Mechanics of cranial sutures using the finite element method

To investigate how cranial suture morphology and the arrangement of sutural collagen fibres respond to compressive and tensile loads, an idealised bone–suture–bone complex was analysed using a two-dimensional finite element model. Three suture morphologies were simulated with an increasing interdigitation index (I.I.): butt-ended, moderate interdigitated, and complex interdigitated. The collagen matrix within all sutures was modelled as an isotropic material, and as an orthotropic material in the interdigitated sutures with fibre alignment as reported in studies of miniature pigs. Static uniform compressive or tensile loading was applied to the complex. In interdigitated sutures with isotropic material properties, the orientation of the maximum (tensile) principal stresses within the suture matched the collagen fibre orientation observed in compressed and tensed sutures of miniature pigs. This suggests that randomly arranged sutural collagen fibres could optimise to an orientation most appropriate to withstand the predominant type of loading. A compression-resistant fibre arrangement imparted the highest suture strain energy relative to the isotropic and tension-resistant arrangements, indicating that this configuration maximises energy storage. A comparison across the different suture morphologies indicated that bone strain energy generally decreased with a decrease in I.I., irrespective of the sutural fibre arrangement. However, high bone stress at the interdigitation apices shifted to the limbs of the suture with an increase in I.I. These combined findings highlight the importance of suture morphology and anisotropy as properties having a significant influence on sutural mechanics.     

Strain accommodation in the zygomatic arch of the pig: A validation study using digital speckle pattern interferometry and finite element analysis

It has been repeatedly suggested that mammalian cranial sutures act not only to allow growth but also to reduce the levels of strain experienced by the skull during feeding. However, because of the added complexity they introduce, sutures are rarely included in finite element (FE) models, despite their potential to influence strain results. Because sutures present different morphologies and with differing degrees of internal fusion, many different methods of modeling may be necessary to accurately measure strain environments. Alternatively, these variables may exert very little influence on the scale of a whole‐skull model. To validate suture modeling methods, four alternative ways of including a suture in 3D FE models of the pig zygomatic arch were considered and compared with ex vivo experimental data from digital speckle pattern interferometry (DSPI). The use of DSPI rather than traditional strain gauge techniques allows strain gradients around the suture as well as the motions of the two bones to be observed. Results show that the introduction of 3D elements assigned more compliant material properties than the surrounding bone, is the most effective way of modeling both morphologies of suture, both in tension and compression. However, models containing no suture are almost indistinguishable from these compliant suture models, beyond the high strain gradient immediately adjacent to the suture. Conversely, modeling the suture as an open break in the mesh, or with spring elements assigned suture properties, fails to reproduce the experiment. Thus, although a solid but flexible model of sutures is preferred, the similarity between these models and those without sutures tentatively suggests that such extra detail may be unnecessary in pigs if the behavior of the whole skull is of interest. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

Calvarial suture interdigitation in hadrosaurids (Ornithischia: Ornithopoda): Perspectives through ontogeny and evolution

Lambeosaurine hadrosaurids exhibited extreme modifications to the skull, where the premaxillae, nasals, and prefrontals were modified to form their iconic supracranial crests. This morphology contrasts with their sister group, Hadrosaurinae, which possessed the plesiomorphic arrangement of bones. Although studies have discussed differences between lambeosaurine and hadrosaurine skull morphology and ontogeny, there is little information detailing suture modifications through ontogeny and evolution. Suture morphology is of particular interest due to its correlation with the mechanical loading of the skull in extant vertebrates. We quantify and contrast the morphology of calvarial sutures in iguanodontians and ontogenetic series of Corythosaurus and Gryposaurus to test whether the evolution of lambeosaurine crests impacted the mechanical loading of the skull. We found that suture interdigitation (SI) increases through ontogeny in hadrosaurids, although this increase is more extreme in Corythosaurus than Gryposaurus, and overall suture complexity (i.e., overall shape) remained constant. Lambeosaurines also have higher SI than other iguanodontians, even in crestless juveniles, suggesting that increased sinuosity is unrelated to the structural support of the crest. Hadrosaurines and basal iguanodontians did not differ. Similarly, lambeosaurines have more complexly shaped sutures than hadrosaurines and basal iguanodontians, while the latter two groups do not differ. Taken together, these results suggest that lambeosaurine calvarial sutures are more interdigitated than other iguanodontians, and although suture sinuosity increased through ontogeny, the suture shape remained constant. These ontogenetic and evolutionary patterns suggest that increased suture complexity in lambeosaurines coincided with crest evolution, and corresponding modifications to their facial skeleton altered the distribution of stress while feeding.     

