The functional significance of morphological variation of the human mandible and masticatory muscles

A review is given of what is known about the functional significance of variation of the morphology of the human mandible and jaw muscles. First, the mandible is a lever transferring muscular forces to the teeth. The angle between corpus and ramus and the width of the ramus are particularly relevant in this respect as they determine the mechanical advantage of the lever system and the capacity for sagittal (open-close) movement. The stability of the mandible in asymmetric bites is especially affected by the ratio between the intermolar and intercondylar distances. The repertoire of bite forces that can be generated at any tooth and the loading pattern of the temporomandibular joint are strongly dependent on the relative size of the masseter, temporalis and medial pterygoid muscles. Second, executing its function as a lever, the mandible is subjected to shearing, bending and torsional forces. The bony parts harbouring the teeth, joints and muscle attachments serve to counter these forces; additional strength is needed in three areas i.e. in the symphysis, the condylar neck and in the transition area between corpus and ramus. In human populations there are clear-cut patterns of correlation between some facial skeletal traits, jaw joint morphology and strength and line of action of the jaw muscles. As a result, facial morphologies can be distinguished with marked differences in mechanical performance of their masticatory apparatus. It is suggested that they emerge as a result of diverging environmental influences during postnatal growth.     

Electromyography and mechanics of mastication in the albino rat.

The masticatory apparatus in the albino rat was studied by means of electromyography and subsequent estimation of muscular forces. The activity patterns of the trigeminal and suprahyoid musculature and the mandibular movements were recorded simultaneously during feeding. The relative forces of the individual muscles in the different stages of chewing cycles and biting were estimated on the basis of their physiological cross sections and their activity levels, as measured from integrated electromyograms. Workinglines and moment arms of these muscles were determined for different jaw positions. In the anteriorly directed masticatory grinding stroke the resultants of the muscle forces at each side are identical; they direct anteriorly, dorsally and slightly lingually and pass along the lateral side of the second molar. Almost the entire muscular resultant force is transmitted to the molars while the temporo-mandibular joint remains unloaded. A small transverse force, produced by the tense symphyseal cruciate ligaments balances the couple of muscle resultant and molar reaction force in the transverse plane. After each grinding stroke the mandible is repositioned for the next stroke by the overlapping actions of three muscle groups: the pterygoids and suprahyoids produce depression and forward shift, the suprahyoids and temporal backward shift and elevation of the mandible while the subsequent co-operation of the temporal and masseter causes final closure of the mouth and starting of the forward grinding movement. All muscles act in a bilaterally symmetrical fashion. The pterygoids contract more strongly, the masseter more weakly during biting than during chewing. The wide gape shifts the resultant of the muscle forces more vertically and moreposteriorly. The joint then becomes strongly loaded because the reaction forces are applied far anteriorly on the incisors. The charateristic angle between the almost horizontal biting force and the surface of the food pellet indicates that the lower incisors produce a chisel-like action. Tooth structure reflects chewing and biting forces. The transverse molar lamellae lie about parallel to the chewing forces whereas perpendicular loading of the occlusal surfaces is achieved by their inclination in the transverse plane. The incisors are loaded approximately parallel to their longitudinal axis, placement that avoids bending forces during biting. It is suggested that a predominantly protrusive musculature favors the effective force transmission to the lower incisors, required for gnawing. By grinding food across transversely oriented molar ridges the protrusive components of the muscles would be utilized best. From the relative weights of the masticatory muscles in their topographical relations with joints, molars and incisors it may be concluded that the masticatory apparatus is a construction adapted to optimal transmission of force from muscles to teeth.     

Using "Mighty Mouse" to understand masticatory plasticity: myostatin-deficient mice and musculoskeletal function

Knockout mice lacking myostatin (Mstn), a negative regulatorof the growth of skeletal muscle, develop significant increasesin the relative mass of masticatory muscles as well as the abilityto generate higher maximal muscle forces. Wild-type and Mstn-deficientmice were compared to investigate the postnatal influence ofelevated masticatory loads due to increased jaw-adductor andbite forces on the biomineralization of mandibular articularand cortical bone, the internal structure of the jaw joints,and the composition of temporomandibular joint (TMJ) articularcartilage. To provide an interspecific perspective on the long-termresponses of mammalian jaw joints to altered loading conditions,the findings on mice were compared to similar data for growingrabbits subjected to long-term dietary manipulation. Statisticallysignificant differences in joint proportions and bone mineraldensity between normal and Mstn-deficient mice, which are similarto those observed between rabbit loading cohorts, underscorethe need for a comprehensive analysis of masticatory tissueplasticity vis-à-vis altered mechanical loads, one inwhich variation in external and internal structure are considered.Differences in the expression of proteoglycans and type-II collagenin TMJ articular cartilage between the mouse and rabbit comparisonssuggest that the duration and magnitude of the loading stimuluswill significantly affect patterns of adaptive and degradativeresponses. These data on mammals subjected to long-term loadingconditions offer novel insights regarding variation in ontogeny,life history, and the ecomorphology of the feeding apparatus.     

Investigation on masticatory muscular functionality following oral reconstruction – An inverse identification approach

The human masticatory system has received significant attention in the areas of biomechanics due to its sophisticated co-activation of a group of masticatory muscles which contribute to the fundamental oral functions. However, determination of each muscular force remains fairly challenging in vivo; the conventional data available may be inapplicable to patients who experience major oral interventions such as maxillofacial reconstruction, in which the resultant unsymmetrical anatomical structure invokes a more complex stomatognathic functioning system. Therefore, this study aimed to (1) establish an inverse identification procedure by incorporating the sequential Kriging optimization (SKO) algorithm, coupled with the patient-specific finite element analysis (FEA) in silico and occlusal force measurements at different time points over a course of rehabilitation in vivo; and (2) evaluate muscular functionality for a patient with mandibular reconstruction using a fibula free flap (FFF) procedure. The results from this study proved the hypothesis that the proposed method is of certain statistical advantage of utilizing occlusal force measurements, compared to the traditionally adopted optimality criteria approaches that are basically driven by minimizing the energy consumption of muscle systems engaged. Therefore, it is speculated that mastication may not be optimally controlled, in particular for maxillofacially reconstructed patients. For the abnormal muscular system in the patient with orofacial reconstruction, the study shows that in general, the magnitude of muscle forces fluctuates over the 28-month rehabilitation period regardless of the decreasing trend of the maximum muscular capacity. Such finding implies that the reduction of the masticatory muscle activities on the resection side might lead to non-physiological oral biomechanical responses, which can change the muscular activities for stabilizing the reconstructed mandible.     

Three-dimensional finite element stress analysis of the dentate human mandible.

The biomechanical events which accompany functional loading of the human mandible are not fully understood. The techniques normally used to record them are highly invasive. Computer modelling offers a promising alternative approach in this regard, with the additional ability to predict regional stresses and strains in inaccessible locations. In this study, we built two three-dimensional finite element (FE) models of a human mandible reconstructed from tomographs of a dry dentate jaw. The first model was used for a complete mechanical characterization of physical events. It also provided comparative data for the second model, which had an increased vertical corpus depth. In both cases, boundary conditions included rigid restraints at the first right molar and endosteal cortical surfaces of the articular eminences of temporal bones. Groups of parallel multiple vectors simulated individual masticatory muscle loads. The models were solved for displacements, stresses, strains, and forces. The simulated muscle loads in the first model deformed the mandible helically upward and toward its right (working) side. The highest principal stresses occurred at the bite point, anterior aspects of the coronoid processes, symphyseal region, and right and left sides of the mandibular corpus. In general, the observed principal stresses and strains were highest on the periosteal cortical surface and alveolar bone. At the symphyseal region, maximum principal stresses and strains were highest on the lower lingual mandibular aspect, whereas minimum principal stresses and strains were highest on its upper labial side. Subcondylar principal strains and condylar forces were higher on the left (balancing or nonbiting) side than on the right mandibular side, with condylar forces more concentrated on the anteromedial aspect of the working-side condyle and on the central and lateral aspects of the left. When compared with in vivo strain data from macaques during comparable biting events, the predictive strain values from the first model were qualitatively similar. In the second model, the reduced tensile stress on the working-side, and decreased shear stress bilaterally, confirmed that lower stresses occurred on the lower mandibular border with increased jaw depth. Our results suggested that although the mandible behaved in a beam-like manner, its corpus acted more like a combination of open and closed cross sections due to the presence of tooth sockets, at least for the task modelled.(ABSTRACT TRUNCATED AT 400 WORDS)     

Modeling the biomechanics of the mandible: a three-dimensional finite element study.

Three-dimensional finite element models of a partially edentulated human mandible were generated to calculate the mechanical response to simulated isometric biting and mastication loads. The level of mesh refinement was established via a convergence test and showed that a model with over 30,000 degrees of freedom was required to obtain analysis accuracy. The functional loading cases included muscle loading based on an algorithm that assigns muscle forces in accordance with muscle cross-sectional area, while maintaining static equilibrium. Results were found for isometric application of unilateral and bilateral bite and mastication loading, and two different sets of displacement boundary conditions were imposed at the condyles. The mechanical response is shown in terms of displacements, principal strains, and a new measure called the 'mechanical intensity scalar'. For each load case studied, there was substantial bending in the molar region of the corpus and high tensile strains in the anterior portion of the ramus.     

Validation of a musculo-skeletal model of the mandible and its application to mandibular distraction osteogenesis

Mandibular distraction osteogenesis will lead to a change in muscle coordination and load transfer to the temporomandibular joints (TMJ). The objective of this work is to present and validate a rigid-body musculo-skeletal model of the mandible based on inverse dynamics for calculation of the muscle activations, muscle forces and TMJ reaction forces for different types of clenching tasks and dynamic tasks. This approach is validated on a symmetric mandible model and an application will be presented where the TMJ reaction forces during unilateral clenching are estimated for a virtual distraction patient with a shortened left ramus. The mandible model consists of 2 rigid segments and has 4 degrees-of-freedom. The model was equipped with 24 hill-type musculotendon actuators. During the validation experiment one subject was asked to do several tasks while measuring EMG activity, bite force and kinematics. The bite force and kinematics were used as input for the simulations of the same tasks after which the estimated muscle activities were compared with the measured muscle activities. This resulted in an average correlation coefficient of 0.580 and an average of the Mean Absolute Error of 0.109. The virtual distraction model showed a large difference in the TMJ reaction forces between left and right compared with the symmetric model for the same loading case. The present work is a step in the direction of building patient-specific mandible models, which can assess the mechanical effects on the TMJ before mandibular distraction osteogenesis surgery.     

The effects of external bending moments on lumbar muscle force distribution

A detailed biomechanical model of the low-back musculature that predicts muscle-force distribution in response to external loading is presented. The paper shows that the class of loading tasks that involve an erect posture and an arbitrary load placed on the upper limbs can be described as a loading plane whose axes are the flexion and lateral bending moments. Under these conditions, the individual muscle forces are described as a three-dimensional surface defined by the loading plane and termed the muscle activity surface (MAS). The MAS and the loading plane intersect along the switching curve which separates the load combinations that activate the muscle from those that do not. The paper suggests the existence of a recruitment order of low back muscles in response to external loads and presents a comprehensive framework for examining earlier studies that used EMG measurements to validate physiological and mechanical predictions.     

Fast and Powerful: Biomechanics and Bite Forces of the Mandibles in the American Cockroach Periplaneta americana

Knowing the functionality and capabilities of masticatory apparatuses is essential for the ecological classification of jawed organisms. Nevertheless insects, especially with their outstanding high species number providing an overwhelming morphological diversity, are notoriously underexplored with respect to maximum bite forces and their dependency on the mandible opening angles. Aiming for a general understanding of insect biting, we examined the generalist feeding cockroach Periplaneta americana, characterized by its primitive chewing mouth parts. We measured active isometric bite forces and passive forces caused by joint resistance over the entire mandibular range with a custom-built 2D force transducer. The opening angle of the mandibles was quantified by using a video system. With respect to the effective mechanical advantage of the mandibles and the cross-section areas, we calculated the forces exerted by the mandible closer muscles and the corresponding muscle stress values. Comparisons with the scarce data available revealed close similarities of the cockroaches’ mandible closer stress values (58 N/cm2) to that of smaller specialist carnivorous ground beetles, but strikingly higher values than in larger stag beetles. In contrast to available datasets our results imply the activity of faster and slower muscle fibres, with the latter becoming active only when the animals chew on tough material which requires repetitive, hard biting. Under such circumstances the coactivity of fast and slow fibres provides a force boost which is not available during short-term activities, since long latencies prevent a specific effective employment of the slow fibres in this case.     

Biomechanics of the masticatory apparatus of Pteropus giganteus (Megachiroptera)

Jaw mechanics in Pteropus were studied by means of a three-dimensional model. The model included several parameters of muscle architecture, combined with quantified movement and electromyographical data. Estimates of the nature of the applied forces that act upon the mandible during a chewing cycle, and subsequent estimates of reaction forces at the bite point and joints during the powerstroke, were thus obtained for different food consistencies. The resultant muscle force (relative to the palate) shifts from upward and slightly backward at large gapes to upward and markedly backward at the end of closing. The resultant simultaneously moves anteriorly. During the powerstroke it retains a constant position and orientation along the thickened anterior edge of the coronoid process. The early stages of opening are guided by the slope of the teeth and mandibular fossa; during the remaining part of opening the working line of the resultant crosses the skull behind the joint and thus acquires an opening moment. The bite force has downward and forward components, and a slight transverse component. For a given applied muscular force its magnitude is larger in more posteriorly positioned bite points. Both joints are loaded, the contralateral one more than the ipsilateral. Food consistency affects magnitude and orientation of the applied force, and hence, magnitude and orientation of the bite force and magnitude of the joint reaction forces. The magnitude of masseter activity relative to temporalis activity appears to be the key factor for the orientation of the bite force, and hence for the mechanical optimal position of the food. The adaptive value of the general topography of the masticatory muscles in Pteropus is discussed.     

Muscle activity and spine load during pulling exercises: Influence of stable and labile contact surfaces and technique coaching

This study examined pulling exercises performed on stable surfaces and unstable suspension straps. Specific questions included: which exercises challenged particular muscles, what was the magnitude of resulting spine load, and did technique coaching influence results. Fourteen males performed pulling tasks while muscle activity, external force, and 3D body segment motion were recorded. These data were processed and input to a sophisticated and anatomically detailed 3D model that used muscle activity and body segment kinematics to estimate muscle force, in this way the model was sensitive to each individual’s choice of motor control for each task. Muscle forces and linked segment joint loads were used to calculate spine loads. There were gradations of muscle activity and spine load characteristics to every task. It appears that suspension straps alter muscle activity less in pulling exercises, compared to studies reporting on pushing exercises. The chin-up and pull-up exercises created the highest spine load as they required the highest muscle activation, despite the body “hanging” under tractioning gravitational load. Coaching shoulder centration through retraction increased spine loading but undoubtedly adds proximal stiffness. An exercise atlas of spine compression was constructed to help with the decision making process of exercise choice for an individual.     

Coactivation of jaw muscles: recruitment order and level as a function of bite force direction and magnitude

The aim of this study was to obtain insight into the coactivation behaviour of the jaw muscles under various a priori defined static loading conditions of the mandible. As the masticatory system is mechanically redundant, an infinite number of recruitment patterns is theoretically possible to produce a certain bite force. Using a three-component force transducer and a feedback method, subjects could be instructed to produce a bite force of specific direction and magnitude under simultaneous registration of the EMG activity of anterior and posterior temporal, masseter and digastric muscles on each side. Forces were measured at the second premolars. Vertical, anterior, posterior, lateral and medial force directions were examined; in each direction force levels between 50 N and maximal voluntary force were produced. The results show that for all muscles the bite force-EMG relationship obeys a straight-line fit for forces exceeding 50 N. The relationship varies with bite force direction, except in the case of the digastric muscles. Variation is small for the anterior temporal and large for the posterior temporal and masseter muscles. The relative activation of muscles for a particular force in a particular direction in unique, despite the redundancy.     

The craniomandibular mechanics of being human

Diminished bite force has been considered a defining feature of modern Homo sapiens, an interpretation inferred from the application of two-dimensional lever mechanics and the relative gracility of the human masticatory musculature and skull. This conclusion has various implications with regard to the evolution of human feeding behaviour. However, human dental anatomy suggests a capacity to withstand high loads and two-dimensional lever models greatly simplify muscle architecture, yielding less accurate results than three-dimensional modelling using multiple lines of action. Here, to our knowledge, in the most comprehensive three-dimensional finite element analysis performed to date for any taxon, we ask whether the traditional view that the bite of H. sapiens is weak and the skull too gracile to sustain high bite forces is supported. We further introduce a new method for reconstructing incomplete fossil material. Our findings show that the human masticatory apparatus is highly efficient, capable of producing a relatively powerful bite using low muscle forces. Thus, relative to other members of the superfamily Hominoidea, humans can achieve relatively high bite forces, while overall stresses are reduced. Our findings resolve apparently discordant lines of evidence, i.e. the presence of teeth well adapted to sustain high loads within a lightweight cranium and mandible.     

Influence of weak hip abductor muscles on joint contact forces during normal walking: probabilistic modeling analysis

The weakness of hip abductor muscles is related to lower-limb joint osteoarthritis, and joint overloading may increase the risk for disease progression. The relationship between muscle strength, structural joint deterioration and joint loading makes the latter an important parameter in the study of onset and follow-up of the disease. Since the relationship between hip abductor weakness and joint loading still remains an open question, the purpose of this study was to adopt a probabilistic modeling approach to give insights into how the weakness of hip abductor muscles, in the extent to which normal gait could be unaltered, affects ipsilateral joint contact forces. A generic musculoskeletal model was scaled to each healthy subject included in the study, and the maximum force-generating capacity of each hip abductor muscle in the model was perturbed to evaluate how all physiologically possible configurations of hip abductor weakness affected the joint contact forces during walking. In general, the muscular system was able to compensate for abductor weakness. The reduced force-generating capacity of the abductor muscles affected joint contact forces to a mild extent, with 50th percentile mean differences up to 0.5 BW (maximum 1.7 BW). There were greater increases in the peak knee joint loads than in loads at the hip or ankle. Gluteus medius, particularly the anterior compartment, was the abductor muscle with the most influence on hip and knee loads. Further studies should assess if these increases in joint loading may affect initiation and progression of osteoarthritis.     

Plasticity of mandibular biomineralization in myostatin-deficient mice

Compared with the normal or wild-type condition, knockout mice lacking myostatin (Mstn), a negative regulator of skeletal muscle growth, develop significant increases in relative masticatory muscle mass as well as the ability to generate higher maximal muscle forces. Wild-type and myostatin-deficient mice were compared to assess the postweaning influence of elevated masticatory loads because of increased jaw-adductor muscle and bite forces on the biomineralization of mandibular cortical bone and dental tissues. Microcomputed tomography (microCT) was used to quantify bone density at a series of equidistant external and internal sites in coronal sections for two symphysis and two corpus locations. Discriminant function analyses and nonparametric ANOVAs were used to characterize variation in biomineralization within and between loading cohorts. Multivariate analyses indicated that 95% of the myostatin-deficient mice and 95% of the normal mice could be distinguished based on biomineralization values at both symphysis and corpus sections. At the corpus, ANOVAs suggest that between-group differences are due to the tendency for cortical bone mineralization to be higher in myostatin-deficient mice, coupled with higher levels of dental biomineralization in normal mice. At the symphysis, ANOVAs indicate that between-group differences are related to significantly elevated bone-density levels along the articular surface and external cortical bone in the knockout mice. Both patterns, especially those for the symphysis, appear because of the postweaning effects of increased masticatory stresses in the knockout mice versus normal mice. The greater number of symphyseal differences suggest that bone along this jaw joint may be characterized by elevated plasticity. Significant differences in bone-density levels between normal and myostatin-deficient mice, coupled with the multivariate differences in patterns of plasticity between the corpus and symphysis, underscore the need for a comprehensive analysis of the plasticity of masticatory tissues vis-à-vis altered mechanical loads.     

The physiology and ontogeny of daily oral behaviors

In the masticatory system, activities of muscles are the main source of force. The daily activity of the jaw muscle is a measure of the total daily loading of the tissues involved. This article gives an overview on the recent assessments of the physiology and ontogeny of the daily use of the jaw muscles. Variations in the characteristics of daily activity could be linked to differences in the types of fibers composing the muscles as well as to the properties of the underlying bone, although these relationships are not absolute. Experimental decrease of the hardness of foods eaten by rats and rabbits showed a significant decrease in the number of daily bursts of feeding. These reductions in daily muscular activity were accompanied by higher mineralization of bone and by a transition toward "faster" fiber types in the muscles. It was revealed in rabbits that the characteristics of the daily activities of muscles (total duration of activity, number and lengths of bursts) were not altered during the transition from suckling to chewing and remained largely unaffected during further postnatal development. These results suggest that, despite large anatomical and functional changes, the average daily load on the jaw muscles by the masticatory system appears to be established before chewing develops and remains largely unchanged all the way through development. Whenever the daily muscular activity changes, this seems to have a significant effect on the properties of the tissues involved.     

Microscopic study of the rabbit mandibular periosteum and attached structures.

The structure of the mandibular periosteum in rabbits of different ages has been studied by different histological staining techniques and polarization microscopy. The periosteum consisted of two layers. From the inner, cellular layer the functional state could be determined. A reproducible pattern of resorptive and depository areas was found on the bony surface. In the outer, fibrous periosteal layer, collagenous and elastin fibers were running in distinct directions. The masticatory muscles appeared to be attached directly endomysially or indirectly endomysially, via the perimysium or tendinous attachment. From the periosteal structures and the characteristics of muscular fiber attachments to the bone and periosteum, especially in the ramal and condylar areas, it could be concluded that a mechanical influence of the periosteum on condylar growth is very well possible, which will probably vary during life. The masticatory muscles seemed to be only of minor influence in condylar activity.     

A proprioception based regulation model to estimate the trunk muscle forces

Evaluation of loads acting on the spine requires the knowledge of the muscular forces acting on it, but muscles redundancy necessitates developing a muscle forces attribution strategy. Optimisation, EMG, or hybrid models allow evaluating muscle force patterns, yielding a unique muscular arrangement or/and requiring EMG data collection. This paper presents a regulation model of the trunk muscles based on a proprioception hypothesis, which searches to avoid the spinal joint overloading. The model is also compared to other existing models for evaluation. Compared to an optimisation model, the proposed alternative muscle pattern yielded a significant spine postero-anterior shear decrease. Compared to a model based on combination of optimisation criteria, present model better fits muscle activation observed using EMG (38% improvement). Such results suggest that the proposed model, based on regulation of all spinal components, may be more relevant from a physiologic point of view.     

A Proprioception Based Regulation Model to Estimate the Trunk Muscle Forces

Evaluation of loads acting on the spine requires the knowledge of the muscular forces acting on it, but muscles redundancy necessitates developing a muscle forces attribution strategy. Optimisation, EMG, or hybrid models allow evaluating muscle force patterns, yielding a unique muscular arrangement or/and requiring EMG data collection. This paper presents a regulation model of the trunk muscles based on a proprioception hypothesis, which searches to avoid the spinal joint overloading. The model is also compared to other existing models for evaluation. Compared to an optimisation model, the proposed alternative muscle pattern yielded a significant spine postero-anterior shear decrease. Compared to a model based on combination of optimisation criteria, present model better fits muscle activation observed using EMG (38% improvement). Such results suggest that the proposed model, based on regulation of all spinal components, may be more relevant from a physiologic point of view.     

Occlusal force and craniofacial biomechanics during growth in rhesus monkeys

The masticatory muscles in 132 anesthetized male and female rhesus monkeys ranging in age from juvenile to adult were unilaterally stimulated. Muscle forces and speeds were measured with a bite force transducer positioned at the incisors, premolars, and molars during twitch and tetanic contractions. Lateral cephalographs of all animals were used to estimate the orientation and mechanical advantage of the masticatory muscles. Results showed that maximal occlusal forces increased at a greater rate than body weight during growth. However, maximal occlusal forces increased isometrically relative to mandibular length. Mean forces at the incisors ranged from 70.3 newtons (n) in juveniles up to 139.9 n in adult males. Forces at the molars were 2-2.5 times greater than at the incisors. Time-to-peak tension decreased with increasing body size from 44.1 msec in juveniles to 37.4 msec in adult females to 31.0 msec in adult males. Regression analysis showed that adult males have faster muscles than adult females or juveniles even when corrected for body size. Temporalis and masseter orientation was found to change little throughout growth. The mechanical advantage of the masseter and temporalis muscles for producing occlusal forces on the distal molars improved between juveniles and adults, which is contrary to findings of Oyen et al. (Growth 43:174-187, 1979). Among adults, females had a greater mechanical advantage of the masseter muscles than males.