Functional cues in the development of osseous tooth support in the pig, Sus scrofa

Alveolar bone supports teeth during chewing through a ligamentous interface with tooth roots. Although tooth loads are presumed to direct the development and adaptation of these tissues, strain distribution in the alveolar bone at different stages of tooth eruption and periodontal development is unknown. This study investigates the biomechanical effects of tooth loading on developing alveolar bone as a tooth erupts into occlusion. Mandibular segments from miniature pigs, Sus scrofa, containing M₁ either erupting or in functional occlusion, were loaded in compression. Simultaneous recordings were made from rosette strain gages affixed to the lingual alveolar bone and the M₂ crypt. Overall, specimens with erupting M₁s were more deformable than specimens with occluding M₁s (mean stiffness of 246 vs. 944 MPa, respectively, p=0.004). The major difference in alveolar strain between the two stages was in orientation. The vertically applied compressive loads were more directly reflected in the alveolar bone strains of erupting M₁s, than those of occluding M₁s, presumably because of the mediation of a more mature periodontal ligament (PDL) in the latter. The PDL interface between occluding teeth and alveolar bone is likely to stiffen the system, allowing transmission of occlusal loads. Alveolar strains may provide a stimulus for bone growth in the alveolar process and crest.     

The Biomechanical Function of Periodontal Ligament Fibres in Orthodontic Tooth Movement

Orthodontic tooth movement occurs as a result of resorption and formation of the alveolar bone due to an applied load, but the stimulus responsible for triggering orthodontic tooth movement remains the subject of debate. It has been suggested that the periodontal ligament (PDL) plays a key role. However, the mechanical function of the PDL in orthodontic tooth movement is not well understood as most mechanical models of the PDL to date have ignored the fibrous structure of the PDL. In this study we use finite element (FE) analysis to investigate the strains in the alveolar bone due to occlusal and orthodontic loads when PDL is modelled as a fibrous structure as compared to modelling PDL as a layer of solid material. The results show that the tension-only nature of the fibres essentially suspends the tooth in the tooth socket and their inclusion in FE models makes a significant difference to both the magnitude and distribution of strains produced in the surrounding bone. The results indicate that the PDL fibres have a very important role in load transfer between the teeth and alveolar bone and should be considered in FE studies investigating the biomechanics of orthodontic tooth movement.     

The effects of modeling simplifications on craniofacial finite element models: the alveoli (tooth sockets) and periodontal ligaments

Several finite element models of a primate cranium were used to investigate the biomechanical effects of the tooth sockets and the material behavior of the periodontal ligament (PDL) on stress and strain patterns associated with feeding. For examining the effect of tooth sockets, the unloaded sockets were modeled as devoid of teeth and PDL, filled with teeth and PDLs, or simply filled with cortical bone. The third premolar on the left side of the cranium was loaded and the PDL was treated as an isotropic, linear elastic material using published values for Young's modulus and Poisson's ratio. The remaining models, along with one of the socket models, were used to determine the effect of the PDL's material behavior on stress and strain distributions under static premolar biting and dynamic tooth loading conditions. Two models (one static and the other dynamic) treated the PDL as cortical bone. The other two models treated it as a ligament with isotropic, linear elastic material properties. Two models treated the PDL as a ligament with hyperelastic properties, and the other two as a ligament with viscoelastic properties. Both behaviors were defined using published stress-strain data obtained from in vitro experiments on porcine ligament specimens. Von Mises stress and strain contour plots indicate that the effects of the sockets and PDL material behavior are local. Results from this study suggest that modeling the sockets and the PDL in finite element analyses of skulls is project dependent and can be ignored if values of stress and strain within the alveolar region are not required.     

