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.     

Linking form and function of the fibrous joints in the skull: a new quantification scheme for cranial sutures using the extant fish Polypterus endlicherii

The aim of this study is to connect specific sutural morphologies with the specific types of deformation they experience. To meet this goal, we quantified the morphologies of the interfrontal (IF), interparietal (IP), and frontoparietal (FP) sutures in the extant fish Polypterus endlicherii, and used our published measurements of in vivo deformation of these sutures during feeding to infer how suture morphology and function are connected. Specifically, we found that three relatively simple measures of cross-sectional suture complexity (i.e., the ratio of total sutural length to its shortest end-to-end length; amount of sutural overlap; and size of the largest interdigitation) can be used to distinguish between the IF, FP, and IP sutures, which exhibit very different cross-sectional shapes and responses to loading. Interestingly, these differences in cross-sectional morphology are not reflected by the linear traces of these sutures on the surface of the skull, implying that cross-sectional shape of a suture must be known to infer the loading conditions it experiences. Plotting the three cross-sectional metrics against one another to yield a sutural morphospace shows that the IF, IP, and FP sutures define regions that are largely distinct from one another. Our previous measurements of strain across these sutures suggested that the FP region would lie between the IF and IP regions; instead, the FP region is largely set apart from the other two fields. Based on this discovery, and on the locations of cranial muscles, we propose a new model of deformation in the skull of P. endlicherii during feeding, in which rotation parallel to the skull roof is combined with bending, subjecting the FP suture to complex shearing. Finally, although the sutures of P. endlicherii appear to be significantly less complex than those of mammals, these fish sutures show a similar range of morphologies and perform similar functions as do mammalian sutures.     

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.     

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.     

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.     

Characterization of craniofacial sutures using the finite element method

Characterizing the biomechanical behavior of sutures in the human craniofacial skeleton (CFS) is essential to understand the global impact of these articulations on load transmission, but is challenging due to the complexity of their interdigitated morphology, the multidirectional loading they are exposed to and the lack of well-defined suture material properties. This study aimed to quantify the impact of morphological features, direction of loading and suture material properties on the mechanical behavior of sutures and surrounding bone in the CFS. Thirty-six idealized finite element (FE) models were developed. One additional specimen-specific FE model was developed based on the morphology obtained from a µCT scan to represent the morphological complexity inherent in CFS sutures. Outcome variables of strain energy (SE) and von Mises stress (σ_vm) were evaluated to characterize the sutures’ biomechanical behavior. Loading direction was found to impact the relationship between SE and interdigitation index and yielded varied patterns of σ_vm in both the suture and surrounding bone. Adding bone connectivity reduced suture strain energy and altered the σ_vm distribution. Incorporating transversely isotropic material properties was found to reduce SE, but had little impact on stress patterns. High-resolution µCT scanning of the suture revealed a complex morphology with areas of high and low interdigitations. The specimen specific suture model results were reflective of SE absorption and σ_vm distribution patterns consistent with the simplified FE results. Suture mechanical behavior is impacted by morphologic factors (interdigitation and connectivity), which may be optimized for regional loading within the CFS.     

Temporal squama shape in fossil hominins: relationships to cranial shape and a determination of character polarity

In 1943, Weidenreich described the squamosal suture of Homo erectus as long, low, and simian in character and suggested that this morphology was dependent upon the correlation between the size of the calvarium and the face. Many researchers now consider this character to be diagnostic of H. erectus. The relationship between cranial size and shape and temporal squama morphology, however, is unclear, and several authors have called for detailed measurements of squamosal variation to be collected before any conclusions are drawn regarding the nature of the morphology observed in H. erectus. Thirteen fossil and extant taxa were examined to address two questions: 1) Are size and shape of the temporal squama correlated with cranial vault morphology? and 2) Is the H. erectus condition plesiomorphic? To answer these questions, measurements were collected and indices were calculated for squamosal suture height, length, and area in relation to metric variables describing cranial size and shape. A two‐dimensional morphometric study was also completed using High Resolution‐Polynomial Curve Fitting (HR‐PCF) to investigate correlations between curvature of the squamosal suture and curvature of the cranial vault. Results of both analyses indicate that squamosal suture form is related to cranial size and shape. Furthermore, the plesiomorphic condition of the squamosal suture for hominins was identified as high and moderately arched; this condition is retained in H. erectus and is distinct from the great ape condition. It is suggested that this similarity is the result of increased cranial length without a corresponding increase in cranial height. Am J Phys Anthropol, 2008. © 2008 Wiley‐Liss, Inc.     

