Investigative Magnetic Resonance Imaging

Korean Society of Magnetic Resonance in Medicine (대한자기공명의과학회)
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Principles of Magnetic Resonance Angiography Techniques

  • Shin, Taehoon (Division of Mechanical and Biomedical Engineering, Ewha Womans University)
  • Received : 2021.06.16
  • Accepted : 2021.09.17
  • Published : 2021.12.30
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Abstract

Magnetic resonance angiography (MRA) plays an important role in accurate diagnosis and appropriate treatment planning for patients with arterial disease. Contrast-enhanced (CE) MRA is fast and robust, offering hemodynamic information of arterial flow, but involves the risk of a side effect called nephrogenic systemic fibrosis. Various non-contrast-enhanced (NCE) MRA techniques have been developed by utilizing the fact that arterial blood is moving fast compared to background tissues. NCE MRA is completely free of any safety issues, but has different drawbacks for various approaches. This review article describes basic principles of CE and NCE MRA techniques with a focus on how to generate angiographic image contrast from a pulse sequence perspective. Advantages, pitfalls, and key applications are also discussed for each MRA method.

Keywords

Acknowledgement

This work was supported by grants (NRF-2020R1A6A1A03043528, NRF-2020R1A2C1006293) of the Basic Science Research Programs through the National Research Foundation of Korea.

