Abstract: Some epiphyseal growth cartilage canals are surrounded by a ring of hypereosinophilic matrix consisting of collagen type I. Absence of the collagen type I ring may predispose canal vessels to failure and osteochondrosis, which can lead to fragments in joints (osteochondrosis dissecans). It is not known whether the ring develops in response to programming or biomechanical force. The distribution that may reveal the function of the ring has only been described in the distal femur of a limited number of foals. It is also not known which cells are responsible for producing the collagen ring. The aims of the current study were to examine fetuses and foals to infer whether the ring forms in response to biomechanical force or programming, to describe distribution and to investigate which cell type produces the ring. The material consisted of 46 fetuses and foals from 293 days of gestation to 142 days old, of both sexes and different breeds, divided into three groups, designated the naïve group up to and including the day of birth, the adapting group from 2 days up to and including 14 days old, and the loaded group from 15 days and older. The distal tibia was sawn into parasagittal slabs and the cranial half of the central slab from the intermediate ridge was examined by light microscopy and immunohistochemical staining for collagen type I. Presence, completeness and location of the collagen ring was compared, as was the quantity of perivascular mesenchymal cells. An eosinophilic ring present on HE-stained sections was seen in every single fetus and foal examined, which corresponded to collagen type I in immunostained sections. A higher proportion of cartilage canals were surrounded by an eosinophilic ring in the naïve and adapting groups at 73 and 76%, respectively, compared with the loaded group at 51%. When considering only patent canals, the proportion of canals with an eosinophilic ring was higher in the adapting and loaded than the naïve group of foals. The ring was present around 90 and 81% of patent canals in the deep and middle layers, respectively, compared with 58% in the superficial layer, and the ring was more often complete around deep compared with superficial canals. The ring was absent or partial around chondrifying canals. When an eosinophilic ring was present around patent canals, it was more common for the canal to contain one or more layers of perivascular mesenchymal cells rather than few to no layers. It was also more common for the collagen ring to be more complete around canals that contained many as opposed to few mesenchymal cells. In conclusion, the proportion of cartilage canals that had an eosinophilic ring was similar in all three groups of fetuses and foals, indicating that the presence of the collagen ring was mostly programmed, although some adaptation was evident. The ring was more often present around deep, compared with superficial canals, indicating a role in preparation for ossification. The collagen ring appeared to be produced by perivascular mesenchymal cells.
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.
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.
The study investigates the formation and distribution of collagen rings around cartilage canals in the tibia of fetuses and foals and suggests that these rings are mostly formed through genetic programming, but also show signs of adaptation. It also proposes that these rings seem to be produced by perivascular mesenchymal cells.
Objective and Methodology
The main objectives of the study were to examine foal and fetal tibia to determine whether collagen rings around cartilage canals form due to genetic programming or biomechanical force, and to identify which cells produce these rings.
The researchers studied three groups: the naïve group, born or just over birth, the adapting group, aged from to 14 days, and the loaded group, aged 15 days and older. These group classifications aimed to examine the collagen ring at different developmental stages.
The specific part of the tibia under examination was cut into slabs, and the cranial half of the central slab from the intermediate ridge was studied under a light microscope.
The method also utilized immunohistochemical staining, a technique used to identify specific cells, to examine collagen type I, the specific collagen found in the cartilage canals.
Findings
All fetuses and foals examined presented an eosinophilic ring in the cartilage canals, which corresponds with collagen type I. An eosinophilic ring refers to the eosin-positive substance that surrounds the vascular canals of cartilage, visible through particular stainings.
A higher proportion of cartilage canals across the naïve and adapting groups had an eosinophilic ring as compared to the loaded group, suggesting some adaptation in response to biomechanical forces as the foal matures and becomes more active.
This ring was present around 90% and 81% of patent (open) canals in the deep and middle layers but only 58% in the superficial (surface) layer, indicating a role of the ring in preparation for ossification, the process in which cartilage is transformed into bone.
The eosinophilic ring was less apparent or partial around chondrifying canals, canals that are turning into cartilage, demonstrating that the ring’s formation is linked with the canal’s maturity.
The presence of perivascular mesenchymal cells, cells capable of differentiating into a variety of cell types, was more common when an eosinophilic ring was present around patent canals. Moreover, the collagen ring was observed to be more complete surround canals containing larger amounts of mesenchymal cells.
Conclusion
The study concludes that the presence of the collagen ring is mostly genetically programmed, but also shows some adaptation to biomechanics, as revealed by the changes in the presence and completeness of the ring in different age groups.
The analysis also indicated that the collagen rings could be produced by perivascular mesenchymal cells, pointing to a potential cellular contributor behind this growth and maintenance mechanism in cartilage.
Cite This Article
APA
Hellings IR, Dolvik NI, Ekman S, Olstad K.
(2017).
Cartilage canals in the distal intermediate ridge of the tibia of fetuses and foals are surrounded by different types of collagen.
J Anat, 231(4), 615-625.
https://doi.org/10.1111/joa.12650
Faculty of Veterinary Medicine and Biosciences, Department of Companion Animal Clinical Sciences, Equine Section, Norwegian University of Life Sciences, Oslo, Norway.