Functional implications of squamosal suture size in paranthropus boisei

It has been hypothesized that the extensively overlapping temporal and parietal bones of the squamosal sutures in Paranthropus boisei are adaptations for withstanding loads associated with feeding. Finite element analysis (FEA) was used to investigate the biomechanical effects of suture size (i.e., the area of overlap between the temporal and parietal bones) on stress, strain energy, and strain ratio in the squamosal sutures of Pan troglodytes and P. boisei (specimen OH 5) during biting. Finite element models (FEMs) of OH 5 and a P. troglodytes cranium were constructed from CT scans. These models contain sutures that approximate the actual suture sizes preserved in both crania. The FEM of Pan was then modified to create two additional FEMs with squamosal sutures that are 50% smaller and 25% larger than those in the original model. Comparisons among the models test the effect of suture size on the structural integrity of the squamosal suture as the temporal squama and parietal bone move relative to each other during simulated premolar biting. Results indicate that with increasing suture size there is a decreased risk of suture failure, and that maximum stress values in the OH 5 suture were favorable compared to values in the Pan model with the normal suture size. Strain ratios suggest that shear is an important strain regime in the squamosal suture. This study is consistent with the hypothesis that larger sutures help reduce the likelihood of suture failure under high biting loads. Am J Phys Anthropol 153:260–268, 2014. © 2013 Wiley Periodicals, Inc.     

BMP9 induces osteogenesis and adipogenesis in the immortalized human cranial suture progenitors from the patent sutures of craniosynostosis patients

The cranial suture complex is a heterogeneous tissue consisting of osteogenic progenitor cells and mesenchymal stem cells (MSCs) from bone marrow and suture mesenchyme. The fusion of cranial sutures is a highly coordinated and tightly regulated process during development. Craniosynostosis is a congenital malformation caused by premature fusion of cranial sutures. While the progenitor cells derived from the cranial suture complex should prove valuable for studying the molecular mechanisms underlying suture development and pathogenic premature suture fusion, primary human cranial suture progenitors (SuPs) have limited life span and gradually lose osteoblastic ability over passages. To overcome technical challenges in maintaining sufficient and long‐term culture of SuPs for suture biology studies, we establish and characterize the reversibly immortalized human cranial suture progenitors (iSuPs). Using a reversible immortalization system expressing SV40 T flanked with FRT sites, we demonstrate that primary human suture progenitor cells derived from the patent sutures of craniosynostosis patients can be efficiently immortalized. The iSuPs maintain long‐term proliferative activity, express most of the consensus MSC markers and can differentiate into osteogenic and adipogenic lineages upon BMP9 stimulation in vitro and in vivo. The removal of SV40 T antigen by FLP recombinase results in a decrease in cell proliferation and an increase in the endogenous osteogenic and adipogenic capability in the iSuPs. Therefore, the iSuPs should be a valuable resource to study suture development, intramembranous ossification and the pathogenesis of craniosynostosis, as well as to explore cranial bone tissue engineering.     

Brief communication: Histology and micro CT as methods for assessment of facial suture patency

The extent of fusion in facial sutures has implications for topics ranging from biomechanics to phylogeny reconstruction. An unfortunate limitation of studying sutural fusion in skeletal specimens is that it is difficult to assess whether apparently patent sutures are in fact fused internally. Both histology and microcomputed tomography (CT) are potential tools for solving this, but relatively few studies have attempted to discern the limits of micro CT for visualization of microanatomical structures. We examined microanatomical aspects of facial sutures in adult cadaveric samples from captive bushbabies. Premaxillary and nasopremaxillary sutures were examined in serially sectioned snouts of four greater bushbabies (Otolemur garnettii) and four lesser bushbabies (Galago moholi). Sections containing sutures with osseous bridging were rated as “fused,” and the presence or absence of grooves on the external side was recorded. One bushbaby was studied using micro CT prior to physical sectioning. O. garnettii and two of the G. moholi show multiple foci of fusion. Histological examination confirmed that sutural fusion is limited to the internal surface in numerous sections, resulting in an external notch. Such points of internal fusion could be clearly visualized in raw CT slices. The presence of such notches suggests that external examination can underestimate the degree of suture fusion. Thus, microanatomical evidence may be needed to fully assess biomechanical correlates and phylogenetic interpretations based on fusion of facial sutures. Our results also indicate micro CT may be a useful tool to obtain this evidence. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

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.     

