Download PDF
Semin Respir Crit Care Med 2014; 35(01): 074-082
DOI: 10.1055/s-0033-1363453
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Functional Magnetic Resonance Imaging of the Lung

J. Biederer
1   Department of Diagnostic and Interventional Radiology, Section of Pulmonary Imaging, University of Heidelberg, Heidelberg, Germany
2   Translational Lung Research Center (TLRC) Heidelberg, Member of the German Center for Lung Research (DZL), Heidelberg, Germany
3   Department of Radiology, German Cancer Research Center, Heidelberg, Germany
,
C. P. Heussel
2   Translational Lung Research Center (TLRC) Heidelberg, Member of the German Center for Lung Research (DZL), Heidelberg, Germany
4   Department of Diagnostic and Interventional Radiology with Nuclear Medicine, Thoraxklinik at University of Heidelberg, Heidelberg, Germany
,
M. Puderbach
2   Translational Lung Research Center (TLRC) Heidelberg, Member of the German Center for Lung Research (DZL), Heidelberg, Germany
4   Department of Diagnostic and Interventional Radiology with Nuclear Medicine, Thoraxklinik at University of Heidelberg, Heidelberg, Germany
,
M. O. Wielpuetz
1   Department of Diagnostic and Interventional Radiology, Section of Pulmonary Imaging, University of Heidelberg, Heidelberg, Germany
2   Translational Lung Research Center (TLRC) Heidelberg, Member of the German Center for Lung Research (DZL), Heidelberg, Germany
› Author Affiliations
Further Information

Publication History

Publication Date:
30 January 2014 (online)

    Permissions and Reprints

Abstract

Beyond being a substitute for X-ray, computed tomography, and scintigraphy, magnetic resonance imaging (MRI) inherently combines morphologic and functional information more than any other technology. Lung perfusion: The most established method is first-pass contrast-enhanced imaging with bolus injection of gadolinium chelates and time-resolved gradient-echo (GRE) sequences covering the whole lung (1 volume/s). Images are evaluated visually or semiquantitatively, while absolute quantification remains challenging due to the nonlinear relation of T1-shortening and contrast material concentration. Noncontrast-enhanced perfusion imaging is still experimental, either based on arterial spin labeling or Fourier decomposition. The latter is used to separate high- and low-frequency oscillations of lung signal related to the effects of pulsatile blood flow. Lung ventilation: Using contrast-enhanced first-pass perfusion, lung ventilation deficits are indirectly identified by hypoxic vasoconstriction. More direct but still experimental approaches use either inhalation of pure oxygen, an aerosolized contrast agent, or hyperpolarized noble gases. Fourier decomposition MRI based on the low-frequency lung signal oscillation allows for visualization of ventilation without any contrast agent. Respiratory mechanics: Time-resolved series with high background signal such as GRE or steady-state free precession visualize the movement of chest wall, diaphragm, mediastinum, lung tissue, tracheal wall, and tumor. The assessment of volume changes allows drawing conclusions on regional ventilation. With this arsenal of functional imaging capabilities at high spatial and temporal resolution but without radiation burden, MRI will find its role in regional functional lung analysis and will therefore overcome the sensitivity of global lung function analysis for repeated short-term treatment monitoring.

