A novel method for determination of collagen orientation in cartilage by Fourier transform infrared imaging spectroscopy (FT-IRIS).
- Journal Article
- Research Support
- N.I.H.
- Extramural
Summary
This research presents a novel method for determining the orientation of collagen molecules in cartilage using Fourier transform infrared imaging spectroscopy (FT-IRIS). The method offers a more detailed analysis than traditional polarized light microscopy (PLM) techniques, particularly when analyzing human osteoarthritic cartilage.
Objective
The study aimed to establish a new method for determining the alignment of collagen molecules within histological samples of cartilage. Collagen, a critical structural component in connective tissues, performs much of its function based on its molecular orientation. The research uses a technique based on molecular vibrations, known as polarized Fourier transform infrared imaging spectrophony (FT-IRIS).
Methods
- Polarized FT-IRIS data, acquired from highly oriented tendon collagen, was used for calibrating the experiment’s derived spectral parameters.
- The collagen amide I/II absorbances’ integrated areas’ ratio served as an indicator of collagen orientation.
- This method was then applied to the assessment of collagen molecules’ orientation in equine articular cartilage and equine repair cartilage following microfracture treatment.
- The method was also used for evaluating human osteoarthritic cartilage.
- To generate a comparison, polarized light microscopy (PLM), the commonly used technique for evaluating collagen fibril orientation in histological sections, was performed on picrosirius red-stained sections.
Conclusions
- Calculations based on differences in collagen orientation showed that normal equine cartilage thicknesses in each zone were the same with both PLM and FT-IRIS.
- Similar outcomes using both methods were obtained when analyzing repair and osteoarthritis tissues.
- However, PLM images of human osteoarthritic cartilage showed less clear zonal discrimination compared to the FT-IRIS images. This discrepancy could be due to the FT-IRIS method’s capability to detect molecular orientation changes before they become visible at the microscopic level.
Through this research, the FT-IRIS technique was proven to be a potentially more effective tool for detecting finer variations in collagen orientation, thus enhancing our understanding of tissue integrity and disease progression.
Cite This Article
Publication
Researcher Affiliations
- Research Division, Hospital for Special Surgery, 535 E 70th Street, New York, NY 10021, USA. bix@hss.edu
MeSH Terms
- Animals
- Cartilage, Articular / ultrastructure
- Fibrillar Collagens / ultrastructure
- Hindlimb
- Horses
- Humans
- Knee Joint
- Osteoarthritis / pathology
- Rabbits
- Regeneration
- Spectroscopy, Fourier Transform Infrared
Grant Funding
- R01 EB000744 / NIBIB NIH HHS
- AR46121 / NIAMS NIH HHS
- EB000744 / NIBIB NIH HHS
Citations
This article has been cited 54 times.- Hamandi F, Goswami T. Hierarchical Structure and Properties of the Bone at Nano Level.. Bioengineering (Basel) 2022 Nov 10;9(11).
- Mankar R, Gajjela CC, Bueso-Ramos CE, Yin CC, Mayerich D, Reddy RK. Polarization Sensitive Photothermal Mid-Infrared Spectroscopic Imaging of Human Bone Marrow Tissue.. Appl Spectrosc 2022 Apr;76(4):508-518.
- Kistler M, Ku00f6hler H, Theopold J, Gockel I, Roth A, Hepp P, Osterhoff G. Intraoperative hyperspectral imaging (HSI) as a new diagnostic tool for the detection of cartilage degeneration.. Sci Rep 2022 Jan 12;12(1):608.
- Ding J, Mellergaard M, Zhu Z, Kwan P, Edge D, Ma Z, Hebert L, Alrobaiea S, Iwasaki T, Nielsen MCE, Tredget EE. Fluorescent light energy modulates healing in skin grafted mouse model.. Open Med (Wars) 2021;16(1):1240-1255.
- Tits A, Ruffoni D. Joining soft tissues to bone: Insights from modeling and simulations.. Bone Rep 2021 Jun;14:100742.
- Sanden KW, Bu00f6cker U, Ofstad R, Pedersen ME, Hu00f8st V, Afseth NK, Ru00f8nning SB, Pleshko N. Characterization of Collagen Structure in Normal, Wooden Breast and Spaghetti Meat Chicken Fillets by FTIR Microspectroscopy and Histology.. Foods 2021 Mar 6;10(3).