Strain-dependent up-regulation of ephrin-B2 protein in periodontal ligament fibroblasts contributes to osteogenesis during tooth movement

During orthodontic tooth movement, the application of adequate orthodontic forces allows teeth to be moved through the alveolar bone. These forces are transmitted through the periodontal ligaments (PDL) to the supporting alveolar bone and lead to deposition or resorption of bone, depending on whether the tissues are exposed to a tensile or compressive mechanical strain. Fibroblasts within the PDL (PDLF) are considered to be mechanoresponsive. The transduction mechanisms from mechanical loading of the PDLF to the initiation of bone remodeling are not clearly understood. Recently, members of the ephrin/Eph family have been shown to be involved in the regulation of bone homeostasis. For the first time, we demonstrate that PDLF exposed to tensile strain induce the expression of ephrin-B2 via a FAK-, Ras-, ERK1/2-, and SP1-dependent pathway. Osteoblasts of the alveolar bone stimulated with ephrin-B2 increased their osteoblastogenic gene expression and showed functional signs of osteoblastic differentiation. In a physiological setting, ephrin-B2-EphB4 signaling between PDLF and osteoblasts of the alveolar bone might contribute to osteogenesis at tension sites during orthodontic tooth movement.     

The effects of the periodontal ligament on mandibular stiffness: a study combining finite element analysis and geometric morphometrics

It is generally accepted that the periodontal ligament (PDL) plays a crucial role in transferring occlusal forces from the teeth to the alveolar bone. Studies using finite element analysis (FEA) have helped to better understand this role and show that the stresses and strains in the alveolar bone are influenced by whether and how PDL is included in FE models. However, when the overall distribution of stresses and strains in crania and mandibles are of interest, PDL is often not included in FE models, although little is known about how this affects the results. Here we study the effect of representing PDL as a layer of solid material with isotropic homogeneous properties in an FE model of a human mandible using a novel application of geometric morphometrics. The results show that the modelling of the PDL affects the deformation and thus strain magnitudes not only of the alveolar bone around the biting tooth, but that the whole mandible deforms differently under load. As a result, the strain in the mandibular corpus is significantly increased when PDL is included, while the strain in the bone beneath the biting tooth is reduced. These results indicate the importance of the PDL in FE studies. Thus we recommend that the PDL should be included in FE models of the masticatory apparatus, with tests to assess the sensitivity of the results to changes in the Young's modulus of the PDL material.     

Tooth periodontal ligament: Direct 3D microCT visualization of the collagen network and how the network changes when the tooth is loaded

The periodontal ligament (PDL), a soft tissue connecting the tooth and the bone, is essential for tooth movement, bone remodeling and force dissipation. A collagenous network that connects the tooth root surface to the alveolar jaw bone is one of the major components of the PDL. The organization of the collagenous component and how it changes under load is still poorly understood. Here using a state-of-the-art custom-made loading apparatus and a humidified environment inside a microCT, we visualize the PDL collagenous network of a fresh rat molar in 3D at 1 μm voxel size without any fixation or contrasting agents. We demonstrate that the PDL collagen network is organized in sheets. The spaces between sheets vary thus creating dense and sparse networks. Upon vertical loading, the sheets in both networks are stretched into well aligned arrays. The sparse network is located mainly in areas which undergo compressive loading as the tooth moves towards the bone, whereas the dense network functions mostly in tension as the tooth moves further from the bone. This new visualization method can be used to study other non-mineralized or partially mineralized tissues, and in particular those that are subjected to mechanical loads. The method will also be valuable for characterizing diseased tissues, as well as better understanding the phenotypic expressions of genetic mutants.     

Mechanical Response of Bone under Short-term Loading of a Dental Implant with an Internal Layer Simulating the Nonlinear Behaviour of the Periodontal Ligament

We consider a non-standard design for a fixed dental implant, incorporating a soft layer which simulates the presence of the periodontal ligament (PDL). Instead of being aimed at causing an a priori defined stress/strain field within the surrounding bone, upon loading, such a design simply tries to better reproduce the natural tooth–PDL configuration. To do this, the mechanical properties of the internal layer match those of the PDL, determined experimentally to be strongly nonlinear. Three-dimensional finite element analyses show that the presence of such a layer produces (i) a prosthesis mobility very similar to that of a healthy tooth, for several loading conditions, and (ii) a stress/strain distribution substantially different from that arising, upon loading, around a conventional implant. The lack of knowledge of the real mechanical fields existing, under loading, in the bone around a healthy tooth makes it very difficult to state that the stress distribution produced by the modified implant is “better” than that produced by the standard one. Nevertheless, the comparison of the results obtained here, with those of previous refined analyses of the tooth–PDL–bone system, indicates that the modified implant tends to produce a stress distribution in the bone, upon loading, closer to “natural” than that given by the standard one, within the limits imposed by the presence of threads coupling the implant with the bone.     

