Acute cerebral ischemia in rats studied by Carr-Purcell spin-echo magnetic resonance imaging: Assessment of blood oxygenation level-dependent and tissue effects on the transverse relaxation
Martin Kavec
Department of Biomedical NMR and National Bio-NMR Facility, A.I. Virtanen Institute, University of Kuopio, Kuopio, Finland
Search for more papers by this authorOlli H.J. Gröhn
Department of Biomedical NMR and National Bio-NMR Facility, A.I. Virtanen Institute, University of Kuopio, Kuopio, Finland
Search for more papers by this authorMikko I. Kettunen
Department of Biomedical NMR and National Bio-NMR Facility, A.I. Virtanen Institute, University of Kuopio, Kuopio, Finland
Search for more papers by this authorM. Johanna Silvennoinen
Department of Biomedical NMR and National Bio-NMR Facility, A.I. Virtanen Institute, University of Kuopio, Kuopio, Finland
Search for more papers by this authorMichael Garwood
Center for Magnetic Resonance Research, University of Minnesota, Minneapolis, Minnesota
Search for more papers by this authorCorresponding Author
Risto A. Kauppinen
Department of Biomedical NMR and National Bio-NMR Facility, A.I. Virtanen Institute, University of Kuopio, Kuopio, Finland
School of Biological Sciences, University of Manchester, 1.124 Stopford Building, Oxford Road, Manchester M13 9PT, UK===Search for more papers by this authorMartin Kavec
Department of Biomedical NMR and National Bio-NMR Facility, A.I. Virtanen Institute, University of Kuopio, Kuopio, Finland
Search for more papers by this authorOlli H.J. Gröhn
Department of Biomedical NMR and National Bio-NMR Facility, A.I. Virtanen Institute, University of Kuopio, Kuopio, Finland
Search for more papers by this authorMikko I. Kettunen
Department of Biomedical NMR and National Bio-NMR Facility, A.I. Virtanen Institute, University of Kuopio, Kuopio, Finland
Search for more papers by this authorM. Johanna Silvennoinen
Department of Biomedical NMR and National Bio-NMR Facility, A.I. Virtanen Institute, University of Kuopio, Kuopio, Finland
Search for more papers by this authorMichael Garwood
Center for Magnetic Resonance Research, University of Minnesota, Minneapolis, Minnesota
Search for more papers by this authorCorresponding Author
Risto A. Kauppinen
Department of Biomedical NMR and National Bio-NMR Facility, A.I. Virtanen Institute, University of Kuopio, Kuopio, Finland
School of Biological Sciences, University of Manchester, 1.124 Stopford Building, Oxford Road, Manchester M13 9PT, UK===Search for more papers by this authorAbstract
Acute cerebral ischemia has been shown to be associated with an enhanced transverse relaxation rate in rat brain parenchyma, chiefly due to the blood oxygenation level-dependent (BOLD) effect. In this study, Carr-Purcell R2 (CP R2), acquired both with short and long time intervals between centers of adiabatic π-pulses (τCP), was used to assess the contributions of BOLD and tissue effects to the transverse relaxation in two brain ischemia models of rat at 4.7 T. R1ρ and diffusion MR images were also acquired in the same animals. During the first minutes of global ischemia, the long τCP R2 in brain parenchyma increased, whereas the short τCP R2 was unchanged. Based on the simulations, and using constraints of intravascular BOLD effect on parenchymal R2, the former observation was ascribed to be due to susceptibility changes arising in the extravascular compartment. R1ρ declined almost immediately after the onset of focal cerebral ischemia, and further declined during the evolution of ischemic damage. Interestingly, short τCP CP R2 started to decline after some 20 min of focal ischemia and declined over a time course similar to that of R1ρ, indicating that it may be an MRI marker for irreversible tissue changes in cerebral ischemia. The present results show that CP R2 MRI can reveal both tissue- and blood-derived contrast changes in acute cerebral ischemia. Magn Reson Med 51:1138–1146, 2004. © 2004 Wiley-Liss, Inc.
REFERENCES
- 1 Roussel SA, van Bruggen N, King MD, Gadian DG. Identification of collaterally perfused areas following focal ischemia in the rat by comparison of gradient echo and diffusion-weighted MRI. J Cereb Blood Flow Metab 1995; 15: 578–586.
- 2
Grune M,
van Dorsten FA,
Schwindt W,
Olah L,
Hoehn M.
Quantitative T2* and T2′ maps during reversible focal cerebral ischemia in rats: separation of blood oxygenation from nonsusceptibility-based contributions.
Magn Reson Med
1999;
42:
1027–1032.
10.1002/(SICI)1522-2594(199912)42:6<1027::AID-MRM6>3.0.CO;2-# CAS PubMed Web of Science® Google Scholar
- 3 Gröhn OH, Lukkarinen JA, Oja JM, van Zijl PC, Ulatowski JA, Traystman RJ, Kauppinen RA. Noninvasive detection of cerebral hypoperfusion and reversible ischemia from reductions in the magnetic resonance imaging relaxation time, T2. J Cereb Blood Flow Metab 1998; 18: 911–920.
