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. Author manuscript; available in PMC: 2022 Sep 20.
Published in final edited form as: J Biomech. 2021 Jul 10;126:110623. doi: 10.1016/j.jbiomech.2021.110623

Sexual Dimorphisms in Three-Dimensional Masticatory Muscle Attachment Morphometry Regulates Temporomandibular Joint Mechanics

Xin She 1, Shuchun Sun 1, Brooke J Damon 1,2, Cherice N Hill 1,2, Matthew C Coombs 1,2, Feng Wei 1, Michael K Lecholop 3, Martin B Steed 3, Thierry H Bacro 4, Elizabeth H Slate 5, Naiquan Zheng 6, Janice S Lee 7, Hai Yao 1,2
PMCID: PMC8453136  NIHMSID: NIHMS1727832  PMID: 34311291

Abstract

Temporomandibular joint (TMJ) disorders disproportionally affect females, with female to male prevalence varying from 3:1 to 8:1. Sexual dimorphisms in masticatory muscle attachment morphometry and association with craniofacial size, critical for understanding sex-differences in TMJ function, have not been reported. The objective of this study was to determine sex-specific differences in three-dimensional (3D) TMJ muscle attachment morphometry and craniofacial sizes and their impact on TMJ mechanics. Human cadaveric TMJ muscle attachment morphometry and craniofacial anthropometry (10Males; 11Females) were determined by previously developed 3D digitization and imaging-based methods. Sex-differences in muscle attachment morphometry and craniofacial anthropometry, and their correlation were determined, respectively using multivariate general linear and linear regression statistical models. Subject-specific musculoskeletal models of the mandible were developed to determine effects of sexual dimorphisms in mandibular size and TMJ muscle attachment morphometry on joint loading during static biting. There were significant sex-differences in craniofacial size (p=0.024) and TMJ muscle attachment morphometry (p<0.001). TMJ muscle attachment morphometry was significantly correlated with craniofacial size. TMJ contact forces estimated from biomechanical models were significantly, 23% on average (p<0.001), greater for females compared to those for males when generating the same bite forces. There were significant linear correlations between TMJ contact force and both 3D mandibular length (R2=0.48, p<0.001) and muscle force moment arm ratio (R2=0.68, p<0.001). Sexual dimorphisms in masticatory muscle morphology and craniofacial sizes play critical roles in subject-specific TMJ biomechanics. Sex-specific differences in the TMJ mechanical environment should be further investigated concerning mechanical fatigue of TMJ discs associated with TMJ disorders.

Keywords: Sexual dimorphism, Temporomandibular joint, Musculoskeletal modeling, Muscle attachment, Craniofacial morphology

INTRODUCTION

Temporomandibular joint (TMJ) disorders disproportionally affected females, with female to male prevalence varying from 3:1 to 8:1 (Slade et al., 2011). The development of TMJ disorders are likely associated with pathological changes in the TMJ mechanical loading environment since its tissue homeostasis is sensitive to joint load (Nickel et al., 2018). Human masticatory muscles drive mandibular movement, contribute to bite force generation, and determine TMJ loads (Koolstra and Van Eijden, 2005; Throckmorton et al., 1990) and oral function (Lindauer et al., 1993). Studying sexual dimorphisms in masticatory muscle attachment morphometry and its impact on TMJ biomechanics is critical to better understand TMJ pathophysiology.

Sexual dimorphisms in craniofacial sizes have been observed in many human populations (Alarcón et al., 2016; Ingerslev and Solow, 1975; Kimmerle et al., 2008; Steyn and İşcan, 1998). Significant statistical correlations have been described between masticatory muscle cross-sectional area, thickness and craniofacial anthropometric dimensions (Raadsheer et al., 1999; Spronsen et al., 1991; Weijs and Hillen, 1986; Kitai et al., 2002). It has been demonstrated that masticatory muscle forces determine the stress patterns in the growing cranium and cartilage, thus directly influencing human craniofacial growth (Carter et al., 1991; Loth and Henneberg, 1996). It is generally acknowledged that human masticatory system mechanical function is determined by craniofacial size (Proffit et al., 1983; Ringqvist, 1973). As a result, sex-dimorphisms in human masticatory muscle attachment morphometry and its association with craniofacial size may exist. It also remains unknown how sexual differences in human masticatory muscle attachment morphometry affect muscle force generation and joint mechanical loading, which is important as it may predispose women to TMJ disorder development by inducing earlier mechanical fatigue on TMJ discs.

