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Architecture and Mineralization of Developing Cortical and Trabecular Bone of the Mandible

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Architecture and Mineralization of Developing Cortical and Trabecular Bone of the Mandible Anat Embryol (2006) 211: 71–78 DOI 10.1007/s00429-005-0054-0 ORIGINAL ARTICLE Lars Mulder Æ Jan Harm Koolstra Henrie¨tte W. de Jonge Æ Theo M.G.J. van Eijden Architecture and mineralization of developing cortical and trabecular bone of the mandible Accepted: 20 September 2005 / Published online: 17 November 2005 Ó Springer-Verlag 2005 Abstract Ossification of the presumptive trabecular bone Keywords Bone histomorphometry Æ Degree of in the mandibular condyle and the presumptive cortical mineralization Æ Quantitative microCT Æ bone in the mandibular corpus of the pig mandible was Mandible Æ Development investigated during development, using micro-computed tomography (microCT). Three-dimensional architecture and mineralization characteristics were assessed from Introduction ten pigs of different developmental ages. In the condyle, increases in trabecular thickness and separation and a The ossification of bone during prenatal development decrease in the trabecular number, led to an unchanged comprises two different mechanisms. Chondral ossifica- bone volume fraction. A conversion from rod-like into tion is a process in which an initial mesenchymal con- plate-like trabeculae was observed. Bone volume and densation converts into bone through an embryonic trabecular thickness were always higher in the corpus, cartilage intermediate. During desmal ossification the where an increase in bone volume fraction was caused by mesenchyme is directly transformed into bone. Both an increase in the trabecular thickness and a decrease in processes are present in the developing mandible; ossi- separation. A transition from a plate-like structure into fication of the condyle and symphyseal region of the a more compact structure took place. The average de- mandible takes place through both endochondral ossi- gree of mineralization in the condyle and the corpus fication and ossification originating from the perichon- increased with age. In the corpus, the degrees of min- drium, while desmal ossification is responsible for the eralization were higher than in the condyle. The differ- development of the corpus. Regardless of its origin, all ences between the condyle and corpus and the changes bone develops from an initial open structure into either a with age could be explained by differences in the distri- dense (compact) cortical bone structure or a trabecular bution of mineralization within the trabecular elements. bone structure (Leeson and Leeson 1970; Cadet et al. Generally, the degrees of mineralization increased from 2003). It is presumed that the regulation mechanisms of the surface toward the centers of the trabecular ele- trabecular and cortical bone development are similar ments, indicating growth of the trabecular elements by (Tanck et al. 2004). the surface apposition of new mineral. The mandible is among the first bones in the body to ossify during fetal development (Hodges 1953), thus providing the opportunity to study the development of the bone at early fetal stages. The gross development of bony regions of the mandible during fetal life has been L. Mulder (&) Æ J. H. Koolstra Æ T. M.G.J. van Eijden subject to investigation (Goret-Nicaise and Dhem 1984; Department of Functional Anatomy, Lee et al. 2001; Radlanski et al. 2003). These studies, Academic Centre for Dentistry Amsterdam (ACTA), however, have described mostly qualitative observations Universiteit van Amsterdam and Vrije Universiteit, and did not treat the quantitative description of the Meibergdreef 15, 1105 AZ, Amsterdam, The Netherlands E-mail: [email protected] developing bone structure in terms of architecture and Tel.: +31-20-5665357 mineralization. Moreover, they have not differentiated Fax: +31-20-6911856 between the cortical and trabecular bone structure. Therefore, the resemblance of their developmental H. W. de Jonge Division of Veterinary Anatomy and Physiology, pathways remains unknown and is, thus, the object of Department Pathobiology, School of Veterinary Medicine, the present study. Knowledge of the development of University of Utrecht, Utrecht, The Netherlands these early bone structures, and their similarities and 72 differences, augments the basic understanding of both using a microCT system (lCT 40, Scanco Medical AG, normal cortical and trabecular bone formation. Bassersdorf, Switzerland). The hemimandibles were Recently, micro-computed tomography (microCT) mounted in cylindrical specimen holders (Polyetheri- has been established as an accurate and powerful tool mide, 20 mm outer diameter, wall thickness, 1.5 mm) for determining three-dimensional architectural param- and secured with synthetic foam. The mandibular spec- eters of young