Effects of different kinds of cranial deformation on the incidence of wormian bones

Researchers have debated whether the presence and frequency of wormian bones (sutural bones, supernumerary bones, and ossicles) are attributable to genetic factors, environmental factors, or both. This research examines the effects of many different kinds of cranial deformation on the incidence of wormian bones. A sample of 127 deformed and undeformed crania from New World archaeological sites was examined. An undeformed cranial sample (n=35) was compared to the following cranially deformed groups: 1) occipital, 2) lambdoid, 3) annular, 4) fronto-vertico-occipital, 5) parallelo-fronto-occipital, and 6) sagittal synostosis. Three levels of degree of cultural cranial deformation were qualitatively determined. Type and number of wormian bones along each major suture were recorded for each cranium. Group means were analyzed using Kruskal-Wallis one-way ANOVA statistical tests to test the null hypothesis that cranial deformation does not have an effect on wormian bone incidence. Results indicate that all forms of cranial deformation affect the frequency of some types of wormian bones. In particular, all cranially deformed groups exhibited significantly greater frequencies of lambdoid ossicles. Apical, parieto-mastoid, and occipito-mastoid wormian bones also appeared with greater frequency in some groups of culturally deformed crania. Further, varying degrees of cultural deformation all had more lambdoid wormian bones than the undeformed group. These results suggest that wormian bone development in posteriorly placed sutures may be affected more by environmental forces than are their anteriorly placed counterparts.     

The effect of artificial cranial deformation on the incidence of wormian bones in the lambdoidal suture

One hundred and twenty adult and 80 human fetal skulls were examined to find the relationship (if any) between the presence of wormian bones in the lambdoidal suture and artificial deformation of the skull. Wormian bones occur in deformed and undeformed skulls with no significant differences. Wormian bones detected in fetal skulls preclude cultural deformation as an important factor in the formation of these bones. It is hypothesized that a genetic predisposition (genes allowing formation of secondary ossification centers) is present and that wormian bones are under direct genetic control regardless of the presence or absence of detectable cultural deformation.     

Sutural effects of fronto-occipital cranial modification

Maya adult crania from the site of Lamanai, Belize provide a retrospective means of examining growth processes in the cranial vault. The Lamanai population practiced fronto-occipital deformation which is found to be significantly associated with premature sagittal synostosis and wormian bones of the lambdoidal suture. The undeformed members of the population also exhibit an abnormally high frequency of sagittal synostosis, but a significantly lower frequency than the deformed sample. It is suggested that the deforming apparatus creates tensile forces on the sagittal suture during the peak period of growth of the parietals, and that these forces might induce an adaptive response important in producing premature sagittal synostosis. The undeformed sample may have an increased congenital risk of sagittal synostosis created by their natural brachycephalic morphology in utero. The frequency patterning of wormian bones suggests a mixture of genetic and environmental causes in which tensile forces may also play a role. © 1996 Wiley-Liss, Inc.     

The influence of experimental deformation on neurocranial Wormian bones in rats

Two hundred and twenty crania of Wistar rats were experimentally deformed. The growth of the anterior vault was restricted in one subgroup and the growth of the posterior vault was restricted in the second subgroup. Seventy-seven deformed animals survived up to the thirtieth day of age and were sacrificed. Both subgroups were compared with each other as well as with 37 surviving sham-operated animals and 51 controls, all samples being 30 days of age (group A). Additionally, 33 normal crania of animals sacrificed at 1, 10 and 20 days as well as 19 deformed crania of 10 and 20 days old were observed (group B). Chi-square and Z tests were employed. Wormian bones found in the skulls of normal growing rats apparently represent an epigenetic polymorphism. Higher frequencies of wormian bones were found in deformed crania than in sham-operated ones and controls. Experimental deformation may be an extra-genetic factor that affects the normal genetic expression of wormian bones. This concept is relevant to studies of human population differences based on discontinuous cranial traits.     

