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Journal of Nuclear Cardiology

, Volume 15, Issue 5, pp 698–708 | Cite as

Evaluation of the microcirculation: Advances in cardiac magnetic resonance perfusion imaging

  • Amit R. Patel
  • Frederick H. Epstein
  • Christopher M. Kramer
Advances In Nonnuclear Imaging Technologies

Conclusion

In this review we have examined the role of perfusion CMR for evaluating the integrity and function of the microcirculation. We have discussed the techniques for fully quantifying myocardial blood flow and the impact of different imaging parameters on quantification. Perfusion CMR not only identifies the presence of microvascular obstruction after a myocardial infarction but also relates it to patient prognosis. The ability to absolutely quantify myocardial blood flow improves the detection and evaluation of epicardial coronary disease and its risk factors. CMR perfusion imaging has proved to be an invaluable tool for understanding the integral role of the microcirculation in a variety of other cardiac disorders. Another advantage of perfusion CMR is the ability to measure differences in subendocardial and subepicardial blood flow. Newer techniques such as ASL and BOLD imaging promise to further improve the ability of CMR to assess the microcirculation without the use of exogenous contrast agents.

Keywords

Myocardial Perfusion Cardiac Magnetic Resonance Late Gadolinium Enhancement Nuclear Cardiology Arterial Spin Label 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Miller DD, Holmvang G, Gill JB, Dragotakes D, Kantor HL, Okada RD, et al. MRI detection of myocardial perfusion changes by gadolinium-DTPA infusion during dipyridamole hyperemia. Magn Reson Med 1989;10:246–55.PubMedCrossRefGoogle Scholar
  2. 2.
    Atkinson DJ, Burstein D, Edelman RR. First-pass cardiac perfusion: Evaluation with ultrafast MR imaging. Radiology 1990;174:757–62.PubMedGoogle Scholar
  3. 3.
    Manning WJ, Atkinson DJ, Grossman W, Paulin S, Edelman RR. First-pass nuclear magnetic resonance imaging studies using gadolinium- DTPA in patients with coronary artery disease. J Am Coll Cardiol 1991;18:959–65.PubMedCrossRefGoogle Scholar
  4. 4.
    Tsekos NV, Zhang Y, Merkle H, Wilke N, Jerosch-Herold M, Stillman A, et al. Fast anatomical imaging of the heart and assessment of myocardial perfusion with arrhythmia insensitive magnetization preparation. Magn Reson Med 1995;34:530–6.PubMedCrossRefGoogle Scholar
  5. 5.
    Wilke N, Jerosch-Herold M, Wang Y, Huang Y, Christensen BV, Stillman AE, et al. Myocardial perfusion reserve: Assessment with multisection, quantitative, first-pass MR imaging. Radiology 1997;204:373–84.PubMedGoogle Scholar
  6. 6.
    Bertschinger KM, Nanz D, Buechi M, Luescher TF, Marincek B, von Schulthess GK, et al. Magnetic resonance myocardial first-pass perfusion imaging: Parameter optimization for signal response and cardiac coverage. J Magn Reson Imaging 2001;14:556–62.PubMedCrossRefGoogle Scholar
  7. 7.
    Ding S, Wolff SD, Epstein FH. Improved coverage in dynamic contrast-enhanced cardiac MRI using interleaved gradient-echo EPI. Magn Reson Med 1998;39:514–9.PubMedCrossRefGoogle Scholar
  8. 8.
    Judd RM, Reeder SB, Atalar E, McVeigh ER, Zerhouni EA. A magnetization-driven gradient echo pulse sequence for the study of myocardial perfusion. Magn Reson Med 1995;34:276–82.PubMedCrossRefGoogle Scholar
  9. 9.
    Kellman P, Epstein FH, McVeigh ER. Adaptive sensitivity encoding incorporating temporal filtering (TSENSE). Magn Reson Med 2001;45:846–52.PubMedCrossRefGoogle Scholar
  10. 10.
    Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J, et al. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 2002;47:1202–10.PubMedCrossRefGoogle Scholar
  11. 11.
    Lyne JC, Gatehouse PD, Assomull RG, Smith GC, Kellman P, Firmin DN, et al. Direct comparison of myocardial perfusion cardiovascular magnetic resonance sequences with parallel acquisition. J Magn Reson Imaging 2007;26:1444–51.PubMedCrossRefGoogle Scholar
