Changes in collagen fibril network organization and proteoglycan distribution in equine articular cartilage during maturation and growth.
Abstract: The aim of this study was to record growth-related changes in collagen network organization and proteoglycan distribution in intermittently peak-loaded and continuously lower-level-loaded articular cartilage. Cartilage from the proximal phalangeal bone of the equine metacarpophalangeal joint at birth, at 5, 11 and 18 months, and at 6-10 years of age was collected from two sites. Site 1, at the joint margin, is unloaded at slow gaits but is subjected to high-intensity loading during athletic activity; site 2 is a continuously but less intensively loaded site in the centre of the joint. The degree of collagen parallelism was determined with quantitative polarized light microscopy and the parallelism index for collagen fibrils was computed from the cartilage surface to the osteochondral junction. Concurrent changes in the proteoglycan distribution were quantified with digital densitometry. We found that the parallelism index increased significantly with age (up to 90%). At birth, site 2 exhibited a more organized collagen network than site 1. In adult horses this situation was reversed. The superficial and intermediate zones exhibited the greatest reorganization of collagen. Site 1 had a higher proteoglycan content than site 2 at birth but here too the situation was reversed in adult horses. We conclude that large changes in joint loading during growth and maturation in the period from birth to adulthood profoundly affect the architecture of the collagen network in equine cartilage. In addition, the distribution and content of proteoglycans are modified significantly by altered joint use. Intermittent peak-loading with shear seems to induce higher collagen parallelism and a lower proteoglycan content in cartilage than more constant weight-bearing. Therefore, we hypothesize that the formation of mature articular cartilage with a highly parallel collagen network and relatively low proteoglycan content in the peak-loaded area of a joint is needed to withstand intermittent stress and shear, whereas a constantly weight-bearing joint area benefits from lower collagen parallelism and a higher proteoglycan content.
Publication Date: 2009-08-27 PubMed ID: 19732210PubMed Central: PMC2780575DOI: 10.1111/j.1469-7580.2009.01140.xGoogle 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.
- 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 collagen network (a key component for cartilage strength) and the distribution of proteoglycans (molecules that make up the cartilage) in horse joints change as the animals grow and mature. The research suggests that different types of stress on the joints, whether intermittent high-intensity or constant lower-level load, significantly impact the organization of these components in the cartilage.
Study Overview and Methodology
- The research was conducted to understand the changes in the collagen network and the distribution of proteoglycans in horse articular cartilage during maturation and growth.
- The researchers collected cartilage from the proximal phalangeal bone of horse joints at different ages – newborn, 5 months, 11 months, 18 months, and adult (6-10 years).
- They examined two sites on the bone – Site 1 at the joint margin, experiences high-intensity loading during athletic activity but is unloaded otherwise, and Site 2, at the center of the joint, is continuously subjected to less intense loading.
- They used quantitative polarized light microscopy to determine the degree of collagen parallelism and digital densitometry for quantifying the changes in proteoglycan distribution.
Findings
- The investigation found that the index measuring the parallelism of collagen fibrils significantly increased with the horse’s age, with an increase of up to 90%.
- At birth, Site 2 had a more organized collagen network than Site 1. However, this was reversed in adult horses.
- Most extensive collagen reorganization occurred in the superficial and intermediate zones of the cartilage, these are the areas of the cartilage closest to the surface and middle respectively.
- As for proteoglycan distribution, Site 1 had a higher content at birth, but in adult horses, Site 2 demonstrated a higher content.
Conclusions
- The study concluded that changes in joint loading from birth to adulthood significantly affect the collagen network in horse cartilage. Additionally, altered joint use significantly modulates the distribution and content of proteoglycans.
- Intermittent high-intensity loading (like in Site 1) seems to lead to higher collagen parallelism and lower proteoglycan content than more constant lower-level loading (like in Site 2).
- Therefore, the researchers hypothesize that adult horse joints adapt to the type of loading they experience: intermittent stress-induced areas developing highly parallel collagen networks with low proteoglycan content for strength, and constant weight-bearing areas having lower collagen parallelism but higher proteoglycan content for durability and resilience.
