The role of basicranial synchondroses in flexure processes and ontogenetic development of the skull base

The contribution of the basicranial synchondroses in the growth of neurocranial length and ontogenetic development of the cranial base were investigated. The study concentrated on the midsphenoidal synchondrosis and its delayed fusion in nonhuman primates when compared to man, and on the spheno-occipital synchondrosis. The mode and time of fusion of both growth centers were observed, and their role in the ontogenetic growth changes (flattening processes) of the cranial base were established. The chondrogenic ossification of midsphenoidal and spheno-occipital synchondroses was studied on 20 skulls of Macaca mulatta females, ranging in age from newborn specimens to those 24 months old. The technique of in vivo tetracycline bone labeling was used for histologic evaluation of the material. Different chondrogenic growth patterns were observed in both synchondroses. The endochondral activity of the spheno-occipital synchondrosis increased with age, from a nonactive narrow cartilaginous column in the neonatal specimen to a broad band with high chondrogenic ossification in the 24-month-old specimens. This growth center contributes to elongation of the posterior portion of the cranial base and is a secondary factor in its flexion. The midsphenoidal synchondrosis seems to be the primary factor in the mode of flexure of the cranial base in Macaques. This growth center is very active in the first ten months of life but later exhibits cessation of chondrogenic activity and long remains unfused. The first signs of fusion were observed as late as 72 months of age. At the same time, the continuous process of cranial base flattening showed the first signs of tapering off.     

Anterior cervical microsurgical approach to the cranial base in the rabbit: technical note.

Current trends in research on craniofacial syndromes have led to enhanced interest in the cranial base as a contributory factor in the development of normal and abnormal midfacial structure. Indeed, attention has focused upon one particular growth plate in the posterior cranial base, the spheno-occipital synchondrosis, since it has been shown that alterations in this structure are associated with profound changes in craniofacial growth. In this report we describe a surgical approach to the cranial base of the rabbit that is safe, simple and reliable. It is applicable to neonatal as well as adult rabbits.     

A factor analysis of cranial base and vault dimensions in children

Lengths within the cranial base and vault were measured in cephalometric radiographs of 220 boys and 177 girls ranging in age from 0 to 15 years; all these children are participants in The Fels Longitudinal Growth Study. The present study is based on mixed longitudinal data derived from 1640 radiographs for boys and 1260 radiographs for girls. Factor analysis was applied separately for boys and girls for each age group; i.e., 0–3, 4–6, 7–9, 10–12, and 13–15 years. For the 0–3 year age group, two factors were extracted in each sex, whereas four factors were extracted in the rest of the age groups. The factor structures are similar in the three older age groups of boys (7–9, 10–12, and 13–15 years). The first four factors for these groups are labelled, respectively: cranial vault size, posterior cranial base length, presphenoid length, and basisphenoid length. The order of the third and fourth factors is reversed in the 7–9 year olds. For girls, the factors extracted were also the same in both the 7–9 and 10–12 year age groups, even though the order of factors was different between age groups; i.e., anterior cranial base length, cranial vault size, basisphenoid length, and basioccipital length. Differential growth rates among cranial base dimensions probably cause changes in factor patterns. Obliteration of the spheno-occipital synchondrosis is suggested as the mechanism responsible for the change of factor pattern in the girls. Closure of this synchondrosis would have occurred too late to affect the patterns in boys.     

Conditional Kif3a ablation causes abnormal hedgehog signaling topography, growth plate dysfunction, and excessive bone and cartilage formation during mouse skeletogenesis

