DOI QR코드

DOI QR Code

Physiological and Functional Magnetic Resonance Imaging Using Balanced Steady-state Free Precession

  • Park, Sung-Hong (Magnetic Resonance Imaging Lab, Department of Bio and Brain Engineering, Korea Advanced Institute of Science and Technology) ;
  • Han, Paul Kyu (Magnetic Resonance Imaging Lab, Department of Bio and Brain Engineering, Korea Advanced Institute of Science and Technology) ;
  • Choi, Seung Hong (Department of Radiology, Seoul National University College of Medicine)
  • Received : 2014.04.07
  • Accepted : 2015.02.05
  • Published : 2015.06.01

Abstract

Balanced steady-state free precession (bSSFP) is a highly efficient pulse sequence that is known to provide the highest signal-to-noise ratio per unit time. Recently, bSSFP is getting increasingly popular in both the research and clinical communities. This review will be focusing on the application of the bSSFP technique in the context of probing the physiological and functional information. In the first part of this review, the basic principles of bSSFP are briefly covered. Afterwards, recent developments related to the application of bSSFP, in terms of physiological and functional imaging, are introduced and reviewed. Despite its long development history, bSSFP is still a promising technique that has many potential benefits for obtaining high-resolution physiological and functional images.

Keywords

Acknowledgement

Supported by : National Research Foundation of Korea

References

  1. Alsop DC. Phase insensitive preparation of single-shot RARE: application to diffusion imaging in humans. Magn Reson Med 1997;38:527-533 https://doi.org/10.1002/mrm.1910380404
  2. Feinberg DA, Kiefer B, Johnson G. GRASE improves spatial resolution in single shot imaging. Magn Reson Med 1995;33:529-533 https://doi.org/10.1002/mrm.1910330411
  3. Crelier GR, Hoge RD, Munger P, Pike GB. Perfusion-based functional magnetic resonance imaging with single-shot RARE and GRASE acquisitions. Magn Reson Med 1999;41:132-136 https://doi.org/10.1002/(SICI)1522-2594(199901)41:1<132::AID-MRM18>3.0.CO;2-5
  4. Carr HY. Steady-state free precession in nuclear magnetic resonance. Phys Rev 1958;112:1693-1701 https://doi.org/10.1103/PhysRev.112.1693
  5. Zur Y, Stokar S, Bendel P. An analysis of fast imaging sequences with steady-state transverse magnetization refocusing. Magn Reson Med 1988;6:175-193 https://doi.org/10.1002/mrm.1910060206
  6. Oppelt A, Graumann R, Barfuss H, Fischer H, Hartl W, Shajor W. FISP-a new fast MRI sequence. Electromedica 1986;54:15-18
  7. Scheffler K, Lehnhardt S. Principles and applications of balanced SSFP techniques. Eur Radiol 2003;13:2409-2418 https://doi.org/10.1007/s00330-003-1957-x
  8. Miller KL. FMRI using balanced steady-state free precession (SSFP). Neuroimage 2012;62:713-719 https://doi.org/10.1016/j.neuroimage.2011.10.040
  9. Bieri O, Scheffler K. Fundamentals of balanced steady state free precession MRI. J Magn Reson Imaging 2013;38:2-11 https://doi.org/10.1002/jmri.24163
  10. Miller KL, Tijssen RHN, Stikov N, Okell TW. Steady-state MRI: methods for neuroimaging. Imaging in Medicine 2011;3:93-105 https://doi.org/10.2217/iim.10.66
  11. Scheffler K, Hennig J. Is TrueFISP a gradient-echo or a spinecho sequence? Magn Reson Med 2003;49:395-397 https://doi.org/10.1002/mrm.10351
  12. Carr JC, Simonetti O, Bundy J, Li D, Pereles S, Finn JP. Cine MR angiography of the heart with segmented true fast imaging with steady-state precession. Radiology 2001;219:828-834 https://doi.org/10.1148/radiology.219.3.r01jn44828
  13. Hays AG, Schar M, Kelle S. Clinical applications for cardiovascular magnetic resonance imaging at 3 tesla. Curr Cardiol Rev 2009;5:237-242 https://doi.org/10.2174/157340309788970351
  14. Kim SG. Quantification of relative cerebral blood flow change by flow-sensitive alternating inversion recovery (FAIR) technique: application to functional mapping. Magn Reson Med 1995;34:293-301 https://doi.org/10.1002/mrm.1910340303
