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Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP001
Biophysics and Biochemistry of Cartilage by NMR and MRI

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New Developments in NMR
Editor-in-Chief:
Professor William S. Price, University of Western Sydney, Australia
Series Editors:
Professor Bruce Balcom, University of New Brunswick, Canada
Professor István Furó, Industrial NMR Centre at KTH, Sweden
Professor Masatsune Kainosho, Tokyo Metropolitan University, Japan
Professor Maili Liu, Chinese Academy of Sciences, Wuhan, China
Titles in the Series:

1: Contemporary Computer-Assisted Approaches to Molecular Structure
Elucidation
2: New Applications of NMR in Drug Discovery and Development
3: Advances in Biological Solid-State NMR
4: Hyperpolarized Xenon-129 Magnetic Resonance: Concepts, Production,
Techniques and Applications
5: Mobile NMR and MRI: Developments and Applications
6: Gas Phase NMR
7: Magnetic Resonance Technology: Hardware and System Component
Design
8: Biophysics and Biochemistry of Cartilage by NMR and MRI
How to obtain future titles on publication:

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Biophysics and Biochemistry of

Cartilage by NMR and MRI
Edited by
Yang Xia
Oakland University, Rochester, MI, USA
Email: xia@oakland.edu
Konstantin I. Momot
Queensland University of Technology (QUT), Brisbane, Australia
Email: k.momot@qut.edu.au
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP001 View Online
New Developments in NMR No. 8
Print ISBN: 978-1-78262-133-1

PDF eISBN: 978-1-78262-366-3
EPUB eISBN: 978-1-78262-905-4
ISSN: 2044-253X
A catalogue record for this book is available from the British Library
© The Royal Society of Chemistry 2017
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Preface
This is a unique book providing a contemporary snapshot of the roles that

nuclear magnetic resonance (NMR) and magnetic resonance imaging (MRI)
play in the current understanding of the biophysics and biochemistry of
articular cartilage. As a treatise on cartilage research, it is the first book of its
kind. All of its chapters were written by the leading experts who are active in
the field.
Cartilage research is closely intertwined with the development of NMR
and its imaging counterpart, MRI. Since the invention of NMR in 1946,1,2
magnetic resonance has evolved into a highly sophisticated experimental
technique with applications to a wide range of chemical and biological sys-
tems. The first study of cartilage by means of magnetic resonance was likely
published in 19553: it examined the NMR properties of water as well as a
series of biological systems, including calf cartilage. The authors found the
spin relaxation times of 1H nuclei to be significantly shorter in cartilage than
in pure water, surmising that the difference can be attributed to the com-
position of the tissue and the molecular state of water in it. They called for
further research, concluding that “...this will give valuable information of
a biologic and physical nature”. This was certainly a prescient conclusion,
as NMR and relaxometry have become invaluable research tools for bio-
medical applications, including those related to cartilage. The fascinating
background of this historical journey has been recapped recently in a jour-
nal article.4
The “Holy Grail” of cartilage magnetic resonance research is early and
non-invasive diagnosis of osteoarthritis, a musculoskeletal disease that is
the number one cause of disability in most developing and developed coun-
tries. Gradual degradation of articular cartilage is the hallmark of osteoar-
thritis. The degradation process is complex. The disease always results in the

Edited by Yang Xia and Konstantin I. Momot
Published by the Royal Society of Chemistry, www.rsc.org
v
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vi Preface
same end-stage symptom (loss of joint function), but the degradation of the
tissue can have different early-stage characteristics and be either idiopathic
or linked to different initiation events or risk factors, such as trauma, obesity
or biomechanical instability. Although the disease has been studied exten-
sively, an accurate diagnosis of osteoarthritis at a time when the joint is still

structurally sound, remains elusive in current clinical practice. Since early
lesions tend to be small and localized (both topographically and depth-wise),
any early detection tool must be non-invasive, sensitive to molecular-level
changes in the tissue and possess spatial resolution of the order of hundreds
of micrometers or better. Molecular imaging at high resolution meets these
requirements. An invaluable tool in molecular imaging is MRI, which is
unique in osteoarthritis management due to its high sensitivity to molecu-
lar activities and the molecular environment, and its non-invasive nature in
imaging.
This book aims to provide an exposition of the two-way interaction
between the fundamental science of cartilage (physics, chemistry and biol-
ogy) and cartilage imaging. It also aims to capture the current state-of-the-art
in imaging practice and to connect the fundamental science with the clinical
applications. In doing so, the authors of this book take you on an extraor-
dinary journey that shows how advances in the fundamental sciences have
been driving (and will drive in the future) the crucial developments in NMR
and MRI applications in cartilage research, and how contemporary MRI tech-
niques have been able to provide insights into the organisation and function
of cartilage.
Part one of the book introduces cartilage biology, biochemistry and bio-
physics, as well as NMR and MRI and the best-known effect in cartilage mag-
netic resonance—the magic angle effect. Part two covers the experimental
NMR and MRI techniques for cartilage research. This is followed by three
chapters concerned with the biomechanical aspects of cartilage investiga-
tion by NMR and MRI. The final part four deals with the applications and the
future of cartilage research.
Our first and foremost thank you goes to the “dream team” of our star
authors in cartilage research by NMR and MRI, who accepted our invitations
and contributed collectively to this book project. We feel exceptionally privi-
leged to have worked with this outstanding team.
We thank Prof. William S. Price, the editor-in-chief of the book series New
Developments in NMR at the Royal Society of Chemistry, who initiated this
project. We are also grateful to the editorial professionals at RSC, whose help
and patience have made this project a lot easier.
All chapters in this book have been peer-reviewed. In addition to many
contributing authors of this book who anonymously helped us to review
the individual chapters and provide suggestions for improvement, we are
very grateful to following expert colleagues who have critically reviewed sev-
eral chapters in this book: Prof. Hartwig Peemoeller (University of Water-
loo, Canada), Prof. William S. Price (Western Sydney University, Australia),
Prof. John R. Matyas (University of Calgary, Canada) and Prof. Philip W. Kuchel
View Online
Preface vii
(University of Sydney, Australia). Any errors remaining in the book are, of
course, the responsibility of the editors.
Yang Xia and Konstantin Momot
Rochester, MI, USA and Brisbane, Australia
References
1. E. M. Purcell, H. C. Torrey and R. V. Pound, Phys. Rev., 1946, 69, 37–38.
2. F. Bloch, W. W. Hansen and M. Packard, Phys. Rev., 1946, 69, 127.
3. E. Odeblad and G. Lindstrom, Acta Radiol., 1955, 43, 469–476.
4. Y. Xia and P. Stilbs, Cartilage, 2016, 7, 293–297.
Acknowledgements
I dedicate this book to my parents 镇澳 and 钺, for their unconditional love

and unwavering support during the turbulent years during which I and my
sister Xing 星 grew up in Shanghai, China, and to my wonderful children
Aimee 怡元 and Derek 怡康, who make this project worthwhile.
I owe a great debt to the late Sir Paul T. Callaghan (Massey University, New
Zealand) who taught me the art and science of NMR microscopy (µMRI); and
to Lynn W. Jelinski, George Lust, Nancy Burton-Wurster and Tony Farquhar
(Cornell University, Ithaca, NY, USA) who first introduced and supported me
during my initial detour into the world of cartilage research.
In my own cartilage journey at Oakland University since 1994, I am very
grateful for the beautiful works of my PhD students (Jonathan B. Moody,
Hisham A. Alhadlaq, Ji-Hyun Lee, Farid Badar, Daniel J. Mittelstaedt and
David J. Kahn); the mutual education of my former postdocs and techni-
cal personnel (Nagarajan Ramakrishnan, Aruna Bidthanapally, ShaoKuan
Zheng, JianHua Yin, Matthew Szarko and Nian Wang); and the stimulat-
ing exchange of many visiting and sabbatical scientists to my lab (Paul T.
Callaghan, Hisham A. Alhadlaq, Ekrem Cicek, RanHong Xie, ZhiGuo
Zhuang and Zhe Chen). I have also benefited in my cartilage research from
collaboration and interaction with many professional colleagues (John R.
Matyas, Christopher T. Chen, JianRong Xu, Jia Hua, Yong Lu, Siegfried Stapf,
XiangGui Qu, Quan Jiang, Clifford M. Les, Mei Lu, Hani N. Sabbah, Yener N.
Yeni, Ken Elder, Fay Hansen, Jia Li, Edith Chopin, Loan Dang, Andrew Gold-
berg, Shravan Chintala, Anil N. Shetty, Joseph Guettler, Tristan Maerz, Jiani
Hu, Weiping Ren, MaoSheng Xu, TuQiang Xie, Janelle Spann, Dieter Gross,
Rao Bidthanapally, Fred R. Nelson, Douglas Creighton and Bradley Roth). I
would not be able to travel very far on this journey without you—any of you.
I am grateful for the four 5-year R01 grants from the National Institutes
of Health (NIH NIAMS) to my lab, much internal support from the Research

ix
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x Acknowledgements
Excellence Fund in Biotechnology and the Center for Biomedical Research
at Oakland University, the Department of Physics at Oakland University, and
an NMR instrument endorsement from R.B. and J.N. Bennett (Oakland Uni-
versity), which have enabled the initiation and continuation of my cartilage
adventure at Oakland University.

