Sex identification in a sample of Egyptian population using Cone beam computed tomography of maxillary sinus predictors

Sex identification in a sample of Egyptian population using Cone beam computed tomography of maxillary sinus predictors.

Abstract:
Aim: to investigate the possibility of sex identification from radiographic maxillary sinus measurements among a sample of Egyptian population. Methodology: The present study comprised of 100 living non-pathological Egyptians of 200 maxillary sinuses bilaterally 50 males and 50 females aged 20-70 years. All the participants were scanned with CBCT for various purposes. Maxillary sinus width, depth, bizygomatic diatance and intermaxillary distance were measured from axial images and height was measured from coronal images. All measures were obtained between the widest points of the all of the sinuses, and volumes of maxillary sinuses on both sides were calculated using the following equation: (Width × Depth × Height × 0.5). Results: Non-statistically significant difference was revealed between the right and left maxillary sinuses. All measurement of males showed statistically significantly higher mean values than females. The significant predictors for gender were: sinus volume and inter-maxillary distance. The discriminate functions at group centroids (Group means) were 0.620 for males and -0.620 for females. Conclusion: CBCT scan can precisely locate and measure the maxillary sinus dimentions. Thus, It can be used as a supplementary tool for sex determination in forensic anthropology, especially in cases where other traditional methods are not conclusive. From this study it was concluded that the dimensions and volume of the maxillary sinuses of male was found to be larger than those of female.

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Aim: to investigate the possibility of sex identification from radiographic maxillary sinus measurements among a sample of Egyptian population.

Introduction:
Post-mortem identification, a forensic procedure, is troublesome to perform. Forensic odontology helps individual identification through those forms from claiming similar dental identification, post mortem profiling from dental records and examination such as dental documents, assumes a paramount part in the identification about corpses. Next to the pelvis, the skull is the most reliable sex indicator, yet the determination of sex from the skull is not dependable until following puberty. Skull obliges the most frequent sexing in medico legal situations. It seems to be the principle dependable bone exhibiting sexually dimorphic traits, because skull has a high resistance to adverse environmental conditions over time, resulting in the greater stability of dimorphic features as compared to other skeletal bony pieces. (Uthman et al 2011, Amin M, Hassan E 2012, Ekizoglu et al 2014, Jehan et al 2014, Sharma et al 2014, Kanthem et al 2015 and Tambawala et al 2015)
The maxillary sinuses appear at the end of the second embryonic month, and they scope their mature sizes at the age of about 20 years, when the permanent teeth fully develop. They tend to settle then after the second decade of life and the radiographic pictures may give adequate measurements of maxillary sinuses for use in morphometric forensic analysis that cannot be approached by other means. (Amin M, Hassan E 2012, Masri et al 2013, Kanthem et al 2015, Tambawala et al 2015, Paknahad et al 2017)
Sexual dimorphism refers to the systemic distinction in the structure (either in shape or size) between individuals of different sexes in the same species. Maxillary Sexual dimorphism is one of its integral aspects as it has been reported that maxillary sinuses remain sound despite the skull and other bones may be badly deformed in victims who are incinerated thus narrowing down the diagnosis toward a correct possibility. Maxillary sinuses of different species are referred to on show sexual dimorphism. (Kanthem et al 2015, Tambawala et al 2015, Paknahad et al 2017)
Forensic anthropology have used different radiographic techniques to assess paranasal dimensions for sex identification of an individual including measurements on dry skulls, conventional radiography, computed tomography (CT), and cone-beam computed tomography (CBCT). The evolution of Cone-Beam Computed (CBCT) technology in the clinical management of patients is gaining importance in some forensic contexts due to its fast scan time, relatively low cost, beam limitation and improved metric accuracy with isotropic voxel resolutions and simplicity, thus, allowing age estimation and person identification. It gives three dimensional data of an entity within an object that can be studied in an integrated interactive manner. The multiplanar sectioning of the reconstructed data set allows unlimited virtual dissections of the specimen without further physical harm. (, Sarment DP and Christensen AM 2014, Beaini et al 2015 Saccucci et al 2015, Tambawala et al 2015, Paknahad et al 2017, Asif et al 2018)
Methodology:
The present study comprised of 100 living non-pathological Egyptians of 200 maxillary sinuses bilaterally 50 males and 50 females aged 20-70 years. All the participants were scanned with CBCT for various purposes using a Promax® 3DMid CBCT device (PlanmecaOy, Helsinki, Finland).

