The dichotomous pattern of craniofacial expansion during aging

The craniofacial skeleton expands during adult life and previous investigations have demonstrated non-uniformity in continuing growth. This report confirms the fact that sella turcica, frontal sinus and the skull tables remodel at a rate per unit time which is twice the amount of the anterior-posterior skull diameter. The dual enlargement pattern occurs in both males and females and has been observed longitudinally from the third through the eighth decades of life. Though associations in the continuing growth process of separate anatomical parts throughout the human skeleton remain obscure, the degree to which components vary within the craniofacial system is now clearly evident.     

Pattern in craniofacial biology: Evidence from the old world monkeys (Cercopithecidae)

An understanding of craniofacial growth, both evolutionarily and clinically, requires an investigation of pattern —geometric relations that remain relatively constant among growing structures or components of the skull. Several craniofacial biologists have suggested that specific morphological relations remain invariant during growth and in interspecific comparisons of adults of varying size. We tested the hypothesized invariance of a series of craniofacial angles in a sample of adult Old World monkeys. Fifteen angles were determined from lateral cranial radiographs. Criteria for examining angular invariance included tests for significant correlations and regression slopes with palatal length (overall skull size), tests for significant mean differences (ANOVAs) in angular values between the two subfamilies of Cercopithecidae — Cercopithecinae and Colobinae — and the computation and ranking of standard deviations (SDs) and coefficients of variation (CVs). Results indicate that most of the cranial angles purported to be invariant do not in fact meet the criteria for acceptance. One of the few cranial angles that evinces a somewhat constant value is that between the posterior maxillary plane and the neutral axis of the orbits, providing very limited support for Enlow’s (1982) claim that this region represents a fundamental anatomical interface (at least within Old World monkeys). Our analysis suggests that while there may be several relatively invariant structural relations within the skull, most of those previously discussed as representing evidence of pattern in primate-wide or mammal-wide comparisons are incorrect.     

Pattern in craniofacial biology: Evidence from the old world monkeys (Cercopithecidae)

An understanding of craniofacial growth, both evolutionarily and clinically, requires an investigation of pattern —geometric relations that remain relatively constant among growing structures or components of the skull. Several craniofacial biologists have suggested that specific morphological relations remain invariant during growth and in interspecific comparisons of adults of varying size. We tested the hypothesized invariance of a series of craniofacial angles in a sample of adult Old World monkeys. Fifteen angles were determined from lateral cranial radiographs. Criteria for examining angular invariance included tests for significant correlations and regression slopes with palatal length (overall skull size), tests for significant mean differences (ANOVAs) in angular values between the two subfamilies of Cercopithecidae — Cercopithecinae and Colobinae — and the computation and ranking of standard deviations (SDs) and coefficients of variation (CVs). Results indicate that most of the cranial angles purported to be invariant do not in fact meet the criteria for acceptance. One of the few cranial angles that evinces a somewhat constant value is that between the posterior maxillary plane and the neutral axis of the orbits, providing very limited support for Enlow’s (1982) claim that this region represents a fundamental anatomical interface (at least within Old World monkeys). Our analysis suggests that while there may be several relatively invariant structural relations within the skull, most of those previously discussed as representing evidence of pattern in primate-wide or mammal-wide comparisons are incorrect.     

The Developmental Basis of Quantitative Craniofacial Variation in Humans and Mice

The human skull is a complex and highly integrated structure that has long held the fascination of anthropologists and evolutionary biologists. Recent studies of the genetics of craniofacial variation reveal a very complex and multifactorial picture. These findings contrast with older ideas that posit much simpler developmental bases for variation in cranial morphology such as the growth of the brain or the growth of the chondrocranium relative to the dermatocranium. Such processes have been shown to have major effects on cranial morphology in mice. It is not known, however, whether they are relevant to explaining normal phenotypic variation in humans. To answer this question, we obtained vectors of shape change from mutant mouse models in which the developmental basis for the craniofacial phenotype is known to varying degrees, and compared these to a homologous dataset constructed from human crania obtained from a single population with a known genealogy. Our results show that the shape vectors associated with perturbations to chondrocranial growth, brain growth, and body size in mice do largely correspond to axes of covariation in humans. This finding supports the view that the developmental basis for craniofacial variation funnels down to a relatively small number of key developmental processes that are similar across mice and humans. Understanding these processes and how they influence craniofacial shape provides fundamental insights into the developmental basis for evolutionary change in the human skull as well as the developmental-genetic basis for normal phenotypic variation in craniofacial form.     

Visualizing patterns of craniofacial shape variation in Homo sapiens

The geometric morphometric analysis of shape variation in complex biological structures such as the human skull poses a number of specific challenges: the registration of homologous morphologies, the treatment of bilateral symmetry, the graphical representation of form variability in three dimensions and the interpretation of the results in terms of differential growth processes. To visualize complex patterns of shape change, we propose an alternative to classical Cartesian deformation grids in the style of D'Arcy W. Thompson. Reference to the surface structures of the organism under investigation permits a comprehensive visual grasp of shape change and its tentative interpretation in terms of differential growth. The application of this method to the analysis of human craniofacial shape variation reveals distinct modes of growth and development of the neurocranial and viscerocranial regions of the skull. Our data further indicate that variations in the orientation of the viscerocranium relative to the neurocranium impinge on the shapes of the face and the cranial vault.     

Shape of the craniofacial complex in 45,X females: cephalometric study

The shape of the craniofacial complex was analysed cephalometrically in sixty-four adult 45,X females (Turner syndrome) using lateral skull radiographs, and the subjects were compared with first-degree female relatives and control females. The results showed that 45,X females have marked changes in relatively few craniofacial areas compared to the controls. Most of the changes are located in the cranial base, so that the face is retrognathic. The mandible is short, whereas the maxilla is of normal length. The results support the view that the morphology of the cranial base is markedly affected in 45,X females, whereas most other craniofacial changes could be considered secondary to the cranial base abnormality. It is suggested that retarded cartilage growth may be a factor leading to the present findings.     

Growth of cranial synchondroses and sutures requires polycystin-1

In vertebrates, coordinated embryonic and postnatal growth of the craniofacial bones and the skull base is essential during the expansion of the rostrum and the brain. Identification of molecules that regulate skull growth is important for understanding the nature of craniofacial defects and for development of non-invasive biologically based diagnostics and therapies.Here we report on spatially restricted growth defects at the skull base and in craniofacial sutures of mice deficient for polycystin-1 (Pkd1). Mutant animals reveal a premature closure of both presphenoid and sphenooccipital synchondroses at the cranial base. Furthermore, knockout mice lacking Pkd1 in neural crest cells are characterized by impaired postnatal growth at the osteogenic fronts in craniofacial sutures that are subjected to tensile forces. Our data suggest that polycystin-1 is required for proliferation of subpopulations of cranial osteochondroprogenitor cells of both mesodermal and neural crest origin during skull growth. However, the Erk1/2 signalling pathway is up-regulated in the Pkd1-deficient skeletal tissue, similarly to that previously reported for polycystic kidney.     

Cephalometric analysis of the craniofacial region of the northern Foxe Basin Eskimo

Past investigations of the Eskimo have indicated that there are marked morphological differences in the craniofacial skeleton of this relatively isolated ethnic group compared to other ethnic and racial groups. This study, using cephalometric radiography, attempted to characterize the craniofacial phenotype of the Eskimo living in the northern Foxe Basin, Northwest Territories, Canada. Age changes were examined on a cross-sectional basis with comparisons being made with a Winnipeg Caucasian group. This investigation indicates that the Igloolik Eskimo has a phenotype, established early in life, and is distinct from the Winnipeg group. The overall size of the Eskimo craniofacial complex was significantly larger at three years of age and remained larger through the ages studied. Development of the craniofacial region, however, was fairly similar in rate and direction for both populations. The greatest differences between the Eskimo and Caucasian groups were found in the linear measurements assessing cranial width, facial width, mandibular length, facial height, protrusion of the incisors, chin point development, and nasal morphology. Differences between the two groups in the morphological relationships of the component structures include the angular relationships of the maxilla and nasal bones to the anterior cranial base, the gonial angle of the mandible, and the angle of facial convexity.     

Age differences in craniofacial dimensions among adults from Indian Knoll,Kentucky

Adult craniofacial expansion with aging has recently been documented in a living US white population sample (Israel, '73a, '77). The present study extends these findings to a prehistoric Amerindian skeletal sample from the Indian Knoll, Kentucky site. Sixteen craniofacial dimensions available for 136 adult males were compared in younger (20–34 years) and older (35–50 years) age groups. Of these, six dimensions showed a significant difference between age groups; all significantly different dimensions were larger in the older adult age group. The multivariate (T²) difference between age groups was highly significant. Comparison of results before and after a size standardization indicated that the majority of differences between age groups were associated with an overall size increase, or expansion with aging, and did not represent merely remodeling, or “shape” changes. The pattern of craniofacial change with age appeared generally similar to that observed in the modern US white sample; however, some differences were noted. It is shown that the age trends observed at Indian Knoll are most likely to reflect true craniofacial growth in size among the adult male inhabitants of the site, rather than secular trends or other artifacts of the sampling procedure. The causes for continuing adult craniofacial expansion are unknown, and probably involve a complex interaction of many factors. However, this pattern of change with age among adults does appear to be characteristic of population samples of widely differing genetic and environmental backgrounds.     