Test of the relationship between sutural ossicles and cultural cranial deformation: Results from Hawikuh,New Mexico

A number of researchers have hypothesized that the biomechanical forces associated with cultural cranial deformation can influence the formation of sutural ossicles. However, it is still difficult to make definitive conclusions about this relationship because the effects appear to be quite weak, and contradictory results have been obtained when specific sutures and deformation types are compared across studies. This research retests the hypothesis using a single archeological sample of lamdoidally deformed, occipitally deformed, and undeformed crania from Hawikuh, New Mexico (AD 1300–1680). Our results show no significant difference in either the prevalence or number of ossicles between deformed and undeformed crania, suggesting that the abnormal strains generated by cranial shape modification during infancy are not a factor in ossicle development for this population. One significant relationship was detected at the right lambdoid suture in crania with asymmetrical occipital deformation. Crania that were more deformed on the left side showed greater numbers of ossicles on the right side, but the effect was small. Furthermore, the relationship may well reflect a sampling error, due to the small number of crania with greater left side deformation and scorable right side lambdoid ossicles (n = 11). Although it is possible that forms of cranial deformation other than the posterior tabular types examined here may affect ossicle expression, our review of the literature suggests that the relationship in humans is complex and incompletely understood at this time. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

A genomic survey of the fish parasite Spironucleus salmonicida indicates genomic plastiCity among diplomonads and significant lateral gene transfer in eukaryote genome evolution

Background

Craniosynostosis, the premature fusion of calvarial sutures, is a common craniofacial abnormality. Causative mutations in more than 10 genes have been identified, involving fibroblast growth factor, transforming growth factor beta, and Eph/ephrin signalling pathways. Mutations affect each human calvarial suture (coronal, sagittal, metopic, and lambdoid) differently, suggesting different gene expression patterns exist in each human suture. To better understand the molecular control of human suture morphogenesis we used microarray analysis to identify genes differentially expressed during suture fusion in children with craniosynostosis. Expression differences were also analysed between each unfused suture type, between sutures from syndromic and non-syndromic craniosynostosis patients, and between unfused sutures from individuals with and without craniosynostosis.

Results

We identified genes with increased expression in unfused sutures compared to fusing/fused sutures that may be pivotal to the maintenance of suture patency or in controlling early osteoblast differentiation (i.e. RBP4, GPC3, C1QTNF3, IL11RA, PTN, POSTN). In addition, we have identified genes with increased expression in fusing/fused suture tissue that we suggest could have a role in premature suture fusion (i.e. WIF1, ANXA3, CYFIP2). Proteins of two of these genes, glypican 3 and retinol binding protein 4, were investigated by immunohistochemistry and localised to the suture mesenchyme and osteogenic fronts of developing human calvaria, respectively, suggesting novel roles for these proteins in the maintenance of suture patency or in controlling early osteoblast differentiation. We show that there is limited difference in whole genome expression between sutures isolated from patients with syndromic and non-syndromic craniosynostosis and confirmed this by quantitative RT-PCR. Furthermore, distinct expression profiles for each unfused suture type were noted, with the metopic suture being most disparate. Finally, although calvarial bones are generally thought to grow without a cartilage precursor, we show histologically and by identification of cartilage-specific gene expression that cartilage may be involved in the morphogenesis of lambdoid and posterior sagittal sutures.

Conclusion

This study has provided further insight into the complex signalling network which controls human calvarial suture morphogenesis and craniosynostosis. Identified genes are candidates for targeted therapeutic development and to screen for craniosynostosis-causing mutations.     

Restricted growth at the frontonasal suture: alterations in craniofacial growth in rabbits

Apposition of bone at the sutural margin is generally thought to be a compensatory adjustment to growing soft-tissue organs such as the brain or eyes within the skull. The frontonasal suture which is located at the interface between the cranial and facial skeletons is a site of extremely active growth in the young rabbit. Recently, we showed that premature closure of a cranial suture, the coronal suture, can alter the growth not only at the adjacent frontonasal suture but also of the basicranium and midface. This study examines the effects of restricted growth at the frontonasal suture on both growth at adjacent cranial sutures and linear growth of the basicranium and midface. Thirty newborn New Zealand White rabbits were subdivided into experimental and sham-treated groups of equal size and distribution for sex and birth weight. At 9 days of age, the frontonasal suture of each experimental animal was immobilized by bilateral application of methyl-cyanoacrylate adhesive across the frontonasal suture. Growth and morphometric changes were monitored by radiocephalometric methods through 120 days of age by bilateral implantation of radiopague markers on each side of frontonasal, coronal, and anterior lambdoid sutures. Results indicate that restricted growth at the frontonasal suture results not only in a significant shortening of the midface but also in significant decreases in growth at the coronal and internasal sutures. Growth at the interfrontal and sagittal sutures is increased. Furthermore, growth at the anterior portion of the nasal bones is significantly increased, thereby offsetting a portion of the decreased nasal bone length resulting from frontonasal restriction.     

