Magnetic resonance imaging in tissue engineering

427 Pages·2017·9.94 MB·English

by  Kotecha, Mrignayani, Magin, Richard L., Mao, Jeremy J

Magnetic Resonance Imaging in Tissue Engineering
Magnetic Resonance Imaging in Tissue
Engineering
Edited by Mrignayani Kotecha, Richard L. Magin,
and Jeremy J. Mao
This edition first published 2017
© 2017 John Wiley & Sons, Inc.
All rights reserved. No part of this publication may be reproduced, stored in a retrieval system,
or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording
or otherwise, except as permitted by law. Advice on how to obtain permission to reuse material
from this title is available at http://www.wiley.com/go/permissions.
The right of Mrignayani Kotecha, Richard L. Magin, and Jeremy J. Mao to be identified as the
author(s) of this work has been asserted in accordance with law.
Registered Offices
John Wiley & Sons, Inc., 111 River Street, Hoboken, NJ 07030, USA
Editorial Office
111 River Street, Hoboken, NJ 07030, USA
For details of our global editorial offices, customer services, and more information about
Wiley products visit us at www.wiley.com.
Wiley also publishes its books in a variety of electronic formats and by print‐on‐demand.
Some content that appears in standard print versions of this book may not be available in other
formats.
Limit of Liability/Disclaimer of Warranty
The publisher and the authors make no representations or warranties with respect to the
accuracy or completeness of the contents of this work and specifically disclaim all warranties;
including without limitation any implied warranties of fitness for a particular purpose. This
work is sold with the understanding that the publisher is not engaged in rendering professional
services. The advice and strategies contained herein may not be suitable for every situation. In
view of on‐going research, equipment modifications, changes in governmental regulations, and
the constant flow of information relating to the use of experimental reagents, equipment, and
devices, the reader is urged to review and evaluate the information provided in the package insert
or instructions for each chemical, piece of equipment, reagent, or device for, among other things,
any changes in the instructions or indication of usage and for added warnings and precautions.
The fact that an organization or website is referred to in this work as a citation and/or potential
source of further information does not mean that the author or the publisher endorses the
information the organization or website may provide or recommendations it may make. Further,
readers should be aware that websites listed in this work may have changed or disappeared
between when this works was written and when it is read. No warranty may be created or
extended by any promotional statements for this work. Neither the publisher nor the author shall
be liable for any damages arising here from.
Library of Congress Cataloguing‐in‐Publication data has been applied for
ISBN: 9781119193357
Cover image courtesy Temel Kaya Yasar
Cover design by Wiley
Set in 10/12pt Warnock by SPi Global, Pondicherry, India
10 9 8 7 6 5 4 3 2 1
v
Contents
List of Plates xiii
About the Editors xix
List of Contributors xxi
Foreword xxv
Preface xxvii
Book Summary xxxi
Part I Enabling Magnetic Resonance Techniques for Tissue
Engineering Applications 1
