Comparison of Three Methods to Quantify Repair Cartilage Collagen Orientation

Objective: The aim of this study was to determine if the noninvasive or minimally invasive and nondestructive imaging techniques of quantitative T2-mapping or multiphoton microscopy (MPM) respectively, could detect differences in cartilage collagen orientation similar to polarized light microscopy (PLM). It was hypothesized that MRI, MPM, and PLM would all detect quantitative differences between repair and normal cartilage tissue. Methods: Osteochondral defects in the medial femoral condyle were created and repaired in 5 mature goats. Postmortem, MRI with T2-mapping and histology were performed. T2 maps were generated and a mean T2 value was calculated for each region of interest. Histologic slides were assessed using MPM with measurements of autocorrelation ellipticity, and by PLM with application of a validated scoring method. Collagen orientation using each of the 3 modalities (T2-mapping, MPM, and PLM) was measured in the center of the repair tissue and compared to remote, normal cartilage. Results: MRI, MPM, and PLM were able to detect a significant difference between repair and normal cartilage (n = 5). The average T2 value was longer for repair tissue (41.43 ± 9.81 ms) compared with normal cartilage (27.12 ± 14.22 ms; P = 0.04); MPM autocorrelation ellipticity was higher in fibrous tissue (3.75 ± 1.17) compared with normal cartilage (2.24 ± 0.51; P = 0.01); the average PLM score for repair tissue was lower (1.6 ± 1.02) than the score for remote normal cartilage (4.4 ± 0.42; P = 0.002). The strongest correlation among the methods was between MRI and PLM (r = −0.76; P = 0.01), followed by MPM and PLM (r = −0.58; P = 0.08), with the weakest correlation shown between MRI and MPM (r = 0.35; P = 0.31). Conclusion: All 3 imaging methods quantitatively measured differences in collagen orientation between repair and normal cartilage, but at very different levels of resolution. PLM is destructive to tissue and requires euthanasia, but because MPM can be used arthroscopically, both T2-mapping and MPM can be performed in vivo, offering nondestructive means to assess collagen orientation that could be used to obtain longitudinal data in cartilage repair studies.

[1]  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.

[2]  Ali Guermazi,et al.  Why radiography should no longer be considered a surrogate outcome measure for longitudinal assessment of cartilage in knee osteoarthritis , 2011, Arthritis research & therapy.

[3]  Ina Pavlova,et al.  Compact and flexible raster scanning multiphoton endoscope capable of imaging unstained tissue , 2011, Proceedings of the National Academy of Sciences.

[4]  S. Zhuo,et al.  A pilot study of using multiphoton microscopy to diagnose gastric cancer , 2011, Surgical Endoscopy.

[5]  M. Hyttinen,et al.  Quantitative Analysis of Collagen Network Structure and Fibril Dimensions in Cartilage Repair with Autologous Chondrocyte Transplantation , 2010, Cells Tissues Organs.

[6]  W. Zipfel,et al.  Strategies for high-resolution imaging of epithelial ovarian cancer by laparoscopic nonlinear microscopy. , 2010, Translational oncology.

[7]  R. Kandel,et al.  A New Histology Scoring System for the Assessment of the Quality of Human Cartilage Repair: ICRS II , 2010, The American journal of sports medicine.

[8]  C. H. Coyle,et al.  Optical coherence tomography grading correlates with MRI T2 mapping and extracellular matrix content , 2010, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[9]  J. Stoltz,et al.  Collagenous Extracellular Matrix of Cartilage Submitted to Mechanical Forces Studied by Second Harmonic Generation Microscopy , 2010, Photochemistry and photobiology.

[10]  M J Lammi,et al.  Biomechanical, biochemical and structural correlations in immature and mature rabbit articular cartilage. , 2009, Osteoarthritis and cartilage.

[11]  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.

[12]  M. Hyttinen,et al.  Changes in collagen fibril network organization and proteoglycan distribution in equine articular cartilage during maturation and growth , 2009, Journal of anatomy.

[13]  H. Potter,et al.  Noncontrast MR techniques and imaging of cartilage. , 2009, Radiologic clinics of North America.

[14]  A Shirazi-Adl,et al.  Role of cartilage collagen fibrils networks in knee joint biomechanics under compression. , 2008, Journal of biomechanics.

[15]  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.

[16]  M S Laasanen,et al.  Estimation of mechanical properties of articular cartilage with MRI - dGEMRIC, T2 and T1 imaging in different species with variable stages of maturation. , 2007, Osteoarthritis and cartilage.

[17]  W. Zipfel,et al.  Solute transport in growth plate cartilage: in vitro and in vivo. , 2007, Biophysical journal.

[18]  S Majumdar,et al.  Quantitative magnetic resonance imaging of articular cartilage in osteoarthritis. , 2007, European cells & materials.

[19]  Itai Cohen,et al.  Mapping the depth dependence of shear properties in articular cartilage. , 2007, Journal of biomechanics.

