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Library of Congress Cataloging in Publication Data

Names: Tsougos, Ioannis, author.

Title: Advanced MR neuroimaging : from theory to clinical practice / Ioannis Tsougos. Other titles: Series in medical physics and biomedical engineering.

Description: Boca Raton, FL : CRC Press, Taylor & Francis Group, [2018] |

Series: Series in medical physics and biomedical engineering | Includes bibliographical references and index. Identifiers: LCCN 2017037811| ISBN 9781498755238 (hardback ; alk. paper) |

ISBN 1498755232 (hardback ; alk. paper) | ISBN 9781498755252 (e-book) | ISBN 1498755259 (e-book)

Subjects: LCSH: Brain–Magnetic resonance imaging. | Magnetic resonance imaging. Classification: LCC RC386.6.M34 T73 2018 | DDC 616.8/04754–dc23

LC record available at https://lccn.loc.gov/2017037811

Visit the Taylor & Francis Web site at http://www.taylorandfrancis.com

and the CRC Press Web site at http://www.crcpress.com

Series Preface		.............................................................................................................	xi
Preface	....................................................................................................................		xiii
About the Author.....................................................................................................			xv
1 Diffusion MR Imaging
1.1	Introduction .........................................................................................................................................		1
	1.1.1	Diffusion	1
...................................................................	1.1.2	Diffusion in Magnetic Resonance Imaging	2
1.2 ...............................................................................................Diffusion Imaging: Basic Principles			3
...........................................................................................	1.2.1	Diffusion - Weighted Imaging	3
	1.2.2	The b - Value	5
........................................................................................	1.2.3	Apparent Diffusion Coefficient	8
...............................................................................	1.2.4	Isotropic or Anisotropic Diffusion?	10
........................................................................................................	1.2.5	Echo Planar Imaging	12
................................................................................................	1.2.6	Main Limitations of DWI	13
1.3 ...............................................................................................................	Diffusion Tensor Imaging		14

1.3.1“Rotationally Invariant” Parameters (Mean Diffusivity and Fractional

		Anisotropy)	17
	1.3.2	Fiber Tractography	19
1.4	Conclusions and Future Perspectives..........................................................................................		22
References ......................			23

2 Artifacts and Pitfalls in Diffusion MRI

2.1	Introduction.....................................................................................................................................		29
2.2	Artifacts and Pitfalls Categorization...........................................................................................		30
2.3	Artifacts from the Gradient System.............................................................................................		30
	2.3.1	Eddy Current Artifacts...................................................................................................	30
	2.3.2	Eddy Currents—Mitigating Strategies.........................................................................	32
2.4	Motion Artifacts..............................................................................................................................		33
	2.4.1	Motion Artifacts—Mitigating Strategies.....................................................................	35
	2.4.2	EPI Specific Artifacts.......................................................................................................	35
	2.4.3	Distortions Originating from B0 Inhomogeneities....................................................	36
	2.4.4	Misregistration Artifacts from Eddy Currents and Subject Motion.......................	36
	2.4.5	Mitigating Strategies—EPI Specific..............................................................................	37
2.5	Artifacts Due to Properties of the Subject Being Imaged and “Physiological” Noise..........		38
	2.5.1	Susceptibility-Induced Distortions...............................................................................	38
	2.5.2	Physiological Noise..........................................................................................................	38

vi			Contents
2.5.3	Susceptibility Effects and Physiological Noise—Mitigating Strategies		................... 39
2.6 Processing and Interpretation Pitfalls		.........................................................................................	40
2.6.1	Preprocessing of Data......................................................................................................		40
2.6.2	Quantitation of Parameters............................................................................................		42
2.6.3	Dependence of Estimated Mean Diffusivity on b-Factor..........................................		45
2.6.4	Effect on ROI Positioning and Bias on Parametric Maps..........................................		45
2.6.5	CSF Contamination in Tract Specific Measurements................................................		47
2.6.6	Intrasubject and Intersubject Comparisons................................................................		47
2.7 Mitigating Strategies—Available Methods and Software for Diffusion Data Correction... 48
2.7.1	RESTORE Algorithm......................................................................................................		48
2.7.2	ExploreDTI		49
2.7.3	FSL-FDT		49
2.7.4	FreeSurfer—TRACULA..................................................................................................		49
2.7.5	TORTOISE		50