A note on the effect of asymmetry in suture closure in mature human skulls

Studies on suture closure in mature European and East African Bantu skulls revealed marked differences in the degree of suture closure on the left and right side. Asymmetrical closure of sutures may lead to erroneous conclusions being made in ageing skulls if only one-half of the skull is available for examination. Asymmetry in suture closure was rather common in recent skulls, being particularly noticeable in the bregmatic and complicate parts of the coronal suture and in intermediate portions of lambdoid sutures.     

Size and shape of human cranial sutures--a new scoring method

A method for the differentiation of sutural patterns of the human cranial vault is introduced. Three criteria of differentiation are considered, one for size and two for shape: 1) maximal shape extension; 2) basic configuration; 3) secondary protrusion. The method is illustrated here for the coronal and lambdoid sutures of 70 recent Italian skulls (35 adult males and 35 adult females). Differences between coronal and lambdoid sutural size and shape can be detected analytically; for example, the coronal suture commonly shows lesser degrees of shape extension, a simpler basic configuration, and an absence of secondary protrusion. Heterogeneity within each suture, as well as a relationship among corresponding sections and between the three criteria adopted, have been also observed; symmetry predominates for both the sutures, and sexual differences are slight.     

Asymmetry in East African skulls

Skulls from 297 East Africans were examined in relation to their symmetry; 98% were found to be asymmetrical. The most common types of asymmetry were right fronto-petalia, left parieto-petalia, and left occipito-petalia (21.2%). No significant differences were found among the East African populations. Sixteen per cent of the skulls had wormian bones, all of which were found in asymmetrical skulls. The problem of asymmetry of skulls is discussed and the literature on the subject reviewed.     

Nanism with short limbs, dysmorphism, renal dysplasia, growth hormone deficiency with pituitary hypoplasia and psychomotor delay: a new syndrome?

The authors present the case of a male infant affected with short limbed dwarfism already detected in utero by ultrasound. In addition, facial dysmorphism, bilateral hypoplasia and dysplasia of the kidneys with altered renal function, hypotonia and non-evolutive developmental delay are noted. Endocrine tests show a severe and isolated growth hormone deficiency. Metabolic investigations are negative, including peroxisomal functions. Prometaphase chromosomes are normal. Bone x-rays reveal generalized osteoporosis with absence of post-natal osseous maturation and the presence of wormian bones. Major pituitary hypoplasia is demonstrated by nuclear magnetic resonance. The present observation is compared to the case reported by Stratton & Parker (Am. J. Med. Genet., 1989, 32, 169-173). Available data do not allow either to affirm or to exclude the identity of the syndromes presented by these 2 isolated cases.     

Cranial suture complexity in white-tailed deer (Odocoileus virginianus)

Neurocranial expansion and mastication are commonly implicated as the two major biomechanical factors affecting suture morphology. In deer the antlers provide an additional source of biomechanical stress acting on the skull. Equivalent stresses are not found in females, who lack antlers. We analyzed the complexity and interdigitation of the interfrontal and coronal sutures that surround the antler-bearing frontal bones of (n = 67) white-tailed deer (Odocoileus virginianus) to 1) evaluate changes in suture morphology throughout ontogeny, and 2) test the hypothesis that male deer have more complex sutures than females. Two methods were used to quantify suture morphology: fractal analysis and length-ratios (actual suture length divided by direct straightline length). Both techniques produced similar results, although the two methods cannot be considered equivalent. Suture complexity increases markedly throughout ontogeny, but appears to level off after animals have reached adulthood. Cranial size in males, but not females, continues to increase in adults. No significant increase in suture complexity with age in the adult cohort was detected. While deer are highly dimorphic in size and the presence of antlers, no significant differences existed between males and females for any measure of suture complexity. No consistent patterns emerged between suture complexity and skull size or antler characteristics. The presence of antlers appears to have a minimal effect on suture complexity in white-tailed deer. Factors that may contribute to the lack of dimorphism in suture complexity are discussed.     

