Oxygenation-sensitive cardiovascular magnetic resonance
Matthias G Friedrich, Theodoros D Karamitsos, Matthias G Friedrich, Theodoros D Karamitsos
Abstract
Oxygenation-sensitive cardiovascular magnetic resonance (CMR) is a non-contrast technique that allows the non-invasive assessment of myocardial oxygenation. It capitalizes on the fact that deoxygenated hemoglobin in blood can act as an intrinsic contrast agent, changing proton signals in a fashion that can be imaged to reflect the level of blood oxygenation. Increases in O(2) saturation increase the BOLD imaging signal (T2 or T2*), whereas decreases diminish it. This review presents the basic concepts and limitations of the BOLD technique, and summarizes the preclinical and clinical studies in the assessment of myocardial oxygenation with a focus on recent advances. Finally, it provides future directions and a brief look at emerging techniques of this evolving CMR field.
Figures
References
- Pauling L, Coryell CD. The Magnetic Properties and Structure of Hemoglobin. Oxyhemoglobin and Carbonmonoxyhemoglobin. Proc Natl Acad Sci USA. 1936;22:210. doi: 10.1073/pnas.22.4.210.
- Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA. 1990;87:9868–9872. doi: 10.1073/pnas.87.24.9868.
- Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, Ugurbil K. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA. 1992;89:5951–5955. doi: 10.1073/pnas.89.13.5951.
- Reeder SB, Faranesh AZ, Boxerman JL, McVeigh ER. In vivo measurement of T*2 and field inhomogeneity maps in the human heart at 1.5 T. Magn Reson Med. 1998;39:988–998. doi: 10.1002/mrm.1910390617.
- Foltz WD, Al-Kwifi O, Sussman MS, Stainsby JA, Wright GA. Optimized spiral imaging for measurement of myocardial T2 relaxation. Magn Reson Med. 2003;49:1089–1097. doi: 10.1002/mrm.10467.
- Dharmakumar R, Arumana JM, Larson AC, Chung Y, Wright GA, Li D. Cardiac phase-resolved blood oxygen-sensitive steady-state free precession MRI for evaluating the functional significance of coronary artery stenosis. Invest Radiol. 2007;42:180–188. doi: 10.1097/01.rli.0000254407.26068.54.
- Arumana JM, Li D, Dharmakumar R. Deriving blood-oxygen-level-dependent contrast in MRI with T2*-weighted, T2-prepared and phase-cycled SSFP methods: theory and experiment. Magn Reson Med. 2008;59:561–570. doi: 10.1002/mrm.21511.
- Dharmakumar R, Arumana JM, Tang R, Harris K, Zhang Z, Li D. Assessment of regional myocardial oxygenation changes in the presence of coronary artery stenosis with balanced SSFP imaging at 3.0 T: theory and experimental evaluation in canines. J Magn Reson Imaging. 2008;27:1037–1045. doi: 10.1002/jmri.21345.
- Atalay MK, Forder JR, Chacko VP, Kawamoto S, Zerhouni EA. Oxygenation in the rabbit myocardium: assessment with susceptibility-dependent MR imaging. Radiology. 1993;189:759–764.
- Wendland MF, Saeed M, Lauerma K, de Crespigny A, Moseley ME, Higgins CB. Endogenous susceptibility contrast in myocardium during apnea measured using gradient recalled echo planar imaging. Magn Reson Med. 1993;29:273–276. doi: 10.1002/mrm.1910290220.
- Niemi P, Poncelet BP, Kwong KK, Weisskoff RM, Rosen BR, Brady TJ, Kantor HL. Myocardial intensity changes associated with flow stimulation in blood oxygenation sensitive magnetic resonance imaging. Magn Reson Med. 1996;36:78–82. doi: 10.1002/mrm.1910360114.
- Li D, Dhawale P, Rubin PJ, Haacke EM, Gropler RJ. Myocardial signal response to dipyridamole and dobutamine: demonstration of the BOLD effect using a double-echo gradient-echo sequence. Magn Reson Med. 1996;36:16–20. doi: 10.1002/mrm.1910360105.
- Bauer WR, Nadler W, Bock M, Schad LR, Wacker CM, Ertl G. Theory of Coherent and Incoherent Nuclear Spin Dephasing in the Heart. Phys Rev Lett. 1999;83:4215–4218. doi: 10.1103/PhysRevLett.83.4215.
- Wacker CM, Bock M, Hartlep AW, Beck G, van Kaick G, Ertl G, Bauer WR, Schad LR. Changes in myocardial oxygenation and perfusion under pharmacological stress with dipyridamole: assessment using T*2 and T1 measurements. Magn Reson Med. 1999;41:686–695. doi: 10.1002/(SICI)1522-2594(199904)41:4<686::AID-MRM6>;2-9.