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.     

A Phylogenetic Study of Late Growth Events in a Mammalian Evolutionary Radiation—The Cranial Sutures of Terrestrial Artiodactyl Mammals

We recorded the relative timing of fusion of 29 ectocranial sutures in 480 skulls belonging to 35 extant and four fossil species from all major clades of terrestrial artiodactyls. The resulting data were studied in a phylogenetic context, using mapping of event-pairing of suture fusion events and Parsimov. As phylogenetic framework we generated a compound phylogeny from several previously published analyses. Overall suture closure per species ranged from five to all 29 sutures in Hexaprotodon. All living non-ruminants (suids, camelids, and hippopotamids) fuse more than 50% of the studied sutures (most over 75%), whereas in almost all ruminants less than 50% of the sutures fuse completely. Phylogenetic regression found a significant correlation between suture closure and body mass. In all species we observed an early fusion of the sutures surrounding the foramen magnum (Exoccipital-Supraoccipital, Exoccipital-Basioccipital), a consistent scheme also among other mammals. Scaling the number of changes to the number of sutures in each of the usually recognized skull modules reveals relatively equal numbers of changes in the cranial vault, the zygomatic-sphenoid region, the orbit, and the anterior oral-nasal region. Only the basicranium shows a much smaller number in terms of absolute and relative amount of suture fusion change. Some species show a unique pattern of suture fusion, such as the early fusion of many sutures in the palatal region in Pecari or that of premaxillary sutures in †Cainotherium, perhaps related to feeding mode. A strategy to strengthen the skull by obliterating the sutures could explain the pattern of increased sutural fusion in ruminant species with large cranial appendages.     

Craniofacial sutures: morphology, growth, and in vivo masticatory strains.

The growth and morphology of craniofacial sutures are thought to reflect their functional environment. However, little is known about in vivo sutural mechanics. The present study investigates the strains experienced by the internasal, nasofrontal, and anterior interfrontal sutures during masticatory activity in 4-6-month-old miniature swine (Sus scrofa). Measurements of the bony/fibrous arrangements and growth rates of these sutures were then examined in the context of their mechanical environment. Large tensile strains were measured in the interfrontal suture (1,036 microepsilon +/- 400 SD), whereas the posterior internasal suture was under moderate compression (-440 microepsilon +/- 238) and the nasofrontal suture experienced large compression (-1,583 microepsilon +/- 506). Sutural interdigitation was associated with compressive strain. The collagen fibers of the internasal and interfrontal sutures were clearly arranged to resist compression and tension, respectively, whereas those of the nasofrontal suture could not be readily characterized as either compression or tension resisting. The average linear rate of growth over a 1-week period at the nasofrontal suture (133.8 micrometer, +/- 50.9 S.D) was significantly greater than that of both the internasal and interfrontal sutures (39.2 micrometer +/- 11.4 and 65. 5 micrometer +/- 14.0, respectively). Histological observations suggest that the nasofrontal suture contains chondroid tissue, which may explain the unexpected combination of high compressive loading and rapid growth in this suture.     

Assessment of the role of sutures in a lizard skull: a computer modelling study

Sutures form an integral part of the functioning skull, but their role has long been debated among vertebrate morphologists and palaeontologists. Furthermore, the relationship between typical skull sutures, and those involved in cranial kinesis, is poorly understood. In a series of computational modelling studies, complex loading conditions obtained through multibody dynamics analysis were imposed on a finite element model of the skull of Uromastyx hardwickii, an akinetic herbivorous lizard. A finite element analysis (FEA) of a skull with no sutures revealed higher patterns of strain in regions where cranial sutures are located in the skull. From these findings, FEAs were performed on skulls with sutures (individual and groups of sutures) to investigate their role and function more thoroughly. Our results showed that individual sutures relieved strain locally, but only at the expense of elevated strain in other regions of the skull. These findings provide an insight into the behaviour of sutures and show how they are adapted to work together to distribute strain around the skull. Premature fusion of one suture could therefore lead to increased abnormal loading on other regions of the skull causing irregular bone growth and deformities. This detailed investigation also revealed that the frontal-parietal suture of the Uromastyx skull played a substantial role in relieving strain compared with the other sutures. This raises questions about the original role of mesokinesis in squamate evolution.     

Fusion Patterns in the Skulls of Modern Archosaurs Reveal That Sutures Are Ambiguous Maturity Indicators for the Dinosauria

The sutures of the skulls of vertebrates are generally open early in life and slowly close as maturity is attained. The assumption that all vertebrates follow this pattern of progressive sutural closure has been used to assess maturity in the fossil remains of non-avian dinosaurs. Here, we test this assumption in two members of the Extant Phylogenetic Bracket of the Dinosauria, the emu, Dromaius novaehollandiae and the American alligator, Alligator mississippiensis, by investigating the sequence and timing of sutural fusion in their skulls. As expected, almost all the sutures in the emu skull progressively close (i.e., they get narrower) and then obliterate during ontogeny. However, in the American alligator, only two sutures out of 36 obliterate completely and they do so during embryonic development. Surprisingly, as maturity progresses, many sutures of alligators become wider in large individuals compared to younger, smaller individuals. Histological and histomorphometric analyses on two sutures and one synchondrosis in an ontogenetic series of American alligator confirmed our morphological observations. This pattern of sutural widening might reflect feeding biomechanics and dietary changes through ontogeny. Our findings show that progressive sutural closure is not always observed in extant archosaurs, and therefore suggest that cranial sutural fusion is an ambiguous proxy for assessing maturity in non-avian dinosaurs.     

Mechanical properties of cranial sutures

Many bones in mammalian skulls are linked together by cranial sutures, connective tissue joints that are morphologically variable and show different levels of interdigitation among and within species. The goal of this investigation was to determine whether sections of skull with cranial sutures have different mechanical properties than adjacent sections without sutures, and if these properties are enhanced with increased interdigitation. To test these hypotheses, bending strength and impact energy absorption were measured for samples of goat (Capra hircus) cranial bone without sutures and with sutures of different degrees of interdigitation. Bending strength was measured under both dynamic (9.7 mm displacement s-1) and relatively static (0.8 mm s-1) conditions, and at either speed, increased sutural interdigitation provided increased strength during three-point bending. However, except for very highly interdigitated sutures loaded slowly, sutures were not as strong in bending as bone. In contrast, sutures absorbed from 16% to 100% more energy per unit volume during impact loading than did bone. This five-fold increase in energy absorption by the sutures was significantly correlated with increased sutural interdigitation.     

In vivo strain in cranial sutures: the zygomatic arch.

Although cranial sutures presumably play a role in absorbing and/or transmitting loads applied to the skull, loading patterns on facial sutures are poorly understood. The zygomatic arch provides a comparatively isolated mechanical part of the skull containing a single suture, the zygomatico-squamosal. In pigs the zygomatico-squamosal suture has a short vertical segment located within the postorbital process and a longer horizontal segment which extends posteriorly. In anesthetized pigs single-element high-elongation strain gages were bonded over both segments of the suture. Strain was recorded during stimulation of the masseter muscles and while the lightly anesthetized animals masticated food pellets. The predominant strain patterns differed in the two segments of the suture. During mastication compressive strains predominated in the vertical segment, but tensile strains predominated in the horizontal segment. The same patterns were also produced by stimulation of the ipsilateral masseter muscle. Contraction of the contralateral masseter reversed the strain pattern, but strain levels were low and during mastication such reversals occurred only transiently. The two segments of the suture have contrasting morphologies. The vertical segment has broad, interdigitating contacts with fibers arranged in a compression-resisting orientation. The horizontal segment has a simple tongue and groove structure with fibers arranged to resist tension. Thus, the structure of the suture reflects the predominant strain pattern.     