Cell fate specification during calvarial bone and suture development

In this study we have addressed the fundamental question of what cellular mechanisms control the growth of the calvarial bones and conversely, what is the fate of the sutural mesenchymal cells when calvarial bones approximate to form a suture. There is evidence that the size of the osteoprogenitor cell population determines the rate of calvarial bone growth. In calvarial cultures we reduced osteoprogenitor cell proliferation; however, we did not observe a reduction in the growth of parietal bone to the same degree. This discrepancy prompted us to study whether suture mesenchymal cells participate in the growth of the parietal bones. We found that mesenchymal cells adjacent to the osteogenic fronts of the parietal bones could differentiate towards the osteoblastic lineage and could become incorporated into the growing bone. Conversely, mid-suture mesenchymal cells did not become incorporated into the bone and remained undifferentiated. Thus mesenchymal cells have different fate depending on their position within the suture. In this study we show that continued proliferation of osteoprogenitors in the osteogenic fronts is the main mechanism for calvarial bone growth, but importantly, we show that suture mesenchyme cells can contribute to calvarial bone growth. These findings help us understand the mechanisms of intramembranous ossification in general, which occurs not only during cranial and facial bone development but also in the surface periosteum of most bones during modeling and remodeling.     

Cranial deformation and nonmetric trait variation

Cranial deformation is known to influence many traditional craniometric variables, but its effects on nonmetric trait variation are not well characterized. In this study, we examine the effects of three types of deformation (annular, lambdoid flattening, and fronto-occipital) on nonmetric traits, using a large sample of protohistoric and prehistoric crania. Our results indicate that a few traits are increased or decreased in relative frequency by particular types of deformation, but that these effects have little impact on the calculation of biological distances between groups. © 1993 Wiley-Liss, Inc.     

Biomechanics of the rostrum and the role of facial sutures

The rostrum is a large diameter, thin-walled tubular structure that receives loads from the teeth. The rostrum can be conceptualized both as a rigid structure and as an assemblage of several bones that interface at sutures. Using miniature pigs, we measured in vivo strains in rostral bones and sutures to gain a better understanding of how the rostrum behaves biomechanically. Strains in the premaxillary and nasal bones were low but the adjacent maxillary-premaxillary, internasal, and intermaxillary suture strains were larger by an order of magnitude. While this finding emphasizes the composite nature of the rostrum, we also found evidence in the maxillary and nasal bones for rigid structural behavior. Namely, maxillary strain is consistent with a short beam model under shear deformation from molar loading. Strain in the nasal bones is only partially supported by a long beam model; rather, a complex pattern of dorsal bending of the rostrum from incisor contact and lateral compression is suggested. Torsion of the maxilla is ruled out due to the bilateral occlusion of pigs and the similar working and balancing side strains, although it may be important in mammals with a unilateral bite. Torsional loading does appear important in the premaxillae, which demonstrate working and balancing side changes in strain orientation. These differences are attributed to asymmetrical incisor contact occurring at the end of the power stroke.     

Mechanics of cranial sutures during simulated cyclic loading

Previous computational and experimental analyses revealed that cranial sutures, fibrous joints between the bones, can reduce the strain experienced by the surrounding skull bones during mastication. This damping effect reflects the importance of including sutures in finite element (FE) analyses of the skull. Using the FE method, the behaviour of three suture morphologies of increasing complexity (butt-ended, moderate interdigitated, and complex interdigitated) during static loading was recently investigated, and the sutures were assumed to have linear elastic properties. In the current study, viscoelastic properties, derived from published experimental results of the nasofrontal suture of young pigs (Sus scrofa), are applied to the three idealised bone-suture models. The effects of suture viscoelasticity on the stress, strain, and strain energy in the models were computed for three different frequencies (corresponding to periods of 1, 10, and 100s) and compared to the results of a static, linear elastic analysis. The range of applied frequencies broadly represents different physiological activities, with the highest frequency simulating mastication and the lowest frequency simulating growth and pressure of the surrounding tissues. Comparing across all three suture morphologies, strain energy and strain in the suture decreased with the increase in suture complexity. For each suture model, the magnitude of strain decreased with an increase in frequency, and the magnitudes were similar for both the elastic and 1s frequency analyses. In addition, a viscous response is less apparent in the higher frequency analyses, indicating that viscous properties are less important to the behaviour of the suture during those analyses. The FE results suggest that implementation of viscoelastic properties may not be necessary for computational studies of skull behaviour during masticatory loading but instead might be more relevant for studies examining lower frequency physiological activities.     