Tooth movements are guided by specific contact areas between the tooth root and the jaw bone: A dynamic 3D microCT study of the rat molar

Teeth sustain high loads over a lifetime and yet intact tooth failure is rare. The different structures of the tooth, jaw bone and the intervening soft periodontal ligament enable the tooth to endure repeated loading during mastication. Although mechanical and functional properties of the different components are thoroughly investigated, the manner in which the whole tooth functions under load is still enigmatic. A custom-made loading system inside a microCT scanner was used to directly visualize the root movements in relation to the jaw bone as the rat molar tooth was loaded. At low loads no contact was observed between the root surface and the bone, whereas at higher loads three specific contact areas between the root surface and the jaw bone were observed. These contact areas restrict tooth movement in the buccal-lingual direction, but enable the tooth to rock in a "seesaw" like manner in the distal-mesial direction. The contact areas appear to play a role in determining tooth motion and in turn define the manner in which the whole tooth moves when loaded. These observations are important for understanding basic structure-function relations of the tooth-PDL-bone system, and have direct implications for better understanding pathological and therapeutic processes in orthodontics, periodontics and jaw bone regeneration.     

Tissue engineered hybrid tooth-bone constructs

Proper rehabilitation of craniofacial defects is challenging because of the complexity of the anatomy and the component tissue types. The ability to simultaneously coordinate the regeneration of multiple tissues would make reconstruction more efficient and might reduce morbidity and improve outcomes. The craniofacial complex is unique because of the presence of teeth, in addition to skin, bone, cartilage, muscle, vascular, and neural tissues since teeth naturally grow in coordination with the craniofacial skeleton, our group developed an autologous, tooth-bone hybrid model to facilitate repair of mandibular defects in the Yucatan minipig. The hybrid tooth-bone construct was prepared by combining tooth bud cell-seeded scaffolds with autologous iliac crest bone marrow derived stem cell-seeded scaffolds, which were transplanted back into surgically created mandibular defects in the same minipig. The constructs were harvested after 12 and 20 weeks of growth. The resulting bone/tooth constructs were evaluated by X-ray, ultra high-resolution volume computed tomography (VCT), histological, immunohistochemical analyses, and transmission electron microscopy (TEM). The observed formation of small tooth-like structures consisting of organized dentin, enamel, pulp, cementum, periodontal ligament, and surrounded by regenerated alveolar bone, suggests the feasibility for regeneration of teeth and associated alveolar bone, in a single procedure. This model provides an accessible method for future clinical applications in humans.     

A mechanobiological model of orthodontic tooth movement

Orthodontic tooth movement is achieved by the process of repeated alveolar bone resorption on the pressure side and new bone formation on the tension side. In order to optimize orthodontic treatment, it is important to identify and study the biological processes involved. This article presents a mechanobiological model using partial differential equations to describe cell densities, growth factor concentrations, and matrix densities occurring during orthodontic tooth movement. We hypothesize that such a model can predict tooth movement based on the mechanobiological activity of cells in the PDL. The developed model consists of nine coupled non-linear partial differential equations, and two distinct signaling pathways were modeled: the RANKL–RANK–OPG pathway regulating the communication between osteoblasts and osteoclasts and the TGF-β pathway mediating the differentiation of mesenchymal stem cells into osteoblasts. The predicted concentrations and densities were qualitatively validated by comparing the results to experiments reported in the literature. In the current form, the model supports our hypothesis, as it is capable of conceptually simulating important features of the biological interactions in the alveolar bone—PDL complex during orthodontic tooth movement.     