Yang Xia (夏阳)
Oakland University, Rochester, MI, USA
View Online
Acknowledgements xi
To paraphrase (rather loosely) Miguel de Cervantes, “Tell me who your teach-
ers are and I will tell who you are”. As scientists, we are to a large extent
the products of our scientific mentors. I would like to acknowledge mine:
F. Ann Walker and Michael Barfield, who introduced me to magnetic reso-
nance during my PhD; Charles S. Johnson Jr, who taught me a lot of what I
know about diffusion and diffusion measurements; and Philip W. Kuchel,
who introduced me to the fascinating world of NMR of biological tissues.
I would like to acknowledge my colleagues and collaborators at Queensland
University of Technology (QUT), who have collectively built the vibrant
and stimulating environment for tissue and biomaterials research. James
M. Pope founded the QUT MRI laboratory and was instrumental in both
bringing me to QUT and introducing me to MRI of articular cartilage.
Mark J. Pearcy has provided tireless leadership of biomedical engineer-
ing research here. R. Mark Wellard contributed his expertise in NMR elec-
tronics and the network of industry contacts to keep the QUT MRI lab on
track. Kunle Oloyede (now the Vice-Chancellor of Elizade University, Nigeria)
has brought cartilage biomechanics research to QUT. Michael A. Schuetz
(now the Chair of Trauma Surgery at Charité Hospital, Berlin) and Ross W.
Crawford were the first clinicians at QUT to build a bridge between ortho-
paedic surgical practice and imaging research. Dietmar Hutmacher, Daniela
Loessner, Mia Woodruff, Yin Xiao, Rik Thompson, Clayton Adam and Paige
Little have all contributed to creating the nexus between the physics of MRI,
biomaterials and biomedical research. Each of these collaborators has taught
me something new and greatly contributed to my magnetic resonance- and
cartilage-related research.
Last but not least, I would like to acknowledge members of my research
group, past and present: Sean K. Powell, Monique C. Tourell, Sirisha Tadimalla,
Tonima Ali, Jean-Philippe Ravasio, Monika Madhavi Wisman Acharige,
Samuel Guesné, Chris Bell, Aaron Tranter, Nerina Foley, Ying Chi Mui,
Hassan Hawsawi, Wilson Egadwa, Sabrina Barheine, Alf Pawlik, Pierre
Baugnon and Amaury Bruneau. Many of you have contributed directly to the
cartilage research in my group; others were involved in different research
projects; but all of you have sustained and enriched the intellectual and
research atmosphere within the group through your enthusiasm, hard work
and scientific curiosity. I thank every one of you for this.
Konstantin Momot
QUT, Brisbane, Australia
Contents
Part One – Introduction
Chapter 1 Introduction to Cartilage 3

Yang Xia, Konstantin I. Momot, Zhe Chen, Christopher T. Chen,
David Kahn and Farid Badar
1.1 I ntroduction 3
1.2 Cartilage and the Joint 4
1.2.1 Different Types of Cartilage 4
1.2.2 Synovial Joints and Articular Cartilage 5
1.3 Cellular Aspects of Articular Cartilage 7
1.3.1 Cartilage Progenitor Cells 8
1.3.2 Mature Chondrocytes in Cartilage 8
1.3.3 Mesenchymal Stem Cells 10
1.4 Extracellular Matrix of Articular Cartilage 10
1.4.1 Collagen 11
1.4.2 Proteoglycans and Glycosaminoglycans 12
1.4.3 Water 13
1.4.4 Other Components 15
1.5 Histological Structure of Articular Cartilage 16
1.5.1 The Zonal Structure of Articular Cartilage 16
1.5.2 Depth-Dependent Physicochemical Properties 17
1.6 Biomechanical Properties of Articular Cartilage 18
1.6.1 The Uncompressed Equilibrium State 18
1.6.2 Compression of Articular Cartilage 20
1.7 Joint and Gross Morphology of Articular Cartilage 25
1.7.1 Development of Synovial Joint 25
1.7.2 Topographic Distributions in the Knee 26

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xiv Contents
1.7.3 Topographic Distributions in the Shoulder 27
1.7.4 The Split-Line Pattern 28
1.8 The Diseases of Cartilage and Joints 29
1.8.1 Classification and Etiology of Osteoarthritis 29
1.8.2 Pathogenesis 29
1.8.3 The Role of Subchondral Bone 30
1.8.4 Biomarkers 30
1.8.5 Treatment 31
1.9 Osteoarthritis Research 31
1.9.1 In vivo Models of Osteoarthritis 32
1.9.2 In vitro Models of Cartilage Degeneration 33
Acknowledgements 34
References 35
Chapter 2 Osmotic Properties of Cartilage 44

Ferenc Horkay and Peter J. Basser
2.1 I ntroduction 44
2.2 Cartilage Molecular Architecture, Gross Appearance,
and Morphology 46
2.3 Osmotic Swelling Pressure of Cartilage 48
2.4 Molecular Interactions of Cartilage Polymers 51
2.4.1 Osmotic Observations 51
2.4.2 Small-Angle Scattering Measurements 53
2.4.3 Dynamic Properties of Proteoglycan Assemblies 55
2.5 Conclusions 58
Acknowledgements 59
References 59
Chapter 3 Introduction to NMR and MRI 62

Konstantin I. Momot
3.2 Semiclassical Description of NMR 63
3.2.1 NMR-Active Nuclei 63
3.2.2 Vector Description of NMR 66
3.2.3 Excitation 68
3.2.4 Precession and the Bloch Equation 69
3.2.5 Rotating Frame 70
3.2.6 Chemical Shielding and Chemical Shift 71
3.2.7 Spin Relaxation 73
3.2.8 NMR Signal Detection 77
3.2.9 Spin Echo and NMR Pulse Sequences 78
3.3 Quantum Description of NMR 80
3.3.1 Spin and Angular Momentum 81
3.3.2 Conceptual Points 82
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Contents xv
3.3.3 atrix Representation of Spin Operators
M 82
3.3.4 Zeeman Hamiltonian 83
3.3.5 Nuclear Magnetisation 83
3.3.6 Evolution of the Spin Density Matrix 85
3.3.7 NMR Observables and Coherence Order 88

3.3.8 Spin Relaxation 89
3.3.9 Anisotropic Spin Hamiltonians
and NMR Spectra 91
3.4 M
RI 92
3.4.1 Fourier MRI 92
3.4.2 Implementation of Fourier Imaging 95
3.4.3 Image Contrast 98
3.4.4 Spatial Resolution and the SNR 99
3.4.5 Parameter Mapping Versus Weighted Imaging 99
3.5 Conclusion 100
Abbreviations and Symbols 101
Acknowledgements 101
References 102
Chapter 4 The Magic Angle Effect in NMR and MRI of Cartilage 109
Gary D. Fullerton

4.2 Basic Physics and Physical Chemistry 112
4.2.1 Electronegativity and Partial Charges 112
4.2.2 Role of Hydrogen Bonds 112
4.2.3 Protein: Polar Solutes 113
4.2.4 Bound Water 114
4.3 Basic Concepts of NMR Relaxation 115
4.3.1 NMR Spin-Lattice Relaxation and Molecular
Motion 115
4.3.2 Proton Fast Exchange 117
4.3.3 NMR Titration Study of Protein Solutions 117
4.3.4 NMR Titration of Native Bovine Tendon 118
4.3.5 Bound Water Equivalence to Water Bridges 119
4.3.6 Double Water Bridges 121
4.4 Formation of a Molecular Model 122
4.4.1 Stoichiometric Hydration Model 122
4.4.2 SHM Applied to Collagen 125
4.4.3 SHM Water Bridge Binding Energy Predictions 127
4.4.4 Anisotropic Rotation of Water Bridges 129
4.4.5 Water Bridge Source for Magic Angle Effects 131
4.4.6 SHM Explanation of Biphasic and
Monophasic T2 133
4.5 Cartilage and the Magic Angle Effect 134
4.5.1 Collagen in Cartilage 134
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xvi Contents
4.5.2 M agic Angle Effect in Cartilage 135
4.5.3 Multi-Exponential Versus
Mono-Exponential T2 Relaxation 136
4.6 Revisiting the 1985 Tendon Relaxation Report 139
4.7 The T2 Versus T2* Conundrum 139

4.8 Conclusions and Discussion 141
References 142
Part Two – Cartilage Research by Experimental NMR

and MRI Techniques
Chapter 5 Physical Properties of Cartilage by Relaxation

Anisotropy 147
Miika T. Nieminen, Mikko J. Nissi, Matti Hanni
and Yang Xia

5.1.1 Relaxation Anisotropy 148
5.1.2 Physical Properties of Cartilage 148
5.1.3 Relaxation Anisotropy in Cartilage 149
5.1.4 Relaxation Anisotropy in Other Tissues 150
5.1.5 Theoretical and Simulation Work on
Articular Cartilage 151
5.2 Anisotropy of T2 Relaxation Time in Cartilage 151
5.2.1 Dependence of T2 Relaxation on Collagen
Orientation 151
5.2.2 Dependence of T2 Relaxation on Collagen
Content and Tissue Hydration 153
5.2.3 Spatial and Topographical Variation of T2
Relaxation Time 153
5.2.4 T2 Relaxation in Detection of Anisotropy-
Related Cartilage Maturation 154
5.2.5 T2 Relaxation in Detection of Cartilage
Repair 156
5.3 Anisotropy of T1ρ Relaxation in Cartilage 156
5.4 Different Relaxation Mechanisms in T1ρ 161
5.5 Anisotropy of T1 Relaxation in Cartilage 163
5.5.1 Pre-contrast T1 Relaxation Time 163
5.5.2 Delayed Gadolinium-Enhanced MRI of
Cartilage (dGEMRIC) 164
5.6 Sensitivities in Practical Relaxation Measurement 167
5.7 Conclusions 168
Acknowledgement 169
References 169
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Contents xvii
Chapter 6 Chemical Properties of Cartilage Studied Using
Charged Ions 176
Olle Söderman, Jenny Algotsson, Leif E. Dahlberg and Jonas
Svensson

6.2 The dGEMRIC Method 178
6.2.1 The Basis of the dGEMRIC Method 178
6.2.2 Clinical Applications of dGEMRIC 186
6.3 Concluding Remarks and Future Prospects 188
References 189
Chapter 7 Quantification of Articular Cartilage Microstructure

by the Analysis of the Diffusion Tensor 191
Monique C. Tourell, Sean K. Powell and
Konstantin I. Momot