  12. 12.
    Elkington AG, Gatehouse PD, Cannell TM, Moon JC, Prasad SK, Firmin DN, et al. Comparison of hybrid echo-planar imaging and FLASH myocardial perfusion cardiovascular MR imaging. Radiology 2005;235:237–43.PubMedCrossRefGoogle Scholar
  13. 13.
    Storey P, Chen Q, Li W, Edelman RR, Prasad PV. Band artifacts due to bulk motion. Magn Reson Med 2002;48:1028–36.PubMedCrossRefGoogle Scholar
  14. 14.
    Di Bella EVR, Parker DL, Sinusas AJ. On the dark rim artifact in dynamic contrast-enhanced MRI myocardial perfusion studies. Magn Reson Med 2005;54:1295–9.PubMedCrossRefGoogle Scholar
  15. 15.
    Nagel E, Klein C, Paetsch I, Hettwer S, Schnackenburg B, Wegscheider K, et al. Magnetic resonance perfusion measurements for the noninvasive detection of coronary artery disease. Circulation 2003;108:432–7.PubMedCrossRefGoogle Scholar
  16. 16.
    Schwitter J, Nanz D, Kneifel S, Bertschinger K, Büchi M, Knüsel PR, et al. Assessment of myocardial perfusion in coronary artery disease by magnetic resonance: A comparison with positron emission tomography and coronary angiography. Circulation 2001;103:2230–5.PubMedGoogle Scholar
  17. 17.
    Ibrahim T, Nekolla SG, Schreiber K, Odaka K, Volz S, Mehilli J, et al. Assessment of coronary flow reserve: Comparison between contrast-enhanced magnetic resonance imaging and positron emission tomography. J Am Coll Cardiol 2002;39:864–70.PubMedCrossRefGoogle Scholar
  18. 18.
    Rieber J, Huber A, Erhard I, Mueller S, Schweyer M, Koenig A, et al. Cardiac magnetic resonance perfusion imaging for the functional assessment of coronary artery disease: A comparison with coronary angiography and fractional flow reserve. Eur Heart J 2006;27:1465–71.PubMedCrossRefGoogle Scholar
  19. 19.
    Christian TF, Rettmann DW, Aletras AH, Liao SL, Taylor JL, Balaban RS, et al. Absolute myocardial perfusion in canines measured by using dual-bolus first-pass MR imaging. Radiology 2004;232:677–84.PubMedCrossRefGoogle Scholar
  20. 20.
    Jerosch-Herold M, Wilke N, Stillman AE. Magnetic resonance quantification of the myocardial perfusion reserve with a Fermi function model for constrained deconvolution. Med Phys 1998;25:73–84.PubMedCrossRefGoogle Scholar
  21. 21.
    Axel L. Tissue mean transit time from dynamic computed tomography by a simple deconvolution technique. Invest Radiol 1983;18:94–9.PubMedCrossRefGoogle Scholar
  22. 22.
    Gatehouse PD, Elkington AG, Ablitt NA, Yang GZ, Pennell DJ, Firmin DN. Accurate assessment of the arterial input function during high-dose myocardial perfusion cardiovascular magnetic resonance. J Magn Reson Imaging 2004;20:39–45.PubMedCrossRefGoogle Scholar
  23. 23.
    Reffelmann T, Kloner RA. The “no-reflow” phenomenon: Basic science and clinical correlates. Heart 2002;87:162–8.PubMedCrossRefGoogle Scholar
  24. 24.
    Lima JA, Judd RM, Bazille A, Schulman SP, Atalar E, Zerhouni EA. Regional heterogeneity of human myocardial infarcts demonstrated by contrast-enhanced MRI. Potential mechanisms. Circulation 1995;92:1117–25.PubMedGoogle Scholar
  25. 25.
    Judd RM, Lugo-Olivieri CH, Arai M, Kondo T, Croisille P, Lima JA, et al. Physiological basis of myocardial contrast enhancement in fast magnetic resonance images of 2-day-old reperfused canine infarcts. Circulation 1995;92:1902–10.PubMedGoogle Scholar
  26. 26.
    Rochitte CE, Lima JA, Bluemke DA, Reeder SB, McVeigh ER, Furuta T, et al. Magnitude and time course of microvascular obstruction and tissue injury after acute myocardial infarction. Circulation 1998;98:1006–14.PubMedGoogle Scholar
  27. 27.
    Wu KC, Kim RJ, Bluemke DA, Rochitte CE, Zerhouni EA, Becker LC, et al. Quantification and time course of microvascular obstruction by contrast-enhanced echocardiography and magnetic resonance imaging following acute myocardial infarction and reperfusion. J Am Coll Cardiol 1998;32:1756–64.PubMedCrossRefGoogle Scholar