Investigation of effective intrusion and extrusion force for maxillary canine using finite element analysis

Abstract

Orthodontic tooth movement is mainly regulated by the biomechanical responses of loaded periodontal ligament (PDL). We investigated the effective intervals of orthodontic force in pure maxillary canine intrusion and extrusion referring to PDL hydrostatic stress and logarithmic strain. Finite element analysis (FEA) models, including a maxillary canine, PDL and alveolar bone, were constructed based on computed tomography (CT) images of a patient. The material properties of alveolar bone were non-uniformly defined using HU values of CT images; PDL was assumed to be a hyperelastic–viscoelastic material. The compressive stress and tensile stress ranging from 0.47 to 12.8?kPa and 18.8 to 51.2?kPa, respectively, were identified as effective for tooth movement; a strain 0.24% was identified as the lower limit of effective strain. The stress/strain distributions within PDL were acquired in canine intrusion and extrusion using FEA; root apex was the main force-bearing area in intrusion–extrusion movements and was more prone to resorption. Owing to the distinction of PDL biomechanical responses to compression and tension, the effective interval of orthodontic force was substantially lower in canine intrusion (80–90?g) than in canine extrusion (230–260?g). A larger magnitude of force remained applicable in canine extrusion. This study revised and complemented orthodontic biomechanical behaviours of tooth movement with intrusive–extrusive force and could further help optimize orthodontic treatment.     

Mechanical response of bone under short-term loading of a dental implant with an internal layer simulating the nonlinear behaviour of the periodontal ligament

We consider a non-standard design for a fixed dental implant, incorporating a soft layer which simulates the presence of the periodontal ligament (PDL). Instead of being aimed at causing an a priori defined stress/strain field within the surrounding bone, upon loading, such a design simply tries to better reproduce the natural tooth-PDL configuration. To do this, the mechanical properties of the internal layer match those of the PDL, determined experimentally to be strongly nonlinear. Three-dimensional finite element analyses show that the presence of such a layer produces (i) a prosthesis mobility very similar to that of a healthy tooth, for several loading conditions, and (ii) a stress/strain distribution substantially different from that arising, upon loading, around a conventional implant. The lack of knowledge of the real mechanical fields existing, under loading, in the bone around a healthy tooth makes it very difficult to state that the stress distribution produced by the modified implant is "better" than that produced by the standard one. Nevertheless, the comparison of the results obtained here, with those of previous refined analyses of the tooth-PDL-bone system, indicates that the modified implant tends to produce a stress distribution in the bone, upon loading, closer to "natural" than that given by the standard one, within the limits imposed by the presence of threads coupling the implant with the bone.     

The divergent expression of periostin mRNA in the periodontal ligament during experimental tooth movement

A novel 90-kDa protein named periostin, which is preferentially expressed in the periosteum and the periodontal ligament (PDL), may play a role in bone metabolism and remodeling. However, the precise role of periostin in the PDL remains unclear. Therefore, we examined the expression of periostin mRNA during experimental tooth movement. Experimental tooth movement was achieved in 7-week-old male Sprague-Dawley rats. In control specimens without tooth movement, the expression of periostin mRNA was uniformly observed in the PDL surrounding the mesial and distal roots of the upper molars and was weak in the PDL of the root furcation area. The periostin mRNA-expressing cells were mainly fibroblastic cells in the PDL and osteoblastic cells on the alveolar bone surfaces. The divergent expression of periostin mRNA in the PDL began to be observed at 3 h and continued up to 96 h after tooth movement. The maximum changes, which showed stronger staining in the pressure sites than in the tension sites, were observed at 24 h. The expression of periostin mRNA in the PDL 168 h after tooth movement exhibited a similar distribution to that of the control specimens. These results suggest that periostin is one of the local contributing factors in bone and periodontal tissue remodeling following mechanical stress during experimental tooth movement.     

A visco-elastic model for the prediction of orthodontic tooth movement

This study presents a biomechanical model of orthodontic tooth movement. Although such models have already been presented in the literature, most of them incorporate computationally expensive finite elements (FE) methods to determine the strain distribution in the periodontal ligament (PDL). In contrast, the biomechanical model presented in this work avoids the use of FE methods. The elastic deformation of the PDL is modelled using an analytical approach, which does not require setting up a 3D model of the tooth. The duration of the lag phase is estimated using the calculated hydrostatic stresses, and bone remodelling is predicted by modelling the alveolar bone as a viscous material. To evaluate the model, some typically used motion patterns were simulated and a sensitivity analysis was carried out on the parameters. Results show that despite some shortcomings, the model is able to describe commonly used motion patterns in orthodontic tooth movement, in both single- and multi-rooted teeth.     

