{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T06:08:46Z","timestamp":1791180526484,"version":"4.1.0"},"reference-count":50,"publisher":"The Company of Biologists","issue":"18","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2005,9,15]]},"abstract":"<jats:title>SUMMARY<\/jats:title>\n               <jats:p>Mammalian bone is an active tissue in which osteoblasts and osteoclasts balance bone mass. This process of adaptive modelling and remodelling is probably regulated by strain-sensing osteocytes. Bone of advanced teleosts is acellular yet, despite the lack of osteocytes, it is capable of an adaptive response to physical stimuli. Strenuous exercise is known to induce lordosis. Lordosis is a ventrad curvature of the vertebral column, and the affected vertebrae show an increase in bone formation.<\/jats:p>\n               <jats:p>The effects of lordosis on the strain distribution in sea bass(Dicentrarchus labrax L.) vertebrae are assessed using finite element modelling. The response of the local tissue is analyzed spatially and ontogenetically in terms of bone volume.<\/jats:p>\n               <jats:p>Lordotic vertebrae show a significantly increased strain energy due to the increased load compared with normal vertebrae when loaded in compression. High strain regions are found in the vertebral centrum and parasagittal ridges. The increase in strain energy is attenuated by a change in architecture due to the increased bone formation. The increased bone formation is seen mainly at the articular surfaces of the vertebrae, although some extra bone is formed in the vertebral centrum.<\/jats:p>\n               <jats:p>Regions in which the highest strains are found do not spatially correlate with regions in which the most extensive bone apposition occurs in lordotic vertebrae of sea bass. Mammalian-like strain-regulated bone modelling is probably not the guiding mechanism in adaptive bone modelling of acellular sea bass vertebrae. Chondroidal ossification is found at the articular surfaces where it mediates a rapid adaptive response, potentially attenuating high stresses on the dorsal zygapophyses.<\/jats:p>","DOI":"10.1242\/jeb.01808","type":"journal-article","created":{"date-parts":[[2005,9,9]],"date-time":"2005-09-09T20:32:33Z","timestamp":1126297953000},"page":"3493-3502","source":"Crossref","is-referenced-by-count":85,"title":["Adaptive bone formation in acellular vertebrae of sea bass(<i>Dicentrarchus labrax<\/i> L.)"],"prefix":"10.1242","volume":"208","author":[{"given":"Sander","family":"Kranenbarg","sequence":"first","affiliation":[{"name":"Experimental Zoology Group, Wageningen University, Marijkeweg 40, 6709 PG Wageningen, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tim","family":"van Cleynenbreugel","sequence":"additional","affiliation":[{"name":"Division of Biomechanics and Engineering Design, K.U. Leuven,Celestijnenlaan 200A, 3001 Leuven, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Henk","family":"Schipper","sequence":"additional","affiliation":[{"name":"Experimental Zoology Group, Wageningen University, Marijkeweg 40, 6709 PG Wageningen, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johan","family":"van Leeuwen","sequence":"additional","affiliation":[{"name":"Experimental Zoology Group, Wageningen University, Marijkeweg 40, 6709 PG Wageningen, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"237","reference":[{"key":"2021042510343175500_REF1","doi-asserted-by":"crossref","unstructured":"Backiel, T., Kokurewicz, B. and Ogorzalek, A.(1984). High incidence of skeletal anomalies in carp, Cyprinus carpio, reared in cages in flowing water. Aquaculture43,369-380.","DOI":"10.1016\/0044-8486(84)90245-X"},{"key":"2021042510343175500_REF2","unstructured":"Beer, F. P. and Johnston, E. R. (1992). Mechanics of Materials. 2nd edn. London:McGraw-Hill."},{"key":"2021042510343175500_REF3","unstructured":"Beresford, W. A. (1981). Chondroid Bone, Secondary Cartilage, and Metaplasia. Baltimore: Urban and Schwarzenberg."},{"key":"2021042510343175500_REF4","unstructured":"Bertin, L. (1958). Squelette axial. In Traite\u0301 de Zoologie. Vol.XIII (ed. P.-P. Grasse\u0301), pp.688-709. Paris: Masson et Cie."},{"key":"2021042510343175500_REF5","doi-asserted-by":"crossref","unstructured":"Bird, N. C. and Mabee, P. M. (2003). Developmental morphology of the axial skeleton of the zebrafish, Danio rerio (Ostariophysi: Cyprinidae). Dev. Dyn.228,333-357.","DOI":"10.1002\/dvdy.10387"},{"key":"2021042510343175500_REF6","doi-asserted-by":"crossref","unstructured":"Breit, S. (2002). Functional adaptations of facet geometry in the canine thoracolumbar and lumbar spine (th10-l6). Ann. 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