sexual dimorphism in the hard tissue
Since the advent of the cephalostat, orthodontists have analyzed the human skull. Many studies support the idea that the size and shape of the craniofacial hard tissues, which gives the supporting structure for the face, are different between males and females. The most obvious and consistent finding has been that the male skull is larger than the female skull (Ingerslev and Solow, 1975; Bibby 1979; Miyajima et al. 1996; Rosas and Bastir, 2002; Franklin et al. 2005; Veyre-Goulet et al. 2008; Dayal et al. 2008; Green and Curnoe, 2009). Numerous studies have gone further in specifying the areas of the bony head and face that show the greatest sex differences. Franklin et al. (2005), for example, reported the largest dimorphism in facial width, cranial length, and cranial height. Alternatively, Dayal et al. (2008) found the most significant difference in total face height, bizygomatic breadth, and mandibular ramus height. Researchers have also tried to find an efficient method for discriminating and classifying sex on the basis of skull measurements. Size was a key factor in separating the sexes, and several studies have tried to establish a formula with high predictability based on radiograph analyses. For example, Ceballos and Rentschler (1958) claim 88% accuracy in identifying the sex of the skull. Similarly, Townsend et al. (1982) was able to achieve 80% accuracy, Inoue (1990) 85%, Hsiao et al. (1996) 100%, and Patil and Mody (2005) 99% in identifying the correct sex. Patil and Mody (2005) identified seven major variables important to their discriminant function: length of cranial base (Ba-N), mastoid height from cranial base (MaHt), total face height (N-M), mastoid width at the level of cranial base (MaWd), middle facial depth (Ba-ANS), perpendicular distance from mastoidale to FH plane (Ma-FH), and maximum length of skull (G-Op), ordered from most to least important. These studies indicate that males and females are clearly distinguishable on the basis of skull radiographs.
In further breaking down the dimorphism into specific regions, males have been found to exhibit some differences in the configuration of the nasal bones. Several studies have reported that males tend to have a more prominent nasal bone (Ingerslev and Solow, 1975; Inoue et al. 1992; Carels 1998; Rosas and Bastir, 2002). In assessing 153 adult Danish dental students, Ingerslev and Solow (1975) concluded that males have a more prominent nasal bone projection. From 100 Japanese skulls, Inoue et al. (1992) also found that the male nasal bone is more developed. Carels (1998) identified the same characteristic among Dutch people, and Rosas and Bastir (2002) observed that males had an increased angulation of the nasal bones among Portuguese adults.
In assessing the upper facial third, which is usually delineated by trichion and soft tissue glabella, the frontal bone shape and projection may also be important sex discriminators. Ingerslev and Solow (1975) concluded that females have a frontal bone that is more prominent than males. Bulygina et al. (2006) also agreed that males have a relatively smaller and flatter frontal bone. Bigoni et al. (2010) had findings that agreed with the flatter frontal bone in males, but concluded that males have a more prominent glabella. Inoue et al. (1992) and Carels (1998) also agreed that males have a more prominent supraorbital ridge, which forms the interface between the viscerocranium and cranial vault. Bigoni et al. (2010) performed a geometric morphometric analysis, and they found that males had a lower, wider, flatter, and vertically oriented upper face while the females had a higher forehead and face that was more convex.
Bastir et al. (2011) studied the airway in 212 adults. Their finding was in line with previous studies that males have a larger airway than females (Bastir et al. 2011; Rosas and Bastir, 2002; Enlow and Hans, 2008). Males still had a larger airway even after adjustments were made for differences in absolute size. This could translate to a larger midfacial dimensions for males in the overall appearance (Bastir et al. 2006; Bulygina et al. 2006). The larger airway was particularly due to a vertically taller choanae according to Bastir et al. (2011). This is also supported by previous studies which state that there are sexual differences in the choanae (Bastir et al. 2009). According to Bastir and co-workers, males had taller piriform apertures, internal nasal cavities, and choanae than females. And even after standardization for size, males still had larger airways than females (Bastir et al. 2011). Bulygina in 2006 concluded that a larger airway manifest itself as a forward projection of the upper nasal area as well as a wider midface (Bulygina et al. 2006). Overall, a larger airway would result in a dimorphic facial form with males having a taller middle third of the face in the sagittal plane as well as a wider midface in the frontal plane.