Cite This Article
APA
Hyttinen MM, Holopainen J, van Weeren PR, Firth EC, Helminen HJ, Brama PA.
(2009).
Changes in collagen fibril network organization and proteoglycan distribution in equine articular cartilage during maturation and growth.
J Anat, 215(5), 584-591.
https://doi.org/10.1111/j.1469-7580.2009.01140.x Publication
Researcher Affiliations
- Department of Anatomy, Institute of Biomedicine, University of Kuopio, Kuopio, Finland.
MeSH Terms
- Aging / metabolism
- Animals
- Cartilage, Articular / anatomy & histology
- Cartilage, Articular / growth & development
- Cartilage, Articular / metabolism
- Fibrillar Collagens
- Horses / anatomy & histology
- Horses / growth & development
- Horses / metabolism
- Metacarpophalangeal Joint / anatomy & histology
- Metacarpophalangeal Joint / growth & development
- Metacarpophalangeal Joint / metabolism
- Microscopy, Polarization / methods
- Proteoglycans / metabolism
- Weight-Bearing / physiology
References
This article includes 34 references
- Arokoski JP, Hyttinen MM, Lapveteläinen T, Takács P, Kosztáczky B, Módis L, Kovanen V, Helminen H. 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.. Ann Rheum Dis 1996 Apr;55(4):253-64.
- Aspden RM, Hukins DW. Collagen organization in articular cartilage, determined by X-ray diffraction, and its relationship to tissue function.. Proc R Soc Lond B Biol Sci 1981 Jul 14;212(1188):299-304.
- Bader DL, Kempson GE, Egan J, Gilbey W, Barrett AJ. The effects of selective matrix degradation on the short-term compressive properties of adult human articular cartilage.. Biochim Biophys Acta 1992 Apr 22;1116(2):147-54.
- Benninghoff A. Form und Bau der Gelenkknorpel in ihren Beziehungen zur Funktion. Zweiter teil: Der Aufnau des Gelenkknorpels in seinen Beziehungen zur Funktion.. Z Zelforsch Mikrosk Anat 1925;2:783–862.
- Brama PA, Tekoppele JM, Bank RA, van Weeren PR, Barneveld A. Influence of different exercise levels and age on the biochemical characteristics of immature equine articular cartilage.. Equine Vet J Suppl 1999 Nov;(31):55-61.
- Brama PA, TeKoppele JM, Bank RA, van Weeren PR, Barneveld A. Influence of site and age on biochemical characteristics of the collagen network of equine articular cartilage.. Am J Vet Res 1999 Mar;60(3):341-5.
- Brama PA, 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 Vet J 2000 May;32(3):217-21.
- 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 Vet J 2001 Jan;33(1):26-32.
- Brama PA, TeKoppele JM, Bank RA, Barneveld A, van Weeren PR. Development of biochemical heterogeneity of articular cartilage: influences of age and exercise.. Equine Vet J 2002 May;34(3):265-9.
- Clark JM. Variation of collagen fiber alignment in a joint surface: a scanning electron microscope study of the tibial plateau in dog, rabbit, and man.. J Orthop Res 1991 Mar;9(2):246-57.
- Cohen NP, Foster RJ, Mow VC. Composition and dynamics of articular cartilage: structure, function, and maintaining healthy state.. J Orthop Sports Phys Ther 1998 Oct;28(4):203-15.
- Dunham J, Shackleton DR, Billingham ME, Bitensky L, Chayen J, Muir IH. A reappraisal of the structure of normal canine articular cartilage.. J Anat 1988 Apr;157:89-99.
- Herzog W, Federico S. Considerations on joint and articular cartilage mechanics.. Biomech Model Mechanobiol 2006 Jun;5(2-3):64-81.
- Hwang WS, Li B, Jin LH, Ngo K, Schachar NS, Hughes GN. Collagen fibril structure of normal, aging, and osteoarthritic cartilage.. J Pathol 1992 Aug;167(4):425-33.
- Hyttinen MM, Arokoski JP, Parkkinen JJ, Lammi MJ, Lapveteläinen T, Mauranen K, Király K, Tammi MI, Helminen HJ. Age matters: collagen birefringence of superficial articular cartilage is increased in young guinea-pigs but decreased in older animals after identical physiological type of joint loading.. Osteoarthritis Cartilage 2001 Nov;9(8):694-701.
- Kääb MJ, Gwynn IA, Nötzli HP. Collagen fibre arrangement in the tibial plateau articular cartilage of man and other mammalian species.. J Anat 1998 Jul;193 ( Pt 1)(Pt 1):23-34.
- Király K, Hyttinen MM, Lapveteläinen T, Elo M, Kiviranta I, Dobai J, Módis L, Helminen HJ, Arokoski JP. Specimen preparation and quantification of collagen birefringence in unstained sections of articular cartilage using image analysis and polarizing light microscopy.. Histochem J 1997 Apr;29(4):317-27.
- Király K, Lapveteläinen T, Arokoski J, Törrönen K, Módis L, Kiviranta I, Helminen HJ. Application of selected cationic dyes for the semiquantitative estimation of glycosaminoglycans in histological sections of articular cartilage by microspectrophotometry.. Histochem J 1996 Aug;28(8):577-90.
- Kiviranta I, Jurvelin J, Tammi M, Säämänen AM, Helminen HJ. Microspectrophotometric quantitation of glycosaminoglycans in articular cartilage sections stained with Safranin O.. Histochemistry 1985;82(3):249-55.
- Lammi M, Tammi M. Densitometric assay of nanogram quantities of proteoglycans precipitated on nitrocellulose membrane with Safranin O.. Anal Biochem 1988 Feb 1;168(2):352-7.
- Långsjö TK, Hyttinen M, Pelttari A, Kiraly K, Arokoski J, Helminen HJ. 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.. J Anat 1999 Aug;195 ( Pt 2)(Pt 2):281-93.
- Little CB, Ghosh P. Variation in proteoglycan metabolism by articular chondrocytes in different joint regions is determined by post-natal mechanical loading.. Osteoarthritis Cartilage 1997 Jan;5(1):49-62.
- Maroudas A, Palla G, Gilav E. Racemization of aspartic acid in human articular cartilage.. Connect Tissue Res 1992;28(3):161-9.
- Murray RC, Birch HL, Lakhani K, Goodship AE. Biochemical composition of equine carpal articular cartilage is influenced by short-term exercise in a site-specific manner.. Osteoarthritis Cartilage 2001 Oct;9(7):625-32.
- Nieminen MT, Rieppo J, Töyräs J, Hakumäki JM, Silvennoinen J, Hyttinen MM, Helminen HJ, Jurvelin JS. T2 relaxation reveals spatial collagen architecture in articular cartilage: a comparative quantitative MRI and polarized light microscopic study.. Magn Reson Med 2001 Sep;46(3):487-93.
- Rieppo J, Töyräs J, Nieminen MT, Kovanen V, Hyttinen MM, Korhonen RK, Jurvelin JS, Helminen HJ. Structure-function relationships in enzymatically modified articular cartilage.. Cells Tissues Organs 2003;175(3):121-32.
- Rieppo J, Hallikainen J, Jurvelin JS, Kiviranta I, Helminen HJ, Hyttinen MM. Practical considerations in the use of polarized light microscopy in the analysis of the collagen network in articular cartilage.. Microsc Res Tech 2008 Apr;71(4):279-87.
- Rieppo J, Hyttinen MM, Halmesmaki E, Ruotsalainen H, Vasara A, Kiviranta I, Jurvelin JS, Helminen HJ. Changes in spatial collagen content and collagen network architecture in porcine articular cartilage during growth and maturation.. Osteoarthritis Cartilage 2009 Apr;17(4):448-55.