2.8Conclusion........................................................................................................................................ 50

References				...................... 50
3 Perfusion MR Imaging
3.1	Introduction.....................................................................................................................................			55
3.2	DSC MRI..........................................................................................................................................			56
	3.2.1	DSC Imaging Explained.................................................................................................		58
	3.2.2	DSC Perfusion Parameters: CBV, CBF, MTT..............................................................		58
		3.2.2.1	CBV	58
		3.2.2.2	CBF	60
		3.2.2.3	MTT	.61
3.3	DCE-MRI.........................................................................................................................................			.61
	3.3.1	DCE Imaging Explained.................................................................................................		62
3.4	ASL ......................			66
	3.4.1	ASL Imaging Explained..................................................................................................		66
	3.4.2	Different ASL Techniques...............................................................................................		66
		3.4.2.1	CASL and pCASL...........................................................................................	67
		3.4.2.2	PASL	68
		3.4.2.3	VSASL	68
	3.4.3	ASL beyond CBF Estimation..........................................................................................		69
3.5	Conclusions and Future Perspectives..........................................................................................			69
References ......................				70
4 Artifacts and Pitfalls of Perfusion MRI
4.1	Introduction.....................................................................................................................................			75
4.2	Dynamic Susceptibility Contrast (DSC) Imaging Limitations...............................................			76
	4.2.1	Subject Motion		76
	4.2.2	Relationship between MR Signal and Contrast Concentration...............................		76
	4.2.3	Bolus Delay and Dispersion............................................................................................		77
	4.2.4	BBB Disruption and Leakage Correction....................................................................		77
	4.2.5	Absolute versus Relative Quantification......................................................................		78
4.3	Dynamic Contrast Enhancement (DCE) Imaging Limitations...............................................			79
	4.3.1	Suitability of Tumor Lesions..........................................................................................		79
	4.3.2	Subject Motion		79
	4.3.3	Estimation of Arterial Input Function (AIF)..............................................................		79
	4.3.4	Temporal and Spatial Resolutions.................................................................................		80
	4.3.5	Variability of Results According to the Models Used................................................		80

Contents		vii
4.3.6	Quality Assurance	80
4.4 Arterial Spin Labeling (ASL) Imaging Limitations...................................................................		.81
4.4.1	Subject Motion	.81
4.4.2	Physiological Signal Variations......................................................................................	82
4.4.3	Magnetic Susceptibility Artifacts..................................................................................	83
4.4.4	Coil Sensitivity Variations..............................................................................................	84
4.4.5	Labeling Efficiency...........................................................................................................	84
4.4.6	Transit Time Effects.........................................................................................................	84
4.4.7	Errors from Quantification Models..............................................................................	85
4.5 Conclusions and Future Perspectives..........................................................................................		85
References ......................		86

Magnetic Resonance Spectroscopy

5.1	Introduction.....................................................................................................................................		.91
5.2	MRS Basic Principles Explained...................................................................................................		93
	5.2.1	Technical Issues	95
	5.2.2	Data Acquisition	95
	5.2.3	Field Strength (B0)	98
	5.2.4	Voxel Size Dependency..................................................................................................	100
	5.2.5	Shimming	101
	5.2.6	Water and Lipid Suppression Techniques...................................................................	102
5.3	MRS Metabolites and Their Biological and Clinical Significance..........................................		104
	5.3.1	Myo-Inositol	104
	5.3.2	Choline-Containing Compounds................................................................................	106
	5.3.3	Creatine and Phosphocreatine......................................................................................	107
	5.3.4	Glutamate and Glutamine.............................................................................................	107
	5.3.5	N-Acetyl Aspartate	107
	5.3.6	Lactate and Lipids	108
	5.3.7	Less Commonly Detected Metabolites........................................................................	108
5.4	MRS Quantification and Data Analysis.....................................................................................		110
	5.4.1	Quantification	110
	5.4.2	Post Processing Techniques...........................................................................................	.111
5.5	Quality Assurance in MRS...........................................................................................................		113

5.6Conclusion....................................................................................................................................... 113

References .....................