The motor protein Kif3a and primary cilia regulate important developmental processes, but their roles in skeletogenesis remain ill-defined. Here we created mice deficient in Kif3a in cartilage and focused on the cranial base and synchondroses. Kif3a deficiency caused cranial base growth retardation and dysmorphogenesis, which were evident in neonatal animals by anatomical and micro-computed tomography (microCT) inspection. Kif3a deficiency also changed synchondrosis growth plate organization and function, and the severity of these changes increased over time. By postnatal day (P)7, mutant growth plates lacked typical zones of chondrocyte proliferation and hypertrophy, and were instead composed of chondrocytes with an unusual phenotype characterized by strong collagen II (Col2a1) gene expression but barely detectable expression of Indian hedgehog (Ihh), collagen X (Col10a1), Vegf (Vegfa), MMP-13 (Mmp13) and osterix (Sp7). Concurrently, unexpected developmental events occurred in perichondrial tissues, including excessive intramembranous ossification all along the perichondrial border and the formation of ectopic cartilage masses. Looking for possible culprits for these latter processes, we analyzed hedgehog signalling topography and intensity by monitoring the expression of the hedgehog effectors Patched 1 and Gli1, and of the hedgehog-binding cell-surface component syndecan 3. Compared with controls, hedgehog signaling was quite feeble within mutant growth plates as early as P0, but was actually higher and was widespread all along mutant perichondrial tissues. Lastly, we studied postnatal mice deficient in Ihh in cartilage; their cranial base defects only minimally resembled those in Kif3a-deficient mice. In summary, Kif3a and primary cilia make unique contributions to cranial base development and synchondrosis growth plate function. Their deficiency causes abnormal topography of hedgehog signaling, growth plate dysfunction, and un-physiologic responses and processes in perichondrial tissues, including ectopic cartilage formation and excessive intramembranous ossification.     

Retinoic acid modulates chondrogenesis in the developing mouse cranial base

The retinoic acid (RA) signaling pathway is known to play important roles during craniofacial development and skeletogenesis. However, the specific mechanism involving RA in cranial base development has not yet been clearly described. This study investigated how RA modulates endochondral bone development of the cranial base by monitoring the RA receptor RARγ, BMP4, and markers of proliferation, programmed cell death, chondrogenesis, and osteogenesis. We first examined the dynamic morphological and molecular changes in the sphenooccipital synchondrosis-forming region in the mouse embryo cranial bases at E12-E16. In vitro organ cultures employing beads soaked in RA and retinoid-signaling inhibitor citral were compared. In the RA study, the sphenooccipital synchondrosis showed reduced cartilage matrix and lower BMP4 expression while hypertrophic chondrocytes were replaced with proliferating chondrocytes. Retardation of chondrocyte hypertrophy was exhibited in citral-treated specimens, while BMP4 expression was slightly increased and programmed cell death was induced within the sphenooccipital synchondrosis. Our results demonstrate that RA modulates chondrocytes to proliferate, differentiate, or undergo programmed cell death during endochondral bone formation in the developing cranial base.     

Expression of Cre recombinase in chondrocytes causes abnormal craniofacial and skeletal development

The cranial base synchondroses are growth centers that drive cranial and upper facial growth. The intersphenoid synchondrosis (ISS) and the spheno-occipital synchondrosis (SOS) are two major synchondroses located in the middle of the cranial base and are maintained at early developmental stages to sustain cranial base elongation. In this study, we report unexpected premature ossification of ISS and SOS when Cre recombinase is activated in a chondrocyte-specific manner. We used a Cre transgenic line expressing Aggrecan enhancer-driven, Tetracycline-inducible Cre (ATC), of which expression is controlled by a Col2a1 promoter. Neonatal doxycycline injection or doxycycline diet fed to breeders was used to activate Cre recombinase. The premature ossification of ISS and/or SOS led to a reduction in cranial base length and subsequently a dome-shaped skull. Furthermore, the mice carrying either heterozygous or homozygous conditional deletion of Tsc1 or Fip200 using ATC mice developed similar craniofacial abnormalities, indicating that Cre activity itself but not conditional deletion of Tsc1 or Fip200 gene, is the major contributor of this phenotype. In contrast, the Col2a1-Cre mice carrying Cre expression in both perichondrium and chondrocytes and the mice carrying the conditional deletion of Tsc1 or Fip200 using Col2a1-Cre did not manifest the same skull abnormalities. In addition to the defective craniofacial bone development, our data also showed that the Cre activation in chondrocytes significantly compromised bone acquisition in femur. Our data calls for the consideration of the potential in vivo adverse effects caused by Cre expression in chondrocytes and reinforcement of the importance of including Cre-containing controls to facilitate accurate phenotype interpretation in transgenic research.