- 4
Calamante F,
Lythgoe MF,
Pell GS,
Thomas DL,
King MD,
Busza AL,
Sotak CH,
Williams SR,
Ordidge RJ,
Gadian DG.
Early changes in water diffusion, perfusion, T1, and T2 during focal cerebral ischemia in the rat studied at 8.5 T.
Magn Reson Med
1999;
41:
479–485.
10.1002/(SICI)1522-2594(199903)41:3<479::AID-MRM9>3.0.CO;2-2 CAS PubMed Web of Science® Google Scholar
- 5 Kettunen MI, Gröhn OHJ, Silvennoinen MJ, Penttonen M, Kauppinen RA. Quantitative assessment of the balance between oxygen delivery and consumption in the rat brain after transient ischemia with T2-BOLD magnetic resonance imaging. J Cereb Blood Flow Metab 2002; 22: 262–270.
- 6 Kavec M, Gröhn OHJ, Kettunen MI, Silvennoinen MJ, Penttonen M, Kauppinen RA. Use of spin echo T2 BOLD in assessment of misery perfusion at 1.5T. MAGMA 2001; 12: 32–39.
- 7 Kettunen MI, Gröhn OHJ, Penttonen M, Kauppinen RA. Cerebral T1ρ relaxation time increases immediately upon global ischemia in the rat independently of blood glucose and anoxic depolarization. Magn Reson Med 2001; 46: 565–572.
- 8 De Crespigny AJ, Wendland MF, Derugin N, Kozniewska E, Moseley ME. Real time observation of transient focal ischemia and hyperemia in cat brain. Magn Reson Med 1992; 27: 391–397.
- 9 Lin W, Lee J-M, Vo KD, An H, Celik A, Lee Y, Hsu CY. Clinical utility of CMRO2 obtained with MRI in determining ischemic brain tissue at risk. Stroke 2001; 32: 341–342.
- 10 Powers WJ. Cerebral hemodynamics in ischemic cerebrovascular disease. Ann Neurol 1991; 29: 231–240.
- 11 Gröhn OHJ, Kauppinen RA. Assessment of brain tissue viability in acute ischemic stroke by BOLD MRI. NMR Biomed 2001; 14: 432–440.
- 12 Gröhn OHJ, Kettunen MI, Penttonen M, Oja JME, van Zijl PCM, Kauppinen RA. Graded reduction of cerebral blood flow in rat as detected by the nuclear magnetic resonance relaxation time T2: a theoretical and experimental approach. J Cereb Blood Flow Metab 2000; 20: 316–326.
- 13 Haacke EM, Hopkins A, Lai S, Buckley P, Friedman L, Meltzer H, Hedera P, Friedland R, Klein S, Thompson D, Detterman D, Tkach J, Lewin JS. 2D and 3D high resolution gradient echo functional imaging of the brain: venous contributions to signal in motor cortex studies. NMR Biomed 1994; 7: 54–62.
- 14
Oja JME,
Gillen J,
Kauppinen RA,
Kraut M,
van Zijl PCM.
Venous blood effects in spin echo fMRI of human brain.
Magn Reson Med
1999;
42:
617–626.
10.1002/(SICI)1522-2594(199910)42:4<617::AID-MRM1>3.0.CO;2-Q CAS PubMed Web of Science® Google Scholar
- 15 Silvennoinen MJ, Clingman CS, Golay X, Kauppinen RA, van Zijl PCM. Comparision of the dependence of blood R2 and R2* on oxygen saturation at 1.5 and 4.7 tesla. Magn Reson Med 2003; 49: 47–60.
- 16 Gati JS, Menon RS, Ugurbil K, Rutt BK. Experimental determination of the BOLD field strength dependence in vessels and tissue. Magn Reson Med 1997; 38: 296–302.
- 17 Zhu XH, Chen W. Observed BOLD effects on cerebral metabolite resonances in human visual cortex during visual stimulation: a functional 1H MRS study at 4 T. Magn Reson Med 2001; 46: 841–847.
- 18 Lei H, Tian R-X, Zhu X-H, Chen W. BOLD responses and T2 changes of cerebral metabolites during forebrain ischemia in rat at high field. In: Proceedings of the 10th Annual Meeting of ISMRM, Honolulu, 2002. p 1258.
- 19 Lei H, Zhang Y, Zhu XH, Chen W. Changes in the proton T2 relaxation times of cerebral water and metabolites during forebrain ischemia in rat at 9.4 T. Magn Reson Med 2003; 49: 979–984.
- 20 Bartha R, Michaeli S, Merkle H, Adriany G, Andersen P, Chen W, Ugurbil K, Garwood M. In vivo 1H2O T2+ measurement in the human occipital lobe at 4T and 7T by Carr-Purcell MRI: detection of microscopic susceptibility contrast. Magn Reson Med 2002; 47: 742–750.
