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The Potential of Oxygenation-Sensitive CMR in Heart Failure

  • Imaging in Heart Failure (J. Schulz-Menger, Section Editor)
  • Published:
Current Heart Failure Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

Cardiac magnetic resonance imaging (CMR) use in the context of heart failure (HF) has increased over the last decade as it is able to provide detailed, quantitative information on function, morphology, and myocardial tissue composition. Furthermore, oxygenation-sensitive CMR (OS-CMR) has emerged as a CMR imaging method capable of monitoring changes of myocardial oxygenation without the use of exogenous contrast agents.

Recent Findings

The contributions of OS-CMR to the investigation of patients with HF includes not only a fully quantitative assessment of cardiac morphology, function, and tissue characteristics, but also high-resolution information on both endothelium-dependent and endothelium-independent vascular function as assessed through changes of myocardial oxygenation.

Summary

In patients with heart failure, OS-CMR can provide deep phenotyping on the status and important associated pathophysiology as a one-stop, needle-free diagnostic imaging test.

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References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Murphy SP, Ibrahim NE, Januzzi JL Jr. Heart failure with reduced ejection fraction: a review. JAMA. 2020;324(5):488–504.

    Article  PubMed  Google Scholar 

  2. Ferreira JP, Kraus S, Mitchell S, Perel P, Piñeiro D, Chioncel O, et al. World Heart Federation roadmap for heart failure. Glob Heart. 2019;14(3):197–214.

    Article  PubMed  Google Scholar 

  3. Braunwald E. Heart failure. JACC Heart Fail. 2013;1(1):1–20.

    Article  PubMed  Google Scholar 

  4. Bozkurt B, Coats AJ, Tsutsui H, Abdelhamid M, Adamopoulos S, Albert N, et al. Universal definition and classification of heart failure: a report of the Heart Failure Society of America, Heart Failure Association of the European Society of Cardiology, Japanese Heart Failure Society and Writing Committee of the Universal Definition of Heart Failure. J Card Fail. 2021 1;

  5. Lopatin Y. Heart failure with mid-range ejection fraction and how to treat it. Card Fail Rev. 2018;4(1):9–13.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Chioncel O, Lainscak M, Seferovic PM, Anker SD, Crespo-Leiro MG, Harjola V-P, et al. Epidemiology and one-year outcomes in patients with chronic heart failure and preserved, mid-range and reduced ejection fraction: an analysis of the ESC Heart Failure Long-Term Registry. Eur J Heart Fail. 2017;19(12):1574–85.

    Article  CAS  PubMed  Google Scholar 

  7. Rastogi A, Novak E, Platts AE, Mann DL. Epidemiology, pathophysiology and clinical outcomes for heart failure patients with a mid-range ejection fraction. Eur J Heart Fail. 2017;19(12):1597–605.

    Article  CAS  PubMed  Google Scholar 

  8. Cowie MR, Anker SD, Cleland JGF, Felker GM, Filippatos G, Jaarsma T, et al. Improving care for patients with acute heart failure: before, during and after hospitalization. ESC Heart Fail. 2014;1(2):110–45.

    Article  PubMed  Google Scholar 

  9. Čerlinskaitė K, Javanainen T, Cinotti R, Mebazaa A. Acute heart failure management. Korean Circ J. 2018;48(6):463–80.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Sado DM, Hasleton JM, Herrey AS, Moon JC. CMR in Heart Failure [Internet]. Vol. 2011, Cardiology Research and Practice. Hindawi; 2011 [cited 2021 Feb 8]. p. e739157. Available from: https://www.hindawi.com/journals/crp/2011/739157/

  11. Le Ven F, Bibeau K, De Larochellière É, Tizón-Marcos H, Deneault-Bissonnette S, Pibarot P, et al. Cardiac morphology and function reference values derived from a large subset of healthy young Caucasian adults by magnetic resonance imaging. Eur Heart J Cardiovasc Imaging. 2016;17(9):981–90.

