Chapter 3

CH 3 – NATURAL GROWTH OF THE HUMAN JAW SYSTEM 

FUNCTIONALLY STIMULATED GROWTH - This harmoniously functioning, highly adaptive, and longlasting human jaw system is the result of a complex multistaged postnatal growth process resulting from interactions between its genetics and the functional stimuli it receives from chewing and swallowing.  In many ways, humans evolved from an ape born in an embryonic stage.49  This was especially true of the jaw system.  Delaying the growth of the jaw system until it was exposed to functional forces enabled each individual to grow and maintain a jaw system that best fit the particular forces it would have to endure. Thus genetics provides the motive forces, the raw materials that are bound to cause proliferation of tissues according to a pre-determined sequence, but the final form taken by the tissues is also very much determined by the system’s response to the functional environment in which the genetic tendencies are expressed.

The whole jaw system grows in response to biting forces.  In growing rabbits, experimentally altering the plane of the bite table can bend the whole craniofacial skeleton.89 In humans at birth, the TMJs have not yet formed, the squamous portion of the temporal bone is essentially flat, and the lower jawbone is just a bulbous tube enclosing a collection of tooth crowns with a midline that is still unfused, making it not yet even capable of receiving or transmitting significant forces.  Subsequently, the alveolar processes (the bones supporting the teeth) do not form if there are no teeth to receive forces, and the TMJs do not form when there is no condyle.76-77    Even after the TMJs are fully formed, they lose their contours if the condyles are removed or fractured.78-80  Form and function in the jaw system develop together in a harmonious spiral centered around the bite table.  

Functional stimuli like chewing probably stimulate growth by increasing oxygen supply due to the pumping effect of rhythmically alternating forces. In this process, oxygen seems to be a "master controlling switch" – affecting osteoblast metabolism, osteoclast metabolism, and osteoid calcification.52-53   Stimuli that produce osteogenic activity are frequency-specific.  Repetitive loading is osteogenic while constant loading is not. 54-55   

The bite forces that stimulate bone growth are distributed around the whole front half of the cranium, as shown below by Benninghoff, who applied bite forces to a cranium coated with pressure sensitive paint. In pre-industrial eskimos, powerful chewing affected even the cranial vault, producing a distinct thickening along the sagittal suture.69  

The strains produced by biting are highest near the bite table in the lower face, moderate in the middle face, and very low in the upper face.93 The tooth bearing portions of the jawbones and their extensive frameworks of supporting bones experience compressive forces, regions of muscle attachment and insertion (such as the zygomatic arch and the coronoid process) experience tensile forces, and areas between these two portions experienced twisting, bending, and shearing forces.83  In front, the nasal processes carry incisal biting forces from the upper jawbone to the medial (inner) aspects of the supraorbital ridge.  At the canine and premolar areas, the walls of the maxillary sinuses and nasal cavity transfer biting forces up to the sides of the supraorbital ridge and the front portions of the cheekbones. At the molars, the bony prominences over the buccal roots transfer biting forces to the rear portions of the cheekbones, which in turn transfer these forces to the front portions of the temporal bones.  More centrally, biting forces are transferred to the cranial base via the walls of the maxillary sinuses and the wings of the sphenoid bones. 

Where muscles produce functional forces that pull on bones, those bones develop protuberances for the attachments of the muscles.  Where muscles produce bending stresses on bones, those bones develop an internal architecture almost perfectly aligned to withstand those bending forces.   As a result, muscle activity causes the bones at their origins and insertions to strengthen just enough to be able to withstand whatever forces they can apply, and weakness or paralysis of muscles produces bones that are extremely thin and mechanically deficient.50-51  In monkeys, a new layer of bone forms on the supraorbital ridge just after the arrival of each new molar68, and forceful biting bends the whole cranium, opening the sagittal suture that runs along the top of the head.  The mandible thickens as much as needed to resist the functional stress it encounters; therefore the size of the chin is proportional to maximal bite force, the thickness of the condyles is determined by the functional loads they receive 70 71 72 73, the size of the gonial angle varies as a direct function of the size of the masseter and internal pterygoid muscles74-75, and the growth of the coronoid process depends on the presence of the temporal muscle. In animals, softening the diet produces thin craniofacial bones, hardening the diet produces thick craniofacial bones 67, and unilaterally damaging jaw muscles or extracting teeth affects the shape of the cranium.56-66   

In fact, much of postnatal human craniofacial growth and development may be a process of adaptation to biting forces.  The density of all the bones of the cranial vault varies according to jaw and cervical muscle strength.81  Moss pointed out, "The external form of the human skull ... is related directly to imposed loadings, a point verified experimentally in miniature swine skulls.  It is known that unit strains are greatest in infant skulls, less in adolescent skulls and least in adult skulls, suggesting that the growing skull increasingly adapts its structure to masticatory loadings."82 

EARLY BITE FORCES 

The first bite forces that shape the craniofacial area are produced by squeezing the mandible against the tongue or nipple resting between the gum pads.  In response, the TMJs begin to form between the condyles and the temporal bones where opposing periosteal envelopes rubbing against each other produce secondary cartilage on the surfaces of the bones and a fibrocartilaginous pressure-bearing disc from the tendon of the lateral pterygoid muscle, the pressure-bearing articular surfaces of the TMJs become avascular, the TMJ disks acquire a thin central zone surrounded by peripheral wedges, and the upper portions of the TMJs develop bony slopes (articular eminences).    

When the teeth arrive, the bite table replaces the tongue as the platform against which the mandible is squeezed and the jaw closing muscles replace the facial muscles as the source of stabilization for the mandible during swallowing.  Freeing the facial muscles from their crude infantile suckling and swallowing functions allows them to take on the more delicate and complicated functions of speech and facial expression. Experiments have shown that the consistency of the food is at least partly responsible for the change in neuromuscular control.  Older children given a bottle revert to infantile suckling, swallowing, and respiratory rhythms.  

As the jaw muscles develop, biting forces shape the TMJs. The glenoid fossae of the TMJs deepen, the bony slopes at the front of the TMJs begin to develop their characteristic S-shaped profiles, and the cheekbones (zygomatic processes) thicken and begin to bow outward.  By the time the primary dentition is complete, the TMJs are well established and the bony slopes of the TMJs have gained more than half of their adult form. Subsequently, as long as there are still enough teeth to form a bite platform, the structural components of the jawbones keep growing in response to the complex gradient of craniofacial strains produced by biting forces. 

Early bite forces align the teeth. The eruption pathways that the teeth follow into the mouth cannot be controlled very precisely by genetics, therefore their final pathways need to be refined by functional forces as they enter the mouth.  Those functional forces include the light steady soft tissue pressures directed inward from the lips and cheeks and outward from the tongue as well as the eruption forces pushing the teeth out of their basal bones and into the bite table.  Those forces define a trough, called a neutral zone, into which the teeth tend to drift from their eruption pathways.  Because of the importance of these functional forces in alignment of the teeth, dental arch dimensions show very low heretability compared with most other craniofacial dimensions.86-88

BITE STABILITY

The bite table quickly achieves stability, because the eruption of each tooth stops when the bite forces it receives counterbalance the eruption forces that continuously push it out from its basal bones and into the bite table, and the consistency of the biting forces stops all the teeth along the same plane, thereby imparting a uniform height, contour, and stability to the bite table. 

The front teeth meet with an overbite that serves to couple the growth of the upper and lower jawbones and thereby prevent the faster growing lower jawbone from growing past the upper jawbone. The back teeth meet with an interdigitation that refines their alignment by means of the so-called cone and funnel mechanism, illustrated below.     

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Since each upper back tooth interdigitates with two lower back teeth and each lower back tooth interdigitates with two upper back teeth, the interdigitating arrangement of opposing teeth due to this cone and funnel mechanism spreads along the dental arches. 

To ensure that the teeth line up in a manner that not restrict the mandibular range of motion, initial chewing patterns in children include wide lateral thrusts on opening, (as seen below right).  After the bite table is established, the wide lateral opening thrusts disappear, and the chewing pattern reverses to become the normal adult chewing pattern, with the lower jawbone opening near the midline and closing from a more lateral position for maximally effective power-crushing (as seen on the left side illustration below).

chewing_patterns_prim_mod_1.jpgThe stable bite table established on the baby teeth is preserved during the transition to adult teeth by a process in which the adult teeth first erupt in front and in back of the primary bite table to form a structural tripod that supports and extends the bite table before replacing its members (the baby teeth) one or two at a time.  Subsequently, the stable bite table remains a central architectural landmark and a key structural component in the facial growth process, and the forces generated by the jaw muscles on and around the bite table continue to coordinate the growth of the jawbones by molding them to fit the same bite forces.  We can alter the facial growth process by controlling the bite forces by altering the contours of the bite table, and the bite table is an orthopedic structure that we can easily and precisely control non-invasively; but understanding how the bite affects craniofacial growth requires understanding how bite forces affect neurocranial expansion, cartilaginous elongation, maxillary expansion, mandibular translation, and dento-alveolar extrusion.  

NEUROCRANIAL EXPANSION

Bite forces only have minimal influence on neurocranial expansion, because it occurs so early.  Its rapid growth stops at about one year of age, and its growth is almost complete by the age of 7.  Neurocranial expansion enlarges the cranial vault, which is a tabular structure of membrane bones that forms a continuous shell enclosing the expanding brain and eyes.  The cranial vault enlarges as the bones drift away from the center, inner areas less rapidly than outer areas where extensive myelinization is occurring. Lateral and frontal serial X-ray tracings of a growing head look like a slow motion picture of an explosion, as seen on the right side of the illustration below.

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Between the individual cranial bones, growth at the fibrous sutures occurs in sufficient amount to accommodate the expansion.   As a result of this adaptive "fill in" growth, the cranium always expands just enough to perfectly fit the periphery of the brain.  Even when the cranial contents expand much more quickly than normal in hydrocephaly, the sutures are still able to produce enough bone to maintain a continuous shell around the grossly enlarged cranium.   

Like the cranial vault, the orbits also contain an expanding neural mass enclosed by plates of bone connected by adaptive sutures. Removal of the eyeball during growth results in deficiencies in the anterior and lateral growth of the midface.   

While the expansion of the cranium and the orbits is motivated by enlargement of the enclosed neural contents, the shape ultimately acquired by the cranium is at least partly determined by externally imposed forces.84 85  Some pre-industrial human tribes successfully altered head shapes by binding their infants' heads, apparently without impairing brain development.  Limiting cranial growth in one direction causes it to expand in other directions, like pushing on a lump of clay.  For example, compression of the cranium vertically by strong jaw closing muscles favors growth horizontally.  As a result, pre-industrial humans with relatively strong overall musculature had crania that were relatively short and wide (brachycephalic), while pre-industrial humans with relatively weak overall musculature developed crania and faces that were relatively tall and narrow (dolichocephalic). 

CRANIAL BASE ELONGATION 

Functional forces have only slightly more influence on the elongation of the cartilage of the cranial base, the next growth process to shape the craniofacial area. The cranial base is a thick spline which extends from back to front along the midline of the floor of the cranium to form a stable structure on which the brain rests, and it does not burgeon out in response to neurocranial expansion as readily as the thin plates of membrane bone bordering the other sides of the vault.  Instead, the cranial base holds its shape, much like the reinforced bottom of a box which contains an expanding mass, as seen in the illustration below.  The relative independence of cranial base growth from neurocranial expansion can be seen in the way it is only slightly affected in microcephaly and hydrocephaly, while the rest of the cranial vault becomes grossly distorted.

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At the same time, the cranial base grows interstitially due to endochondral ossification, which causes it to elongate like the long bones of the limbs or the vertebrae. As seen below, the cranial base is actually comprised of two sections, a front portion and a back portion, (the basi-occiput and the baso-sphenoid), which are actually phylogenetically cephalized vertebrae that function like cartilaginous growth plates arranged back to back and connected at an angle of about 130 to 135 degrees.   Their growth peaks at puberty but then continues at least through the second decade of life after other cartilaginous growth has ended.  Because the upper jawbone grows from the front section, while the lower jawbone grows from the back section, the angle formed by the cranial base is an important determinant of jawbone relationships.  Sharp cranial base angles produce faces with more rearward growing upper jawbones and more forward growing lower jawbones, while obtuse cranial base angles produce faces with more forward growing upper jawbones and more backward growing (Angle's class 2) lower jawbones, at least in the midline. The lateral portions of the face grow more in response to bite forces.

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Elongation of the more vertically oriented posterior portion of the cranial base causes increases facial height by pushing the cranium up and away from the shoulder girdle and chest.  As a result, facial height increases in proportion to body height and thereby dramatically changes its proportions between childhood and adulthood, as seen below.  

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Elongation of the more horizontally oriented anterior portion of the cranial base pushes the central portion of the face forward.  People with a genetic defect that prevents the cartilage of the cranial base from expanding normally develop a face that looks as if it had been pushed in at its center.  The cartilage of the nasal septum may function as the forward-most extension of the anterior cranial base.   

FACIAL TRANSLATION

From the undersides of the cranial base and the front of the cranial vault, the face grows down and forward.  The general direction of this growth can be seen in the circum-maxillary sutures which are oriented in parallel, as shown below.  

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Unlike the rest of the cranial sutures, these cirum-maxillary sutures stay open throughout life,  because they function like shock absorbers for bite forces.  Experiments have shown that continued slight interosseous movements at sutures keeps them open, while experimental immobilization of sutures leads to ossification and suture closure. 90 91 91.1  Studies have also shown that muscular forces can cause relative movement of the adjacent bones and thereby delay or prevent closure of the suture joining them.91.2    Softening the diet, which diminishes movement at the sutures by exposing them to smaller bite forces produces premature obliteration of facial sutures in rats.  

The downward and forward facial growth pattern causes the facial mask to gradually swing out from the underside of the front of the cranium, as if it were hinged at the forehead, and the profile flattens between infancy and adulthood as shown below.

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The advancement at the midline is largely controlled by cartilaginous elongation, while the advancement of the molars and premolars is controlled more by bite forces.  Because the jaw muscles are all arranged vertically, bite forces produce advancement and limit vertical growth.  Muscle disease or injury cause extremely long anterior faces, and people who chew very forcefully have extremely short anterior faces.  The mechanisms by which bite forces affect facial growth are entirely different in the upper and lower jaws, as discussed below.

THE CRANIOFACIAL GROWTH MATRIX

The angle at which each individual face swings out and grows down and forward is one of the features that produces a characteristic appearance that makes people recognizable throughout life.  Looking at this stability of facial growth patterns, Brodie remarked, "The only agent that could be responsible for such stability was the musculature that connected the mandible with surrounding parts.  It was apparent that this musculature grew in the same orderly fashion as did the bony skeleton of the head and led to a stable relationship of the mandible in each person."  The stability of a typical craniofacial growth pattern can be seen below.

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The stability of this craniofacial growth matrix is due to the field of relatively consistent resting muscle tonus that envelopes the body and creates a "neutral zone" that controls the external shapes of the bones.  Any shift of a bone away from the neutral zone creates an imbalance between opposing myofascial pulls and thereby causes a constant light tension pulling the bone back toward its neutral zone or returning it to its original shape.  Surgeons find that rapid resorption occurs in any part of a bone graft which is located beyond the tension zone controlled by the musculature, and any change in the passive tension of the myofascial curtain can reshape the underlying bones.  The passive tension of the myofascial curtains draped from the front of the cranium down onto the shoulder girdle and sternum in resting posture maintains the resting position of the mandible, and the tonus of the facial muscles maintains the contours of the facial mask, which keeps each face unique and recognizable throughout life.  As a result, although longitudinal studies of children have shown that annual increments of individual facial bones are not evenly distributed among the various bony elements, (some grow faster one year and others grow faster the next year); diminished growth of any one bone is always compensated for by increased growth in neighboring bones, and the steadiness of the overall matrix is preserved.  Even after an experimental bite interference has caused a growth deformity, removal of the experimental bite interference is followed by compensatory growth which re-establishes symmetry.  Similarly, after functional orthodontic appliances are used to alter growth, the treatment period is often followed by "catch up" growth that at least partially restores the previous facial growth pattern. 

INTRAMATRIX CRANIOFACIAL GROWTH

Hidden within that steady craniofacial growth matrix, the upper and lower jawbones have completely independent growth patterns.  They are both designed to contribute to the stability of the matrix by compensating for whatever rate of tooth wear occurred to maintain a steady bite table.  For that reason, they both get stimulated by functional forces.  Thus they grow fastest when they are needed most - in people who chew forcefully enough to wear their teeth down quickly. However they grow by different mechanisms, in slightly different directions, and at different rates.  Between them, the bite table functions like a suture to compensate for differences between the maxillary and mandibular growth patterns.  Around them, the light steady forces of postural tonus hide this jawbone growth so effectively that it was not even suspected until researchers started using implants in longitudinal studies.  Wherever jawbone growth runs into the steady matrix maintained by the muscle postures, bone gets resorbed; and wherever jawbone growth carries a bone away from the steady matrix maintained by the muscle postures, just enough new bone gets deposited to fill in the space.  

MAXILLARY EXPANSION 

The upper jawbone expands primarily due to rotation of its two shell-like membrane bones away from their midline connection, like unfolding a box, to create a platform that can absorb the power-crushing forces that the mandible applies upward and forward against it.  

One way the upper jawbone unfolds is by its right and left maxillary bones rotating around an axis through the midpalatal suture, as can be seen from left to right in the illustration below.  As chewing forces drive the bones upward and outward around their midline connection, they flatten the roof of the palate.  In our ancestors, strong chewers had flat wide palates.

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The other way the upper jawbone unfolds is around its front end, as seen from left to right in the illustration below.  In the presence of vigorous chewing, there is more swinging out of the paired membrane bones around their front ends, which flattens the face.  

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The width of the palate is proportional to the strength of the jaw muscles.  The role of bite forces in this maxillary expansion can be seen in the dramatic effects created by wearing a spinal realignment tool called a Milwaukee brace a few decades ago.  The brace pushed up forcefully on their lower jawbones, which applied continuous bite forces to their upper teeth, which caused extreme expansion of the upper jawbone and outward splaying of all the upper teeth.  

The expansion of the upper jawbone enlarges the nasal airway by widening the floor of the nasal airway as well as the buttresses that carried chewing forces around the nasal airway.  Pre-industrial humans who were strong chewers developed wide flat midfacial structures, including small zygomaxillary angles, large nasomalar and zygomaxillary angles, and flared zygomas. As the structural components of the midface shift laterally, their inner aspects resorb, leaving room for expansion of the sinuses and the nasal airway. Over time, the distribution of bone in the midface becomes virtually identical to the stress distribution experienced by that area during loading, and the midface becomes a lightweight and efficient honeycomb of thin membrane bones ideally constructed to withstand and distribute functional forces. 

ADVANCEMENT AND UPWARD ROTATION OF THE MANDIBULAR CORPUS

On the other side of the bite table, the horseshoe shaped portion of the mandible that houses the lower dental arch (the mandibular corpus), shown below right in black, is advanced and rotated slightly upward in front, supported by growth of bone at its back end (the posterior surface of the ramus) and especially at the mandibular condyles, as if it were suspended by continuously elongating handles. 

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This intramatrix growth is designed to continually carry the roots of the lower teeth further up into the bite table and against the upper teeth in order to compensate for the loss of biting surface caused by continual tooth wear.  People with relatively strong chewing activity and strong jaw muscles needed and also experienced more advancement/upward rotation of the mandibular corpus, because they were the people who experienced the most tooth wear and thereby needed the increased facial growth to compensate for that wear.

Growth at the mandibular condyles, stays highly adaptive throughout life due to periosteum-like properties from a proliferative layer of undifferentiated mesenchymal cells that grow as much as needed to maintain the necessary length of the handle that holds the front half of the lower jawbone under the upper jawbone; even when it become displaced due to disease, injury, extreme functional habits, functional orthodontic appliances, loss of teeth, or surgery.  In rats, experimentally holding the jaw partly open redirects condylar growth until it creates a new handle with a curved shape that reconnects the back ends of the lower jawbone in it new position with the glenoid fossae in the temporal bones to maintain the TMJs.  In rabbits, experimentally shifting the rear portion of the lower jawbone further backward triggers an increase in condylar growth until the integrity of the handle is re-established.  In humans, surgical removal of a condyle is routinely followed by spontaneous regeneration of a new condyle with a functional articular head and condylar neck contained within a normal synovium and in some cases with a fibrocartilaginous cap.  During normal growth, as the corpus of the mandible advances, osteoblasts lay down as much bone as necessary behind the advancement so the ramus can push the corpus forward and upward while maintaining its position as a member of the postural system and controlled by the tendon of the temporalis muscle. 

Many researchers have commented on the important role that condylar adaptability plays in human growth.  Enlow says, "The variable capacity of condylar growth provides adaptation to different facial types, different articular patterns between the individually variable configuration and dimensions of the cranial floor and maxilla, different occlusal patterns, and normal structural changes occurring in conjunction with progressive growth.  As the whole mandible becomes displaced in whatever vectors are involved at different ages and in whatever variations occur among different individuals, the condylar cartilage and the contiguous membranes forming the intramembranous bone of the condylar cortex and the condylar neck grow in whatever directions and in whatever amounts are required to sustain constant functional position and articulation with the cranial floor.”  Petrovic says, “The condylar cartilage growth is integrated into an organized functional whole having the form of a servosystem, which is able to modulate the lengthening of the condyle in such a way that, through postnatal growth, the lengthening of the lower jaw adapts to the lengthening of the upper jaw.” 

Because bite forces largely power the upward rotation of the mandibular corpus, the length of the front of the face is inversely proportional to jaw muscle strength.  When disease or injury damages the jaw muscles, the mandibular corpus rotates sharply down and back. A longitudinal growth study of a patient with muscular dystrophy below shows extreme downward and backward mandibular rotation, compared with the white line showing normal growth in the X-ray on the right side below, because there are no bite forces to oppose the influence of gravity and eruption of the teeth and the alveolar processes.  

krieborg_dotted.png krie.png

Generally, the upward rotation of the mandibular corpus can be seen most clearly relative to the two rami behind it, which function as the handles from which the corpus is suspended.  The rami are stable architectural landmarks, because their positions are controlled by the steady postural tensions of the temporalis muscles, so they function somewhat as a reference point from which the rotation of the corpus can be measured at their intersection - the gonial angles.  Gonial angles are acute in people with strong jaw muscles and obtuse in people with weak jaw muscles.  Generally the gonial angle is obtuse in youth when chewing forces are still small, it becomes more acute with adulthood and increasing jaw muscle strength, and it becomes more obtuse again later in life when the jaw muscles become weak from the effects of aging, as illustrated below.

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COORDINATION OF GROWTH IN THE JAWBONES

The coincidence of advancing the mandibular corpus and expanding the maxilla keeps the lines of upper and lower teeth in close proximity, because a wider portion of the lower dental arch comes to lie under the same area of the upper dental arch, which is simultaneously widening directly.  In dental language, growth brings the mandibular buccal cusp tips up the posteriorly and medially facing inclines of the buccal cusps of the maxillary teeth, even as expansion of the maxillary bite table moves the maxillary teeth further laterally.  In such a manner, the mandibular molars shift anteriorly relative to the maxillary molars while the maxillary molars move laterally relative to the mandibular molars. The net effect is to keep the upper and lower teeth in close proximity for efficient chewing while some slippage between them allows the upper and lower jawbones to shift in slightly different directions as a result of their diverse growth processes.  

THE MAXILLO-MANDIBULAR SUTURE - THE DENTAL JOINT

Connecting and coordinating these diverse growth processes in the upper and lower jawbones, the bite must allow such slippage.  The bite functions like one large dentate maxillo-mandibular joint connecting the tooth containing portions of the lower and upper jawbones and employing the upper and lower bite tables as its articular surfaces. Like other cranial sutures, the dental suture adaptively connects the growth processes on its two sides. Alterations in the growth of one area of the upper jawbone affects growth in the opposing area of the lower jawbone, and vice-versa.92  Adaptive growth at the dental joint maintains the stability of the bite table despite damage to a tooth or even an area of teeth.  Adaptive growth at the dental joint also accommodates both the advancement of the mandibular corpus and the expansion of the maxilla while maintaining a stable bite table, whether wear of the teeth is slow or fast.  However, unlike other cranial sutures, growth at this dental suture is provided by the continual eruption of the teeth rather than proliferation of bone, requiring a number of special mechanisms that were embedded in our jaw systems in order to maximize adaptability.   By adapting its structure to fit the functional forces it encounters, the human jaw system is designed to be able to deal with almost any food source.  However, the human jaw system was not designed to deal with a situation that was almost never encountered in evolution - insufficient functional forces. 

 

FOOTNOTES

48 Wedel A, Carlsson GE, Sagne S. Temporomandibular joint morphology in a medieval skull material. Swed Dent J 1978;2:177-187.

49 Ackermann R, Krovitz G E. Common patterns of facial ontogeny in the hominid lineage. Anat Rec 2002; 269:142-147.

50 Rubin C., McLeod K., Gross T., and Donahue H.; Physical stimuli as potent determinants of bone morphology; in Bone Biodynamics in Orthodontic and Orthopedic Treatment; Carlson D. and Goldstein S. (eds) vol 27 Craniofacial Growth Series. Center for Human Growth and Development, University of Michigan, Ann Arbor p 75-91, 199 

51 (Schumacher G.;Factors Influencing Craniofacial Growth. p 16 in Normal and Abnormal Bone Growth; Basic and Clinical Research. Dixon A. and Sarnat B. (eds) Alan R. Liss Inc. New York 1985.

52 Barker M., Ho D, and Tuncay O.;Metabolic response of osteoblasts to varying oxygen tensions. on p 36 of Orthodontic Review, Nov.-Dec. 1992.

53 Liskova M., and Hert J.; Reaction of bone to mechanical stimuli. Part 2. Periosteal and endosteal reaction of tibial diaphysis in rabbits to intermittent loading. Folia Morph. 19:301-317, 197 

54 Bouvier M. and Hylander W.; Effect of bone strain on cortical bone structure in Macaques. Journal of Morphology 167:1-12, 198 

55 Rubin C., McLeod K., Gross T.,  and Donahue H.; Physical stimuli as potent determinants of bone morphology, in Bone Biodynamics in Orthodontic and Orthopedic Treatment, volume 27, Craniofacial Growth series. Center for Human Growth and Development, Ann Arbor, Michigan 1992 p 75-9 

56   Lu, C., and Sebata, M.: The craniofacial development of rats after denervation of the mandibular nerve, Bull Tokyo dent coll. vol 22 #1 pp. 29-39, Feb. 198 

57   Byrd K.: Masticatory movements and EMG activity following electrolytic lesions of the trigeminal motor nucleus in growing guinea pigs, Am J Ortho, vol 86 #2 p146-161, 1984.

58   Schumacher, G.; Factors influencing craniofacial growth, in Normal and Abnormal Bone Growth p 3-22.

59   Washburn S.; The relation of the temporal muscle to the form of the skull. Anat Rec 99:239-248, 1947.

60   Horowitz S. and Shapiro H.; Modification of skull and jaw architecture following removal of the masseter muscle in the rat. Am J Phys Anthrop 13:301-308, 1955.

61   Horowitz S. and Shapiro H; Modifications of mandibular architecture following removal of temporalis muscle in the rat. J Dent Res 30:276-280, 195 

62   Avis V.; The significance of the angle of the mandible: An experimental and comparative study. Am J Phys Anthrop 19:55-61, 196 

63   Phillips C. Shapiro P., and Luschei E.; Morphologic alterations in Macaca mulatta following destruction of the motor nucleus of the trigeminal nerve. Am J Orthod 81:292-298, 1982.

64   Kikuchi M. Lu C., Sebata M., and Yamamoto Y.; The mandibular development of the rat after the denervation of the masseteric nerve. Bull of Tokyo Dent Coll 19:75-86, 1978.

65   Baker L.;  The influence of the forces of occlusion on the development of the bones of the skull. Int J Orthod. 8, 1922.

66   Hylander W.;The adaptive significance of Eskimo craniofacial morphology p 129 in Dahlberg A. and Graber T. (eds) Orofacial Growth and Development. Mouton Publishers, Paris 1977.

67   Menegaz RA, Sublett SV et al. Evidence for the Influence of Diet on Cranial Form and Robusticity. Anatomical Record 2010;293(4)630-64 

68 Walker A. personal communication 

69 Hylander W.;The adaptive significance of Eskimo craniofacial morphology p 129 in Dahlberg A. and Graber T. (eds) Orofacial Growth and Development. Mouton Publishers, Paris 1977.

70   Avis, V.;The significance of the angle of the mandible: an experimental and comparative study. Amer J Phys Anthrop. 19, 55. 196 

71 10. Petrovic A., Stutzmann J., and Oudet C.;Control processes in the postnatal growth of the condylar cartilage of the mandible. in:McNamara J. (ed)  Determinants of mandibular form and growth, Monograph # 4, Craniofacial growth series. Center for human growth and development, University of Michigan, Ann Arbor 1975, pp 101-154.

72  Horowitz S. and Shapiro, H.;Modification of skull and jaw architecture following the removal of the masseter muscle in the rat. Am J Phys Anthrop 13, 30  1955.

73   Kantomaa T., and Ronning O.;The effect of the electrical stimulation of the lateral pterygoid muscle on the growth of the mandible in the rat. Proc of the Finnish Dental Society 78:215-219, 1982.

74   Avis, V.;The significance of the angle of the mandible: an experimental and comparative study. Amer J Phys Anthrop. 19, 55. 196 

75  Horowitz S. and Shapiro, H.;Modification of skull and jaw architecture following the removal of the masseter muscle in the rat. Am J Phys Anthrop 13, 30  1955

76  (Moffett BC, Johnson LC, McCabe JB, Askew HC. Articular remodeling in the adult temporomandibular joint. Am J Anat. 1964;115:119-142.)          Kazanjian V.;Congenital absence of the ramus of the mandible. J Bone and Joint Surg. 21:761-772,1939.

77   Kazanjian V.;Congenital absence of the ramus of the mandible. Am J Orthodont. 26:175-187, 1940.

78   Sarnat B., and Engel M.:A serial study of mandibular growth after removal of the condyle in the Macaca rhesus monkey. Plast Reconstr Surg. 7:364-380, 195 

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