Selection of Papers on Oxygenation-Sensitive Magnetic Resonance
1.Principles and Physiology
Pernett F, Bergenhed P, Holmström P, Mulder E, Schagatay E. Effects of hyperventilation on oxygenation, apnea breaking points, diving response, and spleen contraction during serial static apneas. Eur J Appl Physiol. 2023. doi:10.1007/s00421-023-05202-7
Das RR, Sankar J, Kabra SK. Role of breathing exercises in asthma-yoga and pranayama. Indian J Pediatr. 2021. doi:10.1007/s12098-021-03998-w
Eberlein HJ. Koronardurchblutung und Sauerstoffversorgung des Herzens unter verschiedenen CO2-Spannungen und Anästhetika. Archiv für Kreislaufforschung. 1966;50: 18–86.
Kety SS, Schmidt CF. The effects of active and passive hyperventilation on cerebral blood flow, cerebral oxygen consumption, cardiac output, and blood pressure of normal young men. J Clin Invest. 1946;25: 107–119.
2. Other OS-CMR Methods
Alogna A, Faragli A, Kolp C, Doeblin P, Tanacli R, Confortola G, et al. Blood-oxygen level dependent (BOLD) T2-mapping reflects invasively measured central venous oxygen saturation in cardiovascular patients. JACC Cardiovasc Imaging. 2022. doi:10.1016/j.jcmg.2022.08.020
Van den Boomen M, Manhard MK, Snel GJH, Han S, Emblem KE, Slart RHJA, et al. Blood Oxygen Level–Dependent MRI of the Myocardium with Multiecho Gradient-Echo Spin-Echo Imaging. Radiology. 2020;294: 538–545.
Ochs MM, Kajzar I, Salatzki J, Ochs AT, Riffel J, Osman N, et al. Hyperventilation/Breath Hold Maneuver to Detect Myocardial Ischemia by Strain-Encoded CMR: Diagnostic Accuracy of a Needle-Free Stress Protocol. JACC Cardiovasc Imaging. 2021. doi:10.1016/j.jcmg.2021.02.022
Kastrup A, Li TQ, Takahashi A, Glover GH, Moseley ME. Functional magnetic resonance imaging of regional cerebral blood oxygenation changes during breath holding. Stroke. 1998;29: 2641–2645.
Posse S, Olthoff U, Weckesser M, Jäncke L, Müller-Gärtner HW, Dager SR. Regional dynamic signal changes during controlled hyperventilation assessed with blood oxygen level-dependent functional MR imaging. AJNR Am J Neuroradiol. 1997;18: 1763–1770.
Ardissino D, De Servi S, Barberis P, Demicheli G, Falcone C, Ochan M, et al. Significance of hyperventilation-induced ST segment depression in patients with coronary artery disease. J Am Coll Cardiol. 1989;13: 804–810.
3. Breathing-Enhanced OS-CMR with SSFP – Methodology and Analysi
Plasa G, Hillier E, Luu J, Boutet D, Benovoy M, Friedrich MG. Automated Data Transformation and Feature Extraction for Oxygenation-Sensitive Cardiovascular Magnetic Resonance Images. J Cardiovasc Transl Res. 2024. doi:10.1007/s12265-023- 10474-7.
Kokotov A, Chetrit M, Friedrich MG, Benovoy M. Machine learning for automated detection of normal and abnormal strain in oxygenation-sensitive cardiovascular magnetic resonance (OS-CMR) of patients with chronic ischemic cardiomyopathy. J Cardiovasc Magn Reson. 2024;26: 100959. [abstract]
Hillier E, Covone J, Friedrich MG. The reproducibility of breathing maneuvers as a vasoactive stimulus in the heart: an oxygenation-sensitive resonance imaging study. J Cardiovasc Magn Reson. 2023;25: 1–5.
Hillier E, Covone J, Friedrich MG. Oxygenation-sensitive Cardiac MRI with Vasoactive Breathing Maneuvers for the Non-invasive Assessment of Coronary Microvascular Dysfunction. Journal of Visualized Experiments. 2022. doi:10.3791/64149
4. Experimental Studies
Hopman LHGA, Hillier E, Liu Y, Hamilton J, Fischer K, Seiberlich N, et al. Dynamic Cardiac Magnetic Resonance Fingerprinting During Vasoactive Breathing Maneuvers: First Results. J Cardiovasc Imaging. 2023;31: 71–82.
Guensch DP, Michel MC, Huettenmoser SP, Jung B, Gulac P, Segiser A, et al. The blood oxygen level dependent (BOLD) effect of in-vitro myoglobin and hemoglobin. Sci Rep. 2021;11: 11464.