1 Stem Cell Tissue Engineering and Regenerative Medicine:
Role of Imaging 3
Bo Chen, Caleb Liebman, Parisa Rabbani, and Michael Cho
1.1 Introduction 3
1.2 3D Biomimetics 5
1.3 Assessment of Stem Cell Differentiation and Tissue Development 8
1.4 Description of Imaging Modalities for Tissue Engineering 8
1.4.1 Optical Microscopy 9
1.4.2 Fluorescence Microscopy 9
1.4.3 Multiphoton Microscopy 11
1.4.4 Magnetic Resonance Imaging 14
Acknowledgments 15
References 15
2 Principles and Applications of Quantitative Parametric MRI
in Tissue Engineering 21
Mrignayani Kotecha
2.1 Introduction 21
2.2 Basics of MRI 25
2.2.1 Nuclear Spins 25
vi Contents
2.2.2 Radio Frequency Pulse Excitation and Relaxation 28
2.2.3 From MRS to MRI 31
2.3 MRI Contrasts for Tissue Engineering Applications 32
2.3.1 Chemical Shift 33
2.3.2 Relaxation Times—T and T 33
1 2
2.3.3 Water Apparent Diffusion Coefficient 36
2.3.4 Fractional Anisotropy 37
2.4 X ‐Nuclei MRI for Tissue Engineering Applications 38
2.5 P reparing Engineered Tissues for MRI Assessment 38
2.5.1 In Vitro Assessment 38
2.5.2 In Vivo Assessment 39
2.6 L imitations of MRI Assessment in Tissue Engineering 39
2.7 F uture Directions 40
2.7.1 Biomolecular Nuclear Magnetic Resonance 40
2.7.2 Cell–ECM–Biomaterial Interaction 40
2.7.3 Quantitative MRI 40
2.7.4 Standardization of MRI Methods for In Vitro and In Vivo
Assessment 40
2.7.5 Super‐Resolution MRI Techniques 41
2.7.6 Magnetic Resonance Elastography 41
2.7.7 Benchtop MRI 41
2.8 C onclusions 41
References 42
3 High Field Sodium MRS/MRI: Application to Cartilage Tissue
Engineering 49
Mrignayani Kotecha
3.1 Introduction 49
3.2 Sodium as an MR Probe 50
3.3 Pulse Sequences 53
3.3.1 Pulse Sequences for Measuring TSC 53
3.3.2 TQC Pulse Sequences for Measuring ω and ω τ 54
Q 0 c
3.4 Assessment of Tissue‐Engineered Cartilage 55
3.4.1 Proteoglycan Assessment 57
3.4.2 Assessment of Tissue Anisotropy and Molecular Dynamics 60
3.4.3 Assessment of Osteochondral Tissue Engineering 61
3.5 Sodium Biomarkers for Engineered Tissue Assessment 63
3.5.1 Engineered Tissue Sodium Concentration (ETSC) 63
3.5.2 Average Quadrupolar Coupling (ω ) 64
Q
3.5.3 Motional Averaging Parameter (ω τ) 64
0 c
3.6 Future Directions 64
3.7 Summary 64
References 65
Contents vii
4 SPIO‐Labeled Cellular MRI in Tissue Engineering: A Case Study
in Growing Valvular Tissues 71
Elnaz Pour Issa and Sharan Ramaswamy
4.1 Setting the Stage: A Clinical Problem Requiring a Tissue
Engineering Solution 71
4.2 SPIO Labeling of Cells 72
4.2.1 Ferumoxides 72
4.2.2 Transfection Agents 73
4.2.3 Labeling Protocols 75
4.3 Applications 76
4.3.1 Traditional Usage of SPIO‐Labeled Cellular MRI 76
4.3.2 SPIO‐Labeled Cellular MRI in Tissue Engineering 76
4.4 Case Study: SPIO‐Labeled Cellular MRI for Heart Valve Tissue
Engineering 77
4.4.1 Experimental Design 77
4.4.2 Potential Approaches—In Vitro 78
4.4.3 Potential Approaches—In Vivo 81
4.5 Conclusions and Future Outlook 83
Acknowledgment 84
References 84
5 Magnetic Resonance Elastography Applications in Tissue Engineering 91
Shadi F. Othman and Richard L. Magin
5.1 Introduction 91
5.2 Introduction to MRE 93
5.2.1 Theoretical Basis of MRE 94
5.2.2 The Inverse Problem and Direct Algebraic Inversion 96
5.2.3 Direct Algebraic Inversion Algorithm 101
5.3 Current Applications of MRE in Tissue Engineering and Regenerative
Medicine 108
5.3.1 In Vitro TE μMRE 108