To better understand the sexual differences in masticatory muscle attachment morphometry and its impacts on TMJ biomechanics, it is necessary to quantify the three-dimensional (3D) male and female TMJ muscle attachment morphometry first. Only one set of studies measured the 3D coordinates of the human temporalis, masseter, lateral and medial pterygoid muscle attachment sites (van Eijden et al., 1995, 1996, 1997). However, these reports intended to study architectural characteristics for masticatory muscles, such as muscle physiological cross-sectional areas and fiber lengths. Therefore, no comparison of the sex-specific differences in human muscle attachment morphometry was made and their influences on TMJ mechanics were never revealed. Our previous work successfully digitized the physiological 3D structure of the male TMJ muscle attachment surface, and determined sizes, spatial locations of centroids, and orientations (She et al., 2018). To the authors’ knowledge there have been no reported sex-specific differences in masticatory 3D muscle attachment morphometry nor was their association with craniofacial size investigated. What is more, given the increased mechanical work in temporal discs among females potentially being related to the sexual disparity in the number of TMJ disorder patients (Spradley and Jantz, 2011), the critical effects of sexual dimorphisms in human masticatory muscle attachment morphometry on TMJ contact mechanics had not been studied.

The objective of this study was to quantify the 3D female and male human TMJ muscle attachment morphometry and craniofacial anthropometry through cadaver dissection using previously developed 3D digitization and imaging-based methods (She et al., 2018), and statistically determine their sexual dimorphisms and correlation relationships. The secondary goal was to quantitatively determine the impact of sex-dimorphism in craniofacial size-associated muscle attachment morphometry on muscle mechanics and joint load during jaw static biting through subject-specific musculoskeletal modeling of both live and cadaveric subjects. The null hypothesis was the TMJ mechanical environment during jaw static biting is not affected by sexual dimorphisms in human masticatory muscle attachment morphometry and craniofacial sizes.

METHODS

Specimen selection and CBCT scanning

Eleven female (73.6±12.8 years) and ten male (75.8±8.3 years) human cadaveric heads without craniofacial anomalies and no known history of TMJ disorders were included, under appropriate institutional approval. Donor heads were scanned using a cone-beam computerized tomography (CBCT) scanner (Planmeca3D Max, Planmeca USA, Roselle, IL) with voxel dimensions of 0.2 × 0.2 × 0.2 mm3. After CBCT scanning, 3D solid models of each head were reconstructed (Amira 5.4, FEI Co., Hillsboro, OR).

Craniofacial dimension measurement

Craniofacial anthropometric dimensions were measured from reconstructed 3D solid models of cadaveric heads (Figure 1A). Anthropometric parameters included nine linear measurements and one angular measurement (Figure 1A), with bilateral measurements of mandible length (ML), ramus height (RH), 3D mandibular length (ML*) and gonial angle (GA). Anthropometric definitions have been reviewed in the forensic anthropology literature, and used to determine intrinsic sex-specific differences in mandibular condyle morphometry (Coombs et al., 2019).

Figure 1.

Figure 1.

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(A) Illustrations of linear and angular craniofacial anthropometric dimensions on CBCT-based 3D models of the human skull and mandible. Anthropometric parameters shown include cranial length (CL): distance between the glabella and opisthocranion in the midsagittal plane (Botha, 1991; Franklin et al., 2013; Jantz, 2001); cranial height (CH): distance from the inferior-most point on the anterior margin of the foramen magnum to the vertex of the skull (Botha, 1991); cranial width (CW): maximum width of the skull perpendicular to the midsagittal plane, wherever it is located with the exception of the inferior temporal lines and the area immediately surrounding them (Botha, 1991; Franklin et al., 2013; Jantz, 2001); bizygomatic breadth (BZB): distance from the widest part of one zygomatic arch to the widest part of the other (Franklin et al., 2013; Jantz, 2001; Raadsheer et al., 1999); mandibular breadth at angle (MBA): distance from each gonion on left and right aspects of the mandible (Raadsheer et al., 1999); inter-condylar width (ICW): distance from the most lateral points on each condyle (Raadsheer et al., 1999); ramus height (RH): distance from the highest point on the mandibular condyle to the gonion (Sella-Tunis et al., 2018); mandible length (ML): distance from the anterior margin of the chin to the gonion (Raadsheer et al., 1999); gonial angle (GA): angle formed by a tangent between the lower border of the mandible and a tangent touching the posterior border of the ramus from the condyle to Gonion (Kemkes-Grottenthaler et al., 2002; Raadsheer et al., 1999); 3D mandibular length (ML*): distance from the highest point on the mandibular condyle to the anterior margin of the chin (Sella-Tunis et al., 2018). (B) The size of the 3D surface of each masticatory muscle attachment (temporalis origin illustrated as an example) was quantified by the Length, Width, and Thickness of a 3D bounding box (black bold frame). A skull-based coordinate system was established to determine the Centroid (C) spatial coordinates (x, y, and z) of each muscle attachment for its location, and the angles between ‘Box Plane’ and Sagittal plane (SA), Frontal plane (FA), and Frankfurt plane (FHA) respectively for its orientation.

3D muscle attachment morphometry analysis

To quantify 3D human TMJ muscle attachment morphometry, a previously developed co-registered 3D digitization and CBCT imaging-based method was utilized to generate the 3D muscle attachment surfaces (Figure 1B) through cadaveric dissection (She et al., 2018). Morphometric analysis using a 3D bounding box technique was performed on each reconstructed 3D muscle attachment surface with a defined skull-based coordinate system. The size (Length, Width, Thickness, Area), 3D centroid coordinates (x, y, z), and orientation relative to the sagittal (SA), frankfurt (FHA) and frontal (FA) anatomical planes were determined for the bilateral temporalis, masseter, lateral pterygoid and medial pterygoid muscles. Masticatory muscle volumes were determined using a density determination kit and analytical balance (Sartorius YDK01, Germany) (Wright et al., 2018).

TMJ biomechanical analysis

To determine the impact of sexual dimorphisms on human masticatory muscle attachment morphometry associated with craniofacial size on TMJ mechanics, inverse dynamics musculoskeletal models of the mandible were developed and validated (She et al., 2018). Such models were utilized in the present study to calculate temporomandibular muscle forces, muscle moment arms, and TMJ reaction forces during static biting (Figure 2A). Under institutional approval, one healthy 24-year-old female and one healthy 44-year-old male underwent CBCT scanning to produce 3D solid models of heads. Each subject’s anthropometry was determined, and their muscle attachment morphometry was determined from the linear regression models predicting TMJ muscle attachment morphometry by craniofacial size from the cadaveric study. Two subject-specific TMJ computational models incorporating the skull, mandible, temporalis, masseter, lateral pterygoid, and medial pterygoid muscles were constructed for the live subjects. Dynamic stereometry with a customized tracking device recorded the relative position of mandible to skull while biting (Palla et al., 2003). Electromyography (EMG) activities of the bilateral temporalis and masseter muscles were recorded with surface electrodes (Biometrics, Newport, UK). Bite forces were measured with a calibrated force sensor (FlexiForce, Tekscan Inc., South Boston, MA) placed between the right first premolars. Each individual subject performed three static biting oral tasks with increasing bite force magnitude: (1) slight biting, with maximum bite force 36.5N; (2) intermediate biting, with maximum bite force 55.3N; and (3) hard biting, with maximum bite force 69.4N (Figure 2B). The range of bite force magnitudes was determined by referring to human bite forces of chewing typical solid foods with various textures (Takahashi et al., 2009). The obtained mandible kinematics, EMGs, and bite forces were input into the two computational models to calculate temporomandibular instant muscle length, moment arm and joint forces magnitude (Figure 2A). The joint forces direction was determined by calculating the angles between 3D joint force vectors and x-, y-, and z-axes of the previously defined skull-based coordinate system. The results of mean normalized bilateral average temporalis and masseter muscle forces, joint forces with respect to bite force at the plateau region of static biting curves (Figure 2B) were compared between the live female and male subjects.

Figure 2.

Figure 2.

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Biomechanical analysis of the influence of sex-dimorphisms in craniofacial sizes and TMJ muscle attachment morphometry on TMJ mechanics at static biting. (A) Custom tracking devices with fiducial markers fixed rigidly to the skull and jaw of one live female/male subjects were utilized to determine relative position of jaw to skull during mandible static biting. Surface electrodes were used for measuring bilateral EMG activities of temporalis and masseter muscles. Force sensors were inserted between right first premolars to record the bite forces. Functional assessment results of live subjects including bite force, muscle EMG activation, and mandibular kinematics as well as subject-specific 3D craniofacial morphologies of both live and cadaveric subjects (11 females and 10 males) fed into the validated inverse dynamics-based musculoskeletal model (She et al., 2018) of TMJ biomechanics to further calculate the masticatory muscle forces, muscle moment arm and TMJ mechanical loading. (B) The measured bite forces at three different static biting oral tasks with increased maximum forces, which are 36.5N, 55.3N and 69.4N for live female and male ‘Slight’, ‘Intermediate’ and ‘Hard’ biting, respectively. Isometric masticatory muscle forces were generated at plateau region of the static biting curves. (C) Mean bilateral average normalized TMJ reaction forces and temporalis and masseter muscle forces with respect to bite forces at ‘Slight’, ‘Intermediate’ and ‘Hard’ biting for live female and male subjects.

To determine whether differences in female and male mandibular size related to TMJ muscle attachment morphometry could result in different TMJ biomechanics, twenty-one additional TMJ musculoskeletal models (Figure 2A) of the cadaveric mandibles were then developed. Inputs included subject-specific 3D craniofacial anatomies and TMJ muscle attachment morphometry and generic experimental recording of the intermediate bite force and corresponding muscle EMG activities from the respective live female and male subjects. It has been shown that human masticatory muscle activation patterns are reasonably similar during biting (Hiraba et al., 2000). Subsequently, moment arms of the resultant masticatory muscle forces and joint loads at an intermediate biting were calculated.

