J Forensic Sci, May 2014, Vol. 59, No. 3 doi: 10.1111/1556-4029.12376 Available online at: onlinelibrary.wiley.com
PAPER ANTHROPOLOGY
Dilhan İlgüy,1 Ph.D.; Mehmet İlgüy,1 Ph.D.; Nilüfer Ersan,1 Ph.D.; Semanur Dölekoğlu,1 Ph.D.; and Erdoğan Fisßekçioğlu,1 Ph.D.
Measurements of the Foramen Magnum and Mandible in Relation to Sex Using CBCT
ABSTRACT: The purpose of this study was to evaluate pre-existing CBCT images of a large sample of adult females and males to provide
data on foramen magnum and mandibular measures of sexual dimorphism for use as a reference sample in cases of establishing identity in unknown fragmentary skulls. The study group consisted of 161 adult patients. 3D images of the patients were assessed retrospectively. FM measurements were obtained from reformatted axial sections. Six mandibular measurements were taken. According to the results, the study identified four mandibular measurements as final predictors of sex which are as follows: the gonial angle (G-angle) and ramus length (RamusL), gonion–gnathion length (G–G-L) and bigonial breadth (BG-Br). It was found that the cross-validated grouped overall predictive accuracy was 83.2% for FM and mandible measurements. It could correctly identify males in 77.3% and females in 87.4% of the cases. To assess sexual dimorphism, the gonial angle and ramus, gonion–gnathion lengths, and bigonial breadth of the mandible and sagittal diameter of the FM may be used on CBCT images.
KEYWORDS: forensic science, sexual dimorphism, foramen magnum, mandible, cone-beam computed tomography, measurement
Identification of skeletal and decomposing human remains is one of the most difficult skills in forensic medicine. Sex is generally understood to be more accurate the more complete the set of human remains (bones) available; however, some caution should be exercised in stating that it can be 100% accurate. In many cases, some features of some bones may be clearly in one sex distribution range, while in other cases, other features/bones may be indeterminate or more consistent with the opposite sex, due to normal human variation. In explosions, warfare, and other mass disasters, identification may be extremely complicated because of skeletal fragmentation (1,2). There are previous studies in forensic anthropology focusing on several cephalo-facial characteristics (3,4). Dimorphic criteria have been reported using osteometric measurements of the mandible such as gonial angle, the ramus length, minimum ramus breadth, bigonial breadth, and bicondylar breadth (5–7). The length and the height of the head, the circumference of the head, and the circumference of the occipital condyles and the foramen magnum (FM) have been used to determine sex in unknown human remains (1,8–12). Radiography may provide clear images of skeletal features in cases where flesh is present, enabling more accurate bone measurements to be taken for use in determining sex (13). Conebeam computed tomography (CBCT) is a relatively new technique that produces 3-D digital imaging. Studies have suggested
1 Department of Dentomaxillofacial Radiology, Faculty of Dentistry, Yedi€ tepe University, Yeditepe Universitesi Diş Hekimliği Fak€ultesi, Bağdat Cad. No:238 34728 G€ oztepe, Istanbul, Turkey. Received 18 May 2012; and in revised form 11 Jan. 2013; accepted 16 Feb. 2013.
© 2014 American Academy of Forensic Sciences
that CBCT provides accurate and reliable linear measurements for reconstruction and imaging of dental and maxillofacial structures (14–16). A review of the published literature revealed no studies on the relationship between dimensions of the foramen magnum and mandible and sexual dimorphism using CBCT. The aim of this report was to assess the FM and mandible measurements of living persons to set forth a database that may be useful for sex identification. Materials and Methods The study group consisted of 161 adults of European descent (66 males and 95 females) ranging in age from 18 to 85 years. 3D images of the patients taken with an Iluma Cone-Beam CT Scanner (Imtec Corporation, Germany) were assessed retrospectively. All CBCT images were prescribed because of other pathologies (dental implant surgery, tumors, cysts, embedded teeth, etc.) to the patients who applied to our dental faculty for treatment. The research was performed in accordance with the Declaration of Helsinki principles (17). Written consent was also taken from each patient in the study prior to exposure. Patients with a fracture or pathology in the region of the FM and mandible were not included in the study. Digital images were obtained at 120 kVp, 3.8 mA, and a voxel size of 0.2 mm, with an exposure time of 40 sec. 3D reconstructions were created by reformatting the axial cone-beam CT scans on a local workstation using the ILUMA dental imaging software in accordance with the manufacturer’s instructions. The orientation of the images was made for each patient prior to the measurements. For the mandibular measurements, the Frankfort plane (a line passing horizontally from the superior border of external auditory meatus 601
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JOURNAL OF FORENSIC SCIENCES
FIG. 1––The FMDS (sagittal), FMTD (transverse), and FMC (circumference) on the axial view. FIG. 3––BG-Br: Bigonial breadth (distance between two Gonion); BIC-Br: bicondylar breadth (distance between two condylion).
FIG. 2––G-angle: Gonion angle; R-length: Ramus length: The distance between condylion and Gonion; G–G-L: (Gonion–Gnathion length): M-Ramus-Br: minimum ramus breadth.
to the inferior border of the orbital rim) was held parallel to the horizontal plane on the lateral view. For the FM measurements on the sagittal view, a line passing from the anterior to posterior border of the FM was oriented parallel to the horizontal plane. Foramen magnum (FM) measurements (sagittal and transverse lengths and circumferences) were obtained from reformatted axial sections with 5 mm slice thickness (18). The foramen magnum sagittal diameter (FMSD) was recorded as the greatest antero-posterior dimension of the FM, and the foramen magnum transverse diameter (FMTD) was recorded as the greatest width of the FM. The circumference (FMC) was measured after tracing the bony margin of the FM on the CBCT image (Fig. 1). Six mandibular measurements were taken according to Kharoshah (19). Four of them were measured from the lateral reconstruction CBCT 3D image, and they were gonial angle (G-angle), ramus length (Ramus-L), minimum ramus breadth (M-Ramus-Br), and mandibular base length, that is
gonion–gnathion length (G–G-L), as shown in Fig. 2. The other two measurements were carried out from the axial 3D image, and they were bigonial breadth (BG-Br) and bicondylar breadth (BIC-Br) as shown in Fig. 3. A specialist in oral radiology evaluated the images in a darkened quiet room with dual monitors (HP LP2475W, resolution 1920 9 1200). One viewing session was limited to 30 min. Care was taken to ensure that 24 h elapsed between each session. For intra-examiner calibration and to determine the reliability and the reproducibility of the FM and mandibular measurements, the images were evaluated by the same observer for a second time after 2 weeks. Data were analyzed using the Statistical Package for Social Sciences (SPSS) 15.0 software for Windows. During the evaluation of the study data, along with the descriptive statistical methods, parameters with normal distribution for the comparison of quantitative data were evaluated using one-way ANOVA and Tukey’s HSD test, Student’s t-test, and discriminant analysis with “the stepwise feature being used to choose the most discriminatory variables.” Significance level was set at p < 0.05. Results The mean age of the study group was 45.66 16.95 years. The results of intraclass correlation coefficient (ICC) reflect the reliability of the observer with inter-ratings, which explains that the observer gave similar ratings within the repeated observations for each measurement. ICC scores of FM measurements for sagittal, transverse, and circumference were 0.95, 0.99, and 0.98, respectively. ICC scores of mandibular measurements (G-angle, Ramus-L, M-Ramus-Br, G–G-L, BG-Br, and BIC-Br) were 0.98, 0.97, 0.98, 0.84, 0.98, and 0.99, respectively. For all re-measurements, the observer gave similar ratings (p < 0.01). The metric parameters of the FM and mandible according to sex are shown in Tables 1 and 2, respectively. The mean values of foramen magnum measurements and mandibular measurements except the G-angle were greater for males than females (Tables 1 and 2, p < 0.01).
_ILGUY € ET AL.
.
The sample was divided into age groups, and there was no statistically significant difference between age groups and measurements of FM (p > 0.05). For mandibular measurements, no statistically significant correlation was found between age groups and G-angle, Ramus-L, M-Ramus-Br, G–G-L, and TABLE 1––The mean values of measurements of foramen magnum according to gender. FM measurements – mm Sagittal diameter Transverse diameter Circumference
Female Mean SD
Male Mean SD
p
35.62 2.43 31.09 2.36 102.21 6.88
37.79 2.25 32.69 2.29 108.10 7.11
0.001** 0.001** 0.001**
Student t-test. **p < 0.01.
TABLE 2––The metric parameters of mandible regarding to gender.
Mandibular Measurements Gonial angle° Ramus length (mm) Min ramus breadth (mm) Gon–Gnat length (mm) Bigonial breadth (mm) Bicondylar breadth (mm)
Female Mean SD 122.31 54.72 28.09 67.73 94.77 116.23
6.79 4.86 2.83 5.69 5.90 5.50
Male Mean SD 121.14 61.67 29.89 71.86 100.33 120.79
p
6.56 5.47 3.20 4.33 4.99 5.68
0.278 0.001** 0.001** 0.001** 0.001** 0.001**
Student t-test. **p < 0.01.
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MEASUREMENTS OF THE FORAMEN MAGNUM AND MANDIBLE
BG-Br (p > 0.05). Only bicondylar breadth (BIC-Br) was found to be statistically significant between different age groups according to the one-way ANOVA test (p < 0.01). According to the Tukey’s HSD test, bicondylar breadth in the 18–29 years age group was found to be shorter than the age group of >60 years (p < 0.05). In the mandibular measurements of females according to age groups, a statistically significant difference was found between G-angle and BIC-Br (Table 3, p < 0.01, p < 0.05). According to the Tukey’s HSD test, the mean values of G-angle in the 18–29 and 50–59 years age group were found to be higher than the age group of >60 years (p < 0.05). The measurements of BIC-Br in the 18–29 years age group were found to be lower than the age group of >60 years (p < 0.05). In males, there was a statistically significant difference between age groups and the measurements of BIC-Br (Table 4, p < 0.05). The mean value in the 18–29 years age group was found to be lower than the 50–59 years age group. The discriminant analysis test of FM and mandibular measurements showed that the eigenvalue was 0.951(0.208; acceptable when >0.40) and Wilks’ lambda = 0.513 (p < 0.01). According to the results, only the sagittal diameter of FM serves as a final predictor of sex. The study identified four mandibular measurements as final predictors of sex determination which are as follows: the gonial angle (G-angle) and ramus length (Ramus-L), gonion–gnathion length (G–G-L) and bigonial breadth (BG-Br). It was found that the cross-validated grouped overall predictive accuracy was 83.2% for FM and mandible measurements.
TABLE 3––According to age groups the mandibular and FM measurements in females. Age Groups Female Gonial angle° Ramus length (mm) Min ramus breadth (mm) Gon–Gnat length (mm) Bigonial breadth (mm) Bicondylar breadth (mm) Sagittal diameter Transverse diameter Circumference
18–29 Mean SD 125.20 53.70 28.15 69.73 94.00 113.35 36.00 31.32 103.64
8.69 5.10 3.30 4.90 6.18 4.78 3.02 3.01 8.98
30–39 Mean SD 120.72 55.18 27.29 66.46 95.36 116.58 35.59 30.74 100.90
4.90 3.65 2.56 3.99 6.16 6.44 2.61 2.22 6.40
40–49 Mean SD 120.90 55.21 28.24 64.98 93.67 114.05 35.90 30.85 102.35
5.78 4.92 1.40 10.95 4.98 3.61 1.85 2.52 6.43
50–59 Mean SD 124.55 54.33 27.51 67.57 94.73 117.57 35.08 30.97 101.11
>60 Mean SD
6.00 5.06 2.73 3.98 5.81 5.86 1.93 1.72 5.49
118.85 55.57 29.17 68.39 95.77 118.43 35.73 31.37 102.94
5.50 5.29 3.08 4.57 6.34 4.66 2.56 2.45 6.82
p 0.007** 0.743 0.241 0.166 0.823 0.011* 0.750 0.913 0.682
One-way ANOVA test. *p < 0.05; **p < 0.01. TABLE 4––According to age groups the mandibular and FM measurements in males. Age Groups
Male Gonial angle° Ramus length (mm) Min ramus breadth (mm) Gon-Gnat length (mm) Bigonial breadth (mm) Bicondylar breadth (mm) Sagittal diameter Transverse diameter Circumference One-way ANOVA test. *p < 0.05.
18–29 Mean SD 121.34 61.87 29.50 70.20 98.75 117.27 38.95 33.10 109.82
7.71 8.01 3.95 5.40 4.90 6.05 2.82 2.96 8.24
30–39 Mean SD 122.84 59.39 28.47 72.41 101.20 120.34 37.47 33.14 107.92
7.52 3.65 3.38 4.07 6.51 5.05 2.64 2.82 8.74
40–49 Mean SD 119.01 62.03 30.88 74.43 100.74 121.37 37.38 33.61 108.00
8.31 4.43 2.67 4.37 3.39 5.67 0.76 1.23 2.47
50–59 Mean SD 120.48 63.86 31.12 72.12 101.27 123.39 37.76 32.49 109.33
3.83 4.18 2.91 4.02 5.01 5.45 1.63 1.95 6.72
60 Mean SD 121.41 59.90 28.25 71.39 99.47 121.03 36.92 31.35 103.82
7.22 4.89 1.92 3.12 3.97 4.45 2.23 1.11 5.04
F; p 0.444; 1.742; 1.793; 1.283; 0.732; 2.806; 1.584; 1.548; 1.400;
0.777 0.152 0.142 0.287 0.573 0.033* 0.190 0.200 0.245
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TABLE 5––Classification for males and females using stepwise discriminant analysis for FM and mandibula. Predicted Group Sex F M
Cross-validated
95 66
Accuracy
F
M
Correct %
Incorrect %
83 15
12 51
87.4 77.3
12.6 22.7
Cross-validated grouped overall predictive accuracy 83.2%.
It could correctly identify males in 77.3% and females in 87.4% of the cases (Table 5). Discussion Deaths due to warfare and mass disasters may result in fragmentary human remains in various conditions such as burned and decomposed, thus making identification difficult. (20). Craniometric features can be used to aid in identifying an individual from a skull found detached from its skeleton (21). Next to the pelvis, the skull is the most easily sexed portion of the skeleton. The craniofacial structures have the advantage of being composed largely of hard tissue, which is relatively indestructible (22). Attempts at approaching the problem of correctly sexing skeletal materials can be accomplished using either a metric or nonmetric (morphological) assessment (23). CBCT measurements of specific distances on a human dry skull are highly accurate and reproducible (24). For FM Dimensions Murshed et al. (25) reported the mean value of the FMSD (34.6 3.16 mm in females and 37.2 3.43 mm in males) and of the FMTD (29.3 2.19 mm in females and 31.6 2.99 mm in males). According to Uthman et al. (18), FMSD was 32.9 2 mm in females and 34.9 2 mm in males; and FMTD was 27.3 2.2 in females and 29.5 2.5 mm in males. In the present study, the mean value of FMSD was found to be 35.62 2.43 in females and 37.79 2.25 in males, which is in accordance with Murshed’s (25) study. Also FMTD was found to be 31.09 2.36 in females and 32.69 2.29 in males, close to the results reported in Murshed’s (24) study. On the subject of FMC, there seems to be only one study which reports the measurement as 92.6 6.5 mm for females and 99.3 6.2 mm for males (18). The present study reports the mean value of FMC to be 102.2 6.8 for females and 108.1 7.1 for males. These results were lower than the ones recorded in the present study. These differences might be due to the difference between the anatomic and radiographic methods. It was noticeable that the mean values of FMSD, FMTD, and FMC in males were significantly higher than in females among all studies carried out on the FM. Similarly, the values of males were higher than females in the present study (Table 1, p < 0.01). Previous studies have controversial results about the usage of FM measurements for sexual dimorphism (9,18,26). In the present study, the accuracy rate of sex determination from FM measurements was 87.4% in females and 77.3% in males, with an overall accuracy rate of 83.2%. First, only the sagittal diameter of foramen magnum seems as a final predictor of
sex determination, other FM measurements seem not to be valuable for sex dimorphism. This result was not compatible with Utman’s (18) and Uysal’s (26) studies, which may be due to the additional measurements on FM in the studied samples. For Mandibular Dimensions In the present study, mandibular measurements were found to have significantly higher mean values in males except the gonion angle. Kharoshah (19) reported the gonion angle to be one of the measurements which had higher values in males, conflicting with the findings of the present study. Dayal et al. (23) studied the assessment of sex using 120 skulls, using 6 mandibular measurements, and the application of discriminant function analysis and had an average accuracy of 85%. The study concludes that the stepwise feature discriminant analysis could identify the gonial angle and ramus length, gonion–gnathion length and bigonial breadth as final predictors of sex determination with overall predictive accuracy of 83.2% as the best predictor of sex dimorphism. In a previous study, bicondylar breadth, gonial angle, minimum ramus breadth, and ramus length were reported as final predictors of sex determination (19). The current study showed that bicondylar breadth and minimum ramus breadth did not contribute to the sex identification. Patients under 18 years of age were excluded from the study such that skeletal growth or development factors would not confound any differences in the measurements assumed to be due to sex. In general, the overall predictive accuracy of this study is similar to other studies; 83.9% in Egyptian population (19), 82% in South Africans (7), 91% in black South Africans (27), and 84.1% in Japanese skulls (28). In conclusion, to identify sex using CBCT images, the gonial angle and ramus, gonion–gnathion lengths and bigonial breadth of mandible may be used, while only the sagittal diameter of foramen magnum seems to be useful according to the discriminant analysis test. The results gathered from this study may be used as a reference for the cranial measurements of individuals of European descent. Future studies may include larger numbers of participants from various ethnic backgrounds to form a more circumspect data, so that skulls from different populations can be assigned sex more accurately. The FM and mandibular measurements of living persons may serve as a database that may be useful for sex identification. Additional studies on a larger number of cases are needed due to the variation which might be present between different populations which may affect the bone measurements. References 1. G€unay Y, Altink€ok M, Cagdir S, Kirangil B. Sex determination with skull measurements. J Forensic Med 1997;13:13–9. 2. Holland TD. Use of the cranial base in the identification of fire victims. J Forensic Sci 1984;29:1087–93. 3. Iscan MY. Forensic anthropology of sex and body size. Forensic Sci Int 2005;147:107–12. 4. Patil KR, Mody RN. Determination of sex and body by discriminant function analysis and stature by regression analysis: a lateral cephalometric study. Forensic Sci Int 2005;147:175–80. 5. Giles E. Sex determination by discriminant functions, analysis of mandibular shape. J Craniofacial Genet Dev Biol 1996;16:208–17. 6. Iscan MY, Steyn M. Craniometric determination of population affinity in South Africans. Int J Legal Med 1999;112:91–7. 7. Steyn M, Iscan MY. Sexual dimorphism in the crania and mandibles of South African Whites. Forensic Sci Int 1998;98:9–16.
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8. Quatrehomme G, Fronty P, Sapanet M, Grevin G, Bailet P, Olier A. Identification by frontal sinus pattern in forensic anthropology. Forensic Sci Int 1996;83:147–53. 9. G€ unay Y, Altink€ ok MC, C ß agdir S, Sari H. Is foremen magnum size useful for gender determination (in Turkish). Bull Legal Med 1998;3:41–5. 10. Cameriere R, Ferrante L, Mirtella D, Rollo UF, Cingolani M. Frontal sinuses for identification. quality of classifications, possible error and potential corrections. J Forensic Sci 2005;50:1–4. 11. Rogers LT. Determining the sex of human remains through cranial morphology. J Forensic Sci 2005;50:1–7. 12. Gruber P, Henneberg M, Boni T, R€uhli FJ. Variability of human foramen magnum size. Anat Rec (Hoboken) 2009;292:1713–9. 13. Di Vella G, Campobasso CP, Dragone M, Introna F Jr. Skeletal sex determination by scapular measurements. Boll Soc Ital Biol Sper 1994; 70:299–305. 14. Mischkowski RA, Pulsfort R, Ritter L, Neugebauer J, Brochhagen HG, Keeve E, et al. Geometric accuracy of a newly developed cone-beam device for maxillofacial imaging. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007;104:(4) 551–9. 15. Watanabe H, Honda E, Kurabayashi T. Modulation transfer function evaluation of cone beam computed tomography for dental use with the oversampling method. Dentomaxillofac Radiol 2010;39:(1) 28–32. 16. Scarfe WC, Farman AG, Sukovic P. Clinical applications of conebeam computed tomography in dental practice. J Can Dent Assoc 2006;72:(1) 75–80. 17. The Declaration of Helsinki (DoH). http://www.wma.net/en/20activities/ 10ethics/10helsinki/. 18. Uthman AT, Al-Raw NH, Al-Timimi JF. Evaluation of foramen magnum in gender determination using helical CT scanning. Dentomaxillofacial Radiology 2011;000:1–6. 19. Kharoshah MA, Almadani O, Ghaleb SS, Zaki MK, Fattah YA. Sexual dimorphism of the mandible in a modern Egyptian population. J Forensic Leg Med 2010;17:(4) 213–5.
MEASUREMENTS OF THE FORAMEN MAGNUM AND MANDIBLE
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20. Krogman WM, Iscan MY. The human skeleton in forensic medicine, 2nd edn. Springfield, IL: Charles C Thomas Publishing, 1986. 21. Ono I, Ohura T, Narumi E, Kawashima K, Matsuno I, Nakamura S, et al. Analysis of craniofacial bones using three dimensional computed tomography. J Cranio Maxillofacial Surg 1992;20:49–60. 22. Patil KR, Mody RN. Determination of sex by discriminant function analysis. Am J Orthod Dentofacial Orthop 2005;128:157–60. 23. Dayal MR, Spocter MA, Bidmos MA. An assessment of sex using the skull of black South Africans by discriminant function analysis. Homo 2008;59:(3) 209–21. € 24. Kamburoglu K, Kolsuz E, Kurt H, Kilicß C, Ozen T, Paksoy CS. Accuracy of CBCT measurements of a human skull. J Digit Imaging 2011;24: (5) 787–93. 25. Murshed KA, C ßicekcibasi AE, Tuncer I. Morphometric evaluation of the foramen magnum and variations in its shape. a study on computerized tomographic images of normal adults. Turk J Med Sci 2003;33:301–6. 26. Uysal S, Gokharman D, Kacar M, Tuncbilek I, Kosa U. Estimation of sex by 3D CT measurements of the foramen magnum. J Forensic Sci 2005;50:1310–4. 27. Kieser JA, Groeneveld HT. Multivariate sexing of the human viserocranium. J Forensic Odontostomatol 1986;4:41–6. 28. Iscan MY, Yoshino M, Kato S. Sexual dimorphism in modem Japanese crania. Am J Hum Biol 1995;7:459–64. Additional information and reprint requests: _ uy, Ph.D. Dilhan Ilg€ € Yeditepe Universitesi Disß Hekimligi Fak€ultesi Bagdat cad. No 238 34728 G€oztepe-Istanbul Turkiye E-mail: [email protected]
PAPER ANTHROPOLOGY
Dilhan İlgüy,1 Ph.D.; Mehmet İlgüy,1 Ph.D.; Nilüfer Ersan,1 Ph.D.; Semanur Dölekoğlu,1 Ph.D.; and Erdoğan Fisßekçioğlu,1 Ph.D.
Measurements of the Foramen Magnum and Mandible in Relation to Sex Using CBCT
ABSTRACT: The purpose of this study was to evaluate pre-existing CBCT images of a large sample of adult females and males to provide
data on foramen magnum and mandibular measures of sexual dimorphism for use as a reference sample in cases of establishing identity in unknown fragmentary skulls. The study group consisted of 161 adult patients. 3D images of the patients were assessed retrospectively. FM measurements were obtained from reformatted axial sections. Six mandibular measurements were taken. According to the results, the study identified four mandibular measurements as final predictors of sex which are as follows: the gonial angle (G-angle) and ramus length (RamusL), gonion–gnathion length (G–G-L) and bigonial breadth (BG-Br). It was found that the cross-validated grouped overall predictive accuracy was 83.2% for FM and mandible measurements. It could correctly identify males in 77.3% and females in 87.4% of the cases. To assess sexual dimorphism, the gonial angle and ramus, gonion–gnathion lengths, and bigonial breadth of the mandible and sagittal diameter of the FM may be used on CBCT images.
KEYWORDS: forensic science, sexual dimorphism, foramen magnum, mandible, cone-beam computed tomography, measurement
Identification of skeletal and decomposing human remains is one of the most difficult skills in forensic medicine. Sex is generally understood to be more accurate the more complete the set of human remains (bones) available; however, some caution should be exercised in stating that it can be 100% accurate. In many cases, some features of some bones may be clearly in one sex distribution range, while in other cases, other features/bones may be indeterminate or more consistent with the opposite sex, due to normal human variation. In explosions, warfare, and other mass disasters, identification may be extremely complicated because of skeletal fragmentation (1,2). There are previous studies in forensic anthropology focusing on several cephalo-facial characteristics (3,4). Dimorphic criteria have been reported using osteometric measurements of the mandible such as gonial angle, the ramus length, minimum ramus breadth, bigonial breadth, and bicondylar breadth (5–7). The length and the height of the head, the circumference of the head, and the circumference of the occipital condyles and the foramen magnum (FM) have been used to determine sex in unknown human remains (1,8–12). Radiography may provide clear images of skeletal features in cases where flesh is present, enabling more accurate bone measurements to be taken for use in determining sex (13). Conebeam computed tomography (CBCT) is a relatively new technique that produces 3-D digital imaging. Studies have suggested
1 Department of Dentomaxillofacial Radiology, Faculty of Dentistry, Yedi€ tepe University, Yeditepe Universitesi Diş Hekimliği Fak€ultesi, Bağdat Cad. No:238 34728 G€ oztepe, Istanbul, Turkey. Received 18 May 2012; and in revised form 11 Jan. 2013; accepted 16 Feb. 2013.
© 2014 American Academy of Forensic Sciences
that CBCT provides accurate and reliable linear measurements for reconstruction and imaging of dental and maxillofacial structures (14–16). A review of the published literature revealed no studies on the relationship between dimensions of the foramen magnum and mandible and sexual dimorphism using CBCT. The aim of this report was to assess the FM and mandible measurements of living persons to set forth a database that may be useful for sex identification. Materials and Methods The study group consisted of 161 adults of European descent (66 males and 95 females) ranging in age from 18 to 85 years. 3D images of the patients taken with an Iluma Cone-Beam CT Scanner (Imtec Corporation, Germany) were assessed retrospectively. All CBCT images were prescribed because of other pathologies (dental implant surgery, tumors, cysts, embedded teeth, etc.) to the patients who applied to our dental faculty for treatment. The research was performed in accordance with the Declaration of Helsinki principles (17). Written consent was also taken from each patient in the study prior to exposure. Patients with a fracture or pathology in the region of the FM and mandible were not included in the study. Digital images were obtained at 120 kVp, 3.8 mA, and a voxel size of 0.2 mm, with an exposure time of 40 sec. 3D reconstructions were created by reformatting the axial cone-beam CT scans on a local workstation using the ILUMA dental imaging software in accordance with the manufacturer’s instructions. The orientation of the images was made for each patient prior to the measurements. For the mandibular measurements, the Frankfort plane (a line passing horizontally from the superior border of external auditory meatus 601
602
JOURNAL OF FORENSIC SCIENCES
FIG. 1––The FMDS (sagittal), FMTD (transverse), and FMC (circumference) on the axial view. FIG. 3––BG-Br: Bigonial breadth (distance between two Gonion); BIC-Br: bicondylar breadth (distance between two condylion).
FIG. 2––G-angle: Gonion angle; R-length: Ramus length: The distance between condylion and Gonion; G–G-L: (Gonion–Gnathion length): M-Ramus-Br: minimum ramus breadth.
to the inferior border of the orbital rim) was held parallel to the horizontal plane on the lateral view. For the FM measurements on the sagittal view, a line passing from the anterior to posterior border of the FM was oriented parallel to the horizontal plane. Foramen magnum (FM) measurements (sagittal and transverse lengths and circumferences) were obtained from reformatted axial sections with 5 mm slice thickness (18). The foramen magnum sagittal diameter (FMSD) was recorded as the greatest antero-posterior dimension of the FM, and the foramen magnum transverse diameter (FMTD) was recorded as the greatest width of the FM. The circumference (FMC) was measured after tracing the bony margin of the FM on the CBCT image (Fig. 1). Six mandibular measurements were taken according to Kharoshah (19). Four of them were measured from the lateral reconstruction CBCT 3D image, and they were gonial angle (G-angle), ramus length (Ramus-L), minimum ramus breadth (M-Ramus-Br), and mandibular base length, that is
gonion–gnathion length (G–G-L), as shown in Fig. 2. The other two measurements were carried out from the axial 3D image, and they were bigonial breadth (BG-Br) and bicondylar breadth (BIC-Br) as shown in Fig. 3. A specialist in oral radiology evaluated the images in a darkened quiet room with dual monitors (HP LP2475W, resolution 1920 9 1200). One viewing session was limited to 30 min. Care was taken to ensure that 24 h elapsed between each session. For intra-examiner calibration and to determine the reliability and the reproducibility of the FM and mandibular measurements, the images were evaluated by the same observer for a second time after 2 weeks. Data were analyzed using the Statistical Package for Social Sciences (SPSS) 15.0 software for Windows. During the evaluation of the study data, along with the descriptive statistical methods, parameters with normal distribution for the comparison of quantitative data were evaluated using one-way ANOVA and Tukey’s HSD test, Student’s t-test, and discriminant analysis with “the stepwise feature being used to choose the most discriminatory variables.” Significance level was set at p < 0.05. Results The mean age of the study group was 45.66 16.95 years. The results of intraclass correlation coefficient (ICC) reflect the reliability of the observer with inter-ratings, which explains that the observer gave similar ratings within the repeated observations for each measurement. ICC scores of FM measurements for sagittal, transverse, and circumference were 0.95, 0.99, and 0.98, respectively. ICC scores of mandibular measurements (G-angle, Ramus-L, M-Ramus-Br, G–G-L, BG-Br, and BIC-Br) were 0.98, 0.97, 0.98, 0.84, 0.98, and 0.99, respectively. For all re-measurements, the observer gave similar ratings (p < 0.01). The metric parameters of the FM and mandible according to sex are shown in Tables 1 and 2, respectively. The mean values of foramen magnum measurements and mandibular measurements except the G-angle were greater for males than females (Tables 1 and 2, p < 0.01).
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The sample was divided into age groups, and there was no statistically significant difference between age groups and measurements of FM (p > 0.05). For mandibular measurements, no statistically significant correlation was found between age groups and G-angle, Ramus-L, M-Ramus-Br, G–G-L, and TABLE 1––The mean values of measurements of foramen magnum according to gender. FM measurements – mm Sagittal diameter Transverse diameter Circumference
Female Mean SD
Male Mean SD
p
35.62 2.43 31.09 2.36 102.21 6.88
37.79 2.25 32.69 2.29 108.10 7.11
0.001** 0.001** 0.001**
Student t-test. **p < 0.01.
TABLE 2––The metric parameters of mandible regarding to gender.
Mandibular Measurements Gonial angle° Ramus length (mm) Min ramus breadth (mm) Gon–Gnat length (mm) Bigonial breadth (mm) Bicondylar breadth (mm)
Female Mean SD 122.31 54.72 28.09 67.73 94.77 116.23
6.79 4.86 2.83 5.69 5.90 5.50
Male Mean SD 121.14 61.67 29.89 71.86 100.33 120.79
p
6.56 5.47 3.20 4.33 4.99 5.68
0.278 0.001** 0.001** 0.001** 0.001** 0.001**
Student t-test. **p < 0.01.
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BG-Br (p > 0.05). Only bicondylar breadth (BIC-Br) was found to be statistically significant between different age groups according to the one-way ANOVA test (p < 0.01). According to the Tukey’s HSD test, bicondylar breadth in the 18–29 years age group was found to be shorter than the age group of >60 years (p < 0.05). In the mandibular measurements of females according to age groups, a statistically significant difference was found between G-angle and BIC-Br (Table 3, p < 0.01, p < 0.05). According to the Tukey’s HSD test, the mean values of G-angle in the 18–29 and 50–59 years age group were found to be higher than the age group of >60 years (p < 0.05). The measurements of BIC-Br in the 18–29 years age group were found to be lower than the age group of >60 years (p < 0.05). In males, there was a statistically significant difference between age groups and the measurements of BIC-Br (Table 4, p < 0.05). The mean value in the 18–29 years age group was found to be lower than the 50–59 years age group. The discriminant analysis test of FM and mandibular measurements showed that the eigenvalue was 0.951(0.208; acceptable when >0.40) and Wilks’ lambda = 0.513 (p < 0.01). According to the results, only the sagittal diameter of FM serves as a final predictor of sex. The study identified four mandibular measurements as final predictors of sex determination which are as follows: the gonial angle (G-angle) and ramus length (Ramus-L), gonion–gnathion length (G–G-L) and bigonial breadth (BG-Br). It was found that the cross-validated grouped overall predictive accuracy was 83.2% for FM and mandible measurements.
TABLE 3––According to age groups the mandibular and FM measurements in females. Age Groups Female Gonial angle° Ramus length (mm) Min ramus breadth (mm) Gon–Gnat length (mm) Bigonial breadth (mm) Bicondylar breadth (mm) Sagittal diameter Transverse diameter Circumference
18–29 Mean SD 125.20 53.70 28.15 69.73 94.00 113.35 36.00 31.32 103.64
8.69 5.10 3.30 4.90 6.18 4.78 3.02 3.01 8.98
30–39 Mean SD 120.72 55.18 27.29 66.46 95.36 116.58 35.59 30.74 100.90
4.90 3.65 2.56 3.99 6.16 6.44 2.61 2.22 6.40
40–49 Mean SD 120.90 55.21 28.24 64.98 93.67 114.05 35.90 30.85 102.35
5.78 4.92 1.40 10.95 4.98 3.61 1.85 2.52 6.43
50–59 Mean SD 124.55 54.33 27.51 67.57 94.73 117.57 35.08 30.97 101.11
>60 Mean SD
6.00 5.06 2.73 3.98 5.81 5.86 1.93 1.72 5.49
118.85 55.57 29.17 68.39 95.77 118.43 35.73 31.37 102.94
5.50 5.29 3.08 4.57 6.34 4.66 2.56 2.45 6.82
p 0.007** 0.743 0.241 0.166 0.823 0.011* 0.750 0.913 0.682
One-way ANOVA test. *p < 0.05; **p < 0.01. TABLE 4––According to age groups the mandibular and FM measurements in males. Age Groups
Male Gonial angle° Ramus length (mm) Min ramus breadth (mm) Gon-Gnat length (mm) Bigonial breadth (mm) Bicondylar breadth (mm) Sagittal diameter Transverse diameter Circumference One-way ANOVA test. *p < 0.05.
18–29 Mean SD 121.34 61.87 29.50 70.20 98.75 117.27 38.95 33.10 109.82
7.71 8.01 3.95 5.40 4.90 6.05 2.82 2.96 8.24
30–39 Mean SD 122.84 59.39 28.47 72.41 101.20 120.34 37.47 33.14 107.92
7.52 3.65 3.38 4.07 6.51 5.05 2.64 2.82 8.74
40–49 Mean SD 119.01 62.03 30.88 74.43 100.74 121.37 37.38 33.61 108.00
8.31 4.43 2.67 4.37 3.39 5.67 0.76 1.23 2.47
50–59 Mean SD 120.48 63.86 31.12 72.12 101.27 123.39 37.76 32.49 109.33
3.83 4.18 2.91 4.02 5.01 5.45 1.63 1.95 6.72
60 Mean SD 121.41 59.90 28.25 71.39 99.47 121.03 36.92 31.35 103.82
7.22 4.89 1.92 3.12 3.97 4.45 2.23 1.11 5.04
F; p 0.444; 1.742; 1.793; 1.283; 0.732; 2.806; 1.584; 1.548; 1.400;
0.777 0.152 0.142 0.287 0.573 0.033* 0.190 0.200 0.245
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TABLE 5––Classification for males and females using stepwise discriminant analysis for FM and mandibula. Predicted Group Sex F M
Cross-validated
95 66
Accuracy
F
M
Correct %
Incorrect %
83 15
12 51
87.4 77.3
12.6 22.7
Cross-validated grouped overall predictive accuracy 83.2%.
It could correctly identify males in 77.3% and females in 87.4% of the cases (Table 5). Discussion Deaths due to warfare and mass disasters may result in fragmentary human remains in various conditions such as burned and decomposed, thus making identification difficult. (20). Craniometric features can be used to aid in identifying an individual from a skull found detached from its skeleton (21). Next to the pelvis, the skull is the most easily sexed portion of the skeleton. The craniofacial structures have the advantage of being composed largely of hard tissue, which is relatively indestructible (22). Attempts at approaching the problem of correctly sexing skeletal materials can be accomplished using either a metric or nonmetric (morphological) assessment (23). CBCT measurements of specific distances on a human dry skull are highly accurate and reproducible (24). For FM Dimensions Murshed et al. (25) reported the mean value of the FMSD (34.6 3.16 mm in females and 37.2 3.43 mm in males) and of the FMTD (29.3 2.19 mm in females and 31.6 2.99 mm in males). According to Uthman et al. (18), FMSD was 32.9 2 mm in females and 34.9 2 mm in males; and FMTD was 27.3 2.2 in females and 29.5 2.5 mm in males. In the present study, the mean value of FMSD was found to be 35.62 2.43 in females and 37.79 2.25 in males, which is in accordance with Murshed’s (25) study. Also FMTD was found to be 31.09 2.36 in females and 32.69 2.29 in males, close to the results reported in Murshed’s (24) study. On the subject of FMC, there seems to be only one study which reports the measurement as 92.6 6.5 mm for females and 99.3 6.2 mm for males (18). The present study reports the mean value of FMC to be 102.2 6.8 for females and 108.1 7.1 for males. These results were lower than the ones recorded in the present study. These differences might be due to the difference between the anatomic and radiographic methods. It was noticeable that the mean values of FMSD, FMTD, and FMC in males were significantly higher than in females among all studies carried out on the FM. Similarly, the values of males were higher than females in the present study (Table 1, p < 0.01). Previous studies have controversial results about the usage of FM measurements for sexual dimorphism (9,18,26). In the present study, the accuracy rate of sex determination from FM measurements was 87.4% in females and 77.3% in males, with an overall accuracy rate of 83.2%. First, only the sagittal diameter of foramen magnum seems as a final predictor of
sex determination, other FM measurements seem not to be valuable for sex dimorphism. This result was not compatible with Utman’s (18) and Uysal’s (26) studies, which may be due to the additional measurements on FM in the studied samples. For Mandibular Dimensions In the present study, mandibular measurements were found to have significantly higher mean values in males except the gonion angle. Kharoshah (19) reported the gonion angle to be one of the measurements which had higher values in males, conflicting with the findings of the present study. Dayal et al. (23) studied the assessment of sex using 120 skulls, using 6 mandibular measurements, and the application of discriminant function analysis and had an average accuracy of 85%. The study concludes that the stepwise feature discriminant analysis could identify the gonial angle and ramus length, gonion–gnathion length and bigonial breadth as final predictors of sex determination with overall predictive accuracy of 83.2% as the best predictor of sex dimorphism. In a previous study, bicondylar breadth, gonial angle, minimum ramus breadth, and ramus length were reported as final predictors of sex determination (19). The current study showed that bicondylar breadth and minimum ramus breadth did not contribute to the sex identification. Patients under 18 years of age were excluded from the study such that skeletal growth or development factors would not confound any differences in the measurements assumed to be due to sex. In general, the overall predictive accuracy of this study is similar to other studies; 83.9% in Egyptian population (19), 82% in South Africans (7), 91% in black South Africans (27), and 84.1% in Japanese skulls (28). In conclusion, to identify sex using CBCT images, the gonial angle and ramus, gonion–gnathion lengths and bigonial breadth of mandible may be used, while only the sagittal diameter of foramen magnum seems to be useful according to the discriminant analysis test. The results gathered from this study may be used as a reference for the cranial measurements of individuals of European descent. Future studies may include larger numbers of participants from various ethnic backgrounds to form a more circumspect data, so that skulls from different populations can be assigned sex more accurately. The FM and mandibular measurements of living persons may serve as a database that may be useful for sex identification. Additional studies on a larger number of cases are needed due to the variation which might be present between different populations which may affect the bone measurements. References 1. G€unay Y, Altink€ok M, Cagdir S, Kirangil B. Sex determination with skull measurements. J Forensic Med 1997;13:13–9. 2. Holland TD. Use of the cranial base in the identification of fire victims. J Forensic Sci 1984;29:1087–93. 3. Iscan MY. Forensic anthropology of sex and body size. Forensic Sci Int 2005;147:107–12. 4. Patil KR, Mody RN. Determination of sex and body by discriminant function analysis and stature by regression analysis: a lateral cephalometric study. Forensic Sci Int 2005;147:175–80. 5. Giles E. Sex determination by discriminant functions, analysis of mandibular shape. J Craniofacial Genet Dev Biol 1996;16:208–17. 6. Iscan MY, Steyn M. Craniometric determination of population affinity in South Africans. Int J Legal Med 1999;112:91–7. 7. Steyn M, Iscan MY. Sexual dimorphism in the crania and mandibles of South African Whites. Forensic Sci Int 1998;98:9–16.
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20. Krogman WM, Iscan MY. The human skeleton in forensic medicine, 2nd edn. Springfield, IL: Charles C Thomas Publishing, 1986. 21. Ono I, Ohura T, Narumi E, Kawashima K, Matsuno I, Nakamura S, et al. Analysis of craniofacial bones using three dimensional computed tomography. J Cranio Maxillofacial Surg 1992;20:49–60. 22. Patil KR, Mody RN. Determination of sex by discriminant function analysis. Am J Orthod Dentofacial Orthop 2005;128:157–60. 23. Dayal MR, Spocter MA, Bidmos MA. An assessment of sex using the skull of black South Africans by discriminant function analysis. Homo 2008;59:(3) 209–21. € 24. Kamburoglu K, Kolsuz E, Kurt H, Kilicß C, Ozen T, Paksoy CS. Accuracy of CBCT measurements of a human skull. J Digit Imaging 2011;24: (5) 787–93. 25. Murshed KA, C ßicekcibasi AE, Tuncer I. Morphometric evaluation of the foramen magnum and variations in its shape. a study on computerized tomographic images of normal adults. Turk J Med Sci 2003;33:301–6. 26. Uysal S, Gokharman D, Kacar M, Tuncbilek I, Kosa U. Estimation of sex by 3D CT measurements of the foramen magnum. J Forensic Sci 2005;50:1310–4. 27. Kieser JA, Groeneveld HT. Multivariate sexing of the human viserocranium. J Forensic Odontostomatol 1986;4:41–6. 28. Iscan MY, Yoshino M, Kato S. Sexual dimorphism in modem Japanese crania. Am J Hum Biol 1995;7:459–64. Additional information and reprint requests: _ uy, Ph.D. Dilhan Ilg€ € Yeditepe Universitesi Disß Hekimligi Fak€ultesi Bagdat cad. No 238 34728 G€oztepe-Istanbul Turkiye E-mail: [email protected]
