Depth-wise progression of osteoarthritis in human articular cartilage: investigation of composition, structure and biomechanics.

OBJECTIVE Osteoarthritis (OA) is characterized by the changes in structure and composition of articular cartilage. However, it is not fully known, what is the depth-wise change in two major components of the cartilage solid matrix, i.e., collagen and proteoglycans (PGs), during OA progression. Further, it is unknown how the depth-wise changes affect local tissue strains during compression. Our aim was to address these issues. METHODS Data from the previous microscopic and biochemical measurements of the collagen content, distribution and orientation, PG content and distribution, water content and histological grade of normal and degenerated human patellar articular cartilage (n=73) were reanalyzed in a depth-wise manner. Using this information, a composition-based finite element (FE) model was used to estimate tissue function solely based on its composition and structure. RESULTS The orientation angle of collagen fibrils in the superficial zone of cartilage was significantly less parallel to the surface (P<0.05) in samples with early degeneration than in healthy samples. Similarly, PG content was reduced in the superficial zone in early OA (P<0.05). However, collagen content decreased significantly only at the advanced stage of OA (P<0.05). The composition-based FE model showed that under a constant stress, local tissue strains increased as OA progressed. CONCLUSION For the first time, depth-wise point-by-point statistical comparisons of structure and composition of human articular cartilage were conducted. The present results indicated that early OA is primarily characterized by the changes in collagen orientation and PG content in the superficial zone, while collagen content does not change until OA has progressed to its late stage. Our simulation results suggest that impact loads in OA joint could create a risk for tissue failure and cell death.

[1]  Jukka S Jurvelin,et al.  Practical considerations in the use of polarized light microscopy in the analysis of the collagen network in articular cartilage , 2008, Microscopy research and technique.

[2]  R. Haut,et al.  The extent of matrix damage and chondrocyte death in mechanically traumatized articular cartilage explants depends on rate of loading , 2001, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[3]  R. J. Pawluk,et al.  Osteoarthritic changes in the biochemical composition of thumb carpometacarpal joint cartilage and correlation with biomechanical properties. , 2000, The Journal of hand surgery.

[4]  Robert L Sah,et al.  Boundary lubrication of articular cartilage: role of synovial fluid constituents. , 2007, Arthritis and rheumatism.

[5]  G E Kempson,et al.  The tensile properties of the cartilage of human femoral condyles related to the content of collagen and glycosaminoglycans. , 1973, Biochimica et biophysica acta.

[6]  Won C Bae,et al.  Biomechanics of cartilage articulation: effects of lubrication and degeneration on shear deformation. , 2008, Arthritis and rheumatism.

[7]  M. Worsfold,et al.  Microplate assay for the measurement of hydroxyproline in acid-hydrolyzed tissue samples. , 2001, BioTechniques.

[8]  D. Bertrand,et al.  Multivariate image analysis of a set of FTIR microspectroscopy images of aged bovine muscle tissue combining image and design information , 2007, Analytical and bioanalytical chemistry.

[9]  Alpo Pelttari,et al.  Articular cartilage superficial zone collagen birefringence reduced and cartilage thickness increased before surface fibrillation in experimental osteoarthritis , 1998, Annals of the rheumatic diseases.

[10]  Mirela Ionescu,et al.  The pathobiology of focal lesion development in aging human articular cartilage and molecular matrix changes characteristic of osteoarthritis. , 2003, Arthritis and rheumatism.

[11]  Xiaohong Bi,et al.  Fourier transform infrared imaging spectroscopic analysis of tissue engineered cartilage: histologic and biochemical correlations. , 2005, Journal of biomedical optics.

[12]  R K Korhonen,et al.  Mechanical characterization of articular cartilage by combining magnetic resonance imaging and finite-element analysis—a potential functional imaging technique , 2008, Physics in medicine and biology.

[13]  A. Boskey,et al.  FT-IR imaging of native and tissue-engineered bone and cartilage. , 2007, Biomaterials.

[14]  J. Jurvelin,et al.  Quantitative ultrasound imaging detects degenerative changes in articular cartilage surface and subchondral bone , 2006, Physics in medicine and biology.

[15]  H J Helminen,et al.  Changes in spatial collagen content and collagen network architecture in porcine articular cartilage during growth and maturation. , 2009, Osteoarthritis and cartilage.

[16]  J M Huyghe,et al.  A composition-based cartilage model for the assessment of compositional changes during cartilage damage and adaptation. , 2006, Osteoarthritis and cartilage.

[17]  A Ratcliffe,et al.  Mechanical and biochemical changes in the superficial zone of articular cartilage in canine experimental osteoarthritis , 1994, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[18]  X. Bi,et al.  A novel method for determination of collagen orientation in cartilage by Fourier transform infrared imaging spectroscopy (FT-IRIS). , 2005, Osteoarthritis and cartilage.

[19]  Petro Julkunen,et al.  Stress-relaxation of human patellar articular cartilage in unconfined compression: prediction of mechanical response by tissue composition and structure. , 2008, Journal of biomechanics.

[20]  H J Helminen,et al.  Normal and pathological adaptations of articular cartilage to joint loading , 2000, Scandinavian journal of medicine & science in sports.

[21]  H. J. Mankin,et al.  Instructional Course Lectures, The American Academy of Orthopaedic Surgeons - Articular Cartilage. Part II: Degeneration and Osteoarthrosis, Repair, Regeneration, and Transplantation*† , 1997 .

[22]  S Majumdar,et al.  Fourier Transform Infrared Imaging of focal lesions in human osteoarthritic cartilage. , 2005, European cells & materials.

[23]  R Mendelsohn,et al.  FTIR microscopic imaging of collagen and proteoglycan in bovine cartilage. , 2001, Biopolymers.

[24]  N. Blumenkrantz,et al.  New method for quantitative determination of uronic acids. , 1973, Analytical biochemistry.

[25]  Carol V Ward,et al.  Evaluation of the chondral modeling theory using fe‐simulation and numeric shape optimization , 2009, Journal of anatomy.

[26]  W. Bae,et al.  Indentation probing of human articular cartilage: Effect on chondrocyte viability. , 2007, Osteoarthritis and cartilage.

[27]  Xiaohong Bi,et al.  Fourier transform infrared imaging spectroscopy investigations in the pathogenesis and repair of cartilage. , 2006, Biochimica et biophysica acta.

[28]  H. Muir Cartilage structure and metabolism and basic changes in degenerative joint disease. , 1978, Australian and New Zealand journal of medicine.

[29]  Xiaohong Bi,et al.  Fourier transform infrared imaging and MR microscopy studies detect compositional and structural changes in cartilage in a rabbit model of osteoarthritis , 2007, Analytical and bioanalytical chemistry.

[30]  Juha Töyräs,et al.  Speed of sound in normal and degenerated bovine articular cartilage. , 2003, Ultrasound in medicine & biology.

[31]  J Töyräs,et al.  Indentation diagnostics of cartilage degeneration. , 2008, Osteoarthritis and cartilage.

[32]  V. Mow,et al.  Biphasic creep and stress relaxation of articular cartilage in compression? Theory and experiments. , 1980, Journal of biomechanical engineering.

[33]  M S Laasanen,et al.  Proteoglycan and collagen sensitive MRI evaluation of normal and degenerated articular cartilage , 2004, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[34]  P. Torzilli,et al.  Influence of stress rate on water loss, matrix deformation and chondrocyte viability in impacted articular cartilage. , 2005, Journal of biomechanics.

[35]  Helen Brown,et al.  Applied Mixed Models in Medicine , 2000, Technometrics.

[36]  S. Jimenez,et al.  Osteoarthritis cartilage histopathology: grading and staging. , 2006, Osteoarthritis and cartilage.