  15. Martirosian P, Klose U, Mader I, Schick F. FAIR true-FISP perfusion imaging of the kidneys. Magn Reson Med 2004;51:353-361 https://doi.org/10.1002/mrm.10709
  16. Boss A, Martirosian P, Graf H, Claussen CD, Schlemmer HP, Schick F. High resolution MR perfusion imaging of the kidneys at 3 Tesla without administration of contrast media. Rofo 2005;177:1625-1630 https://doi.org/10.1055/s-2005-858761
  17. Fenchel M, Martirosian P, Langanke J, Giersch J, Miller S, Stauder NI, et al. Perfusion MR imaging with FAIR true FISP spin labeling in patients with and without renal artery stenosis: initial experience. Radiology 2006;238:1013-1021 https://doi.org/10.1148/radiol.2382041623
  18. Boss A, Martirosian P, Klose U, Nagele T, Claussen CD, Schick F. FAIR-TrueFISP imaging of cerebral perfusion in areas of high magnetic susceptibility differences at 1.5 and 3 Tesla. J Magn Reson Imaging 2007;25:924-931 https://doi.org/10.1002/jmri.20893
  19. Ludescher B, Martirosian P, Klose U, Nagele T, Schick F, Ernemann U. Determination of the rCBF in the amygdala and rhinal cortex using a FAIR-TrueFISP sequence. Korean J Radiol 2011;12:554-558 https://doi.org/10.3348/kjr.2011.12.5.554
  20. Zun Z, Wong EC, Nayak KS. Assessment of myocardial blood flow (MBF) in humans using arterial spin labeling (ASL): feasibility and noise analysis. Magn Reson Med 2009;62:975-983 https://doi.org/10.1002/mrm.22088
  21. Boss A, Martirosian P, Claussen CD, Schick F. Quantitative ASL muscle perfusion imaging using a FAIR-TrueFISP technique at 3.0 T. NMR Biomed 2006;19:125-132 https://doi.org/10.1002/nbm.1013
  22. Buchbender S, Obenauer S, Mohrmann S, Martirosian P, Buchbender C, Miese FR, et al. Arterial spin labelling perfusion MRI of breast cancer using FAIR TrueFISP: initial results. Clin Radiol 2013;68:e123-e127 https://doi.org/10.1016/j.crad.2012.10.011
  23. Dai W, Garcia D, de Bazelaire C, Alsop DC. Continuous flowdriven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn Reson Med 2008;60:1488-1497 https://doi.org/10.1002/mrm.21790
  24. Wu WC, Fernandez-Seara M, Detre JA, Wehrli FW, Wang J. A theoretical and experimental investigation of the tagging efficiency of pseudocontinuous arterial spin labeling. Magn Reson Med 2007;58:1020-1027 https://doi.org/10.1002/mrm.21403
  25. Park SH, Wang DJ, Duong TQ. Balanced steady state free precession for arterial spin labeling MRI: initial experience for blood flow mapping in human brain, retina, and kidney. Magn Reson Imaging 2013;31:1044-1050 https://doi.org/10.1016/j.mri.2013.03.024
  26. Wu WC, Jain V, Li C, Giannetta M, Hurt H, Wehrli FW, et al. In vivo venous blood T1 measurement using inversion recovery true-FISP in children and adults. Magn Reson Med 2010;64:1140-1147 https://doi.org/10.1002/mrm.22484
  27. Hori M, Shiraga N, Watanabe Y, Aoki S, Isono S, Yui M, et al. Time-resolved three-dimensional magnetic resonance digital subtraction angiography without contrast material in the brain: initial investigation. J Magn Reson Imaging 2009;30:214-218 https://doi.org/10.1002/jmri.21823
  28. Yan L, Li C, Kilroy E, Wehrli FW, Wang DJ. Quantification of arterial cerebral blood volume using multiphase-balanced SSFP-based ASL. Magn Reson Med 2012;68:130-139 https://doi.org/10.1002/mrm.23218
  29. Yan L, Wang S, Zhuo Y, Wolf RL, Stiefel MF, An J, et al. Unenhanced dynamic MR angiography: high spatial and temporal resolution by using true FISP-based spin tagging with alternating radiofrequency. Radiology 2010;256:270-279 https://doi.org/10.1148/radiol.10091543
  30. Park SH, Duong TQ. Alternate ascending/descending directional navigation approach for imaging magnetization transfer asymmetry. Magn Reson Med 2011;65:1702-1710 https://doi.org/10.1002/mrm.22568