In the lower third of the face, Schmittbuhl et al. (2001) found that the mandible is significantly different between the sexes via elliptical Fourier analysis of mandibular outlines; his finding are consistent with other studies by Giles (1964), Steyn and Iscan (1998), Iscan and Steyn (1999), and Franklin et al. (2008). Thayer and Dobson (2010) inspected the chin via elliptical Fourier functions analysis and found that, “males tend to have more protruding chins with well-developed lateral tubercles”. This is in accord with previous findings by Bass (1995), Byers (2002), and Schwartz (2007). A more protrusive chin would lead to straighter and more concave profiles as well as the capability to camouflage retrognathia. De Freitas et al. (2007) concluded in their study of 130 lateral cephalograms that “boys have a greater tendency for a vertical pattern of growth than girls”, and therefore a greater potential for increased lower face height. Yamauchi et al. (1967) came to a similar conclusion in an adult study that males had a taller lower face height than females. Coquerelle et al. (2011) used 159 CT scans and geometric morphometric analysis to conclude that the mental region is located more inferiorly in males than females, which would again add to the lower third dimension in males.
Although a universal agreement does not exist as to the precise nature of the differences, it is clear that sex differences are present in the craniofacial hard tissues. Therefore the hard tissue differences should manifest themselves in the soft tissue makeup of the sexes. However, in light of Subtleny’s (1959) observation, “all parts of the soft tissue profile do not directly follow the underlying skeletal profile”, the hard tissue differences may not fully express themselves onto the overlaying soft tissue.
In 1931, Broadbent and Hofrath standardized the method in taking lateral cephalograms for analysis, and since then, dentoskeletal analysis was the mainstream method in diagnosis and treatment planning (Fernandez-Riveiro et al. 2002). In 1956, Downs started to utilize the filters in order to capture the soft tissue profile in a lateral cephalogram after realizing that “possible anomalies in the hard tissues could be masked or exaggerated by the soft tissues. In other words, soft tissues did not always follow the underlying dentoskeletal profile” (Fernandez-Riveiro et al. 2002). Subtleny, in 1959, produced a paper on longitudinal soft tissue structures, and concluded that not all of the soft tissues follow the underlying hard tissues equally (Subtleny, 1959). In 1960, Steiner developed the S-line to quantify the position of upper and lower lips (Steiner, 1960). Ricketts, in 1968, developed a similar reference, the E-plane, to create some sort of norms in evaluating the position of upper and lower lips (Ricketts, 1969). Burstone also produced papers in 1958 and 1967 highlighting the importance of the soft tissue profile and lip position in treatment planning (Burstone 1958; 1967). This trend continues into current literature in shifting the focus onto incorporating the soft tissue analyses in diagnosis and treatment planning.
Arnett et al. published an article in 1999 highlighting the difference in soft tissue thickness between the sexes (Arnett et al. 1999). Similarly, Skinazi et al. and Kalha et al. found that soft tissues of the upper lip, lower lip, and chin were all thicker in males than in females (Skinazi et al. 1994, Kalha et al. 2008). In recognition of these differences, Arnett et al. suggested that, “separate values are suggested for male and female patients” (Arnett et al. 1999). Begg and Harkness also pushed for similar standards to be established stating, “age and sexual differences in nasal size and proportions indicate that separate standards are necessary for men and women” (Begg and Harkness, 1995).
Many papers agree that the soft tissue dimensions are significantly larger in men than in women (Budai et al. 2003; Evison et al. 2010; Ferrario et al. 1993, 1994, 1995, 1996, 1998; He et al. 2009; Hennessy et al. 2002; Lundstrom et al. 1992; Scheideman et al. 1980; Starck and Epker, 1996). Ferrario et al. even quantified this measure concluding that, “male faces are 6-7% larger than female faces” (Ferrario et al. 1994). Other studies tried to further dissect this finding by focusing on different parts of the face. For example, Sforza et al. found significant differences in the orbit where males had larger binocular width, intercanthal width, length of the eye fissure, soft tissue orbital area, and inclination of the orbit relative to the true horizontal (Sforza et al. 2009a). In line with Sforza et al.’s findings, Ferrario et al. also concluded that males had larger binocular width, intercanthal width, height and length of the orbits (Ferrario et al. 2001). In the lip, males had significantly larger mouth width, width of the philtrum, total lip height, and lip volumes; however, vermilion height to mouth width ratio was larger in females (Sforza et al. 2010). Differences were also seen in the nose, as males had larger nasal linear dimensions, larger external nasal volume and area, and larger nasal width to height ratios (Sforza et al. 2011). A study from Japan in 1995 separated parts of the face in a frontal photograph in order to identify the sex from the isolated part of the face, and correct identification of sex was made in 68% of the time in assessing the mouth, 65% in assessing the eyes, and 58% in assessing the nose (Inoue et al. 1995). Toma et al. also came to a similar conclusion in that females tended to have more prominent eyes and cheeks while males tended to have more prominent noses and mouths; thus establishing sexual dimorphism in these individual areas that constitute the face (Toma et al. 2008). In the ear, Sforza et al. found differences where males had significantly larger dimensions in all categories they assessed (Sforza et al. 2009b).
Moving beyond linear comparison, criteria such as angular measurements and ratios can be compared. Ferrario and colleagues found that while there was a significant difference in linear measures, there was no difference in angular measures between the sexes (Ferrario et al. 1996, 1999). But a study in 2003 found some significant angular differences in nasofrontal, nasal, vertical nasal, nasal dorsum, and cervicomental angles (Fernandez-Riveiro et al. 2003). Although Begg and Harkness found no differences in nasofrontal or nasolabial angles, there was a significant difference in the nasal dorsum angle where males had a straighter nose while the females had more supratip break angle to their noses (Begg and Harkness, 1995). The supratip break in females has been well documented in various sources. Enlow stated that the male nose tips downwards while the female nose tips upwards (Enlow, 1990). Ferrario et al., via harmonic analysis, found that the male nose is more likely to be straight or convex while the female nose is more concave (Ferrario et al. 1992). Kale-Varlik also found differences in nasofacial angle, middle facial height angle, nasal angle, and nasolabial angle; but found no difference in nasofrontal angle, nasomental angle, labiomental angle, facial angle, and lower facial height angle (Kale-Varlik 2008). He et al., in observing Chinese adults, found that nasal tip angle and nasolabial angle had no significant differences while the nasofrontal angle was more acute in men possibly owing to a more prominent supraorbital ridge (He et al. 2009).
In looking at proportionality, Ferrario et al. concluded that males had a longer lower 1/3 of the face while females had a longer middle 1/3 of the face (Ferrario et al. 1996). In the sagittal plane, Skinazi et al. observed that the percentage contribution of the lips were the same in both sexes; key difference was that the female nose ratio to profile was higher resulting in a more convex profile, while in men, the chin contribution was larger resulting in a straighter profile (Skinazi et al. 1994). He et al. and Sforza et al. noted that men had a larger base to height ratio of the nose (He et al. 2009, Sforza et al. 2011).
Size as well as shape can both contribute to differences in morphology. With size being a consistent sexually dimorphic finding as stated above, several articles focused on taking size out of the equation by comparing male and female faces scaled to the same size. However, the findings were not consistent. Ferrario et al. in 1994 used Euclidean distance matrix analysis and found that there was no significant sexual dimorphism in 3-dimensional facial shape (Ferrario et al. 1994). Starck and Epker in 1996 also came to similar conclusions via ratio comparisons (Starck and Epker, 1996). Ferrario et al. took a different approach by using mesh diagrams in 1998 and 1999 and found that the differences were very limited. But small findings included that males had a lower gonia and more posterior cheeks than females; the lower facial third was larger, more anterior, and more inferior in males; females had more anterior cheeks; and females had more anteriorly positioned forehead/trichion (Ferrario et al. 1998, 1999). Halazonetis, via morphometric analysis, came to a similar conclusion in that “sex differences in shape were small” (Halazonetis 2007). In using the Fourier analysis to assess the soft tissue, Ferrario et al. concluded that, “the present 3-dimensional study did not find a significant sex difference in the shape of the soft tissue facial contour” (Ferrario et al. 1995). Contrastingly, in 1993 Ferrario et al. concluded that there are sexual differences in size and shape according to Euclidean distance matrix analysis (Ferrario et al. 1993). Moreover, Hennessy and co-workers explores this question using a geometric morphometric approach and concluded that there was strong evidence of sexual dimorphism in their assessment of 131 individuals; they stated “our findings are that among females: the face is wider and, as seen from the side flatter; in the upper face the eyes are more lateral and anterior, and nasion is posterior; the nose is smaller, narrower and less protrusive; the distance between the lower and upper margins of the lips is greater, and the upper lip is located more posteriorly, as is the chin” (Hennessy et al. 2002). Hennessy et al. expanded on their earlier finding by describing the following features that make a face feminine: “greater posterior and superior displacement of the upper lip and philtrum; more reduced anterior projection of the nose; more outwardly displaced malar regions; increased superior and posterior displacement of the chin along with medial displacement of the gonial angle; increased medial displacement of the inferior ear attachment point and inferior displacement of the superior ear attachment point; and increased superior and posterior displacement of the superior medial orbital margins and lateral displacement of the superior lateral orbital margins” (Hennessy et al. 2005). Size differences were removed with analyses such as Euclidean distance matrix analysis, ratio comparisons, mesh diagrams, geometric morphometric analysis, and Fourier analysis. As the underlying sexual dimorphism was revealed, the soft tissue facial morphology differences seem to be very subtle.