5.3.2 In Vivo TE μMRE 110
5.4 Conclusion 114
References 114
6 Finite‐Element Method in MR Elastography: Application in 
Tissue Engineering 117
Yifei Liu and Thomas J. Royston
6.1 Introduction 117
6.2 FEA in MRE Inversion Algorithm Verification 118
6.3 FEM in Stiffness Estimation from MRE Data 120
6.4 FEA in Experimental Validation in Tissue Engineering
Application 121
viii Contents
6.5 Conclusions and Discussion 124
Acknowledgment 125
References 125
7 In Vivo EPR Oxygen Imaging: A Case for Tissue Engineering 129
Boris Epel, Mrignayani Kotecha, and Howard J. Halpern
7.1 Introduction 129
7.2 History of EPROI 131
7.3 Principles of EPR Imaging 132
7.4 EPR Oxymetry 134
7.5 EPROI Instrumentation and Methodology 135
7.5.1 EPR Frequency 135
7.5.2 Resonators 135
7.5.3 Magnets 136
7.5.4 EPR Imagers 137
7.6 Spin Probes for Pulse EPR Oxymetry 138
7.7 Image Registration 139
7.8 Tissue Engineering Applications 140
7.8.1 EPROI in Scaffold Design 140
7.8.2 EPROI in Tissue Engineering 142
7.9 Summary and Future Outlook 142
Acknowledgment 142
References 143
Part II Tissue‐Specific Applications of Magnetic Resonance
Imaging in Tissue Engineering 149
8 Tissue‐Engineered Grafts for Bone and Meniscus Regeneration and Their
Assessment Using MRI 151
Hanying Bai, Mo Chen, Yongxing Liu, Qimei Gong, Ling He, Juan Zhong,
Guodong Yang, Jinxuan Zheng, Xuguang Nie, Yixiong Zhang,
and Jeremy J. Mao
8.1 Overview of Tissue Engineering with MRI 151
8.2 Assessment of Bone Regeneration by Tissue Engineering
with MRI 152
8.3 MRI for 3D Modeling and 3D Print Manufacturing in Tissue
Engineering 157
8.4 Assessment of Menisci Repair and Regeneration by Tissue Engineering
with MRI 161
8.5 Conclusion 168
Acknowledgments 168
References 169
Contents ix
9 MRI Assessment of Engineered Cartilage Tissue Growth 179
Mrignayani Kotecha and Richard L. Magin
9.1 Introduction 179
9.2 Cartilage 181
9.3 Cartilage Tissue Engineering 182
9.3.1 Cells 183
9.3.1.1 Chondrocytes 183
9.3.1.2 Stem Cells 183
9.3.2 Biomaterials 183
9.3.3 Growth Factors 184
9.3.4 Growth Conditions 184
9.4 Animal Models in Cartilage Tissue Engineering 184
9.5 Tissue Growth Assessment 186
9.6 MRI in the Assessment of Tissue‐Engineered Cartilage 187
9.7 Periodic Assessment of Tissue‐Engineered Cartilage Using MRI 187
9.7.1 Assessment of Tissue Growth In Vitro 187
9.7.1.1 Accounting for Scaffold in Tissue Assessment 191
9.7.2 Assessment of Tissue Growth In Vivo 191
9.7.3 Assessment of Tissue Anisotropy and Dynamics 193
9.7.3.1 Assessment of Macromolecule Composition 194
9.7.3.2 Assessment of Tissue Anisotropy 198
9.8 Summary and Future Directions 199
References 200
10 Emerging Techniques for Tendon and Ligament MRI 209
Braden C. Fleming, Alison M. Biercevicz, Martha M. Murray,
Weiguo Li, and Vincent M. Wang
10.1 Tendon and Ligament Structure, Function, Injury, and Healing 209
10.2 MRI Studies of Tendon and Ligament Healing 211
10.3 MRI and Contrast Mechanisms 219
10.3.1 Conventional MRI Techniques 219
10.3.2 Advanced MR Techniques 222
10.4 Significance and Conclusion 228
Acknowledgments 228
References 228
11 MRI of Engineered Dental and Craniofacial Tissues 237
Anne George and Sriram Ravindran
11.1 Introduction 237
11.2 Scaffolds 238
11.3 Extracellular Matrix 238
11.4 Tissue Regeneration of Dental–Craniofacial Complex 239
11.4.1 Advantages of Using ECM Scaffolds with Stem Cells 240
x Contents