- Rodrigues JFS, da Silva LCM, Cardoso-Sousa L, Caixeta DC, Lu00fcckemeyer DD, Henrique AS, Pontes JP, da Silva LMG, Macedo JSS, Carvalho Ju00fanior PS, Silva E Silva C, Martins MMRS, Monteiro-Neto V, Grisotto MAG, Fernandes AMR, Ferreira J, Calixto JB, Sabino-Silva R, Fernandes ES. Monitoring of Peripheral Blood Leukocytes and Plasma Samples: A Pilot Study to Examine Treatment Response to Leflunomide in Rheumatoid Arthritis.. Pharmaceuticals (Basel) 2021 Jan 29;14(2).
- Querido W, Kandel S, Pleshko N. Applications of Vibrational Spectroscopy for Analysis of Connective Tissues.. Molecules 2021 Feb 9;26(4).
- Leclech C, Villard C. Cellular and Subcellular Contact Guidance on Microfabricated Substrates.. Front Bioeng Biotechnol 2020;8:551505.
- Bakir G, Girouard BE, Wiens R, Mastel S, Dillon E, Kansiz M, Gough KM. Orientation Matters: Polarization Dependent IR Spectroscopy of Collagen from Intact Tendon Down to the Single Fibril Level.. Molecules 2020 Sep 19;25(18).
- Ebrahimi M, Turunen MJ, Finnilu00e4 MA, Joukainen A, Kru00f6ger H, Saarakkala S, Korhonen RK, Tanska P. Structure-Function Relationships of Healthy and Osteoarthritic Human Tibial Cartilage: Experimental and Numerical Investigation.. Ann Biomed Eng 2020 Dec;48(12):2887-2900.
- Basso PR, Carava' E, Protasoni M, Reguzzoni M, Raspanti M. The synovial surface of the articular cartilage.. Eur J Histochem 2020 Jul 1;64(3).
- Ramakrishnan N, Xia Y. Fourier-transform infrared spectroscopic imaging of articular cartilage and biomaterials: A review.. Trends Appl Spectrosc 2013;10:1-23.
- Karchner JP, Querido W, Kandel S, Pleshko N. Spatial correlation of native and engineered cartilage components at micron resolution.. Ann N Y Acad Sci 2019 Apr;1442(1):104-117.
- Oinas J, Ronkainen AP, Rieppo L, Finnilu00e4 MAJ, Iivarinen JT, van Weeren PR, Helminen HJ, Brama PAJ, Korhonen RK, Saarakkala S. Composition, structure and tensile biomechanical properties of equine articular cartilage during growth and maturation.. Sci Rep 2018 Jul 27;8(1):11357.
- Karchner JP, Yousefi F, Bitman SR, Darvish K, Pleshko N. Non-Destructive Spectroscopic Assessment of High and Low Weight Bearing Articular Cartilage Correlates with Mechanical Properties.. Cartilage 2019 Oct;10(4):480-490.
- Spiesz EM, Thorpe CT, Thurner PJ, Screen HRC. Structure and collagen crimp patterns of functionally distinct equine tendons, revealed by quantitative polarised light microscopy (qPLM).. Acta Biomater 2018 Apr 1;70:281-292.
- Querido W, Falcon JM, Kandel S, Pleshko N. Vibrational spectroscopy and imaging: applications for tissue engineering.. Analyst 2017 Oct 23;142(21):4005-4017.
- Qu D, Subramony SD, Boskey AL, Pleshko N, Doty SB, Lu HH. Compositional mapping of the mature anterior cruciate ligament-to-bone insertion.. J Orthop Res 2017 Nov;35(11):2513-2523.
- Georgiadis M, Guizar-Sicairos M, Gschwend O, Hangartner P, Bunk O, Mu00fcller R, Schneider P. Ultrastructure Organization of Human Trabeculae Assessed by 3D sSAXS and Relation to Bone Microarchitecture.. PLoS One 2016;11(8):e0159838.
- Georgiadis M, Mu00fcller R, Schneider P. Techniques to assess bone ultrastructure organization: orientation and arrangement of mineralized collagen fibrils.. J R Soc Interface 2016 Jun;13(119).
- Mansour JM, Lee Z, Welter JF. Nondestructive Techniques to Evaluate the Characteristics and Development of Engineered Cartilage.. Ann Biomed Eng 2016 Mar;44(3):733-49.
- Liebi M, Georgiadis M, Menzel A, Schneider P, Kohlbrecher J, Bunk O, Guizar-Sicairos M. Nanostructure surveys of macroscopic specimens by small-angle scattering tensor tomography.. Nature 2015 Nov 19;527(7578):349-52.
- O'Brien MP, Penmatsa M, Palukuru U, West P, Yang X, Bostrom MP, Freeman T, Pleshko N. Monitoring the Progression of Spontaneous Articular Cartilage Healing with Infrared Spectroscopy.. Cartilage 2015 Jul;6(3):174-84.
- Ross KA, Williams RM, Schnabel LV, Mohammed HO, Potter HG, Bradica G, Castiglione E, Pownder SL, Satchell PW, Saska RA, Fortier LA. Comparison of Three Methods to Quantify Repair Cartilage Collagen Orientation.. Cartilage 2013 Apr;4(2):111-20.
- Gollwitzer H, Yang X, Spevak L, Lukashova L, Nocon A, Fields K, Pleshko N, Courtland HW, Bostrom MP, Boskey AL. Fourier Transform Infrared Spectroscopic Imaging of Fracture Healing in the Normal Mouse.. J Spectrosc (Hindawi) 2015 Jan 1;2015.
- Matcher SJ. What can biophotonics tell us about the 3D microstructure of articular cartilage?. Quant Imaging Med Surg 2015 Feb;5(1):143-58.
- Silverberg JL, Barrett AR, Das M, Petersen PB, Bonassar LJ, Cohen I. Structure-function relations and rigidity percolation in the shear properties of articular cartilage.. Biophys J 2014 Oct 7;107(7):1721-30.
- Izadifar Z, Chen X, Kulyk W. Strategic design and fabrication of engineered scaffolds for articular cartilage repair.. J Funct Biomater 2012 Nov 14;3(4):799-838.
- Khanarian NT, Boushell MK, Spalazzi JP, Pleshko N, Boskey AL, Lu HH. FTIR-I compositional mapping of the cartilage-to-bone interface as a function of tissue region and age.. J Bone Miner Res 2014 Dec;29(12):2643-52.
- Spalazzi JP, Boskey AL, Pleshko N, Lu HH. Quantitative mapping of matrix content and distribution across the ligament-to-bone insertion.. PLoS One 2013;8(9):e74349.
- Hanifi A, McCarthy H, Roberts S, Pleshko N. Fourier transform infrared imaging and infrared fiber optic probe spectroscopy identify collagen type in connective tissues.. PLoS One 2013;8(5):e64822.
- Hanifi A, McGoverin C, Ou YT, Safadi F, Spencer RG, Pleshko N. Differences in infrared spectroscopic data of connective tissues in transflectance and transmittance modes.. Anal Chim Acta 2013 May 24;779:41-9.
- Julkunen P, Wilson W, Isaksson H, Jurvelin JS, Herzog W, Korhonen RK. A review of the combination of experimental measurements and fibril-reinforced modeling for investigation of articular cartilage and chondrocyte response to loading.. Comput Math Methods Med 2013;2013:326150.
- Lee JH, Xia Y. Quantitative zonal differentiation of articular cartilage by microscopic magnetic resonance imaging, polarized light microscopy, and Fourier-transform infrared imaging.. Microsc Res Tech 2013 Jun;76(6):625-32.
- Hanifi A, Bi X, Yang X, Kavukcuoglu B, Lin PC, DiCarlo E, Spencer RG, Bostrom MP, Pleshko N. Infrared fiber optic probe evaluation of degenerative cartilage correlates to histological grading.. Am J Sports Med 2012 Dec;40(12):2853-61.
- Mu00e4kelu00e4 JT, Huttu MR, Korhonen RK. Structure-function relationships in osteoarthritic human hip joint articular cartilage.. Osteoarthritis Cartilage 2012 Nov;20(11):1268-77.
- Hanifi A, Richardson JB, Kuiper JH, Roberts S, Pleshko N. Clinical outcome of autologous chondrocyte implantation is correlated with infrared spectroscopic imaging-derived parameters.. Osteoarthritis Cartilage 2012 Sep;20(9):988-96.
- Yin J, Xia Y, Lu M. Concentration profiles of collagen and proteoglycan in articular cartilage by Fourier transform infrared imaging and principal component regression.. Spectrochim Acta A Mol Biomol Spectrosc 2012 Mar;88:90-6.
- Kim M, Pugarelli J, Miller TL, Wolfson MR, Dodge GR, Shaffer TH. Brief mechanical ventilation impacts airway cartilage properties in neonatal lambs.. Pediatr Pulmonol 2012 Aug;47(8):763-70.
- Rosenbaum AJ, Wicker JF, Dines JS, Bonasser L, Razzano P, Dines DM, Grande DA. Histologic stages of healing correlate with restoration of tensile strength in a model of experimental tendon repair.. HSS J 2010 Sep;6(2):164-70.
- Shimizu T, Wakitani S, Tanaka Y, Yonetani Y, Shiozaki Y, Shimizu K, Horibe S. Ultrasonic probe is useful for in vivo quantitative assessment of medial femoral condyle articular cartilage.. Knee Surg Sports Traumatol Arthrosc 2011 Nov;19(11):1895-900.
- Cotofana S, Eckstein F, Wirth W, Souza RB, Li X, Wyman B, Hellio-Le Graverand MP, Link T, Majumdar S. In vivo measures of cartilage deformation: patterns in healthy and osteoarthritic female knees using 3T MR imaging.. Eur Radiol 2011 Jun;21(6):1127-35.
- Xia Y, Mittelstaedt D, Ramakrishnan N, Szarko M, Bidthanapally A. Depth-dependent anisotropies of amides and sugar in perpendicular and parallel sections of articular cartilage by Fourier transform infrared imaging.. Microsc Res Tech 2011 Feb;74(2):122-32.
- Yin J, Xia Y. Macromolecular concentrations in bovine nasal cartilage by Fourier transform infrared imaging and principal component regression.. Appl Spectrosc 2010 Nov;64(11):1199-208.
- Zheng N, Yang T, Liang M, Zhang H, Li L, Sunnassee A, Liu L. Characterization of protein in old myocardial infarction by FTIR micro-spectroscopy.. J Huazhong Univ Sci Technolog Med Sci 2010 Aug;30(4):546-50.
- Lopez Franco GE, Blank RD, Akhter MP. Intrinsic material properties of cortical bone.. J Bone Miner Metab 2011 Jan;29(1):31-6.
- Kim M, Foo LF, Uggen C, Lyman S, Ryaby JT, Moynihan DP, Grande DA, Potter HG, Pleshko N. Evaluation of early osteochondral defect repair in a rabbit model utilizing fourier transform-infrared imaging spectroscopy, magnetic resonance imaging, and quantitative T2 mapping.. Tissue Eng Part C Methods 2010 Jun;16(3):355-64.
- Ateshian GA. The role of interstitial fluid pressurization in articular cartilage lubrication.. J Biomech 2009 Jun 19;42(9):1163-76.
- Ramakrishnan N, Xia Y, Bidthanapally A. Fourier-transform infrared anisotropy in cross and parallel sections of tendon and articular cartilage.. J Orthop Surg Res 2008 Oct 6;3:48.
- Xia Y, Alhadlaq H, Ramakrishnan N, Bidthanapally A, Badar F, Lu M. Molecular and morphological adaptations in compressed articular cartilage by polarized light microscopy and Fourier-transform infrared imaging.. J Struct Biol 2008 Oct;164(1):88-95.
- Xia Y, Ramakrishnan N, Bidthanapally A. The depth-dependent anisotropy of articular cartilage by Fourier-transform infrared imaging (FTIRI).. Osteoarthritis Cartilage 2007 Jul;15(7):780-8.
- Boskey A, Pleshko Camacho N. FT-IR imaging of native and tissue-engineered bone and cartilage.. Biomaterials 2007 May;28(15):2465-78.
- Bi X, Yang X, Bostrom MP, Bartusik D, Ramaswamy S, Fishbein KW, Spencer RG, Camacho NP. Fourier transform infrared imaging and MR microscopy studies detect compositional and structural changes in cartilage in a rabbit model of osteoarthritis.. Anal Bioanal Chem 2007 Mar;387(5):1601-12.