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Estimating Sex of Modern Greeks Based on the Foramen Magnum Region.

1. Introduction

Reliable sex determination is one of the principal aims when examining human skeletal remains. In forensics or anthropology, the occipital bone is frequently used in sex determination because the cranial base tends to withstand both physical insults and inhumation more successfully than many other areas of the cranium [1].

There are two major methods for sex determination from the cranium. The first one is based on morphological criteria [2-4]. The roughness of the nuchal lines and the prominence of the external occipital protuberance are good indicators for the qualitative diagnosis of sex [5]. The second one is based on metric criteria using discriminant functions [6, 7]. The dimensions of the occipital condyles and the foramen magnum have been reported as useful for quantitative diagnosis of sex by several authors [8-10]. According to Gapert and his colleagues [11], the correctly classified crania ranged from 65.8% for univariate functions to 70.3% for multivariate functions. Gapert and his colleagues [11] evaluated the foramen magnum of eighteenth and nineteenth century British adult skulls. However, discriminant functions should be used only when the individual is known to come from the same population from which the functions were derived [12,13], since sexual dimorphism is population-specific [14].

The aim of the present study is to assess the use of the foramen magnum as well as the occipital condyles for sex determination on adults by developing discriminant functions for a modern Greek population. Previous research regarding the foramen magnum region in a Greek population was conducted by Natsis and his colleagues in 2013 [15]. Natsis and his colleagues [15] classified the foramen magnum region according to its shape and they investigated possible correlations between anatomic metric values and various parameters. According to their results, the foramen magnum region exhibits sexual dimorphism.

2. Material and Methods

The sample consisted of 154 adult crania of Greek individuals of known sex and age at death: 77 males and 77 females. These crania constitute part of the modern skeletal reference collection (known as the Athens Collection) housed in the Department of Animal and Human Physiology (Faculty of Biology, National and Kapodistrian University of Athens). All individuals are Greek nationals who died in Athens and were buried and then exhumed from local cemeteries. The age at death of the individuals ranges from 19 to 99 years old and their year of birth from 1879 to 1965. Year of death for all individuals ranges between 1960 and 1996, while the place of birth covers the entire country. Individuals without any evidence of trauma or dysmorphism were selected. The parameters examined were as follows:

(1) The foramen magnum length (FML) direct distance from basion to opisthion

(2) The foramen magnum breadth (FMB) maximum distance between the lateral margins of foramen magnum

(3) The foramen magnum index (FMI) calculated using the formula: (FMB x 100)/FML

(4) The foramen magnum area (FMA) calculated using Radinsky's [16] formula: (1/4) xnx FMB x FML

(5) The occipital condyle length (OCL) direct distance along the long axis from the most anterior to the most posterior point on the margin of the occipital condyle

(6) The occipital condyle breadth (OCB) direct distance perpendicular to the long axis from the most lateral to the most medial point on the margin of the occipital condyle

(7) The minimum intercondylar distance (MID) direct distance from the most medial point on the margin of the left occipital condyle to the most medial point on the margin of the right occipital condyle

The 3D coordinates of the foramen magnum region were collected using an Immersion Corporation MicroScribe 3DX digitizer with a standard error of 0.23 mm. Microsoft Excel was used with MicroScribe 3DX to obtain the coordinates (x,y,z) of each landmark and to calculate the equivalent interlandmark distances (Figure 1).

Initially, descriptive statistics (mean, standard deviation) were carried out for each parameter. Additionally, regarding the occipital condyles parameters, an independent samples t-test was performed in order to ascertain whether any bilateral asymmetry exists. Finally, to analyze sex differences, independent samples t-test and discriminant function analysis (DFA) were used. The DFA was calculated for all parameters. However, the foramen magnum index as well as the area of the foramen magnum was not combined with the foramen magnum length or breadth, since a DFA is optimal when few of the single variables correlate.

All the statistical analyses were performed using the Statistical Package for Social Sciences (IBM SPSS version 23.0, Armonk, NY).