Relationships between growth at the sutures of the rabbit calvarium

The present study was designed to elucidate the relationships between growth increments at the cranial vault sutures in rabbits. Thirteen male New Zealand white rabbits were followed regularly from age 31 to 142 days using a roentgen stereophotogrammetric system. Spherical tantalum markers were implanted into the nasal, frontal, and parietal bones, and implant stability was checked at each stereo examination. Problems with instability were encountered only in the nasal bones. Registered growth rates conformed to our previous investigations. High correlations were observed between the following areas; the coronal suture to the frontonasal suture, the first principal component of the neurocranial suture group to the frontonasal suture, and the principal component of the craniofacial suture group to the coronal suture. Remaining relationships demonstrated dispersion to various extents. The findings indicate that there seems to exist a basic mutual dependence between neural and facial skeletal growth, as well as complex covariations between the various sutures of the rabbit calvarium.     

The influence of artificial cranial vault deformation on the expression of cranial nonmetric traits: its importance in the study of evolutionary relationships

Nonmetric cranial traits have been commonly used in evolutionary relationship studies. They develop during the growth and development of an individual, and for this reason its expression presents different sources of genetic and nongenetic variation. However, the use of these features in evolutionary relationship studies carries the implicit assumption that much of the nonmetric trait variation is essentially genetic. Among the nonheritable factors, cranial vault deformation has been the most studied in human populations. Because of the widespread distribution and elevated rate of artificial cranial vault deformation found in America, and the importance of nonmetric traits in evolutionary relationship studies in this area, the objectives of this paper are as follows: (a) to study the influence of artificial cranial vault deformation on the presence of nonmetric traits within samples of human craniofacial remains; and (b) to establish artificial cranial vault deformation influence on evolutionary relationships between local populations on a regional scale. Our results indicate that artificial cranial vault deformations alter the variation and covariation of metric and nonmetric traits in some samples. Wormian bones, placed in cranial vault sutures, are the most influenced by this factor. However, our results suggest that when all nonmetric traits were used the artificial cranial vault deformation did not influence the basic pattern of variation among samples. The exclusion or inclusion of wormians bones in evolutionary relationships analysis did not modify the results, but using only wormians bones lead to inconsistent results indicating that these traits have little value on these kind of studies.     

Long-term effects of tissue expansion on cranial and skeletal bone development in neonatal miniature swine: clinical findings and histomorphometric correlates

Progressive tissue expansion induces significant gross, histologic, and bony changes in skulls and long bones of neonatal miniature swine. These bony changes consist of erosion underlying tissue expanders, with bony lipping and bone deposition at the periphery of the expander. Cranial suture lines underneath expanders appear effaced and convoluted. Serial CT scans reveal decreased bone thickness and volume (p less than 0.02) but identical bone density (p = 0.60) beneath expanders. Increased bone volume and thickness occur at the periphery of expanders (p less than 0.02). Bone density (CT number) is unaffected by tissue expansion in both cranial and long bones. These findings have histomorphometric correlates: Osteoclastic bone resorption occurs underneath expanders with periosteal reaction at the periphery of expanders. Cranial sutures are similarly affected, but no cranial synostosis results. No changes to the inner table of the skull or stigmata of increased intracranial pressure were observed either in CT scans or in behavioral changes in long-term animals. The pathophysiology of bony changes is a remodeling effect, not one of simple pressure deformation. Increased bone resorption and complete inhibition of bone formation occur until the pressure is removed. Cranial bone is significantly more affected than long bone. After removal of the expanders, reparative bone remodeling begins within 5 days and nearly complete healing of the cranial defects occurs within 2 months (p less than 0.02). No plagiocephaly results despite early coronal suture changes. On the basis of this study, we conclude that tissue expansion causes significant but reversible effects, readily monitored by high-resolution CT scans, on neonatal and infant cranial and long bones.