    Article  PubMed  Google Scholar 

  12. Karamitsos TD. Arvanitaki Alexandra, Karvounis Haralambos, Neubauer Stefan, Ferreira Vanessa M. Myocardial tissue characterization and fibrosis by imaging. JACC Cardiovasc Imaging. 2020;13(5):1221–34.

    Article  PubMed  Google Scholar 

  13. Barison A, Aimo A, Todiere G, Grigoratos C, Aquaro GD, Emdin M. Cardiovascular magnetic resonance for the diagnosis and management of heart failure with preserved ejection fraction. Heart Fail Rev [Internet]. 2020 22 [cited 2021 Feb 8]; Available from. https://doi.org/10.1007/s10741-020-09998-w.

  14. Mitropoulou P, Georgiopoulos G, Figliozzi S, Klettas D, Nicoli F, Masci PG. Multi-modality imaging in dilated cardiomyopathy: with a focus on the role of cardiac magnetic resonance. Front Cardiovasc Med [Internet]. 2020 [cited 2021 Feb 19];7. Available from. https://doi.org/10.3389/fcvm.2020.00097/full.

  15. Simpson R, Bromage D, Dancy L, McDiarmid A, Monaghan M, McDonagh T, et al. 6 Comparing echocardiography and cardiac magnetic resonance measures of ejection fraction: implications for HFMRF research. Heart. 2018;104(Suppl 5):A3.

    Google Scholar 

  16. Paterson D. Ian, Wells George, Erthal Fernanda, Mielniczuk Lisa, O’Meara Eileen, White James, et al. Outsmart hf Circulation. 2020;141(10):818–27.

    Article  PubMed  Google Scholar 

  17. Kanagala P, Cheng ASH, Singh A, McAdam J, Marsh A-M, Arnold JR, et al. Diagnostic and prognostic utility of cardiovascular magnetic resonance imaging in heart failure with preserved ejection fraction – implications for clinical trials. J Cardiovasc Magn Reson. 2018;20(1):4.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Taqueti VR, Di Carli MF. Coronary microvascular disease pathogenic mechanisms and therapeutic options: JACC State-of-the-Art Review. J Am Coll Cardiol. 2018;72(21):2625–41.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Katz SD, Katarzyna H, Ingrid H, Kujtim B, Clarito D, Alhakam H, et al. Vascular endothelial dysfunction and mortality risk in patients with chronic heart failure. Circulation. 2005;111(3):310–4.

    Article  PubMed  Google Scholar 

  20. Giannotti G, Landmesser U. Endothelial dysfunction as an early sign of atherosclerosis. Herz. 2007;32(7):568–72.

    Article  PubMed  Google Scholar 

  21. Shah SJ, Lam CSP, Svedlund S, Saraste A, Hage C, Tan R-S, et al. Prevalence and correlates of coronary microvascular dysfunction in heart failure with preserved ejection fraction: PROMIS-HFpEF. Eur Heart J. 2018;39(37):3439–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Dryer K, Gajjar M, Narang N, Lee M, Paul J, Shah AP, et al. Coronary microvascular dysfunction in patients with heart failure with preserved ejection fraction. Am J Physiol-Heart Circ Physiol. 2018;314(5):H1033–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zuchi C, Tritto I, Carluccio E, Mattei C, Cattadori G, Ambrosio G. Role of endothelial dysfunction in heart failure. Heart Fail Rev. 2020;25(1):21–30. This paper reviews the role of endothelial dysfunction, notably alteraed endothelium dependent vasodilatation mechanisms, in the pathophysiology of heart failure and its association with worse prognosis and higher rates of cardiovascular events.

  24. Franssen C, Chen S, Unger A, Korkmaz HI, De Keulenaer GW, Tschöpe C, et al. Myocardial microvascular inflammatory endothelial activation in heart failure with preserved ejection fraction. JACC Heart Fail. 2016;4(4):312–24.

    Article  PubMed  Google Scholar 

  25. 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(1):e53282.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 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(10):e0164524.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. 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(1):31. This study demonstrated the feasibility of oxygenation-sensitive CMR with standardized vasoactive breathing maneuvers to identify regional myocardial oxygenation abnormalities in patients with coronary artery disease.