114

Artifacts and Pitfalls of MRS

6.1	Introduction....................................................................................................................................			123
6.2	Artifacts and Pitfalls......................................................................................................................			124
	6.2.1	Effects of Patient Movement..........................................................................................		124
	6.2.2	Field Homogeneity and Linewidth...............................................................................		124
	6.2.3	Frequency Shifts and Temperature Variations...........................................................		125
	6.2.4	Voxel Positioning		126
	6.2.5	Use of Contrast and Positioning in MRS....................................................................		128
	6.2.6	Chemical Shift Displacement........................................................................................		129
	6.2.7	Spectral Contamination or Voxel Bleeding................................................................		130
	6.2.8	To Quantify or Not to Quantify?..................................................................................		131
		6.2.8.1	Relative Quantification................................................................................	131
		6.2.8.2	Absolute Quantification...............................................................................	132
	6.2.9	Available Software Packages for Quantification and Analysis of MRS Data........		134
		6.2.9.1	LCModel	134

viii		Contents
6.2.9.2	jMRUI	135
6.2.9.3	TARQUIN	135
6.2.9.4	SIVIC	136

6.2.9.5AQSES 137

6.3Conclusion.......................................................................................................................................138

References .....................				138
7 Functional Magnetic Resonance Imaging (fMRI)
7.1	Introduction....................................................................................................................................			141
	7.1.1	What Is Functional Magnetic Resonance Imaging (fMRI) of the Brain?..............		141
	7.1.2	Blood Oxygenation Level Dependent (BOLD) fMRI................................................		142
	7.1.3	fMRI Paradigm Design and Implementation............................................................		144
		7.1.3.1	Blocked versus Event-Related Paradigms..................................................	145
		7.1.3.2	Mixed Paradigm Designs............................................................................	146
7.2	fMRI Acquisitions—MR Scanning Sequences..........................................................................			148
	7.2.1	Spatial Resolution		148
	7.2.2	Temporal Resolution......................................................................................................		148
	7.2.3	Pulse Sequences Used in fMRI.....................................................................................		149
7.3	Analysis and Processing of fMRI Experiments........................................................................			151
	7.3.1	fMRI Datasets		151
	7.3.2	Data Preprocessing		152
		7.3.2.1	Slice-Scan Timing Correction....................................................................	152
		7.3.2.2	Head Motion Correction.............................................................................	152
		7.3.2.3	Distortion Correction..................................................................................	153
		7.3.2.4	Spatial and Temporal Smoothing...............................................................	153
	7.3.3	Statistical Analysis		153
7.4	Pre-Surgical Planning with fMRI...............................................................................................			154
7.5	Resting State fMRI.........................................................................................................................			154
	7.5.1	Resting State fMRI Procedure......................................................................................		155
7.6	Conclusion and the Future of fMRI............................................................................................			156
References .....................				157
8 Artifacts and Pitfalls of fMRI
8.1	Introduction to Quantitative fMRI Limitations.......................................................................			161
8.2	Image Acquisition Limitations....................................................................................................			162
	8.2.1	Spatial and Temporal Resolution..................................................................................		162
	8.2.2	Spatial and Temporal fMRI Resolution—Mitigating Strategies.............................		164
	8.2.3	EPI-Related Image Distortions.....................................................................................		166
8.3	Physiological Noise and Motion Limitations.............................................................................			167
	8.3.1	Physiological Noise—Mitigating Strategies................................................................		169
		8.3.1.1	Cardiac Gating..............................................................................................	169
		8.3.1.2	Acquisition-Based Image Corrections.......................................................	170
		8.3.1.3	Calibration	170
8.4	Interpretation Limitations............................................................................................................			171
8.5	Quality Assurance in fMRI..........................................................................................................			173

8.6Conclusion.......................................................................................................................................174

References .....................

174

9 The Role of Multiparametric MR Imaging—Advanced MR Techniques in the Assessment of Cerebral Tumors

9.1

Introduction....................................................................................................................................