Guensch DP, Fischer K, Jung C, Hurni S, Winkler BM, Jung B, et al. Relationship between myocardial oxygenation and blood pressure: Experimental validation using oxygenation sensitive cardiovascular magnetic resonance. PLoS One. 2019;14: e0210098. doi:10.1371/journal.pone.0210098
Fischer K, Guensch DP, Shie N, Lebel J, Friedrich MG. Breathing Maneuvers as a Vasoactive Stimulus for Detecting Inducible Myocardial Ischemia – An Experimental Cardiovascular Magnetic Resonance Study. PLoS One. 2016;11: e0164524.
Guensch DP, Fischer K, Shie N, Lebel J, Friedrich MG. Hyperoxia Exacerbates Myocardial Ischemia in the Presence of Acute Coronary Artery Stenosis in Swine. Circ Cardiovasc Interv. 2015;8: e002928.
Guensch DP, Fischer K, Flewitt JA, Friedrich MG. Myocardial oxygenation is maintained during hypoxia when combined with apnea – a cardiovascular MR study. Physiol Rep. 2013;1: e00098.
5. Pre-Clinical OS-CMR Studies
Guensch DP, Nadeshalingam G, Fischer K, Stalder AF, Friedrich MG. The impact of hematocrit on oxygenation-sensitive cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2016;18: 42.
Fischer K, Guensch DP, Friedrich MG. Response of myocardial oxygenation to breathing manoeuvres and adenosine infusion. Eur Heart J Cardiovasc Imaging. 2015;16: 395–401
Fischer K, Guensch DP, Friedrich MG. Breathing maneuvers may elicit a stronger myocardial vascular response than clinical adenosine protocols. J Cardiovasc Magn Reson. 2014;16: 1–2.
Nadeshalingam G, Guensch DP, Fischer K, Friedrich MG. EFFECTS OF THE HYDRATION STATUS ON OXYGENATION-SENSITIVE CARDIOVASCULAR MAGNETIC RESONANCE IMAGING. Can J Card. 2014. p. S174. doi:10.1016/j.cjca.2014.07.271 [abstract]
Guensch DP, Fischer K, Flewitt JA, Yu J, Lukic R, Friedrich JA, et al. Breathing manoeuvre-dependent changes in myocardial oxygenation in healthy humans. Eur Heart J Cardiovasc Imaging. 2014;15: 409–414.
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.
6. Clinical Studies OS-CMR without Breathing Manoeuvres
Zhou Z, Xu R, Cai X, Fu H, Xu K, Yuan W, et al. Association Between Myocardial Oxygenation and Fibrosis in Duchenne Muscular Dystrophy: Analysis by Rest Oxygenation-Sensitive Magnetic Resonance Imaging. J Magn Reson Imaging. 2024. doi:10.1002/jmri.29273
Hillier E, Dignowity L, Luu J, Plasa G, Palmer C, Friedrich MG, Quesada O. Coronary vascular and structural function in females with a history of pre-eclampsia—an oxygenation-sensitive cardiovascular magnetic resonance imaging study. J Cardiovasc Magn Reson. 2024;26: 100384. [abstract]
Guensch DP, Utz CD, Jung B, Dozio S, Huettenmoser SP, Friess JO, et al. Introducing a free-breathing MRI method to assess peri-operative myocardial oxygenation and function: A volunteer cohort study. Eur J Anaesthesiol. 2024;41: 480–489.
Raman B, Chan K, Mahmod M, Hundertmark M, Ariga R, Sivalokanathan S, et al. Stress myocardial oxygenation and not perfusion reserve determines arrhythmic risk in hypertrophic cardiomyopathy: insights from a novel oxygen-sensitive CMR approach. Heart. 2019;105: A183–A183. [abstract]
Raman KS, Grover S, Woodman R. Myocardial Oxygenation in Hibernating Myocardium: Insights from Oxygen-Sensitive (OS) Cardiac Magnetic Resonance Imaging (CMR). Heart Lung333 Circ 2019. [abstract]
Luu JM, Schmidt A, Flewitt J, Mikami Y, Ter Keurs H, Friedrich MG. Cardiovascular risk is associated with a transmural gradient of myocardial oxygenation during adenosine infusion. Eur Heart J Cardiovasc Imaging. 2019;20: 1287–1295.
Mahmod M, Francis JM, Pal N, Lewis A, Dass S, De Silva R, et al. Myocardial perfusion and oxygenation are impaired during stress in severe aortic stenosis and correlate with impaired energetics and subclinical left ventricular dysfunction. J Cardiovasc Magn Reson. 2014;16: 29.