  28. Friedrich MG, Karamitsos TD. Oxygenation-sensitive cardiovascular magnetic resonance. J Cardiovasc Magn Reson Off J Soc Cardiovasc Magn Reson. 2013;15:43.

    Google Scholar 

  29. Vöhringer M, Flewitt JA, Green JD, Dharmakumar R, Wang J, Tyberg JV, et al. Oxygenation-sensitive CMR for assessing vasodilator-induced changes of myocardial oxygenation. J Cardiovasc Magn Reson. 2010;12(1):20.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Raman KS, Nucifora G, Selvanayagam JB. Novel cardiovascular magnetic resonance oxygenation approaches in understanding pathophysiology of cardiac diseases. Clin Exp Pharmacol Physiol. 2018;45(5):475–80.

    Article  CAS  Google Scholar 

  31. Karamitsos TD, Dass S, Suttie J, Sever E, Birks J, Holloway CJ, et al. Blunted myocardial oxygenation response during vasodilator stress in patients with hypertrophic cardiomyopathy. J Am Coll Cardiol. 2013;61(11):1169–76.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Sairia D, Holloway CJ, Cochlin LE, Rider OJ, Masliza M, Matthew R, et al. No evidence of myocardial oxygen deprivation in nonischemic heart failure. Circ Heart Fail. 2015;8(6):1088–93.

    Article  CAS  Google Scholar 

  33. 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(1):29.

    Article  PubMed  PubMed Central  Google Scholar 

  34. 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(2):489–94.

    Article  PubMed  Google Scholar 

  35. 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(7):764–6. Novel biomarkers derived from oxygenation-sensitive CMR images with breathing maneuvers as a vasoactive stress identified regional heterogeneity in the mypcardial oxygenation reserve of women with ischemia and no obstructive coronary artery stenosis, which may highlight underlying vascular dysfunction in this poorly understood patient population.

  36. 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. Transpl Int. 2021; 16 [cited 2021 Feb 19];Online First. Available from: https://journals.lww.com/transplantjournal/Abstract/9000/Myocardial_Vascular_Function_Assessed_by_Dynamic.95567.aspx.

  37. Ogawa S, Lee TM, Kay AR, Tank DW. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci U S A. 1990;87(24):9868–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci U S A. 1992;89(13):5951–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Ogawa S, Lee TM, Nayak AS, Glynn P. Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields. Magn Reson Med. 1990;14(1):68–78.

    Article  CAS  PubMed  Google Scholar 

  40. Rostrup E, Knudsen GM, Law I, Holm S, Larsson HBW, Paulson OB. The relationship between cerebral blood flow and volume in humans. NeuroImage. 2005;24(1):1–11.

    Article  PubMed  Google Scholar 

  41. Bauer WR, Nadler W, Bock M, Schad LR, Wacker C, Hartlep A, et al. Theory of the BOLD effect in the capillary region: an analytical approach for the determination of T*2 in the capillary network of myocardium. Magn Reson Med. 1999;41(1):51–62.

    Article  CAS  PubMed  Google Scholar 

  42. Wacker CM, Bock M, Hartlep AW, Beck G, van Kaick G, Ertl G, et al. Changes in myocardial oxygenation and perfusion under pharmacological stress with dipyridamole: assessment using T*2 and T1 measurements. Magn Reson Med. 1999;41(4):686–95.

    Article  CAS  PubMed  Google Scholar 

  43. 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(4):409–14.

    Article  PubMed  Google Scholar 

  44. Duncker DJ, Bache RJ. Regulation of coronary blood flow during exercise. Physiol Rev. 2008 Jul;88(3):1009–86.

    Article  CAS  PubMed  Google Scholar 

  45. Fischer K, Guensch DP, Friedrich MG. Response of myocardial oxygenation to breathing manoeuvres and adenosine infusion. Eur Heart J Cardiovasc Imaging. 2015;16(4):395–401.

