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J Forensic Sci, 2015

doi: 10.1111/1556-4029.12630
Available online at: onlinelibrary.wiley.com

PAPER
ANTHROPOLOGY

Justin Michel,1,2 M.D., M.Sc.; Arnaud Paganelli,1,2 M.D., M.Sc.; Arthur Varoquaux,3 M.D., M.Sc.;
Marie-Dominique Piercecchi-Marti,2,4 M.D., Ph.D.; Pascal Adalian,2 Ph.D.;
Georges Leonetti,2,4 M.D., Ph.D.; and Patrick Dessi,1,2 M.D., M.Sc.

Determination of Sex: Interest of Frontal Sinus


3D Reconstructions*

ABSTRACT: Frontal sinuses (FSs) have been studied in radiology, anthropology, and forensic anthropology. This study aimed to determine

whether it was possible to predict the age and sex of an individual using FS volume. