FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Scientific reports2018; 8(1); 11357; doi: 10.1038/s41598-018-29655-5

Composition, structure and tensile biomechanical properties of equine articular cartilage during growth and maturation.

Abstract: Articular cartilage undergoes structural and biochemical changes during maturation, but the knowledge on how these changes relate to articular cartilage function at different stages of maturation is lacking. Equine articular cartilage samples of four different maturation levels (newborn, 5-month-old, 11-month-old and adult) were collected (N = 25). Biomechanical tensile testing, Fourier transform infrared microspectroscopy (FTIR-MS) and polarized light microscopy were used to study the tensile, biochemical and structural properties of articular cartilage, respectively. The tensile modulus was highest and the breaking energy lowest in the newborn group. The collagen and the proteoglycan contents increased with age. The collagen orientation developed with age into an arcade-like orientation. The collagen content, proteoglycan content, and collagen orientation were important predictors of the tensile modulus (p < 0.05 in multivariable regression) and correlated significantly also with the breaking energy (p < 0.05 in multivariable regression). Partial least squares regression analysis of FTIR-MS data provided accurate predictions for the tensile modulus (r = 0.79) and the breaking energy (r = 0.65). To conclude, the composition and structure of equine articular cartilage undergoes changes with depth that alter functional properties during maturation, with the typical properties of mature tissue reached at the age of 5-11 months.
Get Full Text
Publication Date: 2018-07-27 PubMed ID: 30054498PubMed Central: PMC6063957DOI: 10.1038/s41598-018-29655-5Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This study investigates how the composition and structure of equine (horse) articular cartilage changes as it matures. The research determined that as the cartilage ages, the contents of collagen and proteoglycans increase and the orientation of collagen develops into an arcade-like structure, all of which influence its functional properties.

Study Design and Methods

The study collected equine articular cartilage samples from four different developmental stages – newborn, 5-month-old, 11-month-old, and adult. They used various analysis methods to study different properties of the cartilage.

  • Biomechanical tensile testing: This measures the tensile strength or resistance to breaking under tension of the articular cartilage.
  • Fourier transform infrared microspectroscopy (FTIR-MS): This technique identifies and quantifies the biochemical components of the cartilage, specifically the collagen and proteoglycan content.
  • Polarized light microscopy: Used to examine the structure of the cartilage, particularly the orientation of the collagen fibres.

Findings

The results showed changes in the tensile modulus – the resistance to elasticity, the collagen and proteoglycan contents, and the collagen orientation as cartilage matured.

  • The tensile modulus was found to be highest, and the breaking energy lowest, in the newborn group. This indicates that the cartilage is most resistant to stretching but least resistant to breakage at this stage.
  • As the cartilage aged, the collagen and proteoglycan contents increased. Both are essential components of cartilage that contribute to its strength and resilience.
  • The orientation of collagen fibres developed into an arcade-like arrangement with age. Collagen provides tensile strength to the cartilage, and its orientation can affect how force is distributed through the tissue.

Conclusions

The research concluded that the key functional properties of mature equine articular cartilage are reached by the age of 5-11 months. The collagen content, proteoglycan content, and collagen orientation were significant determinants of the tensile modulus and correlated with the breaking energy. Understanding these changes will likely provide insights towards the growth and maturation of the equine joint, and could potentially be indicative of similar processes in other mammals, including humans.

Cite This Article

APA
Oinas J, Ronkainen AP, Rieppo L, Finnilä MAJ, Iivarinen JT, van Weeren PR, Helminen HJ, Brama PAJ, Korhonen RK, Saarakkala S. (2018). Composition, structure and tensile biomechanical properties of equine articular cartilage during growth and maturation. Sci Rep, 8(1), 11357. https://doi.org/10.1038/s41598-018-29655-5

Publication

Scientific reports
ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 8
Issue: 1
Pages: 11357

Researcher Affiliations

Oinas, J
  • Research Unit of Medical Imaging, Physics and Technology, Faculty of Medicine, University of Oulu, Oulu, Finland.
  • Medical Research Center, University of Oulu and Oulu University Hospital, Oulu, Finland.
Ronkainen, A P
  • Department of Applied Physics, University of Eastern Finland, Kuopio, Finland. ari.p.ronkainen@uef.fi.
Rieppo, L
  • Research Unit of Medical Imaging, Physics and Technology, Faculty of Medicine, University of Oulu, Oulu, Finland.
  • Medical Research Center, University of Oulu and Oulu University Hospital, Oulu, Finland.
  • Department of Applied Physics, University of Eastern Finland, Kuopio, Finland.
Finnilä, M A J
  • Research Unit of Medical Imaging, Physics and Technology, Faculty of Medicine, University of Oulu, Oulu, Finland.
  • Medical Research Center, University of Oulu and Oulu University Hospital, Oulu, Finland.
  • Department of Applied Physics, University of Eastern Finland, Kuopio, Finland.
Iivarinen, J T
  • Department of Applied Physics, University of Eastern Finland, Kuopio, Finland.
  • Institute of Biomedicine, University of Eastern Finland, Kuopio, Finland.
van Weeren, P R
  • Department of Equine Sciences, University of Utrecht, Utrecht, Netherlands.
Helminen, H J
  • Institute of Biomedicine, University of Eastern Finland, Kuopio, Finland.
Brama, P A J
  • Veterinary Clinical Sciences, School of Veterinary Medicine, University College Dublin, Dublin, Ireland.
Korhonen, R K
  • Department of Applied Physics, University of Eastern Finland, Kuopio, Finland.
Saarakkala, S
  • Research Unit of Medical Imaging, Physics and Technology, Faculty of Medicine, University of Oulu, Oulu, Finland.
  • Medical Research Center, University of Oulu and Oulu University Hospital, Oulu, Finland.
  • Department of Diagnostic Radiology, Oulu University Hospital, Oulu, Finland.

MeSH Terms

  • Animals
  • Biomechanical Phenomena
  • Cartilage, Articular / anatomy & histology
  • Cartilage, Articular / growth & development
  • Collagen / metabolism
  • Horses / physiology
  • Least-Squares Analysis
  • Multivariate Analysis
  • Proteoglycans / metabolism
  • Regression Analysis
  • Tensile Strength / physiology

Grant Funding

  • 336267 / European Research Council

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 73 references
  1. Aigner T, Sachse A, Gebhard PM, Roach HI. Osteoarthritis: Pathobiology-targets and ways for therapeutic intervention.. Advanced Drug Delivery Reviews 2006;58:128–149.
    doi: 10.1016/j.addr.2006.01.020pubmed: 16616393google scholar: lookup
  2. Huber M, Trattnig S, Lintner F. Anatomy, Biochemistry, and Physiology of Articular Cartilage.. Investigative Radiology 2000;35:573–580.
    doi: 10.1097/00004424-200010000-00003pubmed: 11041151google scholar: lookup
  3. Sophia Fox AJ, Bedi A, Rodeo SA. The basic science of articular cartilage: structure, composition, and function.. Sports health 2009;1:461–468.
    doi: 10.1177/1941738109350438pmc: PMC3445147pubmed: 23015907google scholar: lookup
  4. Bi X, Yang X, Bostrom MPG, Camacho NP. Fourier transform infrared imaging spectroscopy investigations in the pathogenesis and repair of cartilage.. Biochimica et Biophysica Acta - Biomembranes 2006;1758:934–941.
    doi: 10.1016/j.bbamem.2006.05.014pubmed: 16815242google scholar: lookup
  5. Bayliss MT, Venn M, Maroudas A, Ali SY. Structure of proteoglycans from different layers of human articular cartilage.. The Biochemical journal 1983;209:387–400.
    doi: 10.1042/bj2090387pmc: PMC1154105pubmed: 6405736google scholar: lookup
  6. Maroudas, A. In Adult Articular Cartilage (ed. Freeman, M. A. R.) 215–290 (J. B. Lippincott & Co., 1979).
  7. Weightman B, Chappell DJ, Jenkins EA. A second study of tensile fatigue properties of human articular cartilage.. Annals of the rheumatic diseases 1978;37:58–63.
    doi: 10.1136/ard.37.1.58pmc: PMC1000190pubmed: 629605google scholar: lookup
  8. Charlebois M, McKee MD, Buschmann MD. Nonlinear Tensile Properties of Bovine Articular Cartilage and Their Variation With Age and Depth.. Journal of Biomechanical Engineering 2004;126:129.
    doi: 10.1115/1.1688771pubmed: 15179842google scholar: lookup
  9. Mow VC, Ratcliffe A, Poole AR. Cartilage and diarthrodial joints as paradigms for hierarchical materials and structures.. Biomaterials 1992;13:67–97.
    doi: 10.1016/0142-9612(92)90001-5pubmed: 1550898google scholar: lookup
  10. van Turnhout MC. Postnatal development of collagen structure in ovine articular cartilage.. BMC Developmental Biology 2010;10:62.
    doi: 10.1186/1471-213X-10-62pmc: PMC2906441pubmed: 20529268google scholar: lookup
  11. Akizuki S. Tensile properties of human knee joint cartilage: I. Influence of ionic conditions, weight bearing, and fibrillation on the tensile modulus.. Journal of Orthopaedic Research 1986;4:379–392.
    doi: 10.1002/jor.1100040401pubmed: 3783297google scholar: lookup
  12. Kiviranta P. Collagen network primarily controls poisson’s ratio of bovine articular cartilage in compression.. Journal of Orthopaedic Research 2006;24:690–699.
    doi: 10.1002/jor.20107pubmed: 16514661google scholar: lookup
  13. Hyttinen MM. Changes in collagen fibril network organization and proteoglycan distribution in equine articular cartilage during maturation and growth.. Journal of Anatomy 2009;215:584–591.
    doi: 10.1111/j.1469-7580.2009.01140.xpmc: PMC2780575pubmed: 19732210google scholar: lookup
  14. van Turnhout M. Quantitative description of collagen structure in the articular cartilage of the young and adult equine distal metacarpus.. Animal Biology 2008;58:353–370.
    doi: 10.1163/157075608X383674google scholar: lookup
  15. Benninghoff A. Form und Bau der Gelenkknorpel in ihren Beziehungen zur Funktion.. Zeitschrift für Zellforschung und Mikroskopische Anatomie 1925;2:783–862.
    doi: 10.1007/BF00583443google scholar: lookup
  16. Rieppo J. Changes in spatial collagen content and collagen network architecture in porcine articular cartilage during growth and maturation.. Osteoarthritis and Cartilage 2009;17:448–455.
    doi: 10.1016/j.joca.2008.09.004pubmed: 18849174google scholar: lookup