The CBCT measurements were gained using “PlanmecaRomexis viewer 3.5.1.R” software with the distance measurement tool. The measurements were done on mulitiplanar coronal and axial images (Figures). All the CBCT measurements were done twice at two different sessions and the average of the two measurements was considered the final one.

Coronal and axial images were used for the radiographic evaluation of the inferior and superior walls of maxillary sinus and to observe the anterior and posterior limit of the sinus. Width, depth, bizygomatic diatance and intermaxillary distance were measured from axial images; height was measured from coronal images. All measures were taken between the widest points of the all of the sinuses, and volumes of maxillary sinuses on both sides were calculated using the following equation: (Width × Depth × Height × 0.5).
Image analysis
The width the optimal axial cut showing both lateral and medial walls clearly was obtained by scrolling through the axial slices and the longest distance perpendicular between both walls was representing it.
The depth the optimal axial cut showing medial wall of the sinus clearly was obtained by scrolling through the axial slices and the longest distance from the most anterior point to the most posterior point of the medial wall was representing it.

The height The optimal coronal cut showing both most superior and inferior walls clearly was obtained by scrolling through the coronal slices and the longest distance from the lowest point of the sinus floor to the highest point of the sinus roof was representing it.

The Bizygomatic distance The optimal axial cut showing most prominent points of the right & left zygomatic arches clearly was obtained by scrolling through the axial slices and the maximum distance between the most prominent points of the right & left zygomatic arches was representing it.

The Intermaxillary distance The optimal axial cut showing medial walls of the sinus clearly was obtained by scrolling through the axial slices and the maximum distance between medial walls of right & left maxillary air sinuses was representing it.

Two independent well trained radiologists with experience more than 10 years made all the CBCT measurements after appropriate training and working on the software used in this study (Planmeca Romexis viewer 3.5.1.R).

Statistical analysis
Data were presented as mean, standard deviation (SD, median, minimum, maximum and 95% Confidence Interval (95% CI) values. Paired t-test was used to compare between right and left side measurements. Student’s t-test was used to compare between males and females. Cronbach’s alpha reliability coefficient and Intra-class Correlation Coefficient (ICC) were used to determine inter-observer agreement.

Stepwise discriminant analysis was conducted to predict gender (Male or Female) from the different maxillary measurements. Stepwise statistics reveals the significant predictors which are used to determine the discriminate function. Then group centroids (group means) are calculated, they represent the determinant points for discrimination between males and females. Finally, classification table represents the percentage of accurately classified cases according to the discriminate function.

The significance level was set at P ? 0.05. Statistical analysis was performed with IBM® SPSS® Statistics Version 20 for Windows.

Results
Descriptive statistics
The present study was conducted on 100 subjects; 50 males (50.0%) and 50 females (50.0%). Descriptive statistics of the present study are presented in Table (1). Comparisons between right and left sides revealed non-statistically significant difference between the two sides, so the mean of the two sides was used in further statistical analysis.