  28. 28.
    Rogers WJ Jr, Kramer CM, Geskin G, Hu YL, Theobald TM, Vido DA, et al. Early contrast-enhanced MRI predicts late functional recovery after reperfused myocardial infarction. Circulation 1999;99:744–50.PubMedGoogle Scholar
  29. 29.
    Hombach V, Grebe O, Merkle N, Waldenmaier S, Höher M, Kochs M, et al. Sequelae of acute myocardial infarction regarding cardiac structure and function and their prognostic significance as assessed by magnetic resonance imaging. Eur Heart J 2005;26:549–57.PubMedCrossRefGoogle Scholar
  30. 30.
    Wu KC, Zerhouni EA, Judd RM, Lugo-Olivieri CH, Barouch LA, Schulman SP, et al. Prognostic significance of microvascular obstruction by magnetic resonance imaging in patients with acute myocardial infarction. Circulation 1998;97:765–72.PubMedGoogle Scholar
  31. 31.
    Wei K, Kaul S. The coronary microcirculation in health and disease. Cardiol Clin 2004;22:221–31.PubMedCrossRefGoogle Scholar
  32. 32.
    Kwong RY, Schussheim AE, Rekhraj S, Aletras AH, Geller N, Davis J, et al. Detecting acute coronary syndrome in the emergency department with cardiac magnetic resonance imaging. Circulation 2003;107:531–7.PubMedCrossRefGoogle Scholar
  33. 33.
    Ingkanisorn WP, Kwong RY, Bohme NS, Geller NL, Rhoads KL, Dyke CK, et al. Prognosis of negative adenosine stress magnetic resonance in patients presenting to an emergency department with chest pain. J Am Coll Cardiol 2006;47:1427–32.PubMedCrossRefGoogle Scholar
  34. 34.
    Selvanayagam JB, Jerosch-Herold M, Porto I, Sheridan D, Cheng AS, Petersen SE, et al. Resting myocardial blood flow is impaired in hibernating myocardium-a magnetic resonance study of quantitative perfusion assessment. Circulation 2005;112:3289–96.PubMedCrossRefGoogle Scholar
  35. 35.
    Jerosch-Herold M, Hu XD, Murthy NS, Seethamraju RT. Time delay for arrival of MR contrast agent in collateral-dependent myocardium. IEEE Trans Med Imaging 2004;23:881–90.PubMedCrossRefGoogle Scholar
  36. 36.
    Chilian WM, Layne SM, Klausner EC, Eastham CL, Marcus ML. Redistribution of coronary microvascular resistance produced by dipyridamole. Am J Physiol Heart Circ Physiol 1989;256:H383–90.Google Scholar
  37. 37.
    Klocke FJ, Simonetti OP, Judd RM, Kim RJ, Harris KR, Hedjbeli S, et al. Limits of detection of regional differences in vasodilated flow in viable myocardium by first-pass magnetic resonance perfusion imaging. Circulation 2001;104:2412–6.PubMedCrossRefGoogle Scholar
  38. 38.
    Nandalur KR, Dwamena BA, Choudhri AF, Nandalur MR, Carlos RC. Diagnostic performance of stress cardiac magnetic resonance imaging in the detection of coronary artery disease: A metaanalysis. J Am Coll Cardiol 2007;50:1343–53.PubMedCrossRefGoogle Scholar
  39. 39.
    Schwitter J, Wacker CM, van Rossum AC, Lombardi M, Al-Saadi N, Ahlstrom H, et al. MR-IMPACT: Comparison of perfusioncardiac magnetic resonance with single-photon emission computed tomography for the detection of coronary artery disease in a multicentre, multivendor, randomized trial. Eur Heart J 2008;29:480–9.PubMedCrossRefGoogle Scholar
  40. 40.
    Klem I, Heitner JF, Shah DJ, Sketch MH Jr, Behar V, Weinsaft J, et al. Improved detection of coronary artery disease by stress perfusion cardiovascular magnetic resonance with the use of delayed enhancement infarction imaging. J Am Coll Cardiol 2006;47:1630–8.PubMedCrossRefGoogle Scholar
  41. 41.
    Jahnke C, Nagel E, Gebker R, Kokocinski T, Kelle S, Manka R, et al. Prognostic value of cardiac magnetic resonance stress tests: Adenosine stress perfusion and dobutamine stress wall motion imaging. Circulation 2007;115:1769–76.PubMedCrossRefGoogle Scholar
  42. 42.