    Article  PubMed  Google Scholar 

  46. Moreton FC, Dani KA, Goutcher C, O’Hare K, Muir KW. Respiratory challenge MRI: Practical aspects. NeuroImage Clin. 2016;11:667–77.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Udelson JE. Cardiac magnetic resonance imaging for long-term prognosis in heart failure. Circ Cardiovasc Imaging. 2018;11(9):e008264.

    Article  PubMed  Google Scholar 

  48. Maggioni AP, Dahlström U, Filippatos G, Chioncel O, Crespo Leiro M, Drozdz J, et al. EURObservational Research Programme: regional differences and 1-year follow-up results of the Heart Failure Pilot Survey (ESC-HF Pilot). Eur J Heart Fail. 2013;15(7):808–17.

    Article  PubMed  Google Scholar 

  49. Pilz G, Patel PA, Fell U, Ladapo JA, Rizzo JA, Fang H, et al. Adenosine-stress cardiac magnetic resonance imaging in suspected coronary artery disease: a net cost analysis and reimbursement implications. Int J Card Imaging. 2011;27(1):113–21.

    Article  Google Scholar 

  50. Kwong RY. Ge Yin, Steel Kevin, Bingham Scott, Abdullah Shuaib, Fujikura Kana, et al. Cardiac magnetic resonance stress perfusion imaging for evaluation of patients with chest pain. J Am Coll Cardiol. 2019;74(14):1741–55.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Nagel E, Greenwood JP, McCann GP, Bettencourt N, Shah AM, Hussain ST, et al. Magnetic resonance perfusion or fractional flow reserve in coronary disease. N Engl J Med. 2019;380(25):2418–28.

    Article  PubMed  Google Scholar 

  52. 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(1):54.

    Article  PubMed  PubMed Central  Google Scholar 

  53. 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(5):580–6.

    Article  PubMed  Google Scholar 

  54. Karamitsos TD, Leccisotti L, Arnold JR, Recio-Mayoral A, Bhamra-Ariza P, Howells RK, et al. 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(1):32–40.

    Article  PubMed  Google Scholar 

  55. 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(22):1954–64.

    Article  PubMed  Google Scholar 

  56. Luu JM, Friedrich MG, Harker J, Dwyer N, Guensch D, Mikami Y, et al. Relationship of vasodilator-induced changes in myocardial oxygenation with the severity of coronary artery stenosis: a study using oxygenation-sensitive cardiovascular magnetic resonance. Eur Heart J Cardiovasc Imaging. 2014;15(12):1358–67.

    Article  PubMed  Google Scholar 

  57. Maron DJ, Hochman JS, Reynolds HR, Bangalore S, O’Brien SM, Boden WE, et al. Initial invasive or conservative strategy for stable coronary disease. N Engl J Med. 2020;382(15):1395–407.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Bernhardt P, Manzke R, Bornstedt A, Gradinger R, Spiess J, Walcher D, et al. 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(3):416–9.

    Article  PubMed  Google Scholar 

  59. Shantsila E, Wrigley BJ, Blann AD, Gill PS, Lip GYH. A contemporary view on endothelial function in heart failure. Eur J Heart Fail. 2012;14(8):873–81.

    Article  CAS  PubMed  Google Scholar 

  60. Hasdai D, Cannan CR, Mathew V, Holmes DR, Lerman A. Evaluation of patients with minimally obstructive coronary artery disease and angina. Int J Cardiol. 1996;53(3):203–8.

    Article  CAS  PubMed  Google Scholar 

  61. Coronary vasomotion in response to sympathetic stimulation in humans: importance of the functional integrity of the endothelium. J Am Coll Cardiol. 1989 Nov 1;14(5):1181–90.

  62. Kety SS, Schmidt CF. The effects of altered arterial tensions of carbon dioxide and oxygen on cerebral blood flow and cerebral oxygen consumption of normal young men. J Clin Invest. 1948;27(4):484–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Coverdale NS, Gati JS, Opalevych O, Perrotta A, Shoemaker JK. Cerebral blood flow velocity underestimates cerebral blood flow during modest hypercapnia and hypocapnia. J Appl Physiol Bethesda Md 1985. 2014;117(10):1090–6.