  31. Park SH, Duong TQ. Brain MR perfusion-weighted imaging with alternate ascending/descending directional navigation. Magn Reson Med 2011;65:1578-1591 https://doi.org/10.1002/mrm.22580
  32. Park SH, Zhao T, Kim JH, Boada FE, Bae KT. Suppression of effects of gradient imperfections on imaging with alternate ascending/descending directional navigation. Magn Reson Med 2012;68:1600-1606 https://doi.org/10.1002/mrm.24169
  33. Hodnett PA, Koktzoglou I, Davarpanah AH, Scanlon TG, Collins JD, Sheehan JJ, et al. Evaluation of peripheral arterial disease with nonenhanced quiescent-interval singleshot MR angiography. Radiology 2011;260:282-293 https://doi.org/10.1148/radiol.11101336
  34. 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
  35. Santini F, Wetzel SG, Bock J, Markl M, Scheffler K. Timeresolved three-dimensional (3D) phase-contrast (PC) balanced steady-state free precession (bSSFP). Magn Reson Med 2009;62:966-974 https://doi.org/10.1002/mrm.22087
  36. Scheffler K, Seifritz E, Bilecen D, Venkatesan R, Hennig J, Deimling M, et al. Detection of BOLD changes by means of a frequency-sensitive trueFISP technique: preliminary results. NMR Biomed 2001;14:490-496 https://doi.org/10.1002/nbm.726
  37. Miller KL, Hargreaves BA, Lee J, Ress D, deCharms RC, Pauly JM. Functional brain imaging using a blood oxygenation sensitive steady state. Magn Reson Med 2003;50:675-683 https://doi.org/10.1002/mrm.10602
  38. Miller KL, Smith SM, Jezzard P, Pauly JM. High-resolution FMRI at 1.5T using balanced SSFP. Magn Reson Med 2006;55:161-170 https://doi.org/10.1002/mrm.20753
  39. Lee J, Santos JM, Conolly SM, Miller KL, Hargreaves BA, Pauly JM. Respiration-induced B0 field fluctuation compensation in balanced SSFP: real-time approach for transition-band SSFP fMRI. Magn Reson Med 2006;55:1197-1201 https://doi.org/10.1002/mrm.20879
  40. Lee J, Shahram M, Schwartzman A, Pauly JM. Complex data analysis in high-resolution SSFP fMRI. Magn Reson Med 2007;57:905-917 https://doi.org/10.1002/mrm.21195
  41. Wu ML, Wu PH, Huang TY, Shih YY, Chou MC, Liu HS, et al. Frequency stabilization using infinite impulse response filtering for SSFP fMRI at 3T. Magn Reson Med 2007;57:369-379 https://doi.org/10.1002/mrm.21138
  42. Bowen CV, Menon RS, Gati JS. High field balanced-SSFP fMRI: a BOLD technique with excellent tissue sensitivity and superior large vessel suppression. Proc Intl Soc Mag Reson Med 2005:119
  43. Lee JH, Dumoulin SO, Saritas EU, Glover GH, Wandell BA, Nishimura DG, et al. Full-brain coverage and high-resolution imaging capabilities of passband b-SSFP fMRI at 3T. Magn Reson Med 2008;59:1099-1110 https://doi.org/10.1002/mrm.21576
  44. Miller KL, Smith SM, Jezzard P, Wiggins GC, Wiggins CJ. Signal and noise characteristics of SSFP FMRI: a comparison with GRE at multiple field strengths. Neuroimage 2007;37:1227-1236 https://doi.org/10.1016/j.neuroimage.2007.06.024
  45. Zhong K, Leupold J, Hennig J, Speck O. Systematic investigation of balanced steady-state free precession for functional MRI in the human visual cortex at 3 Tesla. Magn Reson Med 2007;57:67-73 https://doi.org/10.1002/mrm.21103
  46. Bowen C, Mason J, Menon R, Gati J. High field balanced-SSFP fMRI: examining a diffusion contrast mechanism using varied flip-angles. Seattle: Proc 14th ISMRM, 2006:665
  47. Miller KL, Jezzard P. Modeling SSFP functional MRI contrast in the brain. Magn Reson Med 2008;60:661-673 https://doi.org/10.1002/mrm.21690
  48. Kim TS, Lee J, Lee JH, Glover GH, Pauly JM. Analysis of the BOLD Characteristics in Pass-Band bSSFP fMRI. Int J Imaging Syst Technol 2012;22:23-32 https://doi.org/10.1002/ima.21296
  49. Patterson S, Beyea S, Bowen C. Quantification of the BOLD contrast mechanism, including its dynamic approach to steady state, for pass-band balanced-SSFP fMRI. Toronto: Proc Intl Soc Mag Reson Med, 2008:2382
  50. Park SH, Kim T, Wang P, Kim SG. Sensitivity and specificity of high-resolution balanced steady-state free precession fMRI at high field of 9.4T. Neuroimage 2011;58:168-176 https://doi.org/10.1016/j.neuroimage.2011.06.010