    Cullen JHS, Horsfield MA, Reek CR, Cherryman GR, Barnett DB, Samani NJ. A myocardial perfusion reserve index in humans using first-pass contrast-enhanced magnetic resonance imaging. J Am Coll Cardiol 1999;33:1386–94.PubMedCrossRefGoogle Scholar
  43. 43.
    Futamatsu H, Wilke N, Klassen C, Shoemaker S, Angiolillo DJ, Siuciak A, et al. Evaluation of cardiac magnetic resonance imaging parameters to detect anatomically and hemodynamically significant coronary artery disease. Am Heart J 2007;154:298–305.PubMedCrossRefGoogle Scholar
  44. 44.
    Costa MA, Shoemaker S, Futamatsu H, Klassen C, Angiolillo DJ, Nguyen M, et al. Quantitative magnetic resonance perfusion imaging detects anatomic and physiologic coronary artery disease as measured by coronary angiography and fractional flow reserve. J Am Coll Cardiol 2007;50:514–22.PubMedCrossRefGoogle Scholar
  45. 45.
    Patel AR, Antkowiak P, Nandalur KR, et al. Differentiating moderate from severe coronary artery stenosis using quantitative myocardial perfusion imaging [abstract]. J Cardiovasc Magn Reson 2008;11:239.Google Scholar
  46. 46.
    Selvanayagam JB, Cheng AS, Jerosch-Herold M, Rahimi K, Porto I, van Gaal W, et al. Effect of distal embolization on myocardial perfusion reserve after percutaneous coronary intervention: A quantitative magnetic resonance perfusion study. Circulation 2007;116:1458–64.PubMedCrossRefGoogle Scholar
  47. 47.
    Marcus ML, Chilian WM, Kanatsuka H, Dellsperger KC, Eastham CL, Lamping KG. Understanding the coronary circulation through studies at the microvascular level. Circulation 1990;82:1–7.PubMedGoogle Scholar
  48. 48.
    Chilian WM. Coronary microcirculation in health and disease. Summary of an NHLBI workshop. Circulation 1997;95:522–8.PubMedGoogle Scholar
  49. 49.
    Wang L, Jerosch-Herold M, Jacobs DR Jr, Shahar E, Detrano R, Folsom AR, et al. Coronary artery calcification and myocardial perfusion in asymptomatic adults: The MESA (Multi-Ethnic Study of Atherosclerosis). J Am Coll Cardiol 2006;48:1018–26.PubMedCrossRefGoogle Scholar
  50. 50.
    Wang L, Jerosch-Herold M, Jacobs DR Jr, Shahar E, Folsom AR. Coronary risk factors and myocardial perfusion in asymptomatic adults: The Multi-Ethnic Study of Atherosclerosis (MESA). J Am Coll Cardiol 2006;47:565–72.PubMedCrossRefGoogle Scholar
  51. 51.
    Taskiran M, Fritz-Hansen T, Rasmussen V, Larsson HB, Hilsted J. Decreased myocardial perfusion reserve in diabetic autonomic neuropathy. Diabetes 2002;51:3306–10.PubMedCrossRefGoogle Scholar
  52. 52.
    Wang L, Wong TY, Sharrett AR, Klein R, Folsom AR, Jerosch-Herold M. Relationship between retinal arteriolar narrowing and myocardial perfusion: Multi-ethnic study of atherosclerosis. Hypertension 2008;51:119–26.PubMedCrossRefGoogle Scholar
  53. 53.
    Rosen BD, Lima JA, Nasir K, Edvardsen T, Folsom AR, Lai S, et al. Lower myocardial perfusion reserve is associated with decreased regional left ventricular function in asymptomatic participants of the multi-ethnic study of atherosclerosis. Circulation 2006;114:289–97.PubMedCrossRefGoogle Scholar
  54. 54.
    Epstein FH, London JF, Peters DC, Goncalves LM, Agyeman K, Taylor J, et al. Multislice first-pass cardiac perfusion MRI: Validation in a model of myocardial infarction. Magn Reson Med 2002;47:482–91.PubMedCrossRefGoogle Scholar
  55. 55.
    Bache RJ, McHale PA, Greenfield JC Jr. Transmural myocardial perfusion during restricted coronary inflow in the awake dog. Am J Physiol 1977;232:H645–51.PubMedGoogle Scholar
  56. 56.
    Klocke FJ. Coronary blood flow in man. Prog Cardiovasc Dis 1976;19:117–66.PubMedCrossRefGoogle Scholar
  57. 57.
    Yada T, Hiramatsu O, Kimura A, Goto M, Ogasawara Y, Tsujioka K, et al. In vivo observation of subendocardial microvessels of the beating porcine heart using a needle-probe videomicroscope with a CCD camera. Circ Res 1993;72:939–46.PubMedGoogle Scholar
  58. 58.