7.2 Diffusion Magnetic Resonance 192
7.2.1 Diffusion NMR Spectroscopy 193
7.2.2 General Treatment and the Diffusion
Propagator 195
7.2.3 Diffusion Imaging 196
7.3 Diffusion Magnetic Resonance of Articular
Cartilage 199
7.4 Diffusion Simulations in Articular Cartilage 200
7.4.1 Constructing Idealised Fibre Networks 200
7.4.2 Diffusion of Water in Model Networks 204
7.4.3 Reconstructing the Diffusion Tensor 208
7.4.4 Simulation Parameters and Considerations 210
7.4.5 Diffusion Trends Through Model Networks 212
7.5 Combining Experiments and Simulations 215
7.6 Post-DTI Approaches to Cartilage Diffusion
Imaging 216
7.7 Conclusions 218
References 219
Chapter 8 Sodium and Other Exotic Methods in NMR and MRI of

Cartilage 225
Ravinder Reddy and Arijitt Borthakur
8.1 C
linical Need 225
8.1.1 Current Methods of Detecting Cartilage
Degeneration with Imaging 226
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xviii Contents
8.2 Sodium NMR 227
8.2.1 Sodium MRI of Cartilage 227
8.2.2 Advantage of Sodium MRI 227
8.2.3 Limitations of Sodium MRI 229
8.3 T1ρ MRI 229

8.3.1 Mechanism of T1ρ Relaxation in Tissues 231
8.3.2 T1ρ MRI Methods 231
8.3.3 T1ρ MRI Pulse Sequences 232
8.3.4 T1ρ MRI as a Biomarker of Cartilage 235
8.4 Chemical Exchange Saturation Transfer 238
8.4.1 CEST MRI of Cartilage 238
8.5 Summary 240
References 242
Chapter 9 Multi-Quantum Filtered NMR and MRI of Cartilage 246

Hadassah Shinar and Gil Navon

9.2 Theoretical Background 248
2
9.3 H and 23Na DQF NMR of Nasal Cartilage 253
9.4 Mapping the Orientation of the Collagen Fibers in
9.5 The Effect of the Detachment from the Bone 258
9.6 Comparison of the Effects of Mechanical Load and
Osmotic Pressure on Articular Cartilage 260
9.7 The Effect of Decalcification 263
9.8 Maturation of Pig Articular Cartilage 266
9.9 23 Na Spectroscopy and Imaging of Intact and
Proteoglycan-Depleted Articular Cartilage 270
9.10 23
Na and 2H Studies of Osteoarthritic and
Osteoporotic Articular Cartilage 270
9.11 Sodium Triple Quantum Imaging 272
9.12 1H DQF Imaging of Connective Tissues 273
9.13 Conclusions 275
References 275
Chapter 10 Solid-State NMR Techniques to Study the Molecular

Dynamics in Cartilage 279
Daniel Huster

10.2 Methodological Concepts of Studying Cartilage
by Solid-State NMR Spectroscopy 281
10.2.1 Static Solid-State NMR Techniques 281
10.2.2 Magic-Angle Spinning Solid-State NMR
Techniques 284
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Contents xix
10.3 M
olecular Dynamics of GAGs and Collagen in
Cartilage Tissue 285
10.3.1 GAG Dynamics in Native Cartilage Tissue 285
10.3.2 Collagen Dynamics in Native Cartilage
Tissue 287
10.4 Hydration of Cartilage 290
10.5 Solid-State NMR as a Tool to Study the Quality of
Tissue-Engineered Cartilage 292
References 296
Chapter 11 Ultrashort Echo Time Imaging of Articular Cartilage 299

Soorena Azam Zanganeh, Hongda Shao, Graeme M. Bydder
and Jiang Du

11.2 Morphological UTE Imaging of Articular Cartilage 301
11.2.1 Multi-Echo UTE Imaging of Articular
Cartilage 301
11.2.2 DIR-UTE Imaging of Articular Cartilage 302
11.2.3 AWSOS Imaging of Articular Cartilage 304
11.2.4 SWIFT Imaging of Articular Cartilage 305
11.3 Quantitative UTE Imaging of Articular Cartilage 308
11.3.1 T1 Quantification of Calcified Cartilage 308
11.3.2 T2* Quantification of Calcified Cartilage 309
11.3.3 T1ρ Quantification of Calcified Cartilage 310
11.3.4 UTE T2* Bi-Component Analysis of Articular
Cartilage 311
11.3.5 AWSOS T2* Multi-Component Analysis of
References 317
Chapter 12 Low-Field and Field-Cycling NMR and MRI of Cartilage 320

Siegfried Stapf, Carlos Mattea and Erik Rössler
12.1 I ntroduction: Low Field vs. Variable Field 320

12.2 Theoretical Background 321
12.3 Hardware Considerations 326
12.3.1 Low-Field Studies: The Single-Sided
Scanner 326
12.3.2 Variable Magnetic Field Strengths by Field
Variation 329
12.3.3 Field-Cycling MRI 330
12.4 Low-Field Investigations of Cartilage 331
12.4.1 Relaxation Profiles 331
12.4.2 Diffusion Profiles 333
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xx Contents
12.4.3 I nfluence of Sample Curvature and
Resolution Limit 334
12.4.4 Contrast Agents and Enzymes 334
12.4.5 Cartilage Under Loading 336
12.5 Variable-Field Studies of Cartilage 337

12.5.1 Relaxometry Studies 337
12.5.2 Field-Cycling Imaging 341
12.6 Summary and Outlook 343
References 344
Chapter 13 The Influence of Specimen and Experimental

Conditions on NMR and MRI of Cartilage 347
ShaoKuan Zheng and Yang Xia

13.2 Pre-Experiment Specimen Preparation and
Storage 348
13.2.1 Specimen Harvesting 348
13.2.2 Specimen Storage 350
13.2.3 Alternative Specimens for Articular
Cartilage 352
13.3 Specimen Solutions During NMR and MRI
Experiments 356
13.3.1 NMR/MRI of Cartilage in H2O, Simple
Salt and Phosphate-Buffered Solutions 356
13.3.2 NMR/MRI of Cartilage in Phosphate Salt
Solutions 357
13.3.3 NMR/MRI of Cartilage in Commercial
Buffers at Different pH Values 359
13.3.4 NMR/MRI of Cartilage in Fixation Solutions 361
13.4 Experimental Issues in NMR and MRI
Measurement of Cartilage 361
13.4.1 Basic Optimization in Experimental Setup
and Data Analysis 362
13.4.2 Effect of the Repetition Time on Cartilage
Laminae in MRI 362
13.4.3 Effect of the Echo Time in Cartilage MRI 363
13.4.4 Strength of the Spin-Lock Field in
Cartilage T1ρ Experiments 364
13.4.5 Pulse Sequences in Quantitative MRI 364
13.4.6 Considerations in Multi-Component
Relaxation Measurements 366
13.5 Final Remarks 367
References 367
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Contents xxi
Part Three – Biomechanical Properties of Cartilage

by NMR and MRI
Chapter 14 Diffusion MRI and Poroelastic Biomechanics of


Daniel Topgaard

14.2 Cartilage as a Poroelastic Material 377
14.3 Mechanisms of Cartilage Lubrication 379
14.4 Microscopic Structure of the Collagen Network 380
14.5 MRI Methods for Mapping Fluid Translational
Motion 383
14.6 MRI Studies of Cartilage Poroelastic Biomechanics 386
14.7 Conclusions and Outlook 390
References 390
Chapter 15 Combining Multi-Modal MRI and Biomechanical

Modeling to Investigate the Response of Cartilage and
Chondrocytes to Mechanical Stimuli 395
Luyao Cai, Corey P. Neu and David M. Pierce

15.2 Cartilage Architecture and MRI 397
15.2.1 Cartilage Composition and MRI
Morphology 397
15.2.2 Cartilage Composition and Diffusion 398
15.2.3 Cartilage Composition and MRI Relaxivity 399
15.3 Chondrocytes and Mechanical Stimuli 401
15.3.1 Force Transfer from Global to Cellular Scales 401
15.3.2 Response of Chondrocytes to Global Stimuli 402
15.3.3 MRI and Single Chondrocytes 402
15.4 MRI Measures of Mechanical Behavior 403
15.4.1 Correlation Between Quantitative MRI and
Mechanical Properties 403
15.4.2 Measurement of Zonal Mechanics by MRI 403
15.4.3 Measurement of Zonal Mechanics by
Magnetic Resonance Elastography 406
15.4.4 Multi-Modal MRI 407
15.5 Image-Based Modeling 409
15.5.1 2D Constitutive Models 410
15.5.2 3D Constitutive Models 411
15.6 Applications of Image-Based Modeling 416
15.6.1 Modeling Applications in 2D 416
15.6.2 Modeling Applications in 3D 418
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xxii Contents
15.7 Outlook 421
References 423
Chapter 16 Loading-Induced Changes in Cartilage Studied by

NMR and MRI 433
Nian Wang and Yang Xia

16.2 Loading of Articular Cartilage 434
16.2.1 Mechanical Properties of Articular Cartilage 434
16.2.2 MRI Study of Cartilage Loading 436
16.3 Effect of Tissue Loading on T1 Relaxation and
GAG Quantification 437
16.3.1 Strain- and Depth-Dependent Deformation
of Articular Cartilage 437
16.3.2 Critical Point Phenomenon in Compressed
16.3.3 Quantification of Gd and GAG
Concentrations in Compressed Cartilage 442
16.4 Effect of Tissue Loading on T2 and T1ρ Relaxation
Times 443
16.4.1 Articular Cartilage Deformation by Proton
Images 443
16.4.2 Articular Cartilage Deformation by
T2 and T1ρ Relaxation Times 444
16.4.3 A Model of Collagen Deformation in
Healthy and Lesioned Cartilage 445
16.5 Functional Study of Human Cartilage Using
Clinical MRI 446
References 449
Part Four – Applications and the Future of Cartilage

Research by NMR and MRI
Chapter 17 The Critical Role of High Imaging Resolution in

