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Clinical

Human Masticatory Muscle Forces during Static Biting

J.C. Nickel1,2, L.R. Iwasaki1,2,3, R.D. Walker4, K.R. McLachlan5 and W.D. McCall, Jr.6

1 University of Nebraska Medical Center College of Dentistry, Departments of Growth and Development and
2 Oral Biology, 40th and Holdrege Streets, PO Box 830740, Lincoln, NE 68583-0755, USA;
4 Private Practice, 3200 North Dobson Rd., Building A, Chandler, AZ 85224, USA;
5 University of Manitoba, Faculty of Engineering, Department of Civil Engineering, Winnipeg, MB R3T 2N2, Canada; and
6 University at Buffalo School of Dental Medicine, Department of Oral Diagnostic Sciences, 355 Squire Hall, Buffalo, NY 14214-3008, USA;

Correspondence: 3 corresponding author, liwasaki{at}unmc.edu


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Muscle forces determine joint loads, but the objectives governing the mix of muscle forces involved are unknown. This study tested the hypothesis that masticatory muscle forces exerted during static biting are consistent with objectives of minimization of joint loads (MJL) or muscle effort (MME). To do this, we compared numerical model predictions with data measured from six subjects. Biting tasks which produced moments on molar and incisor teeth were modeled based on MJL or MME. The slope of predicted vs. electromyographic (EMG) data for an individual was compared with a perfect match slope of 1.00. Predictions based on MME matched best with EMG activity for molar biting (slopes, 0.89-1.16). Predictions from either or both models matched EMG results for incisor biting (best-match slopes, 0.95-1.07). Muscle forces during isometric biting appear to be consistent with objectives of MJL or MME, depending on the individual, biting location, and moment.

Key Words: numerical modeling • TMJ • loading • electromyography


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In humans, muscle recruitment during biting and chewing depends in part on bite force direction (van Eijden et al., 1990, 1993). Directional information is provided by periodontal ligament mechanoreceptors (Trulsson and Johansson, 1994, 1996). However, it is unknown whether there is a governing neuromuscular objective for the mix of masticatory muscle forces produced for a given biting situation. Data from living subjects are sparse. The mix of muscle forces determines the magnitudes and directions of temporomandibular joint (TMJ) loads (Throckmorton et al., 1990; Trainor et al., 1995), and thus, is clinically important, especially since the likelihood of degenerative joint disease increases with increased TMJ loads (Iwasaki et al., 1997). Recent analysis of the mix of muscle outputs measured in post-orthognathic surgery patients suggested that the neuromuscular objectives of minimization of joint load (MJL) or minimization of muscle effort (MME) determined the magnitudes of joint loads (Nickel et al., 2002).

The aim of this project was to elucidate neuromuscular control of craniomandibular mechanics by testing the hypothesis that masticatory muscle forces, in response to static biting which produces moments on molars and incisors, can be predicted on the basis of MJL or MME, or both. To test this hypothesis, we compared data from living subjects with numerical model predictions of muscle forces calculated from the three-dimensional geometry of the individual and an objective function of MJL or MME.


    MATERIALS & METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
One female and five male subjects, aged 23 to 32 yrs, participated. Informed consent was obtained, and the project was approved by the appropriate Institutional Review Board.

Anatomical Geometry
We developed a three-dimensional geometry for each individual using standardized lateral and postero-anterior cephalometric radiographs to determine the relative positions of the masticatory muscles, condyles, and tooth row (Fig. 1AGo). The x-, y-, and z-coordinates were determined for centroids of the origins and insertions of 5 muscle pairs (masseter, anterior temporalis, medial pterygoid, lateral pterygoid, and anterior digastric muscles), the center supero-anterior point on the mandibular condyles, and positions of the mandibular central incisors, canines, and first molars. Preliminary studies utilizing cadaver material aided protocol development for soft- and hard-tissue coordinate identification in living subjects, with the use of these radiographs. Maximum measurement errors for all coordinates, from serial radiographic tracings, were + 3.5 mm. This geometry was used in computer models for the prediction of effective sagittal TMJ eminence morphology and the calculation of muscle and joint forces for unilateral molar and centered incisor biting.


Figure 1
Figure 1
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Figure 1. Mechanical schemes. (A) Force vectors involved in numerical models of isometric biting in humans. Forces on the mandible (e.g., vertical bite force), at the joints (Fcondyle, R = right, L = left), and representing 5 muscle pairs (m1,2 = masseter, m3,4 = anterior temporalis, m5,6 = lateral pterygoid, m7,8 = medial pterygoid, m9,10 = anterior digastric muscles), plus the axis system, are shown. (Modified from Smith et al., 1986). (B) Equivalent moments for in vivo (1) and modeled (2) molar (+ Mx) and incisor (+ Mz) biting tasks. Line diagrams illustrate mesial views of mandibular right first molar (top) and left central incisor (bottom) with acrylic crowns in place, where: CR is the center of resistance of the tooth/teeth, r-> is the moment arm vector, {Theta}y is the angle away from vertical, and {Theta}xz is in a plane parallel to the occlusal plane.