- Fieno DS, Shea SM, Li Y, Harris KR, Finn JP, Li D. Myocardial perfusion imaging based on the blood oxygen level-dependent effect using T2-prepared steady-state free-precession magnetic resonance imaging. Circulation. 2004;110:1284–1290. doi: 10.1161/01.CIR.0000140673.13057.34.
- Shea SM, Fieno DS, Schirf BE, Bi X, Huang J, Omary RA, Li D. T2-prepared steady-state free precession blood oxygen level-dependent MR imaging of myocardial perfusion in a dog stenosis model. Radiology. 2005;236:503–509. doi: 10.1148/radiol.2362040149.
- Tsaftaris SA, Zhou X, Tang R, Li D, Dharmakumar R. Detecting myocardial ischemia at rest with cardiac phase-resolved blood oxygen level-dependent cardiovascular magnetic resonance. Circ Cardiovasc Imaging. 2013;6:311–319. doi: 10.1161/CIRCIMAGING.112.976076.
- Bauer WR, Nadler W, Bock M, Schad LR, Wacker C, Hartlep A, Ertl G. Theory of the BOLD effect in the capillary region: an analytical approach for the determination of T2 in the capillary network of myocardium. Magn Reson Med. 1999;41:51–62. doi: 10.1002/(SICI)1522-2594(199901)41:1<51::AID-MRM9>;2-G.
- Vohringer M, Flewitt JA, Green JD, Dharmakumar R, Wang J, Tyberg JV, Friedrich MG. Oxygenation-sensitive CMR for assessing vasodilator-induced changes of myocardial oxygenation. J Cardiovasc Magn Reson. 2010;12:20. doi: 10.1186/1532-429X-12-20.
- Utz W, Jordan J, Niendorf T, Stoffels M, Luft FC, Dietz R, Friedrich MG. Blood oxygen level-dependent MRI of tissue oxygenation: relation to endothelium-dependent and endothelium-independent blood flow changes. Arterioscler Thromb Vasc Biol. 2005;25:1408–1413. doi: 10.1161/01.ATV.0000170131.13683.d7.
- Zheng J, Wang J, Rowold FE, Gropler RJ, Woodard PK. Relationship of apparent myocardial T2 and oxygenation: towards quantification of myocardial oxygen extraction fraction. J Magn Reson Imaging. 2004;20:233–241. doi: 10.1002/jmri.20111.
- McCommis KS, O’Connor R, Lesniak D, Lyons M, Woodard PK, Gropler RJ, Zheng J. Quantification of global myocardial oxygenation in humans: initial experience. J Cardiovasc Magn Reson. 2010;12:34. doi: 10.1186/1532-429X-12-34.
- Guensch DP, Fischer K, Flewitt JA, Friedrich MG. Impact of Intermittent Apnea on Myocardial Tissue Oxygenation – A Study Using Oxygenation-Sensitive Cardiovascular Magnetic Resonance. PLoS One. 2013;8:e53282. doi: 10.1371/journal.pone.0053282.
- Tamura H, Hatazawa J, Toyoshima H, Shimosegawa E, Okudera T. Detection of deoxygenation-related signal change in acute ischemic stroke patients by T2*-weighted magnetic resonance imaging. Stroke. 2002;33:967–971. doi: 10.1161/01.STR.0000013672.70986.E2.
- Morita N, Harada M, Uno M, Matsubara S, Matsuda T, Nagahiro S, Nishitani H. Ischemic findings of T2*-weighted 3-tesla MRI in acute stroke patients. Cerebrovasc Dis. 2008;26:367–375. doi: 10.1159/000151640.
- Brown JM, Wilson WR. Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer. 2004;4:437–447. doi: 10.1038/nrc1367.
- Christen T, Bolar DS, Zaharchuk G. Imaging Brain Oxygenation with. Methods, Validation, and Clinical Applications. AJNR Am J Neuroradiol.: MRI Using Blood Oxygenation Approaches; 2012.
- Wacker CM, Bock M, Hartlep AW, Bauer WR, van Kaick G, Pfleger S, Ertl G, Schad LR. BOLD-MRI in ten patients with coronary artery disease: evidence for imaging of capillary recruitment in myocardium supplied by the stenotic artery. MAGMA. 1999;8:48–54.
- Wacker CM, Hartlep AW, Pfleger S, Schad LR, Ertl G, Bauer WR. Susceptibility-sensitive magnetic resonance imaging detects human myocardium supplied by a stenotic coronary artery without a contrast agent. J Am Coll Cardiol. 2003;41:834–840. doi: 10.1016/S0735-1097(02)02931-5.
- Friedrich MG, Niendorf T, Schulz-Menger J, Gross CM, Dietz R. Blood oxygen level-dependent magnetic resonance imaging in patients with stress-induced angina. Circulation. 2003;108:2219–2223. doi: 10.1161/01.CIR.0000095271.08248.EA.