Statistical analysis

A repeated measures general linear model (RM GLM) with skull side (left, right) as a within-subject factor and donor age as a covariate determined symmetry in muscle attachment morphometry for female and male cadaveric specimens separately. Multivariate GLM with sex (female, male) as a fixed factor and Holm-Bonferroni post-hoc correction for multiple comparisons was used to determine sex-specific differences in TMJ muscle attachment morphometry and joint force direction. The same RM and multivariate GLM procedures were performed on four bilateral mandibular anthropometries to determine asymmetry, and on overall craniofacial anthropometry to determine sex-specific differences. The associations of each muscle attachment morphometric outcome to craniofacial dimensions, including a variable for donor sex, were determined by backward stepwise linear regression analysis. Independent t-tests were conducted to determine the sex-specific differences in 3D mandibular length, mean bilateral average normalized TMJ reaction forces, and the masticatory muscle force moment arm ratio. The correlations of normalized joint forces to mandible sizes and muscle force moment arm ratio under intermediate bite conditions for live and cadaveric subjects were determined by backward linear regression analysis. Normality of the 3D female and male human TMJ muscle attachment morphometry, craniofacial anthropometry, normalized joint forces, and muscle force moment arm ratio was assessed using Shapiro-Wilk’s test and graphically. Descriptive statistics were reported as mean ± standard deviation, and statistically significant differences reported at p<0.05. All statistical analysis was performed using SPSS (Version 24.0, IBM Corp., Armonk, NY).

RESULTS

Sex differences in craniofacial dimension

Craniofacial anthropometry was measured from 3D solid models of cadaveric heads (Figure 1A). No significant asymmetry was discovered in mandibular size for females (p=0.821) or males (p=0.421), therefore bilateral mandibular measurements were averaged. The multivariate GLM showed significant sex effects on overall craniofacial anthropometry (p=0.024), with sex-specific pairwise contrasts for BZB (p<0.001), MBA (p<0.001), ML (p=0.006), RH (p<0.001) and ML* (p<0.001) (Figure 4A). All five linear dimensions were greater in males than females.

Figure 4.

Figure 4.

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Sex-specific differences in cadaveric craniofacial anthropometry (A), and masticatory muscle attachment morphometric sizes, consisting of 3D bounding box Length (B), Width (C), Thickness (D), attachment Area (E) and muscle volumes (F) (11 females and 10 males). ‘T’, ‘M’, ‘LP’ and ‘MP’ are abbreviations of temporalis, masseter, lateral pterygoid and medial pterygoid muscles. ‘TO’ and ‘TI’ denote origin and insertion of temporalis muscle, with ‘TO#’ indicating tenth of the original temporalis origin area listed hereby to be consistent with the scales of areas of other masticatory muscles; ‘MO’ and ‘MI’ denote origin and insertion of masseter muscle; ‘LPIO’ and ‘LPI’ denote inferior origin and insertion of lateral pterygoid muscle; ‘MPI’ denote insertion of medial pterygoid muscle. **: Multivariate general linear model, p<0.01; ***: Multivariate general linear model, p<0.001.

Sex differences in 3D muscle attachment morphometry

Cadaveric human TMJ muscle attachment 3D shapes were created (Figure 3). The 3D TMJ muscle attachment size (Length, Width, Thickness, and Area), centroid coordinates (x, y, and z), orientation (SA, FA, FHA), and muscle volume were successfully determined. RM GLM showed no significant (p>0.05) effects of skull side on TMJ muscle attachment morphometry, therefore female and male bilateral muscle attachment morphometry and volumes were averaged across sides (Figure 4B–F and Figure 5A–F). The multivariate GLM showed significant sex-specific differences in muscle attachment morphometry for temporalis origin (p=0.011), masseter origin (p=0.02) and insertion (p=0.01), lateral pterygoid inferior origin (p=0.035) and medial pterygoid insertion (p=0.011). Pairwise contrasts for temporalis origin determined significant sex-specific differences for Length (p=0.001) (Figure 4B), Thickness (p=0.003) (Figure 4D), Area (p=0.006) (Figure 4E), anterior-posterior position y (p<0.001) (Figure 5B), SA (p=0.002) (Figure 5D), FA (p=0.01) (Figure 5E), and FHA (p=0.012) (Figure 5F). Pairwise contrasts for masseter origin determined significant sex-specific differences for medial-lateral position x (p<0.001) (Figure 5A). Pairwise contrasts for masseter insertion determined significant sex-specific differences for x (p=0.004) (Figure 5A), superior-inferior position z (p<0.001) (Figure 5C), SA (p=0.001) (Figure 5D) and FA (p=0.001) (Figure 5E). Pairwise contrasts for lateral pterygoid insertion determined significant sex-specific differences for Area (p<0.001) (Figure 4E). Pairwise contrasts for medial pterygoid insertion determined significant sex-specific differences for x (p<0.001) (Figure 5A) and z (p=0.004) (Figure 5C). Significant sex-specific pairwise contrasts were determined for temporalis (p=0.002) (Figure 4F) and medial pterygoid (p<0.001) (Figure 4F) muscle volumes.