[20]  A Jay Khanna,et al.  Magnetic resonance imaging of cartilage in the athlete: current techniques and spectrum of disease. , 2006, The Journal of bone and joint surgery. American volume.

[21]  M. Gardner,et al.  Unsuspected lymphoma diagnosed with use of biopsy during kyphoplasty. , 2006, The Journal of bone and joint surgery. American volume.

[22]  George Tomlinson,et al.  Cartilage T2 assessment: differentiation of normal hyaline cartilage and reparative tissue after arthroscopic cartilage repair in equine subjects. , 2006, Radiology.

[23]  H. Potter,et al.  Meniscal Allograft Transplantation in the Sheep Knee , 2006, The American journal of sports medicine.

[24]  Rebecca M. Williams,et al.  Quasistatic and dynamic nanomechanical properties of cancellous bone tissue relate to collagen content and organization , 2006 .

[25]  Jeffrey D. Gordon,et al.  Comparison of Fresh Osteochondral Autografts and Allografts: a Canine Model on Behalf Of: American Orthopaedic Society for Sports Medicine Comparison of Fresh Osteochondral Autografts and Allografts a Canine Model , 2006 .

[26]  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.

[27]  E. Cocker,et al.  In vivo brain imaging using a portable 3.9 gram two-photon fluorescence microendoscope. , 2005, Optics letters.

[28]  I ap Gwynn,et al.  The ultrastructure of mouse articular cartilage: collagen orientation and implications for tissue functionality. A polarised light and scanning electron microscope study and review. , 2005, European cells & materials.

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

[30]  Watt W Webb,et al.  Interpreting second-harmonic generation images of collagen I fibrils. , 2005, Biophysical journal.

[31]  J R Matyas,et al.  Detecting structural changes in early experimental osteoarthritis of tibial cartilage by microscopic magnetic resonance imaging and polarised light microscopy , 2004, Annals of the rheumatic diseases.

[32]  P. Choyke,et al.  Imaging of angiogenesis: from microscope to clinic , 2003, Nature Medicine.

[33]  W. Webb,et al.  Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[34]  P. Bullough,et al.  Histological Assessment of Cartilage Repair: A Report by the Histology Endpoint Committee of the International Cartilage Repair Society (ICRS) , 2003, The Journal of bone and joint surgery. American volume.

[35]  H. Potter,et al.  T2 quantitation of articular cartilage at 1.5 T , 2003, Journal of magnetic resonance imaging : JMRI.

[36]  Peter Friedl,et al.  Compensation mechanism in tumor cell migration , 2003, The Journal of cell biology.

[37]  Sally Roberts,et al.  Autologous chondrocyte implantation for cartilage repair: monitoring its success by magnetic resonance imaging and histology , 2002, Arthritis research & therapy.

[38]  W. Webb,et al.  Multiphoton microscopy in biological research. , 2001, Current opinion in chemical biology.

[39]  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.

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

[41]  Yang Xia Heterogeneity of cartilage laminae in MR imaging , 2000 .

[42]  R M Henkelman,et al.  Image resolution and signal-to-noise ratio requirements for MR imaging of degenerative cartilage. , 1997, AJR. American journal of roentgenology.

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

[44]  E B Hunziker,et al.  Ultrastructure of adult human articular cartilage matrix after cryotechnical processing , 1997, Microscopy research and technique.

[45]  T Lapveteläinen,et al.  Decreased birefringence of the superficial zone collagen network in the canine knee (stifle) articular cartilage after long distance running training, detected by quantitative polarised light microscopy. , 1996, Annals of the rheumatic diseases.

[46]  F. Silver,et al.  Cartilage wound healing. An overview. , 1995, Otolaryngologic clinics of North America.

[47]  G W Blunn,et al.  Three-dimensional collagen architecture in bovine articular cartilage. , 1991, The Journal of bone and joint surgery. British volume.

[48]  L. Módis Organization of the Extracellular Matrix: A Polarization Microscopic Approach , 1990 .

[49]  L. Dahners,et al.  The collagenous architecture of articular cartilage. Correlation of scanning electron microscopy and polarized light microscopy observations. , 1979, Clinical orthopaedics and related research.

[50]  R. Brentani,et al.  Differential staining of collagens type I, II and III by Sirius Red and polarization microscopy. , 1978, Archivum histologicum Japonicum = Nihon soshikigaku kiroku.

[51]  A. J. Helfet,et al.  An ultrastructural study of normal young adult human articular cartilage. , 1968, The Journal of bone and joint surgery. American volume.

[52]  M. Shive,et al.  A polarized light microscopy method for accurate and reliable grading of collagen organization in cartilage repair. , 2011, Osteoarthritis and cartilage.

[53]  T. Schaer,et al.  Single site osteochondral resurfacing – an in vivo caprine study , 2009 .

[54]  F H Silver,et al.  Relationship among biomechanical, biochemical, and cellular changes associated with osteoarthritis. , 2001, Critical reviews in biomedical engineering.

[55]  P. Carmeliet,et al.  In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy , 2001, Nature Medicine.