Outracing Lung Signal Decay – Potential of Ultrashort Echo Time MRI

Mark Oliver Wielpütz; Simon M. F. Triphan; Yoshiharu Ohno; Bertram J. Jobst; Hans-Ulrich Kauczor

doi:10.1055/a-0715-2246

RöFo - Fortschritte auf dem Gebiet der Röntgenstrahlen und der bildgebenden Verfahren, Inhaltsverzeichnis

Rofo 2019; 191(05): 415-423
DOI: 10.1055/a-0715-2246

Review

Outracing Lung Signal Decay – Potential of Ultrashort Echo Time MRI

Dem Signalzerfall in der Lunge zuvorkommen – Potenzial der Ultrashort-Echo-Time-MRT

Autoren

Mark Oliver Wielpütz

¹Department of Diagnostic and Interventional Radiology, Subdivision of Pulmonary Imaging, University Hospital of Heidelberg, Heidelberg, Germany

²Translational Lung Research Center Heidelberg (TLRC), German Lung Research Center (DZL), Heidelberg, Germany

³Department of Diagnostic and Interventional Radiology with Nuclear Medicine, Thoraxklinik at the University Hospital of Heidelberg, Heidelberg, Germany
Simon M. F. Triphan

¹Department of Diagnostic and Interventional Radiology, Subdivision of Pulmonary Imaging, University Hospital of Heidelberg, Heidelberg, Germany

²Translational Lung Research Center Heidelberg (TLRC), German Lung Research Center (DZL), Heidelberg, Germany

³Department of Diagnostic and Interventional Radiology with Nuclear Medicine, Thoraxklinik at the University Hospital of Heidelberg, Heidelberg, Germany
Yoshiharu Ohno

⁴Advanced Biomedical Imaging Research Center, Kobe University Graduate School of Medicine, Kobe, Japan
Bertram J. Jobst

¹Department of Diagnostic and Interventional Radiology, Subdivision of Pulmonary Imaging, University Hospital of Heidelberg, Heidelberg, Germany

²Translational Lung Research Center Heidelberg (TLRC), German Lung Research Center (DZL), Heidelberg, Germany

³Department of Diagnostic and Interventional Radiology with Nuclear Medicine, Thoraxklinik at the University Hospital of Heidelberg, Heidelberg, Germany
Hans-Ulrich Kauczor

¹Department of Diagnostic and Interventional Radiology, Subdivision of Pulmonary Imaging, University Hospital of Heidelberg, Heidelberg, Germany

²Translational Lung Research Center Heidelberg (TLRC), German Lung Research Center (DZL), Heidelberg, Germany

³Department of Diagnostic and Interventional Radiology with Nuclear Medicine, Thoraxklinik at the University Hospital of Heidelberg, Heidelberg, Germany

Abstract

Background Magnetic resonance imaging (MRI) of the pulmonary parenchyma is generally hampered by multiple challenges related to patient respiratory- and circulation-related motion, low proton density and extremely fast signal decay due to the structure of the lungs evolved for gas exchange.

Methods Systematic literature database research as well as annual participation in conferences dedicated to pulmonary MRI for more than the past 20 years by at least one member of the author team.

Results and Conclusion The problem of motion has been addressed in the past by developments such as triggering, gating and parallel imaging. The second problem has, in part, turned out to be an advantage in those diseases that lead to an increase in lung substance and thus an increase in signal relative to the background. To reduce signal decay, ultrashort echo time (UTE) methods were developed to minimize the time between excitation and readout. Having been postulated a while ago, improved hardware and software now open up the possibility of achieving echo times shorter than 200 µs, increasing lung signal significantly by forestalling signal decay and more effectively using the few protons available. Such UTE techniques may not only improve structural imaging of the lung but also enhance functional imaging, including ventilation and perfusion imaging as well as quantitative parameter mapping. Because of accelerating progress in this field of lung MRI, the review at hand seeks to introduce some technical properties as well as to summarize the growing data from applications in humans and disease, which promise that UTE MRI will play an important role in the morphological and functional assessment of the lung in the near future.

Key Points:

Ultrashort echo time MRI is technically feasible with state-of-the-art scanner hardware.
UTE MRI allows for CT-like image quality for structural lung imaging.
Preliminary studies show improvements over conventional morphological imaging in lung cancer and airways diseases.
UTE may improve sensitivity for functional processes like perfusion and tissue characterization.

Citation Format

Wielpütz MO, Triphan SM, Ohno Y et al. Outracing Lung Signal Decay – Potential of Ultrashort Echo Time MRI. Fortschr Röntgenstr 2019; 191: 415 – 423

Zusammenfassung

Hintergrund Die Herausforderungen der Magnetresonanztomografie (MRT) des Lungenparenchyms liegen in der Herz- und Atembewegung der Patienten, niedrigen Protonendichte und vor allem dem extrem schnellen Signalabfall. Dieser entsteht durch die für den Gasaustausch optimierte Lungenstruktur.

Methoden Diese Übersicht basiert auf systematischer Literaturrecherche sowie jährlicher Teilnahme an Konferenzen zum Thema Lungen-MRT über mehr als 20 Jahre durch mindestens einen Autor.

Ergebnisse und Schlussfolgerung Das Problem der Bewegung wurde durch Entwicklungen wie Triggering, Gating und parallele Bildgebung angegangen. Das Problem der geringen Protonendichte hat sich bei Krankheiten, die zu einer Zunahme an Gewebedichte und damit Signal relativ zum Hintergrund, teilweise als Vorteil erwiesen. Um den Signalabfall auszugleichen, wurden ultrashort-echo-time (UTE)-Methoden entwickelt, um die Zeit zwischen Anregung und Auslese zu minimieren. Während diese bereits vor längerer Zeit postuliert wurden, erlauben verbesserte Scanner-Hard- und -Software jetzt Echozeiten unterhalb von 200µs und damit ein signifikant höheres Signal aus der Lunge. Indem man so dem Signalabfall zuvorkommt, lässt sich das Signal der wenigen verfügbaren Protonen effizienter ausnutzen. Solche UTE-Techniken können nicht nur die morphologische Bildgebung in der Lunge verbessern, sondern auch die Möglichkeiten der funktionellen Bildgebung erweitern, einschließlich Ventilations- und Perfusions-Bildgebung sowie der Quantifizierung anderer Parameter. Dem wachsenden Fortschritt in der Lungen-MRT folgend, zeigt diese Übersicht technische Möglichkeiten und liefert einen Überblick über aufkommende Anwendungen am Menschen bzw. Krankheiten. Diese zeigen, dass die UTE-MRT in naher Zukunft eine wichtige Rolle in der morphologischen und funktionellen bildgestützten Untersuchung der Lunge spielen wird.

Kernaussagen:

Ultrashort-echo-time (UTE)-MRT ist auf modernen Scannern technisch machbar und verfügbar.
UTE-MRT erlaubt CT-artige Bildqualität für die morphologische Darstellung der Lunge.
Vorläufige Studien zeigen Verbesserungen gegenüber konventionellen Echozeiten für die morphologische Bildgebung von Lungenkrebs und Atemwegserkrankungen.
UTE-MRT könnte die Sensitivität funktioneller Prozesse wie Perfusionsquantifizierung und Gewebscharakterisierung erhöhen.

Key words

ultrashort TE - lung imaging - functional lung imaging - lung MRI

Volltext

Referenzen

References
1 Bergin CJ, Glover GH, Pauly JM. Lung parenchyma: magnetic susceptibility in MR imaging. Radiology 1991; 180: 845-848
2 Wielpütz M, Kauczor HU. MRI of the lung: state of the art. Diagn Interv Radiol 2012; 18: 344-353
3 Hansell DM, Bankier AA, MacMahon H. et al. Fleischner Society: Glossary of Terms for Thoracic Imaging. Radiology 2008; 246: 697-722
4 Wormanns D, Hamer OW. Glossary of Terms for Thoracic Imaging-German Version of the Fleischner Society Recommendations.
5 Ohno Y, Koyama H, Yoshikawa T. et al. Three-way comparison of whole-body MR, coregistered whole-body FDG PET/MR, and integrated whole-body FDG PET/CT imaging: TNM and stage assessment capability for non--small cell lung cancer patients. Radiology 2015; 275: 849-861
6 Stahl M, Wielpütz MO, Graeber SY. et al. Comparison of Lung Clearance Index and Magnetic Resonance Imaging for Assessment of Lung Disease in Children with Cystic Fibrosis. Am J Respir Crit Care Med 2017; 195: 349-359
7 Bergin CJ, Pauly JM, Macovski A. Lung parenchyma: projection reconstruction MR imaging. Radiology 1991; 179: 777-781
8 Pauly J, Conolly S, Nishimura D. Slice selective excitation for very short T2 species. SMRM.
9 Pauly J, Nishimura D, Macovski A. A k-space analysis of small-tip-angle excitation. J Magn Reson Imaging 1989; 81: 43-56
10 Hatabu H, Alsop DC, Listerud J. et al. T2* and proton density measurement of normal human lung parenchyma using submillisecond echo time gradient echo magnetic resonance imaging. Eur J Radiol 1999; 29: 245-252
11 Hatabu H, Gaa J, Tadamura E. et al. MR imaging of pulmonary parenchyma with a half-Fourier single-shot turbo spin-echo (HASTE) sequence. Eur J Radiol 1999; 29: 152-159
12 Stock KW, Chen Q, Hatabu H. et al. Magnetic resonance T2∗ measurements of the normal human lung in vivo with ultra-short echo times. Magnetic Resonance Imaging 1999; 17: 997-1000
13 Yu J, Xue Y, Song HK. Comparison of lung T2* during free-breathing at 1.5 T and 3.0 T with ultrashort echo time imaging. Magn Reson Med 2011; 66: 248-254
14 Biederer J, Beer M, Hirsch W. et al. MRI of the lung (2/3). Why ... when ... how?. Insights Imaging 2012; 3: 355-371
15 Johnson KM, Fain SB, Schiebler ML. et al. Optimized 3D ultrashort echo time pulmonary MRI. Magnetic Resonance in Medicine 2013; 70: 1241-1250
16 Herrmann KH, Krämer M, Reichenbach JR. Time Efficient 3D Radial UTE Sampling with Fully Automatic Delay Compensation on a Clinical 3T MR Scanner. PLOS ONE 2016; 11: e0150371
17 Marta T, Jan P, Andrea B. et al. Multistage three-dimensional UTE lung imaging by image-based self-gating. Magnetic Resonance in Medicine 2016; 75: 1324-1332
18 Delacoste J, Chaptinel J, Beigelman-Aubry C. et al. A double echo ultra short echo time (UTE) acquisition for respiratory motion-suppressed high resolution imaging of the lung. Magn Reson Med 2018; 79: 2297-2305
19 Jinil P, Taehoon S, Ho YS. et al. A radial sampling strategy for uniform k-space coverage with retrospective respiratory gating in 3D ultrashort-echo-time lung imaging. NMR in Biomedicine 2016; 29: 576-587
20 Glover GH, Pauly JM, Bradshaw KM. Boron‐11 imaging with a three-dimensional reconstruction method. Journal of Magnetic Resonance Imaging 1992; 2: 47-52
21 Duyn JH, Yang Y, Frank JA. et al. Simple Correction Method for k-Space Trajectory Deviations in MRI. J Magn Reson Imaging 1998; 132: 150-153
22 Hafner S. Fast imaging in liquids and solids with the Back-projection Low Angle ShoT (BLAST) technique. Magnetic Resonance Imaging 1994; 12: 1047-1051