  51. Park SH, Masamoto K, Hendrich K, Kanno I, Kim SG. Imaging brain vasculature with BOLD microscopy: MR detection limits determined by in vivo two-photon microscopy. Magn Reson Med 2008;59:855-865 https://doi.org/10.1002/mrm.21573
  52. Cheng JS, Gao PP, Zhou IY, Chan RW, Chan Q, Mak HK, et al. Resting-state fMRI using passband balanced steady-state free precession. PLoS One 2014;9:e91075 https://doi.org/10.1371/journal.pone.0091075
  53. Zhou IY, Cheung MM, Lau C, Chan KC, Wu EX. Balanced steady-state free precession fMRI with intravascular susceptibility contrast agent. Magn Reson Med 2012;68:65-73 https://doi.org/10.1002/mrm.23202
  54. Bieri O, Scheffler K. Flow compensation in balanced SSFP sequences. Magn Reson Med 2005;54:901-907 https://doi.org/10.1002/mrm.20619
  55. Markl M, Leupold J, Bieri O, Scheffler K, Hennig J. Double average parallel steady-state free precession imaging: optimized eddy current and transient oscillation compensation. Magn Reson Med 2005;54:965-974 https://doi.org/10.1002/mrm.20615
  56. Nielsen JF, Nayak KS. Interleaved balanced SSFP imaging: artifact reduction using gradient waveform grouping. J Magn Reson Imaging 2009;29:745-750 https://doi.org/10.1002/jmri.21628
  57. Lee J, Lustig M, Kim DH, Pauly JM. Improved shim method based on the minimization of the maximum off-resonance frequency for balanced steady-state free precession (bSSFP). Magn Reson Med 2009;61:1500-1506 https://doi.org/10.1002/mrm.21800
  58. Bangerter NK, Hargreaves BA, Vasanawala SS, Pauly JM, Gold GE, Nishimura DG. Analysis of multiple-acquisition SSFP. Magn Reson Med 2004;51:1038-1047 https://doi.org/10.1002/mrm.20052
  59. Elliott AM, Bernstein MA, Ward HA, Lane J, Witte RJ. Nonlinear averaging reconstruction method for phase-cycle SSFP. Magn Reson Imaging 2007;25:359-364 https://doi.org/10.1016/j.mri.2006.09.013
  60. Cukur T, Lustig M, Nishimura DG. Multiple-profile homogeneous image combination: application to phasecycled SSFP and multicoil imaging. Magn Reson Med 2008;60:732-738 https://doi.org/10.1002/mrm.21720
  61. Bieri O, Klarhofer M, Scheffler K. Chimera steady state free precession (chimera SSFP). Hawaii: Proceedings of the 17th Scientific Meeting of International Society for Magnetic Resonance in Medicine, 2009:2767
  62. Benkert T, Ehses P, Blaimer M, Jakob PM, Breuer FA. Dynamically phase-cycled radial balanced SSFP imaging for efficient banding removal. Magn Reson Med 2014 Jan 29 [Epub]. http://dx.doi.org/10.1002/mrm.25113
  63. Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J, et al. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 2002;47:1202-1210 https://doi.org/10.1002/mrm.10171
  64. Pruessmann KP, Weiger M, Scheidegger MB, Boesiger P. SENSE: sensitivity encoding for fast MRI. Magn Reson Med 1999;42:952-962 https://doi.org/10.1002/(SICI)1522-2594(199911)42:5<952::AID-MRM16>3.0.CO;2-S
  65. Gamper U, Boesiger P, Kozerke S. Compressed sensing in dynamic MRI. Magn Reson Med 2008;59:365-373 https://doi.org/10.1002/mrm.21477
  66. Jung H, Sung K, Nayak KS, Kim EY, Ye JC. k-t FOCUSS: a general compressed sensing framework for high resolution dynamic MRI. Magn Reson Med 2009;61:103-116 https://doi.org/10.1002/mrm.21757
  67. 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
  68. Lustig M, Donoho DL, Santos JM, Pauly JM. Compressed sensing MRI. IEEE Signal Processing Magazine 2008;25:72-82 https://doi.org/10.1109/MSP.2007.914728
  69. Chappell M, Haberg AK, Kristoffersen A. Balanced steadystate free precession with parallel imaging gives distortionfree fMRI with high temporal resolution. Magn Reson Imaging 2011;29:1-8 https://doi.org/10.1016/j.mri.2010.07.007
  70. Han PK, Park SH, Kim SG, Ye JC. Compressed Sensing for fMRI: Feasibility Study on the Acceleration of Non-EPI fMRI at 9.4T. Biomed Res Int 2015 [Epub ahead of print]

