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Bone Strain Patterns of the Zygomatic Complex in Response to Simulated Orthopedic ForcesDepartments of Orthodontics and Bioengineering (MC 841), University of Illinois at Chicago, Colleges of Dentistry and Engineering, 801 South Paulina Street, Chicago, IL 60612-7211, USA; Correspondence: * corresponding author, jmao2{at}uic.edu
Craniofacial bone strain upon orthopedic loading has rarely been characterized, despite its fundamental importance in our understanding of the anabolic and catabolic effects of orthopedic forces. The present study tested the hypothesis that zygomatic bone strain is modulated upon loading by headgear, a device widely used in craniofacial orthopedics. Ramp forces from 0 to 50 Newtons were applied via headgear attached to the permanent maxillary first molars in four juvenile and five adult human skulls. The average peak bone strain of the juvenile temporal articular eminence was significantly higher than the adult articular eminence (p < 0.05). Contrasting bone strain patterns were identified in the zygomatic arch: tensile in its lateral surface but compressive in its medial surface. The peak bone strain of the temporal articular eminence and the zygomatic arch both depend upon loading direction. Thus, headgear-generated orthopedic forces evoke bending of the zygomatic arch and stresses of the temporal articular eminence in vitro, suggesting the need to verify whether bone strain induces in vivo bone modeling and remodeling.
Key Words: bone • bone strain • headgear • orthopedics • orthodontics
Craniofacial orthopedics aims at effectively changing the macroscopic shape of the craniofacial skeleton by using mechanical forces in patients with dentofacial deformities and craniofacial anomalies. Exogenous forces applied to bone are transmitted as bone strain. Bone strain directly or indirectly evokes microscopic structural changes in bone, the sum of which leads to macroscopic changes in shape (Martin et al., 1998). Cranial bone strain upon orthopedic loading has rarely been characterized, despite its fundamental importance in our understanding of the anabolic and catabolic effects of orthopedic forces. Since craniofacial orthopedics is currently aimed at the juvenile population, a comparison of orthopedic loading in juvenile bones with that in adult bones is desirable. The mandibular condyle experiences compressive bone strain during mastication in experimental animals (Hylander and Bays, 1979; Herring et al., 1996), and in dry human skulls upon simulated masticatory loading (Throckmorton and Dechow, 1994). Exogenous orthopedic forces applied to the teeth evoke bone strain in craniofacial bones by modeling (Tanne et al., 1993) and experimental (Mao et al., 1999) approaches. Whether of functional or exogenous forces, sustained mechanical stresses induce modeling and remodeling of both the cartilaginous and osseous tissues of the temporomandibular joint (e.g., Kantomaa et al., 1994; Mao et al., 1998). The articular eminence of the temporal bone is the articulating counterpart of the mandibular condyle. There is no direct evidence of whether or in what fashion the temporal articular eminence withstands biomechanical loading. The first goal of the present study was to explore whether the temporal articular eminence is loaded upon simulated orthopedic forces by headgear, a device widely used in craniofacial orthopedics. The zygomatic arch withstands mechanical stresses during mastication in experimental animals (Herring et al., 1996; Hylander and Johnson, 1997) and upon simulated orthopedic loading in dry human skulls (Mao et al., 1999). Despite species differences among these reports, bone strain differed across the zygomatico-temporal suture in the lateral (outer) surface of the zygomatic arch. These differences in strain magnitude in the lateral surfaces of the zygomatic arch across the zygomatico-temporal suture have inspired the present hypothesis that the medial (inner) and lateral surfaces of the zygomatic arch experience different bone strain patterns. As the second goal, the present study determined the potential presence of different bone strain patterns between the medial and lateral surfaces of the zygomatic arch. The present effort is anticipated to form the basis of further investigation of potential modulation of bone modeling and remodeling by exogenously induced bone strain.
Dry Skull Model and Craniometrics Four juvenile dry human skulls (from 6 to 14 yrs of age) and five adult dry human skulls (ca. 40+ yrs of age) were used without the investigators’ knowledge of gender and provenance. The skull ages were estimated from dental age, tooth wear, and the status of suture closure. All skulls had nearly complete mixed (primary and permanent) dentitions or permanent dentitions for their corresponding dental ages, with no craniofacial deformities or trauma upon visual examination. These criteria severely limited the number of specimens in the present study, in addition to the general scarcity of intact skulls. Straight stainless steel wires were clayed onto the skull surface for measurement of: (1) the angle between the Frankfort plane (FP), which was defined as a line connecting the inferior border of the orbit and superior rim of the external auditory meatus, and the slope of the temporal articular eminence (AE); and (2) the distance from the mesiobuccal cusp of the maxillary first molar (MI) to the most inferior (prominent) point of the temporal articular eminence (Hinton and Carlson, 1983). The present study was determined to be exempt from IRB review.
Orthopedic Loading
Bone Strain Bone strain techniques followed the methods that were previously described in detail (Mao and Osborn, 1994; Mao et al., 1996, 1999). A three-element rectangular, stacked strain rosette (WK-06-060WR-350, Measurements Group, Raleigh, NC, USA, and hereafter for all strain-gauge-related supplies) was bonded on the cortical bone of the temporal articular eminence with its middle grid aligned with the posterior end of the zygomatic arch (cf. Fig. 1B  ). Uni-axial strain gauges (EA-06-032-UW-350) were bonded in both the lateral and medial surfaces of the zygomatic arch approximately 1 mm anterior and posterior to the zygomatico-temporal suture, with the longitudinal gauge axes parallel to both the zygomatic arch and to each other (Fig. 1A). For the medial surface of the zygomatic arch, the strain gauges were bonded with their orientations and locations both parallel to and corresponding to those of the gauges in the lateral arch surface. Dummy strain gauges were installed in regions adjacent to the temporoparietal suture and accounted for any potential change in room temperature during strain recordings. All strain gauges and rosettes were arranged in 1/4 bridge configuration and excited with 500 mV DC. In response to each force, bone strain was conditioned and recorded with computer data acquisition (System 5000; Measurements Group, Raleigh, NC, USA). Each loading and associated bone strain recordings were repeated up to 10 times. By convention, tensile strain was expressed as positive values, and compressive strain as negative values.
Data Analysis and Statistics
Tensile strain was recorded consistently in the temporal articular eminence in both the juvenile and adult skulls. The juvenile articular eminence experienced significantly higher tensile bone strain than the adult (p < 0.05) (Fig. 2  ). The peak bone strain for the juvenile articular eminence was 52.2 ± 4.5 (µ ), 45.3 ± 4.3 (µ), and 41.2 ± 4.6 (µ) for simulated orthopedic loading 30° superior to the OP (30° up OP in Fig. 2), parallel to the OP, and 30° inferior to the OP (30° down OP in Fig. 2), respectively. The principal angles were -0.25° (± 30.5), 47.5° (± 23.9), and 2.25° (± 34.9) for 30° superior to the OP, parallel to OP, and 30° inferior to the OP, respectively. The mean peak bone strain of the temporal articular eminence in both juvenile and adult skulls showed significant differences among the three loading directions: 30° superior to, parallel to, and 30° inferior to the occlusal plane. The relationship between the simulated orthopedic forces and the bone strain they evoked was quasi-linear, as shown in Fig. 3 with representative samples for the juvenile articular eminence (Fig. 3A) and adult articular eminence (Fig. 3B).
The average angle between the FP and the AE slope was 42.0° ± 4.8 (mean ± SD) in the five adult skulls and significantly larger than the corresponding average angle of 32.0° ± 4.3 in the four juvenile skulls (p < 0.05). The average distance from the mesiobuccal cusp of the maxillary first molar to the most inferior (prominent) point of the AE in the five adult skulls was 71.8 ± 3.8 mm, significantly longer than the corresponding average distance of 50.5 ± 1.7 mm in the four juvenile skulls (p < 0.05). An attempt is made below to explain the impact of these craniometric characteristics on differences in bone strain between juvenile and adult articular eminences.
Contrasting bone strain patterns were identified between the lateral and medial surfaces of the zygomatic arch: tensile in the lateral surface (upward histograms in Fig. 4
Mechanical forces cannot be applied from zero to a given magnitude without a ramp phase. Besides this physical law, the present application of ramp forces from 0 to 50 N was designed to simulate the entire range of orthopedic headgear forces that have been used in a clinical setting. Empirically, headgear forces have been applied in a range from 2.5 N to 50 N (Gianelly and Valentini, 1976; Proffit et al., 2000). The present choices of the zygomatic arch and temporal articular eminence on which bone strain was recorded can be attributed to the potential importance of these structures in bone modeling and remodeling in response to headgear loading. Bone apposition/resorption in the zygomatico-temporal suture or the temporal articular eminence likely will have direct impact on the shape of facial skeleton. The significantly larger tensile strain in the juvenile than in the adult articular eminence is the first direct evidence of mechanical stresses of this structure, and can perhaps be attributed to several factors. First, the articular eminence is significantly steeper in adult skulls. This steeper adult articular eminence appears to account for smaller bone strain in the adult (Osborn, 1996). Second, the distance from the mesiobuccal cusp of the maxillary first molar to the most inferior (prominent) point of the articular eminence is significantly longer in the adult than in the juvenile. It seems plausible that, in response to the same force, higher strain is concentrated in the juvenile articular eminence than in the adult, due to shorter distance from the loading point in the former. Third, juvenile bone is generally less stiff than adult bone (Zioupos and Currey, 1998) and therefore subject to greater deformation and higher bone strain. The contrasting bone strain patterns between the lateral and medial surfaces of the zygomatic arch, tensile strain in the lateral surface but compressive strain in the medial surface, suggest potential biomechanical and biological effects. First, the zygomatic arch is bent outward at its middle and inward at both ends. Second, this biomechanical bending suggests a possibility of differential bone modeling between the lateral and medial surfaces. Bone resorption takes place in both the zygomatico-maxillary and zygomatico-temporal sutures upon headgear loading in macaques in vivo (Elder and Tuenge, 1974; Kokich, 1992), and in the pig zygomatico-temporal suture upon compressive loading (Ferrari and Herring, 1995; Teng et al., 1996). Analysis of these in vivo data, coupled with the present in vitro data, indicates the necessity for investigation of whether the lateral and medial surfaces of the zygomatic arch undergo different bone modeling processes in vivo. It is of further interest to speculate about the potential in vivo effects, if any, of the observed bone strain in the temporal articular eminence. Although the mandibular condyle has been found to contribute significantly to facial growth, the temporal articular eminence has received less attention, despite its comparable tissue composition as the mandibular condyle (Enlow, 1990). In response to altered dental occlusion leading to increasing mechanical stimuli in vivo, the mandibular condyle undergoes increasing proliferation of chondroblast-like cells and enhanced expression of proteoglycans (e.g., Kantomaa et al., 1994; Mao et al., 1998). This, along with the observation of increased cell proliferation and decreased type II collagen expression in the articular eminence in response to raised dental occlusion (Pirttiniemi et al., 1994), suggests a potential for chondrogenic and osteogenic modeling of the articular eminence upon headgear loading. The dry human skull model is appropriate for studying bone strain responses to orthopedic loading because it provides human anatomy unmatchable by other animal models. Important limitations of the dry skull model include bone properties different from those in vivo and the absence of periosteum, hydrated matrix, and muscular and sutural fibrous tissues, in addition to a lack of periodontal ligament. In a rare study of combined bone strain recordings upon in vivo headgear loading in Macaca irus and dry skulls obtained thereafter, bone strain patterns for corresponding locations were similar, although the magnitude of bone strain was approximately five-fold higher in vivo than in dry skulls (Kannan, 1982). Thus, it is probable that bone strain patterns in humans in vivo in response to headgear loading are similar to those in the present work, along with several-fold-higher bone strain magnitude. The main difference between the present in vitro model and in vivo animal models (e.g., Herring et al., 1996; Hylander and Johnson, 1997) is a lack of masseter muscle with its superior attachment to the zygomatic arch. In two different species of macaques and pigs, masseter contraction has been shown to affect zygomatic bone strain, likely inducing bending moments and shearing forces along the anterior portion of the arch (Herring et al., 1996; Hylander and Johnson, 1997). In dry human skulls, simulated masseter and temporalis contractile forces of about 40 Newtons have been shown to evoke bone strain across several frontal sutures (Endo, 1970). Another lack of consideration of the overall loading of the skull in the present model is reactive forces of the mandibular condyle (Osborn and Baragar, 1992). Thus, the present data and associated interpretations should be limited to an in vitro model without contribution of masseter contraction to zygomatic bone strain. However, the present model is justified because headgear application does not require, and is in the absence of, contraction of jaw musculature (Proffit et al., 2000). Taken together, both the articular eminence and the zygomatic arch experience bone strain evoked by posteriorly directed craniofacial orthopedic forces. For corresponding cortical locations, bone strain in juvenile skulls is, with rare exceptions, significantly higher than that in adult skulls. Partly on the basis of a comparative study of orthopedic loading in macaques in vivo and dry skulls obtained thereafter (Kannan, 1982), bone strain in the zygomatic complex identified in the present study is likely present and of higher magnitude in humans in vivo. The functional implication of bone strain in the zygomatic complex, including the temporal articular eminence, warrants further investigation. We hypothesize that headgear-evoked bone strain in the temporal articular eminence induces modeling of the articular eminence and glenoid fossa, which, if proven to be the case in vivo, may add to headgear’s therapeutic effects.
The work reported here was a part of the research project leading to the Master of Dental Science degree, awarded to Mark Oberheim at the University of Pittsburgh. Mr. Michael Tassick is thanked for his technical assistance. We thank Hashil Al-Syabi for providing some of the control data for the adult articular eminence from his thesis project. We thank Dr. Mark Mooney and Mr. Charles Mandella for making available some of the skulls used in the present study. We are indebted to Dr. David Burr for his insightful comments on an earlier draft of the manuscript. Two anonymous reviewers are thanked for their suggestions that have improved the quality of our manuscript. This research was partially supported by grants from two competitive seed funds, CMRF and CRDF, from the University of Pittsburgh and the University of Pittsburgh Medical Center. Part of the effort on preparation of this manuscript was supported by NIH Grants DE13964 and DE-13088. Received for publication March 21, 2001. Revision received May 23, 2002. Accepted for publication July 8, 2002.
Journal of Dental Research, Vol. 81, No. 9,
608-612 (2002)
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