MRI of Cartilage—The MRI Microscope 457
Yang Xia

17.2 High Resolution in MRI 458
17.3 Complex Interplay of Imaging Resolution in
MRI of Cartilage 459
17.3.1 Depth-Dependent Zonal Structure of
View Online
Contents xxiii
17.3.2 T
opographical Distribution of Cartilage
Properties 460
17.3.3 Long Degradation Process with Diverse
Early Characteristics 462
17.3.4 Orientation of the Specimen in the Magnet 463

17.3.5 Orientation of a Pencil-Shaped Imaging
Voxel in MRI 463
17.3.6 Boundary Tissue Averaging in MRI 464
17.4 Resolution Scaling Law in MRI of Cartilage 465
17.5 A Sweet Spot— µMRI of Animal Models of
Osteoarthritis 467
Acknowledgement 468
References 468
Chapter 18 Multicomponent Relaxation in NMR and MRI of Cartilage 471

David A. Reiter, Richard G. Spencer and Yang Xia

18.2 Methodological Considerations in Relaxometry 473
18.2.1 Tissue Heterogeneity and Dipolar Interaction 473
18.2.2 Ex vivo Sample Handling 475
18.2.3 NMR and MRI Acquisition Parameters 476
18.2.4 Multicomponent Analysis 477
18.2.5 Additional Considerations in Clinical MRI 479
18.3 Multicomponent NMR Relaxation Studies 479
18.3.1 Model Systems 479
18.3.2 Tissue-Engineered Cartilage 481
18.3.3 Bovine Nasal Cartilage 483
18.3.4 Articular Cartilage 485
18.4 Multicomponent MRI Relaxation Studies 487
18.4.1 Spin Echo Imaging 487
18.4.2 Gradient Echo Imaging 488
Acknowledgement 491
References 491
Chapter 19 Uni- and Multi-Parametric Magnetic Resonance

Analysis of Cartilage 494
Beth G. Ashinsky and Richard G. Spencer
19.1 I ntroduction to Cartilage MRI Classification 494

19.2 Classification 497
19.2.1 Sensitivity and Specificity 497
19.3 Empirical Studies of Univariate Classification of
Cartilage 497
19.3.1 Assignment Based on Euclidean Distance 498
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xxiv Contents
19.3.2 Assignment Based on Mahalanobis Distance 499
19.3.3 Limitations to Univariate Classification 508
19.4 Empirical Studies of Multivariate Classification of
Cartilage 508
19.4.1 Multivariate Classification of Cartilage

Using Cluster Analysis 508
19.4.2 Multivariate Classification of Cartilage
Using Support Vector Machine Analysis 514
19.4.3 Multiexponential and Multivariate
Analysis 516
19.4.4 Application of Machine Learning to
Sodium MRI Data 522
19.4.5 Pattern Recognition and Machine Learning
Classification 524
19.5 Conclusion 525
References 526
Chapter 20 Magnetic Resonance in the Assessment of Tissue

Engineered Cartilage 529
Mrignayani Kotecha, Ziying Yin and Richard L. Magin

20.2 Cartilage 530
20.3 Cartilage Tissue Engineering 531
20.3.1 Cells 531
20.3.2 Scaffolds 532
20.3.3 Growth Factors and Growth Strategies 532
20.3.4 Tissue Growth Assessment 533
20.4 MRS and MRI in Cartilage Tissue Engineering 533
20.5 Magnetic Resonance Accessible Components
of Tissue Engineered and Regenerating Cartilage 535
20.5.1 Assessment of Tissue Growth 535
20.5.2 Assessment of Tissue Anisotropy and
Dynamics 539
20.5.3 Assessment of GAG Amount 545
20.6 Future Directions 547
20.6.1 New Biomaterials 547
20.6.2 Magnetic Resonance Standards 547
20.6.3 ECM-Specific Techniques 547
20.7 Summary 548
References 548
Chapter 21 Complementary Imaging in MRI of Cartilage 552

Yang Xia and Jukka S. Jurvelin

21.2 Polarized Light Microscopy 553
21.3 Fourier-Transform Infrared Imaging (FTIRI) 558
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Contents xxv
21.4 E lectron Microscopy 561
21.5 Microscopic Computed Tomography 563
21.6 Additional Imaging Techniques in Cartilage
Research 564

Acknowledgement 569
References 569
Chapter 22 Quantitative MRI for Detection of Cartilage Damage 575

José G. Raya and Uran Ferizi

22.2 MRI Biomarkers 577
22.2.1 Quantitative Morphology 577
22.2.2 Sodium (Na) Imaging 577
22.2.3 Delayed Gadolinium Enhanced MRI
of Cartilage (dGEMRIC) 578
22.2.4 T2 Relaxation Time 578
22.2.5 Spin-Lattice Relaxation Time in the
Rotating Frame (T1ρ) 578
22.2.6 Magnetization Transfer 579
22.2.7 Diffusion-Weighted MRI 579
22.3 Validation of MRI Biomarkers 580
22.3.1 Techniques Used in the Validation of
MRI Biomarkers 581
22.3.2 Clinical MRI 586
22.3.3 Quantitative Morphology 590
22.3.4 Biomarkers for Cartilage Composition 598
22.3.5 Summary 607
22.4 Validation of Diffusion-Weighted Imaging of
22.4.1 Value of DTI for the Detection of Change
of Cartilage After Mechanical Injury 608
22.4.2 Validation of a Clinical Protocol for DTI
of Articular Cartilage with Histology 611
Acknowledgement 617
References 617
Chapter 23 Challenges for the Early Detection of Degenerative

Cartilage Changes Using Magnetic Resonance
Imaging In vivo in Humans 628
Matthew C. Gallo, Hsiang-Ling Teng and
Sharmila Majumdar

23.2 Morphologic MRI Techniques 629
23.2.1 Field Strength and Coil 629
23.2.2 Pulse Sequences 630
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xxvi Contents
23.3 Q
uantitative Morphological Measurements of
Cartilage 634
23.3.1 Magnetic Resonance Considerations 634
23.3.2 Segmentation and Quantification 635
23.3.3 Semi-Quantitative vs. Quantitative

Measurements 635
23.3.4 Assessment in Osteoarthritis 637
23.3.5 Assessment After Injury 639
23.3.6 Assessment After Loading 639
23.3.7 Measurement Variability 640
23.4 Quantitative MRI Techniques for Assessment
of Cartilage Composition 640
23.4.1 T2 Relaxation Time Mapping 641
23.4.2 Delayed Gadolinium-Enhanced MRI of
Cartilage 645
23.4.3 T1ρ Relaxation Time Mapping 649
23.4.4 Sodium (23Na) Imaging 652
23.4.5 Diffusion-Weighted Imaging and
Diffusion Tensor Imaging 655
23.4.6 Magnetization Transfer and Chemical
Exchange-Dependent Saturation Transfer 656
23.5 Conclusion 656
References 657
Chapter 24 Ultrahigh-Field Whole-Body MRI for Cartilage Imaging:

Technical Challenges 671
Casey P. Johnson, Pierre-Francois Van de Moortele,
Luning Wang, Kâmil Uğurbil and Jutta M. Ellermann

24.2 Technical Solutions 674
24.2.1 Overview 674
24.2.2 Radiofrequency Coil Technology 675
24.2.3 B1+ Shimming and Parallel Transmission 681
24.2.4 B1+-Insensitive Radiofrequency Pulse Design 686
24.2.5 SAR Monitoring and Modeling of
Radiofrequency Heating 686
24.2.6 Field Monitoring and B0 Shimming 687
24.2.7 Image Acceleration Strategies 688
24.2.8 Summary 690
24.3 Emerging Applications 691
24.3.1 High-Resolution Anatomical Imaging
of Cartilage 691
24.3.2 Quantitative Mapping of Cartilage Damage
and Repair 691
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Contents xxvii
24.3.3 S
usceptibility-Weighted Imaging of
Cartilage Vascular Canals 693
24.3.4 UTE Imaging of the Osteochondral Junction 694
24.3.5 Quantitative Sodium Imaging of
Proteoglycan Content 695

24.4 Outlook 695
References 697
Subject Index 706

Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-00001
Part One
Introduction
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-00001 View Online
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-00001 View Online
Chapter 1
Introduction to Cartilage
Yang Xia*a, Konstantin I. Momotb, Zhe Chena,c,
Christopher T. Chend, David Kahna and Farid Badara
a
Department of Physics and Center for Biomedical Research, Oakland
University, Rochester, MI 48309, USA; bSchool of Chemistry, Physics and
Mechanical Engineering, Queensland University of Technology (QUT),
Brisbane, Qld 4001, Australia; cDepartment of Radiology, Ruijin Hospital,
Shanghai JiaoTong University School of Medicine, Shanghai 200025, China;
d
Center for Mineral Metabolism and Clinical Research / Department of
Orthopedic Surgery, University of Texas Southwestern Medical Center,
Dallas, TX 75390, USA
*E-mail: xia@oakland.edu
1.1 Introduction
Cartilage is a skeletal tissue that, together with the bone, forms the frame-
work supporting the body as a whole.1 It is a tissue of great biological
importance, which is apparent from the fact that vertebrate life would be
impossible without cartilage: different types of cartilage play major roles in
the function of such crucial systems as the spine and the respiratory system.
Among different types of cartilage, articular cartilage is the best known and
perhaps the most studied type. Articular cartilage is the thin layer of connec-
tive tissue that covers the articulating ends of bones in synovial joints (e.g.,
knee, hip, shoulder, and many other movable joints in the body). The intense
interest in articular cartilage is motivated by the critical role its degradation

3
View Online
4 Chapter 1
plays in arthritis and related joint diseases, which are the number one cause
of disability in humans.2
This chapter provides an essential (albeit incomplete) introduction to
the multi-level and multi-scale properties of articular cartilage that give
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-00001
this tissue its extraordinary load-bearing characteristics. Section 1.2

describes the general relationship between cartilage and the joint, while
the following sections focus on different aspects of articular cartilage that
are important to understanding its biological properties and its magnetic
resonance behaviour. Sections 1.3–1.6 introduce cartilage at cellular, extra-
cellular, histological and biomechanical levels. Sections 1.7–1.9 discuss
the spatial heterogeneity of cartilage properties over the whole joint, dis-
eases of cartilage and joint, and research into arthritis and related joint
diseases.
1.2 Cartilage and the Joint