     

The craniofacial pattern of the Lengua Indians of Paraguay

Lateral cephalometric headfilms of 30 male and 30 female Lengua Indians taken in the Chaco area of Paraguay were compared with a sample of 23 male and 25 female South African Caucasoids with excellent occlusion. The most obvious difference noted between the two population groups was the degree of prognathism evident in the Lengua. This was attributed to the generally shorter anterior cranial base in the latter group rather than to the size or forward positioning of their jaws. The significantly larger ANB (Subspinale, Nasion, Supramentale) angle observed in the Lengua was attributed to one or both of two factors, namely, the short anterior cranial base or the clockwise rotation (forward tipping) of the jaws relative to the anterior cranial base. Chinpoint position relative to the anterior cranial base in the Lengua is not much different from that of our Caucasoid sample. The lower incisor teeth in the Lengua, but not the upper ones, are more labially inclined than those of the Caucasoids.     

13—18岁正常人上、中面部对称性生长发育的纵向研究

本文运用13— 18岁正常纯纵向样本资料 ,头颅定位后前位 X线头影测量法 ,分析正常人上、中面部的对称性与变异 ,探讨其随生长发育的变化趋势 ,为客观区分对称性的正常变异和不对称畸形提供依据。结果表明 :正常人上、中面部骨骼存在对称性的正常变异 ,其范围在13—18岁保持稳定 ,水平向小于8% ,垂直向不超过9mm;在其相对于颅底的位置关系及其骨骼各对应部位之间 ,有较好对称性 ;面部骨骼的生长发育具有潜在的优势特点。     

Brief Communication: Timing of spheno‐occipital closure in modern Western Australians

The spheno‐occipital synchondrosis is a craniofacial growth centre between the occipital and sphenoid bones—its ossification persists into adolescence, which for the skeletal biologist, means it has potential application for estimating subadult age. Based on previous research the timing of spheno‐occipital fusion is widely variable between and within populations, with reports of complete fusion in individuals as young as 11 years of age and nonfusion in adults. The aim of this study is, therefore, to examine this structure in a mixed sex sample of Western Australian individuals that developmentally span late childhood to adulthood. The objective is to develop statistically quantified age estimation standards based on scoring the degree of spheno‐occipital fusion. The sample comprises multidetector computed tomography (MDCT) scans of 312 individuals (169 male; 143 female) between 5 and 25 years of age. Each MDCT scan is visualized in a standardized sagittal plane using three‐dimensional oblique multiplanar reformatting. Fusion status is scored according to a four‐stage system. Transition analysis is used to calculate age ranges for each defined stage and determine the mean age for transition between an unfused, fusing and fused status. The maximum likelihood estimates for the transition from open to fusing in the endocranial half is 14.44 years (male) and 11.42 years (female); transition from fusion in the ectocranial half to complete fusion is 16.16 years (male) and 13.62 years (female). This study affirms the potential value of assessing the degree of fusion in the spheno‐occipital synchondrosis as an indicator of skeletal age. Am J Phys Anthropol 153:132–138, 2014. © 2013 Wiley Periodicals, Inc.     

Patterns of postnatal development in skulls of lynxes,genus Lynx (Mammalia: Carnivora)

Studies on ossification patterns and other ontogenetic events associated with postnatal cranial growth of wild felids are scarce. An analysis of developmental processes undergone by several cranial structures (presphenoidal and sphenooccipital synchondroses, temporal and sagittal crests, and deciduous and permanent teeth) during postnatal growth has been conducted on a sample of 336 specimens belonging to the four Recent species of lynxes (Lynx pardinus, Lynx lynx, Lynx rufus, and Lynx canadensis). Age has been estimated based on tooth replacement, skull size, and by counting the annual lines of cementum growth. Comparison of the results obtained for each of the four species reveal (1) a single pattern for both tooth replacement and ossification of the sphenooccipital synchondrosis, (2) two ossification patterns for the presphenoidal synchondrosis, (3) a common pattern for development of temporal ridges and sagittal crest showing different degrees of morphological expression, and (4) evidence suggesting the involvement of a heterochronic process, neoteny, in the morphological differentiation of several populations and species of the genus Lynx. These data also support the hypothesis that processes involved in the replacement of carnassials are based on functional requirements. © 1996 Wiley-Liss, Inc.     