3. Results and Discussion

3.1. Results. The results of the descriptive statistics are presented in Table 1. The mean values for all parameters were higher in males than females. All data were normally distributed according to the results of the Shapiro-Wilk test. Consequently, a parametric test was performed in order to ascertain whether any bilateral asymmetry exists regarding the dimensions of the occipital condyles and to analyze sex differences. According to Table 2, no statistically significant difference between right and left side was found in either the occipital condyle length or the occipital condyle breadth. Therefore, the averages of the distances obtained from both sides were used in the subsequent analysis.

The results shown in Table 3 indicate that, with the exception of the foramen magnum index, all parameters are influenced by sex (p < 0.05). The discriminant functions for each single parameter and five possible combinations of them are given in Table 4. Additionally, Table 4 shows the results of the cross-validation based on "leave-one-out" principle. The most reliable single parameter for sex determination was the occipital condyle length (69.5%) followed by Radinsky's area (66.9%). Finally, the minimum intercondylar distance combined with the occipital condyle length as well as the occipital condyle breadth proved to be the best combination of parameters regarding sex determination (74.0%) followed by the combination of Radinsky's area, the occipital condyle length, and the occipital condyle breadth (72.1%).

3.2. Discussion. Regarding the nonexistence of bilateral asymmetry of the occipital condyles, our results are in agreement with those of other populations [17, 18]. Additionally, the present study confirms the results of Natsis and his colleagues [15] regarding the presence of sexual dimorphism in the foramen magnum region in the modern Greek population. Natsis and his colleagues' [15] sample included skulls of unknown age, mainly from the collection of the Departments of Anatomy of Aristotle University (Thessaloniki). On the other hand, all the individuals we examined were acquired from cemeteries in the Athens area with known age at death and year of birth. The mean values of length and width of the foramen magnum and the mean value of breadth of the occipital condyle of our sample are similar to Natsis and his colleagues sample. However, when comparing the mean values of the length of the occipital condyle and minimum intercondylar distance, our sample shows smaller and bigger values, respectively (Table 5). According to our observations, there might be variation in the occipital condyles among different parts of Greece.

Comparison of the distance parameters in different populations is given in Table 5. When observing the description of the foramen magnum length and the foramen magnum breadth, the modern Greek population seems to show similar values for males and females, as the Turkish [19, 20], British [11], and Spanish [21] populations. The Indian [22] population, especially the Indian females, seems to show smaller values, when compared to the aforementioned populations.

In regard to the occipital condyle variables, the Greek population has higher OCB value than the European American [23], the African American [23], the Turkish [20], and the British [24] populations. According to Uysal and her colleagues [20], the Turkish population demonstrates by far the lowest values of MID. The extreme values for MID in Uysal et al.'s [20] paper suggests an error in reporting or a typo in the final manuscript. Finally, according to our results, the Greek population has similar OCL value with the European American [23] and the British [24] populations.

In the Greek population, the best determination of the correct sex, regarding the foramen magnum variables, was achieved through the foramen magnum area (66.9%), while the combination of the foramen magnum variables achieved only 65.6% (Table 4). In comparison, the occipital condyles provide a higher determination of the correct sex than the foramen magnum. The combination of the occipital condyle variables allowed for the development of discriminant functions that predicted the correct sex in 74% of all cases, while the best single variable (OCL) achieved 69.5%. These relatively low classification accuracies reflect the low amount of sexual dimorphism and indicate that these variables should be used with caution when attempting to estimate sex.

The low degree of sexual dimorphic expression within the foramen magnum may be explained by the fact that it reaches the end of growth rather early in childhood [25]. Therefore, no significant secondary sexual changes are expected to develop. Additionally, the prime function of the for a men magnum is to transmit the medulla oblongata and its membranes as well as the spinal component of the accessory nerve into the skull and no muscles act upon its shape and size. Although sex differences of the occipital condyles, whose prime function are to enable the head to move relative to the cervical vertebral column, are low compared to other anatomical regions [26], they are still higher when compared to the foramen magnum. The cranial base's cartilages are known to resist compression [27] and the atlantooccipital joint is primarily under static strain [28]. However, although loading stresses do not seem to play a major role in influencing dimorphic expression in the occipital condyle, the biomechanical function of the craniocervical joint could be one reason for the increased expression of sex dimorphism in occipital condyles when compared to the foramen magnum. According to Gapert and his colleagues [24], it is more likely that the expression of sexual dimorphism in the occipital condyles is mainly due to genetic rather than epigenetic factors. Therefore, it is important to know the origin of any unidentified skull in order to choose the appropriate population-specific discriminant function formula for estimating sex.