    Google Scholar 

  64. Tancredi FB, Lajoie I, Hoge RD. A simple breathing circuit allowing precise control of inspiratory gases for experimental respiratory manipulations. BMC Res Notes. 2014;7:235.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Winklhofer S, Pazahr S, Manka R, Alkadhi H, Boss A, Stolzmann P. Quantitative blood oxygenation level-dependent (BOLD) response of the left ventricular myocardium to hyperoxic respiratory challenge at 1.5 and 3.0 T. NMR Biomed. 2014;27(7):795–801.

    Article  CAS  PubMed  Google Scholar 

  66. Yang H-J, Yumul R, Tang R, Cokic I, Klein M, Kali A, et al. Assessment of myocardial reactivity to controlled hypercapnia with free-breathing T2-prepared cardiac blood oxygen level-dependent MR imaging. Radiology. 2014;272(2):397–406.

    Article  PubMed  Google Scholar 

  67. 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(2):577–85.

    Article  PubMed  Google Scholar 

  68. Yang H-J, Oksuz I, Dey D, Sykes J, Klein M, Butler J, et al. Accurate needle-free assessment of myocardial oxygenation for ischemic heart disease in canines using magnetic resonance imaging. Sci Transl Med [Internet]. 2019; 29 [cited 2021 Jan 31];11(494). Available from: https://stm.sciencemag.org/content/11/494/eaat4407.

  69. Patel S, Miao JH, Yetiskul E, Anokhin A, Majmundar SH. Physiology, carbon dioxide retention. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2021 [cited 2021 Feb 25]. Available from: http://www.ncbi.nlm.nih.gov/books/NBK482456/

  70. Raichle ME, Plum F. Hyperventilation and cerebral blood flow. Stroke. 1972;3(5):566–75.

    Article  CAS  PubMed  Google Scholar 

  71. Vogt KM, Ibinson JW, Schmalbrock P, Small RH. Comparison between end-tidal CO2 and respiration volume per time for detecting BOLD signal fluctuations during paced hyperventilation. Magn Reson Imaging. 2011;29(9):1186–94.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Wendland MF, Saeed M, Lauerma K, Crespigny AD, Moseley ME, Higgins CB. Endogenous susceptibility contrast in myocardium during apnea measured using gradient recalled echo planar imaging. Magn Reson Med. 1993;29(2):273–6.

    Article  CAS  PubMed  Google Scholar 

  73. Guensch DP, Fischer K, Flewitt JA, Friedrich MG. Myocardial oxygenation is maintained during hypoxia when combined with apnea – a cardiovascular MR study. Physiol Rep [Internet]. 2013;1(5) Oct [cited 2021 Jan 31] Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3841034/.

  74. Teixeira T, Nadeshalingam G, Fischer K, Marcotte F, Friedrich MG. Breathing maneuvers as a coronary vasodilator for myocardial perfusion imaging. J Magn Reson Imaging. 2016;44(4):947–55.

    Article  PubMed  Google Scholar 

  75. Farrehi PM, Bernstein SJ, Rasak M, Dabbous SA, Stomel RJ, Eagle KA, et al. Frequency of negative coronary arteriographic findings in patients with chest pain is related to community practice patterns. Am J Manag Care. 2002;8(7):643–8.

    PubMed  Google Scholar 

  76. Gulati M, Cooper-DeHoff RM, McClure C, Johnson BD, Shaw LJ, Handberg EM, et al. Adverse cardiovascular outcomes in women with nonobstructive coronary artery disease. Arch Intern Med. 2009;169(9):843–50. This paper from the Women’s Ischemia Syndrome Evaluation (WISE) cohort found that women with signs and symptoms that are suggestive of ischemia but with no obstructive coronary artery disease on angiography have a higher risk of cardiovascular events when compared to asymptomatic women.

  77. Kothawade K, Bairey Merz CN. Microvascular coronary dysfunction in women: pathophysiology, diagnosis, and management. Curr Probl Cardiol. 2011;36(8):291–318.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Panting JR, Gatehouse PD, Yang G-Z, Grothues F, Firmin DN, Collins P, et al. Abnormal subendocardial perfusion in cardiac syndrome X detected by cardiovascular magnetic resonance imaging. N Engl J Med. 2002;346(25):1948–53.

