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Fluorine Magnetic
Resonance Imaging
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Fluorine Magnetic
Resonance Imaging

edited by
editors Ulrich Flögel
Preben Maegaard
Anna Krenz Eric Ahrens
Wolfgang Palz

The Rise of Modern Wind Energy

Wind Power
for the World
Published by
Pan Stanford Publishing Pte. Ltd.
Penthouse Level, Suntec Tower 3
8 Temasek Boulevard
Singapore 038988

Email: [email protected]
Web: www.panstanford.com

British Library Cataloguing-in-Publication Data

A catalogue record for this book is available from the British Library.

Fluorine Magnetic Resonance Imaging

Copyright © 2017 Pan Stanford Publishing Pte. Ltd.

All rights reserved. This book, or parts thereof, may not be reproduced in any
form or by any means, electronic or mechanical, including photocopying,
recording or any information storage and retrieval system now known or
to be invented, without written permission from the publisher.

For photocopying of material in this volume, please pay a copying fee

through the Copyright Clearance Center, Inc., 222 Rosewood Drive,
Danvers, MA 01923, USA. In this case permission to photocopy is not
required from the publisher.

Cover image: “Universe of Imaging,” courtesy of Prof. Juerg Schwitter,

Division of Cardiology and Cardiac MR Center of the University Hospital
Lausanne, CHUV, Switzerland.

ISBN 978-981-4745-31-4 (Hardcover)

ISBN 978-981-4745-32-1 (eBook)

Printed in the USA

 Contents
Preface xv

Part 1: Technical Issues

1. Pulse Sequence Considerations and Schemes 3

Cornelius Faber and Florian Schmid

1.1 Introduction 3
1.2 General Considerations 5
1.2.1 The Pulse Sequences 5
1.2.2 More General Pulse Sequence Considerations 9
1.3 Sensitivity of Particular Sequences in Parameter
Space 11
1.3.1 SNR Efficiencies and Optimum Parameters
for UTE, FLASH and bSSFP 14
1.3.2 SNR Efficiencies and Optimum Parameters
for RARE 17
1.4 The Best Pulse Sequence for 19F MRI 20
1.5 Implications for Actual 19F MRI Measurements 22
1.6 Further Methods to Increase SNR: Heteronuclear
Overhauser Enhancement 23

2. Advanced Detection Techniques and Hardware:

Simultaneous 19F/1H MRI 29
Lingzhi Hu, Jochen Keupp, Shelton D. Caruthers, Matthew J. Goette,
Gregory M. Lanza, and Samuel A. Wickline

2.1 Imaging Applications of Perfluorocarbon

Nanoparticles and Introduction of Simultaneous
19F/1H MRI 30
2.2 MRI Hardware and Reconstruction for
Simultaneous 19F/1H Imaging 33
vi Contents

2.2.1 Scanner Hardware Design 33

2.2.2 MR Reconstruction Methods 34
2.3 19F/1H Dual-Frequency RF Coil Design and System
Calibration for Simultaneous 19F/1H Imaging 38
2.3.1 19F/1H Dual-Frequency RF Coil Design 38
2.3.2 MR System and RF Coil Calibration for
Simultaneous 19F/1H Imaging 43
2.4 Advanced MR Sequences for Simultaneous 19F/1H

Imaging 46
2.4.1 Balanced Ultrashort TE Steady State-Free
Precession Sequence 47
2.4.2 Fluorine Ultrafast Turbo Spectroscopic
Imaging Sequence 49
2.4.3 Blood-Flow Enhanced Saturation Recovery
Sequence 50
2.5 Conclusion 52

3. Hyperpolarization for Signal Enhancement in Fluorine

MR Applications 59
Ute Bommerich, Johannes Bernarding, Denise Lego,
Thomas Trantzschel, and Markus Plaumann

3.1 Introduction 59
3.2 Hyperpolarization Techniques: History and Physical
Principles 60
3.2.1 Dynamic Nuclear Polarization 61
3.2.2 Chemically Induced Dynamic Nuclear
Polarization 66
3.2.3 Parahydrogen-Induced Polarization 70
3.2.4 Application of HP Methods to MRI 74
3.3 Hyperpolarized 19F: Chronological Results 77
3.3.1 DNP 77
3.3.2 CIDNP 80
3.3.3 PHIP 83
3.4 Perspectives 86
 Contents vii