Figure 3.

Figure 3.

Figure 3.

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Morphology of cadaveric Temporalis, Masseter, Lateral and Medial Pterygoid muscle attachments (11 females and 10 males), where the magenta shaded area on each skull and mandible indicates a representative digitization of the masticatory muscle attachment surfaces. TO is Temporalis Origin; TI is Temporalis Insertion; MO is Masseter Origin; MI is Masseter Insertion; LPIO is Inferior Lateral Pterygoid Origin; LPI and MPI are Lateral and Medial Pterygoid Insertions, respectively. A, P, M, and L stand for the anterior, posterior, medial and lateral directions. These images do not reflect the relative size of the muscle attachments between muscle groups (see Figure 4 and 5) but do represent the relative sizes within a muscle group.

Figure 5.

Figure 5.

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Sex-specific differences in cadaveric masticatory muscle attachment morphometric locations and orientations, including attachment centroid coordinates x (A), y (B), z (C), attachment sagittal angle ‘SA’ (D), frontal angle ‘FA’ (E) and frankfurt angle ‘FHA’ (F) (11 females and 10 males). ‘LPSO’ denotes superior origin of lateral pterygoid muscle. *: Multivariate general linear model, p<0.05; **: Multivariate general linear model, p<0.01; ***: Multivariate general linear model, p<0.001.

Muscle attachment morphometry association with craniofacial size and sex

Significant backward linear regression models between bilateral average muscle attachment morphometric outcomes and the anthropometric parameters, including a variable for donor sex, were developed (Table 1). For masticatory muscle volume, significant linear regression models were determined for the temporalis (p<0.001), masseter (p=0.001), lateral pterygoid (p<0.001) and medial pterygoid (p<0.001). Regression models were determined for temporalis insertion Width (p=0.052) and z (p=0.053), masseter origin SA (p=0.19) and FHA (p=0.16), masseter insertion Area (p=0.083), lateral pterygoid inferior origin FHA (p=0.069), and medial pterygoid insertion Thickness (p=0.091), with none being significant.

Table 1.

Relationship between bilateral average TMJ muscle attachment morphometry, donor sex, and craniofacial anthropometry (backward stepwise regression analysis). Standardized coefficient Beta weights (Lorenzo-Seva et al., 2010) of each predictor variable in linear regression equations were employed to compare relative importance of sex and craniofacial anthropometric parameters in explaining variance of muscle attachment morphometric outcomes. Three anthropometric parameters most frequently correlated with morphometric outcomes for each muscle attachment were presented. No measurements for masseter origin (MO) area or lateral pterygoid superior origin (LPSO) sizes and orientations were applicable because of their limited physiological area, thus labeled by ‘−’. The medial pterygoid origin (MPO) and lateral pterygoid inferior origin (LPIO) were located on the medial-lateral side of the lateral pterygoid plate and were considered to be co-localized and similarly shaped.

