen level- dependent MRI in Pati ents with arteri al steno‑occlusive dise ase: comparison with arteri al spin labeling MRI. Stroke 2008; 39(7): 2021– 2028.

47. Ohnishi T, Nakano S, Yano T, Hoshi H, Jinno uchi S,Nagamachi S et al. Susceptibility- weighted MR for evalu ati on of vasodilatory capacity with acetazolamide challenge. AJNR Am J Ne uroradi ol 1996; 17(4): 631– 637.

48. Shiino A, Morita Y, Tsuji A, Maeda K, Ito R, Furukawa A et al. Estimati on of cerebral perfusi on reserve by blo od oxygenati on level- dependent imaging: comparison with single‑photon emissi on computed tomography. J Cereb Blo od Flow Metab 2003; 23(1): 121– 135.

49. Ziyeh S, Rick J, Reinhard M, Hetzel A, Mader I, Speck O. Blo od oxygen level- dependent MRI of cerebral CO2 re activity in severe carotid stenosis and occlusi on. Stroke 2005; 36(4): 751– 756.

50. van der Zande FH, Hofman PA, Backes WH. Mapping hypercapni a‑induced cerebrovascular re activity using BOLD MRI. Ne uroradi ology 2005; 47(2): 114– 120.

51. Hedera P, Lai S, Lewin JS, Haacke EM, Wu D, Lerner AJ et al. Assessment of cerebral blo od flow reserve using functi onal magnetic resonance imaging. J Magn Reson Imaging 1996; 6(5): 718– 725.

52. Nari ai T, Suzuki R, Hirakawa K, Maehara T, Ishii K, Senda M. Vascular reserve in chronic cerebral ischemi a me asured by the acetazolamide challenge test: comparison with positron emissi on tomography. AJNR Am J Ne uroradi ol 1995; 16(3): 563– 570.

53. Widder B, Kleiser B, Krapf H. Co urse of cerebrovascular re activity in pati ents with carotid artery occlusi ons. Stroke 1994; 25(10): 1963– 1967.

54. He X, Yablonskiy DA. Qu antitative BOLD: mapping of human cerebral de oxygenated blo od volume and oxygen extracti on fracti on: defa ult state. Magn Reson Med 2007; 57(1): 115– 126.

55. He X, Zhu M, Yablonskiy DA. Validati on of oxygen extracti on fracti on me asurement by qBOLD technique. Magn Reson Med 2008; 60(4): 882– 888.

56. Kavec M, Useni us JP, Tuunanen PI, Rissanen A, Ka uppinen RA. Assessment of cerebral hemodynamics and oxygen extracti on using dynamic susceptibility contrast and spin echo blo od oxygenati on level- dependent magnetic resonance imaging: applicati ons to carotid stenosis pati ents. Ne uro image 2004; 22(1): 258– 267.

57. Anderson CM, Ka ufman MJ, Lowen SB, Rohan M, Renshaw PF, Teicher MH. Brain T2 relaxati on times correlate with regi onal cerebral blo od volume. MAGMA 2005; 18(1): 3– 6.

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