    Article  PubMed  Google Scholar 

  79. 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(2):194–200.

    Article  PubMed  Google Scholar 

  80. Lanza GA. Cardiac syndrome X: a critical overview and future perspectives. Heart. 2007;93(2):159–66.

    Article  CAS  PubMed  Google Scholar 

  81. Haseeb R, Matthew R, Matthew L, Bhavik M, Hannah MC, Howard E, et al. Coronary microvascular dysfunction is associated with myocardial ischemia and abnormal coronary perfusion during exercise. Circulation. 2019;140(22):1805–16.

    Article  Google Scholar 

  82. Hillier E, Hawkins S, Friedrich M. Healthy aging reduces the myocardial oxygenation reserve as assessed with oxygenation sensitive CMR. Can J Cardiol. 2019;35(10):S81.

    Article  Google Scholar 

  83. Hillier E, Hafyane T, Friedrich MG. 285Myocardial and cerebral oxygenation deficits in heart failure patients - a multi-parametric study. Eur Heart J - Cardiovasc Imaging [Internet]. 2019 Jun 1 [cited 2021 Feb 19];20(jez114.003). Available from. https://doi.org/10.1093/ehjci/jez114.003.

  84. Beache GM, Herzka DA, Boxerman JL, Post WS, Gupta SN, Faranesh AZ, et al. Attenuated myocardial vasodilator response in patients with hypertensive hypertrophy revealed by oxygenation-dependent magnetic resonance imaging. Circulation. 2001;104(11):1214–7.

    Article  CAS  PubMed  Google Scholar 

  85. Betty R, Kenneth C, Rina A, Masliza M, Moritz H, Sanjay S, et al. Abstract 10875: Impaired stress myocardial oxygenation and not perfusion reserve is associated with arrhythmic risk in hypertrophic cardiomyopathy: insights from a novel oxygen sensitive cardiac magnetic resonance approach. Circulation. 2019;140(Suppl_1):A10875.

    Google Scholar 

  86. K SR, R S, M S, A W, Rj W, R A, et al. Left ventricular ischemia in pre-capillary pulmonary hypertension: a cardiovascular magnetic resonance study. Cardiovasc Diagn Ther. 2020;10(5):1280–92.

    Article  Google Scholar 

  87. Smiseth OA, Torp H, Opdahl A, Haugaa KH, Urheim S. Myocardial strain imaging: how useful is it in clinical decision making? Eur Heart J. 2016;37(15):1196–207.

    Article  PubMed  Google Scholar 

  88. Amzulescu MS, De Craene M, Langet H, Pasquet A, Vancraeynest D, Pouleur AC, et al. Myocardial strain imaging: review of general principles, validation, and sources of discrepancies. Eur Heart J Cardiovasc Imaging. 2019;20(6):605–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Gerald B, Hoffman Julien IE, Aman M, Saleh S, Cecil C. Cardiac mechanics revisited. Circulation. 2008;118(24):2571–87.

    Article  Google Scholar 

  90. Joo PJ, Alexandre M, In-Chang H, Jun-Bean P, Jae-Hyeong P, Goo-Yeong C. Phenotyping heart failure according to the longitudinal ejection fraction change: myocardial strain, predictors, and outcomes. J Am Heart Assoc. 2020;9(12):e015009.

    Article  Google Scholar 

  91. Kaufman DP, Kandle PF, Murray I, Dhamoon AS. Physiology, oxyhemoglobin dissociation curve. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2020 [cited 2020 Aug 3]. Available from: http://www.ncbi.nlm.nih.gov/books/NBK499818/

  92. Ashish K, Faisaluddin M, Bandyopadhyay D, Hajra A, Herzog E. Prognostic value of global longitudinal strain in heart failure subjects: a recent prototype. Int J Cardiol Heart Vasc. 2018;22:48–9.