Length Width Thickness Area x y z SA FA FHA
TO R2 0.75 0.35 0.84 0.73 0.90 0.57 0.44 0.77 0.80 0.29
p <0.001 0.005 <0.001 <0.001 <0.001 <0.001 0.018 <0.001 <0.001 0.012
Sex 0.89 0.69 0.85 0.67 −0.80 0.44 0.54
CW 0.53 0.59 0.72 0.58 0.71 0.47
MBA −0.56 −0.52 −0.63 −0.66 0.85 −0.76
RH 0.34 −0.75
TI R2 0.33 0.68 0.47 0.67 0.70 0.49 0.37 0.43 0.32 0.40
p 0.008 0.052 0.041 0.001 0.002 0.012 0.053 0.026 0.037 0.036
Sex 0.91 0.58 −0.64 0.45
CW 0.57 −0.47 0.40 0.69 −0.57
GA −0.72 −0.37 −0.77 0.41 0.41 0.4 0.43 −0.34
MO R2 0.82 0.57 0.34 - 0.78 0.82 0.44 0.37 0.47 0.44
p <0.001 0.007 0.025 - <0.001 0.001 0.018 0.19 0.004 0.16
Sex 0.77 0.52 - 0.42
ICW 1.24 - 0.58 1.01 −1.01 1.60
CL −0.57 - −1.06
MBA −0.33 −0.58 - −1.42 0.49 −0.31
MI R2 0.44 0.39 0.54 0.39 0.93 0.26 0.91 0.76 0.87 0.43
p 0.047 0.033 0.027 0.083 <0.001 0.019 <0.001 <0.001 <0.001 0.007
Sex 0.50 −0.58
MBA −0.80 0.53 −0.49 0.69 −0.65
ML 0.79 0.88 0.62 0.51 0.40 0.54
GA −0.53 −0.50 −0.55 −0.49 0.51
LPSO R2 - - - - 0.72 0.54 0.85 - - -
p - - - - <0.001 0.004 0.001 - - -
Sex - - - - - - -
BZB - - - - −0.95 −1.26 −1.03 - - -
ICW - - - - 1.82 0.68 1.10 - - -
LPIO R2 0.42 0.72 0.88 0.67 0.76 0.41 0.50 0.73 0.48 0.33
p 0.007 0.003 <0.001 0.007 <0.001 0.002 0.007 <0.001 0.003 0.069
Sex −0.59 0.57 0.50
ML 0.74 0.82 0.88 1.00 0.64
GA −0.62 −0.55 −0.51 0.59 −0.41 −0.46
ML* 0.55 0.54 −0.44 0.54
LPI R2 0.51 0.58 0.37 0.78 0.83 0.36 0.58 0.31 0.32 0.43
p 0.031 0.012 0.006 0.001 <0.001 0.028 0.004 0.013 0.012 0.035
Sex 0.34
BZB −0.94 −1.03 −0.60 −0.56 0.22
MBA 0.61 0.38
ML* 0.74 0.53 0.81 −0.32 −0.44 0.56 −0.56
MPI R2 0.75 0.70 0.38 0.76 0.96 0.25 0.86 0.67 0.64 0.35
p <0.001 <0.001 0.091 <0.001 <0.001 0.021 <0.001 0.001 <0.001 0.021
Sex −0.85 0.50 0.34
ICW 0.56 0.81 0.50 0.20 −0.64
MBA 0.50 0.47 −0.37 1.29 −1.18 0.62
GA −0.74 −0.35 −0.56 0.50 0.44
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Effect of sexual dimorphisms of muscle attachment morphometry on TMJ mechanics

The effect of sexual dimorphisms in masticatory muscle attachment morphometry and correlated craniofacial size on TMJ biomechanics under static biting was determined by subject-specific musculoskeletal modeling. Although large differences were found between the two live subjects in mean normalized bilateral average temporalis and masseter muscle forces with respect to bite forces (Figure 2C), the mean normalized bilateral average TMJ reaction forces were nearly identical. Similarities in normalized TMJ reaction forces may be due to similar mandible size with mean joint forces ratios of 0.67 and 0.72 (Figure 2C) and 3D mandibular length of 127.44 mm and 129.73 mm respectively (Figure 6A).

Figure 6.

Figure 6.

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Statistically significant sex-specific differences and correlations in human craniofacial sizes, masticatory muscle mechanics and TMJ mechanical loadings for both live and cadaveric subjects at static biting (12 females and 11 males). The live female and male subjects were denoted in black circle. (A) Qualitative and quantitative variation of female and male mandible morphologies, with male 3D mandibular length significantly larger than that of female (p<0.001). (B) Female TMJ loadings are significantly larger than that of male under the same biting condition (p<0.001). (C) Female muscle force moment arm ratios are significantly larger than that of male under the same biting condition (p<0.01). (D) Linear regression models predicting normalized TMJ reaction force by 3D mandibular length (ML*), with an R2 of 0.48 and p<0.001. (E) Linear regression models predicting normalized TMJ reaction force by inter-condylar width (ICW), with an R2 of 0.43 and p<0.001. (F) Linear regression models predicting normalized TMJ reaction force by the ratio between 3D mandibular length (ML*) and moment arm of the resultant masticatory muscle forces, with an R2 of 0.68 and p<0.001. **: Multivariate general linear model, p<0.01; ***: Multivariate general linear model, p<0.001.

A dispersed distribution of 3D mandibular length variation, representing the overall size change of mandibles for the live and cadaveric subjects, was determined for the female study population (Figure 6A), however male mandible sizes were concentrated within a narrow range. Statistically significant sex-specific differences in 3D mandibular length were determined for the live and cadaveric subjects. When considering the natural variation observed in human mandible size and underlying sexually different muscle attachment morphometry, sex-specific differences in normalized TMJ reaction forces and muscle force moment arm ratios at intermediate biting were found (Figure 6B and 6C). Female joint loads, calculated by musculoskeletal models during jaw static biting, were 23% larger than the male on average (p<0.001) when producing the same biting force. The multivariate GLM showed significant sex-specific differences in the direction of joint reaction forces (p=0.001). Pairwise contrasts determined the angle between 3D joint force vector and y-axe of the skull-based coordinate system for females (86.02±2.26°) were significantly smaller than the males (102.22±2.36°) (p<0.001). Significant linear regression models were developed between normalized joint forces, 3D mandibular sizes and muscle force moment arm ratio. Significant negative linear correlations existed between normalized joint forces and 3D mandibular length (R2=0.48, p<0.001) (Figure 6D) and inter-condylar width (R2=0.43, p<0.001) (Figure 6E). Significant positive linear correlation existed between normalized joint forces and muscle force moment arm ratio (R2=0.68, p<0.001) (Figure 6F). Shapiro-Wilk’s test (p>0.05) and visual inspection of the histograms, normal Q-Q plots, and box plots showed that the TMJ muscle attachment morphometry, craniofacial anthropometry, normalized joint forces, and muscle force moment arm ratio were approximately normally distributed for both males and female.