  17. Moger CJ. Regional variations of collagen orientation in normal and diseased articular cartilage and subchondral bone determined using small angle X-ray scattering (SAXS). Osteoarthritis and Cartilage 2007;15:682–687.
    doi: 10.1016/j.joca.2006.12.006pubmed: 17306566google scholar: lookup
  18. Mansfield JC, Winlove CP, Moger J, Matcher SJ. Collagen fiber arrangement in normal and diseased cartilage studied by polarization sensitive nonlinear microscopy.. Journal of Biomedical Optics 2008;13:44020.
    doi: 10.1117/1.2950318pubmed: 19021348google scholar: lookup
  19. Mahmoodian R. Changes in mechanics and composition of human talar cartilage anlagen during fetal development.. Osteoarthritis and Cartilage 2011;19:1199–1209.
    doi: 10.1016/j.joca.2011.07.013pmc: PMC3217246pubmed: 21843650google scholar: lookup
  20. Brommer H. Functional adaptation of articular cartilage from birth to maturity under the influence of loading: a biomechanical analysis.. Equine Veterinary Journal 2005;37:148–154.
    doi: 10.2746/0425164054223769pubmed: 15779628google scholar: lookup
  21. Heinemeier KM. Radiocarbon dating reveals minimal collagen turnover in both healthy and osteoarthritic human cartilage.. Science translational medicine 2016;8:346ra90.
    doi: 10.1126/scitranslmed.aad8335pubmed: 27384346google scholar: lookup
  22. Potter K, Kidder LH, Levin IW, Lewis EN, Spencer RG. Imaging of collagen and proteoglycan in cartilage sections using Fourier transform infrared spectral imaging.. Arthritis and rheumatism 2001;44:846–855.
    doi: 10.1002/1529-0131(200104)44:4<846::AID-ANR141>3.0.CO;2-Epubmed: 11315924google scholar: lookup
  23. Boskey A, Camacho N. FT-IR imaging of native and tissue-engineered bone and cartilage.. Biomaterials 2007;28:2465–2478.
    doi: 10.1016/j.biomaterials.2006.11.043pmc: PMC1892909pubmed: 17175021google scholar: lookup
  24. Camacho NP, West P, Torzilli PA, Mendelsohn R. FTIR microscopic imaging of collagen and proteoglycan in bovine cartilage.. Biopolymers 2001;62:1–8.
    doi: 10.1002/1097-0282(2001)62:1<1::AID-BIP10>3.0.CO;2-Opubmed: 11135186google scholar: lookup
  25. Baker MJ, Trevisan J, Bassan P, Bhargava R, Butler HJ. Using Fourier transform IR spectroscopy to analyze biological materials.. Nat Protoc 2015;9:1771–1791.
    doi: 10.1038/nprot.2014.110pmc: PMC4480339pubmed: 24992094google scholar: lookup
  26. Rieppo L, Saarakkala S, Jurvelin JS, Rieppo J. Prediction of compressive stiffness of articular cartilage using Fourier transform infrared spectroscopy.. Journal of Biomechanics 2013;46:1269–1275.
    doi: 10.1016/j.jbiomech.2013.02.022pubmed: 23538002google scholar: lookup
  27. Rieppo L, Rieppo J, Jurvelin JS, Saarakkala S. Fourier transform infrared spectroscopic imaging and multivariate regression for prediction of proteoglycan content of articular cartilage.. Plos One 2012;7:e32344.
    doi: 10.1371/journal.pone.0032344pmc: PMC3281137pubmed: 22359683google scholar: lookup
  28. Williamson AK, Chen AC, Masuda K, Thonar EJMA, Sah RL. Tensile mechanical properties of bovine articular cartilage: Variations with growth and relationships to collagen network components.. Journal of Orthopaedic Research 2003;21:872–880.
    doi: 10.1016/S0736-0266(03)00030-5pubmed: 12919876google scholar: lookup
  29. Brama PA, Karssenberg D, Barneveld A, van Weeren PR. Contact areas and pressure distribution on the proximal articular surface of the proximal phalanx under sagittal plane loading.. Equine veterinary journal 2001;33:26–32.
    doi: 10.2746/042516401776767377pubmed: 11191606google scholar: lookup
  30. Brama PA. Topographical mapping of biochemical properties of articular cartilage in the equine fetlock joint.. Equine veterinary journal 2000;32:19–26.
    doi: 10.2746/042516400777612062pubmed: 10661380google scholar: lookup