4. Conclusions

This study confirms that the foramen magnum region exhibits sexual dimorphism; however, the dimorphic expression is low to moderate. Although other anatomical regions, such as the pelvis, can discriminate between sexes with higher accuracy, the functions developed in this study could be used in cases of fragmented cranial remains. Finally, since the discriminant function sexing formulas are population-specific, this method should be applied on samples that belong to Greek populations or at least to populations with similar expression of sexual dimorphism in the foramen magnum region. Because error rates are expected to be relatively high (26% or higher), sex estimation using these discriminant functions should be done with extreme caution.

https://doi.org/10.1155/2017/9129801

Conflicts of Interest

The authors declare that there are no conflicts of interest regarding the publication of this paper.

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Maria-Eleni Chovalopoulou and Andreas Bertsatos

Department of Animal and Human Physiology, Faculty of Biology, School of Sciences, University of Athens, Panepistimiopolis, 157 81 Athens, Greece

Correspondence should be addressed to Maria-Eleni Chovalopoulou; marilenachov@biol.uoa.gr

Received 2 March 2017; Revised 28 May 2017; Accepted 3 July 2017; Published 31 July 2017

Academic Editor: Hugo Cardoso

Caption: FIGURE 1: Foramen magnum region parameters. (1) FML: foramen magnum length; (2) FMB: foramen magnum breadth; (3) OCL: occipital condyle length; (4) OCB: occipital condyle breadth; (5) MID: minimum intercondylar distance.
TABLE 1: Descriptive statistics: dimensions, index, and
area of the foramen magnum and the occipital condyles
(in mm).

             Mean    Std. deviation   Minimum   Maximum

FMB
  Male      32.48         2.70         26.92     40.01
  Female    30.62         2.18         24.80     36.52
FML
  Male      36.69         2.47         30.02     42.18
  Female    34.87         2.41         27.97     40.98
FMI
  Male      88.70         6.87         74.43    104.55
  Female    88.04         6.76         75.73    108.67
FMA
  Male      938.12       123.20       669.14    1238.50
  Female    839.82       99.91        613.63    1144.62
OCL-left
  Male      24.36         2.68         17.76     30.83
  Female    22.21         2.33         16.41     26.57
OCL-right
  Male      24.52         3.07         16.43     30.46
  Female    22.51         2.41         15.51     28.46
OCB-left
  Male      13.99         1.96         10.03     20.37
  Female    13.17         1.84         9.14      17.72
OCB-right
  Male      13.80         1.92         10.33     18.68
  Female    12.76         1.76         8.78      17.51
MID
  Male      24.28         3.01         15.95     32.53
  Female    22.21         2.58         16.34     28.06

TABLE 2: Mean differences in dimensions of the
occipital condyles between right and left side.

             t     df    Sig. (2-tailed)

OCL
  Male     -.347   152        .729
  Female   -.795   152        .428
OCB
  Male     .607    152        .545
  Female   1.415   152        .159

p value < 0.05 is accepted as statistically significant.

TABLE 3: Mean differences of the parameters of the foramen
magnum and the occipital condyle between males and females.

         t      df    Sig. (2-tailed)

FMB   4.716 *   152        .000
FML   4.626 *   152        .000
FMI    .592     152        .554
FMA   5.438 *   152        .000
OCL   5.326 *   152        .000
OCB   3.410 *   152        .001
MID   4.522 *   152        .000

* Parameters are significant at the 0.05 level.

TABLE 4: Discriminant function (DF) equations for the foramen
magnum region.