 
Modeled Eminence Shape
The effective sagittal TMJ eminence morphology was defined as the shape of hard- and soft-tissue structures articulating with the mandibular condyle in sagittal view. We used a custom program with optimization based on unconstrained MJL and the subject’s geometry to predict the effective sagittal eminence morphology (Trainor et al., 1995). In brief, it operated as follows. Joint load directions were calculated for a series of bilateral vertical bite forces applied in 20 steps from first molars to central incisors. The mandibular position, consistent with bite force position for each calculation, ranged from relatively retruded (molar biting) to protruded (incisor biting). For equilibrium, the joint load must be directed perpendicular to the effective eminence. Therefore, the effective eminence shape for an individual was delineated by a series of 20 lines, each perpendicular to the predicted joint load direction for a given step, to which a cubic polynomial was fitted.

Modeled Muscle Forces
Muscle forces were predicted by 2 three-dimensional models with different objective functions: (a) minimization and equalization of right and left TMJ loads and (b) minimization of the sum of squared muscle force magnitudes. In both models, the sagittal eminence shape was determined as described above. This eminence shape constrained the sagittal component ({Theta}x, {Theta}y) of the joint load directions (perpendicular to the predicted eminence), while maintaining an independent mediolateral component ({Theta}z). We used an optimization strategy of either MJL or MME to calculate muscle and joint forces for any prescribed mandibular position, and position and direction of mandibular load. The optimizing process was achieved by means of quadratic programming. Companion algorithms were constructed for data management and systematic and sequential testing of possible force combinations until the designated objective was satisfied for the given biting situation (Trainor et al., 1995).

Modeled conditions produced moments on the molar and incisor teeth that were similar to those tested in vivo (see below). Bite forces of 100 units, at angles from vertical ({Theta}y) of 0 to 30°, were loaded unilaterally on mandibular first molars at azimuth angles ({Theta}xz) of -90 and 90°, and centrally on the incisors at {Theta}xz of 0 and 180° (Fig. 1BGo). The mandibular position during each biting task was simulated based on in vivo data (e.g., Appendix Tables A1, A2).

Experimental Eminence Shape
In vivo effective sagittal eminence morphology was determined by a simplified method of tracking the condylar pathway using a modified mandibular orthodontic retainer with a facebow attached. Colored markers on the facebow were positioned opposite palpated lateral poles of both mandibular condyles, and recorded by means of video cameras set up directly lateral to the subject. Graph paper affixed medially to the markers provided a reference system and orthogonal axes for determining scale.

A set of 10 protrusion/retrusion movements, with upper and lower teeth separated by 1 to 3 mm, was recorded at each of 2 sessions, at least 3 days apart. Recordings were viewed frame-by-frame, and the condylar marker position was traced on acetate mounted on the video screen. Points along the path of the marker were quantified in two dimensions with occlusal plane and a perpendicular line as axes. The occlusal plane was chosen as a reference axis, given its importance in the mechanics of biting. A custom computer program was used to correct for scale, to record x- and y-coordinates for each point, and to calculate a best-fit third-order polynomial which delineated the effective eminence shape. Intra- and inter-session measurement errors in condylar position were, on average, + 0.3 mm or + 10% of full scale.

Experimental Biting Tasks
Biting tasks were performed during 2 or 3 recording sessions, at least 3 days apart. Static biting occurred on a small steel ball between acrylic crowns cemented to maxillary and mandibular first molars and central incisors. Each acrylic crown had a flat occlusal/incisal surface that was approximately parallel to the occlusal plane. For mandibular crowns, these surfaces each had three small depressions, 3 to 4 mm apart, which ensured that bolus position was consistent relative to the center of resistance of loaded teeth, and a range of mechanical moments was tested (Fig. 1BGo). The depressions were parallel to the z-axis on mandibular molar crowns, and the x-axis on mandibular incisor crowns. Incisor crowns had extra-oral reference markers attached, so that changes in mandibular position could be monitored directly or from video images. Each subject produced a moderate static bite force for 5 sec, 5 times at each of 3 positions on molars and incisors, with 20 seconds’ rest between bite positions.