  31. Wilson W, van Donkelaar CC, van Rietbergen B, Ito K, Huiskes R. Stresses in the local collagen network of articular cartilage: a poroviscoelastic fibril-reinforced finite element study.. Journal of Biomechanics 2004;37:357–366.
    doi: 10.1016/S0021-9290(03)00267-7pubmed: 14757455google scholar: lookup
  32. LeRoux MA. Simultaneous changes in the mechanical properties, quantitative collagen organization, and proteoglycan concentration of articular cartilage following canine meniscectomy.. Journal of orthopaedic research: official publication of the Orthopaedic Research Society 2000;18:383–92.
    doi: 10.1002/jor.1100180309pubmed: 10937624google scholar: lookup
  33. Brama PAJ, Tekoppele JM, Bank RA, Barneveld A, van Weeren PR. Functional adaptation of equine articular cartilage: the formation of regional biochemical characteristics up to age one year.. Equine veterinary journal 2000;32:217–221.
    doi: 10.2746/042516400776563626pubmed: 10836476google scholar: lookup
  34. Asanbaeva A. Articular cartilage tensile integrity: Modulation by matrix depletion is maturation-dependent.. Archives of Biochemistry and Biophysics 2008;474:175–182.
    doi: 10.1016/j.abb.2008.03.012pmc: PMC2440786pubmed: 18394422google scholar: lookup
  35. Khanarian NT. FTIR-I compositional mapping of the cartilage-to-bone interface as a function of tissue region and age.. Journal of Bone and Mineral Research 2014;29:2643–2652.
    doi: 10.1002/jbmr.2284pmc: PMC4963234pubmed: 24839262google scholar: lookup
  36. Klein TJ, Chaudhry M, Bae WC, Sah RL. Depth-dependent biomechanical and biochemical properties of fetal, newborn, and tissue-engineered articular cartilage.. Journal of Biomechanics 2007;40:182–190.
    doi: 10.1016/j.jbiomech.2005.11.002pubmed: 16387310google scholar: lookup
  37. Julkunen P. Biomechanical, biochemical and structural correlations in immature and mature rabbit articular cartilage.. Osteoarthritis and Cartilage 2009;17:1628–1638.
    doi: 10.1016/j.joca.2009.07.002pubmed: 19615962google scholar: lookup
  38. Williamson AK. Compressive properties and function - composition relationships of developing bovine articular cartilage.. Journal of Orthopaedic Research 2001;19:1113–1121.
    doi: 10.1016/S0736-0266(01)00052-3pubmed: 11781013google scholar: lookup
  39. Khan IM. In vitro growth factor-induced bio engineering of mature articular cartilage.. Biomaterials 2013;34:1478–1487.
    doi: 10.1016/j.biomaterials.2012.09.076pmc: PMC3543901pubmed: 23182922google scholar: lookup
  40. Mansfield JC, Bell JS, Winlove CP. The micromechanics of the superficial zone of articular cartilage.. Osteoarthritis and Cartilage 2015;23:1806–1816.
    doi: 10.1016/j.joca.2015.05.030pubmed: 26050867google scholar: lookup
  41. Bell JS, Christmas J, Mansfield JC, Everson RM, Winlove CP. Micromechanical response of articular cartilage to tensile load measured using nonlinear microscopy.. Acta Biomaterialia 2014;10:2574–2581.
    doi: 10.1016/j.actbio.2014.02.008pubmed: 24525036google scholar: lookup
  42. Jurvelin JS, Buschmann MD, Hunziker EB. Optical and mechanical determination of Poisson’s ratio of adult bovine humeral articular cartilage.. Journal of Biomechanics 1997;30:235–241.
    doi: 10.1016/S0021-9290(96)00133-9pubmed: 9119822google scholar: lookup
  43. Gorissen BMC, Wolschrijn CF, van Vilsteren AAM, van Rietbergen B, van Weeren PR. Trabecular bone of precocials at birth; Are they prepared to run for the wolf(f)?. Journal of morphology 2016;277:948–956.
    doi: 10.1002/jmor.20548pmc: PMC5111789pubmed: 27098190google scholar: lookup
  44. Schmidt MB, Mow VC, Chun LE, Eyre DR. Effects of proteoglycan extraction on the tensile behavior of articular cartilage.. Journal of Orthopaedic Research 1990;8:353–363.
    doi: 10.1002/jor.1100080307pubmed: 2324854google scholar: lookup
  45. Kempson GE, Muir H, Pollard C, Tuke M. The tensile properties of the cartilage of human femoral condyles related to the content of collagen and glycosaminoglycans.. BBA - General Subjects 1973;297:456–472.