Variables               Wilk's lambda     x2     Sig.

FMB                         0.872       20.689   0.000
FML                         0.877       19.955   0.000
FMA                         0.837       26.932   0.000
FMB + FML                   0.836       26.980   0.000
OCL                         0.843       25.924   0.000
OCB                         0 929       11.170   0.001
MID                         0.881       19.124   0.000
OCL + OCB                   0.831       27.884   0.000
OCL + OCB + MID             0.698       54.052   0.000
FMA + OCL + OCB             0.753       42.693   0.000
FMA + OCL + OCB + MID       0.681       57.681   0.000

Variables                     Function       Cross-validation'
                            coefficients         hit ratio

FMB                     Constant   -12.851         65.6%
                          FMB       0.407
FML                     Constant   -14.658         63.6%
                          FML       0.410
FMA                     Constant   -7.926          66.9%
                        FM area     0.009
                        Constant   -16.026
FMB + FML                 FMB       0.244          65.6%
                          FML       0.233
OCL                     Constant   -9.670          69 5%
                          OCL       0.413
OCB                     Constant   -7.954          57.1%
                          OCB       0.592
MID                     Constant   -8.199          64.3%
                          MID       0.353
                        Constant   -10.616
OCL + OCB                 OCL       0.350          67.5%
                          OCB       0.180
                        Constant   -15.026
OCL + OCB + MID           OCL       0.317          74.0%
                          OCB       0.108
                          MID       0.265
                        Constant   -12.167
FMA + OCL + OCB         FM area     0.006
                          OCL       0.176          72.1%
                          OCB       0.211
                        Constant   -15.113
                        FM area     0.003
FMA + OCL + OCB + MID     OCL       0.244          71.4%
                          OCB       0.140
                          MID       0.214

* Based on "leave-one-out" principle. p value [less than or equal
to] 0.05 is accepted as statistically significant.

TABLE 5: Comparison of the distance parameters (mean [+ or -]
SD in mm) in various studies.

A                                                   N
                             Sample origin
                                                  Total

Routal et al. (1984)            Indian             141
Catalina-Herrera (1987)         Spanish            100
We scott and Moore         African American        133
  -Jansen (a) (2001)       European American       389
Murshedetal. (2003)             Turkish            110
Uysal et al. (a) (2005)         Turkish            100
Gapert et al (b) (2009)         British        158/146 (c)
Natsis et al. (b) (2013)         Greek             143
Present study (b) (2017)         Greek             154

A                                           FML

                                  Male                 Female

Routal et al. (1984)        35.5 [+ or -] 2.8     32.0 [+ or -] 2.8
Catalina-Herrera (1987)     36.2 [+ or -] 0.3    34.30 [+ or -] 0.4
We scott and Moore                 --                    --
  -Jansen (a) (2001)               --                    --
Murshedetal. (2003)        37.2 [+ or -] 3.43    34.6 [+ or -] 3.16
Uysal et al. (a) (2005)    37.08 [+ or -] 1.93   34.87 [+ or -] 2.6
Gapert et al (b) (2009)    35.91 [+ or -] 2.41   34.71 [+ or -] 1.91
Natsis et al. (b) (2013)   36.20 [+ or -] 3.39   34.79 [+ or -] 2.39
Present study (b) (2017)   36.69 [+ or -] 2.47   34.87 [+ or -] 2.41

A                                            FMB

                                  Male                 Female

Routal et al. (1984)        29.6 [+ or -] 1.9     27.1 [+ or -] 1.6
Catalina-Herrera (1987)     31.1 [+ or -] 0.3     29.6 [+ or -] 0.3
We scott and Moore                 --                    --
  -Jansen (a) (2001)               --                    --
Murshedetal. (2003)        31.6 [+ or -] 2.99    29.3 [+ or -] 2.19
Uysal et al. (a) (2005)    30.83 [+ or -] 2.04   28.93 [+ or -] 2.43
Gapert et al (b) (2009)    30.51 [+ or -] 1.77   29.36 [+ or -] 1.96
Natsis et al. (b) (2013)   30.92 [+ or -] 3.15   29.61 [+ or -] 2.08
Present study (b) (2017)   32.48 [+ or -] 2.7    30.62 [+ or -] 2.18