A cranial base of Australopithecus robustus from the hanging remnant of Swartkrans, South Africa

SKW 18, a partial hominin cranium recovered from the site of Swartkrans, South Africa, in 1968 is described. It is derived from ex situ breccia of the Hanging Remnant of Member 1, dated to approximately 1.5-1.8 Mya. Although partially encased in breccia, it was refit to the facial fragment SK 52 (Clarke 1977 The Cranium of the Swartkrans Hominid SK 847 and Its Relevance to Human Origins, Ph.D. dissertation, University of the Witwatersrand, Johannesburg), producing the composite cranium SKW 18/SK 52. Subsequent preparation revealed the most complete cranial base attributable to the species Australopithecus robustus. SKW 18 suffered weathering and slight postdepositional distortion, but retains considerable anatomical detail. The composite cranium most likely represents a large, subadult male, based on the incomplete fusion of the spheno-occipital synchondrosis; unerupted third molar; pronounced development of muscular insertions; and large teeth. Cranial base measures of SKW 18 expand the range of values previously recorded for A. robustus. SKW 18 provides information on anatomical features not previously visible in this taxon, and expands our knowledge of morphological variability recognizable in the cranial base. Morphological heterogeneity in the development of the prevertebral and nuchal muscular insertions is likely the result of sexual dimorphism in A. robustus, while differences in cranial base angles and the development of the occipital/marginal sinus drainage system cannot be attributed to size dimorphism.     

Presphenoidal synchondrosis fusion in DBA/2J mice

Cranial base growth plates are important centers of longitudinal growth in the skull and are responsible for the proper anterior placement of the face and the stimulation of normal cranial vault development. We report that the presphenoidal synchondrosis (PSS), a midline growth plate of the cranial base, closes in the DBA/2J mouse strain but not in other common inbred strains. We investigated the genetics of PSS closure in DBA/2J mice by evaluating F1, F1 backcross, and/or F1 intercross offspring from matings with C57BL/6J and DBA/1J mice, whose PSS remain open. We observed that PSS closure is genetically determined, but not inherited as a simple Mendelian trait. Employing a genome-wide SNP array, we identified a region on chromosome 11 in the C57BL/6J strain that affected the frequency of PSS closure in F1 backcross and F1 intercross offspring. The equivalent region in the DBA/1J strain did not affect PSS closure in F1 intercross offspring. We conclude that PSS closure in the DBA/2J strain is complex and modified by different loci when outcrossed with C57BL/6J and DBA/1J mice.     

Hawaiian craniofacial morphometrics: Average Mokapuan skull,artificial cranial deformation,and the “rocker” mandible

Craniofacial morphology and cultural cranial deformation were analyzed by the computer morphometric system in 79 adult Hawaiian skulls from Mokapu, Oahu. The average Hawaiian male was large, but similar in shape to the female. Both were larger than the present Caucasian, showed a greater dental protrusion, and possessed a larger ANB angle, flatter cranial base, and larger facial heights. Correlations in Hawaiian craniofacial structure were found between an increasing mandibular plane angle and (1) shorter posterior facial height, (2) larger gonial angle, (3) larger cranial base angle, and (4) smaller SNA and SNB angles. Of the 79 skulls studied, 8. 9% were found to have severe head molding or intentional cranial deformation. Significant statistical differences between the molded group and the nonmolded group are, in decreasing significance: (1) larger upper face height, (2) smaller glabella to occiput distance, and (3) increased lower face height with deformation. The morphometric differences were readily seen by graphic comparison between groups. It is postulated that external forces to the neurocranium result in redirection of the growth vectors in the neurocranial functional matrix, including the cranial base, and secondarily, to the orofacial functional matrix. There is a possibility that the cranial deformation is a retention of the normal birth molding changes. The Polynesian “rocker jaw” was found in 81% to 95% of this populace. This mandibular form occurs only with attainment of adult stature and craniofacial form. This data agrees with the hypothesis that mandibular form is modified by the physical forces present and their direction in the orofacial functional matrix.     