Atelencephalic microcephaly: craniofacial anatomy and morphologic comparisons with holoprosencephaly and anencephaly

This is the first detailed report of the craniofacial anatomy of atelencephaly. Comparisons were made with a control specimen and others with holoprosencephaly, anencephaly, and anencephaly with holoprosencephalic facial features. In the atelencephalic fetus, severe microcephaly, flattened calvaria, and partial synostosis of the metopic suture were apparent. The cranial fossae were much smaller than usual; lesser wings of the sphenoid were folded into a rounded basal mass. Facial features were pronounced, and orbits were hyperteloric, lowset, and rounded. Ethmoidal cartilages, nasal bones, and maxillary structures were distorted and elongated. The secondary palate was displaced inferiorly and cleft. Because major components of the craniofacial complex were generally present, although misshapen, changes in the atelencephalic skull seem to be deformations rather than malformations. Differences in the cranial morphology of associated disorders--holoprosencephaly and anencephaly--can be construed as aberrations of separate developmental fields. Relationships between atelencephaly and these fields are unclear.     

Masticatory function and post-pleistocene evolution in Nubia

The present research focuses on craniofacial variation in Nubia over approximately 10,000 years. Samples were grouped according to their temporal location and subsistence pattern, and represent a transition from a hunting-gathering adaptation (Mesolithic) to a transitional hunting-gathering-agricultural adaptation (A-C Group) and finally to a fully agricultural adaptation (Meroitic/X-Group/Christian). The purposes were: (1) to compare the Mesolithic sample with the later Nubian populations; and (2) to evaluate further the hypothesis that change in Nubian craniofacial morphology was due to changing functional demands associated with the progressive change in subsistence adaptation and associated behavior. The results tend to support recent views that the Nubian Mesolithic population is probably ancestral to later Nubian groups, and that the masticatory-functional hypothesis can best account for craniofacial change among the Nubians since 12,000 B.P. According to this hypothesis systematic reduction in functional demand placed on the masticatory complex from the Mesolithic led, secondarily, to an alteration of the growth of the maxillomandibular complex such that the face became progressively less robust and more inferoposteriorly located relative to the cranial vault. Both the increase in the height of the vault relative to its length, producing a more “globular” appearance, and the reduction in dental size were tertiary, compensatory responses to altered facial size and position.     

The influence of experimental deformation on craniofacial development in rats

Cranial deformation was produced experimentally in rats 8 to 40 days old for the purpose of studying the rotation of the craniofacial bones and the modification of the growth rates of the functional cranial components. One hundred and twenty four skulls (65 males and 59 females) were employed, classified as: deformed , deformed-hydrocephalic, sham-operated and controls. A midsagittal diagram was drawn for each skull and the angle subtended by each bone with respect to the vestibular plane was measured. Growth indices were worked out for both the neural skull and the facial skull. Deformation altered the rotation of the parietal, interparietal and basisphenoidal bones and restricted the rotation of the fronto-ethmo-facial complex. Alteration of the longitudinal growth rates of the dorsal and basilar components of the neurocranium and the splanchnocranium produced the persistence of the klinorynchal state.     

Postnatal growth of skull linear measurements of Cape Hare Lepus capensis in northern China: an analysis in an adaptive context

304 skulls of Cape hare (Lepus capensis) were collected from two climatically distinct localities in northern China. With eye lens weight as a continuous age variable, postnatal growth patterns of 25 cranial linear measurements in relation to sex, growth season and region were analysed to understand the morphological basis of life history adaptation. In almost all the skull measurements, no significant differences were found between either sex or growth seasons. Principal component analysis revealed that facial elements accounted for the greatest proportion of skull morphological variation. Von Bertalanffy function was applied to describe growth trajectories of the skull elements. Based on this model, the growth rates of skull elements and the age at which they reached a certain proportion (95%) of asymptotes were compared. The results showed that skull growth exhibited an allometric pattern, with neural components attaining their final size more rapidly (at about 2–3 months old in tympanic bulla and 4–6 months old in others) than did the facial, which continued to grow well into postnatal life (at 6–10 months old). The earlier establishment of neurocranial morphology was associated with a fully developed central nervous system, which may play a key role in improving the survival of animals during the early phase of life. There was a regional difference in developmental rate of the hare skull. For all the skull parameters, northern hares had a more rapid rate of cranial growth compared to the southern, i.e. skull elements of juveniles from northern population were relatively larger at comparable ages and achieved adult size 0.5–4.0 months earlier than those from the south. In adult hares, however, no significant regional differences in any of the skull parameters were present. Adaptive explanations for the regional difference in ontogenetic pattern of skull morphology include age‐specific thermoregulation constraint, season‐related food availability and age‐dependent predation pressure. Based on the findings of this study, it is suggested that the postnatal growing period represents a crucial time of life, and that improvement of survivorship when young by growth adaptation forms an important aspect of the hare's life history strategies. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 78 , 343–353.     