    doi: 10.1016/0304-4165(73)90093-7pubmed: 4267503google scholar: lookup
  46. Nickien M, Thambyah A, Broom ND. How a decreased fibrillar interconnectivity influences stiffness and swelling properties during early cartilage degeneration.. Journal of the Mechanical Behavior of Biomedical Materials 2017;75:390–398.
    doi: 10.1016/j.jmbbm.2017.07.042pubmed: 28803113google scholar: lookup
  47. Brama PAJ, TeKoppele JM, Bank RA, Barneveld A, van Weeren PR. Development of biochemical heterogeneity of articular cartilage: influences of age and exercise.. Equine veterinary journal 2002;34:265–269.
    doi: 10.2746/042516402776186146pubmed: 12108744google scholar: lookup
  48. Korhonen RK, Jurvelin JS. Compressive and tensile properties of articular cartilage in axial loading are modulated differently by osmotic environment.. Medical Engineering and Physics 2010;32:155–160.
    doi: 10.1016/j.medengphy.2009.11.004pubmed: 19955010google scholar: lookup
  49. Maroudas AI. Balance between swelling pressure and collagen tension in normal and degenerate cartilage.. Nature 1976;260:808–809.
    doi: 10.1038/260808a0pubmed: 1264261google scholar: lookup
  50. Grodzinsky AJ, Roth V, Myers E, Grossman WD, Mow VC. The Significance of Electromechanical and Osmotic Forces in the Nonequilibrium Swelling Behavior of Articular Cartilage in Tension.. Journal of Biomechanical Engineering 1981;103:221.
    doi: 10.1115/1.3138284pubmed: 7311487google scholar: lookup
  51. Elliott DM, Guilak F, Vail TP, Wang JY, Setton LA. Tensile properties of articular cartilage are altered by meniscectomy in a canine model of osteoarthritis.. Journal of Orthopaedic Research 1999;17:503–508.
    doi: 10.1002/jor.1100170407pubmed: 10459755google scholar: lookup
  52. Asanbaeva A, Masuda K, Thonar EJMA, Klisch SM, Sah RL. Mechanisms of cartilage growth: Modulation of balance between proteoglycan and collagen in vitro using chondroitinase ABC.. Arthritis and Rheumatism 2007;56:188–198.
    doi: 10.1002/art.22298pubmed: 17195221google scholar: lookup
  53. Natoli RM, Revell CM, Athanasiou KA. Chondroitinase ABC Treatment Results in Greater Tensile Properties of Self-Assembled Tissue-Engineered Articular Cartilage.. Tissue Engineering Part A 2009;15:3119–3128.
    doi: 10.1089/ten.tea.2008.0478pmc: PMC2792048pubmed: 19344291google scholar: lookup
  54. Rieppo L. Application of second derivative spectroscopy for increasing molecular specificity of fourier transform infrared spectroscopic imaging of articular cartilage.. Osteoarthritis and Cartilage 2012;20:451–459.
    doi: 10.1016/j.joca.2012.01.010pubmed: 22321720google scholar: lookup
  55. Rieppo L, Töyräs J, Saarakkala S. Vibrational spectroscopy of articular cartilage.. Applied Spectroscopy Reviews 2017;52:249–266.
    doi: 10.1080/05704928.2016.1226182google scholar: lookup
  56. Bi X, Li G, Doty SB, Camacho NP. A novel method for determination of collagen orientation in cartilage by Fourier transform infrared imaging spectroscopy (FT-IRIS). Osteoarthritis and Cartilage 2005;13:1050–1058.
    doi: 10.1016/j.joca.2005.07.008pubmed: 16154778google scholar: lookup
  57. Jackson M, Choo LP, Watson PH, Halliday WC, Mantsch HH. Beware of connective tissue proteins: Assignment and implications of collagen absorptions in infrared spectra of human tissues.. BBA - Molecular Basis of Disease 1995;1270:1–6.
    doi: 10.1016/0925-4439(94)00056-Vpubmed: 7827129google scholar: lookup
  58. Mader KT. Investigation of intervertebral disc degeneration using multivariate FTIR spectroscopic imaging.. Faraday Discuss 2016;187:393–414.
    doi: 10.1039/C5FD00160Apmc: PMC5047047pubmed: 27057647google scholar: lookup
  59. Muir H, Bullough P, Maroudas A. The distribution of collagen in human articular cartilage with some of its physiological implications.. The Journal of bone and joint surgery 1970;52:554–563.
    doi: 10.1302/0301-620X.52B3.554pubmed: 4247851google scholar: lookup