Table 1. Descriptive statistics of the different maxillary measurements
Gender Measurement Mean SD Median Minimum Maximum 95% CI
Lower bound Upper bound
Male Sinus width (mm) 24.6 3.8 25.0 14.8 33.4 23.5 25.6
Sinus depth (mm) 33.7 3.4 33.5 26.2 41.5 32.7 34.6
Sinus height (mm) 35.9 5.4 35.6 24.8 51.6 34.4 37.5
Sinus volume (cc) 30.6 10.0 31.0 10.8 57.9 27.7 33.4
Inter-maxillary distance (mm) 35.0 3.3 35.6 26.4 40.8 34.1 36.0
Bi-zygomatic distance (mm) 93.5 7.2 93.6 80.1 110.7 91.4 95.5
Female Sinus width (mm) 22.3 3.7 22.3 15.2 31.2 21.3 23.4
Sinus depth (mm) 31.4 3.5 32.1 22.4 37.7 30.4 32.4
Sinus height (mm) 31.4 4.2 31.7 22.4 45.1 30.2 32.6
Sinus volume (cc) 22.7 7.4 22.2 9.3 35.8 20.7 24.8
Inter-maxillary distance (mm) 32.7 3.2 32.8 24.4 39.6 31.8 33.6
Bi-zygomatic distance (mm) 88.7 6.3 89.9 71.2 100.2 86.9 90.5
Inter-observer agreement
There was very good inter-observer agreement regarding all measures with Cronbach’s alpha values ranging from 0.956 to 0.990.

Comparison between males and females
All measurement of males showed statistically significantly higher mean values than females.
Table 3. Mean, standard deviation (SD) values and results of Student’s t-test for comparison between males and females
Measurement Males (n=50) Females (n=50) P-value
Mean SD Mean SD Sinus width 24.6 3.8 22.3 3.7 0.004*
Sinus depth 33.7 3.4 31.4 3.5 0.002*
Sinus height 35.9 5.4 31.4 4.2 <0.001*
Sinus volume 30.6 10.0 22.7 7.4 <0.001*
Inter-maxillary distance 35.0 3.3 32.7 3.2 <0.001*
Bi-zygomatic distance 93.5 7.2 88.7 6.3 0.001*
*: Significant at P ? 0.05
Gender estimation
A discriminant analysis was conducted to predict gender (Male or Female). The significant predictors for gender were: sinus volume and inter-maxillary distance.

The discriminate function is:
D = 0.093 sinus volume + 0.218 Inter-maxillary distance – 9.848
The discriminate functions at group centroids (Group means) were 0.620 for males and -0.620 for females.

Classification results revealed that 66.0% of the males were correctly classified while 74.0% of the females were correctly classified according to the prediction equation. Hence, the overall correct classification was 70.0%.
Discussion:
The skull is the vast majority effectively sexed part of the skeleton. The craniofacial structures have the benefit of being composed largely of hard tissue, which is relatively indestructible. (Tambawala et al 2015)
Bones of preadolescent individuals are not effective for sex determination because the secondary sexual characteristics don’t appear until the bones are remodeled under the influence of estrogen and androgen at puberty. The reliability of sex determination from maxillary size dimensions is not feasible until the maxillary sinus reaches its full size after puberty. To overcome this problem, in this study, samples below the age of 20 were excluded. Paknahad et al 2017
.

CBCT is a recently introduced an effective and noninvasive diagnostic imaging modality in clinical dentistry because of its limited radiation exposure and the ability of providing highly accurate life size images. Thus, ensuring their increasing accessibility in cases demanding personal identification as a tool for sex determination in mass disasters or when badly decomposed and incinerated bodies are available. CBCT could thus prove advantageous and serve as an accessible alternative to CT in many cases of forensics. Image enhancing softwares allow the 3-dimensional reconstruction of the CBCT images. (Tambawala et al 2015, Asif et al 2018)
Due to the complex anatomic structure of maxillary sinuses, CBCT imaging has provided an essential adjunctive radiographic technique for maxillary sinus assessment. Therefore, in this study, we chose CBCT for evaluating maxillary sinus dimensions. Paknahad et al 2017
In this study, the measurements were done by two radiologists. There was very good inter-observer agreement regarding all measures with Cronbach’s alpha values ranging from 0.956 to 0.990.One of the limitations of this study was that some selection bias might have occurred by the subjective selection of the slice by each reader. However, the reader’s choice of the slice should have been almost identical to give such a good agreement in most of the measurements.
In This study, Comparisons between right and left sides revealed non-statistically significant difference between the two sides, so the mean of the two sides was used in further statistical analysis.
Against our results, Amin and Hassan E 2012 reported that the measurements of the right maxillary sinus are larger than those of the left sinus in females, and these results were accepted in Turkey by Teke et al. 2007 and confirmed by Uthman et al 2011 and Amusa et al 2011
Supporting our results, Ekizoglu et al 2014 found that the comparison of values of right and left maxillary sinus measurements in both males and females did not show a significant difference (for all variables P ; 0.05).
It has been declared in previous studies that the maxillary sinuses are significantly larger in males than in females in most maxillary sinus measurements, mainly due to the higher and wider maxillary sinuses of males than females. First, males need to have correspondingly bigger lungs to help their relatively more massive muscles and body organs. Second, the males need a larger airway, which begins with the nose and nasopharynx. Thus, physiological changes in nasal cavity size and shape occur as a direct result of respiration-related needs. As the rest of the nasomaxillary complex is occupied by the maxillary sinus, its size is also increased. (Sharma et al 2014, Tambawala et al 2015)
The traditional measurements that are used for morphometric analyses of maxillary sinus are anteroposterior (AP), transverse (T), and cephalocaudal (CC) diameters, and the volume of maxillary sinus which is obtained by means of these parameters volume = (AP × T × CC) × 0.5). Because of complex anatomical characteristics, it must be suggested that the simple measurements, particularly the calculation of volume, are inaccurate and prone to error. (Sahlstrand-Johnson et al 2011, Ekizoglu et al 2014, Möhlhenrich et al 2015)
Following our results the mean sinus width for females was 24.6mm, 33.7 for sinus depth, the mean sinus height for males was 35.9 and the mean volume was 30.6cc. While in females the mean sinus width was 22.3mm, sinus depth 31.4mm, the mean sinus height was 31.4mm and the mean volume was 22.7cc
In consistence with our results, Gray’s Anatomy described the overall measurements of the maxillary sinus to be as 32 mm in anterior-posterior diameter, 25 mm in mediolateral diameter (transverse), and 35 mm in superior-inferior diameter (cephalo-caudal). (Williams et al 1995 and Amin and Hassan 2012)
Sahlstrand-Johnson et al in 2011 assessed the dimensions of 120 maxillary and frontal sinuses using head CT images. They reported that the mean value of the maxillary sinus volume was 15.7 ? 5.3 cm3 and significantly larger in males than in females with no statistically significant correlation between the volume of maxillary sinuses with age or side.

Approximating our results, Baweja et al 2013 assessed the average sinus depth to be 34.1 _ 5.1 mm for male and 33_ 5.6mm for female. The average sinus AP reported by Baweja et al 2013 was 37.3 _ 8.0 mm for male and 36.9 _ 7.4 mm for female.

Gender determination is really important for identification. In this study all measurement of males showed statistically significantly higher mean values than females.

Amin and Hassan 2012 estimated that the transverse, cephalo-caudal, and size of the maxillary sinuses of the female were smaller than those of men. cephalo-caudal and size of the left maxillary sinus showed significant differences between males and females.

Fernandes 2004 also confirmed that the maxillary sinuses are larger in males than in females in Europe and these results resembling ours. But in Zululand, the maxillary sinuses are narrower in males than in females. This might a chance to be demonstrated as the maxillary sinus has a racial role or due to the higher ages of the specimens. The study accounted for no significant difference between males and females for the maxillary sinus width. On the other hand, maxillary sinus depth, height and volume indicated significant differences between the sexes. Slight discrepancy between our results and those of Fernandes may be attributed to many factors like different Ethnic and racial groups with difference in body stature, skeletal size, height of an individual; sample size, Genetic and Environmental factors; difference in Osteoclastic and Osteoblastic activity and pneumatization process of sinus in different age and sex groups Jun et al 2005 reported that the maxillary sinus has a maximum growth period at the third decade in males and the second decade in females. (Sharma et al 2014, Möhlhenrich et al 2015 , Paknahad et al 2017)
Ekizoglu et al 2014 study of the morphometric characteristics of maxillary sinus in Turkish population described that all maxillary sinus measurements of males were significantly higher than those of females (P < 0.001). Uthman et al 2011 and Teke et al 2007 also reported greater values for maxillary sinus width, length, and height in males.