Cartilage is a specialised connective tissue present in animals, including
humans, distinct from connective tissue proper.3 Cartilage tissue is stiff but
also flexible. As a result, it is an integral part of many parts of the body where
the supporting structures must accommodate limited movement.
1.2.1 Different Types of Cartilage

Different varieties of cartilage occur at specific anatomical locations. Three
types of cartilage are commonly distinguished morphologically.
(1) Hyaline cartilage is named from the Latin word “hyalinus”, meaning
“smooth”, “clear” or “glass-like”. It has a homogeneous appearance
and a semi-solid consistency. Hyaline cartilage is the most abundant
type of cartilage in the body and includes articular cartilage, which
lines the articulating surfaces of bones within many movable joints.
Other varieties of hyaline cartilage include costal cartilage connecting
the anterior ends of the ribs to the sternum, nasal cartilage, and many
laryngeal and tracheobronchial cartilages. In the foetus, hyaline car-
tilage forms most of the embryonic skeleton (“temporary cartilage”)
before it is replaced by bone during ossification. Hyaline cartilage also
forms epiphyseal growth plates, which enable rapid growth of long
bones during childhood (see Section 1.3.1).1,4
(2) Fibrocartilage is fasciculated and fibrous. It exhibits significant tensile
strength and occurs in many areas subject to high mechanical stress.
Fibrocartilage forms the annuli of intervertebral discs in the spine (anu-
lus fibrosus), the menisci of the knee and certain other joints, and the
plates connecting the opposing surfaces of bones within many immov-
able joints (e.g. the pubic symphysis). It is also present in some movable
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a prayer but chiefly ecstatic description of his power, the worshipper
is really endeavouring to charge himself with higher religious magic
by this outpouring. In fact, here and elsewhere, a magic origin for the
practice of theologic exegesis may be obscurely traced; narrative
might acquire an apotropaeic effect; thus tablets containing the
narrative of the achievements of the plague-god, hung up before the
houses, could avert pestilence,296.2 or, again, the reading aloud the
tablet narrating the victory of Shamash and Ramman over the seven
demons who attacked the moon-god Sin served to defeat the seven
demons by the same sympathetic magic as would be worked by a
dramatic representation of that event.296.3
There is no record or hint that the Hellenes recited hymns to
Demeter or wrote up passages of Homer to avert demons.
It belongs to the magic use of formulae that minute exactness in
respect of every syllable is necessary to the power of the spell or the
spell-prayer. An Assyrian king who is consulting the sun-god
concerning success in a war with which he is threatened, prays that
the ritual which the enemy may be employing may go wrong and fail;
and in this context occurs the curious petition, “May the lips of the
priest’s son hurry and stumble over a word.”297.1 The idea seems to
be that a single slip in the ritual-formulae destroyed their whole
value; and such a view belongs to magic rather than to religion.
Now it is probable that in his earliest mental stage the Hellene had
been in bondage to the religious magic of sacred formulae and
sacred names; and as a tradition of that stage, the divine epithet
whereby he appealed to his deities according to his needs retained
always for him a mysterious potency; but otherwise we have no
proof that he worked word-magic by means of his sacred texts.
Babylonian sorcery, whether legitimate or illegitimate, was
intended to work upon or through demons; and its familiarity with the
names and special qualities of demons is its peculiar mark. In the
ritual of exorcism of the demons, idols play a prominent and often
singular rôle. The following performance is probably unique: in the
exorcism of disease two idols, male and female, were set up before
the sick man, then the evil spirits of sickness are invited thus: “Oh ye
all wicked, all evil, who pursue so-and-so, if thou art male, here is thy
wife; if thou art female, here is thy husband.”297.2 The intent of the
exorciser seems to be to attract the demon of disease, of whose sex
he is not sure, into one or the other of these images, and he lures it
by amorous enticement into the figure of opposite sex to its own;
having got the demon into the image, he doubtless takes it out and
burns or buries it. Or the evil spirit may be attracted from the patient
by means of its own image placed near him. One document
prescribes various images of bestial form, all of which are to be
taken by night to the bank of the river, probably that they may be
thrown in and carry the impurity of sickness away.298.1 Another
shows us how to deal with Labartu, the daughter of Anu;298.2 her
image, made of clay, is placed above the head of the sick man, so as
to draw her or her power out from him; it is then taken out, slain, and
buried. And this exorcism is all the more notable because Labartu is
rather an evil goddess than a mere demon, being styled in another
text “August lady,” “Mistress of the dark-haired men.”298.3 Such
magical drama, in which the demon-image might be slain to annul its
potency, seems characteristically Babylonian: it entered also into the
ritual of the high gods. For, at the feast of the New Year, when Nebo
arrived from Borsippa, two images are brought before him and in his
presence decapitated with the sword. Dr. Langdon interprets
them298.4 as representing probably “the demons who aided the
dragon in her fight with Marduk; they are the captive gods of
darkness which ends with the Equinox.” This is dramatic magic
helpful to the gods.
The elaboration of exorcism must have led to a minuter articulation
of the demon-world; the exorciser is most anxious to know and
discover all about his unseen foes: he gives them a name, a sex if
possible, and a number: he says of the powerful storm-demons Utuk
“they are seven, they are seven, they are neither male nor female,
they take no wife and beget no children;”299.1 for knowledge of the
name or nature of the personality gives magic power.
Many of these examples, which might easily be multiplied, show
us magic applied to private but beneficent purposes, the healing of
disease, the exorcism of spirits of moral and physical evil. It was also
in vogue for national purposes—for instance, for the destruction of
the enemies of the king; one of our documents describes such a
process as the making of a tallow-image of the enemy of the king
and binding his face with a cord, so as to render the living foe
impotent of will and speech.299.2
We have already noticed that the Babylonian gods themselves
work magic, and that it was also worked on behalf of the gods.299.3
And in the ritual-records much that might be interpreted as religion
may find its truer account from the other point of view; for instance,
the ritual of placing by the bedside of a sick man the image of Nergal
or those of the “twins who overthrow the wicked Gallu”299.4 might
appear at first sight as a religious appeal to the deities to come to his
aid; but as in form it is exactly similar to the use made on the same
occasion, as noted above, of the images of demons, we may rather
suppose that the intention was magical in this act also, and that the
divine idols were supposed to combat the demon of sickness by their
magical influence. Or, again, in part of the ritual of exorcism we find
acts that bear the semblance of sacrifice, such as throwing onions
and dates into the fire; but they were charged with a curse before
thrown, and the act is more naturally interpreted as a magic
transference of evil.300.1
For the purpose of the exorcism, to deliver a “banned” person, the
high god, Marduk or another, might be called in; but Marduk also
works the effect by magic: a rope is woven by Ishtar’s maidens,
which Marduk (or his priest) turns round the head of the sufferer,
then breaks it through and throws it out into the desert.300.2 This
looks like symbolic magic; the knotted rope represents the ban,
which is then broken and thrown away.
There are many features in these methods of exorcism, such as
the apotropaeic use of idols, that are common to other peoples at a
certain stage of culture; there remains much also that seems
peculiar to Babylon.
But what is uniquely characteristic of this Mesopotamian people,
and at the same time most un-Hellenic, is the all-pervading
atmosphere of magic, which colours their view of life and their theory
of the visible and invisible world. Babylonia, at least, was the one
salient exception to the historic induction that a distinguished
writer300.3 has recently sanctioned—“religion once firmly established
invariably seeks to exclude magic; and the priest does his best to
discredit the magician.” The psalmody of Babylon, with its occasional
outbursts of inspiration and its gleams of spiritual insight, would have
appealed to an Isaiah; its magic would have appealed to many a
modern African. The Babylonian prophet does not frown on it; the
high gods accept it, the priest is its skilled and beneficent
practitioner. And at no other point, perhaps, is the contrast between
the Hellenic and the Mesopotamian religions so glaring as at this.
This comparison of Eastern and Western ritual may close with
some observations on another religious function that may be of
some value for the question of early ethnic influence.
It has been remarked that divination played an important, perhaps
a dominant part in the Babylonian ritual of sacrifice, divination, that
is, by inspection of the victim’s entrails, especially the liver; and that
this method was adopted in Greece only in the later centuries.301.1
But there are other salient differences between the Babylonian and
the more ancient mantic art of Hellas.301.2 Another method much in
vogue in the former was a curious mode of divining by mixing oil and
water and watching the movements and behaviour of the two
liquids.301.3 The first and only indication of a similar practice in Hellas
is a passage in the Agamemnon of Æschylus, of which the true
meaning has hitherto escaped the interpreters.301.4 And here, as
usual, an obvious example of Mesopotamian influence on Hellenic
custom belongs only to a late epoch. It is also true that the ancient
divination of the two peoples agreed in certain respects, namely, in
that both used, like most communities at a certain stage of culture,
the auguries of birds and the revelations of dreams. As regards the
facts relating to the former, we know more about Greece than at
present about Babylon. But in the matter of dream-oracles, it is
manifest that the Hellenic phenomena are entirely independent of
Mesopotamian fashion. The Assyrian and Babylonian documents
reveal the fashion of dream-prophecy in its simplest and highest
form: the high deity of his own pleasure sends a dream, and the
divining priest or skilled interpreter interprets it. No hint has so far
been detected of that artificial method of provoking prophetic dreams
by “incubation” or ἐγκοίμησις, the fashion of laying oneself down in
some sacred shrine and sleeping with one’s ear to the ground, that
was much in vogue in ancient Hellas and still survives in parts of the
modern Greek world and which may be regarded as an immemorial
tradition. In this divination, the divine spokesman was the power of
the underworld. And this was the most important difference between
the Western and the Eastern society in respect of the divine agency.
In an early period of Hellenic history that may be called pre-Apolline,
the earth-mother was conspicuously oracular by the vehicle of
dreams; and this power of hers was generally shared by the nether
god and buried heroes. Nor could the religion of Apollo suppress this
“chthonian” divination. But in Mesopotamia the earth-powers and the
nether world have no part or lot in this matter. It is almost the
prerogative of Shamash, the sun-god, though Adad is sometimes
associated with him;302.1 both being designated as “Bēlē-Biri” or
“Lords of Oracles.”303.1
Another remarkable distinction is the fact that the ecstatic or
enthusiastic form of prophecy, that of the Shaman or Pythoness
possessed and maddened by the inworking spirit of god, is not found
in the Babylonian record, which only attests the cool and scientific
method of interpreting by signs and dreams and the stars. Perhaps
Mesopotamia from the third millennium onward was too civilised to
admit the mad prophet and prophetess to its counsels. But such
characters were attached to certain Anatolian cults, especially to
those of Kybele,303.2 and also to the Syrian goddess at
Hierapolis;303.3 we have evidence of them also in a record of the
Cretan Phaistos in the service of the Great Mother.303.4 Some
scholars have supposed that prophetic ecstasy was only a late
phenomenon in Hellas, because Homer is silent about it. But there
are reasons for suspecting that demoniac possession was
occasionally found in the pre-Homeric divination of Hellas,303.5 an
inheritance perhaps from the pre-Hellenic period.
In any case, the theory that primitive Hellas was indebted to
Babylonia for its divination-system is strongly repugnant to the facts.
CHAPTER XIV.
Summary of Results.
This comparative exposition of the Sumerian-Babylonian and the

