Top

Journal of Cardiovascular Magnetic Resonance

Published in:

Open Access 01-12-2013 | Review

Oxygenation-sensitive cardiovascular magnetic resonance

Authors: Matthias G Friedrich, Theodoros D Karamitsos

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2013

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 O₂ 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.

Available only for authorised users

Pauling L, Coryell CD: The Magnetic Properties and Structure of Hemoglobin. Oxyhemoglobin and Carbonmonoxyhemoglobin. Proc Natl Acad Sci USA. 1936, 22: 210-10.1073/pnas.22.4.210.PubMedCentralCrossRefPubMed

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: 9868-72. 10.1073/pnas.87.24.9868.PubMedCentralCrossRefPubMed

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: 5951-55. 10.1073/pnas.89.13.5951.PubMedCentralCrossRefPubMed

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: 988-98. 10.1002/mrm.1910390617.PubMedCentralCrossRefPubMed

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: 1089-97. 10.1002/mrm.10467.CrossRefPubMed

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: 180-88. 10.1097/01.rli.0000254407.26068.54.CrossRefPubMed

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: 561-70. 10.1002/mrm.21511.CrossRefPubMed

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: 1037-45. 10.1002/jmri.21345.CrossRefPubMed

Atalay MK, Forder JR, Chacko VP, Kawamoto S, Zerhouni EA: Oxygenation in the rabbit myocardium: assessment with susceptibility-dependent MR imaging. Radiology. 1993, 189: 759-64. 10.1148/radiology.189.3.8234701.CrossRefPubMed

10.

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: 273-76. 10.1002/mrm.1910290220.CrossRefPubMed

11.

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. 10.1002/mrm.1910360114.CrossRefPubMed

12.

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. 10.1002/mrm.1910360105.CrossRefPubMed

13.

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: 4215-18. 10.1103/PhysRevLett.83.4215.CrossRef

14.

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: 686-95. 10.1002/(SICI)1522-2594(199904)41:4<686::AID-MRM6>3.0.CO;2-9.CrossRefPubMed

15.

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: 1284-90. 10.1161/01.CIR.0000140673.13057.34.CrossRefPubMed

16.

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: 503-09. 10.1148/radiol.2362040149.CrossRefPubMed

17.

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: 311-19. 10.1161/CIRCIMAGING.112.976076.PubMedCentralCrossRefPubMed

18.

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. 10.1002/(SICI)1522-2594(199901)41:1<51::AID-MRM9>3.0.CO;2-G.CrossRefPubMed

19.

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: 20-10.1186/1532-429X-12-20.PubMedCentralCrossRefPubMed

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: 1408-13. 10.1161/01.ATV.0000170131.13683.d7.CrossRefPubMed

21.

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: 233-41. 10.1002/jmri.20111.CrossRefPubMed

22.

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: 34-10.1186/1532-429X-12-34.PubMedCentralCrossRefPubMed

23.

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: e53282-10.1371/journal.pone.0053282.PubMedCentralCrossRefPubMed

24.

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: 967-71. 10.1161/01.STR.0000013672.70986.E2.CrossRefPubMed

25.

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: 367-75. 10.1159/000151640.CrossRefPubMed

26.

Brown JM, Wilson WR: Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer. 2004, 4: 437-47. 10.1038/nrc1367.CrossRefPubMed

27.

Christen T, Bolar DS, Zaharchuk G: Imaging Brain Oxygenation with. 2012, Methods, Validation, and Clinical Applications. AJNR Am J Neuroradiol.: MRI Using Blood Oxygenation Approaches

28.

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. 10.1007/BF02590635.CrossRefPubMed

29.

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: 834-40. 10.1016/S0735-1097(02)02931-5.CrossRefPubMed

30.

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: 2219-23. 10.1161/01.CIR.0000095271.08248.EA.CrossRefPubMed

31.

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: 54-10.1186/1532-429X-12-54.PubMedCentralCrossRefPubMed

32.

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.CrossRefPubMed

33.

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: 416-19. 10.1016/j.ijcard.2009.09.547.CrossRefPubMed

34.

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. 10.1161/CIRCIMAGING.111.969667.CrossRefPubMed

35.

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: 1954-64. 10.1016/j.jacc.2012.01.055.CrossRefPubMed

36.

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: 375-84. 10.1016/j.jcmg.2009.12.008.

37.

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. 2012, Imaging: Circ Cardiovasc, 5:580–6

38.

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

39.

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: 1214-17. 10.1161/hc3601.096307.CrossRefPubMed

40.

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: 1169-76. 10.1016/j.jacc.2012.12.024.PubMedCentralCrossRefPubMed

41.

Friedrich MG: Testing for myocardial ischemia: the end of surrogates?. JACC: Cardiovasc Img. 2010, 3: 385-87. 10.1016/j.jcmg.2010.02.001.

42.

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: 1004-10. 10.1002/(SICI)1522-2594(199912)42:6<1004::AID-MRM2>3.0.CO;2-M.CrossRefPubMed

43.

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: 863-71. 10.1002/jmri.22116.PubMedCentralCrossRefPubMed

Title: Oxygenation-sensitive cardiovascular magnetic resonance
Authors: Matthias G Friedrich
Theodoros D Karamitsos
Publication date: 01-12-2013
Publisher: BioMed Central
Published in: Journal of Cardiovascular Magnetic Resonance / Issue 1/2013
Electronic ISSN: 1532-429X
DOI: https://doi.org/10.1186/1532-429X-15-43

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Oxygenation-sensitive cardiovascular magnetic resonance

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2013

Cardiovascular magnetic resonance with an MR compatible pacemaker

In-vivo quantitative T2 mapping of carotid arteries in atherosclerotic patients: segmentation and T2 measurement of plaque components

A novel technique to quantify the instantaneous mitral regurgitant rate

Normal variation of magnetic resonance T1 relaxation times in the human population at 1.5 T using ShMOLLI

Comparison of diffusion-weighted with T2-weighted imaging for detection of edema in acute myocardial infarction

Pediatric cardiovascular interventional devices: effect on CMR images at 1.5 and 3 Tesla