    Lee DC, Simonetti OP, Harris KR, Holly TA, Judd RM, Wu E, et al. Magnetic resonance versus radionuclide pharmacological stress perfusion imaging for flow-limiting stenoses of varying severity. Circulation 2004;110:58–65.PubMedCrossRefGoogle Scholar
  59. 59.
    Muehling OM, Jerosch-Herold M, Panse P, Zenovich A, Wilson BV, Wilson RF, et al. Regional heterogeneity of myocardial perfusion in healthy human myocardium: Assessment with magnetic resonance perfusion imaging. J Cardiovasc Magn Reson 2004;6:499–507.PubMedCrossRefGoogle Scholar
  60. 60.
    Petersen SE, Jerosch-Herold M, Hudsmith LE, Robson MD, Francis JM, Doll HA, et al. Evidence for microvascular dysfunction in hypertrophic cardiomyopathy. New insights from multiparametric magnetic resonance imaging. Circulation 2007;115:2418–25.PubMedCrossRefGoogle Scholar
  61. 61.
    Muehling OM, Wilke NM, Panse P, Jerosch-Herold M, Wilson BV, Wilson RF, et al. Reduced myocardial perfusion reserve and transmural perfusion gradient in heart transplant arteriopathy assessed by magnetic resonance imaging. J Am Coll Cardiol 2003;42:1054–60.PubMedCrossRefGoogle Scholar
  62. 62.
    Panting JR, Gatehouse PD, Yang GZ, 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;346:1948–53.PubMedCrossRefGoogle Scholar
  63. 63.
    Wöhrle J, Nusser T, Merkle N, Kestler HA, Grebe OC, Marx N, et al. Myocardial perfusion reserve in cardiovascular magnetic resonance: Correlation to coronary microvascular dysfunction. J Cardiovasc Magn Reson 2006;8:781–7.PubMedCrossRefGoogle Scholar
  64. 64.
    Williams DS, Detre JA, Leigh JS, Koretsky AP. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci U S A 1992;89:212–6.PubMedCrossRefGoogle Scholar
  65. 65.
    Reeder SB, Atalay MK, McVeigh ER, Zerhouni EA, Forder JR. Quantitative cardiac perfusion: A noninvasive spin-labeling method that exploits coronary vessel geometry. Radiology 1996;200:177–84.PubMedGoogle Scholar
  66. 66.
    Wacker CM, Fidler F, Dueren C, Hirn S, Jakob PM, Ertl G, et al. Quantitative assessment of myocardial perfusion with a spinlabeling technique: Preliminary results in patients with coronary artery disease. J Magn Reson Imaging 2003;18:555–60.PubMedCrossRefGoogle Scholar
  67. 67.
    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;87:9868–72.PubMedCrossRefGoogle Scholar
  68. 68.
    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.PubMedCrossRefGoogle Scholar
  69. 69.
    Lindner JR, Skyba DM, Goodman NC, Jayaweera AR, Kaul S. Changes in myocardial blood volume with graded coronary stenosis. Am J Physiol 1997;272:H567–75.PubMedGoogle Scholar
  70. 70.
    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.PubMedCrossRefGoogle Scholar
  71. 71.
    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.PubMedCrossRefGoogle Scholar
  72. 72.
    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.PubMedCrossRefGoogle Scholar
  73. 73.
    Reeder SB, Holmes AA, McVeigh ER, Forder JR. Simultaneous noninvasive determination of regional myocardial perfusion and oxygen content in rabbits: Toward direct measurement of myocardial oxygen consumption at MR imaging. Radiology 1999;212:739–47.PubMedGoogle Scholar
  74. 74.
    McCommis KS, Zhang H, Herrero P, Gropler RJ, Zheng J. Feasibility study of myocardial perfusion and oxygenation by noncontrast MRI: Comparison with PET study in a canine model. Magn Reson Imaging 2008;26:11–9.PubMedCrossRefGoogle Scholar

Copyright information

© American Society of Nuclear Cardiology 2003

Authors and Affiliations

  • Amit R. Patel
    • 1
    • 3
  • Frederick H. Epstein
    • 3
    • 2
  • Christopher M. Kramer
    • 1
    • 3
    • 2
  1. 1.Departments of Medicine and RadiologyUniversity of Virginia Health SystemCharlottesville
  2. 2.From the Department of RadiologyUniversity of Virginia Health SystemCharlottesville
  3. 3.Department of Cardiovascular Imaging CenterUniversity of Virginia Health SystemCharlottesville

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