DISCUSSION

The objectives of this study were to determine the sexual dimorphisms in 3D human masticatory muscle attachment morphometry and craniofacial anthropometry, and to determine their impact on TMJ biomechanics. The multivariate GLM determined significant sex-specific differences in overall muscle attachment morphometry for temporalis origin, masseter origin and insertion, lateral pterygoid inferior origin, medial pterygoid insertion, and craniofacial sizes (Figure 4 and 5). Backward linear regression models determined significant correlation between human TMJ muscle attachment morphometry and craniofacial anthropometry (Table 1). The impact of sexual dimorphisms in masticatory muscle attachment morphometry and correlated craniofacial sizes on TMJ biomechanics at static biting was determined through subject-specific musculoskeletal modeling. It was demonstrated that TMJ joint loading was correlated with mandibular sizes (Figure 6D and 6E) and muscle force moment arm ratio (Figure 6F). Female joint loadings were significantly greater, 23% on average, than that of males when producing the same bite forces (Figure 6B).

Male craniofacial sizes are significantly larger than female, which is consistent with population reference values (Hannam and Wood, 1989; Spradley and Jantz, 2011; Weijs and Hillen, 1986; Walker and Kowalski, 1972). Among all ten anthropometric parameters, sex-specific morphologic differences were primarily observed in mandibular sizes concerning the length, breadth and height of the entire mandible. Significant sex-specific differences in human mandibular sizes indicate the differences in moment arm lengths of bite forces and potential dissimilarities in masticatory biomechanics between females and males as it was found that bite force magnitude and craniofacial morphology was correlated (Enlow, 1968).

Significant sex-specific differences in TMJ overall muscle attachment morphometry for temporalis, masseter, lateral and medial pterygoid muscles were determined in the present study. Pairwise contrasts of muscle attachment morphometric outcomes revealed that male temporalis, masseter and medial pterygoid muscle attachment spatial locations and orientations, which directly influence the muscle force generation and determine the muscle moment arm, significantly differ from females. Sex-specific pairwise contrasts were determined for temporalis, masseter and lateral pterygoid muscle attachment sizes and muscle volumes, suggesting physiological cross-sectional areas of these muscles, an indication of the maximal force a muscle is capable of producing (Schantz et al., 1983), may be different between males and females. As a result, it is reasonable to infer that sexual dimorphisms of human masticatory muscle mechanics may exist and thus would influence the resultant TMJ mechanical loadings.

Significant correlation between nearly all masticatory muscle attachment morphometric outcomes, craniofacial anthropometric parameters and donor sex were established (Table 1). The correlation relationship between TMJ muscle attachment morphometry and craniofacial sizes supports the critical role of masticatory muscle forces in human craniofacial growth (Carter et al., 1991). The linear regression analysis determined that craniofacial anthropometry accounted for the majority of the variance in TMJ muscle attachment size and shape, which again highlights the importance of muscle mechanics in craniofacial bone formation. Transverse dimensions of the human head, including bilateral zygomatic breadth and inter-condylar width, were most frequently correlated with muscle attachment morphometry (Table 1), suggesting craniofacial breadth may determine the moment arm length of masticatory muscle forces and corresponding mechanical function. Masseter and medial pterygoid muscle volumes were significantly correlated with gonial angle and ramus height in this study, consistent with previous literature (Benington et al., 1999; Gionhaku and Lowe, 1989).

Sex-specific differences in craniofacial sizes and correlated masticatory muscle attachment morphometry significantly determined TMJ mechanics. It was observed through musculoskeletal modeling that normalized TMJ reaction forces and muscle forces remained constant for the live male and female when maximum bite forces increased from 36.5N to 69.4N (Figure 2C), suggesting a linear relationship between muscle activation EMG and bite force, matching well with previous literature (Gonzalez et al., 2011; Koolstra and Van Eijden, 2005; Uchida et al., 2008). Although large differences in normalized temporalis and masseter muscle forces between live male and female subjects were observed due to inter-subject variability of muscle use when performing similar biting tasks (Hannam and Wood, 1981), normalized TMJ mechanical loads between live male and female subjects with nearly identical mandibular sizes were similar (Figure 2C). With considering natural morphological variation of both live and cadaveric subjects, statistically significant sex-specific differences in normalized TMJ reaction forces (Figure 6B) were determined for the intermediate biting condition. Consistent with their morphology’s description (Figure 6A), males had lower, 23% on average, normalized TMJ reaction forces compared to females when generating the same biting forces, with negative correlations determined between normalized joint forces and 3D mandibular sizes (Figure 6D and 6E). Influence of mandibular size on TMJ mechanics observed in this study is supported by reports indicating that changes in mandibular sizes, especially jaw anteroposterior length, significantly influenced stress magnitude inside the TMJ during the evolutionary transition from cynodont with long mandible to mammaliaform of relatively short jaw (Lautenschlager et al., 2018).