Keywords

functional MRI lung - ventilation - perfusion - respiratory mechanics
 

  • References

  • 1 Biederer J, Beer M, Hirsch W , et al. MRI of the lung (2/3). Why … when … how? Insights into Imaging [Internet] 2012 [cited 2012 Feb 27]. Available at: http://www.springerlink.com/content/t576m50360717212/
    PubMedGoogle Scholar
  • 2 Biederer J, Mirsadraee S, Beer M , et al. MRI of the lung (3/3)—current applications and future perspectives. Insights into Imaging [Internet] 2012 [cited 2012 Feb 27]. Available at: http://www.springerlink.com/content/6161267064564774/
    PubMedGoogle Scholar
  • 3 Puderbach M, Hintze C, Ley S, Eichinger M, Kauczor H-U, Biederer J. MR imaging of the chest: a practical approach at 1.5T. Eur J Radiol 2007; 64 (3) 345-355
    CrossrefPubMedGoogle Scholar
  • 4 Eichinger M, Puderbach M, Fink C , et al. Contrast-enhanced 3D MRI of lung perfusion in children with cystic fibrosis—initial results. Eur Radiol 2006; 16 (10) 2147-2152
    CrossrefPubMedGoogle Scholar
  • 5 Hopkins SR, Wielpütz MO, Kauczor H-U. Imaging lung perfusion. J Appl Physiol (1985) 2012; 113 (2) 328-339
    CrossrefPubMedGoogle Scholar
  • 6 Scholz A-WK, Eberle B, Heussel CP , et al. Ventilation-perfusion ratio in perflubron during partial liquid ventilation. Anesth Analg 2010; 110 (6) 1661-1668
    CrossrefPubMedGoogle Scholar
  • 7 Morbach AE, Gast KK, Schmiedeskamp J , et al. [Microstructure of the lung: diffusion measurement of hyperpolarized 3Helium]. Z Med Phys 2006; 16 (2) 114-122
    PubMedGoogle Scholar
  • 8 Gast KK, Biedermann A, Herweling A , et al. Oxygen-sensitive 3He-MRI in bronchiolitis obliterans after lung transplantation. Eur Radiol 2008; 18 (3) 530-537
    CrossrefPubMedGoogle Scholar
  • 9 Hopkins SR, Levin DL, Emami K , et al. Advances in magnetic resonance imaging of lung physiology. J Appl Physiol (1985) 2007; 102 (3) 1244-1254
    PubMedGoogle Scholar
  • 10 Risse F, Eichinger M, Kauczor H-U, Semmler W, Puderbach M. Improved visualization of delayed perfusion in lung MRI. Eur J Radiol [Internet] 2009; [cited 2010 Feb 10]. Available at: http://www.ncbi.nlm.nih.gov/pubmed/19713064
    PubMedGoogle Scholar
  • 11 Biederer J, Puderbach M. MR imaging of the chest. HIRE 2009; 3: 39-42
    PubMedGoogle Scholar
  • 12 Hopkins SR, Prisk GK. Lung perfusion measured using magnetic resonance imaging: New tools for physiological insights into the pulmonary circulation. J Magn Reson Imaging 2010; 32 (6) 1287-1301
    CrossrefPubMedGoogle Scholar
  • 13 Hatabu H, Gaa J, Kim D, Li W, Prasad PV, Edelman RR. Pulmonary perfusion: qualitative assessment with dynamic contrast-enhanced MRI using ultra-short TE and inversion recovery turbo FLASH. Magn Reson Med 1996; 36 (4) 503-508
    CrossrefPubMedGoogle Scholar
  • 14 Matsuoka S, Uchiyama K, Shima H , et al. Effect of the rate of gadolinium injection on magnetic resonance pulmonary perfusion imaging. J Magn Reson Imaging 2002; 15 (1) 108-113
    CrossrefPubMedGoogle Scholar
  • 15 Levin DL, Hatabu H. MR evaluation of pulmonary blood flow. J Thorac Imaging 2004; 19 (4) 241-249
    CrossrefPubMedGoogle Scholar
  • 16 Nikolaou K, Schoenberg SO, Brix G , et al. Quantification of pulmonary blood flow and volume in healthy volunteers by dynamic contrast-enhanced magnetic resonance imaging using a parallel imaging technique. Invest Radiol 2004; 39 (9) 537-545
    CrossrefPubMedGoogle Scholar
  • 17 Berthezène Y, Croisille P, Wiart M , et al. Prospective comparison of MR lung perfusion and lung scintigraphy. J Magn Reson Imaging 1999; 9 (1) 61-68
    CrossrefPubMedGoogle Scholar
  • 18 Altes TA, Eichinger M, Puderbach M. Magnetic resonance imaging of the lung in cystic fibrosis. Proc Am Thorac Soc 2007; 4 (4) 321-327
    CrossrefPubMedGoogle Scholar
  • 19 Wielpütz MO, Eichinger M, Puderbach M. Magnetic resonance imaging of cystic fibrosis lung disease. J Thorac Imaging 2013; 28 (3) 151-159
    CrossrefPubMedGoogle Scholar
  • 20 Ohno Y, Hatabu H, Higashino T , et al. Dynamic perfusion MRI versus perfusion scintigraphy: prediction of postoperative lung function in patients with lung cancer. AJR Am J Roentgenol 2004; 182 (1) 73-78
    CrossrefPubMedGoogle Scholar
  • 21 Puderbach M, Risse F, Biederer J , et al. In vivo Gd-DTPA concentration for MR lung perfusion measurements: assessment with computed tomography in a porcine model. Eur Radiol 2008; 18 (10) 2102-2107
    CrossrefPubMedGoogle Scholar
  • 22 Eichinger M, Optazaite D-E, Kopp-Schneider A , et al. Morphologic and functional scoring of cystic fibrosis lung disease using MRI. Eur J Radiol 2012; 81 (6) 1321-1329
    CrossrefPubMedGoogle Scholar
  • 23 Keilholz SD, Mai VM, Berr SS, Fujiwara N, Hagspiel KD. Comparison of first-pass Gd-DOTA and FAIRER MR perfusion imaging in a rabbit model of pulmonary embolism. J Magn Reson Imaging 2002; 16 (2) 168-171
    CrossrefPubMedGoogle Scholar
  • 24 Arai TJ, Henderson AC, Dubowitz DJ , et al. Hypoxic pulmonary vasoconstriction does not contribute to pulmonary blood flow heterogeneity in normoxia in normal supine humans. J Appl Physiol (1985) 2009; 106 (4) 1057-1064
    CrossrefPubMedGoogle Scholar
  • 25 Burnham KJ, Arai TJ, Dubowitz DJ , et al. Pulmonary perfusion heterogeneity is increased by sustained, heavy exercise in humans. J Appl Physiol (1985) 2009; 107 (5) 1559-1568
    CrossrefPubMedGoogle Scholar
  • 26 Mai VM, Hagspiel KD, Christopher JM , et al. Perfusion imaging of the human lung using flow-sensitive alternating inversion recovery with an extra radiofrequency pulse (FAIRER). Magn Reson Imaging 1999; 17 (3) 355-361
    CrossrefPubMedGoogle Scholar
  • 27 Bauman G, Puderbach M, Deimling M , et al. Non-contrast-enhanced perfusion and ventilation assessment of the human lung by means of fourier decomposition in proton MRI. Magn Reson Med 2009; 62 (3) 656-664
    CrossrefPubMedGoogle Scholar
  • 28 Tetzlaff R, Schwarz T, Kauczor H-U, Meinzer H-P, Puderbach M, Eichinger M. Lung function measurement of single lungs by lung area segmentation on 2D dynamic MRI. Acad Radiol 2010; 17 (4) 496-503
    CrossrefPubMedGoogle Scholar
  • 29 Biederer J, Hintze C, Fabel M, Dinkel J. Magnetic resonance imaging and computed tomography of respiratory mechanics. J Magn Reson Imaging 2010; 32 (6) 1388-1397
    CrossrefPubMedGoogle Scholar
  • 30 Molinari F, Puderbach M, Eichinger M , et al. Oxygen-enhanced magnetic resonance imaging: influence of different gas delivery methods on the T1-changes of the lungs. Invest Radiol 2008; 43 (6) 427-432
    CrossrefPubMedGoogle Scholar
  • 31 Molinari F, Eichinger M, Risse F , et al. Navigator-triggered oxygen-enhanced MRI with simultaneous cardiac and respiratory synchronization for the assessment of interstitial lung disease. J Magn Reson Imaging 2007; 26 (6) 1523-1529
    CrossrefPubMedGoogle Scholar
  • 32 Ohno Y, Koyama H, Nogami M , et al. Dynamic oxygen-enhanced MRI versus quantitative CT: pulmonary functional loss assessment and clinical stage classification of smoking-related COPD. AJR Am J Roentgenol 2008; 190 (2) W93-9