References

  1. Kadir S. Diagnostic angiography. Philadelphia: Saunders, 1986
  2. Abrams HL, Baum S, Pentecost MJ. Abrams' angiograph: vascular and interventional radiology. Boston: Little Brown, 1997
  3. Waugh JR, Sacharias N. Arteriographic complications in the DSA era. Radiology 1992;182:243-246 https://doi.org/10.1148/radiology.182.1.1727290
  4. Bettmann MA, Heeren T, Greenfield A, Goudey C. Adverse events with radiographic contrast agents: results of the SCVIR Contrast Agent Registry. Radiology 1997;203:611-620 https://doi.org/10.1148/radiology.203.3.9169677
  5. Willinsky RA, Taylor SM, TerBrugge K, Farb RI, Tomlinson G, Montanera W. Neurologic complications of cerebral angiography: prospective analysis of 2,899 procedures and review of the literature. Radiology 2003;227:522-528 https://doi.org/10.1148/radiol.2272012071
  6. Smith SC Jr, Feldman TE, Hirshfeld JW Jr, et al. ACC/AHA/SCAI 2005 guideline update for percutaneous coronary intervention: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (ACC/AHA/SCAI Writing Committee to Update the 2001 Guidelines for Percutaneous Coronary Intervention). J Am Coll Cardiol 2006;47:e1-121 https://doi.org/10.1016/j.jacc.2005.07.067
  7. Edelman RR, Sheehan JJ, Dunkle E, Schindler N, Carr J, Koktzoglou I. Quiescent-interval single-shot unenhanced magnetic resonance angiography of peripheral vascular disease: technical considerations and clinical feasibility. Magn Reson Med 2010;63:951-958 https://doi.org/10.1002/mrm.22287
  8. Met R, Bipat S, Legemate DA, Reekers JA, Koelemay MJ. Diagnostic performance of computed tomography angiography in peripheral arterial disease: a systematic review and meta-analysis. JAMA 2009;301:415-424 https://doi.org/10.1001/jama.301.4.415
  9. Villablanca JP, Jahan R, Hooshi P, et al. Detection and characterization of very small cerebral aneurysms by using 2D and 3D helical CT angiography. AJNR Am J Neuroradiol 2002;23:1187-1198
  10. Mehran R, Nikolsky E. Contrast-induced nephropathy: definition, epidemiology, and patients at risk. Kidney Int Suppl 2006:S11-15
  11. Rundback JH, Nahl D, Yoo V. Contrast-induced nephropathy. J Vasc Surg 2011;54:575-579 https://doi.org/10.1016/j.jvs.2011.04.047
  12. Prince MR. Gadolinium-enhanced MR aortography. Radiology 1994;191:155-164 https://doi.org/10.1148/radiology.191.1.8134563
  13. van Vaals JJ, Brummer ME, Dixon WT, et al. "Keyhole" method for accelerating imaging of contrast agent uptake. J Magn Reson Imaging 1993;3:671-675 https://doi.org/10.1002/jmri.1880030419
  14. Korosec FR, Frayne R, Grist TM, Mistretta CA. Time-resolved contrast-enhanced 3D MR angiography. Magn Reson Med 1996;36:345-351 https://doi.org/10.1002/mrm.1910360304
  15. Hennig J, Scheffler K, Laubenberger J, Strecker R. Time-resolved projection angiography after bolus injection of contrast agent. Magn Reson Med 1997;37:341-345 https://doi.org/10.1002/mrm.1910370306
  16. Lustig M, Donoho D, Pauly JM. Sparse MRI: the application of compressed sensing for rapid MR imaging. Magn Reson Med 2007;58:1182-1195 https://doi.org/10.1002/mrm.21391
  17. Rapacchi S, Han F, Natsuaki Y, et al. High spatial and temporal resolution dynamic contrast-enhanced magnetic resonance angiography using compressed sensing with magnitude image subtraction. Magn Reson Med 2014;71:1771-1783 https://doi.org/10.1002/mrm.24842
  18. Chandarana H, Feng L, Block TK, et al. Free-breathing contrast-enhanced multiphase MRI of the liver using a combination of compressed sensing, parallel imaging, and golden-angle radial sampling. Invest Radiol 2013;48:10-16 https://doi.org/10.1097/rli.0b013e318271869c
  19. Jaspan ON, Fleysher R, Lipton ML. Compressed sensing MRI: a review of the clinical literature. Br J Radiol 2015;88:20150487 https://doi.org/10.1259/bjr.20150487
  20. Baum RA, Rutter CM, Sunshine JH, et al. Multicenter trial to evaluate vascular magnetic resonance angiography of the lower extremity. American College of Radiology Rapid Technology Assessment Group. JAMA 1995;274:875-880 https://doi.org/10.1001/jama.1995.03530110037032
  21. Gilfeather M, Yoon HC, Siegelman ES, et al. Renal artery stenosis: evaluation with conventional angiography versus gadolinium-enhanced MR angiography. Radiology 1999;210:367-372 https://doi.org/10.1148/radiology.210.2.r99fe44367
  22. Liu X, Bi X, Huang J, Jerecic R, Carr J, Li D. Contrast-enhanced whole-heart coronary magnetic resonance angiography at 3.0 T: comparison with steady-state free precession technique at 1.5 T. Invest Radiol 2008;43:663-668 https://doi.org/10.1097/RLI.0b013e31817ed1ff
  23. Debrey SM, Yu H, Lynch JK, et al. Diagnostic accuracy of magnetic resonance angiography for internal carotid artery disease: a systematic review and meta-analysis. Stroke 2008;39:2237-2248 https://doi.org/10.1161/strokeaha.107.509877