23 Madio DP, Lowe IJ. Ultra-fast imaging using low flip angles and fids. Magnetic Resonance in Medicine 1995; 34: 525-529
24 Weiger M, Brunner DO, Dietrich BE. et al. ZTE imaging in humans. Magnetic Resonance in Medicine 2013; 70: 328-332
25 Dournes G, Grodzki D, Macey J. et al. Quiet Submillimeter MR Imaging of the Lung Is Feasible with a PETRA Sequence at 1.5 T. Radiology 2015; 276: 258-265
26 Grodzki DM, Jakob PM, Heismann B. Ultrashort echo time imaging using pointwise encoding time reduction with radial acquisition (PETRA). Magnetic Resonance in Medicine 2012; 67: 510-518
27 Balcom BJ, Macgregor RP, Beyea SD. et al. Single-Point Ramped Imaging withT1Enhancement (SPRITE). Journal of Magnetic Resonance, Series A 1996; 123: 131-134
28 Pauly JM. Selective Excitation for Ultrashort Echo Time Imaging. John Wiley & Sons, Ltd; 2007
29 Triphan SMF, Breuer FA, Gensler D. et al. Oxygen enhanced lung MRI by simultaneous measurement of T1 and T2* during free breathing using ultrashort TE. Journal of Magnetic Resonance Imaging 2015; 41: 1708-1714
30 Togao O, Tsuji R, Ohno Y. et al. Ultrashort echo time (UTE) MRI of the lung: Assessment of tissue density in the lung parenchyma. Magnetic Resonance in Medicine 2010; 64: 1491-1498
31 Lederlin M, Crémillieux Y. Three-dimensional assessment of lung tissue density using a clinical ultrashort echo time at 3 tesla: A feasibility study in healthy subjects. Journal of Magnetic Resonance Imaging 2014; 40: 839-847
32 Biederer Jr, Schoene A, Freitag S. et al. Simulated pulmonary nodules implanted in a dedicated porcine chest phantom: sensitivity of MR imaging for detection 1. Radiology 2003; 227: 475-483
33 Sommer G, Tremper J, Koenigkam-Santos M. et al. Lung nodule detection in a high-risk population: Comparison of magnetic resonance imaging and low-dose computed tomography. European Journal of Radiology 2014; 83: 600-605
34 Burris NS, Johnson KM, Larson PEZ. et al. Detection of small pulmonary nodules with ultrashort echo time sequences in oncology patients by using a PET/MR system. Radiology 2015; 278: 239-246
35 Ohno Y, Koyama HH, Yoshikawa T. et al. Standard-, Reduced- and No-Dose Thin-Section Radiological Examinations: Comparison of Capability for Nodule Detection and Nodule Type Assessment in Patients Suspected of Having Pulmonary Nodules. Radiology 2017 (in press)
36 Wielpütz MO, Lee HY, Koyama H. et al. Morphological Characterization of Pulmonary Nodules With Ultrashort TE MRI at 3T. Am J Roentgenol 2018; 210: 1216-1225
37 Ohno Y, Koyama H, Yoshikawa T. et al. Pulmonary high-resolution ultrashort TE MR imaging: Comparison with thin-section standard- and low-dose computed tomography for the assessment of pulmonary parenchyma diseases. Journal of Magnetic Resonance Imaging 2016; 43: 512-532
38 Hahn AD, Higano NS, Walkup LL. et al. Pulmonary MRI of neonates in the intensive care unit using 3D ultrashort echo time and a small footprint MRI system. Journal of Magnetic Resonance Imaging 2017; 45: 463-471
39 Niwa T, Nozawa K, Aida N. Visualization of the airway in infants with MRI using pointwise encoding time reduction with radial acquisition (PETRA). J Magn Reson Imaging 2017; 45: 839-844
40 Wielpütz MO, Eichinger M, Biederer J. et al. Imaging of Cystic Fibrosis Lung Disease and Clinical Interpretation. Fortschr Röntgenstr 2016; 188: 834-845
41 Eichinger M, Optazaite DE, Kopp-Schneider A. et al. Morphologic and functional scoring of cystic fibrosis lung disease using MRI. European Journal of Radiology 2012; 81: 1321-1329