- Manka R, Paetsch I, Schnackenburg B, Gebker R, Fleck E, Jahnke C. BOLD cardiovascular magnetic resonance at 3.0 tesla in myocardial ischemia. J Cardiovasc Magn Reson. 2010;12:54. doi: 10.1186/1532-429X-12-54.
- Karamitsos TD, Leccisotti L, Arnold JR, Recio-Mayoral A, Bhamra-Ariza P, Howells RK, Searle N, Robson MD, Rimoldi OE, Camici PG, Neubauer S, Selvanayagam JB. Relationship between regional myocardial oxygenation and perfusion in patients with coronary artery disease: insights from cardiovascular magnetic resonance and positron emission tomography. Circ Cardiovasc Imaging. 2010;3:32–40. doi: 10.1161/CIRCIMAGING.109.860148.
- Bernhardt P, Manzke R, Bornstedt A, Gradinger R, Spieß J, Walcher D, Rasche V, Hombach V. Blood oxygen level-dependent magnetic resonance imaging using T2-prepared steady-state free-precession imaging in comparison to contrast-enhanced myocardial perfusion imaging. Int J Cardiol. 2011;147:416–419. doi: 10.1016/j.ijcard.2009.09.547.
- Karamitsos TD, Arnold JR, Pegg TJ, Francis JM, Birks J, Jerosch-Herold M, Neubauer S, Selvanayagam JB. Patients With Syndrome X Have Normal Transmural Myocardial Perfusion and Oxygenation: A 3-T Cardiovascular Magnetic Resonance Imaging Study. Circ Cardiovasc Imaging. 2012;5:194–200. doi: 10.1161/CIRCIMAGING.111.969667.
- Arnold JR, Karamitsos TD, Bhamra-Ariza P, Francis JM, Searle N, Robson MD, Howells RK, Choudhury RP, Rimoldi OE, Camici PG, Banning AP, Neubauer S, Jerosch-Herold M, Selvanayagam JB. Myocardial oxygenation in coronary artery disease: insights from blood oxygen level-dependent magnetic resonance imaging at 3 tesla. J Am Coll Cardiol. 2012;59:1954–1964. doi: 10.1016/j.jacc.2012.01.055.
- Jahnke C, Gebker R, Manka R, Schnackenburg B, Fleck E, Paetsch I. Navigator-gated 3D blood oxygen level-dependent CMR at 3.0-T for detection of stress-induced myocardial ischemic reactions. JACC: Cardiovasc Img. 2010;3:375–384. doi: 10.1016/j.jcmg.2009.12.008.
- Walcher T, Manzke R, Hombach V, Rottbauer W, Wöhrle J, Bernhardt P. Myocardial Perfusion Reserve Assessed by T2-Prepared Steady-State Free-Precession Blood Oxygen Level-Dependent (BOLD) Magnetic Resonance Imaging in Comparison to Fractional Flow Reserve. Imaging: Circ Cardiovasc; 2012. 5:580–6.
- Tsaftaris SA, Tang R, Zhou X, Li D, Dharmakumar R. Ischemic extent as a biomarker for characterizing severity of coronary artery stenosis with blood oxygen-sensitive MRI. J Magn Reson Imaging. 2012.
- Beache GM, Herzka DA, Boxerman JL, Post WS, Gupta SN, Faranesh AZ, Solaiyappan M, Bottomley PA, Weiss JL, Shapiro EP, Hill MN. Attenuated myocardial vasodilator response in patients with hypertensive hypertrophy revealed by oxygenation-dependent magnetic resonance imaging. Circulation. 2001;104:1214–1217. doi: 10.1161/hc3601.096307.
- Karamitsos TD, Dass S, Suttie J, Sever E, Birks J, Holloway CJ, Robson MD, Jerosch-Herold M, Watkins H, Neubauer S. Blunted myocardial oxygenation response during vasodilator stress in patients with hypertrophic cardiomyopathy. J Am Coll Cardiol. 2013;61:1169–1176. doi: 10.1016/j.jacc.2012.12.024.
- Friedrich MG. Testing for myocardial ischemia: the end of surrogates? JACC: Cardiovasc Img. 2010;3:385–387. doi: 10.1016/j.jcmg.2010.02.001.
- Bauer WR, Nadler W, Bock M, Schad LR, Wacker C, Hartlep A, Ertl G. The relationship between the BOLD-induced T(2) and T(2)(*): a theoretical approach for the vasculature of myocardium. Magn Reson Med. 1999;42:1004–1010. doi: 10.1002/(SICI)1522-2594(199912)42:6<1004::AID-MRM2>;2-M.
- Zhou X, Tsaftaris SA, Liu Y, Tang R, Klein R, Zuehlsdorff S, Li D, Dharmakumar R. Artifact-reduced two-dimensional cine steady state free precession for myocardial blood- oxygen-level-dependent imaging. J Magn Reson Imaging. 2010;31:863–871. doi: 10.1002/jmri.22116.
Source: PubMed