    PubMedGoogle Scholar
  • 33 Haage P, Karaagac S, Spüntrup E, Truong HT, Schmidt T, Günther RW. Feasibility of pulmonary ventilation visualization with aerosolized magnetic resonance contrast media. Invest Radiol 2005; 40 (2) 85-88
    CrossrefPubMedGoogle Scholar
  • 34 Suga K, Ogasawara N, Tsukuda T, Matsunaga N. Assessment of regional lung ventilation in dog lungs with Gd-DTPA aerosol ventilation MR imaging. Acta Radiol 2002; 43 (3) 282-291
    CrossrefPubMedGoogle Scholar
  • 35 Heussel CP, Scholz A, Schmittner M , et al. Measurements of alveolar pO2 using 19F-MRI in partial liquid ventilation. Invest Radiol 2003; 38 (10) 635-641
    CrossrefPubMedGoogle Scholar
  • 36 Wolf U, Scholz A, Heussel CP, Markstaller K, Schreiber WG. Subsecond fluorine-19 MRI of the lung. Magn Reson Med 2006; 55 (4) 948-951
    CrossrefPubMedGoogle Scholar
  • 37 Scholz A-W, Wolf U, Fabel M , et al. Comparison of magnetic resonance imaging of inhaled SF6 with respiratory gas analysis. Magn Reson Imaging 2009; 27 (4) 549-556
    CrossrefPubMedGoogle Scholar
  • 38 Adolphi NL, Kuethe DO. Quantitative mapping of ventilation-perfusion ratios in lungs by 19F MR imaging of T1 of inert fluorinated gases. Magn Reson Med 2008; 59 (4) 739-746
    CrossrefPubMedGoogle Scholar
  • 39 Matsuoka S, Patz S, Albert MS , et al. Hyperpolarized gas MR Imaging of the lung: current status as a research tool. J Thorac Imaging 2009; 24 (3) 181-188
    CrossrefPubMedGoogle Scholar
  • 40 van Beek EJR, Wild JM, Kauczor H-U, Schreiber W, Mugler III JP, de Lange EE. Functional MRI of the lung using hyperpolarized 3-helium gas. J Magn Reson Imaging 2004; 20 (4) 540-554
    CrossrefPubMedGoogle Scholar
  • 41 Lutey BA, Lefrak SS, Woods JC , et al. Hyperpolarized 3He MR imaging: physiologic monitoring observations and safety considerations in 100 consecutive subjects. Radiology 2008; 248 (2) 655-661
    CrossrefPubMedGoogle Scholar
  • 42 Hersman FW, Ruset IC, Ketel S , et al. Large production system for hyperpolarized 129Xe for human lung imaging studies. Acad Radiol 2008; 15 (6) 683-692
    CrossrefPubMedGoogle Scholar
  • 43 Driehuys B, Möller HE, Cleveland ZI, Pollaro J, Hedlund LW. Pulmonary perfusion and xenon gas exchange in rats: MR imaging with intravenous injection of hyperpolarized 129Xe. Radiology 2009; 252 (2) 386-393
    PubMedGoogle Scholar
  • 44 van Beek EJR, Dahmen AM, Stavngaard T , et al. Hyperpolarised 3He MRI versus HRCT in COPD and normal volunteers: PHIL trial. Eur Respir J 2009; 34 (6) 1311-1321
    CrossrefPubMedGoogle Scholar
  • 45 Haczku A, Emami K, Fischer MC , et al. Hyperpolarized 3He MRI in asthma measurements of regional ventilation following allergic sensitization and challenge in mice—preliminary results. Acad Radiol 2005; 12 (11) 1362-1370
    CrossrefPubMedGoogle Scholar
  • 46 Mata JF, Altes TA, Cai J , et al. Evaluation of emphysema severity and progression in a rabbit model: comparison of hyperpolarized 3He and 129Xe diffusion MRI with lung morphometry. J Appl Physiol (1985) 2007; 102 (3) 1273-1280
    PubMedGoogle Scholar
  • 47 Eberle B, Markstaller K, Schreiber WG, Kauczor HU. Hyperpolarised gases in magnetic resonance: a new tool for functional imaging of the lung. Swiss Med Wkly 2001; 131 (35-36) 503-509
    PubMedGoogle Scholar
  • 48 Bruells CS, Rossaint R, Dembinski R. [Ventilation in acute respiratory distress. Lung-protective strategies]. Med Klin Intensivmed Notfmed 2012; 107 (8) 596-602