The interplay between increased tooth crown‐height and chewing efficiency,and implications for Cervidae evolution

Mammals of numerous lineages have evolved high‐crowned (hypsodont) teeth particularly during the last 20 million years. This major phenotypic change is one of the most widely studied evolutionary phenomena in a broad range of disciplines, though the mechanisms underlying its transformation remain unresolved. Here, we present the first Finite Element Analysis (FEA) to investigate the alternative hypothesis that there is a biomechanical link between increased hypsodonty and a more effective mastication in deer. Our FE experiments compared patterns of stress and strain within and between different fossil and living species under different loading conditions, and found that more hypsodont teeth are suited for restricting stresses to those areas where chewing loading occurs. This mechanical improvement is consequence of specific and pronounced variations in tooth geometry and morphology of the occlusal surface that are strongly related to crown growth in the vertical plane. We demonstrate that hypsodonty enables selenodont‐teeth to adopt a mechanically improved design that increases the pressure whilst shearing foods. As ruminants are physiologically limited by both the quantity of food consumed and the time spent in the mastication and digestion, hypsodonty is highly advantageous when feeding on mechanically resistant, tough and fibrous foods. Consequently, it allows grass‐eaters to spend less time chewing, thereby increasing the volume of food ingested and/or providing more time for digestion. This study provides a promising line of evidences in support of biomechanical effectiveness, in addition to or instead of increased wear resistance, as a factor in explaining the evolutionary origins of the hypsodont phenotype.     

Focal adhesion kinase mediates β-catenin signaling in periodontal ligament cells

Periodontal ligament (PDL) cells convert the orthodontic forces into biological responses by secreting signaling molecules to induce modeling of alveolar bone and tooth movement. Beta-catenin pathway is activated in response to mechanical loading in PDL cells. The upstream signaling pathways activated by mechanical loading resulting in the activation of β-catenin pathway through Wnt-independent mechanism remains to be characterized. We hypothesized that mechanical loading induces activation of β-catenin signaling by mechanisms that dependent on focal adhesion kinase (FAK) and nitric oxide (NO). We found that mechanical or pharmacological activation of β-catenin signaling in PDL cells upregulated the expression of β-catenin target genes. Pre-treatment of PDL cells with FAK inhibitor-14 prior to mechanical loading abolished the mechanical loading-induced phosphorylation of Akt and dephosphorylation of β-catenin. PDL cells pre-treated with NO donor or NO inhibitor and subjected to mechanical loading. Western blot analysis showed that the mechanical loading or pre-treatment with NO donor increased the levels of dephosphorylated β-catenin, pAkt, and pGSK-3β. Pre-treatment with NO inhibitor blocked the mechanical loading-induced phosphorylation of Akt and dephosphorylation of β-catenin. These data indicate that mechanical loading-induced β-catenin stabilization in PDL cells involves phosphorylation of Akt by two parallel pathways requiring FAK and NO.     

Differential expression of osteoblast and osteoclast chemmoatractants in compression and tension sides during orthodontic movement

Orthodontic tooth movement is achieved by the remodeling of alveolar bone in response to mechanical loading, and is supposed to be mediated by several host mediators, such as chemokines. In this study we investigated the pattern of mRNAs expression encoding for osteoblast and osteoclast related chemokines, and further correlated them with the profile of bone remodeling markers in palatal and buccal sides of tooth under orthodontic force, where tensile (T) and compressive (C) forces, respectively, predominate. Real-time PCR was performed with periodontal ligament mRNA from samples of T and C sides of human teeth submitted to rapid maxillary expansion, while periodontal ligament of normal teeth were used as controls. Results showed that both T and C sides exhibited significant higher expression of all targets when compared to controls. Comparing C and T sides, C side exhibited higher expression of MCP-1/CCL2, MIP-1α/CCL3 and RANKL, while T side presented higher expression of OCN. The expression of RANTES/CCL5 and SDF-1/CXCL12 was similar in C and T sides. Our data demonstrate a differential expression of chemokines in compressed and stretched PDL during orthodontic tooth movement, suggesting that chemokines pattern may contribute to the differential bone remodeling in response to orthodontic force through the establishment of distinct microenvironments in compression and tension sides.     