most complex and developed pre-Christian religion of Europe cannot
claim to be complete or at any point finally decisive, but it may at
least have helped to reveal the high value and interest of these
phenomena for the workers in this broad field of inquiry. This was
one of the main objects of this course. The other was the discussion
of a question of religious ethnology, concerning the possible
influence of Mesopotamia on the earliest development of Hellenic
religion. The verdict must still remain an open one, awaiting the light
of the new evidence that the future will gather. But the evidence at
present available—and it may be hoped that none of first importance
has been missed—constrains us to a negative answer or at least a
negative attitude of mind.
Confining ourselves generally to the second millennium B.C., we
have surveyed the religions of the adjacent peoples between the
valley of the Euphrates and the western shores of the Aegean; and
have observed that morphologically they are generally on the same
plane of polytheism, but that those of Mesopotamia and Hellas
reveal inner differences, striking and vital enough to be serious
stumbling-blocks to a theory of affiliation. These differences concern
the personality of the divinities and their relations to the various parts
of the world of nature; the most salient being the different attitude of
the two peoples to the divine luminaries of heaven and to the
chthonian powers of the lower world. They concern the cosmogonies
of East and West, their views of the creation of the world, and the
origin of man; on these matters, certain myths which are easily
diffused do not appear to have reached Hellas in this early period.
They concern the religious temperaments of the Babylonian and
Hellene, which appear as separate as the opposite points of the
pole; the rapturous fanatic and self-abasing spirit of the East
contrasting vividly with the coolness, civic sobriety, and self-
confidence of the West. They concern the eschatologic ideas of the
two peoples: the cult of the dead and some idea of a posthumous
judgment being found in early Hellas, while the former was rare, and
the latter is scarcely discoverable, in Mesopotamia. They concern,
finally, the ritual; and here the salient points of contrast are the
different views of the sacrifice, of the sacrificial victim, and the
sacrificial blood; the different methods of purification and the
expulsion of sin; the ritual of sorrow associated with the death of the
god, so powerful in Babylonia and so insignificant (by comparison) in
Hellas; the un-Hellenic Mylitta-rite, and the service of the
“hierodoulai”; and, to conclude with the most vital difference of all,
the manifestations of magic and its relation to the national religions,
so complex, so pregnant for thought and faith, and so dominant in
Mesopotamia; on the other hand, so insignificant and unobtrusive in
Hellas.
Two other points have been incidentally noticed in our general
survey, but it is well in a final summing up to emphasise their great
importance as negative evidence. The first concerns the higher
history of European religion: the establishment of religious mysteries,
a phenomenon of dateless antiquity, and of powerful working in
Hellenic and Aegean society, has not yet been discovered in the
Mesopotamian culture. The second is a small point that concerns
commerce and the trivialities of ritual: the use of incense, universal
from immemorial times in Mesopotamia, and proved by the earliest
documents, begins in Greece not earlier than the eighth century B.C.
This little product, afterwards everywhere in great demand, for it is
pleasant to the sense, soothing to the mind, and among the
harmless amenities of worship, was much easier to import than
Babylonian theology or more complex ritual. It might have come
without these, but they could scarcely have come without it. Yet it did
not come to Hellenic shores in the second millennium. And this
trifling negative fact is worth a volume of the higher criticism for the
decision of our question.
Those who still cling to the faith that Babylonia was the centre
whence emanated much Mediterranean religion, may urge that the
negative value of the facts exposed above may be destroyed by
future discoveries. This is true, but our preliminary hypotheses
should be framed on the facts that are already known. Or they may
urge that the generic resemblances of the two religious systems with
which we have been mainly concerned are also great. But, as has
been observed, the same generic resemblance exists between
Greek and Vedic polytheism. And for the question of religious origin
general resemblances are far less decisive than specific points of
identity, such, for instance, as the identity of divine names or of some
peculiar divine attribute. Later we can trace the migrations of Isis and
Mithras throughout Europe by their names or by the sistrum or by the
type of the fallen bull, of the Hittite god Teschub in the Graeco-
Roman guise of Jupiter Dolichenos as far as Hungary, perhaps as
far as Scandinavia, by the attribute of the hammer. It is just this sort
of evidence of any trace of Babylonian influence that is lacking
among the records of early Greece. No single Babylonian name is
recognisable in its religious or mythologic nomenclature; just as no
characteristically Babylonian fashion is found in its ritual or in the
appurtenances of its religion. This well accords with what is already
known of the Mediterranean history of the second millennium. For
long centuries the Hittite empire was a barrier between the
Babylonian power and the coastlands of Asia Minor.
So far, then, as our knowledge goes at present, there is no reason
for believing that nascent Hellenism, wherever else arose the
streams that nourished its spiritual life, was fertilised by the deep
springs of Babylonian religion or theosophy.
INDEX OF NAMES AND
SUBJECTS.
Adad (Ramman), 62, 101-102, 142, 143.
Adonis, 251, 255, 273-274.
Alilat, 44.
Allatu, 57, 206, 218.
Aniconic worship, 225-230.
Animism, 43.
Anthropomorphism, in Greece, 10-12, 75-80; in Mesopotamia, 51-
52, 55-57; in Canaan, 57-58; in Hittite religion, 60-61; in Phrygia,
63-64; in Crete, 64-75.
Aphrodite, Cretan-Mycenaean, 96; in Cyprus, 261; Ourania, 272-
273.
Apollo, 49, 295; theory of Lycian origin, 90; Agyieus, 136; Delphinios,
291; Lykeios, 76.
Arabian divinities, 85, 263.
Aramaic divinities, 85.
Artemis, of Brauron, 244; in Cilicia, 89; at Ephesos, 91; aboriginal
Mediterranean goddess, 96.
Aryan migration into Greece, 34.
Asshur, 58, 225.
Astarte, 57, 58, 59, 86, 107.
Astral cults, in Mesopotamia, 102; in Greece, 111-114.
Atargatis (Derketo), 57.
Athena, aboriginal Mediterranean goddess, 96.
Athtar, Arabian deity, 85, 263.
Attar, in Arabia, 168.
Attis, 91, 254-258, 266; Παπαῖος, 95.
Axe-cult, in Crete, 70, 93.
Baalbec, 273-274.
Baptism, 284.
Bau, Babylonian goddess, 263.
Belit, Babylonian goddess, 83, 84, 104.
Birds, cult of, 63, 69-73.
Boghaz-Keui, reliefs of, 47, 60, 125; cuneiform texts at, 61.
Borrowing, tests of, in religion, 37.
Boundaries, sanctity of, 127-128.
Bouphonia, in Attica, 237-238.
Britomartis, 170.
Bull, Hittite worship of, 252-253.
Burial-customs, 208-210.
Byblos, Adonis-rites at, 273-274.
Chemosh, of Moab, 59, 86.
Cilicia, Assyrian conquests in, 35 (vide Typhoeus).
Cities, religious origin of, 118.
Communion-service with dead, 209.
Confessional-service in Mesopotamia, 151, 288.
Convent-system in Mesopotamia, 268-269.
Cook, Mr., 66, 69, 73.
Cosmogonies, 179-182.
Courtesans, sacred, 269-283.
Cowley, Dr., 90.
Creation of man, 184-185.
Cyprus, religious prostitution in, 273-274.
Days, sacred character of, 293-295.
Dead, worship of, 122, 210, 211, 213; tendance of, 211, 212;
evocation of, 214-215.
Death of deity, 27-28, 238-240, 249-263.
Demeter, 80.
Demonology, 154, 206-208, 297-300.
Dionysos, 239-240; marriage with Queen-Archon, 267.
Divination, through sacrifice, 248-249, 301-302; ecstatic, 303.
Dualism, 19, 158.
Ea, Babylonian god, 53, 102, 117, 121.
Eagle, Hittite worship of, 63.
Earth, divinity of, in Mesopotamia, 103; in Greece, 114.
Enlil, Babylonian god, 59, 103-104, 142.
Eros, cosmic principle, 181.
Eschatology, 204-220.
Esmun, Phoenician god, 57.
Eunostos, Tanagran vegetation-hero, 262.
Eunuchs, in Phrygian religion, 92, 256-258.
Euyuk, relief at, 61.
Evans, Sir Arthur, 17, 30, 64, 69-71, 73-74, 91, 97, 211, 227.
Evil gods, 19, 142-143.
Faith, not a religious virtue in Greece, 23-24.
Fanaticism, in Mesopotamia, 197-203.
Fassirlir, Lion-goddess at, 88.
Father-god, 48, 95.
Fetichism, 225-228.
Fire-god, in Greece and Babylon, 146-147, 285.
Fire-purification, 285-286.
Frazer, Dr., 17, 60, 79, 89, 257 n. 1, 277, 282.
Functional deities (Sondergötter), 110, 133.
Goddess-worship, importance of, 5, 81-82; in Mesopotamia, 17, 82-
84; among Western Semites, 85-86; Hittites, 87-88; on Asia-
Minor coast, 88-91; in Crete, 92-94; Aryan tradition of, 94-96; in
early Greece, 96-98.
Hammer, sacred Hittite symbol, 63.
Hammurabi, code of, 129-132, 212.
Harpalyke, legend of, 239.
Harrison, Miss Jane, 67, 69-70.
Hartland, Mr. Sidney, 271 n. 1, 280-281.
Hearth-worship, 132-133.
Helios, at Tyre and Palmyra, 107; in Greece, 110-111.
Hell, Babylonian conception of, 205-206.
Hera, ? Aryan-Hellenic, 96; βοῶπις, 76.
Hierodoulai, 272.
Hittite ethnology, 36.
Hogarth, Dr., 74.
Homicide, Babylonian laws concerning, 129-130; Hellenic religious
feeling about, 138-140; purification from, 287-288.
Hyakinthos, 262.
Ibriz, Hittite monument at, 47.
Idolatry, in Greece, 12-13, 228.
Incense, 231-232, 306.
Incest, Babylonian laws concerning, 131.
Incubation, divination by, 302.
Ira, goddess of plague, 143.
Ishtar, 55, 83, 103, 120, 142, 164-167; descent of, 204, 208.
Jastrow, Prof., 37, 58.
Katharsis, Homeric, 289-291.
Kingship, divine character of, in Mesopotamia, 119, 122-123; among
Western Semites, 123; among Hittites, 124-125; in Phrygia, 125;
in Crete, 125-126; in Greece, 126-127.
Knots, magic use of, 300.
Kybele, 63, 91-92, 109, 170, 226.
Labartu, demon-goddess, 298.
Langdon, Dr., 56, 205 n. 1, 296, 298.
Leto ? Lycian origin of, 89-90.
Leukothea, 261.
Linos, 197, 262.
Lion-divinity, Phrygian Hittite Mesopotamian type, 62-63.
Lykaon, Arcadian sacrifice of, 239.
Ma, Anatolian goddess, 169, 272.
Magic, in Greece, 158, 176-179, 292-293; in Babylon, 291-301.
Male deity, predominant among Semites, 85-86; at Olba and Tarsos
and in Lycia, 89.
Mannhardt, 276.
Marduk, 103, 120, 265.
Marriage of god and goddess, 263-268; marriage ceremonies in
Babylon, 134.
Mercy, attribute of divinity, 158-160.
Minotaur, 74, 266-267.
Mitani inscriptions, 46.
Monotheism, 187-189.
Monsters, in Cretan art, 74-75.
Moon-worship, Semitic, 85; Hellenic, 112.
Morality and religion, 20.
Mylitta, rites of, 269-271.
Nature-worship, 40-41, 97; in Mesopotamia, 99-106; West-Semitic,
106-107; Hittite, 108; Hellenic, 110-114.
Nebo, 52, 102, 119, 121, 188.
Nergal, 101, 142.
Νηφάλια, wineless offerings, 112.
Ninib, 101, 117, 127, 263.
Ninlil, 84.
Ninni, relief of, 52.
Nusku, 117.
Omnipotence, divine attribute, 173-175.
Orotal, Arabian deity, 44.
Pan-Babylonism, 30-33.
Pantheism, 161-162.
Perjury, 147-149.
Personal religion, 191-196.
Pessimism, in Babylonian hymns, 155.
Petrie, Professor, 223.
Phallic cults, 228-230.
Phratric system, religious sanction of, in Greece, 138; non-existent
(?) in Mesopotamia, 138.
Poseidon, 146.
Punishment, posthumous, 215-216.
Purification, 155-158, 282-291.
Purity, 163-172.
Qadistu, meaning of, 269.
Ramman, vide Adad.
Ramsay, Sir William, 117, 170, 273, 277.
Rewards, posthumous, 216-218.
Sacrament, 25-26, 236-242, 250.
Sacrifice, theory of, 24-26, 235-236, 240-242; bloodless, 230-231;
chthonian, 233; human, 244-246; at oath-taking, 247-248;
“sober,” 231-232; vicarious, 242-244.
Sandon, 252-253.
Sayce, Professor, 169, 253.
Scapegoat, 247.
Science, relation to religion, in Greece and Mesopotamia, 23.
Sentimentality, in Babylonian religion, 196-197.
Sex, confusion of, 58-60.
Shamash, Babylonian sun-god, 99, 100, 120-121, 127, 142, 208,
302.
Sin, Babylonian moon-god, 99, 100.
Sin, non-moral ideas of, 152-154.
Sinjerli, relief at, 61.
Smith, Prof. Robertson, 25, 226, 235, 238, 241.
Snake-goddess, in Crete, 64-65; snake-cult, 78.
Tammuz, 105-106, 219-220, 242, 250-263.
Tanit, Carthaginian goddess, 168.
Taurobolion, 253.
Temples, erection of, 223-225; deification of, 225.
Teshup, Hittite god, 46, 62.
Teukridai, at Olba, 89.
Theanthropic animal, 77-78.
Theism, 7-9, 40-49.
Theriomorphism, in Egypt, 15; in Mesopotamia, 14, 52-55; in other
Semitic communities, 57-58; Hittite, 60-62; in Crete, 66-75; in
Greece, 75-80.
Tiâmat, in Babylonian cosmogony, 181.
Tiele, Professor, 40, 42, 81, 199.
Tralles, religious prostitutes at, 275.
Trinities, 185-187.
Truthfulness, religious virtue, 148.
Typhoeus, legend of, 182-183.
Van Gennep, 279.
Ver Sacrum, in Greece, 137.
Virgin-goddesses, not found among Aryans, 95; Mediterranean, 96.
Virginity, sacrifice of, 269-281.
Virgin-Mother, idea of, 166-171.
Westermarck, Professor, 41 n. 1, 278.
Wilde, Dr., 1.
Word, mystic value of, 15, 56, 57, 176-179, 295-297.
Worship, ambiguity in term, 67, 77.
Zeus, 49; grave of, in Crete, 93, 259-260; Herkeios, 149-150; Horios,
152; Kouros, 259; Panamaros in Caria, 90; Polieus, 238;
Thunderer in Bithynia, 95.
ENDNOTES
CHAPTER I NOTES
11.1 I am aware that there are exceptions to this principle, which I
propose to consider in a future course; no single formula can ever
sum up all the phenomena of a complex religion.
14.1 Vide Langdon, in Transactions of Congress of the History of
Religions, 1908, vol. i. p. 251.
15.1 P. 382, C.
15.2 Vide Petrie, in Transactions of Congress of the History of
Religions, 1908, vol. i. p. 192.
17.1 Archiv für Religionswissenschaft, 1904.
17.2 Vide Jastrow, Religion Babyloniens u. Assyriens, vol. i. p. 545.
20.1 Vide my Evolution of Religion, pp. 139-152.
21.1 1. 132.
25.1 Transactions of Congress of History of Religions, 1908, vol. i.
p. 192.
25.2 Hibbert Journal, 1904, “Sacrificial Communion in Greek
Religion.”
CHAPTER II NOTES
31.1 Vide the critical remarks on such a view by Prof. Jastrow in
Transactions of the Third International Congress of the History of
Religions, vol. i. pp. 234-237.
34.1 Vide Annual of the British School, 1909, 1910.
35.1 Vide Zimmern, Die Keilinschriften und das alte Testament
(K.A.T.)3, pp. 37-38.