Part 2: 19F Imaging Agents

4. Active Targeting of Perfluorocarbon Nanoemulsions 103

Sebastian Temme, Christoph Grapentin, Tuba Güden-Silber,
and Ulrich Flögel

4.1 A Short Introduction to Perfluorocarbons and

Perfluorocarbon Nanoemulsions 103
4.2 Generation of Targeted Perfluorocarbon
Nanoemulsions 105
4.2.1 Targeting Ligands 106
4.2.1.1 Antibodies and antibody
derivatives 106
4.2.1.2 Peptides and other targeting
ligands 109
4.2.2 Coupling of Targeting Ligands to PFC-NE 109
4.2.2.1 Functional groups for coupling
reactions 109
4.2.2.2 Generation of targeted PFC-NE 112
4.3 Applications Using Actively Targeted PFC-NE 113
4.3.1 Inflammation 114
4.3.1.1 Imaging immune cells 114
4.3.1.2 Visualization of the activated
endothelium 116
4.3.1.3 Inflammation-associated
angiogenesis 116
4.3.2 Cancer 117
4.3.3 Thrombosis 120
4.3.4 Atherosclerotic Plaques and Restenosis 123
4.3.5 Targeting of Stem Cells 125
4.4 Summary and Outlook 126

5. Responsive Probes for 19F MRS/MRI 141

Aneta Keliris, Klaus Scheffler, and Jörn Engelmann

5.1 Introduction 141

5.2 Response Mechanisms 143
viii Contents

5.3 Classes of 19F Responsive Probes 144

5.3.1 pH-Activatable 19F Probes 144
5.3.2 Metal Ion Responsive 19F Sensors 147
5.3.3 Responsive 19F Probes for Detection of
Proteins and Their Function 149
5.3.3.1 Enzyme responsive probes 150
5.3.3.2 Sensing non-enzymatic proteins
and nucleic acids 155
5.3.4 19 F Probes Responsive to pO2 158
5.4 Sensitivity and Detection Levels for 19F MRI/MRS 159
5.5 Conclusions 161

Part 3: Inflammation Imaging

6. Imaging Acute Organ Transplant Rejection with 19F MRI 171

T. Kevin Hitchens, Lesley M. Foley, and Qing Ye

6.1 Organ Transplantation 171

6.2 Organ Rejection 173
6.3 In vivo Macrophage Labeling and MRI Cell
Tracking 174
6.4 Detection of Acute Kidney Transplant Rejection
Using MRI Cell Tracking 176
6.5 Detection of Acute Allograft Rejection in the
Heart with MRI Cell Tracking 180
6.6 Conclusions 185

7. Cardiac Disease 191

Ruud B. van Heeswijk, Christine Gonzales, and Juerg Schwitter

7.1 Introduction 191

7.2 Motion Compensation and Pulse Sequences 195
7.2.1 Cardiac Motion 195
7.2.2 Respiratory Motion 196
7.2.3 Bulk Motion 198
7.3 Animal Models of Cardiovascular Diseases 199
7.3.1 Angiography 199
 Contents ix

7.3.2 Myocarditis 199

7.3.3 Heart Transplantation 202
7.3.4 Myocardial Infarction 203
7.3.5 Atherosclerosis 207
7.4 In vitro 19F-Labeling of Inflammatory Cells 209
7.5 Conclusions and Perspectives 210

Part 4: Monitoring of Specific Cell Populations

8. Tracking Lymphocytes in vivo 221
Ghaith Bakdash and Mangala Srinivas

8.1 Introduction 222

8.2 Lymphocytes 222
8.2.1 Function 222
8.2.2 Migration 223
8.2.3 Autoimmune Disease, Cancer and
Transplant Rejection 225
8.3 Lymphocyte Tracking with Other Imaging
Modalities 226
8.3.1 Nuclear Imaging Techniques 226
8.3.2 Fluorescence Imaging and Microscopy 227
8.4 MRI for Tracking Lymphocytes 228
8.4.1 Iron-Based Imaging 229
8.4.2 Gadolinium-Based Imaging 231
8.5 19F MRI for Tracking Lymphocytes 231
8.5.1 Labels and Cell Loading 231
8.5.2 In vivo Imaging Data 233
8.5.3 Ex vivo Studies 236
8.6 Conclusion 237

9. Tracking of Dendritic Cells 243

Sonia Waiczies, MinChi Ku, and Thoralf Niendorf

9.1 Introduction 243

9.2 About Dendritic Cells 244
9.2.1 Dendritic Cell Classification: Challenges
Ahead 245
 Contents

9.2.2 Dendritic Cells in Health and Disease 246

9.2.2.1 Dendritic cells in autoimmunity 246
9.2.2.2 Dendritic cells in tumor and
infectious disease 247
9.3 Why Is Tracking of Dendritic Cells So Important? 248
9.3.1 Dendritic Cell Immunotherapy 249
9.3.2 In vitro Generation of Mouse and Human
DCs 251
9.3.3 How Can We Modulate Dendritic Cells
as Therapies 252
9.4 Tracking Methods for Dendritic Cells 253
9.4.1 Optical Imaging: Bioluminescence and
Fluorescence Tomography 254
9.4.2 Nuclear Imaging: Scintigraphy, SPECT,
and PET 255
9.4.3 Cell Tracking Using Magnetic Resonance
Methods 257
9.4.3.1 Contrast agents modulating
relaxation times 258
9.4.3.2 Fluorine magnetic resonance 259
9.5 Conclusion 266