  24. Farb RI, McGregor C, Kim JK, et al. Intracranial arteriovenous malformations: real-time auto-triggered elliptic centric-ordered 3D gadolinium-enhanced MR angiography--initial assessment. Radiology 2001;220:244-251 https://doi.org/10.1148/radiology.220.1.r01jn15244
  25. Kruger DG, Riederer SJ, Grimm RC, Rossman PJ. Continuously moving table data acquisition method for long FOV contrast-enhanced MRA and whole-body MRI. Magn Reson Med 2002;47:224-231 https://doi.org/10.1002/mrm.10061
  26. Kuo PH, Kanal E, Abu-Alfa AK, Cowper SE. Gadolinium-based MR contrast agents and nephrogenic systemic fibrosis. Radiology 2007;242:647-649 https://doi.org/10.1148/radiol.2423061640
  27. Martin DR, Krishnamoorthy SK, Kalb B, et al. Decreased incidence of NSF in patients on dialysis after changing gadolinium contrast-enhanced MRI protocols. J Magn Reson Imaging 2010;31:440-446 https://doi.org/10.1002/jmri.22024
  28. Thomsen HS. NSF: still relevant. J Magn Reson Imaging 2014;40:11-12 https://doi.org/10.1002/jmri.24422
  29. Masaryk TJ, Laub GA, Modic MT, Ross JS, Haacke EM. Carotid-CNS MR flow imaging. Magn Reson Med 1990;14:308-314 https://doi.org/10.1002/mrm.1910140215
  30. Laub GA. Time-of-flight method of MR angiography. Magn Reson Imaging Clin N Am 1995;3:391-398 https://doi.org/10.1016/S1064-9689(21)00251-8
  31. Kanazawa H, Miyazaki M. Time-spatial labeling inversion tag (t-SLIT) using a selective IR-tag on/off pulse in 2D and 3D half-Fourier FSE as arterial spin labeling. In Proceeding of the 10th Annual Meeting ISMRM, 2002:140
  32. Braendli M, Bongartz G. Combining two single-shot imaging techniques with slice-selective and non-slice-selective inversion recovery pulses: new strategy for native MR angiography based on the long T1 relaxation time and inflow properties of blood. AJR Am J Roentgenol 2003;180:725-728 https://doi.org/10.2214/ajr.180.3.1800725
  33. Katoh M, Buecker A, Stuber M, Gunther RW, Spuentrup E. Free-breathing renal MR angiography with steady-state free-precession (SSFP) and slab-selective spin inversion: initial results. Kidney Int 2004;66:1272-1278 https://doi.org/10.1111/j.1523-1755.2004.00882.x
  34. Oppelt A, Graumann R, Barfuss H, Fischer H, Hartl W, Shajor W. FISP - a new fast MRI sequence. Electromedica 1986;54:15-18
  35. Deshpande VS, Shea SM, Laub G, Simonetti OP, Finn JP, Li D. 3D magnetization-prepared true-FISP: a new technique for imaging coronary arteries. Magn Reson Med 2001;46:494-502 https://doi.org/10.1002/mrm.1219
  36. Atanasova IP, Kim D, Lim RP, et al. Noncontrast MR angiography for comprehensive assessment of abdominopelvic arteries using quadruple inversion-recovery preconditioning and 3D balanced steady-state free precession imaging. J Magn Reson Imaging 2011;33:1430-1439 https://doi.org/10.1002/jmri.22564
  37. Hodnett PA, Koktzoglou I, Davarpanah AH, et al. Evaluation of peripheral arterial disease with nonenhanced quiescent-interval single-shot MR angiography. Radiology 2011;260:282-293 https://doi.org/10.1148/radiol.11101336
  38. Ward EV, Galizia MS, Usman A, Popescu AR, Dunkle E, Edelman RR. Comparison of quiescent inflow single-shot and native space for nonenhanced peripheral MR angiography. J Magn Reson Imaging 2013;38:1531-1538 https://doi.org/10.1002/jmri.24124
  39. Wu G, Yang J, Zhang T, et al. The diagnostic value of non-contrast enhanced quiescent interval single shot (QISS) magnetic resonance angiography at 3T for lower extremity peripheral arterial disease, in comparison to CT angiography. J Cardiovasc Magn Reson 2016;18:71
  40. Koktzoglou I, Aherne EA, Walker MT, Meyer JR, Edelman RR. Ungated nonenhanced radial quiescent interval slice-selective (QISS) magnetic resonance angiography of the neck: evaluation of image quality. J Magn Reson Imaging 2019;50:1798-1807 https://doi.org/10.1002/jmri.26781
  41. Edelman RR, Giri S, Pursnani A, Botelho MP, Li W, Koktzoglou I. Breath-hold imaging of the coronary arteries using Quiescent-Interval Slice-Selective (QISS) magnetic resonance angiography: pilot study at 1.5 Tesla and 3 Tesla. J Cardiovasc Magn Reson 2015;17:101 https://doi.org/10.1186/s12968-015-0205-2
  42. Koktzoglou I, Huang R, Ong AL, Aouad PJ, Walker MT, Edelman RR. High spatial resolution whole-neck MR angiography using thin-slab stack-of-stars quiescent interval slice-selective acquisition. Magn Reson Med 2020;84:3316-3324 https://doi.org/10.1002/mrm.28339
  43. Wang Y, Riederer SJ, Ehman RL. Respiratory motion of the heart: kinematics and the implications for the spatial resolution in coronary imaging. Magn Reson Med 1995;33:713-719 https://doi.org/10.1002/mrm.1910330517