  60. 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 and Cartilage 2012;20:988–996.
    doi: 10.1016/j.joca.2012.05.007pmc: PMC3426917pubmed: 22659601google scholar: lookup
  61. van Grevenhof EM. Genetic variables of various manifestations of osteochondrosis and their correlations between and within joints in Dutch warmblood horses.. Journal of animal science 2009;87:1906–1912.
    doi: 10.2527/jas.2008-1199pubmed: 19213707google scholar: lookup
  62. Szarko M, Muldrew K, Bertram JE. Freeze-thaw treatment effects on the dynamic mechanical properties of articular cartilage.. BMC Musculoskeletal Disorders 2010;11:231.
    doi: 10.1186/1471-2474-11-231pmc: PMC2958988pubmed: 20932309google scholar: lookup
  63. Changoor A, Fereydoonzad L, Yaroshinsky A, Buschmann MD. Effects of Refrigeration and Freezing on the Electromechanical and Biomechanical Properties of Articular Cartilage.. Journal of Biomechanical Engineering 2010;132:64502.
    doi: 10.1115/1.4000991pubmed: 20887036google scholar: lookup
  64. Laouar L. Cryopreservation of porcine articular cartilage: MRI and biochemical results after different freezing protocols.. Cryobiology 2007;54:36–43.
    doi: 10.1016/j.cryobiol.2006.10.193pubmed: 17174945google scholar: lookup
  65. Zheng S. Damages to the extracellular matrix in articular cartilage due to cryopreservation by microscopic magnetic resonance imaging and biochemistry.. Magnetic Resonance Imaging 2009;27:648–655.
    doi: 10.1016/j.mri.2008.10.003pmc: PMC2742905pubmed: 19106023google scholar: lookup
  66. McLeod MA, Wilusz RE, Guilak F. Depth-dependent anisotropy of the micromechanical properties of the extracellular and pericellular matrices of articular cartilage evaluated via atomic force microscopy.. Journal of Biomechanics 2013;46:586–592.
    doi: 10.1016/j.jbiomech.2012.09.003pmc: PMC3549024pubmed: 23062866google scholar: lookup
  67. Danso EK, Honkanen JTJ, Saarakkala S, Korhonen RK. Comparison of nonlinear mechanical properties of bovine articular cartilage and meniscus.. Journal of Biomechanics 2014;47:200–206.
    doi: 10.1016/j.jbiomech.2013.09.015pubmed: 24182695google scholar: lookup
  68. Kempson GE. Relationship between the tensile properties of articular cartilage from the human knee and age.. Annals of the rheumatic diseases 1982;41:508–511.
    doi: 10.1136/ard.41.5.508pmc: PMC1001032pubmed: 7125720google scholar: lookup
  69. Li LP, Herzog W, Korhonen RK, Jurvelin JS. The role of viscoelasticity of collagen fibers in articular cartilage: Axial tension versus compression.. Medical Engineering and Physics 2005;27:51–57.
    doi: 10.1016/j.medengphy.2004.08.009pubmed: 15604004google scholar: lookup
  70. Brama P, Tekoppele J, Bank R, van Weeren P, Barneveld A. Influence of different exercise levels and age on the biochemical characteristics of immature equine articular cartilage.. Equine veterinary journal. Supplement 1999;31:55–61.
    doi: 10.1111/j.2042-3306.1999.tb05314.xpubmed: 10999661google scholar: lookup
  71. Rieppo J. Practical considerations in the use of polarized light microscopy in the analysis of the collagen network in articular cartilage.. Microscopy research and technique 2008;71:279–287.
    doi: 10.1002/jemt.20551pubmed: 18072283google scholar: lookup
  72. Mittelstaedt D, Xia Y, Shmelyov A, Casciani N, Bidthanapally A. Quantitative Determination of Morphological and Territorial Structures of Articular Cartilage from Both Perpendicular and Parallel Sections by Polarized Light Microscopy.. Connective Tissue Research 2011;52:512–522.
    doi: 10.3109/03008207.2011.595521pmc: PMC3674864pubmed: 21787136google scholar: lookup
  73. Li H, Liang Y, Xu Q, Cao D. Key wavelengths screening using competitive adaptive reweighted sampling method for multivariate calibration.. Analytica Chimica Acta 2009;648:77–84.
    doi: 10.1016/j.aca.2009.06.046pubmed: 19616692google scholar: lookup

