Modeling optical behavior of birefringent biological tissues for evaluation of quantitative polarized light microscopy.

Quantitative polarized light microscopy (qPLM) is a popular tool for the investigation of birefringent architectures in biological tissues. Collagen, the most abundant protein in mammals, is such a birefringent material. Interpretation of results of qPLM in terms of collagen network architecture and anisotropy is challenging, because different collagen networks may yield equal qPLM results. We created a model and used the linear optical behavior of collagen to construct a Jones or Mueller matrix for a histological cartilage section in an optical qPLM train. Histological sections of tendon were used to validate the basic assumption of the model. Results show that information on collagen densities is needed for the interpretation of qPLM results in terms of collagen anisotropy. A parameter that is independent of the optical system and that measures collagen fiber anisotropy is introduced, and its physical interpretation is discussed. With our results, we can quantify which part of different qPLM results is due to differences in collagen densities and which part is due to changes in the collagen network. Because collagen fiber orientation and anisotropy are important for tissue function, these results can improve the biological and medical relevance of qPLM results.

[1]  R. Oldenbourg,et al.  New polarized light microscope with precision universal compensator , 1995, Journal of microscopy.

[2]  N. Akkas Biomechanics of Active Movement and Deformation of Cells , 1990, NATO ASI Series.

[3]  H. Kasprzak,et al.  Linear birefringence measurements of the in vitro human cornea , 2003, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[4]  Richard H. Newton,et al.  Quantitative image analysis of birefringent biological material , 1997 .

[5]  S. Tsukahara,et al.  Effect of Uncompensated Corneal Polarization on the Detection of Localized Retinal Nerve Fiber Layer Defects , 2008, Ophthalmic Research.

[6]  Y. Xia,et al.  The depth-dependent anisotropy of articular cartilage by Fourier-transform infrared imaging (FTIRI). , 2007, Osteoarthritis and cartilage.

[7]  M. Koehl,et al.  The mechanics of notochord elongation, straightening and stiffening in the embryo of Xenopus laevis. , 1990, Development.

[8]  M. Koehl,et al.  Mechanical Development of the Notochord in Xenopus Early Tail-Bud Embryos , 1990 .

[9]  Sharmila Majumdar,et al.  Long-term cyclical in vivo loading increases cartilage proteoglycan content in a spatially specific manner: an infrared microspectroscopic imaging and polarized light microscopy study , 2006, Arthritis research & therapy.

[10]  Johan L van Leeuwen,et al.  Evidence for an elastic projection mechanism in the chameleon tongue. , 2004, Proceedings. Biological sciences.

[11]  H. Tinneberg,et al.  High magnitude of light retardation by the zona pellucida is associated with conception cycles. , 2005, Human reproduction.

[12]  C. Dohlman,et al.  CORNEA AND SCLERA. , 1963, Archives of ophthalmology.

[13]  J. Arokoski,et al.  Electron microscopic stereological study of collagen fibrils in bovine articular cartilage: volume and surface densities are best obtained indirectly (from length densities and diameters) using isotropic uniform random sampling , 1999, Journal of anatomy.

[14]  E. M. Slayter Optical methods in biology , 1970 .

[15]  Michael Shribak,et al.  Techniques for fast and sensitive measurements of two-dimensional birefringence distributions. , 2003, Applied optics.

[16]  Johan L. van Leeuwen,et al.  Why the chameleon has spiral-shaped muscle fibres in its tongue , 1997 .

[17]  Juha Töyräs,et al.  Collagen network primarily controls Poisson's ratio of bovine articular cartilage in compression , 2006, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[18]  T. Wilson,et al.  Quantitative polarized light microscopy , 2003, Journal of microscopy.

[19]  R. Oldenbourg Analysis of microtubule dynamics by polarized light. , 2007, Methods in molecular medicine.

[20]  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.

[21]  E D Salmon,et al.  Birefringence of single and bundled microtubules. , 1998, Biophysical journal.

[22]  R. Simon The connection between Mueller and Jones matrices of polarization optics , 1982 .

[23]  V. Lunin,et al.  IR Laser and Heat‐induced Changes in Annulus Fibrosus Collagen Structure , 2007, Photochemistry and photobiology.

[24]  C. Boote,et al.  Spatial mapping of collagen fibril organisation in primate cornea-an X-ray diffraction investigation. , 2004, Journal of Structural Biology.

[25]  A. Benninghoff,et al.  Form und Bau der Gelenkknorpel in ihren Beziehungen zur Funktion , 2004, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[26]  R. Oldenbourg,et al.  Strctural analysis with quantitative birefringence imaging , 1999 .

[27]  E. Salmon,et al.  Quantifying single and bundled microtubules with the polarized light microscope. , 1995, The Biological bulletin.

[28]  D. Kelly Turtle and mammal penis designs are anatomically convergent , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[29]  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.

[30]  A. Maroudas,et al.  Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage. I. Chemical composition. , 1977, Annals of the rheumatic diseases.