Bipolar surface electromyographic (EMG) data were measured as surrogates for forces during biting tasks. The muscle bulk center was located by palpation for masseter, anterior temporalis, and anterior digastric muscles. The skin over each muscle was debrided, and paired electrodes (E5SH Standard Silver®, 7 mm, Grass Instrument Company, Quincy, MA, USA) with conducting paste (Liqui-Cor®, Burdock Corp., Milton, WI, USA) were held in place with adhesive pads. Surface impedances were less than 30 k{Omega}, applied input impedance was 20 M{Omega}, and band width was 0.1 to 3 kHz. Muscle activity was amplified (P511 AC Grass Preamplifiers®, Astor-Med Inc., West Warwick, RI, USA), viewed in real-time with commercial software (PCScan MKII PCIF250NI Real-time Data Transfer System®, Sony Magnescale America Inc., Farmington Hills, MI, USA), and stored digitally (Sony PC-216A 16 Channel Recorder®, Spectris Technologies Inc., Decatur, GA, USA). Signal-to-noise ratios were better than 8 to 1.

Muscle output data were replayed and analyzed with commercial software (Microsoft Excel®, Microsoft Corp., Seattle, WA, USA). Muscle activities over a two-second period were sampled at 1.7 kilo-samples/second/channel and expressed as root-mean-square (RMS) values (mV).

Eminence Shape Comparisons
Predicted and measured effective eminence shapes for each subject were compared by means of the polynomial equations for determination of y-axis coordinates, representing eminence height (mm), and for x-axis coordinates, representing anteroposterior condylar positions over the range x = 0 to 5 mm in 0.5-mm increments. Predicted and measured y-axis coordinates were plotted for each subject, and a linear correlation coefficient was calculated.

Muscle Output Comparisons
Predicted and measured muscle outputs for the biting tasks were compared. We calculated ipsilateral-to-contralateral (I/C) muscle output ratios to compare molar biting results quantitatively. This use of ratios obviated the need for bite force measurements and force-EMG calibration for individual muscles. At each of 3 molar bite positions, RMS values from 5 bites were averaged, and I/C muscle output ratios were calculated. For example, the I/C masseter muscle output ratio for lateral biting on right and left first molars was calculated as:


Formula

where I and C were the ipsilateral and contralateral muscle output for lateral molar biting, and R and L indicated right and left sides. In vivo intra- and inter-sessional ratio variabilities were, on average, + 13%. Predicted vs. measured I/C muscle output ratios for biting moments were plotted for each subject. Linear regressions were calculated and slopes were tested for significant differences from a perfect-match slope of 1.00.

Incisor biting tasks were centered on the mandible, so RMS values for right and left muscles were averaged for 5 bites at each of 3 bite positions. These data for each subject and recording session were normalized relative to the peak RMS value for a given muscle. Similarly, predicted muscle forces for incisor biting were normalized relative to the peak predicted muscle force for the subject and muscle. Intra- and inter-sessional normalized RMS value variabilities were, on average, + 14%. Predicted vs. measured normalized muscle output values for biting moments were plotted for each subject. Linear regressions were calculated and slopes were tested for significant differences from a perfect-match slope of 1.00.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Eminence Shapes
The maximum vertical difference between predicted and experimental results for the group was 0.4 mm for protrusion up to 5 mm. Plots of predicted vs. measured effective sagittal eminence shapes for each subject showed slopes from 0.87 to 1.13, and a range of correlations, 0.92 < R2 < 0.99 (Fig. 2AGo). The mean slope was 0.94 with a standard deviation (SD) of 0.12. An independent t test showed no significant difference between predicted and experimental results for eminence shape. However, in vivo eminence shapes showed inter-subject variability, where the individual slopes of fitted polynomials differed by up to 3 to 1 (Fig. 2BGo).


Figure 2
Figure 2
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Figure 2. Effective TMJ eminence results. (A) Eminence height (mm), predicted by the model vs. measured, for a given postero-anterior position from 0 to 5.0 mm anterior to a retruded condylar position, in 0.5-mm increments, for subject m1 ("worst-case", {diamondsuit}) and subject m4 ("best-case", *). (B) Sagittal morphology of the effective TMJ eminence in each of the six subjects. The vertical axis represents the eminence height (mm) relative to a retruded condylar position and perpendicular to the occlusal plane, and the horizontal axis represents condylar protrusion (mm) from the retruded position. Function beyond 5 mm of protrusion was unlikely, since this placed mandibular incisors anterior to maxillary incisors in all subjects.

