High-resolution measurements of the multilayer ultra-structure of articular cartilage and their translational potential

Current musculoskeletal imaging techniques usually target the macro-morphology of articular cartilage or use histological analysis. These techniques are able to reveal advanced osteoarthritic changes in articular cartilage but fail to give detailed information to distinguish early osteoarthritis from healthy cartilage, and this necessitates high-resolution imaging techniques measuring cells and the extracellular matrix within the multilayer structure of articular cartilage. This review provides a comprehensive exploration of the cellular components and extracellular matrix of articular cartilage as well as high-resolution imaging techniques, including magnetic resonance image, electron microscopy, confocal laser scanning microscopy, second harmonic generation microscopy, and laser scanning confocal arthroscopy, in the measurement of multilayer ultra-structures of articular cartilage. This review also provides an overview for micro-structural analysis of the main components of normal or osteoarthritic cartilage and discusses the potential and challenges associated with developing non-invasive high-resolution imaging techniques for both research and clinical diagnosis of early to late osteoarthritis.

[1]  Guy Cox,et al.  3-dimensional imaging of collagen using second harmonic generation. , 2003, Journal of structural biology.

[2]  J. B. Kneeland,et al.  Sensitivity of MRI to proteoglycan depletion in cartilage: comparison of sodium and proton MRI. , 2000, Osteoarthritis and cartilage.

[3]  P. Eggli,et al.  Zone‐specific cell biosynthetic activity in mature bovine articular cartilage: A new method using confocal microscopic stereology and quantitative autoradiography , 1996, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[4]  Michael P Recht,et al.  MRI of articular cartilage: revisiting current status and future directions. , 2005, AJR. American journal of roentgenology.

[5]  J. Yoo,et al.  MR imaging of articular cartilage at 1.5T and 3.0T: comparison of IDEAL 2D FSE and 3D SPGR with fat-saturated 2D FSE and 3D SPGR in a porcine model , 2014, Acta radiologica.

[6]  H J Mankin,et al.  Water content and binding in normal and osteoarthritic human cartilage. , 1975, The Journal of bone and joint surgery. American volume.

[7]  Andrew D Pearle,et al.  Basic science of articular cartilage and osteoarthritis. , 2005, Clinics in sports medicine.

[8]  D. Eyre.  Articular cartilage and changes in Arthritis: Collagen of articular cartilage , 2001, Arthritis research.

[9]  Gil Navon,et al.  Assessment of glycosaminoglycan concentration in vivo by chemical exchange-dependent saturation transfer (gagCEST) , 2008, Proceedings of the National Academy of Sciences.

[10]  J. Buckwalter,et al.  Structural differences between two populations of articular cartilage proteoglycan aggregates , 1994, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[11]  D. Burstein,et al.  Diffusion of small solutes in cartilage as measured by nuclear magnetic resonance (NMR) spectroscopy and imaging , 1993, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[12]  T. B. Kirk,et al.  Laser scanning confocal arthroscopy of a fresh cadaveric knee joint. , 2007, Osteoarthritis and cartilage.

[13]  Mark Bydder,et al.  Magnetic Resonance: An Introduction to Ultrashort TE (UTE) Imaging , 2003, Journal of computer assisted tomography.

[14]  C. A. Poole.  Articular cartilage chondrons: form, function and failure. , 1997, Journal of anatomy.

[15]  Y. Hirasawa,et al.  Acridine orange induces binucleation in chondrocytes. , 2001, Osteoarthritis and cartilage.

[16]  D G Disler,et al.  MR imaging of articular cartilage. , 1998, Skeletal radiology.

[17]  T. B. Kirk,et al.  Microstructural analysis of collagen and elastin fibres in the kangaroo articular cartilage reveals a structural divergence depending on its local mechanical environment. , 2013, Osteoarthritis and cartilage.

[18]  T. Andrews,et al.  Massively parallel sequencing of the mouse exome to accurately identify rare, induced mutations: an immediate source for thousands of new mouse models , 2012, Open Biology.

[19]  C. A. Poole.  Review. Articular cartilage chondrons: form, function and failure , 1997 .

[20]  A. Hall,et al.  The osmotic sensitivity of isolated and in situ bovine articular chondrocytes , 2001, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[21]  V. Mlynárik,et al.  A method for generating magnetic resonance microimaging T2 maps with low sensitivity to diffusion , 1996, Magnetic resonance in medicine.

[22]  Bruce J Tromberg,et al.  Nonlinear optical microscopy of articular cartilage. , 2005, Osteoarthritis and cartilage.