Ontogeny of the spheno‐occipital synchondrosis in a modern Queensland,Australian population using computed tomography

Due to disparity regarding the age at which skeletal maturation of the spheno‐occipital synchondrosis occurs in forensic and biological literature, this study provides recalibrated multislice computed tomography (MSCT) age standards for the Australian (Queensland) population, using a Bayesian statistical approach. The sample comprises retrospective cranial/cervical MSCT scans obtained from 448 males and 416 females aged birth to 20 years from the Skeletal Biology and Forensic Anthropology Research Osteological Database. Fusion status of the synchondrosis was scored using a modified six‐stage scoring tier on an MSCT platform, with negligible observer error (κ = 0.911 ± 0.04, intraclass correlation coefficient = 0.994). Bayesian transition analysis indicates that females are most likely to transition to complete fusion at 13.1 years and males at 15.6 years. Posterior densities were derived for each morphological stage, with complete fusion of the synchondrosis attained in all Queensland males over 16.3 years of age and females aged 13.8 years and older. The results demonstrate significant sexual dimorphism in synchondrosis fusion and are suggestive of intrapopulation variation between major geographic regions in Australia. This study contributes to the growing repository of contemporary anthropological standards calibrated for the Queensland milieu to improve the efficacy of the coronial process for medicolegal death investigation. As a stand‐alone age indicator, the basicranial synchondrosis may be consulted as an exclusion criterion when determining the age of majority that constitutes 17 years in Queensland forensic practice. Am J Phys Anthropol 157:42–57, 2015. © 2014 Wiley Periodicals, Inc.     

Determination of cranial capacity in fossil men

The cranial capacity of a skull of unknown origin can be determined by assuming that the product of the chief dimensions corresponds to a part of the endocranial volume. We start with formulas for present day man and determine their validity for fossil man. The equivalence differs in fossil men according to their taxonomic position. This method is useful even for damaged skulls, with porion and basion missing.     

Ontogenic growth changes of the skull base in four genera of nonhuman primates.

Cross-sectional studies of the degree of the cranial base flexion were carried out in infant, juvenile and adult skulls in four genera of nonhuman primates (P. paniscus, H. lar, P. urinus, and M. mullatta). The cephalometric observations of the cranial base included linear and angular measurements of each specimen. The data obtained in this study showed that the anterior portion of the cranial base exhibits a significant shortening trend as the mammalian evolutionary scale ascends. Moreover, the growth pattern of the anterior portion of the skull base follows that of the facial bony structures. The ontogenic growth changes of the posterior portion of the skull base follows the growth pattern of the endocranial cavity. The significant trend of elongation in this area directly contributes to the posterior migration of the foramen magnum. The magnitude of these growth changes decreases as the evolutionary scale ascends. The angular measurements of the cranial flexion showed a less obtuse cranial base angle in young specimens and the ones higher on the mammalian scale. The skull kyphosis was less pronounced in these specimens and the anatomical features of the cranial base were more humanlike, including the balance of the head expressed by the position of the foramen magnum.     

Cranial growth and growth dimorphism in Ateles geoffroyi

With the exception of the work of Schultz (1960), cranial growth in Ateles is not well documented. This paper describes the results of a detailed quantitative study of cranial ontogeny in male and female Ateles geoffroyi. Using Euclidean Distance Matrix Analysis (EDMA), local areas of form change due to growth within spider monkey crania are identified. We found substantial change local to the zygomatic region in the face, identified mediolaterally directed changes in the palate, detected relatively larger amounts of change local to the anterior neurocranium compared to the posterior neurocranium, and demonstrate a greater amount of basicranial growth along a mediolateral axis than previously reported. Cranial sexual dimorphism is also examined. A. geoffroyi is noted for being monomorphic, and we found a general similarity between male and female cranial forms at all developmental ages. However, differences in overall cranial size between the sexes were found in the oldest subadult age group but not between male and female adults. This difference suggests that A. geoffroyi females attain their adult cranial form slightly before males and implies a pattern of earlier onset of female maturity relative to males. © 1993 Wiley-Liss, Inc.