 
Muscle Outputs
Anterior digastric muscle force predictions and RMS values were similar for the biting tasks investigated, and near or at baseline levels. The 2 models predicted quite different I/C masseter and anterior temporalis muscle force ratios for moments resulting from lateral and medial molar biting angles (Fig. 3AGo). Plots of predicted vs. measured muscle output during molar biting were compared for the models (Table). All subjects’ molar biting I/C muscle output ratios were predicted better according to the MME model (mean slope, SD: 0.98, 0.10) compared with the MJL model (mean slope, SD: 3.71, 3.74). Similarly, plots of predicted vs. measured normalized masseter and anterior temporalis muscle output values for incisor biting were compared for the two models (Table). The predictions from the MJL and MME models were the same for two subjects (e.g., f1, Fig. 3BGo) and matched well with the EMG data for these subjects. Predictions from the 2 models were not the same for the other four subjects (e.g., m5, Fig. 3BGo). The MJL model results matched best with the EMG data from two of these subjects, while the MME model results matched best with the EMG data from the two remaining subjects. Slopes from plots of predicted vs. measured results for molar and incisor biting (Table) were compared with perfect-match slopes of 1.00. Separate independent t tests showed no significant differences between best model-predicted and experimental data for each biting condition (p > 0.05). However, post hoc power analyses indicated that sample sizes were too small for statistically significant differences between predicted and measured values to be excluded.


Figure 3
Figure 3
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Figure 3. Examples of model results for biting tasks. (A) Predicted I/C muscle force ratios for molar biting tasks at a range of bite force angles that created moments equivalent to in vivo biting at lateral, center, and medial positions. MJL model predictions for masseter ({diamond}) and anterior temporalis ({square}) muscles and MME model predictions for masseter ({triangleup}) and anterior temporalis (X) muscles are shown for subject f1. Please note the discontinuity of scale in the vertical axis. (B) Predicted normalized muscle forces for incisor biting tasks at a range of bite force angles that created moments equivalent to in vivo biting at posterior, center, and anterior positions. Masseter muscle force predictions from MJL model ({diamond} subject f1, {diamondsuit} subject m5) and from MME model ({triangleup} subject f1, {blacktriangleup} subject m5), and anterior temporalis muscle force predictions from MJL model ({square} subject f1, {blacksquare} subject m5) and from MME model ({circ} subject f1, • subject m5).

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Computer-generated models based on human anatomy render solutions based on an optimal strategy or objective function, which is of biological importance and thus represents a theory of underlying neuromuscular control (Pruim et al., 1980; Osborn and Baragar, 1985, 1992; Smith et al., 1986; Koolstra et al., 1988; Herzog and Binding, 1994; Koolstra and van Eijden, 1995, 1997, 1999; Osborn, 1995; Trainor et al., 1995; Buchanan and Shreeve, 1996; Itoh et al., 1997; Raikova, 1999). A neuromuscular objective of MJL is of interest because cartilage has limited repair potential, and theoretically, this objective reduces the likelihood of mechanical fatigue. However, MJL tends to increase muscle forces for given biting tasks, theoretically increasing the likelihood of muscle fatigue. In contradistinction, an objective of MME reduces muscle forces for a biting task, but increases joint loading, especially in the TMJ contralateral to a molar bite force. The data presented here are the first, to our knowledge, to test model predictions of masticatory muscle output for changes in biting moments in individual subjects. Variance seen between predicted and experimental data is likely due to factors such as the use of synthetic crowns, a static biting task rather than routine masticatory activity, and the limitations of the numerical model, which necessitated that the in vivo biting tasks be represented by bite force positions that would produce equivalent moments, but not identical force vectors. Experimental evidence comparable with model predictions from the current study has been reported (van Eijden et al., 1993). Human I/C masseter muscle peak EMG ratios calculated from unilateral gum-chewing data ranged from 1.18 to 2.66. In the current study, mean predicted I/C masseter muscle force ratios were 1.5 (SD 0.7) for non-vertical bite forces.

In summary, predictions of muscle recruitment were tested with experimental data. The mix of masticatory muscle outputs during isometric unilateral molar biting and centered incisor biting was generally consistent with MJL or MME for the individuals investigated. The specific objective function involved appeared to depend on the individual’s anatomy and the specific location and direction of bite force. These factors are the focus of further inquiry.


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Table. Slopes and R2 Values for the Relationship between Predicted and Measured Masseter and Anterior Temporalis Muscle Outputs for Equivalent Biting Moments (e.g., Appendix Fig.)
 

    FOOTNOTES
 
A supplemental appendix to this article is published electronically only at http://www.dentalresearch.org.

Received for publication December 5, 2001. Revision received October 30, 2002. Accepted for publication November 7, 2002.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Journal of Dental Research, Vol. 82, No. 3, 212-217 (2003)
DOI: 10.1177/154405910308200312


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