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Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP001
Editor-in-Chief:
Professor William S. Price, University of Western Sydney, Australia
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP001
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
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
A catalogue record for this book is available from the British Library
Apart from fair dealing for the purposes of research for non-commercial purposes or for
private study, criticism or review, as permitted under the Copyright, Designs and Patents
Act 1988 and the Copyright and Related Rights Regulations 2003, this publication may
not be reproduced, stored or transmitted, in any form or by any means, without the prior
permission in writing of The Royal Society of Chemistry or the copyright owner, or in
the case of reproduction in accordance with the terms of licences issued by the Copyright
Licensing Agency in the UK, or in accordance with the terms of the licences issued by the
appropriate Reproduction Rights Organization outside the UK. Enquiries concerning
reproduction outside the terms stated here should be sent to The Royal Society of
Chemistry at the address printed on this page.
The RSC is not responsible for individual opinions expressed in this work.
The authors have sought to locate owners of all reproduced material not in their
own possession and trust that no copyrights have been inadvertently infringed.
Printed in the United Kingdom by CPI Group (UK) Ltd, Croydon, CR0 4YY, UK
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP005
Preface
v
View Online
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-
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP005
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
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP005
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.
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP009
Acknowledgements
ix
View Online
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
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP009
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-
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP009
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
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
Contents
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
xiii
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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
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
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
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
3.1 I ntroduction 62
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
View Online
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
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
Chapter 4 The Magic Angle Effect in NMR and MRI of Cartilage 109
Gary D. Fullerton
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
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
Contents xvii
Chapter 6 Chemical Properties of Cartilage Studied Using
Charged Ions 176
Olle Söderman, Jenny Algotsson, Leif E. Dahlberg and Jonas
Svensson
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
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
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
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
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
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
10.6 Conclusions 295
References 296
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
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
Contents xxi
xxii Contents
15.7 Outlook 421
Acknowledgements 423
References 423
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
Contents xxiii
17.3.2 T
opographical Distribution of Cartilage
Properties 460
17.3.3 Long Degradation Process with Diverse
Early Characteristics 462
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
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
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
Contents xxv
21.4 E lectron Microscopy 561
21.5 Microscopic Computed Tomography 563
21.6 Additional Imaging Techniques in Cartilage
Research 564
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
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
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
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
Published on 26 September 2016 on http://pubs.rsc.org | doi:10.1039/9781782623663-FP013
(Melyben Spuller Jeannette saját személyében lép fel és rangjához méltó állásába
visszavonul.)
(Az illem még ma tiltja a szív hangján megszólalni, de megengedi, hogy üzleti
ügyeket tisztába hozzunk.)