Effect of altered occlusal function on transseptal ligament and new bone thicknesses in the periodontium of the rat

Alteration of tooth function is assumed to change stress/strain on the adjacent alveolar bone and its mucoperiosteum, producing changes in morphology similar to those described for other load-bearing bones. The present study suggested that crestal alveolar bone and its mucoperiosteum respond differently to stress/strain than load-bearing bones in other locations, possibly due to differences in the mechanism of bone loading by muscles and teeth. Occlusal hypofunction was initiated by extraction of agonist teeth; the contralateral teeth were placed in hyperfunction by the surgery. Untreated animals were also studied. 3H-proline was injected, animals were killed 1-5 weeks later, and the thicknesses of new bone and transseptal ligament were measured. After 5 weeks of altered function, total thickness (new bone + transseptal ligament) was similar in untreated and in hypofunctional and hyperfunctional situations; however, a new ratio between transseptal ligament and new bone thicknesses was established. Occlusal force was negatively correlated with new bone and positively correlated with transseptal ligament thickness; both thicknesses were statistically correlated in each functional situation (P less than 0.001). Hyperfunction resulted in increased transseptal ligament thickness, but decreased new bone thickness as compared to untreated controls (P less than 0.001). In contrast, hypofunction resulted in an increased new bone thickness, but a decreased transseptal ligament thickness (P less than 0.001). Tissue responses assure appropriate support for the teeth in each functional situation.     

Development of a novel intraoral measurement device to determine the biomechanical characteristics of the human periodontal ligament

Periodontal diseases like gingivitis and periodontitis have damaging effects on the periodontium and commonly affect the mechanical properties of the periodontal ligament (PDL), which in the end might lead to loss of teeth. Monitoring tooth mobility and changes of the material properties of the PDL might help in early diagnosis of periodontal diseases and improve their prognosis. It was the aim of this study to develop a novel intraoral device to determine the biomechanical characteristics of the periodontal ligament. This includes the measurement of applied forces and resulting tooth displacement in order to investigate the biomechanical behaviour of the periodontium with varying loading protocols with respect to velocity and tooth displacement. The developed device uses a piezoelectric actuator to apply a displacement to a tooth's crown, and the resulting force is measured by an integrated force sensor. To measure the tooth displacement independently and non-invasively, two magnets are fixed on the teeth. The change in the magnetic field caused by the movement of the magnets is measured by a total of 16 Hall sensors. The displacement of the tooth is calculated from the movement of the magnets. The device was tested in vitro on premolars of four porcine mandibular segments and in vivo on two volunteers. The teeth were loaded with varying activation curves. Comparing the force progression of different activation velocities, the forces decreased with decreasing velocity. Intensive testing demonstrated that the device fulfils all requirements. After acceptance of the ethical committee, further testing in clinical measurements is planned.     

Finite element simulation of the behavior of the periodontal ligament: A validated nonlinear contact model

Due to its significance in tooth movement, the stress/deformation field of periodontium and the alveolar bone remodeling process, periodontal ligament (PDL) cannot be excluded from the studies investigating dental biomechanics regarding its excessive deformability. Therefore, many analytical and numerical researches are carried out to simulate its response and to create a constitutive model via experiments intending to discover the material properties of PDL. The aim of this study is to formulate a user specified contact model that can be used in conjunction with finite element (FE) software and reflects PDL’s influence on neighboring structures based on the currently available information, without requiring an actual volumetric finite element mesh of ligament. The results show good agreement with available experimental tooth mobility data. Smooth stress fields are obtained on the tooth root and alveolar bone, which is a significant aspect in bone-remodeling studies. The advantage of simulating PDL as a contact model at the interface of tooth root and the alveolar process instead of a solid-meshed FE model with poor geometric morphology and/or very dense mesh is expected to save pre/post-processing workforce, to increase the accuracy and to contribute to the smoothness of interface stress distributions.