Adenovirus-mediated transmission of a dominant negative transforming growth factor-beta receptor inhibits in vitro mouse cranial suture fusion

Recent studies have implicated the transforming growth factor (TGF)-beta family in the regulation of pathological sporadic cranial suture fusion. In addition, these studies have shown that TGF-beta is highly expressed by the dura mater underlying fusing murine cranial sutures. The purpose of the present experiments was to analyze the effects of disrupting TGF-beta signaling during programmed mouse cranial suture fusion. Using recombinant DNA technology, a replication-deficient adenovirus encoding a defective TGF-beta receptor (Ad.DN-TbetaRII) capable of blocking TGF-beta biological activity was constructed. Mouse posterior frontal sutures were harvested before the initiation of suture fusion (postnatal day 25), and the dura mater underlying the suture was infected with vehicle, Ad.DN-TbetaRII, or control virus (Ad.LacZ; n = 10 each). Sutures were cultured for 14 or 30 days in an organ culture system and analyzed macroscopically and histologically.X-gal staining of Ad.LacZ-infected sutures 14 days after culture revealed strong staining of cells localized to the dura mater. Macroscopic analysis revealed complete sutural fusion in vehicle and Ad.LacZ-infected sutures. In contrast, Ad.DN-TBRII-infected sutures demonstrated nearly complete patency. Histological analysis confirmed our macroscopic observations with sutural fusion in 81.3 +/- 10 percent and 74.5 +/- 9 percent of vehicle and Ad.LacZ-infected sutures, respectively, versus 38.1 +/- 12 percent (p < 0.001) in Ad.DN-TbetaRII-infected sutures. In addition, transfection with the Ad.DN-TbetaRII virus resulted in a significant attenuation of anterior-to-posterior suture fusion, with the majority of fused sections localized to anterior sections. These data strongly implicate TGF-beta biological activity in the dura mater underlying the posterior frontal suture in the regulation of programmed sutural fusion. In addition, this study demonstrates the utility of adenovirus-mediated gene transfer in preventing programmed sutural fusion.     

The sutural pattern of skull-roof bones in Lower Permian Discosauriscus austriacus from Moravia

Sutures between ornamented bones of Discosauriscus austriacus are mostly simple, but there are also more complicated, rarely serrated, sutures between some bones. In small individuals, the sutures are simple, but the same sutures also occur in the largest specimens. The character of the sutures and the incomplete ossification of bones around the pineal foramen indicate the larva type of organization of Discosauriscus The fenestra between premaxillaries and nasals appears to be absent. In the majority of specimens, a squamosal-intertemporal sutural contact is present, althought it is sometimes reduced and in a few cases interrupted by a postorbital and supratemporal contact Therefore the character 'intertemporal-squamosal suture present or absent' cannot be used in this rigorous sense for testing the relationships of early tetrapods. The configuration of the suture between both parietals in osteolepiforms, Discosauriscus , and various early amphibians and reptiles indicates that the bones enclosing the pineal foramen in osteolepifonns are frontals. *** D iscosauriscus . Seymouriamorpha, Lower Permian tetrapod, skull exoskeleton, sutures.     

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.     

Sutural complexity in artificially deformed human (Homo sapiens) crania.

The pattern of complexity of cranial sutures is highly variable both among and within species. Intentional cranial vault deformation in human populations provides a controlled natural experiment by which we were able to quantify aspects of sutural complexity and examine the relationship between sutural patterns and mechanical loading. Measures of sutural complexity (interdigitation, number, and size of sutural bones) were quantified from digitized tracings of 13 sutures and compared among three groups of crania (n = 70) from pre-European contact Peru. These groups represent sample populations deformed in 1) anteroposterior (AP) and 2) circumferential (C) directions and 3) an undeformed population. Intergroup comparisons show few differences in degree or asymmetry of sutural interdigitation. In the few comparisons which show differences, the C group is always more interdigitated than the other two while the AP group has more sutural bones. The sutures surrounding the temporal bone (sphenotemporal, occipitotemporal, and temporoparietal) most frequently show significant differences among groups. These differences are related to the more extreme binding of C type deformation and are consistent with hypothesized increases in tension at coronally oriented sutures in this group. The larger number of sutural bones in the AP group is consistent with the general broadening of the cranium in this group and with experimental evidence indicating the development of ossicles in areas of tension. We suggest that so few changes in sutural complexity occurred either because the magnitude of the growth vectors, unlike their direction, is not substantially altered or because mechanisms other than sutural growth modification are responsible for producing the altered vault shapes. In addition, the presence of fontanelles in the infant skulls during binding and the static nature of the binding may have contributed to the similarity in complexity among groups.     