179

Contents			ix
9.2	Gliomas		............. 181
	9.2.1	DWI Contribution in Gliomas......................................................................................	183
	9.2.2	DTI Contribution in Gliomas.......................................................................................	186
	9.2.3	Perfusion Contribution in Gliomas.............................................................................	187
	9.2.4	MRS Contribution in Gliomas......................................................................................	188
9.3	Cerebral Metastases.......................................................................................................................		189
	9.3.1	DWI/DTI Contribution in Metastases........................................................................	191
	9.3.2	Perfusion Contribution in Metastases.........................................................................	193
	9.3.3	MRS Contribution in Metastases.................................................................................	193
9.4	Meningiomas..................................................................................................................................		194
	9.4.1	DWI/DTI Contribution in Meningiomas...................................................................	194
	9.4.2	Perfusion Contribution in Meningiomas....................................................................	196
	9.4.3	MRS Contribution in Meningiomas............................................................................	197
9.5	Primary Cerebral Lymphoma......................................................................................................		198
	9.5.1	DWI/DTI Contribution in PCLs..................................................................................	198
	9.5.2	Perfusion Contribution in PCLs...................................................................................	198
	9.5.3	MRS Contribution in PCLs...........................................................................................	199
9.6	Intracranial Abscesses..................................................................................................................		200
	9.6.1	DWI DTI Contribution in Abscesses.........................................................................	200
	9.6.2	Perfusion Contribution in Abscesses...........................................................................	201
	9.6.3	MRS Contribution in Abscesses..................................................................................	202
9.7	Summary and Conclusion...........................................................................................................		202
References ....................			203

Index 215

Series Preface

The Series in Medical Physics and Biomedical Engineering describes the applications of physical sciences, engineering, and mathematics in medicine and clinical research.

The series seeks (but is not restricted to) publications in the following topics:

•	Artificial organs	•	Medical/surgical devices
•	Assistive technology	•	Patient monitoring
•	Bioinformatics	•	Physiological measurement
•	Bioinstrumentation	•	Prosthetics
•	Biomaterials	•	Radiation protection, health
•	Biomechanics	•	physics, and dosimetry
•	Biomedical engineering	•	Regulatory issues
•	Clinical engineering	•	Rehabilitation engineering
•	Imaging	•	Sports medicine
•	Implants	•	Systems physiology
•	Medical computing and	•	Telemedicine
	mathematics	•	Tissue engineering
		•	Treatment

The Series in Medical Physics and Biomedical Engineering is an international series that meets the need for up-to-date texts in this rapidly developing field. Books in the series range in level from introductory graduate textbooks and practical handbooks to more advanced expositions of current research.

The Series in Medical Physics and Biomedical Engineering is the official book series of the International Organization for Medical Physics.

The International Organization for Medical Physics

The International Organization for Medical Physics (IOMP) represents over 18,000 medical physicists worldwide and has a membership of 80 national and 6 regional organizations, together with a number of corporate members. Individual medical physicists of all national member organisations are also automatically members.

The mission of IOMP is to advance medical physics practice worldwide by disseminating scientific and technical information, fostering the educational and professional development of medical physics and promoting the highest quality medical physics services for patients.

A World Congress on Medical Physics and Biomedical Engineering is held every three years in cooperation with International Federation for Medical and Biological Engineering (IFMBE)

xii	Series Preface

and International Union for Physics and Engineering Sciences in Medicine (IUPESM). A regionally based international conference, the International Congress of Medical Physics (ICMP) is held between world congresses. IOMP also sponsors international conferences, workshops and courses.

The IOMP has several programmes to assist medical physicists in developing countries. The joint IOMP Library Programme supports 75 active libraries in 43 developing countries, and the Used Equipment Programme coordinates equipment donations. The Travel Assistance Programme provides a limited number of grants to enable physicists to attend the world congresses.

IOMP co-sponsors the Journal of Applied Clinical Medical Physics. The IOMP publishes, twice a year, an electronic bulletin, Medical Physics World. IOMP also publishes e-Zine, an electronic news letter about six times a year. IOMP has an agreement with Taylor & Francis for the publication of the Medical Physics and Biomedical Engineering series of textbooks. IOMP members receive a discount.

IOMP collaborates with international organizations, such as the World Health Organisations (WHO), the International Atomic Energy Agency (IAEA) and other international professional bodies such as the International Radiation Protection Association (IRPA) and the International Commission on Radiological Protection (ICRP), to promote the development of medical physics and the safe use of radiation and medical devices.