Fischer K, Guensch DP, Shie N, Friedrich MG. The relationship of myocardial oxygenation to coronary flow and oxygen saturation during CO2 manipulations. J Cardiovasc Magn Res. 2014. doi:10.1186/1532-429x-16-s1-o110
Luu J, Schmidt A, Flewitt J, Howarth AG, Friedrich MG. Transmural variations of vasodilator-induced changes of myocardial oxygenation vary with age and the presence of diabetes mellitus type II: a study using oxygen-sensitive cardiovascular MR. J Cardiovasc Magn Reson. 2013;15. doi:10.1186/1532-429x-15-s1-p132
Karamitsos TD, Arnold JR, Pegg TJ, Francis JM, Birks J, Jerosch-Herold M, et al. 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.
Arnold JR, Karamitsos TD, Bhamra-Ariza P, Francis JM, Searle N, Robson MD, et al. 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.
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;35: 1338–1348.
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 magnetic resonance imaging in comparison to fractional flow reserve. Circ Cardiovasc Imaging. 2012;5: 580–586. doi:10.1161/CIRCIMAGING.111.971507
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.
7. Clinical Studies OS-CMR with Breathing Manoeuvres
Hillier E, Elharram M, White JA, Anderson T, Luu J, Labib D, et al. Heterogeneity of Coronary Vascular Function and Myocardial Oxygenation in Women with Angina and Non-obstructive Coronary Artery Disease. Eur Heart J Cardiovasc Imaging. 2024; jeae076.
Lindsay K, Hillier E, Luu J, Plasa G, Benovoy M, Leo M, et al. The breathing-induced myocardial oxygenation reserve as a marker for vascular function in metabolic syndrome. J Cardiovasc Magn Reson. 2024;26: 100301. [abstract]
Shi K, Yang M-X, Xia C-C, Peng W-L, Zhang K, Li Z-L, et al. Noninvasive oxygenation assessment after acute myocardial infarction with breathing maneuvers-induced oxygenation-sensitive magnetic resonance imaging. J Magn Reson Imaging. 2021;54: 284– 289.
Hillier E, Luu J, Plasa G, Palmer C, Moukarzel M, Lindsay K, et al. Coronary vascular function in females with history of hypertensive disorders of pregnancy an oxygenation sensitive cardiovascular magnetic resonance imaging study. Eur Heart J. 2023;44: ehad655.165. [abstract]
Siry, D., Riffel, J.H., Salatzki, J. et al. Hyperventilation strain CMR imaging in patients with acute chest pain. Sci Rep 12, 13584 (2022). https://doi.org/10.1038/s41598-022- 17856-y
Fischer K, Guensch DP, Jung B, King I, von Tengg-Kobligk H, Giannetti N, et al. Insights Into Myocardial Oxygenation and Cardiovascular Magnetic Resonance Tissue Biomarkers in Heart Failure With Preserved Ejection Fraction. Circ Heart Fail. 2022;15: e008903.
Spicher B, Fischer K, Zimmerli ZA, Yamaji K, Ueki Y, Bertschinger CN, et al. Combined Analysis of Myocardial Deformation and Oxygenation Detects Inducible Ischemia Unmasked by Breathing Maneuvers in Chronic Coronary Syndrome. Front Cardiovasc Med. 2022;9: 800720.
Iannino N, Fischer K, Friedrich M, Hafyane T, Mongeon F-P, White M. Myocardial Vascular Function Assessed by Dynamic Oxygenation-sensitive Cardiac Magnetic Resonance Imaging Long-term Following Cardiac Transplantation. Transplantation. 2021;105: 1347–1355.
Elharram M, Hillier E, Hawkins S, Mikami Y, Heydari B, Merchant N, et al. Regional Heterogeneity in the Coronary Vascular Response in Women With Chest Pain and Nonobstructive Coronary Artery Disease. Circulation. 2021;143: 764–766.
Hillier, E., Hawkins, S. & Friedrich, M. HEALTHY AGING REDUCES THE MYOCARDIAL OXYGENATION RESERVE AS ASSESSED WITH OXYGENATION SENSITIVE CMR. Canadian Journal of Cardiology vol. 35 S81 (2019) [abstract]
Fischer K, Yamaji K, Luescher S, Ueki Y, Jung B, von Tengg-Kobligk H, et al. Feasibility of cardiovascular magnetic resonance to detect oxygenation deficits in patients with multi vessel coronary artery disease triggered by breathing maneuvers. J Cardiovasc Magn Reson. 2018;20: 31.