Cranial anatomy of Ignacius graybullianus and the affinities of the Plesiadapiformes

A nearly complete cranium of Ignacius graybullianus provides increased understanding of the cranial anatomy of Plesiadapiformes. In nearly all details of cranial anatomy, Ignacius differs markedly from primates. USNM 421608 exhibits a long tapering snout, small widely spaced orbits, and a complete lack of postorbital process or bar. Large olfactory bulbs are inferred from the wide interorbital space. The marked flare of the zygomatic arches suggests that Ignacius possessed large and powerful temporal muscles. The basicranial region is particularly well preserved and reveals a distinct suture between the petrosal bone and an entotympanic bulla. This suture is visible on both the left and right sides of the skull and dispels the hypothesis that Ignacius and, by inference, other Plesiadapiformes share the primate synapomorphy of a petrosal bulla. To test the phylogenetic position of Ignacius, cranial characters were identified and scored for Ignacius, Plesiadapis, Cynocephalus, and a number of primates, bats, and scandentians. Two erinaceomorph insectivores were also included to allow the assessment of archontan monophyly. These characters were incorporated into a maximum-parsimony analysis to determine the phylogenetic position of Plesiadapiformes. There are several important phylogenetic conclusions that can be inferred from this analysis: 1) Ignacius and Plesiadapis make up a monophyletic clade; 2) Plesiadapiformes may be the sister group of Dermoptera; 3) Scandentia, not Plesiadapiformes, is the sister group of Primates; and 4) Primates, plesiadapiforms, bats, colugos, and scandentians may not form a monophyletic clade Archonta. Consequently, the taxon Archonta is in need of review. © 1992 Wiley-Liss, Inc.     

Do extraordinarily high growth rates in Permo‐Triassic dicynodonts (Therapsida,Anomodontia) explain their success before and after the end‐Permian extinction?

Dicynodonts were the most diverse and abundant herbivorous therapsids of the Permo‐Triassic. They include Lystrosaurus, one of the few taxa known to survive the end‐Permian extinction and the most abundant tetrapod during the Early Triassic postextinction recovery. Explanations for the success of Lystrosaurus and other dicynodonts remain controversial. This study presents an assessment of dicynodont growth patterns using bone histology, with special focus on taxa associated with the end‐Permian extinction event. Bone histological analysis reveals a high cortical thickness throughout the clade, perhaps reflecting a phylogenetic constraint. Growth rings are absent early in ontogeny, and combined with high vascular density, indicate rapid, sustained growth up to the subadult stage. Extraordinarily enlarged vascular channels are present in the midcortex of many dicynodonts, including adults, and may have facilitated a more efficient assimilation of nutrients and rapid bone growth compared to other therapsids. Both increased channel density and enlarged vascular channels evolved at or near the base of major radiations of dicynodonts, implying that the changes in growth and life history they represent may have been key to the success of dicynodonts. Furthermore, this exceptionally rapid growth to adulthood may have contributed to the survival of Lystrosaurus during the end‐Permian extinction and its dominance during the postextinction recovery period. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 160 , 341–365.     

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.     

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.     

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.     

Power scaling of ammonitic suture patterns from Cretaceous Ancyloceratina: constraints on septal/sutural complexity

The spatial scaling of 77 hemisutures from 65 species of Cretaceous heteromorphic ammonites was quantified with the fractal box‐counting method. Fractal dimensions within Baculites compressus did not significantly differ between adult hemisutures; however, the juvenile suture of this species did exhibit a significantly lower fractal dimension. This suggests that variation in sutural complexity between explicitly adult ontogenetic stages may not contribute to significant noise in comparisons between other species/morphotypes. High‐spired, three‐dimensionally coiled heteromorphs with a larger degree of septal asymmetry exhibit higher fractal dimensions in outer whorl hemisutures than inner whorl hemisutures due to their elongation and improved space occupation over a larger whorl surface. Three‐dimensionally coiled ammonites also have higher fractal dimensions on average (mean D_b = 1.45) with respect to their 2‐D coiled counterparts (mean D_b = 1.38). All ammonites in this study exhibit a positive trend between sutural complexity and shell size (proxied by whorl height). These relationships suggest that septal frilling is constrained by shell morphology and whorl section geometry during septal morphogenesis. This, in turn, influences the scaling, space‐filling properties and scaling limits of ammonitic suture patterns. Sutural/septal complexity is also found to positively influence the amount of liquid retained in marginal septal recesses. However, as these septa approach larger scales, less cameral liquid is retained per septal mass. This may further explain the positive relationship between sutural complexity and shell size.