Dolvik, Nils Ivar
Faculty of Veterinary Medicine and Biosciences, Department of Companion Animal Clinical Sciences, Equine Section, Norwegian University of Life Sciences, Oslo, Norway.
Ekman, Stina
Department of Biomedical Sciences and Veterinary Public Health, Section of Pathology, Swedish University of Agricultural Sciences, Uppsala, Sweden.
Olstad, Kristin
Faculty of Veterinary Medicine and Biosciences, Department of Companion Animal Clinical Sciences, Equine Section, Norwegian University of Life Sciences, Oslo, Norway.
MeSH Terms
Animals
Cartilage / embryology
Cartilage / metabolism
Collagen / metabolism
Female
Horses / embryology
Horses / metabolism
Male
Tibia / embryology
Tibia / metabolism
References
This article includes 47 references
Albro MB, Banerjee RE, Li R, Oungoulian SR, Chen B, del Palomar AP, Hung CT, Ateshian GA. Dynamic loading of immature epiphyseal cartilage pumps nutrients out of vascular canals.. J Biomech 2011 Jun 3;44(9):1654-9.
Blumer MJ, Longato S, Richter E, Pérez MT, Konakci KZ, Fritsch H. The role of cartilage canals in endochondral and perichondral bone formation: are there similarities between these two processes?. J Anat 2005 Apr;206(4):359-72.
Blumer MJ, Schwarzer C, Pérez MT, Konakci KZ, Fritsch H. Identification and location of bone-forming cells within cartilage canals on their course into the secondary ossification centre.. J Anat 2006 Jun;208(6):695-707.
Carlson CS, Hilley HD, Henrikson CK, Meuten DJ. The ultrastructure of osteochondrosis of the articular-epiphyseal cartilage complex in growing swine.. Calcif Tissue Int 1986 Jan;38(1):44-51.
Etterlin PE, Ytrehus B, Lundeheim N, Heldmer E, Österberg J, Ekman S. Effects of free-range and confined housing on joint health in a herd of fattening pigs.. BMC Vet Res 2014 Sep 11;10:208.
Finnøy A, Olstad K, Lilledahl MB. Second harmonic generation imaging reveals a distinct organization of collagen fibrils in locations associated with cartilage growth.. Connect Tissue Res 2016 Sep;57(5):374-87.
Grindflek E, Hamland H, Aasmundstad T (2014) Genome‐wide association study for conformation traits and osteochondrosis in pigs. In 10th World Congress on Genetics Applied to Livestock Production). Vancouver.
Hurtig M, Green SL, Dobson H. Correlative study of defective cartilage and bone growth in foals fed a low‐copper diet. Equine Vet J Suppl 1993;16:66–73.
Komarova SV, Safranek L, Gopalakrishnan J, Ou MJ, McKee MD, Murshed M, Rauch F, Zuhr E. Mathematical model for bone mineralization.. Front Cell Dev Biol 2015;3:51.
Lutfi AM. Study of cell multiplication in the cartilaginous upper end of the tibia of the domestic fowl by tritiated thymidine autoradiography.. Acta Anat (Basel) 1970;76(3):454-63.
Nowlan NC, Sharpe J, Roddy KA, Prendergast PJ, Murphy P. Mechanobiology of embryonic skeletal development: Insights from animal models.. Birth Defects Res C Embryo Today 2010 Sep;90(3):203-13.
Oostendorp C, Uijtdewilligen PJ, Versteeg EM, Hafmans TG, van den Bogaard EH, de Jonge PK, Pirayesh A, Von den Hoff JW, Reichmann E, Daamen WF, van Kuppevelt TH. Visualisation of newly synthesised collagen in vitro and in vivo.. Sci Rep 2016 Jan 7;6:18780.
Reiland S, Ordell N, Lundeheim N, Olsson SE. Heredity of osteochondrosis, body constitution and leg weakness in the pig. A correlative investigation using progeny testing.. Acta Radiol Suppl 1978;358:123-37.
Ross MH, Pawlina W (2012) Histology. A Text and Atlas. With Correlated Cell and Molecular Biology Baltimore. Hagerstown: Lippincott Williams & Wilkins.
Stockwell RA. The ultrastructure of cartilage canals and the surrounding cartilage in the sheep fetus.. J Anat 1971 Sep;109(Pt 3):397-410.
van Turnhout MC, Schipper H, van Lagen B, Zuilhof H, Kranenbarg S, van Leeuwen JL. Postnatal development of depth-dependent collagen density in ovine articular cartilage.. BMC Dev Biol 2010 Oct 22;10:108.
Ytrehus B, Carlson CS, Lundeheim N, Mathisen L, Reinholt FP, Teige J, Ekman S. Vascularisation and osteochondrosis of the epiphyseal growth cartilage of the distal femur in pigs--development with age, growth rate, weight and joint shape.. Bone 2004 Mar;34(3):454-65.
Ytrehus B, Ekman S, Carlson CS, Teige J, Reinholt FP. Focal changes in blood supply during normal epiphyseal growth are central in the pathogenesis of osteochondrosis in pigs.. Bone 2004 Dec;35(6):1294-306.