Comparative morphology and functional interpretation of the sutures in the dermal skull roof of temnospondyl amphibians

Sutures in the dermal skull roof of several Palaeozoic temnospondyl amphibians were studied, including Archegosaurus decheni, Sclerocephalus haeuseri, Cheliderpeton latirostre (Archegosauridae), Acanthostomatops vorax (Zatrachydidae), Onchiodon labyrinthicus (Eryopidae), Micromelerpeton credneri and Branchierpeton amblystomum (Dissorophoidea). Lamellae, flat bevels, butt joints, steep walls, and grooves are the sutural types occurring. Morphological sutural differences cannot be used as taxonomically relevant characters, as they mainly differ in their functional manifestations. Similarities of sutural patterns in taxa not closely related are most probably based on convergence, therefore sutural morphology allows functional conclusions rather than revealing phylogenetic relationships. The basic sutural pattern is described in Micromelerpeton credneri. Different textures and obliquity patterns of the sutural surfaces are characteristic of each region of the skull roof. In all temnospondyls studied, the median plane and the margin of the skull roof show a nearly uniform sutural morphology; the circumorbital region is most complex. Although the skulls studied are akinetic, mesokinetic movements of dermal elements along their sutures must have been permitted to guarantee the dynamic stability of the skull construction.     

Evaluation of cranial bone suture autotransplants in the growing rabbit

A coronal bone suture segment was autotransplanted into an experimentally created defect in the nongrowing portion of the nasal bone in 12 5-week-old male New Zealand white rabbits. The animals were sacrificed 90 days postoperatively. In most specimens the transplants were well incorporated into the recipient site. The transplanted sutures appeared narrower radiographically, and the bony projections of the sutures were not as long as those seen in control sutures. In each case the transplanted sutural ligament had atrophied, and six of the transplants showed bony union across the sutural space. The results suggest that growth and biomechanical stresses are important for maintenance of the sutural ligament and for the stimulation of bone deposition.     

The effects of morphological irregularity on the mechanical behavior of interdigitated biological sutures under tension

Irregular interdigitated morphology is prevalent in biological sutures in nature. Suture complexity index has long been recognized as the most important morphological parameter to govern the mechanical properties of biological sutures. However, the suture complexity index alone does not reflect all aspects of suture morphology. The goal of this investigation was to determine that besides suture complexity index, whether the degree of morphological irregularity of biological sutures has influences on the mechanical properties, and if there is any, how to quantify these influences. To explore these issues, theoretical and finite element (FE) suture models with the same suture complexity index but different levels of morphological irregularity were developed. The quasi-static stiffness, strength for damage initiation and post-failure process of irregular sutures were studied. It was shown that for the same suture complexity index, when the level of morphological irregularity increases, the overall strain to failure will increase while tensile stiffness is retained; also, the total energy to fracture increases with a sacrifice in strength to damage initiation. These results reveal that morphological irregularity is another important independent parameter to govern and balance the mechanical properties of biological sutures. Therefore, from the mechanics point of view, the prevalence of irregular suture morphology in nature is a merit, not a defect.     

The importance of craniofacial sutures in biomechanical finite element models of the domestic pig

Craniofacial sutures are a ubiquitous feature of the vertebrate skull. Previous experimental work has shown that bone strain magnitudes and orientations often vary when moving from one bone to another, across a craniofacial suture. This has led to the hypothesis that craniofacial sutures act to modify the strain environment of the skull, possibly as a mode of dissipating high stresses generated during feeding or impact. This study tests the hypothesis that the introduction of craniofacial sutures into finite element (FE) models of a modern domestic pig skull would improve model accuracy compared to a model without sutures. This allowed the mechanical effects of sutures to be assessed in isolation from other confounding variables. These models were also validated against strain gauge data collected from the same specimen ex vivo. The experimental strain data showed notable strain differences between adjacent bones, but this effect was generally not observed in either model. It was found that the inclusion of sutures in finite element models affected strain magnitudes, ratios, orientations and contour patterns, yet contrary to expectations, this did not improve the fit of the model to the experimental data, but resulted in a model that was less accurate. It is demonstrated that the presence or absence of sutures alone is not responsible for the inaccuracies in model strain, and is suggested that variations in local bone material properties, which were not accounted for by the FE models, could instead be responsible for the pattern of results.