CHAPTER III NOTES
40.1 Vide supra, p. 9.
41.1 Westermarck maintains the view in his Origin and
Development of Moral Ideas, pp. 663-664, that in many savage
religions the gods have no concern with ordinary morality; but the
statistics he gives need careful testing.
42.1 Op. cit., p. 170; as far as I know, only one fact might be cited in
support of Tiele’s view, a fact mentioned by Jastrow, op. cit., p. 52,
that the ideogram of Enlil, the god of Nippur, signifies Lord-Daimon
(Lil = Daimon); but we might equally well interpret it “Lord of Winds.”
42.2 Vide Hüsing, Der Zagros und seine Völker, p. 16.
43.1 Vide Plate in Winckler, “Die Gesetze Hammurabi,” in Der Alte
Orient, 1906.
43.2 Perrot et Chipiez, Histoire de l’art, Assyrie, p. 109, fig. 29
(Roscher, Lexikon, ii. p. 2358).
44.1 3, 8.
45.1 Messerschmidt, Die Hettiter, p. 9; Stanley Cook, Religion of
Ancient Palestine, p. 73.
45.2 So Cook, op. cit., p. 73, who interprets her as Astarte.
45.3 Winckler, Tel-El-Amarna Letters, 17.
46.1 Vide Winckler, Mittheil des deutsch. Orientgesellsch., 1907,
No. 35.
46.2 Winckler, Die Völker Vorderasiens, p. 21; Messerschmidt, op.
cit., p. 5; Kennedy, Journ. Royal Asiat. Soc., 1909, p. 1110, declares
that their language has been proved to belong to the Ural-Altaic
group and to be akin to Vannic.
46.3 Vide Messerschmidt, p. 25 (plate); Von Oppenheim, Der Tel-
Halaf und die verschleierte Gottin, p. 17, publishes a somewhat
similar figure holding a kind of club.
47.1 Perrot et Chipiez, Histoire de l’art, iv. p. 354 (fig.).
47.2 Vide Garstang, The Land of the Hittites, pl. lxiii.-lxxi.;
Messerschmidt, op. cit., pp. 26-27.
48.1 e.g. Outlines of Greek Religion, by R. Karsten, p. 6.
48.2 Vide supra, p. 46; cf. E. Meyer, Das erste Auftreten der Arier in
der Geschichte in Sitzungsb. d. konigl. Preuss. Akad. Wissensch.,
1908, pp. 14 seq.
CHAPTER IV NOTES
52.3 Vide Roscher, Lexikon, vol. iii. p. 48, s.v. “Nebo.”
52.4 Vide Roscher, op. cit., iii. p. 67 (Mitth. aus dem Orient.
Sammlung. zu Berlin, Heft xi. p. 23).
52.5 Monuments of Nineveh, i. p. 65 (Roscher, op. cit., ii. p. 2350).
52.6 P. 43.
52.7 Roscher, op. cit., vol. iv. p. 29.
53.1 Roscher, op. cit., iii. p. 254-255.
53.2 Schrader, Keil. Bibl., ii. p. 141.
53.3 Frag. Hist. Graec., ii. p. 496. Frag. 1, 3.
53.4 Nineveh and Babylon, pl. vi. (Roscher, op. cit., iii. p. 580).
54.1 Layard, Nineveh and Babylon, fig. 2. Roscher, op. cit., iii. p.
580.
54.2 In the Amer. Journ. Archael., 1887, pp. 59-60, Frothingham
cites examples from Assyrian cylinders of birds on pillars or altar with
worshippers approaching: one of these shows us a seated god in
front of the bird (pl. vii. 1); on another, a warrior approaches a
tabernacle, within which is a horse’s head on an altar, and near it a
bird on a column (pl. vii. 2; cf. the boundary-stone of
Nebuchadnezzar I., published by Miss Harrison, Trans. Congr. Hist.
Rel., 1908, vol. ii. p. 158); we find also a winged genius adoring an
altar on which is a cock. But cocks and other birds were sacrificial
animals in Babylonian ritual, and might be interpreted in all these
cases as mere temporary embodiments of the divinity’s power; the
human-shaped divinity is once represented by the side of the bird,
and might always have been imagined as present though unseen.
55.1 Roscher, Lexikon, iii. p. 268.
55.2 Vide chapter i. pp. 14-15.
56.1 Langdon, Sumerian and Babylonian Psalms, p. 127.
56.2 Schrader, Keilinsch. Bibl., ii. pp. 79, 83.
56.3 Op. cit., p. xix.
57.1 Langdon, op. cit., p. 159, n. 18. Compare with this the
personification of abstract ideas; the children of Shamash are Justice
(Kettu) and Law (Mésaru), and remain impersonal agencies, unlike
the Greek Θέμις. A deified Righteousness (sedek) has been inferred
from personal names that occur in the Amarna documents; vide
Cook, Palestine, p. 93.
57.2 Vide his article on “Eschmun-Asklepios,” in Orient. Stud. zu
Th. Nöldeke am 70ten Geburtstag gewidmet: the proofs are doubtful,
but snake-worship in Phoenicia is attested by Sanchuniathon, Eus.
Praep. Ev., 1, 10, 46.
57.3 Cook, Religion of Ancient Palestine, pp. 30-31.
58.1 Praep. Ev., 1, 10, 31. Glaser, Mittheilungen uber einige
Sabaeische Inschriften, p. 3-4, gives reasons for affirming the
worship of black bulls in heathen Arabia; but it is not clear in what
relation these stood to the high personal divinities.
58.2 Op. cit., p. 545.
59.1 Langdon, op. cit., p. 223.
59.2 Zimmern, Babyl. Hymn. w. Gebete, p. 11.
59.3 C. I. Sem., 250.
60.1 For references, vide my Cults of the Greek States, vol. ii.,
“Aphrodite,” R. 113a.
60.2 Vide Head, Hist. Num., p. 586.
61.1 Perrot et Chipiez, Histoire de l’art, iv. fig. 329; cf. Garstang, op.
cit., p. 256.
61.2 Supra, p 43.
61.3 Messerschmidt, op. cit., p. 23.
61.4 Journ. Roy. Asiat. Soc., 1909, p. 971.
62.1 Luschan, Ausgrabungen in Sendschirli, Heft iii. Taf. 42, 43; cf.
Garstang, op. cit., p. 274.
62.2 Vide Roscher, op. cit., iii., s.v. “Ramman.”
62.3 Perrot et Chipiez, op. cit., iv. p. 549, fig. 276; cf. fig. 278.