[23]  T. B. Kirk,et al.  Confocal arthroscopic assessment of osteoarthritis in situ. , 2008, Arthroscopy : the journal of arthroscopic & related surgery : official publication of the Arthroscopy Association of North America and the International Arthroscopy Association.

[24]  M. Glimcher,et al.  Changes in the hexosamine content and swelling ratio of articular cartilage as functions of depth from the surface. , 1976, The Journal of bone and joint surgery. American volume.

[25]  T. B. Kirk,et al.  ASSESSMENT OF THREE-DIMENSIONAL ARCHITECTURE OF COLLAGEN FIBERS IN THE SUPERFICIAL ZONE OF BOVINE ARTICULAR CARTILAGE , 2004 .

[26]  A. Hall,et al.  Abnormal Human Chondrocyte Morphology is Related to Increased Levels of Cell-Associated IL-1β and Disruption to Pericellular Collagen Type VI , 2010, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[27]  Thomas M. Link,et al.  T1rho, T2 and focal knee cartilage abnormalities in physically active and sedentary healthy subjects versus early OA patients—a 3.0-Tesla MRI study , 2008, European Radiology.

[28]  G. Lust,et al.  Origin of cartilage laminae in MRI , 1997, Journal of magnetic resonance imaging : JMRI.

[29]  J. Dunn,et al.  In vitro MR imaging of hyaline cartilage: correlation with scanning electron microscopy. , 2000, AJR. American journal of roentgenology.

[30]  G. S. Montes,et al.  Distribution of elastic system fibers in hyaline and fibrous cartilages of the rat. , 1984, Acta anatomica.

[31]  M. McKee,et al.  Aged bovine chondrocytes display a diminished capacity to produce a collagen‐rich, mechanically functional cartilage extracellular matrix , 2005, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[32]  T. B. Kirk,et al.  Matrix‐induced autologous chondrocyte implantation in sheep: objective assessments including confocal arthroscopy , 2008, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[33]  T. B. Kirk,et al.  Histological assessment of the chondral and connective tissues of the knee by confocal arthroscope , 2004 .

[34]  F. Young.  Biochemistry , 1955, The Indian Medical Gazette.

[35]  L. Debelle,et al.  Elastin: molecular description and function. , 1999, The international journal of biochemistry & cell biology.

[36]  Andrew J Wheaton,et al.  Proteoglycan loss in human knee cartilage: quantitation with sodium MR imaging--feasibility study. , 2004, Radiology.

[37]  M. A. R. Freeman,et al.  Adult Articular Cartilage , 1973 .

[38]  Hugh C Burry,et al.  Adult Articular Cartilage , 1974 .

[39]  Fernando Boada,et al.  MRI of articular cartilage in OA: novel pulse sequences and compositional/functional markers. , 2006, Osteoarthritis and cartilage.

[40]  Van,et al.  Spatial variation of T2 in human articular cartilage. , 1997, Radiology.

[41]  Paul Campagnola,et al.  Second harmonic generation imaging microscopy: applications to diseases diagnostics. , 2011, Analytical chemistry.

[42]  M. Ferguson,et al.  Novel articular cartilage structure in the South American opossum, Monodelphis domestica. , 1993, Journal of anatomy.

[43]  D. Heinegård,et al.  The Articular Cartilage , 2008 .

[44]  Comparison of 3T and 7T MRI clinical sequences for ankle imaging. , 2012, European journal of radiology.

[45]  Charles A McKenzie,et al.  Delayed gadolinium-enhanced magnetic resonance imaging of cartilage in knee osteoarthritis: findings at different radiographic stages of disease and relationship to malalignment. , 2005, Arthritis and rheumatism.

[46]  Peter Bachert,et al.  Cartilage quality assessment by using glycosaminoglycan chemical exchange saturation transfer and (23)Na MR imaging at 7 T. , 2011, Radiology.

[47]  W M Lai,et al.  A triphasic theory for the swelling and deformation behaviors of articular cartilage. , 1991, Journal of biomechanical engineering.

[48]  Julian Moger,et al.  The elastin network: its relationship with collagen and cells in articular cartilage as visualized by multiphoton microscopy , 2009, Journal of anatomy.

[49]  T. B. Kirk,et al.  Elastin fibers display a versatile microfibril network in articular cartilage depending on the mechanical microenvironments , 2013, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[50]  V. Mlynárik,et al.  Investigation of laminar appearance of articular cartilage by means of magnetic resonance microscopy. , 1996, Magnetic resonance imaging.