and adult trabecular bone in a non- imens were completely submerged in 70% ethanol. The destructive manner (Ru¨egsegger et al. 1996;Mu¨ller et al. scans yielded an isotropic spatial resolution of 10 lm. A 1998). It has been proven applicable to investigate 45 kV peak voltage X-ray beam was used, which corre- changes in trabecular architecture during postnatal sponds to an effective energy of approximately 24 keV. development and aging (Ding 2000; Nafei et al. 2000; The microCT system was equipped with an aluminum Tanck et al. 2001). Furthermore, it has been recently filter and a correction algorithm, which reduced the beam demonstrated that commercial microCT systems are hardening artifacts sufficiently to enable quantitative capable of not only describing the architectural, but also measurements of the degree and distribution of miner- the physical properties of bone, such as the degree and alization of developing bone (Mulder et al. 2004). The distribution of mineralization, right down to the level of computed linear attenuation coefficient of the X-ray individual trabeculae (Mulder et al. 2004, 2005). beam in each volume element (voxel) was stored in an Therefore, in the present study, microCT was used to attenuation map and represented by a gray value in a analyze mandibles from ten pig specimens of different three-dimensional reconstruction. This attenuation developmental ages. It was applied to investigate the coefficient can be considered to be proportional to the concurrent architectural and mineralization properties local degree of mineralization (Nuzzo et al. 2002). of developing trabecular (condyle) and cortical bone (corpus). Architecture Materials and methods The architecture and degree of mineralization of the bone specimens were determined in volumes of interest Materials that were built up out of 10·10·10 lm3 voxels and segmented using an adaptive threshold, which was The mandibles from ten pigs (standard Dutch com- visually checked. In a segmented reconstruction, every mercial hybrid race) of different developmental ages voxel with a linear attenuation value below the threshold were used in this study. Included were eight fetuses with (assumingly representing soft tissue or background) was an estimated age of 40–45, 45–50, 50–55, 55–60, 65–70, made transparent and voxels above this threshold (rep- 70–75, 82–87, and 95–100 days of gestation, obtained resenting bone) were made opaque. from sows in a commercial slaughterhouse. The fetal age The volumes of interest were chosen at six different was estimated from the mean weight of the litter, using locations in the mandibular corpus; three regions, from growth curves (Evans and Sack 1973). Furthermore, one anterior to posterior on the buccal side, and three more newborn (112–115 days postconception) and one on the lingual side. They were chosen in regions of 2 weeks old (130 days postconception) piglet, obtained presumptive cortical bone. In the condyle, four volumes from the experimental farm of the Faculty of Veterinary of interest were chosen that were located anteroinferi- Medicine in Utrecht, The Netherlands, were used. They orly, anterosuperiorly, posteroinferiorly, and poster- were euthanized by an intravenous overdose of ketamine osuperiorly. The data from the selected regions of the (Narcetan) after premedication. The specimens were corpus and condyle were averaged to obtain values obtained from other experiments that were approved by representative for the entire corpus and condyle. the Committee for Animal Experimentation of the To quantify changes in the architecture of the bone Faculty of Veterinary Medicine, Utrecht, The Nether- during development, several bone architectural param- lands. They were stored at À20°C prior to assessment. eters (BV/TV: bone volume fraction, Tb.N: trabecular The mandibles were harvested by dissection and cut number, Tb.Th: trabecular thickness, Tb.Sp: trabecular in half at the symphyseal region. No attempt was made separation, Conn.D: connectivity density, SMI: struc- at removing all the soft tissue. The older specimens were ture model index, DA: degree of anisotropy) were cal- divided into smaller sections in order to be able to culated (Software Revision 3.2, Scanco Medical AG). analyze all specimens with the same resolution, which was limited by the diameter of the microCT specimen holders. Degree and distribution of mineralization The degree of mineralization was estimated from the Micro-computed tomography attenuation values in the portion of the reconstructed samples that were characterized as bone. The previously Three-dimensional, high resolution reconstructions of determined threshold, used to separate bone from back- the trabecular bone of the specimens were obtained, ground, was applied. For this analysis, the voxels 73 exceeding the threshold kept their original gray value. The (Fig. 1), it was calculated that the fetal
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