10. Neural Stem Cells 283

Markus Aswendt, Philipp Boehm-Sturm, and Mathias Hoehn

10.1 Introduction 283

10.2 Neural Stem Cells Used for Cell Therapy 284
10.2.1 Definition 284
10.2.2 Mechanisms of Action in Therapy 286
10.2.3 19F MRI of NSCs 287
10.3 Labeling NSCs for in vivo Tracking Using 19F MRI 289
10.3.1 19F Cell Labels 289
10.3.2 Optimization of 19F Cellular Uptake 291
10.3.3 Cell Characterization 292
10.4 In vitro and in vivo 19F MRI of NSCs 295
10.4.1 Cell Preparation and Implantation 295
 Contents xi

10.4.2 Imaging Hardware and Pulse Sequences 295

10.4.3 Estimating Cell Detection Limit 296
10.5 Validation 297
10.5.1 Determining the Location of Transplanted
Cells and the 19F Cell Label by Histology 297
10.5.2 Multimodal Approaches: The Better
Imaging? 299
10.6 Summary 299

Part 5: Pharmacology

11. Fluorinated Natural Compounds and Synthetic Drugs 311

Thoralf Niendorf, Yiyi Ji, and Sonia Waiczies

11.1 Introduction 311

11.2 Organofluorine Compounds 312
11.2.1 Naturally Occurring Organofluorine
Compounds 312
11.2.2 Redesign and Scale-Up of Natural
Synthesis 314
11.2.3 Organofluorine Synthesis 315
11.2.4 Advantages of Incorporating Fluorine
to Bioactive Molecules 316
11.2.4.1 Changes in polarity 317
11.2.4.2 Influence on lipophilicity 317
11.2.4.3 Changes in the acid
dissociation constant 318
11.2.4.4 Influence on metabolic
stability 318
11.2.5 Organofluorine Compounds in
Medicinal Chemistry 319
11.2.5.1
Fluorine in the pharmaceutical
industry 320
11.3 Fluorine MR-Based Spectroscopy
11.3.1 Pharmacokinetic Studies Employing 19F
MR Spectroscopy 325
xii Contents

11.3.2 Methods of Studying 19F Drugs in vivo 326

11.3.2.1 From in vitro to animal and
human 19F MRS studies 327
11.3.2.2 19F MR imaging studies of
fluorinated drugs 329
11.3.2.3 19F MRI of fluorinated drugs at
ultrahigh magnetic field
strength 329
11.3.2.4 The future 331
11.4 Conclusion 332

Part 6: Other Biomedical Applications

12. Imaging of the Respiratory System 345

Marcus J. Couch, Alexei V. Ouriadov, and Mitchell S. Albert

12.1 Introduction 346

12.2 1H MRI of the Lung 347
12.3 Hyperpolarized Noble Gas MRI 349
12.4 Properties of Inert Fluorinated Gas MRI 351
12.5 Static Breath-Hold Imaging 354
12.6 Dynamic Imaging 359
12.7 Diffusion Imaging 362
12.8 V/Q Measurement 364
12.9 Gravitational Distribution 366
12.10 Conclusions 368

13. Tracking of Capsules and Catheters in the Human

Gastrointestinal Tract 379
Andreas Steingötter and Tobias Hahn

13.1 19F
for GI Applications 379
13.1.1 Gastrointestinal (GI) Function 379
13.1.2 Imaging of GI Function 380
13.1.3 Monitoring of GI Drug Delivery 381
13.1.4 Requirements for Combined 19F/1H
MRI of the GI Tract 382
13.2 19F Labeling of Capsules and Catheters 383
 Contents xiii

13.2.1 Dual-Shell 19F Capsule 384

13.2.2 Single-Shell 19F Capsule 386
13.2.3 19F-Labeled GI Catheter 387
13.3 In vivo 19F Tracking: Methodology and Application 388
13.3.1 Tracking by Cartesian Projection 388
13.3.2 In vivo Dual Compound Tracking by
Cartesian Projection 390
13.3.3 Tracking Multiple 19F Signal Sources by
3D Golden Angle Radial Imaging 393
13.4 Real-Time 19F Tracking System 396
13.5 Conclusion and Outlook 400

Part 7: Perspectives

14. Perfluorocarbon Theranostic Nanomedicines:

Pharmaceutical Scientist’s Perspective 407
Jelena M. Janjic and Sravan K. Patel

14.1 Theranostic Nanomedicines as Future Medicines 407

14.2 Perfluorocarbons as Building Blocks for
Theranostic Nanomedicines 411
14.3 Triphasic Perfluorocarbon Nanoemulsions as
a Theranostic Platform 412
14.4 Macrophage-Targeted Perfluorocarbon
Theranostic Nanoemulsions 417
14.5 Pharmaceutical Perspective on Perfluorocarbon
Theranostics 422
14.6 Conclusions 424