[31]  R. Knighton,et al.  Microtubules contribute to the birefringence of the retinal nerve fiber layer. , 2005, Investigative ophthalmology & visual science.

[32]  J. Walsh,et al.  Quantitative measurements of linear birefringence during heating of native collagen , 1997, Lasers in surgery and medicine.

[33]  R. Jones A New Calculus for the Treatment of Optical SystemsI. Description and Discussion of the Calculus , 1941 .

[34]  Zhanfeng Cui,et al.  Microfibrils, elastin fibres and collagen fibres in the human intervertebral disc and bovine tail disc , 2007, Journal of anatomy.

[35]  R. Shadwick,et al.  The mechanical properties of fin whale arteries are explained by novel connective tissue designs. , 1996, The Journal of experimental biology.

[36]  L. Picken,et al.  Orientation of Fibrils in Natural Membranes , 1947, Nature.

[37]  John M. Clark,et al.  Variation of collagen fiber alignment in a joint surface: A scanning electron microscope study of the tibial plateau in dog, rabbit, and man , 1991, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[38]  Yang Xia,et al.  Imaging the physical and morphological properties of a multi‐zone young articular cartilage at microscopic resolution , 2003, Journal of magnetic resonance imaging : JMRI.

[39]  E. Collett Field Guide to Polarization , 2005 .

[40]  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.

[41]  S Inoué,et al.  Muscle fine structure and microtubule birefringence measured with a new pol-scope. , 1994, The Biological bulletin.

[42]  W. Hutton,et al.  Effect of Tail Suspension (or Simulated Weightlessness) on the Lumbar Intervertebral Disc: Study of Proteoglycans and Collagen , 2002, Spine.

[43]  R. Jones A New Calculus for the Treatment of Optical Systems. IV. , 1942 .

[44]  H. Helminen,et al.  Collagenase-Induced Changes in Articular Cartilage as Detected by Electron-Microscopic Stereology, Quantitative Polarized Light Microscopy and Biochemical Assays , 2002, Cells Tissues Organs.

[45]  Frank P T Baaijens,et al.  The role of collagen cross-links in biomechanical behavior of human aortic heart valve leaflets--relevance for tissue engineering. , 2007, Tissue engineering.

[46]  D. Keefe,et al.  Noninvasive polarized light microscopy quantitatively distinguishes the multilaminar structure of the zona pellucida of living human eggs and embryos. , 2004, Fertility and sterility.

[47]  J. Arokoski,et al.  Specimen preparation and quantification of collagen birefringence in unstained sections of articular cartilage using image analysis and polarizing light microscopy , 1997, The Histochemical Journal.

[48]  J. Bueno,et al.  Spatially resolved polarization properties for in vitro corneas , 2001, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

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

[50]  P. Canham,et al.  Fluorescence spectroscopy and birefringence of molecular changes in maturing rat tail tendon. , 2007, Journal of biomedical optics.

[51]  A. Maroudas,et al.  Chemical composition and swelling of normal and osteoarthrotic femoral head cartilage , 1977 .

[52]  Petro Julkunen,et al.  Characterization of articular cartilage by combining microscopic analysis with a fibril-reinforced finite-element model. , 2007, Journal of biomechanics.

[53]  K. Fackler,et al.  Polarizing light microscopy of intestine and its relationship to mechanical behaviour , 1981, Journal of microscopy.

[54]  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.

[55]  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.

[56]  Theodore T. Tower,et al.  Fiber Alignment Imaging During Mechanical Testing of Soft Tissues , 2002, Annals of Biomedical Engineering.

[57]  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.

[58]  R. Appleyard,et al.  Topographical analysis of the structural, biochemical and dynamic biomechanical properties of cartilage in an ovine model of osteoarthritis. , 2003, Osteoarthritis and cartilage.

[59]  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.

[60]  Vuk Milisic,et al.  Analysis of the fiber architecture of the heart by quantitative polarized light microscopy. Accuracy, limitations and contribution to the study of the fiber architecture of the ventricles during fetal and neonatal life. , 2007, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[61]  R. Knighton,et al.  Linear birefringence of the central human cornea. , 2002, Investigative ophthalmology & visual science.

[62]  R. Teshima,et al.  Structure of the most superficial layer of articular cartilage. , 1995, The Journal of bone and joint surgery. British volume.

[63]  Peter Fratzl,et al.  Collagen : structure and mechanics , 2008 .

[64]  D.A. Kelly Axial orthogonal fiber reinforcement in the penis of the Nine‐banded Armadillo (Dasypus novemcinctus) , 1997, Journal of morphology.

[65]  R. B. Clark,et al.  Factors Controlling the Change of Shape of Certain Nemertean and Turbellarian Worms , 1958 .

[66]  D. Keefe,et al.  Increased Birefringence in the Meiotic Spindle Provides a New Marker for the Onset of Activation in Living Oocytes1 , 2000, Biology of reproduction.