A                                  OCL

                                   Male

Routal et al. (1984)                --
Catalina-Herrera (1987)             --
We scott and Moore          23.2 [+ or -] 2.9
  -Jansen (a) (2001)        24.7 [+ or -] 2.7
Murshedetal. (2003)                 --
Uysal et al. (a) (2005)    22.73 [+ or -] 2.26
Gapert et al (b) (2009)    24.95 [+ or -] 2.53
                           /25.16 [+ or -] 2.51
Natsis et al. (b) (2013)   26.30 [+ or -] 2.92
                           /26.48 [+ or -] 2.80
Present study (b) (2017)   24.52 [+ or -] 3.07
                           /24.36 [+ or -] 2.68

A                                  OCL

                                  Female

Routal et al. (1984)                --
Catalina-Herrera (1987)             --
We scott and Moore           22 [+ or -] 1.2
  -Jansen (a) (2001)        22.8 [+ or -] 2.2
Murshedetal. (2003)                 --
Uysal et al. (a) (2005)     20.58 [+ or -] 2.24
Gapert et al (b) (2009)    23.30 [+ or -] 2.28
                           /23.74 [+ or -] 2.44
Natsis et al. (b) (2013)   24.70 [+ or -] 2.66
                           /24.57 [+ or -] 2.13
Present study (b) (2017)   22.51 [+ or -] 2.41
                           /22.21 [+ or -] 2.33

A                                  OCB

                                   Male

Routal et al. (1984)                --
Catalina-Herrera (1987)             --
We scott and Moore          12.8 [+ or -] 1.2
  -Jansen (a) (2001)        12.3 [+ or -] 1.2
Murshedetal. (2003)                 --
Uysal et al. (a) (2005)     12.5 [+ or -] 1.57
Gapert et al (b) (2009)    12.01 [+ or -] 1.41
                           /12.05 [+ or -] 1.69
Natsis et al. (b) (2013)   13.13 [+ or -] 2.01
                           /13.24 [+ or -] 2.20
Present study (b) (2017)    13.8 [+ or -] 1.92
                           /13.99 [+ or -] 1.96

A                                  OCB                   MID

                                  Female                 Male

Routal et al. (1984)                --                    --
Catalina-Herrera (1987)             --                    --
We scott and Moore           12 [+ or -] 1.5       20.1 [+ or -] 3.0
  -Jansen (a) (2001)        11.7 [+ or -] 1.3      20.9 [+ or -] 2.4
Murshedetal. (2003)                 --                    --
Uysal et al. (a) (2005)    11.78 [+ or -] 1.06     5.6 [+ or -] 0.97
Gapert et al (b) (2009)    11.42 [+ or -] 1.21    21.12 [+ or -] 3.18
                           /11.57 [+ or -] 1.16
Natsis et al. (b) (2013)   13.04 [+ or -] 1.99    19.82 [+ or -] 3.19
                           /12.74 [+ or -] 1.63
Present study (b) (2017)   12.76 [+ or -] 1.76    24.28 [+ or -] 3.01
                           /13.17 [+ or -] 1.84

A                                 MID

                                 Female

Routal et al. (1984)               --
Catalina-Herrera (1987)            --
We scott and Moore          18.6 [+ or -] 2.5
  -Jansen (a) (2001)        19.2 [+ or -] 2.0
Murshedetal. (2003)                --
Uysal et al. (a) (2005)    4.91 [+ or -] 0.83
Gapert et al (b) (2009)    19.0 [+ or -] 2.40
Natsis et al. (b) (2013)   18.77 [+ or -] 3.26
Present study (b) (2017)   22.21 [+ or -] 2.58

(a) Left; (b) right/left; (c) foramen magnum/occipital condyles.
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Publication:Journal of Anthropology
Date:Jan 1, 2017
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