42 Puderbach M, Eichinger M, Haeselbarth J. et al. Assessment of morphological MRI for pulmonary changes in cystic fibrosis (CF) patients: comparison to thin-section CT and chest x-ray. Investigative radiology 2007; 42: 715-724
43 Mall MA, Stahl M, Graeber SY. et al. Early detection and sensitive monitoring of CF lung disease: Prospects of improved and safer imaging. Pediatric Pulmonology 2016; 51: S49-S60
44 Wielpütz MO, Puderbach M, Kopp-Schneider A. et al. Magnetic Resonance Imaging Detects Changes in Structure and Perfusion, and Response to Therapy in Early Cystic Fibrosis Lung Disease. Am J Respir Crit Care Med 2014; 189: 956-965
45 Edelman RR, Hatabu H, Tadamura E. et al. Noninvasive assessment of regional ventilation in the human lung using oxygen-enhanced magnetic resonance imaging. Nat Med 1996; 2: 1196-1236
46 Pracht ED, Arnold JFT, Wang T. et al. Oxygen-enhanced proton imaging of the human lung using T2*. Magn Reson Med 2005; 53: 1193-1196
47 Hemberger KR, Jakob PM, Breuer FA. Multiparametric oxygen-enhanced functional lung imaging in 3D. Magma (New York, NY) 2015; 28: 217-226
48 Kruger SJ, Fain SB, Johnson KM. et al. Oxygen-enhanced 3D radial ultrashort echo time magnetic resonance imaging in the healthy human lung. NMR in biomedicine 2014; 27: 1535-1541
49 Zha W, Kruger SJ, Johnson KM. et al. Pulmonary ventilation imaging in asthma and cystic fibrosis using oxygen-enhanced 3D radial ultrashort echo time MRI. J Magn Reson Imaging 2018; 47: 1287-1297
50 Sheikh K, Guo F, Capaldi DP. et al. Ultrashort echo time MRI biomarkers of asthma. J Magn Reson Imaging 2017; 45: 1204-1215
51 Ohno Y, Koyama H, Yoshikawa T. et al. T2* measurements of 3-T MRI with ultrashort TEs: capabilities of pulmonary function assessment and clinical stage classification in smokers. American Journal of Roentgenology 2011; 197: W279-W285
52 Ohno Y, Nishio M, Koyama H. et al. Pulmonary MR imaging with ultra-short TEs: utility for disease severity assessment of connective tissue disease patients. European journal of radiology 2013; 82: 1359-1365
53 Ohno Y, Nishio M, Koyama H. et al. Pulmonary 3 T MRI with ultrashort TEs: Influence of ultrashort echo time interval on pulmonary functional and clinical stage assessments of smokers. Journal of Magnetic Resonance Imaging 2014; 39: 988-997
54 Jakob PM, Wang T, Schultz G. et al. Assessment of human pulmonary function using oxygen-enhanced T1 imaging in patients with cystic fibrosis. Magn Reson Med 2004; 51: 1009-1016
55 Jobst BJ, Triphan SMF, Sedlaczek O. et al. Functional Lung MRI in Chronic Obstructive Pulmonary Disease: Comparison of T1 Mapping, Oxygen-Enhanced T1 Mapping and Dynamic Contrast Enhanced Perfusion. PLoS ONE 2015; 10: e0121520
56 Hopkins SR, Wielpütz MO, Kauczor HU. Imaging lung perfusion. J Appl Physiol 2012; 113: 328-339
57 Triphan SMF, Jobst BJ, Breuer FA. et al. Echo time dependence of observed T1 in the human lung. Journal of Magnetic Resonance Imaging 2015; 42: 610-616
58 Bauman G, Johnson KM, Bell LC. et al. Three-dimensional pulmonary perfusion MRI with radial ultrashort echo time and spatial–temporal constrained reconstruction. Magnetic Resonance in Medicine 2015; 73: 555-564
59 Bell LC, Johnson KM, Fain SB. et al. Simultaneous MRI of lung structure and perfusion in a single breathhold. Journal of Magnetic Resonance Imaging 2015; 41: 52-59
60 Bannas P, Bell LC, Johnson KM. et al. Pulmonary embolism detection with three-dimensional ultrashort echo time MR imaging: experimental study in canines. Radiology 2015; 278: 413-421
61 Tibiletti M, Bianchi A, Stiller D. et al. Pulmonary perfusion quantification with flow-sensitive inversion recovery (FAIR) UTE MRI in small animal imaging. NMR Biomed 2016; 29: 1791-1799