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Biophysics and biochemistry of

cartilage by nmr and mri 1st Edition

Biochemistry, Biophysics, and Molecular Chemistry-

Sectional Anatomy by MRI and CT 4th Edition Mark W.

Modern Tools of Biophysics 1st Edition Thomas Jue

The Illustrative Book of Cartilage Repair 1st Edition

Applications of EPR and NMR spectroscopy in homogeneous

Biophysics of Skin and Its Treatments: Structural,

Articular Cartilage Second Edition Kyriacos A.

A Mathematical Primer of Molecular Phylogenetics 1st

Biophysics and Biochemistry of Cartilage by NMR and MRI

New Developments in NMR

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Biophysics and Biochemistry of

New Developments in NMR No. 8

Print ISBN: 978-1-78262-133-1

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This is a unique book providing a contemporary snapshot of the roles that

New Developments in NMR No. 8

sively, an accurate diagnosis of osteoarthritis at a time when the joint is still

I dedicate this book to my parents 镇澳 and 钺, for their unconditional love

New Developments in NMR No. 8

adventure at Oakland University.

Part One – Introduction

Chapter 1 Introduction to Cartilage  3

New Developments in NMR No. 8

Chapter 2 Osmotic Properties of Cartilage  44

Chapter 3 Introduction to NMR and MRI  62

3.3.7 NMR Observables and Coherence Order  88

4.1 I ntroduction  109

4.7 The T2 Versus T2* Conundrum  139

Part Two – Cartilage Research by Experimental NMR

Chapter 5 Physical Properties of Cartilage by Relaxation

5.1 I ntroduction  147

6.1 I ntroduction  176

Chapter 7 Quantification of Articular Cartilage Microstructure

7.1 I ntroduction  191

Chapter 8 Sodium and Other Exotic Methods in NMR and MRI of

8.3 T1ρ MRI  229

Chapter 9 Multi-Quantum Filtered NMR and MRI of Cartilage  246

9.1 I ntroduction  246

Chapter 10 Solid-State NMR Techniques to Study the Molecular

10.1 I ntroduction  279

Chapter 11 Ultrashort Echo Time Imaging of Articular Cartilage  299

11.1 I ntroduction  299

Chapter 12 Low-Field and Field-Cycling NMR and MRI of Cartilage  320

12.1 I ntroduction: Low Field vs. Variable Field  320

12.5 Variable-Field Studies of Cartilage  337

Chapter 13 The Influence of Specimen and Experimental

13.1 I ntroduction  347

Part Three – Biomechanical Properties of Cartilage

Chapter 14 Diffusion MRI and Poroelastic Biomechanics of

Articular Cartilage  375

14.1 I ntroduction  375

Chapter 15 Combining Multi-Modal MRI and Biomechanical

15.1 I ntroduction  395

Chapter 16 Loading-Induced Changes in Cartilage Studied by

Chapter 1 Introduction to Cartilage 3

Chapter 2 Osmotic Properties of Cartilage 44

Chapter 3 Introduction to NMR and MRI 62

3.3.7 NMR Observables and Coherence Order 88

4.1 I ntroduction 109

4.7 The T2 Versus T2* Conundrum 139

Chapter 5 Physical Properties of Cartilage by Relaxation

5.1 I ntroduction 147

6.1 I ntroduction 176

Chapter 7 Quantification of Articular Cartilage Microstructure

7.1 I ntroduction 191

Chapter 8 Sodium and Other Exotic Methods in NMR and MRI of

8.3 T1ρ MRI 229

Chapter 9 Multi-Quantum Filtered NMR and MRI of Cartilage 246

9.1 I ntroduction 246

Chapter 10 Solid-State NMR Techniques to Study the Molecular

10.1 I ntroduction 279

Chapter 11 Ultrashort Echo Time Imaging of Articular Cartilage 299

11.1 I ntroduction 299

Chapter 12 Low-Field and Field-Cycling NMR and MRI of Cartilage 320

12.1 I ntroduction: Low Field vs. Variable Field 320

12.5 Variable-Field Studies of Cartilage 337

Chapter 13 The Influence of Specimen and Experimental

13.1 I ntroduction 347

Chapter 14 Diffusion MRI and Poroelastic Biomechanics of

Articular Cartilage 375

14.1 I ntroduction 375

Chapter 15 Combining Multi-Modal MRI and Biomechanical

15.1 I ntroduction 395

Chapter 16 Loading-Induced Changes in Cartilage Studied by

16.1 I ntroduction 433

Chapter 17 The Critical Role of High Imaging Resolution in

17.1 I ntroduction 457

17.3.4 Orientation of the Specimen in the Magnet 463

Chapter 18 Multicomponent Relaxation in NMR and MRI of Cartilage 471

18.1 I ntroduction 471

Chapter 19 Uni- and Multi-Parametric Magnetic Resonance

19.1 I ntroduction to Cartilage MRI Classification 494

19.4.1 Multivariate Classification of Cartilage

Chapter 20 Magnetic Resonance in the Assessment of Tissue

20.1 I ntroduction 529

Chapter 21 Complementary Imaging in MRI of Cartilage 552

21.1 I ntroduction 552

21.7 Final Remarks 567

Chapter 22 Quantitative MRI for Detection of Cartilage Damage 575

22.1 I ntroduction 575

Chapter 23 Challenges for the Early Detection of Degenerative

23.1 I ntroduction 628

23.3.3 Semi-Quantitative vs. Quantitative

Chapter 24 Ultrahigh-Field Whole-Body MRI for Cartilage Imaging:

24.1 I ntroduction 671

Proteoglycan Content 695

Subject Index 706

1.2 Cartilage and the Joint

1.2.1 Different Types of Cartilage