[51]  T. B. Kirk,et al.  Microstructural and Compositional Features of the Fibrous and Hyaline Cartilage on the Medial Tibial Plateau Imply a Unique Role for the Hopping Locomotion of Kangaroo , 2013, PloS one.

[52]  T. B. Kirk,et al.  QUANTIFICATION OF CHONDROCYTE MORPHOLOGY BY CONFOCAL ARTHROSCOPY , 2004 .

[53]  J. B. Kneeland,et al.  Human knee: in vivo T1(rho)-weighted MR imaging at 1.5 T--preliminary experience. , 2001, Radiology.

[54]  R M Henkelman,et al.  Effects of collagen orientation on MR imaging characteristics of bovine articular cartilage. , 1993, Radiology.

[55]  S. Kranenbarg,et al.  Quantitative description of collagen structure in the articular cartilage of the young and adult equine distal metacarpus , 2008 .

[56]  D. Burstein,et al.  MRI Techniques in Early Stages of Cartilage Disease , 2000, Investigative radiology.

[57]  A. Simpson,et al.  Chondrocyte death in mechanically injured articular cartilage—the influence of extracellular calcium , 2009, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[58]  M. Glimcher,et al.  Predominance of type I collagen at the surface of avian articular cartilage , 1978, FEBS letters.

[59]  Young Cheol Yoon,et al.  Qualitative and Quantitative Assessment of Wrist MRI at 3.0t: Comparison between Isotropic 3d Turbo Spin Echo and Isotropic 3D Fast Field Echo and 2D Turbo Spin Echo , 2013, Acta radiologica.

[60]  G. McConnell,et al.  Advances in laser sources for confocal and multiphoton microscopy , 2005, Microscopy research and technique.

[61]  J Silvennoinen,et al.  T2 relaxation reveals spatial collagen architecture in articular cartilage: A comparative quantitative MRI and polarized light microscopic study , 2001, Magnetic resonance in medicine.

[62]  R. Dalziel,et al.  Articular cartilage. , 1971, Lancet.

[63]  Won C Bae,et al.  Ultrashort echo time MR imaging of osteochondral junction of the knee at 3 T: identification of anatomic structures contributing to signal intensity. , 2010, Radiology.

[64]  Chen-Yuan Dong,et al.  The discrimination of type I and type II collagen and the label-free imaging of engineered cartilage tissue. , 2010, Biomaterials.

[65]  Charles E McCulloch,et al.  Patellar cartilage: T2 values and morphologic abnormalities at 3.0-T MR imaging in relation to physical activity in asymptomatic subjects from the osteoarthritis initiative. , 2010, Radiology.

[66]  Gregory Chang,et al.  Rapid isotropic 3D‐sodium MRI of the knee joint in vivo at 7T , 2009, Journal of magnetic resonance imaging : JMRI.

[67]  S Trattnig,et al.  Multimodal approach in the use of clinical scoring, morphological MRI and biochemical T2-mapping and diffusion-weighted imaging in their ability to assess differences between cartilage repair tissue after microfracture therapy and matrix-associated autologous chondrocyte transplantation: a pilot stu , 2009, Osteoarthritis and cartilage.

[68]  J. Urban,et al.  The elastic network of articular cartilage: an immunohistochemical study of elastin fibres and microfibrils , 2010, Journal of anatomy.

[69]  F. C. Linn,et al.  MOVEMENT AND COMPOSITION OF INTERSTITIAL FLUID OF CARTILAGE. , 1965, Arthritis and rheumatism.

[70]  D. Heinegård,et al.  Structure and function of extracellular matrix proteoglycans. , 1990, Biochemical Society transactions.

[71]  S. Majumdar,et al.  T2 relaxation time of cartilage at MR imaging: comparison with severity of knee osteoarthritis. , 2004, Radiology.

[72]  A. Hall,et al.  The volume and morphology of chondrocytes within non-degenerate and degenerate human articular cartilage. , 2003, Osteoarthritis and cartilage.

[73]  M. Shive,et al.  Structural characteristics of the collagen network in human normal, degraded and repair articular cartilages observed in polarized light and scanning electron microscopies. , 2011, Osteoarthritis and cartilage.

[74]  Toshikazu Shirai,et al.  Haematopoietic cell-specific CDM family protein DOCK2 is essential for lymphocyte migration , 2001, Nature.

[75]  N. Adachi,et al.  Clinical significance of magnetic resonance imaging (MRI) for focal chondral lesions. , 1999, Magnetic resonance imaging.