    PubMed  PubMed Central  Google Scholar 

  93. Buggey J, Alenezi F, Yoon HJ, Phelan M, DeVore AD, Khouri MG, et al. Left ventricular global longitudinal strain in patients with heart failure with preserved ejection fraction: outcomes following an acute heart failure hospitalization. ESC Heart Fail. 2017;4(4):432–9.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Park JJ, Park J-B, Park J-H, Cho G-Y. Global longitudinal strain to predict mortality in patients with acute heart failure. J Am Coll Cardiol. 2018;71(18):1947–57.

    Article  PubMed  Google Scholar 

  95. Tony S, Rodel L, Marwick Thomas H. Prediction of all-cause mortality from global longitudinal speckle strain. Circ Cardiovasc Imaging. 2009;2(5):356–64.

    Article  Google Scholar 

  96. Pedrizzetti G, Claus P, Kilner PJ, Nagel E. Principles of cardiovascular magnetic resonance feature tracking and echocardiographic speckle tracking for informed clinical use. J Cardiovasc Magn Reson. 2016;18(1):51.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Mangion K, Burke NMM, McComb C, Carrick D, Woodward R, Berry C. Feature-tracking myocardial strain in healthy adults- a magnetic resonance study at 3.0 tesla. Sci Rep. 2019;9(1):3239.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Pryds K, Larsen AH, Hansen MS, Grøndal AYK, Tougaard RS, Hansson NH, et al. Myocardial strain assessed by feature tracking cardiac magnetic resonance in patients with a variety of cardiovascular diseases – a comparison with echocardiography. Sci Rep. 2019;9(1):11296.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  99. Valente F, Gutierrez L, Rodríguez-Eyras L, Fernandez R, Montano M, Sao-Aviles A, et al. Cardiac magnetic resonance longitudinal strain analysis in acute ST-segment elevation myocardial infarction: a comparison with speckle-tracking echocardiography. IJC Heart Vasc. 2020;29:100560.

    Article  Google Scholar 

  100. Kajzar I, Ochs M, Salatzki J, Ochs A, Riffel J, Osman N, et al. Hyperventilation-breath-hold maneuver to detect ischemia by strain-encoded CMR: a pilot study to evaluate a needle-free stress protocol. Eur Heart J - Cardiovasc Imaging [Internet]. 2021;22:jeaa356.294). Available from. https://doi.org/10.1093/ehjci/jeaa356.294. This study demonstrated that fast strain encoded CMR in conjunction with standardized vasoactive breathing maneuvers is a fast, pharmacologic agent and contrast-free approach with a high diagnostic accuracy for the detection of significant coronary artery stenosis.

  101. Tanacli R, Hashemi D, Lapinskas T, Edelmann F, Gebker R, Pedrizzetti G, et al. Range variability in CMR feature tracking multilayer strain across different stages of heart failure. Sci Rep. 2019;9(1):16478.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Kempny A, Fernández-Jiménez R, Orwat S, Schuler P, Bunck AC, Maintz D, et al. Quantification of biventricular myocardial function using cardiac magnetic resonance feature tracking, endocardial border delineation and echocardiographic speckle tracking in patients with repaired tetralogy of Fallot and healthy controls. J Cardiovasc Magn Reson Off J Soc Cardiovasc Magn Reson. 2012;14:32.

    Google Scholar 

  103. Romano S, Romer B, Evans K, Trybula M, Shenoy C, Kwong RY, et al. Prognostic implications of blunted feature-tracking global longitudinal strain during vasodilator cardiovascular magnetic resonance stress imaging. JACC Cardiovasc Imaging. 2020;13(1 Pt 1):58–65.

    Article  PubMed  Google Scholar 

  104. Kammerlander AA. Feature tracking by cardiovascular magnetic resonance imaging. JACC Cardiovasc Imaging. 2020;13(4):948–50.

    Article  PubMed  Google Scholar 

  105. Ito H, Ishida M, Makino W, Goto Y, Ichikawa Y, Kitagawa K, et al. Cardiovascular magnetic resonance feature tracking for characterization of patients with heart failure with preserved ejection fraction: correlation of global longitudinal strain with invasive diastolic functional indices. J Cardiovasc Magn Reson. 2020;22(1):42. This study demonstrated that CMR feature tracking is a reliable, noninvasive method that can identify impaired global longitudinal strain and diastolic dysfunction in heart failure patients with preserved ejection fraction that can independently predict altered left ventricular relaxation.

