EXAMINING THE TEMPORO-MANDIBULAR JOINT FROM A BIOTENSEGRITY PERSPECTIVE: A CHANGE IN THINKING
Journal of Applied Biomedicine
2017, 15: 55-62 link
CBiol., FRSB., FLS., DO. request copy
The temporo-mandibular joint is a characteristic feature of mammalian development, and essential to mastication and speech, yet it causes more problems than any other joint in the body and remains the least understood. While it is generally accepted that the normal joint is loaded under compression, the problems and controversies surrounding this view remain unresolved and the disparity in opinion over its treatment continues. Although difficulties in the acquisition of reliable information have undoubtedly contributed to this situation, it is now considered that deficits in neural control and shortcomings in the underlying biomechanical theory and analysis have also played a part, and that a re-assessment from a different perspective could resolve these.
Biotensegrity considers the TMJ from this position, where the mandible is suspended within a tensioned network that extends over a much wider anatomical field than is generally recognized and significant motion control is contained within the structure itself. It is an evolutionary-conserved arrangement that enables the system to rapidly respond to changing functional demands and provides a more complete model of joint physiology that can be used to guide further research.
Biomechanics; Biotensegrity; Four-bar mechanism; Joint loading; Kinematic chain; Orthodontic; Temporomandibular; Tensegrity
The temporo-mandibular joint (TMJ) is part of a multi-tasking mechanical system that contributes to biting, chewing, swallowing, speech, facial expression and breathing. The mandibular condyles simply press the discs against the articular surfaces of the temporal bones and rotate and slide forwards during mouth opening, with complex movement patterns guided by muscles under neural control; but things are not that simple (Davids and Glazier, 2010; Levin, 2006).
In spite of the wealth of published research, the pathologies associated with this joint are still poorly understood and important aspects of its mechanics remain controversial (Herring and Liu, 2001; Scarr and Harrison, 2016). While it is generally accepted that the joint acts like a third-class lever and is therefore loaded under compression, it is also recognized that such stresses can lead to degenerative changes within the articular structures (Juran et al., 2013; Tanaka and Van Eijden, 2003) and the question of how much loading should be considered ‘normal’ remains unanswered.
The lack of information
One of the reasons for this situation has been the difficulty in acquiring information, as the joint is not easy to access, particularly in animals where it is concealed behind the temporal arch and practical and ethical constraints have ensured the almost complete absence of reliable in vivo data on joint loading and muscle forces.
The contribution of certain bones, muscles, ligaments and fascial structures to joint mobility and stability also remains debatable, as electromyography does not provide direct information on muscle loading, cannot record resting muscle tone and is technically very difficult (Hiraba et al., 2000; Masi and Hannon, 2008); stress analysis of bone loading does not take account of the heterarchical complexity of such tissues; and the dynamic significance of ligamentous (Van der Wal, 2009) and fascial tissues (Huijing and Baan, 2008) to motion remains under-appreciated. In vivo measurements of joint loading are inconclusive and the results of cadaver experiments can only ever be approximations (Scarr and Harrison, 2016).
While finite-element analysis is widely used to model the behaviour of the TMJ and its associated structures (Koolstra, 2003) it should always be treated with caution, as the input values are frequently estimated and the operating protocols are essentially based on classical principles that govern the inanimate behaviour of columns, beams and levers (Freutel et al., 2014; Scarr and Harrison, 2016). Many assumptions must thus be made in setting up the experimental parameters and protocols that relate them to each other, and although the short-comings of such models are recognized, it is generally assumed that the acquisition of ‘just a bit more data’ will ultimately provide the relevant answers (Singh and Detamore, 2009; Tanaka and Koolstra, 2008).
Biological tissues are not constrained by the rules of classical theory, and their mechanics follow more complex non-linear stress-strain relationships that allow them to operate quite differently from their lifeless counterparts (Ewoldt, 2014; Humphrey, 2003; Levin, 1982, 2006).
The established model
The lever model is now over three hundred years old and remains essentially unchanged since Borelli (1608 – 1679) compared the anatomy of human movement with man-made machines of the day (Ethier and Simmons, 2007), but this view is too simplistic in a biological context. While levers inherently generate potentially damaging stress concentrations that must be contained within the engineered design (Salvadori, 2002, p. 84) they would be likely to cause material fatigue if they appeared in developing tissues, and that really would be the end of them (Levin, 2006), and a moving fulcrum dramatically complicates their control.
While lever theory essentially dictates that the discs must be compressed between the articular surfaces, so the (unproven) assertion that they do behave like this has been used to justify the lever (Standring, 2005 p. 526; Tanaka and Koolstra, 2008), and it is now considered that the consequences of this circular reasoning have hindered real progress in understanding the aetiology and treatment of TMJ disorders (Scarr and Harrison, 2016). There is nothing wrong with classical mechanical theory but its usefulness in describing the properties of living tissues has its limitations (Levin, 2006; Lighthill, 1986).
Current biomechanics does not have a satisfactory model that enables synovial joint surfaces to be routinely decompressed (or even ‘pulled apart’) and the recognition that this might be actively regulated during movement is an alternative view that has profound implications. The biotensegrity model considers the temporo-mandibular joint from this perspective, where the mandible is suspended within a tensioned network that extends over a much wider anatomical field than is generally recognized and significant motion control is contained within the structure itself. It is an evolutionarily-conserved arrangement that enables the system to rapidly respond to changing functional demands and provides a more complete model of mandibular physiology that can be used to guide further research.
Biotensegrity is a structural design principle that describes a relationship between every part of the organism and the mechanical system that integrates them into a complete functional unit. It looks at the whole picture first and then examines each part in context, where the human body is the complete functional unit, and evolution and developmental processes have ensured that each ‘part’ is integrated into that whole (Kiely and Collins, 2016; Levin, 2006; Scarr, 2014).
Modularity and the global heterarchy
Implicit in this model is the concept of modularity, where multiple sub-systems are inter-linked at every size scale and contribute to the global structural and functional heterarchy (Levin, 2006; Simon, 1962; Turvey and Fonseca, 2014). Thus, we might consider the ‘TMJ’ module as consisting of the mandible, disc, capsule and temporal bone, which combines with the dentition and associated muscle modules to form the ‘masticatory’ module with its links to the ‘hyoid’, ‘pharyngeal’ and ‘neck’ modules. Each one is structurally and functionally connected with all the others and contains a sequence of nested sub-systems that extend down to the cellular and molecular levels; such as muscles, fascicles, endomysium, myofibres, cells and the cytoskeleton.
Architecturally, all these structural entities are modular tensegrity systems that are nested within others at multiple size scales and evolutionarily designed to respond to the specific loadings imposed on them (Levin, 2006; Wilson and Kiely, 2016); but while the terminology we use is derived from our reductionist need to classify anatomy and communicate what we find, the distinctions between them are not always clear cut and important functional relationships can be obscured (Engel, 1977; Guimberteau and Armstrong, 2015).
The anatomy is thus examined from a different perspective that now gives relatively ‘minor’ structures important functions for the first time.
The structural network
Biotensegrity systems are configured in such a way that they stabilize and rapidly adjust themselves in response to the forces acting on them during movement, and maintain a high level of resiliency to external perturbations. They can change shape with the minimum of effort and automatically return to the same position of stable equilibrium with the structure itself guiding motion (Bansod et al, 2014; Silva et al. 2010). These are properties that offer distinct advantages in cyclic systems such as the TMJ, where the mandible must move in a coordinated way that rapidly adapts to the ever-changing environment but whose control is beyond the sole capability of neural processing networks (Brown and Loeb, 2000; Valero-Cuevas et al., 2007). It is a mechanically-efficient system that maintains a high level of structural autonomy and substantially reduces the amount of neural effort needed to regulate movement (Kiely and Collins, 2016; Levin, 2006; Turvey and Fonseca, 2014).
The importance of this new structural system was first recognized in 1948 by the sculptor Kenneth Snelson (Heartney, 2009) and architect/inventor Buckminster Fuller (1975); while the appreciation of biological structures as tensegrities really began in the 1970’s with Stephen Levin, an orthopaedic surgeon who recognized things at the operating table that could not be explained by conventional biomechanical theory (Levin, 1982, 2006), and Donald Ingber who was investigating the behaviour of the cellular cytoskeleton in neoplastic tissues (Ingber et al., 1981, 2014).
Since then, biotensegrity has been described in the cranium (Scarr, 2008), shoulder (Levin, 1997), elbow (Scarr, 2012), spine (Levin, 2002), pelvis (Levin, 2007; Pardehshenas et al., 2014), knee (Hakkak et al., 2015), foot (Wilson and Kiely, 2016), cellular cytoskeleton (Ingber et al., 2014), extra-cellular matrix and fascia (Guimberteau and Armstrong, 2015; Tadeo et al., 2014), molecules (Edwards et al., 2012) and the haptic perceptual system (Turvey and Fonseca 2014); and applied in the development of prosthetic limbs (Lessard et al., 2016) and robotics (Lian et al., 2012; Caluwaerts et al., 2014).
Levin (2002) introduced the term biotensegrity to distinguish this structural system in living tissues from the field of tensegrity engineering, which is related but contains some fundamental differences that do not apply in biology (Scarr, 2014 p 65).
The mechanical model
Biotensegrity systems maintain their integrity solely through the balance of structures under tension and others that are compressed, and it is the particular way in which they are arranged that makes them so distinctive (fig. 1). Their inherent stability and ease of movement is not due to the strength of individual members but because of the way the entire system is configured to distribute mechanical forces (Bansod et al, 2014; Juan and Tur, 2008). In simple terms, the compressed ‘struts’ are suspended within the tensioned network of ‘cables’, where the cables pull on the strut ends and try to shorten them (compress) and the struts resist this and tension the cables, with each one having a mechanical influence on all the others and contributing to the overall structural behaviour. It is a reciprocal relationship that balances the entire system so that the struts do not compress each other at any point and are suspended within the tensioned network of cables.
Fuller (1975, p. 354) recognized the bicycle wheel as the prime example of tensegrity, with its central compressed hub and outer rim suspended in position by the tensioned spokes, but later moved to the six-strut T-icosa (tensegrity-icosahedron), which is the simplest non-trivial tensegrity system that is spatially isotropic (Ethier and Simmons, 2007) and the most useful model for understanding biological systems (Levin and Martin, 2012) (Fig. 1).
The balance of unseen forces
While it is easy to think of bones as compression struts, and muscles as tensioned cables, it might seem difficult to reconcile these simple models with the anatomical complexity of the TMJ and associated structures because the reality is more complicated than that. Biotensegrity systems are best understood in terms of the global balance of forces, where each cable ‘module’ is transmitting tensional forces and each strut ‘module’ is transmitting compressional forces, and they are effectively acting in every direction of space (omni-directional), and for this reason, Snelson considered them as the “physical representation of invisible forces” (Heartney, 2009).
The value of these models is that they show how the struts can remain separated and do not have to compress each other, as classical lever theory dictates they must (Bansod et al, 2014; Levin, 2006), because the entire system (nested modularity) is contributing to regulating the position of each one in relation to the other. The biotensegrity model shows how the anatomy itself can be configured in a way that is capable of controlling complex movements, with the geometric relationship between each part contributing to its kinematic behaviour and the nervous system acting at a higher level of control.
THE TEMPORO-MANDIBULAR MODEL
Mastication naturally involves the transfer of a compressional force to the food, and a considerable amount of effort has been put into estimating how much this biting force actually is (Koc et al., 2010); but just like the TMJ, reliable data is scarce because of the many practical and ethical difficulties, and the relationship between muscle tension, mandibular motion and bite force remains poorly understood.
In order for the mandible to be able to deal with the functional demands placed on it, it must remain stable throughout motion, and it can only do this if the forces acting on it are balanced (Pileicikiene and Surna, 2004; Woda et al, 1001). While neural control increases muscle forces so that the mandible can move in a particular direction, the intrinsic tissue tension (Masi and Hannon, 2008; Schleip et al., 2006), eccentric muscle contractions and ligamentous, fascial and articular constraints are also contributing to its stability (fig. 2).
The suspended mandible
During mouth opening, mandibular motion commences with rotation of the condyles and is initiated by the geniohyoid, mylohyoid and anterior digastric muscles, which are stabilized through their attachments to the hyoid and which is itself suspended between the temporal bones, sternum, clavicles and scapulae. While the temporo-mandibular ligaments constrain any posterior movement of the condyles, they also guide them into forward translation, and a pull from the lateral pterygoid muscles also contributes to this. The initial ‘centre of movement’ then rapidly changes as tensional constraints from the spheno-mandibular (SpML) and stylo-mandibular (StML) ligaments assume greater prominence.
Meanwhile, the hyoid is held in position through the tensioned sterno-hyoid and omohyoid muscles, stylo-hyoid muscles and ligaments (StHL) and posterior digastric muscles etc, and this enables the mandibulo-stylo-hyoid ligaments (MStHL) to become significant in a way that has not been described before. Any downward change in position of the hyoid will tension the MStHL and potentially pull the mandibular angles in the same direction, thus causing the condyles to move inferiorly and decompress the discs and articular surfaces (fig. 2).
Such a description enables the mandible to be held in complete suspension throughout movement, just like the hyoid, hub of the bicycle wheel and compression struts of the tensegrity model (fig. 1), and biotensegrity is currently the only model that explains this possibility. It could even resolve the decades-old controversy over joint loading and suggests that established conventions need revising (Scarr and Harrison, 2016).
The theoretical model described above is, of course, a gross simplification of the physiological reality but it does indicate the potential. The controversy over the mechanics of the TMJ has been ongoing since at least the beginning of the twentieth-century, with assertions over whether (or not) it acts as a third-class lever based on such things as force-vector analysis, experimental observations and the capability of certain tissues to withstand the potentially destructive forces that result from this model; and detractors on each side continue to snipe at the others point of view (Herring and liu, 2001; Scarr and Harrison, 2016).
Even though a characteristic feature of tensegrity is that compressional forces are not transferred directly between the ‘struts’ (condyle/disc/glenoid), the ability of the discs and joint surfaces to just glide alongside each other without being compressed is still compatible with this in a biological context (Fuller, 1975 p 391; Levin, 2002). Tanaka and Koolstra (2008) noted that mechanical loading is essential for the growth, development and maintenance of living tissues, and that unloading can suppress bone remodelling, but they also observed that excessive and even ‘normal’ stresses on the joint can lead to degenerative changes.
The soft tissues
The articular discs
The discs are complex structures composed of dense fibro-cartilage that glide between the condyles and glenoid fossae, and it is their internal cross-ply arrangement of collagen fibres that provides their high tensile stiffness and strength (Minarelli et al., 1997; Singh and Detamore, 2009). These tensioned fibres are also inter-linked with highly hydrated and viscous proteoglycans that regulate fluid (and nutrient) flow and maintain a certain amount of compressive stiffness, and it is this arrangement that contributes to the stability of the discs and allows them to easily accommodate to the changing surface contours during movement (Tanaka and van Eijden. 2003); but compressional loading could have profound consequences on their ability to maintain this (Juran et al., 2013; Wright et al., 2013).
Disc compression inevitably leads to an increase in collagen fibre tension, and the ability of crossed-fibre networks to contain this is already an established biomechanical principle in the inter-vertebral disc (Hukins and Meakin, 2000) and muscles, etc (Scarr, 2016). However, discs that are under excessive compression and sliding between the highly incongruent articular surfaces will be vulnerable to the damaging effects of internal shear stresses, no matter how effective the lubrication, and their ability to absorb, adapt or nullify the effects of these would be paramount to normal function (Tanaka et al., 2008).
As biotensegrity configurations, the discs would normally avoid the effects of these stresses by dissipating them throughout their internal structure (Levin, 2006; Scarr, 2016), while a prolonged increase in compression would place the fibrous matrix and capsular attachments under a much greater amount of stress and potentially lead to degenerative changes (Tanaka et al., 2008). This latter situation is considered almost inevitable if the TMJ acted as a lever, while as a biotensegrity module, the highly compliant discs would glide with minimal compression and act more as protective cushions than major load bearers.
The widespread belief that biological tissues operate in a piecemeal-like way is a reductionist view that stems from comparisons with mechanical engineering and anatomical classifications that perpetuate that view (Engel, 1977; Fricton, 2014), but the biotensegrity perspective emphasizes that each modular ‘part’ should always be considered in relation to the whole (Levin and Martin, 2012; Scarr, 2014).
Thus, the mandibulo-stylo-hyoid ligaments are thickened sheets lying deep within the cervical fascia and that consistently connect the angles of the mandible with the hyoid bone (Shimada and Gasser, 1988); but they only function as described because of their integration within the global structural system. Similarly, the conventional view of the spheno-mandibular ligaments as being “slack”, when the mouth is closed ((Standring, 2005, p. 526) should be considered in relation to the continuous tensional environment within living tissues; while the assertion that the stylo-mandibular ligaments “cannot mechanically constrain any normal movements of the mandible and do not seem to warrant the status of ligaments of the joint” (Standring, 2005, p. 527) should no longer be accepted as a fair assessment of their function.
Van der Wal (2009) showed that elbow ligaments are more than just passive restrainers of motion but specialized parts of the tensioned fascial network that is continuously adjusting itself throughout motion, and the cruciate ligaments within the knee are also a well-recognized example of this (Bradley et al., 1988). Huijing and Baan (2008) highlighted fascial tension pathways that transfer muscle forces between both agonist and antagonist muscles and alter their behaviour, and similar regions are likely to be found in relation to the jaw. Muscles, ligaments and fascial tissues are always under tension in vivo (Levin, 2002; Masi and Hannon, 2008; Schleip et al, 2006) and their intertwined and multi-directional fibre orientations suggest important contributions to joint kinematics (Guimberteau and Armstrong, 2015) (fig. 2).
On a related note, it is widely thought that the forces of mastication are exerted directly by the mandible, but this is not the case as the teeth are suspended within their sockets by periodontal ligaments, highly-collagenous tissues some 0.2 mm wide that transfer biting forces between the bone and teeth through tensional pathways. They also provide important proprioceptive information about the dentition and are inextricably linked with TMJ function (Pileicikiene and Surna, 2004).
The neuro-muscular system
The mandible operates within a wide spatial field, with each muscle pulling in a direction that is parallel with its contractile fibres (or tendinous aponeurosis in the case of pennate muscles) and contributing to placing the mandible in any particular position during movement (Pileicikiene and Surna, 2004; Woda et al, 2001); and it is their complex internal organization and fibre variability that contributes to the great assortment of contractile behaviours and adaptability to changing functional demands (Grünheid et al., 2009).
While the motor cortex and central pattern generators regulate cyclic and purposeful muscle contractions, complex reflex patterns within the brainstem and spinal cord exchange information between different parts of the system; and depend on a vast amount of sensory information from the joint capsules, retro-discal tissues, tongue, periodontal, pharyngeal and laryngeal tissues, and associated muscles, ligaments and fascia (Renton and Egbuniwe, 2015; Yin et al., 2007). Reflex systems assimilate this and initiate muscle contractions in a way that supplements supra-spinal control, but their ability to respond to unexpected changes within the system is incomplete as even the fastest mono-synaptic reflex experiences a time-delay (Brown and Loeb, 2000; Turvey and Fonseca, 2014).
Jaw movements are among the most complex in the body, and a structural control system that responds instantly to unexpected perturbations would have a distinct evolutionary advantage (Kiely and Collins, 2016; Levin, 2006). Closed-chain kinematics is such a mechanism that links every part of the structure into a continuous mechanical loop, with the motion of each one causing controlled changes in position, velocity and kinetic energy of all the others and with a definable relationship that depends entirely on the geometry (Levin et al., under review).
The structural mechanics
Closed kinematic chains (CKC) are widely used in mechanical engineering because they provide a simple and efficient mechanism that allows each part to determine the behaviour of all the others (Phelan, 1962); and in a biological context, they create an information processing network that enables the tissues themselves to perform logic computations that the nervous system is incapable of (Valero-Cuevas et al., 2007). Such configurations have been described in the feeding mechanism of shrimps (Claverie et al., 2010), the jaws of fish (Hulsey et al., 2005; Muller, 1996) and reptiles (Kardong, 2003), the limbs of ungulates (Van Weeren et al, 1990) and the human body (Bradley et al., 1988; Levin et al, under review); and provide an evolutionary mechanism for increasing morphological diversity (Alfaro et al., 2005).
The simplest geometric arrangement that enables the structure itself to control motion is then the ‘four-bar’ CKC (fig. 3a), where the length and position of each bar determines the behaviour of all the others and characterizes the overall changes in shape, and the angular relationships between them define its mechanical properties (functions) (Muller, 1996). In three-dimensions, the hub and rim of the bicycle wheel maintain their positions because of the high tensional-stiffness of the spokes acting within the inter-linked 4-bars (fig. 3b); and figure 3c shows how multiple three and four-bars act together to enable the entire tensegrity structure to expand and contract in a controlled way when any two parallel struts are pulled apart.
In simple biological terms, each bony ‘strut’ is a stiff compression bar that alters its position and orientation in relation to the others because of changes in the relative length and tensional-stiffness of the muscular, ligamentous and fascial bars (cables), with each one mechanically guiding and constraining all the others and contributing to movement (fig. 2). They all become part of an inter-linked complex of CKC’s that structurally unite the anatomy and transfer mechanical forces along and between the ‘bars’ through multiple inter-linked sub-modules nested within each other; and these extend down to the extra-cellular matrix (Guimberteau and Armstrong, 2015), cellular (Ingber et al., 2014) and molecular levels (Edwards et al. 2012), with each bar/strut/cable/module having its own unique set of mechanical properties that reciprocally influence the behaviour of all the others.
From a biotensegrity perspective, the position and orientation of the mandible (in three-dimensions) results from the mechanical behaviour of a huge number of inter-linked CKC’s, with the entire structural system guiding these changes and enabling an instantaneous response to changing conditions. Muscles can then be considered more as active tensioners of the biotensegrity network, with the nervous system acting at a higher level of control and regulating the amount of force exerted across the joint surfaces.
The global anatomical network
While the spatial relationships between the dentition, mandibular condyles and temporal bones are recognized as key to normal function (and clinical reasoning when things go awry) (Cuccia et al. 2011; Pileicikiene and Surna, 2004; Woda et al. 2001), the same CKC/biotensegrity principles will also extend to other structures in the head, neck and body because of their mechanical connections (Saccucci et al. 2011).
Gelb (2014) emphasized the importance of the tongue and naso-pharyngeal structures to the restoration and maintenance of normal TMJ function; and sutural patency is reported to significantly influence the positions of the maxillae, sphenoid and temporal bones in relation to each other and the mandible, and thus all structures associated with the TMJ (James and Strokon, 2003; Liem and Vogt, 2012); and Scarr (2008) outlined the tensegrity principles of this in the cranial vault. The contribution of the cervical spine and head posture to TMJ and dental disorders is also well recognized (Sonnesen, 2010; Zafar, 2000) and implicit in the biotensegrity model.
What is ‘normal’?
Biotensegrity over-rides many of the controversies surrounding TMJ function because it is inherently a complete system, where every modular ‘part’ has a mechanical influence on all the others, for good and ill, and allows the details to be assessed from a much broader global perspective than has traditionally been the case. Such a network distributes normal and ‘aberrant’ forces over complex heterarchical pathways that influence the TMJ and mandibular motion and extend far beyond the joint.
Postural changes (including malocclusion), injury, micro-trauma and pathology will inevitably alter the mechanical balance of the joint and cause the nervous system to assume control in a way that is beyond its ‘normal’ remit (Brown and Loeb, 2000; Kiely and Collins, 2016). While this may temporarily ease the situation, it could also change movement patterns and create imbalances in the tissue network that eventually lead to chronicity, which means that treatment protocols that recognize the unique contributions of the tissues themselves in controlling motion would be more likely to succeed.
The application of Joint Vibration Analysis (JVA) as an objective means to observe the behaviour of the TMJ in vivo (Deregibus et al. 2014; Radke and Kull, 2015), and the use of manual therapies (Cuccia et al. 2011; Martins et al., 2016), advanced lightwire functional (ALF) (Delz, 2009; James and Strokon, 2003) and certain other appliances (Jabłońska -Zrobek et al. 2014) to orthodontics and orofacial reorganisation are all fully compatible with a biotensegrity approach to assessing and treating joint dysfunction.
The future of TMJ analysis
While Scarr and Harrison (2016) highlighted some of the problems associated with conventional joint analysis, the introduction of closed-chain kinematics (Muller, 1996) and tensegrity-dedicated analytical platforms (Baudriller et al., 2006; Juan and Tur, 2008; Caluwaerts et al., 2014) may also have a place in resolving these; but only if the cautions on such analyses are taken into account. CKC’s enable multiple mechanical properties (functions) to be optimized between different tissues throughout embryological development and normal maintenance and repair processes (Alfaro et al, 2005), and a more thorough understanding of these in a biotensegrity context is likely to add considerably to our knowledge.
This examination of TMJ mechanics from a biotensegrity perspective is essentially a qualitative assessment that places the mandible (and all other structures) within a global balance of interconnected forces: an automatic shifting suspension system that contributes to the control of motion and regulates the amount of force exerted across the articular surfaces.
Biotensegrity is a structural design principle that describes a relationship between every part of the organism and the mechanical system that integrates them into a complete functional unit. It looks at the whole picture first and then examines each part in context, where the human body is the complete functional unit, and evolution and developmental processes have ensured that each ‘part’ is integrated into that whole.
The temporo-mandibular joint has thus been considered as part of this structural network, where each anatomical ‘part’ is a complex modular tensegrity system nested within others at multiple size scales and that facilitates the suspension of the mandible within the tensioned network of muscles, ligaments and fascia. Such a mechanically-efficient system would be able to move in a coordinated way that rapidly adapts to the ever-changing environment and substantially reduces the amount of effort needed from the nervous system. Closed-chain kinematic geometry then describes the mechanics of biotensegrity where substantial movement control is contained within the structure itself and previously unrecognized aspects of TMJ physiology can be revealed.
Such simplicity is at the heart of biology but has been obscured by its apparent complexity; and the rigid application of lever theory, reductionist methods and questionable analyses have unwittingly stifled progress (Engel, 1977; Fricton, 2014; Scarr and Harrison, 2016). The biotensegrity concept represents a paradigm shift in thinking because it is based on the rules of physics first and from which everything else is derived (Levin, 2006; Scarr, 2014). It escapes the lever controversy and provides a more comprehensive way to assess TMJ mechanics; and multi-disciplinary approaches that recognize these factors are likely to lead to more predictable and successful treatments in the future.
Potential conflict of interest
Helen Harrison of Granta Diagnostics is the UK distributor for JVA (Joint vibration analysis).
Alfaro, M.E., Bolnick, D.I., Wainwright, P.C., 2005. Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. Am. Nat. 165, E140–E154.
Bansod, Y.D., Nandanwar, D., Burša, J., 2014. Overview of tensegrityI: basic structures. Eng. Mech. 21, 355–367.
Baudriller, H., Maurin, B., Cañadas, P., Montcourrier, P., Parmeggiani, A., Bettache, N., 2006. Form-finding of complex tensegrity structures: application to cell cytoskeleton modelling. C. R. Mecanique 334, 662–668.
Bradley, J., Fitzpatrick, D., Daniel, D., Shercliff, T., O’Connor, J., 1988. Orientation of the cruciate ligament in the sagittal plane. J. Bone Jt. Surg. (Br.) 70, 94–99.
Brown, I.E., Loeb, G.E., 2000. A reductionist approach to creating and using neuromusculoskeletal models. In: Winsters, J.M., Crago, P.E. (Eds.), Biomechanics and Neural Control of Posture and Movement. Springer-Verlag, New York, pp. 148–163.
Caluwaerts, K., Despraz, J., Iscen, A., Sabelhaus, A.P., Bruce, J., Schrauwen, B., SunSpiral, V., 2014. Design and control of compliant tensegrity robots through simulation and hardware validation. J. R. Soc. 11, 20140520. doi:http://dx.doi.org/10.1098/rsif.2014.05201742-5662. https://ti.arc.nasa.gov/tech/asr/intelligent-robotics/tensegrity/ntrt/.
Claverie, T., Chan, E., Patek, S.N., 2010. Modularity and scaling in fast movements: power amplification in mantis shrimp. Evolution 65, 443–461.
Cuccia, A.M., Caradonna, C., Caradonna, D., 2011. Manual therapy of the mandibular accessory ligaments for the management of temporo-mandibular joint disorders. J. Am. Osteo Assoc. 111, 102–112.
Davids, K., Glazier, P., 2010. Deconstructing neurobiological coordination: the role of the biomechanics-motor control nexus. Exerc. Sport Sci. Rev. 38, 86–90.
Delz, E., 2009. The ALF (Advanced Lightwire Functional appliance) creating facial beauty and balance. Int. J. Orthod. 20, 23–27.
Deregibus, A., Castroflorio, T., De Giorgi, I., Burzio, C., Debernardi, C., 2014. Could different TMJ disc positions observed in MRI cause different sounds? Analysis on a group of subjects with ADD with reduction: a pilot study. Cranio 32, 265–274.
Edwards, S.A., Wagner, J., Gräter, F., 2012. Dynamic prestress in a globular protein. PLoS. Comput. Biol. 8, e1002509 1–14.
Engel, G.L., 1977. The need for a new medical model: a challenge for biomedicine. Science 196, 129–136.
Ethier, C.R., Simmons, C.A., 2007. Introductory Biomechanics: from Cells to Organisms. Cambridge University Press, Cambridge.
Ewoldt, R.H., 2014. Extremely soft: design with rheologically complex fluids. Soft Rob. 1, 12–20.
Freutel, M., Schmidt, H., Dürselen, L., Ignatius, A., Galbusera, F., 2014. Finite element modelling of soft tissues: material models, tissue interaction and challenges. Clin. Biomech. 29, 363–372.
Fricton, J.R., 2014. Temporomandibular disorders: a human systems approach. J. Calif. Dent. Assoc. 42, 523–534.
Fuller, R.B., 1975. Synergetics: explorations in the geometry of thinking. McMillan, New York.
Gelb, M.L., 2014. Airway centric TMJ philosophy. J. Calif. Dent. Assoc. 42, 551–562.
Grünheid, T., Langenbach, G.E.J., Korfage, J.A.M., Zentner, A., Van Eijden, T.M.G.J., 2009. The adaptive response of jaw muscles to varying functional demands. Eur. J. Orthod. 31, 596–612.
Guimberteau, J.C., Armstrong, C., 2015. Architecture of Human Living Fascia: the Extracellular Matrix and Cells Revealed Through Endoscopy. Handspring, Edinburgh.
Hakkak, F., Jabalameli, M., Rostami, M., Parnianpour, M., 2015. The tibiofemoral joint gaps–an arthroscopic study. SDRP J. Biomed. Eng. (Available at http://www.openaccessjournals.siftdesk.org/articles/pdf/The-Tibiofemoral-Joint-Gaps20151112000118.pdf accessed 03/9/2016).
Heartney, E., 2009. Forces Made Visible. Hard Press Editions, Massechusetts.
Herring, S.W., Liu, Z.J., 2001. Loading of the temporo-mandibular joint: anatomical and in vivo evidence from the bones. Cells Tissue Organs 169, 193–200.
Hiraba, K., Hibino, K., Hiranuma, K., Negoro, T., 2000. EMG activities of two heads of the human lateral pterygoid muscle in relation to mandibular condyle movement and biting force. J. Neurophys. 83, 2120–2137.
Huijing, P.A., Baan, G.C., 2008. Myofascial force transmission via extramuscular pathways occurs between antagonistic muscles. Cells Tissues Organs 188, 400–414.
Hukins, D.W.L., Meakin, J.R., 2000. Relationship between structure and mechanical function of the tissues of the intervertebral joint. Am. Zool. 40, 42–52.
Hulsey, D.C., Fraser, G.J., Streelman, J.T., 2005. Evolution and development of complex biomechanical systems: 300 million years of fish jaws. Zebrafish 2, 243–257.
Humphrey, J.D., 2003. Continuum biomechanics of soft biological tissues. Proc. R.Soc. Lond. A 459, 3–46.
Ingber, D.E., Madri, J.A., Jamieson, J.D., 1981. Role of basal lamina in neoplastic disorganization of tissue architecture. Proc. Nat. Acad. Sci. 78, 3901–3905.
Ingber, D.E., Wang, N., Stamenovic, D., 2014. Tensegrity, cellular biophysics and the mechanics of living systems. Rep. Prog. Phys. 77, 1–42.
Jabłonska-Zrobek, J., Asiewacz, S., Skiba, A., Strzecki, A., Szczepanska, J., Pawłowska, E., 2014. Biotensegrity as the mechanism of the anterior part of maxilla expansion using orthodontic sagittal appliance. J. Stomatol. 67, 630–650.
James, G.A., Strokon, D., 2003. The significance of cranial factors in diagnosis and teatment with the advanced lightwire functional appliance. Int. J. Orthod. 14, 17–27.
Juan, H.S., Tur, J.M.M., 2008. Tensegrity frameworks: static analysis review. Mech. Mach. Theory 43, 859–881.
Juran, C.M., Dolwick, M.F., McFetridge, P.S., 2013. Shear mechanics of the TM: J disc: relationship to common clinical observations. Biomat. Bioeng. 92, 193–198.
Kardong, K.V., 2003. Biomechanics and evolutionary space: a case study. In: Bels, V. L., Gasc, J.P., Casinos, A. (Eds.), Vertebrate Biomechanics and Evolution. Bios Scientific, Oxford, pp. 73–86.
Kiely, J., Collins, D.J., 2016. Uniqueness of human running coordination: the integration of modern and ancient evolutionary innovations. Front. Psychol. 7,
Koc, D., Dogan, A., Bek, B., 2010. Bite force and influential factors on bite force measurements: a literature review. Eur. J. Dent. 4, 223–232.
Koolstra, J.H., 2003. Number crunching with the human masticatory system. J. Dent. Res. 82, 672–676.
Lessard, S., Bruce, J., Jung, E., Teodorescu, M., SunSpiral, S., Agogino, A., 2016. A lightweight, multi-axis compliant tensegrity joint. IEEE Int. Conf. Robot. Autom. (ICRA) doi:http://dx.doi.org/10.1109/icra.2016.7487187.
Levin, S.M., 1982. Continuous tension, discontinuous compression: a model for biomechanical support of the body. Bull. Struct. Integr. 8 (Available online at http://www.biotensegrity.com/
continuous_tension_discontinuous_compression.php accessed 3.9.16).
Levin, S.M., 1997. Putting the shoulder to the wheel: a new biomechanical model for the shoulder girdle. J. Biomed. Sci. Instrum. 33, 412–417.
Levin, S.M., 2002. The tensegrity truss as a model for spine mechanics: biotensegrity. J. Mech. Med. Biol. 2, 375–388.
Levin, S.M., 2006. Tensegrity: the new biomechanics. In: Hutson, M., Ellis, R. (Eds.), Textbook of Musculoskeletal Medicine. University Press, Oxford, pp. 69–80.
Levin, S.M., 2007. A suspensory system for the sacrum in pelvic mechanics: biotensegrity. In: Vleeming, A., Mooney, V., Stoeckart, R. (Eds.), Movement, Stability and Lumbopelvic Pain. Churchill Livingstone, Elsevier, Edinburgh, pp. 229–237.
Levin, S.M., Martin, D.C., 2012. Biotensegrity: the mechanics of fascia. In: Schleip, R., Findley, T.W., Chaitow, L., Huijing, P.A. (Eds.), Fascia: the Tensional Network of the Human Body. Churchill Livingstone Elsevier, Edinburgh, pp. 136–142.
Levin, S.M., Lowell, S., Scarr, G., (under review). The significance of closed kinematic chains to biological movement and stability.
Lian, O.C., Keong, K.C., Yee, L.C., 2012. Biotensegrity inspired robot: future construction alternative. Procedia Eng. 41, 1079–1084.
Liem, T., Vogt, R., 2012. Membranous structures within the cranial bowl and intraspinal space. In: Schleip, R., Findley, T.W., Chaitow, L., Huijing, P.A. (Eds.), Fascia: the Structural Network of the Body. Churchill Livingstone Elsevier, Edinburgh, pp. 57–65.
Lighthill, J., 1986. The recently recognized failure of predictability in Newtonian dynamics. Proc. R. Soc. Lond. A 407, 35–50.
Martins, W.R., Blasczyk, J.C., de Oliveira, M.A.F., Gonçalves, K.F.L., Bonini-Rocha, A.C., Dugailly, P.M., de Oliveira, R.J., 2016. Efficacy of musculoskeletal manual approach in the treatment of temporo-mandibular joint disorder: a systematic review with meta-analysis. Man. Ther. 21, 10–17.
Masi, A.T., Hannon, J.C., 2008. Human resting muscle tone (HRMT): narrative introduction and modern concepts. J. Bodyw. Mov. Ther. 12, 320–332.
Minarelli, A.M., Del Santo, M., Liberti, E.A., 1997. The structure of the human temporomandibular joint disc: a scanning electron microscopy study. J. Orofacial. Pain 11, 95–100.
Muller, M.,1996. A novel classification of planar four-bar linkages and its application to the mechanical analysis of animal systems. Philos. Trans. R. Soc. Lond. B 351, 689–720.
Pardehshenas, H., Maroufi, N., Sanjari, M.A., Parnianpour, M., Levin, S.M., 2014. Lumbopelvic muscle activation patterns in three stances under graded loading conditions: proposing a tensegrity model for load transfer through the sacroiliac joints. J. Bodyw. Mov. Ther. 18, 633–642.
Phelan, R.M., 1962. Fundamentals of Mechanical Design, 2nd ed. McGraw-Hill Book Co, London.
Pileicikiene, G., Surna, A., 2004. The human masticatory system from a biomechanical perspective: a review: stomatologija. Baltic Dent. Maxillofac. J. 6, 81–84.
Radke, J.C., Kull, R.S., 2015. Comparison of TMJ vibration frequencies under different joint conditions. Cranio 33, 174–182.
Renton, T., Egbuniwe, O., 2015. Pain, part 2a: trigeminal anatomy related to pain. Dent. Update 42, 238–244.
Saccucci, M., Tettamanti, L., Mummolo, S., Polimeni, A., Festa, F., Salini, V., Tecco, S., 2011. Scoliosis and dental occlusion: a review of the literature. Scoliosis 6, 15.
Salvadori, M., 2002. Why Buildings Stand Up: The Strength of Architecture. W.W. Norton & Company, Inc, New York.
Scarr, G., 2008. A model of the cranial vault as a tensegrity structure and its significance to normal and abnormal cranial development. Int. J. Osteopath. Med. 11, 80–89.
Scarr, G., 2012. A consideration of the elbow as a tensegrity structure. Int. J. Osteopath. Med. 16, 114–120.
Scarr, G., 2014. Biotensegrity: the Structural Basis of Life. Handspring, Edinburgh.
Scarr, G., 2016. Fascial hierarchies and the relevance of crossed-helical arrangements of collagen to changes in the shape of muscles. J. Bodyw. Mov. Ther. 20, 377–387.
Scarr, G., Harrison, H., 2016. Resolving the problems and controversies surrounding temporo-mandibular mechanics. J. Appl. Biomed. 14, 177–185.
Schleip, R., Naylor, I.L., Ursu, D., Melzer, W., Zorn, A., Wilke, H.J., Lehmann-Horn, F., Klingler, W., 2006. Passive muscle stiffness may be influenced by active contractility of intramuscular connective tissue. Med. Hypotheses 66, 66e71.
Shimada, K., Gasser, R.F.,1988. Morphology of the mandibulo-stylohyoid ligament in human adults. Anat. Rec. 222, 207–210.
Silva, P.L., Fonseca, S.T., Turvey, M.T., 2010. Is tensegrity the functional architecture of the equilibrium point hypothesis? Motor Control 14, e35–e40.
Simon, H.A., 1962. The architecture of complexity. Proc. Am. Philos. Soc. 106, 467–482.
Singh, M., Detamore, M.S., 2009. Biomechanical properties of the mandibular condylar cartilage and their relevance to the TMJ disc. J. Biomech. 42, 405–417.
Sonnesen, L., 2010. Associations between the cervical vertebral column and craniofacial morphology. Int. J. Dent. 29572, 1–6.
Standring, S., 2005. Gray’s Anatomy, thirty-ninth ed. Elsevier Churchill Livingstone, Edinburgh.
Tadeo, I., Berbegall, A.P., Escudero, L.M., Álvaro, T., Noguera, R., 2014. Biotensegrity of the extracellular matrix: physiology, dynamic mechanical balance and implications in oncology and mechanotherapy. Front. Oncol. 4, 1–10.
Tanaka, I., Koolstra, J.H., 2008. Biomechanics of the temporomandibular joint. J. Dent. Res. 11, 989–991.
Tanaka, I., van Eijden, T., 2003. Biomechanical behaviour of the temporomandibular joint disc. Crit. Rev. Oral Biol. Med. 14, 138–150.
Tanaka, I., Detamore, M.S., Tanimoto, K., Kawai, N., 2008. Lubrication of the temporomandibular joint. Ann. Biomed. Eng. 36, 14–29.
Turvey, M.T., Fonseca, S.T., 2014. The medium of haptic perception: a tensegrity hypothesis. J. Mot. Behav. 46, 143–187.
Valero-Cuevas, F.J., Yi, J.W., Brown, D., McNamara, R.V., Paul, C., Lipson, H., 2007. The tendon network of the fingers performs anatomical computation at a microscopic scale. IEEE Trans. Biomed. Eng. 54, 1161–1166.
Van Weeren, P.R., Van den Bogert, A.J., Hartman, A.B.W., Kersjes, A.W., 1990. The role of the reciprocal apparatus in the hind limb of the horse investigated by a modified CODA-3 opto-electronic kinematic analysis system. Equine Vet. J. Suppl. 9, 95–100.
Van der Wal, J., 2009. The architecture of the connective tissue in the musculoskeletal system: an often overlooked functional parameter as to proprioception in the locomotor apparatus. Int. J. Ther. Massage Bodyw. 2, 9–23.
Wilson, J., Kiely, J., 2016. The multi-functional foot in athletic movement: extraordinary feats by our extraordinary feet. Hum. Mov. 17, 15–20.
Woda, A., Pionchon, P., Palla, S., 2001. Regulation of mandibular postures: mechanisms and clinical implications. Crit. Rev. Oral Biol. Med. 12, 166–178.
Wright, G.J., Juo, J., Shi, C., Bacro, T.H., Slate, E.H., Yao, H., 2013. Effect of mechanical strain on solute diffusion in human TM: J discs: an electrical conductivity study. Ann. Biomed. Eng. 41, 1–18.
Yin, C.S., Lee, Y.J., Lee, Y.J., 2007. Neurological influences of the temporomandibular joint. J. Bodyw. Mov. Ther. 11, 285–294.
Zafar, H., 2000. Integrated jaw and neck function in man; studies of mandibular and head-neck movements during jaw opening-closing tasks. Swed. Dent. J. Suppl. 143, 1–41.