  44. Danias PG, Stuber M, Botnar RM, Kissinger KV, Edelman RR, Manning WJ. Relationship between motion of coronary arteries and diaphragm during free breathing: lessons from real-time MR imaging. AJR Am J Roentgenol 1999;172:1061-1065 https://doi.org/10.2214/ajr.172.4.10587147
  45. Nehrke K, Bornert P, Manke D, Bock JC. Free-breathing cardiac MR imaging: study of implications of respiratory motion--initial results. Radiology 2001;220:810-815 https://doi.org/10.1148/radiol.2203010132
  46. Taylor AM, Keegan J, Jhooti P, Firmin DN, Pennell DJ. Calculation of a subject-specific adaptive motion-correction factor for improved real-time navigator echo-gated magnetic resonance coronary angiography. J Cardiovasc Magn Reson 1999;1:131-138 https://doi.org/10.3109/10976649909080841
  47. Keegan J, Gatehouse P, Yang GZ, Firmin D. Coronary artery motion with the respiratory cycle during breath-holding and free-breathing: implications for slice-followed coronary artery imaging. Magn Reson Med 2002;47:476-481 https://doi.org/10.1002/mrm.10069
  48. Miyazaki M, Sugiura S, Tateishi F, Wada H, Kassai Y, Abe H. Non-contrast-enhanced MR angiography using 3D ECG-synchronized half-Fourier fast spin echo. J Magn Reson Imaging 2000;12:776-783 https://doi.org/10.1002/1522-2586(200011)12:5<776::AID-JMRI17>3.0.CO;2-X
  49. Fan Z, Sheehan J, Bi X, Liu X, Carr J, Li D. 3D noncontrast MR angiography of the distal lower extremities using flow-sensitive dephasing (FSD)-prepared balanced SSFP. Magn Reson Med 2009;62:1523-1532 https://doi.org/10.1002/mrm.22142
  50. Priest AN, Graves MJ, Lomas DJ. Non-contrast-enhanced vascular magnetic resonance imaging using flow-dependent preparation with subtraction. Magn Reson Med 2012;67:628-637 https://doi.org/10.1002/mrm.23040
  51. Priest AN, Joubert I, Winterbottom AP, See TC, Graves MJ, Lomas DJ. Initial clinical evaluation of a non-contrast-enhanced MR angiography method in the distal lower extremities. Magn Reson Med 2013;70:1644-1652 https://doi.org/10.1002/mrm.24626
  52. Lim RP, Fan Z, Chatterji M, et al. Comparison of nonenhanced MR angiographic subtraction techniques for infragenual arteries at 1.5 T: a preliminary study. Radiology 2013;267:293-304 https://doi.org/10.1148/radiol.12120859
  53. Liu X, Fan Z, Zhang N, et al. Unenhanced MR angiography of the foot: initial experience of using flow-sensitive dephasing-prepared steady-state free precession in patients with diabetes. Radiology 2014;272:885-894 https://doi.org/10.1148/radiol.14132284
  54. Sheehan JJ, Fan Z, Davarpanah AH, et al. Nonenhanced MR angiography of the hand with flow-sensitive dephasing-prepared balanced SSFP sequence: initial experience with systemic sclerosis. Radiology 2011;259:248-256 https://doi.org/10.1148/radiol.10100851
  55. de Rochefort L, Maitre X, Bittoun J, Durand E. Velocity-selective RF pulses in MRI. Magn Reson Med 2006;55:171-176 https://doi.org/10.1002/mrm.20751
  56. Shin T, Worters PW, Hu BS, Nishimura DG. Non-contrast-enhanced renal and abdominal MR angiography using velocity-selective inversion preparation. Magn Reson Med 2013;69:1268-1275 https://doi.org/10.1002/mrm.24356
  57. Shin T, Hu BS, Nishimura DG. Off-resonance-robust velocity-selective magnetization preparation for non-contrast-enhanced peripheral MR angiography. Magn Reson Med 2013;70:1229-1240 https://doi.org/10.1002/mrm.24561
  58. Qin Q, Shin T, Schar M, Guo H, Chen H, Qiao Y. Velocity-selective magnetization-prepared non-contrast-enhanced cerebral MR angiography at 3 Tesla: improved immunity to B0/B1 inhomogeneity. Magn Reson Med 2016;75:1232-1241 https://doi.org/10.1002/mrm.25764
  59. Watson JDB, Grasu B, Menon R, Pensy R, Crawford RS, Shin T. Novel, non-gadolinium-enhanced magnetic resonance imaging technique of pedal artery aneurysms. J Vasc Surg Cases Innov Tech 2017;3:87-89 https://doi.org/10.1016/j.jvscit.2016.12.003
  60. Shin T, Menon RG, Thomas RB, et al. Unenhanced velocity-selective MR angiography (VS-MRA): initial clinical evaluation in patients with peripheral artery disease. J Magn Reson Imaging 2019;49:744-751 https://doi.org/10.1002/jmri.26268
  61. Zhu D, Li W, Liu D, et al. Non-contrast-enhanced abdominal MRA at 3 T using velocity-selective pulse trains. Magn Reson Med 2020;84:1173-1183 https://doi.org/10.1002/mrm.28187
  62. Shin T, Qin Q, Park JY, Crawford RS, Rajagopalan S. Identification and reduction of image artifacts in non-contrast-enhanced velocity-selective peripheral angiography at 3T. Magn Reson Med 2016;76:466-477 https://doi.org/10.1002/mrm.25870
  63. Shin T, Qin Q. Characterization and suppression of stripe artifact in velocity-selective magnetization-prepared unenhanced MR angiography. Magn Reson Med 2018;80:1997-2005 https://doi.org/10.1002/mrm.27160