Roubille F, Fischer K, Guensch DP, Tardif J-C, Friedrich MG. Impact of hyperventilation and apnea on myocardial oxygenation in patients with obstructive sleep apnea – An oxygenation-sensitive CMR study. J Cardiol. 2017;69: 489–494.
Stalder AF, Schmidt M, Greiser A, Speier P, Guehring J, Friedrich MG, et al. Robust cardiac BOLD MRI using an fMRI-like approach with repeated stress paradigms. Magn Reson Med. 2015;73: 577–585.
8. Studies in other organ systems
Moukarzel M, Hillier E, Benovoy M, Covone J, Leo M, Friedrich MG. Breathing induced myocardial and cerebral oxygenation in generalized anxiety disorders. J Cardiovasc Magn Reson. 2024;26: 100283. [abstract]
Kennedy KG, Ghugre NR, Roifman I, Qi X, Saul K, McCrindle BW, et al. Impaired coronary microvascular reactivity in youth with bipolar disorder. Psychol Med. 2023; 1–11.
Moriyama S, Ichinose M, Dobashi K, Matsutake R, Sakamoto M, Fujii N, et al. Hypercapnia elicits differential vascular and blood flow responses in the cerebral circulation and active skeletal muscles in exercising humans. Physiol Rep. 2022;10: e15274.
Suo S, Tang H, Lu Q, Zhang L, Ni Q, Cao M, et al. Blood oxygenation level-dependent cardiovascular magnetic resonance of the skeletal muscle in healthy adults: Different paradigms for provoking signal alterations. Magn Reson Med. 2021;85: 1590–1601.
Shah R, Parnham S, Liang Z, Perry R, Bradbrook C, Smith E, et al. Prognostic utility of oxygen-sensitive cardiac magnetic resonance imaging in diabetic and nondiabetic chronic kidney disease patients with no known coronary artery disease. JACC Cardiovasc Imaging. 2019;12: 1107–1109. doi:10.1016/j.jcmg.2018.12.014 [letter]
Parnham S, Gleadle JM, Bangalore S, Grover S, Perry R, Woodman RJ, et al. Impaired Myocardial Oxygenation Response to Stress in Patients With Chronic Kidney Disease. J Am Heart Assoc. 2015;4: e002249.
Zhu Y-S, Tarumi T, Tseng BY, Palmer DM, Levine BD, Zhang R. Cerebral vasomotor reactivity during hypo- and hypercapnia in sedentary elderly and Masters athletes. J Cereb Blood Flow Metab. 2013;33: 1190–1196.
Klarhöfer M, Madörin P, Bilecen D, Scheffler K. Assessment of muscle oxygenation with balanced SSFP: a quantitative signal analysis. J Magn Reson Imaging. 2008;27: 1169– 1174.
Ledermann H-P, Schulte A-C, Heidecker H-G, Aschwanden M, Jäger KA, Scheffler K, et al. Blood oxygenation level-dependent magnetic resonance imaging of the skeletal muscle in patients with peripheral arterial occlusive disease. Circulation. 2006;113: 2929–2935
Utz W, Jordan J, Niendorf T, Stoffels M, Luft FC, Dietz R, et al. 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.
9. Reviews and Editorials
Covone J. The Utility and Reproducibility of Oxygenation-sensitive MRI with Vasoactive Breathing Maneuvers to Assess Coronary and Cerebral Vascular Function in Patients with Heart Failure. Thesis. McGill University Libraries; 2022.
Hillier E, Friedrich MG. The Potential of Oxygenation-Sensitive CMR in Heart Failure. Curr Heart Fail Rep. 2021;18: 304–314.
Friedrich MG. Tracking Myocardial Oxygenation over a Breath Hold with Blood Oxygen Level-Dependent MRI: A Radically Different Approach to Study Ischemia. Radiology. 2020. pp. 546–547.
Sree Raman K, Nucifora G, Selvanayagam JB. Novel cardiovascular magnetic resonance oxygenation approaches in understanding pathophysiology of cardiac diseases. Clin Exp Pharmacol Physiol. 2018;45: 475–480
Guensch DP, Friedrich MG. Novel Approaches to Myocardial Perfusion: 3D First-Pass CMR Perfusion Imaging and Oxygenation-Sensitive CMR. Curr Cardiovasc Imaging Rep. 2014;7: 9261.
Friedrich MG, Karamitsos TD. Oxygenation-sensitive cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2013;15: 43.
10. Patient and Physician Preferences
Bertrand T, Bartlett-Esquilant G, Fischer K, Friedrich MG. Patient and physician preferences for non-invasive diagnostic cardiovascular imaging technologies: a discrete choice experiment. J Patient Rep Outcomes. 2022;6: 15.