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.