- Rogers CW, Firth EC, McIlwraith CW, Barneveld A, Goodship AE, Kawcak CE, Smith RK, van Weeren PR. Evaluation of a new strategy to modulate skeletal development in Thoroughbred performance horses by imposing track-based exercise during growth.. Equine Vet J 2008 Mar;40(2):111-8.
- Van Turnhout MC, Haazelager MB, Gijsen MAL. Quantitative description of collagen structure in the articular cartilage of the young and adult equine distal metacarpus. Anim Biol 2008;58:353–370.
- Verzijl N, DeGroot J, Bank RA, Bayliss MT, Bijlsma JW, Lafeber FP, Maroudas A, TeKoppele JM. Age-related accumulation of the advanced glycation endproduct pentosidine in human articular cartilage aggrecan: the use of pentosidine levels as a quantitative measure of protein turnover.. Matrix Biol 2001 Nov;20(7):409-17.
- van Weeren PR, Barneveld A. Study design to evaluate the influence of exercise on the development of the musculoskeletal system of foals up to age 11 months.. Equine Vet J Suppl 1999 Nov;(31):4-8.
- Xia Y, Moody JB, Alhadlaq H, Hu J. Imaging the physical and morphological properties of a multi-zone young articular cartilage at microscopic resolution.. J Magn Reson Imaging 2003 Mar;17(3):365-74.
- Yarker YE, Aspden RM, Hukins DW. Birefringence of articular cartilage and the distribution on collagen fibril orientations.. Connect Tissue Res 1983;11(2-3):207-13.
Citations
This article has been cited 10 times.- Barendregt AM, Mazzoli V, van den Berg JM, Kuijpers TW, Maas M, Nederveen AJ, Hemke R. T(1ρ)-mapping for assessing knee joint cartilage in children with juvenile idiopathic arthritis - feasibility and repeatability.. Pediatr Radiol 2020 Mar;50(3):371-379.
- Zhou X, Ju MJ, Huang L, Tang S. Slope-based segmentation of articular cartilage using polarization-sensitive optical coherence tomography phase retardation image.. J Biomed Opt 2019 Mar;24(3):1-14.
- Oinas J, Ronkainen AP, Rieppo L, Finnilä 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.
- Hellings IR, Dolvik NI, Ekman S, Olstad K. Cartilage canals in the distal intermediate ridge of the tibia of fetuses and foals are surrounded by different types of collagen.. J Anat 2017 Oct;231(4):615-625.
- 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.
- Kulmala KA, Pulkkinen HJ, Rieppo L, Tiitu V, Kiviranta I, Brünott A, Brommer H, van Weeren R, Brama PA, Mikkola MT, Korhonen RK, Jurvelin JS, Töyräs J. Contrast-Enhanced Micro-Computed Tomography in Evaluation of Spontaneous Repair of Equine Cartilage.. Cartilage 2012 Jul;3(3):235-44.
- Wu P, DeLassus E, Patra D, Liao W, Sandell LJ. Effects of serum and compressive loading on the cartilage matrix synthesis and spatiotemporal deposition around chondrocytes in 3D culture.. Tissue Eng Part A 2013 May;19(9-10):1199-208.
- Chen T, Hilton MJ, Brown EB, Zuscik MJ, Awad HA. Engineering superficial zone features in tissue engineered cartilage.. Biotechnol Bioeng 2013 May;110(5):1476-86.
- Balcom NT, Berg-Johansen B, Dills KJ, Van Donk JR, Williams GM, Chen AC, Hazelwood SJ, Sah RL, Klisch SM. In vitro articular cartilage growth with sequential application of IGF-1 and TGF-β1 enhances volumetric growth and maintains compressive properties.. J Biomech Eng 2012 Mar;134(3):031001.
- Julkunen P, Halmesmäki EP, Iivarinen J, Rieppo L, Närhi T, Marjanen J, Rieppo J, Arokoski J, Brama PA, Jurvelin JS, Helminen HJ. Effects of growth and exercise on composition, structural maturation and appearance of osteoarthritis in articular cartilage of hamsters.. J Anat 2010 Sep;217(3):262-74.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists