Zi Jun Liu

Jaw muscles and the skull in mammals: the biomechanics of mastication

Among non-mammalian vertebrates, rigid skulls with tight sutural junctions are associated with high levels of cranial loading. The rigid skulls of mammals presumably act to resist the stresses of mastication. The pig, Sus scrofa, is a generalized ungulate with a diet rich in resistant foods. This report synthesizes previous work using strain gages bonded to the bones and sutures of the braincase, zygomatic arch, jaw joint, and mandible with new studies on the maxilla. Strains were recorded during unrestrained mastication and/or in anesthetized pigs during muscle stimulation. Bone strains were 100-1000 micro epsilon, except in the braincase, but sutural strains were higher, regardless of region. Strain regimes were specific to different regions, indicating that theoretical treatment of the skull as a unitary structure is probably incorrect. Muscle contraction, especially the masseter, caused strain patterns by four mechanisms: (1) direct loading of muscle attachment areas; (2) a compressive reaction force at the jaw joint; (3) bite force loading on the snout and mandible; and (4) movement causing new points of contact between mandible and cranium. Some expected patterns of loading were not seen. Most notably, strains did not differ for right and left chewing, perhaps because pigs have bilateral occlusion and masseter activity.

Functional Properties of Jaw and Tongue Muscles in Rats Fed a Liquid Diet after Being Weaned

Decreased masticatory demands due to liquid or soft diets cause a reduction in the growth of craniofacial bones and in the development of feeding musculature, but the effects on masticatory function and jaw/tongue muscle activities are unclear. The present study was undertaken to test the hypotheses that a liquid diet feeding after weaning affects the critical-period programming of mastication and the motor performances of jaw and tongue muscles. Thirty-six male Wistar rats were divided into two equals groups at weaning and fed either a solid (solid-diet group) or a liquid (liquid-diet group) diet until they reached 50 days of age. Electromyograms (EMG) of the masseter, medial pterygoid, temporalis, anterior digastric, styloglossus, and genioglossus were recorded while animals were naturally ingesting ordinary pellets, apple cubes, and a liquid diet. It was found that: (1) a more irregular chewing rhythm, a shorter chewing sequence, and a longer chewing cycle were found in the liquid-diet group, but there were no differences observed during lapping/licking between the two groups; (2) during the chewing cycles, the EMG onset of each muscle in relation to that of the masseter in the liquid-diet group was similar to that in the lapping/licking cycles in both groups; (3) the activities of jaw elevators (masseter, medial pterygoid, and temporalis) during the chewing cycles were significantly higher in the liquid-diet group; and (4) the increase in the EMG activities of jaw elevators during pellet chewing compared with apple cube chewing was significantly weaker in the liquid-diet group, whereas such an enhancement was found simultaneously in the styloglossus in the solid-diet group, and in the anterior digastric in the liquid-diet group. These findings verify that: (1) the motor output of jaw and tongue muscles may be altered in rats fed a liquid diet after being weaned; (2) the feeding of a liquid diet to rats after being weaned may obstruct the functional transition from suckling to mastication; and (3) jaw elevators that develop without motor learning of mastication are inefficiency when performing functionally.

Modulation of mandibular loading and bite force in mammals during mastication

SUMMARY Modulation of force during mammalian mastication provides insight into force modulation in rhythmic, cyclic behaviors. This study uses in vivo bone strain data from the mandibular corpus to test two hypotheses regarding bite force modulation during rhythmic mastication in mammals: (1) that bite force is modulated by varying the duration of force production, or (2) that bite force is modulated by varying the rate at which force is produced. The data sample consists of rosette strain data from 40 experiments on 11 species of mammals, including six primate genera and four nonprimate species: goats, pigs, horses and alpacas. Bivariate correlation and multiple regression methods are used to assess relationships between maximum (ϵ1) and minimum (ϵ2) principal strain magnitudes and the following variables: loading time and mean loading rate from 5% of peak to peak strain, unloading time and mean unloading rate from peak to 5% of peak strain, chew cycle duration, and chew duty factor. Bivariate correlations reveal that in the majority of experiments strain magnitudes are significantly (P<0.001) correlated with strain loading and unloading rates and not with strain loading and unloading times. In those cases when strain magnitudes are also correlated with loading times, strain magnitudes are more highly correlated with loading rate than loading time. Multiple regression analyses reveal that variation in strain magnitude is best explained by variation in loading rate. Loading time and related temporal variables (such as overall chew cycle time and chew duty factor) do not explain significant amounts of additional variance. Few and only weak correlations were found between strain magnitude and chew cycle time and chew duty factor. These data suggest that bite force modulation during rhythmic mastication in mammals is mainly achieved by modulating the rate at which force is generated within a chew cycle, and less so by varying temporal parameters. Rate modulation rather than time modulation may allow rhythmic mastication to proceed at a relatively constant frequency, simplifying motor control computation.)

Temporomandibular joint in miniature pigs: Anatomy, cell replication, and relation to loading

The mechanical environment is a regulator of growth and adaptation of the musculoskeletal system, including joints. Although pigs (Sus scrofa) are used frequently as models for temporomandibular joint (TMJ) dysfunction, no systematic description of microanatomy exists for this species. We injected the thymidine analog 5‐bromo‐2′‐deoxyuridine (BrdU) into 10‐ to 11‐month‐old miniature pigs that were undergoing measurements of TMJ bone strain. Ten hr later, the animals were sacrificed and their heads were perfused. Histological sections were used to map the distribution of replicating cells. Additional observations were made on gross dissections of jaw joints obtained from an abattoir. The pig TMJ is better supported than that of humans laterally and medially, but more vulnerable posteriorly. The posterior attachment area of the intra‐articular disc is fibro‐fatty rather than vascular, as in humans. Cartilage lines the articular eminence as well as the condylar surface. At the posterosuperior region of the condyle, the cartilage ends abruptly and is replaced by an invaginating, actively replicating periosteum. Almost all of the BrdU‐labeled cells resided in the prechondroblastic zones. The condyle had more replicating cells than did the eminence (P < 0.02), but lateral and medial locations did not differ in either element. In sagittal sections, the condyle had more replicating cells posteriorly (P < 0.001), but no A‐P differences were seen in the eminence. Comparisons of these data with data on bone strain indicate that increased loading is negatively associated with cell replication. Anat Rec 266:152–166, 2002.

Movement of temporomandibular joint tissues during mastication and passive manipulation in miniature pigs

Movement is an important aspect of the biomechanics of the temporomandibular joint (TMJ). To track the relative movements of TMJ components, radio-opaque markers were implanted in the left squamosal bone, mandible and retrodiscal tissue of miniature pigs. Medial-lateral (ML) and dorsal-ventral (DV) fluoroscopic records were made 8-10 weeks later during chewing and passive manipulation. Marker movements were digitized from the videotapes. During passive manipulation, the deformation of the lateral capsule was also measured with a differential variable-reluctance transducer. The results provide new details about porcine chewing pattern, which is distinguished by a regularly alternating chewing side. During masticatory opening, the mandible had a centre of rotation (CR) well inferior to the condyle and close to the angle. In contrast, the passive opening movement showed a higher CR location close to the condylar neck, indicating a different motion from masticatory opening. The retrodiscal tissue followed the movements of the mandibular condyle during both mastication and passive manipulation. The lateral capsule elongated during ipsilateral shifts and retrusion, implying a possible role in limiting such movements. These movement characteristics provide a useful reference for studies on the TMJ using pigs.

Bone surface strains and internal bony pressures at the jaw joint of the miniature pig during masticatory muscle contraction

The long-standing debate on whether the jaw joint is loaded is due in part to the complexity of the factors involved, including a number of different muscles, each with a potentially unique role. This study sought to elucidate how two major jaw muscles, the masseter and the lateral pterygoid, influence jaw-joint loading. Twenty-five 10-month-old miniature pigs were divided into two groups, controls and pigs with the lateral capsular ligament of the jaw joint stripped surgically; this was expected to affect loading by destabilizing the joint. Rosette strain gauges were bonded to: (1) the lateral surface of the squamosal bone (equivalent to the squamosal portion of the temporal bone in humans) at the level of the articular eminence; (2) the lateral surface of the condylar neck; and (3) the lateral surface of the mandibular corpus below the molar region. Semiconductor pressure transducers were placed underneath the surfaces of the anterior slope of the condyle and the posterior slope of the articular eminence through drilled holes. Strains and internal bony pressures were recorded during stimulated tetanic contractions of the masseter or lateral pterygoid muscles. Masseter contraction, either alone or with the contralateral muscle, caused net tension in the squamosal bone and net compression in the condylar neck. The orientations were approximately vertical to the occlusal plane. Masseter contraction elevated both the condylar and eminence pressures from their resting values. The strains caused by lateral pterygoid contractions were much smaller than for the masseter with the exception of the condylar location. Ipsilateral lateral pterygoid contraction decreased both the condylar and eminence pressures from their resting values, perhaps because condylar movement altered the contact between the joint surfaces. Surgical disruption enhanced both pressure changes and bone strains under either muscle contraction but their overall patterns were not altered. In conclusion, both strains and pressures in the jaw joint varied according to specific muscle activity.

Loading of the Temporomandibular Joint: Anatomical and in vivo Evidence from the Bones

‘Loading of the TMJ’ is usually understood to mean a compressive force applied to the articular surfaces of the jaw joint. Theoretical models of jaw mechanics can be manipulated to support either the presence or the absence of loading, depending on the assumed contraction patterns of the muscles and the assumed occlusion. This paper synthesizes a series of studies on jaw joint function using pigs as substitutes for humans. Bone strain (deformation) was directly measured on the lateral surfaces of the condylar neck and the squamosal (equivalent to the human temporal) bone. Chewing strains indicate that loading does occur and is not light. The peak strains on the condyle are indeed primarily compressive, but the situation is dynamic. Small tensile strains can occur during chewing, and protrusive splints may decrease the strain resulting from muscle stimulation. The squamosal bone is even more surprising, in that the major strain is tensile. The most likely explanation for this finding is that the squamosal bone is bent under the load. Thus, the two elements of the TMJ are deformed in different ways by the same movements and muscle activities. Internal bony architecture reflects these differences. The condyle is filled with fine, vertically oriented bony trabeculae. The articular eminence has thick cortices and trabeculae oriented approximately transversely. In conclusion, the TMJ is loaded, but the situation is complex. The largest forces seen by the condyle are compressive, and they arise from muscle contraction. These same forces serve to bend the squamosal bone.

Botulinum toxin in masticatory muscles: Short- and long-term effects on muscle, bone, and craniofacial function in adult rabbits

Paralysis of the masticatory muscles using botulinum toxin (BTX) is a common treatment for cosmetic reduction of the masseters as well as for conditions involving muscle spasm and pain. The effects of this treatment on mastication have not been evaluated, and claims that the treatment unloads the jaw joint and mandible have not been validated. If BTX treatment does decrease mandibular loading, osteopenia might ensue as an adverse result. Rabbits received a single dose of BTX or saline into one randomly chosen masseter muscle and were followed for 4 or 12 weeks. Masticatory muscle activity was assessed weekly, and incisor bite force elicited by stimulation of each masseter was measured periodically. At the endpoint, strain gages were installed on the neck of the mandibular condyle and on the molar area of the mandible for in vivo bone strain recording during mastication and muscle stimulation. After termination, muscles were weighed and mandibular segments were scanned with micro CT. BTX paralysis of one masseter did not alter chewing side or rate, in part because of compensation by the medial pterygoid muscle. Masseter-induced bite force was dramatically decreased. Analysis of bone strain data suggested that at 4 weeks, the mandibular condyle of the BTX-injected side was underloaded, as were both sides of the molar area. Bone quantity and quality were severely decreased specifically at these underloaded locations, especially the injection-side condylar head. At 12 weeks, most functional parameters were near their pre-injection levels, but the injected masseter still exhibited atrophy and percent bone area was still low in the condylar head. In conclusion, although the performance of mastication was only minimally harmed by BTX paralysis of the masseter, the resulting underloading was sufficient to cause notable and persistent bone loss, particularly at the temporomandibular joint.

Effects of tongue volume reduction on craniofacial growth: A longitudinal study on orofacial skeletons and dental arches

The interaction between tongue size/volume and craniofacial skeletal growth is essential for understanding the mechanism of specific types of malocclusion and objectively measuring outcomes of various surgical and/or orthodontic treatments. Currently available information on this interaction is limited. This study was designed to examine how tongue body volume reduction affects craniofacial skeleton and dental arch formation during the rapid growth period in five 12-week-old Yucatan minipig sibling pairs. One of each pair received a standardized reduction glossectomy to reduce tongue volume by 15-17% (reduction group), and the other had the reduction glossectomy incisions without tissue removal (sham group). Before surgery, five stainless steel screws were implanted into standardized craniofacial skeletal locations. A series of cephalograms, lateral and axial, were obtained longitudinally at 1 week preoperative, and 2 and 4 weeks postoperative. These images were traced using superimposition, and linear and angular variables were measured digitally. Upon euthanasia, direct osteometric measurements were obtained from harvested skulls. Five en-bloc bone pieces were further cut for bone mineral examination by dual photon/energy X-ray absorptiometry (DEXA). The results indicate that: (1) while daily food consumption and weekly body weight were not significantly affected, tongue volume reduction showed an overall negative effect on the linear expansion of craniofacial skeletons; (2) premaxilla and mandibular symphysis lengths, and anterior dental arch width were significantly less in reduction than sham animals at 2 and/or 4 weeks after the surgery; (3) both premaxilla/maxilla and mandible bone mineral density and content were lower in reduction than sham animals, significantly lower in anterior mandible; (4) craniofacial skeletal and dental arch size were significantly smaller in reduction than sham animals, being most significant in the mandibular anterior length and ramus height, the anterior dental arch and midface width. These results suggest that reducing tongue body volume in young animals slows craniofacial skeletal growth and anterior dental arch expansion during rapid growth. The mandible, in particular its symphysis portion, and the anterior dental arch width are most affected. These effects may in part contribute to the decrease of functional loads in the anterior mouth by a volume-reduced tongue.

Effect of distraction rate and consolidation period on bone density following mandibular osteodistraction in rats

The high cost of large animal protocols has limited the study of distraction osteogenesis (DO) in the craniofacial region. This study was designed to characterise a rat model for DO with regard to distraction rate and consolidation period. Unilateral mandibular distraction was performed on 129 male Sprague-Dawley rats using an osteotomy from the sigmoid notch to the inferior border of mandible. After a 3-day latency, 12 groups of 8-9 rats underwent distraction for 5 days at four different rates (0, 0.2, 0.4, 0.6mm per day), with three different post-osteotomy sacrifice times (10, 24, and 38 days) and four final predicted distraction lengths (0, 1, 2, and 3mm). Another four groups of rats (N=8 per group) were sacrificed 6 days post-osteotomy, resulting in distraction for 3 days with a predicted distraction length of 0, 0.6, 1.2, 1.8mm. Changes in mandibular morphology were measured from radiographs of disarticluated hemimandibles. The bone density of the regenerate and control sites was measured using microdensitometry calibrated with an epoxy stepwedge. Distraction linearly increased mandibular length, distraction gap width and the area of the distraction gap (P<0.00005). Mandibular length increased by 0.394 mm per distraction rate. Gap width and area increased by 0.67 and 5.8mm(2) per distraction rate, respectively. The increase in length represents only 39.4% of what was predicted, suggesting that compensatory alteration in condylar or mandibular morphology may have occurred. This speculation was further supported by the finding that mandibular length, measured without the condylar landmark, was 53.8% of predicted. During DO and early consolidation, the measures of bone density in the regenerates decreased compared to control for all groups. Thereafter, bone density in the regenerates generally increased in all groups until day 24 (P<0.01), obtaining levels that were comparable to the unoperated side. At both rostral and caudal sites adjacent to the osteotomies, measures of bone density were enhanced over control in all groups, with the rostral site also showing significant increases over time in the sham and the highest distraction groups (P<0.008 and P<0.014). We conclude that this rat model for mandibular distraction osteogenesis provides bone density changes that are consistent with those reported using larger animal protocols.