Cited by

  1. Preliminary Observations on Sensitivity and Specificity of Magnetization Transfer Asymmetry for Imaging Myelin of Rat Brain at High Field vol.2015, pp.None, 2015, https://doi.org/10.1155/2015/565391
  2. Inter-Slice Blood Flow and Magnetization Transfer Effects as A New Simultaneous Imaging Strategy vol.10, pp.10, 2015, https://doi.org/10.1371/journal.pone.0140560
  3. Hemodynamic Measurement Using Four-Dimensional Phase-Contrast MRI: Quantification of Hemodynamic Parameters and Clinical Applications vol.17, pp.4, 2015, https://doi.org/10.3348/kjr.2016.17.4.445
  4. Emerging Techniques in Brain Tumor Imaging: What Radiologists Need to Know vol.17, pp.5, 2015, https://doi.org/10.3348/kjr.2016.17.5.598
  5. Whole‐brain perfusion imaging with balanced steady‐state free precession arterial spin labeling vol.29, pp.3, 2015, https://doi.org/10.1002/nbm.3463
  6. Feasibility of Quantifying Arterial Cerebral Blood Volume Using Multiphase Alternate Ascending/Descending Directional Navigation (ALADDIN) vol.11, pp.6, 2016, https://doi.org/10.1371/journal.pone.0156687
  7. Phase imaging with multiple phase‐cycled balanced steady‐state free precession at 9.4 T vol.30, pp.6, 2015, https://doi.org/10.1002/nbm.3699
  8. Single and double acquisition strategies for compensation of artifacts from eddy current and transient oscillation in balanced steady‐state free precession vol.78, pp.1, 2015, https://doi.org/10.1002/mrm.26338
  9. Investigation of control scans in pseudo‐continuous arterial spin labeling (pCASL): Strategies for improving sensitivity and reliability of pCASL vol.78, pp.3, 2015, https://doi.org/10.1002/mrm.26474
  10. Diagnostic Performance of Diffusion-Weighted Steady-State Free Precession in Differential Diagnosis of Neoplastic and Benign Osteoporotic Vertebral Compression Fractures: Comparison to Diffusion-Weigh vol.21, pp.3, 2015, https://doi.org/10.13104/imri.2017.21.3.154
  11. Evaluation of hydrocephalus patients with 3D-SPACE technique using variant FA mode at 3T vol.118, pp.2, 2015, https://doi.org/10.1007/s13760-017-0838-z
  12. Left Gastric Vein Visualization with Hepatopetal Flow Information in Healthy Subjects Using Non-Contrast-Enhanced Magnetic Resonance Angiography with Balanced Steady-State Free-Precession Sequence and vol.19, pp.1, 2015, https://doi.org/10.3348/kjr.2018.19.1.32
  13. Brain Regional Homogeneity Changes in Cirrhotic Patients with or without Hepatic Encephalopathy Revealed by Multi-Frequency Bands Analysis Based on Resting-State Functional MRI vol.19, pp.3, 2015, https://doi.org/10.3348/kjr.2018.19.3.452
  14. The impact of MRI steady-state sequences as an additional assessment modality in vestibular schwannoma patients after LINAC stereotactic radiotherapy or radiosurgery vol.194, pp.12, 2015, https://doi.org/10.1007/s00066-018-1317-z
  15. Evaluation of Tumor Blood Flow Using Alternate Ascending/Descending Directional Navigation in Primary Brain Tumors: A Comparison Study with Dynamic Susceptibility Contrast Magnetic Resonance Imaging vol.20, pp.2, 2015, https://doi.org/10.3348/kjr.2018.0300
  16. Current landscape and future perspectives in preclinical MR and PET imaging of brain metastasis vol.3, pp.1, 2015, https://doi.org/10.1093/noajnl/vdab151