- 21 Michaeli S, Garwood M, Zhu XH, DelaBarre L, Andersen P, Adriany G, Merkle H, Ugurbil K, Chen W. Proton T2 relaxation study of water, N-acetylaspartate, and creatine in human brain using Hahn and Carr-Purcell spin echoes at 4T and 7T. Magn Reson Med 2002; 47: 629–633.
- 22 Kettunen MI, Grohn OH, Silvennoinen MJ, Penttonen M, Kauppinen RA. Effects of intracellular pH, blood, and tissue oxygen tension on T1ρ relaxation in rat brain. Magn Reson Med 2002; 48: 470–477.
- 23 Longa EZ, Weinstein PR, Carlson S, Cummins R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 1989; 20: 84–91.
- 24 Roussel SA, Vanbruggen N, King MD, Houseman J, Williams SR, Gadian DG. Monitoring the initial expansion of focal ischaemic changes by diffusion-weighted MRI using a remote controlled method of occlusion. NMR Biomed 1994; 7: 21–28.
- 25 Mori S, van Zijl PCM. Diffusion weighting by the trace of the diffusion tensor within a single scan. Magn Reson Med 1995; 33: 41–52.
- 26 Garwood M, DelaBarre L. The return of the frequency sweep: designing adiabatic pulses for contemporary NMR. J Magn Reson 2001; 153: 155–177.
- 27 Shaka A, Rucker S, Pines A. Iterative Carr-Purcell trains. J Magn Reson 1988; 77: 606–611.
- 28 Golay X, Silvennoinen MJ, Zhou J, Clingman CS, Kauppinen RA, Pekar JJ, van Zijl PCM. Measurement of tissue oxygen extraction ratios from venous blood T2: increased precision and validation of principle. Magn Reson Med 2001; 46: 282–291.
- 29
Springer CS Jr.
Physicochemical principles influencing magnetopharmaceuticals. In:
RJ Gillies, editor.
NMR in physiology and biomedicine.
San Diego:
Academic Press;
1994. p
75–99.
10.1016/B978-0-12-283980-1.50010-7 Google Scholar
- 30 Brian JEJ. Carbon dioxide and the cerebral circulation. Anesthesiology 1998; 88: 1365–1386.
- 31 Ulatowski JA, Oja JM, Suarez JI, Kauppinen RA, Traystman RJ, van Zijl PC. In vivo determination of absolute cerebral blood volume using hemoglobin as a natural contrast agent: an MRI study using altered arterial carbon dioxide tension. J Cereb Blood Flow Metab 1999; 19: 809–817.
- 32 van Zijl PC, Eleff SM, Ulatowski JA, Oja JM, Ulug AM, Traystman RJ, Kauppinen RA. Quantitative assessment of blood flow, blood volume and blood oxygenation effects in functional magnetic resonance imaging. Nat Med 1998; 4: 159–167.
- 33 Sandor P, Cox van Put J, de Jong W, de Wied D. Continuous measurement of cerebral blood volume in rats with the photoelectric technique: effect of morphine and noloxone. Life Sci 1986; 39: 1657–1665.
- 34 Knight RA, Dereski MO, Helpern JA, Ordidge RJ, Chopp M. Magnetic resonance imaging assessment of evolving focal cerebral ischemia. Comparison with histopathology in rats. Stroke 1994; 25: 1252–1261.
- 35 Silvennoinen MJ, Kettunen MI, Clingman CS, Kauppinen RA. Blood NMR relaxation in the rotating frame: mechanistic implications. Arch Biochem Biophys 2002; 405: 78–86.
- 36 Mäkelä HI, Gröhn OHJ, Kettunen MI, Kauppinen RA. Proton exchange as a relaxation mechanism for T1 in the rotating frame in native and immobilized protein solutions. Biochem Biophys Res Commun 2001; 289: 813–818.
- 37 Gröhn OHJ, Kettunen MI, Mäkelä HI, Penttonen M, Pitkänen A, Lukkarinen JA, Kauppinen RA. Early detection of irreversible cerebral ischemia in the rat using dispersion of the MRI relaxation time, T1ρ. J Cereb Blood Flow Metab 2000; 20: 1457–1466.
- 38 Mäkelä HI, Kettunen MI, Gröhn OHJ, Kauppinen RA. Quantitative T1ρ and magnetization transfer MRI of acute cerebral ischaemia in the rat. J Cereb Blood Flow Metab 2002; 22: 547–558.
- 39
Gröhn OH,
Lukkarinen JA,
Silvennoinen MJ,
Pitkänen A,
van Zijl PC,
Kauppinen RA.
Quantitative magnetic resonance imaging assessment of cerebral ischemia in rat using on-resonance T1 in the rotating frame.
Magn Reson Med
1999;
42:
268–276.
10.1002/(SICI)1522-2594(199908)42:2<268::AID-MRM8>3.0.CO;2-A CAS PubMed Web of Science® Google Scholar