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      The consequences of living longer—Effects of an experimentally extended velvet antler phase on the histomorphology of antler bone in fallow deer ( Dama dama)

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          Abstract

          Antlers are periodically regenerated paired cranial appendages of male deer (both sexes in reindeer) that constitute the fastest‐growing bones in the animal kingdom. The annual antler cycle of male deer is linked to testicular activity and largely controlled by seasonal fluctuations of testosterone concentrations in their blood. We studied the effects of an experimental doubling (to eight months) of the velvet antler phase, during which the antlers are covered by skin (velvet), on the histomorphology of antler bone in three adult fallow bucks. Extension of the velvet antler phase in the experimental animals had been caused by administration of the antiandrogen cyproterone acetate (CPA). The distal portions of the antlers from two of the CPA‐treated bucks exhibited partial sequestration of the antler cortex, with the separation plane typically located along the border between cortex and spongiosa. It is hypothesized that this was caused by cortical necrosis due to severe ischemia during later stages of the extended velvet antler phase. In places, new cancellous bone had been deposited on the resorption surface of the spongiosa, indicating a regeneration process. Normal fallow deer antlers (“controls”) from this and a previous study, that is, antlers with a timespan of about four months between onset of new antler growth and velvet shedding, exhibited no or only minor bone remodeling and still contained remnants of calcified cartilage in their distal portions. In contrast, the antlers of the three CPA‐treated bucks showed evidence (secondary osteons and resorption cavities) of marked bone remodeling along their entire length and lacked remnants of calcified cartilage. Our results underscore that the typical histological features of antler bone reflect its short‐lived nature. Antlers are not mechanically loaded during the velvet stage, and it is presently unclear what triggered remodeling activity in the antlers whose lifespan had been experimentally extended.

          Abstract

          Secondary osteons (arrows) and resorption cavities (arrowheads) indicate marked remodeling activity in a fallow deer antler with extended velvet antler phase due to treatment of the buck with the antiandrogen cyproterone acetate. PO: primary osteons. Transverse ground section viewed under circularly polarized light.

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          Histological examination of antler regeneration in red deer (Cervus elaphus).

          Annual antler renewal presents the only case of epimorphic regeneration (de novo formation of a lost appendage distal to the level of amputation) in mammals. Epimorphic regeneration is also referred to as a blastema-based process, as blastema formation at an initial stage is the prerequisite for this type of regeneration. Therefore, antler regeneration has been claimed to take place through initial blastema formation. However, this claim has never been confirmed experimentally. The present study set out to describe systematically the progression of antler regeneration in order to make a direct histological comparison with blastema formation. The results showed that wound healing over a pedicle stump was achieved by ingrowth of full-thickness pedicle skin and resulted in formation of a scar. The growth centers for the antler main beam and brow tine were formed independently at the posterior and anterior corners of the pedicle stump, respectively. The hyperplastic perichondrium surmounting each growth center was directly formed in situ by a single type of tissue: the thickening distal pedicle periosteum, which is the derivative of initial antlerogenic periosteum. Therefore, the cells residing in the pedicle periosteum can be called antler stem cells. Antler stem cells formed each growth center by initially forming bone through intramembranous ossification, then osseocartilage through transitional ossification, and finally cartilage through endochondral ossification. There was an overlap between the establishment of antler growth centers and the completion of wound healing over the pedicle stump. Overall, our results demonstrate that antler regeneration is achieved through general wound healing- and stem cell-based process, rather than through initial blastema formation. Pedicle periosteal cells directly give rise to antlers. Histogenesis of antler regeneration may recapitulate the process of initial antler generation.
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            Antlers - Evolution, development, structure, composition, and biomechanics of an outstanding type of bone

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              Mechanistic aspects of the fracture toughness of elk antler bone.

              Bone is an adaptive material that is designed for different functional requirements; indeed, bones have a variety of properties depending on their role in the body. To understand the mechanical response of bone requires the elucidation of its structure-function relationships. Here, we examine the fracture toughness of compact bone of elk antler, which is an extremely fast-growing primary bone designed for a totally different function than human (secondary) bone. We find that antler in the transverse (breaking) orientation is one of the toughest biological materials known. Its resistance to fracture is achieved during crack growth (extrinsically) by a combination of gross crack deflection/twisting and crack bridging via uncracked "ligaments" in the crack wake, both mechanisms activated by microcracking primarily at lamellar boundaries. We present an assessment of the toughening mechanisms acting in antler as compared to human cortical bone, and identify an enhanced role of inelastic deformation in antler which further contributes to its (intrinsic) toughness. Published by Elsevier Ltd.
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                Author and article information

                Contributors
                uwe.kierdorf@uni-hildesheim.de
                Journal
                J Anat
                J Anat
                10.1111/(ISSN)1469-7580
                JOA
                Journal of Anatomy
                John Wiley and Sons Inc. (Hoboken )
                0021-8782
                1469-7580
                24 June 2021
                November 2021
                24 June 2021
                : 239
                : 5 ( doiID: 10.1111/joa.v239.5 )
                : 1104-1113
                Affiliations
                [ 1 ] Department of Biology University of Hildesheim Hildesheim Germany
                [ 2 ] Department of Anatomy and Embryology University Medical Center Göttingen Germany
                Author notes
                [*] [* ] Correspondence

                Uwe Kierdorf, Department of Biology, University of Hildesheim, Universitätsplatz 1, 31141 Hildesheim, Germany.

                Email: uwe.kierdorf@ 123456uni-hildesheim.de

                Author information
                https://orcid.org/0000-0003-0531-2460
                https://orcid.org/0000-0001-6411-9631
                Article
                JOA13495
                10.1111/joa.13495
                8546508
                34169521
                856beb01-6cf9-40b0-84fe-0a6bca348f06
                © 2021 The Authors. Journal of Anatomy published by John Wiley & Sons Ltd on behalf of Anatomical Society

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                : 30 May 2021
                : 02 April 2021
                : 09 June 2021
                Page count
                Figures: 7, Tables: 1, Pages: 10, Words: 7433
                Categories
                Original Paper
                Original Papers
                Custom metadata
                2.0
                November 2021
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.0.8 mode:remove_FC converted:26.10.2021

                Anatomy & Physiology
                antler cortex,bone remodeling,bone sequestration,cyproterone acetate,ischemic necrosis,primary and secondary osteons

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