Citations

This article has been cited 14 times.
  1. Park S, Lim J, Lee J, Jeon S, Kim J, Park J. Acute responses and recovery in the femoral cartilage morphology following running and cool-down protocols. PeerJ 2024;12:e18302.
    doi: 10.7717/peerj.18302pubmed: 39465148google scholar: lookup
  2. Conte R, Finicelli M, Borrone A, Margarucci S, Peluso G, Calarco A, Bosetti M. MMP-2 Silencing through siRNA Loaded Positively-Charged Nanoparticles (AcPEI-NPs) Counteracts Chondrocyte De-Differentiation. Polymers (Basel) 2023 Feb 25;15(5).
    doi: 10.3390/polym15051172pubmed: 36904410google scholar: lookup
  3. Salinas EY, Otarola GA, Kwon H, Wang D, Hu JC, Athanasiou KA. Topographical Characterization of the Young, Healthy Human Femoral Medial Condyle. Cartilage 2023 Sep;14(3):338-350.
    doi: 10.1177/19476035221141421pubmed: 36537020google scholar: lookup
  4. Otarola GA, Hu JC, Athanasiou KA. Ion modulatory treatments toward functional self-assembled neocartilage. Acta Biomater 2022 Nov;153:85-96.
    doi: 10.1016/j.actbio.2022.09.022pubmed: 36113725google scholar: lookup
  5. Wyse Jackson T, Michel J, Lwin P, Fortier LA, Das M, Bonassar LJ, Cohen I. Structural origins of cartilage shear mechanics. Sci Adv 2022 Feb 11;8(6):eabk2805.
    doi: 10.1126/sciadv.abk2805pubmed: 35148179google scholar: lookup
  6. Hafezi M, Nouri Khorasani S, Zare M, Esmaeely Neisiany R, Davoodi P. Advanced Hydrogels for Cartilage Tissue Engineering: Recent Progress and Future Directions. Polymers (Basel) 2021 Nov 30;13(23).
    doi: 10.3390/polym13234199pubmed: 34883702google scholar: lookup
  7. Otarola GA, Hu JC, Athanasiou KA. Intracellular Calcium and Sodium Modulation of Self-Assembled Neocartilage Using Costal Chondrocytes. Tissue Eng Part A 2022 Jul;28(13-14):595-605.
    doi: 10.1089/ten.TEA.2021.0169pubmed: 34877888google scholar: lookup
  8. Boos MA, Grinstaff MW, Lamandé SR, Stok KS. Contrast-Enhanced Micro-Computed Tomography for 3D Visualization and Quantification of Glycosaminoglycans in Different Cartilage Types. Cartilage 2021 Dec;13(2_suppl):486S-494S.
    doi: 10.1177/19476035211053820pubmed: 34696603google scholar: lookup
  9. Świetlicka I, Muszyński S, Prein C, Clausen-Schaumann H, Aszodi A, Arciszewski MB, Blicharski T, Gagoś M, Świetlicki M, Dobrowolski P, Kras K, Tomaszewska E, Arczewska M. Fourier Transform Infrared Microspectroscopy Combined with Principal Component Analysis and Artificial Neural Networks for the Study of the Effect of β-Hydroxy-β-Methylbutyrate (HMB) Supplementation on Articular Cartilage. Int J Mol Sci 2021 Aug 25;22(17).
    doi: 10.3390/ijms22179189pubmed: 34502096google scholar: lookup
  10. Mantripragada VP, Gao W, Piuzzi NS, Hoemann CD, Muschler GF, Midura RJ. Comparative Assessment of Primary Osteoarthritis Progression Using Conventional Histopathology, Polarized Light Microscopy, and Immunohistochemistry. Cartilage 2021 Dec;13(1_suppl):1494S-1510S.
    doi: 10.1177/1947603520938455pubmed: 32659115google scholar: lookup
  11. Fugazzola MC, van Weeren PR. Surgical osteochondral defect repair in the horse-a matter of form or function?. Equine Vet J 2020 Jul;52(4):489-499.
    doi: 10.1111/evj.13231pubmed: 31958175google scholar: lookup
  12. Sarin JK, Torniainen J, Prakash M, Rieppo L, Afara IO, Töyräs J. Dataset on equine cartilage near infrared spectra, composition, and functional properties. Sci Data 2019 Aug 30;6(1):164.
    doi: 10.1038/s41597-019-0170-ypubmed: 31471536google scholar: lookup
  13. Ravanfar M, Yao G. Simultaneous tractography and elastography imaging of the zone-specific structural and mechanical responses in articular cartilage under compressive loading. Biomed Opt Express 2019 Jul 1;10(7):3241-3256.
    doi: 10.1364/BOE.10.003241pubmed: 31467777google scholar: lookup
  14. Inamdar SR, Barbieri E, Terrill NJ, Knight MM, Gupta HS. Proteoglycan degradation mimics static compression by altering the natural gradients in fibrillar organisation in cartilage. Acta Biomater 2019 Oct 1;97:437-450.
    doi: 10.1016/j.actbio.2019.07.055pubmed: 31374336google scholar: lookup
Subscribe to our newsletter
Join 99,658 horse owners like you who receive our email updates on horse health and nutrition.