In consensus with our results, Masri et al 2013 revealed that the males tended to have larger sizes of all variables of the maxillary sinus (width, depth, height and volume than those of females, though only height and width showed significant differences.
Emirzeoglu et al. 2007 examination of coronal CT scan images taken from 77 Turkish patients (38 female and 39 male subjects) aged between 18 and 72 years demonstrated significant difference of maxillary sinus volume between males and females (Males: 19.8±6.3 cm3; Females: 16±5 cm3). (Masri et al 2013)
Jasim and AlTaei 2013 and Jehan et al 2014 confirmed our results that the measurements of the volume and dimensions of maxillary sinuses in both dentate and edentulous groups were larger in males compared with females and they tend to decrease with the older age. These results were also supported by Kanthem et al 2015.
Paknahad et al 2017 reported that while a significant sex difference was found in the length and height of maxillary sinus, there was no significant difference between sexes in maxillary sinus width which is not exactly the same of our findings.
A discriminant analysis was conducted to predict gender (Male or Female). The significant predictors for gender were: sinus volume and inter-maxillary distance. The discriminate functions at group centroids (Group means) were 0.620 for males and -0.620 for females.

Classification results revealed that 66.0% of the males were correctly classified while 74.0% of the females were correctly classified according to the prediction equation. Hence, the overall correct classification was 70.0%.
Amin and Hassan 2012 demonstrated that MDCT measurements of cephalo-caudal and size of the left maxillary sinuses are helpful feature in sex determination in Egyptians. The study reported that the correct predictive accuracy was 70.8% in males and 62.5% in females.

Ekizoglu et al 2014 found that the accuracy rate according to gender was 80% for female gender and 74.3% for male gender (mean accuracy of whole study population was 77.15%). Teke et al 2007 reported rates for the measurements, which was 69.3% for male gender and 69.4% for female gender with overall accuracy rate of 69.3%.4
Kanthem et al 2015 showed statistically significant values with a higher percentage of sexual dimorphism in the case of volume with 85.46% for the right side and 78.38% for the left side.

According to the results of Paknahad et al 2017, the classification accuracy was 78% for females and 74% for males with an overall accuracy of 76%. On the other hand, Fernandes et al 2004 reported higher accuracy rate of 79.2%, using different parameters of the skull including maxillary sinus measurements. This higher accuracy might be due to using multiple parameters in addition to maxillary sinus measurements.

Attia et al 2012 study reported that maxillary sinus dimension measurements, especially the right height, are valuable in studying the sexual dimorphism with overall accuracy 69.9%.However, Tambawala et al 2015 and Uthman et al 2011 studies about sex determination from maxillary sinus dimensions using CT scan showed that the maxillary sinus height was the best discriminant parameter that could be used to study sexual dimorphism with an overall accuracy of 71.6%.

Supporting our results, Jehan et al 2014 concluded that the strongest correlated variable with bizygomatic distance was the intermaxillary distance (r = 0.3037) in male & AP diameter of sinus (r = 0.5980) in female.
Sharma et al 2014 found that 65.16% of males and 68.9% of females were sexed correctly and the overall percentage for sexing maxillary sinuses correctly was 67.03% and sinus AP was the best discriminant parameter with an overall accuracy of 69.81%.
The differences in the reported accuracy rates of the previous studies was probably due to diverse ethnic and racial groups, variation in the methodological and statistical analysis applied, different radiographic techniques, and different sample size. Paknahad et al 2017
Conclusion:.Forensic investigations might provide more accurate indications by the mean of utilization of advanced radiology, and specifically CBCT, exams and modern software for reconstructing 3D virtual models. CBCT scan can precisely locate and measure the maxillary sinus dimentions. Thus CBCT measurements of maxillary sinus can be used as a supplementary tool for sex determination in forensic anthropology, especially in cases where other traditional methods are not conclusive
From this study it was concluded that the dimensions and volume of the maxillary sinuses of male was found to be larger than those of female. By discriminant function analysis it was found that maxillary sinus volume and intermaxillary distance were the best discriminant parameter that could be used to study sexual dimorphism

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