  106. Simone R, Judd RM, Kim RJ, Kim HW, Igor K, Heitner JF, et al. Feature-tracking global longitudinal strain predicts death in a multicenter population of patients with ischemic and nonischemic dilated cardiomyopathy incremental to ejection fraction and late gadolinium enhancement. JACC Cardiovasc Imaging. 2018;11(10):1419–29.

    Article  Google Scholar 

  107. DeVore AD, McNulty S, Alenezi F, Ersboll M, Vader JM, Oh JK, et al. Impaired left ventricular global longitudinal strain in patients with heart failure with preserved ejection fraction: insights from the RELAX trial. Eur J Heart Fail. 2017;19(7):893–900.

    Article  PubMed  CAS  Google Scholar 

  108. Masaru O, Reddy Yogesh NV, Borlaug Barry A. Diastolic dysfunction and heart failure with preserved ejection fraction. JACC Cardiovasc Imaging. 2020;13(1_Part_2):245–57.

    Google Scholar 

  109. Guensch DP, Kady F, Kyohei Y, Silvia L, Yasushi U, Bernd J, et al. Effect of hyperoxia on myocardial oxygenation and function in patients with stable multivessel coronary artery disease. J Am Heart Assoc. 2020;9(5):e014739.

    Article  PubMed  PubMed Central  Google Scholar 

  110. Hillier E, Hawkins S, Friedrich MG, Nuyt AM. 334The assessment of functional cardiovascular health after exercise intervention in young adults born preterm. Eur Heart J - Cardiovasc Imaging [Internet]. 2019;20:jez122.003). Available from. https://doi.org/10.1093/ehjci/jez122.003.

    Article  Google Scholar 

  111. ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure 2012 | European Heart Journal | Oxford Academic [Internet]. [cited 2021 Feb 19]. Available from: https://academic.oup.com/eurheartj/article/33/14/1787/526884

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Authors and Affiliations

  1. Faculty of Medicine and Health Sciences, McGill University, Montreal, QC, Canada

    Elizabeth Hillier & Matthias G. Friedrich

  2. Faculty of Medicine and Dentistry, University of Alberta, Edmonton, AB, Canada

    Elizabeth Hillier

  3. Departments of Medicine and Diagnostic Radiology, McGill University, 1001 Decarie Blvd, Montreal, QC, H4A 3J1, Canada

    Matthias G. Friedrich

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  1. Elizabeth Hillier
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EH and MGF contributed to the idea, design, and editing of the manuscript. EH performed the literature search and drafted the manuscript.

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Correspondence to Matthias G. Friedrich.

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Conflict of Interest

MGF is a shareholder and consultant of Circle Cardiovascular Imaging Inc. Dr Friedrich is listed as a holder of United States Patent No. 14/419,877: Inducing and measuring myocardial oxygenation changes as a marker for heart disease; United States Patent No. 15/483,712: Measuring oxygenation changes in tissue as a marker for vascular function; United States Patent No 10,653,394: Measuring oxygenation changes in tissue as a marker for vascular function - continuation; and Canadian Patent CA2020/051776: Method and apparatus for determining biomarkers of vascular function utilizing bold CMR images. EH is listed as a holder of Canadian Patent CA2020/051776: Method and apparatus for determining biomarkers of vascular function utilizing bold CMR images. The other authors report no conflicts.

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All reported studies/experiments with human or animal subjects performed by the authors have been previously published and complied with all applicable ethical standards (including the Helsinki declaration and its amendments, institutional/national research committee standards, and international/national/institutional guidelines).

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This article is part of the Topical Collection on Imaging in Heart Failure

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Hillier, E., Friedrich, M.G. The Potential of Oxygenation-Sensitive CMR in Heart Failure. Curr Heart Fail Rep 18, 304–314 (2021). https://doi.org/10.1007/s11897-021-00525-y

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