Guidance on education, training and professional development of medical physicists is issued by IOMP, which is collaborating with other professional organizations in development of a professional certification system for medical physicists that can be implemented on a global basis.

The IOMP website (www.iomp.org) contains information on all the activities of the IOMP, policy statements 1 and 2 and the ‘IOMP: Review and Way Forward’ which outlines all the activities of IOMP and plans for the future.

Preface

Since its early medical application about 40 years ago, magnetic resonance imaging has revolutionized brain neuroimaging, providing non-invasively excellent high-resolution images without the use of ionizing radiation.

Nevertheless, despite the superior quality, conventional MR imaging provides only anatomical, rather than physiological, information and may therefore be sometimes non-specific.

During the last decade, some of the greatest achievements in neuroimaging have been related to remarkable advances in MR techniques, which provided insights into tissue microstructure, microvasculature, metabolism, and brain connectivity. These advanced MR neuroimaging techniques include diffusion, perfusion, magnetic resonance spectroscopy, and functional MRI.

Previously available mostly in research environments, they are now establishing themselves firmly in the everyday clinical practice in a plethora of clinical MR systems. However, despite the growing interest and wider acceptance, the lack of a comprehensive body of knowledge, the intrinsic complexity and physical difficulty of the techniques, as well as an appreciable number of associated artifacts and pitfalls, still confine their routine clinical application.

This book focuses on the basic principles and physics theory of diffusion, perfusion, magnetic resonance spectroscopy, and functional MRI, accompanied by their clinical applications, with particular emphasis on the associated artifacts and pitfalls using a comprehensive and didactic approach. It aims to bridge the gap between theoretical applications and optimized clinical practice of advanced techniques by addressing all of them in a single and concise volume.

The book is organized in nine chapters. Four chapters (Chapters 1, 3, 5, and 7) describe the basic principles of the discussed techniques, providing an overview of the methods with a step-by-step didactic approach, explaining fundamentals as well as clinical implications. These are, followed by respective dedicated chapters on the potential artifacts and pitfalls of each technique, including the proposed mitigating strategies, with special attention in the postprocessing techniques (Chapters 2, 4, 6, and 8).

The final chapter (Chapter 9) covers a multiparametric approach utilizing all the aforementioned advanced MR techniques, evaluating the different underlying patho-physiological characteristics of brain tumors in an attempt to illustrate the potential ability of these techniques to contribute to a more accurate diagnosis.

Each chapter, as well as several important sections within each chapter, begins with a dedicated “Focus Point” box, “sensitizing” the reader’s attention to the key features, by highlighting the most important concepts that follow. An introduction in every chapter further guides the reader into the forthcoming more detailed information. Lastly, summary tables and aggregated classifications are used in an attempt to facilitate memorization, supporting those who wish to delve into and apply these techniques in the clinical routine.

xiii

xiv

Preface

The book can serve as an educational manual for neuroimaging researchers and basic scientists (radiologists, neurologists, neurosurgeons, medical physicists, engineers, etc.) with an interest in advanced MR techniques, as well as a reference for experienced clinical scientists who wish to optimize their multi-parametric imaging approach.

In conclusion, I sincerely hope this is an easy-to-read yet comprehensive handbook, which can be used as an essential guide to the advanced MR imaging techniques routinely used in clinical practice for the diagnosis and follow-up of patients with brain tumours.

Ioannis Tsougos

Assistant Professor of Medical Physics

Medical School, University of Thessaly

About the Author

Dr. Ioannis Tsougos holds a BSc in physics, and an MSc and a PhD in medical radiation physics. Currently, he is an assistant professor of Medical Radiation Physics at the medical school of the University of Thessaly, Larissa, Greece and a visiting researcher in the Neuroimaging Division at the Institute of Psychiatry, Psychology, and Neuroscience, King’s College London, London, United Kingdom. He has authored more than 75 research papers and 10 international book chapters. In addition, he frequently acts as a reviewer for several journals in medical physics/radiology and European research foundations projects. Dr. Tsougos has broad multidisciplinary teaching and clinical experience, specializing in advanced MR techniques, and he is a member of the EFOMP, ESR, and ESMRMB.

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