Due to the static equilibrium of the mandible at static biting, the TMJ reaction force is equal to the difference between resultant masticatory muscle forces and biting force according to the force equilibrium. Furthermore, when the biting force remains constant, the torque equilibrium of the entire mandible indicates TMJ reaction force magnitude depends on the ratio between biting force moment arm and moment arm of the resultant muscle forces with respect to the joint center. In the present study, positive correlation with a linear regression slope of 0.32 (coefficient standard error of 0.05) was determined between normalized joint force and the ratio between 3D mandibular length and moment arm of the resultant muscle forces (Figure 6F), which verifies our biomechanical analysis of TMJ mechanics and emphasizes the crucial importance of masticatory muscle attachment morphometry. More specifically, TMJ muscle attachment size, spatial coordinates of the centroid, and orientation regulates the muscle force application, formation of muscle force moment arm, and resultant joint loading. Statistically significant sex-specific differences in the muscle moment arm ratio (Figure 6C) were determined with female muscle moment arm ratio larger than male. Thus, based on force and torque equilibrium of the mandible during static biting, it is reasonable and anticipated to observe female mechanical loading being larger compared to male under the same biting conditions (Figure 6B). Influence of sex-specific differences in craniofacial morphologies on TMJ biomechanics observed in this study are consistent with reported clinical observations that increased TMJ dysfunction risks were found among populations with smaller horizontal and transverse craniofacial dimensions (Sonnesen et al., 2001), since increased TMJ mechanical loading may cause earlier mechanical fatigue and tissue degeneration of TMJ cartilage and disc (Iwasaki et al., 2017; Nickel et al., 2018). Statistically significant sex-specific differences in the direction of TMJ reaction forces were determined. Consistent with previous literature (Iwasaki et al., 2004; May et al., 2001), both female and male joint loads are primarily along the inferior direction of the defined skull-based coordinate system. Nevertheless, female joint force acts at 3.98° on average anteriorly to the vertical coordinate axis, which significantly differs from the 12.22° posterior disposition for the males as a result of the sex-specific differences in the muscle moment arm ratio.

Study limitations include a relatively small size of cadaveric samples (ten males and eleven females) and inclusion of only one live male and female. A power analysis was performed to study the sex-specific differences in the representative measurement outcomes including 3D mandibular length, normalized TMJ reaction forces and masticatory muscle moment arm ratios. With the current sample sizes, there are 80–95% power to detect a large standardized effect (Cohen’s d) ranging from 1.23 to 1.58, indicating more subjects required for adequate power. However, all of the donor’s heads in this study were carefully screened by experienced oral maxillofacial surgeons to meet our inclusion criteria excluding subjects with a known history of TMJ disorder or craniofacial deformity. Given the well-controlled donor populations with normal musculoskeletal anatomy, statistically significant sexual dimorphisms in craniofacial size, TMJ muscle attachment morphometry, muscle force moment arm ratio, and TMJ mechanical loadings were successfully determined. Moreover, subject-specific musculoskeletal modeling of TMJ biomechanics for cadaveric male and female subjects incorporated generic muscle EMG activities from live male and female subjects, respectively. Considering the major purpose of studying the influence of craniofacial sizes and masticatory muscle attachment morphometry on TMJ mechanics, the potential variation of muscle activation across the subjects and its impact on TMJ mechanics shall need to be controlled. In order to further study the impact of sex-specific differences in muscle physiology and craniofacial morphology on masticatory mechanical function, TMJ functional assessment for more normal populations and even TMJ disorder patients are required in the future.

In conclusion, significant sexual dimorphisms in human craniofacial size and TMJ muscle attachment morphometry were determined. Variation in TMJ muscle attachment morphometric size, location and orientation were significantly correlated with craniofacial size and donor sex. Sex-specific differences in craniofacial morphology and muscle attachment morphometry produced the greatest differences in female and male masticatory system mechanical function, with significant correlations between TMJ reaction forces and mandibular size, which would potentially predispose females to the development of TMJ disorders.

ACKNOWLEDGEMENTS

This project was supported by NIH grants DE018741, DE021134 and GM121342, NIH T32 (DE017551) post-doctoral fellowships to CNH and MCC, and a NIH F32 post-doctoral fellowship DE027864 to MCC.

Footnotes

CONFLICT OF INTEREST

None of the authors of this paper has a conflict of interest that might be construed as affecting the conduct or reporting of the work presented.

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