Index 433
 Preface

This book provides an overview of the state of the art in

engineering and biomedical applications of fluorine-19 (19F)
magnetic resonance imaging (MRI). The 19F nucleus is intrinsically
an excellent MRI probe because it has 100% natural abundance,
nuclear spin-1/2, comparable sensitivity to proton, and there
is no background 19F signal in the body. MRI using 19F was first
demonstrated in the 1970s during MRI’s early development. A
variety of 19F-laden materials were investigated as potential
“tracer” agents. Further interest in 19F MRI evolved in the 1980s
and 1990s, when there was significant commercial interest in
developing perfluorocarbon (PFC) emulsion formulations for use
as artificial blood substitutes. This effort helped to devise strategies
for the production of stable, non-toxic PFC emulsion formulations,
in addition to elucidating the safety profiles of these materials,
including pharmacokinetics. During the same period, 19F MRI was
used to study PFCs, for example, as potential angiographic and
oximetry agents; however, 19F imaging during this epoch could still
be characterized as esoteric.
The use of 19F MRI has been reinvigorated in recent years. A
key motivator of this renewed interest surrounds imaging probe
development for the bourgeoning field of in vivo cellular and
molecular imaging. The 19F MRI resurgence also coincides with
the increased use of fluorous chemistry in biomedicine; drug
candidates are increasingly incorporating the fluorine atom.
Fluorine can impart unique properties to compounds, including
metabolic stability, enhanced binding interactions, and selective
reactivities. A further motivator for 19F probe development stems
from increased interest in alternatives to metal-ion based MRI
contrast agents due to the recent awareness of potential toxicities
associated with clinically approved agents, as well as technological
challenges associated with image specificity and quantification
with traditional contrast agents.
This book presents a snapshot of the current activities
surrounding the use of 19F MRI in biomedical research. It covers
xvi Preface

a breadth of topics, including MRI pulse sequence development,

radio frequency hardware considerations, probe chemistry and
formulation, nuclear hyperpolarization, targeted and “smart”
probes, imaging fluorinated drug biodistribution, in vivo
biomedical device imaging, tracking stem and immune cells in
the body, and imaging inflammatory events in the body.
Our view is that the future for 19F is bright. There has been a
groundswell of research interest in 19F MRI, which has evolved into
totally new uses and markets for the MRI technique. As described
in this volume, there are significant avenues for future
improvements in the sensitivity of 19F MRI detection. However, in the
near term, a limiting factor in the growth of 19F MRI is economics;
large-scale MRI research and clinical macro trends are driven, to a
significant degree, by the hardware and software features offered
by MRI manufactures. A bottleneck in the clinical adoption is the
availability of suitable scanner hardware to image 19F in a hospital
setting. However, as technical developments, compelling biomedical
applications, and clinical trial data continue to proliferate, this
bottleneck will subside.
Finally, we offer our sincerest appreciation to all of the
contributors to this book. We feel honored to have had the
opportunity to have shepherded these excellent manuscripts. We
hope that readers will find this volume enlightening and that it
will help stimulate new efforts in 19F MRI.

Ulrich Flögel
Eric Ahrens
 Part 1
Technical Issues
Chapter 1

Pulse Sequence Considerations and

Schemes

Cornelius Faber and Florian Schmid

Department of Clinical Radiology, University Hospital Münster,
48149 Münster, Germany
[email protected]

1.1 Introduction
Since publication of the first 19F magnetic resonance images, a
wide range of potential applications of fluorine MRI in biomedical
imaging have been explored. In particular, since Ahrens and co-
workers have shown that distinct cellular populations can be
labeled with fluorine-containing compounds and subsequently
detected by 19F MRI, this technology has been an accepted method
in the molecular imaging toolbox (Ahrens et al., 2005; Ruiz-
Cabello et al., 2011; Yu et al., 2013). As detailed in other chapters
in this book, 19F possesses a high gyromagnetic ratio (94% of 1H),
which provides an intrinsically high MR signal. A 100% isotopic
abundance and the almost complete lack of any detectable
fluorine signal in the mammalian body makes 19F the ideal nucleus
for cell tracking and molecular imaging approaches by MRI.
Most importantly, 19F provides unambiguous identification of

Fluorine Magnetic Resonance Imaging

Edited by Ulrich Flögel and Eric Ahrens
Copyright © 2017 Pan Stanford Publishing Pte. Ltd.
ISBN 978-981-4745-31-4 (Hardcover), 978-981-4745-32-1 (eBook)
www.panstanford.com
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