11.4.2 Stem Cells 242
11.5 MRI in Tissue Engineering and Regeneration 243
11.5.1 MRI of Human DPSCs 243
11.5.2 MRI of Tissue‐Engineered Osteogenic Scaffolds 244
11.5.3 MRI of Chondrogenic Scaffolds with Cells In Vitro 244
11.5.4 MRI of Chondrogenic Scaffolds with Cells In Vivo 245
11.5.5 MRI Can Differentiate Between Engineered Bone and Engineered
Cartilage 246
11.5.6 MRI to Assess Angiogenesis 246
11.6 Challenges and Future Directions for MRI in Tissue Engineering 246
Acknowledgments 247
References 247
12 Osteochondral Tissue Engineering: Noninvasive Assessment
of Tissue Regeneration 251
Tyler Stahl, Abeid Anslip, Ling Lei, Nilse Dos Santos, Emmanuel Nwachuku,
Thomas DeBerardino, and Syam Nukavarapu
12.1 Introduction 251
12.2 Osteochondral Tissue Engineering 252
12.2.1 Osteochondral Tissue 252
12.2.2 Biomaterials/Scaffolds 252
12.2.3 Cells 255
12.2.4 Growth Factors 256
12.3 Clinical Methods for Osteochondral Defect Repair
and Assessment 257
12.3.1 Diagnostic Modalities 257
12.3.2 Treatment Methods 260
12.3.2.1 Microfracture 260
12.3.2.2 Autografts and Allografts 260
12.3.2.3 Tissue Engineering Grafts 262
12.4 MRI Assessment of Tissue Engineered Osteochondral Grafts 262
12.4.1 In Vitro Assessment 263
12.4.2 In Vivo Assessment 264
12.5 MRI Assessment Correlation with Histology 264
12.6 Conclusions and Challenges 265
Acknowledgments 265
References 265
13 Advanced Liver Tissue Engineering Approaches and Their Measure
of Success Using NMR/MRI 273
Haakil Lee, Rex M. Jeffries, Andrey P. Tikunov, and Jeffrey M. Macdonald
13.1 Introduction 273
13.2 MRS and MRI Compatibilization—Building Compact RF MR Probes
for BALs 278
Contents xi
13.3 Multinuclear MRS of a Hybrid Hollow Fiber–Microcarrier BAL 280
13.3.1 Viability by 31P MRS 282
13.3.2 Quantifying Drug Metabolic Activity and Oxygen Distribution
by 19F MRS 284
13.4 1H MRI of a Hollow Fiber Multicoaxial BAL 286
13.4.1 BAL Integrity and Quality Assurance 286
13.4.2 Inoculation Efficiency and Prototype Redesign Iteration 288
13.4.3 Flow Dynamics 289
13.4.4 Diffusion‐Weighted and Functional Annotation Screening
Technology (FAST) Dynamic Contrast MRI 291
13.5 Magnetic Contrast Agents Used in MRI of Liver Stem Cell
Therapy 293
13.6 31P and 13C MRS of a Fluidized‐Bed BAL Containing Encapsulated
Hepatocytes 294
13.6.1 31P MRS Resolution, SNR, Viability, and pH 296
13.6.2 13C MRS to Monitor Real‐Time Metabolism 296
13.7 Future Studies 298
13.7.1 Dynamic Nuclear Polarization 298
13.7.2 Constructing Artificial Organs 300
13.8 Discussion 301
Acknowledgment 303
References 303
14 MRI of Vascularized Tissue‐Engineered Organs 311
Hai‐Ling Margaret Cheng
14.1 Introduction 311
14.2 Importance of Vascularization in Tissue Engineering 312
14.3 Vessel Formation and Maturation: Implications for Imaging 314
14.4 Imaging Approaches to Assess Vascularization 317
14.5 Dynamic Contrast‐Enhanced MRI for Imaging Vascular
Physiology 318
14.6 Complementary MRI Techniques to Study Vascularization 321
14.7 Considerations for Preclinical Models and Translation to Clinical
Implementation 325
14.8 Future Directions 326
14.9 Conclusions 327
References 327
15 MRI Tools for Assessment of Cardiovascular
Tissue Engineering 333
Laurence H. Jackson, Mark F. Lythgoe, and Daniel J. Stuckey
15.1 The Heart and Heart Failure 333
15.2 Cardiac Engineering and Cell Therapy 334
15.3 Imaging Heart Failure 336