Development of craniofacial musculature in Monodelphis domestica (marsupialia,didelphidae)

Development of craniofacial muscles of Monodelphis domestica (Marsupialia, Didelphidae) is described. In a period of 4–6 days all craniofacial muscles in M. domestica progress from myoblast condensation, to striated myofibers that are aligned in the direction of adult muscles and possess multiple, lateral nuclei. This process begins 1 to 2 days before birth and continues during the first few days after birth. Compared to other aspects of cranial development, muscle development in M. domestica is rapid. This rapid and more or less simultaneous emergence of craniofacial muscles differs from the previously described pattern of development of the cranial skeleton in marsupials, which displays a mosaic of acceleration and deceleration of regions and individual elements. Unlike the skeletal system, craniofacial muscles show no evidence of regional specialization during development. M. domestica resembles eutherian mammals in the relatively rapid and more or less simultaneous differentiation of all craniofacial muscles. It differs from eutherian taxa in that most stages of myogenesis occur postnatally, following the onset of function. The timing of the development of muscular and skeletal structures is compared and it is concluded that the relatively early development of muscle is not reflected by any particular acceleration of the differentiation or growth of skeletal structures. Finally, the difficulties in accounting for complex internal arrangements of muscles such as the tongue, given current models of myogenesis are summarized. © 1994 Wiley-Liss, Inc.     

Cranial ontogeny of<Emphasis Type="Italic">Lutreolina crassicaudata</Emphasis> (Didelphidae): a comparison with<Emphasis Type="Italic">Didelphis albiventris</Emphasis>

Metatherians experience the greatest developmental changes during extrauterine life. Following previous studies onDidelphis albiventris Lund, 1840, we examined the postweaning cranial allometry of size of the Neotropical marsupialLutreolina crassicaudata (Desmerest, 1804). Our aim was to compare growth patterns of both species to identify traits particular to each species and traits common to both species. This may contribute toward identifying a common developmental plan for didelphids. We measured 15 cranial variables in 32–43 specimens from just-weaned young to old adult. Total length of the skull was the estimator of overall size in least squares and reduced major axis regressions. The skull ofLutreolina crassicaudata grows at a rate slower than the overall change in size in its neurocranial components, palate, and postcanine rows, and it grows relatively faster in the rest of the splanchnocranium. This pattern closely resembles that ofDidelphis albiventris, from which it differs mainly in the allometry of the muzzle. In both species, allometry explains most postweaning changes of the trophic apparatus on functional grounds, in relation to interspecific differences in diet. We hypothesize that most local allometric departures from a generalized didelphid plan would relate to main dietary trends.     

Cranial growth in the squirrel monkey (Saimiri sciureus): a quantitative analysis using three dimensional coordinate data.

Improvements in data gathering technology have made it possible to quickly and accurately digitize large numbers of objects. The three dimensional coordinates of 44 homologous landmarks were obtained from a sample of 104 squirrel monkey (Saimiri sciureus) crania. After sorting by sex, the crania were assigned to one of four dental age groups. Two quantitative methods, Euclidean distance matrix analysis (EDMA) and finite element scaling analysis (FESA), were used to study craniofacial form change during growth within each sex. Form differences between the sexes at each developmental age were also examined. Both sexes show a small amount of cranial growth overall; however, there are areas of substantial local growth. These areas include the anterior neurocranium and basicranium, the basioccipital, and the anterior palate. Sexual dimorphism in the craniofacial complex is minimal. The most dimorphic regions are the orbitonasal portion of the lower face, the cranial base, and the palate.     

Common mechanisms in development and disease: BMP signaling in craniofacial development

BMP signaling is one of the key pathways regulating craniofacial development. It is involved in the early patterning of the head, the development of cranial neural crest cells, and facial patterning. It regulates development of its mineralized structures, such as cranial bones, maxilla, mandible, palate, and teeth. Targeted mutations in the mouse have been instrumental to delineate the functional involvement of this signaling network in different aspects of craniofacial development. Gene polymorphisms and mutations in BMP pathway genes have been associated with various non-syndromic and syndromic human craniofacial malformations. The identification of intricate cellular interactions and underlying molecular pathways illustrate the importance of local fine-regulation of Bmp signaling to control proliferation, apoptosis, epithelial-mesenchymal interactions, and stem/progenitor differentiation during craniofacial development. Thus, BMP signaling contributes both to shape and functionality of our facial features. BMP signaling also regulates postnatal craniofacial growth and is associated with dental structures life-long. A more detailed understanding of BMP function in growth, homeostasis, and repair of postnatal craniofacial tissues will contribute to our ability to rationally manipulate this signaling network in the context of tissue engineering.