    CrossrefPubMedGoogle Scholar
  • 49 Rizi RR, Baumgardner JE, Ishii M , et al. Determination of regional VA/Q by hyperpolarized 3He MRI. Magn Reson Med 2004; 52 (1) 65-72
    CrossrefPubMedGoogle Scholar
  • 50 Suga K, Ogasawara N, Okada M, Tsukuda T, Matsunaga N, Miyazaki M. Lung perfusion impairments in pulmonary embolic and airway obstruction with noncontrast MR imaging. J Appl Physiol (1985) 2002; 92 (6) 2439-2451
    PubMedGoogle Scholar
  • 51 Bauman G, Lützen U, Ullrich M , et al. Pulmonary functional imaging: qualitative comparison of Fourier decomposition MR imaging with SPECT/CT in porcine lung. Radiology 2011; 260 (2) 551-559
    CrossrefPubMedGoogle Scholar
  • 52 Bauman G, Scholz A, Rivoire J , et al. Lung ventilation- and perfusion-weighted Fourier decomposition magnetic resonance imaging: in vivo validation with hyperpolarized 3He and dynamic contrast-enhanced MRI. Magn Reson Med 2013; 69 (1) 229-237
    CrossrefPubMedGoogle Scholar
  • 53 Bauman G, Eichinger M, Deimling M. Non-contrast-enhanced lung perfusion MRI in comparison to contrast-enhanced MRI perfusion in young cystic fibrosis patients. Insights into Imaging 2010; 1 (1) S301
    PubMedGoogle Scholar
  • 54 Fabel M, Wintersperger BJ, Dietrich O , et al. MRI of respiratory dynamics with 2D steady-state free-precession and 2D gradient echo sequences at 1.5 and 3.  Tesla: an observer preference study. Eur Radiol 2009; 19 (2) 391-399
    CrossrefPubMedGoogle Scholar
  • 55 Biederer J, Dinkel J, Remmert G , et al. 4D-Imaging of the lung: reproducibility of lesion size and displacement on helical CT, MRI, and cone beam CT in a ventilated ex vivo system. Int J Radiat Oncol Biol Phys 2009; 73 (3) 919-926
    CrossrefPubMedGoogle Scholar
  • 56 Dinkel J, Hintze C, Tetzlaff R , et al. 4D-MRI analysis of lung tumor motion in patients with hemidiaphragmatic paralysis. Radiother Oncol 2009; 91 (3) 449-454
    CrossrefPubMedGoogle Scholar
  • 57 Heussel CP, Ley S, Biedermann A , et al. Respiratory lumenal change of the pharynx and trachea in normal subjects and COPD patients: assessment by cine-MRI. Eur Radiol 2004; 14 (12) 2188-2197
    CrossrefPubMedGoogle Scholar
  • 58 Cai J, Sheng K, Benedict SH , et al. Dynamic MRI of grid-tagged hyperpolarized helium-3 for the assessment of lung motion during breathing. Int J Radiat Oncol Biol Phys 2009; 75 (1) 276-284
    CrossrefPubMedGoogle Scholar
  • 59 Cai J, McLawhorn R, Read PW , et al. Effects of breathing variation on gating window internal target volume in respiratory gated radiation therapy. Med Phys 2010; 37 (8) 3927-3934
    CrossrefPubMedGoogle Scholar
  • 60 Nagendran J, Michelakis E. MRI: one-stop shop for the comprehensive assessment of pulmonary arterial hypertension?. Chest 2007; 132 (1) 2-5
    CrossrefPubMedGoogle Scholar
  • 61 Kreitner K-FJ, Ley S, Kauczor H-U , et al. Chronic thromboembolic pulmonary hypertension: pre- and postoperative assessment with breath-hold MR imaging techniques. Radiology 2004; 232 (2) 535-543
    CrossrefPubMedGoogle Scholar
  • 62 Vonk-Noordegraaf A, Marcus JT, Holverda S, Roseboom B, Postmus PE. Early changes of cardiac structure and function in COPD patients with mild hypoxemia. Chest 2005; 127 (6) 1898-1903
    CrossrefPubMedGoogle Scholar
  • 63 Lorenz J, Bals R, Kauczor H-U , et al. [Meeting of experts on obstructive airway diseases: targets and methods]. Pneumologie 2012; 66 (9) 526-538
    Article in Thieme ConnectPubMedGoogle Scholar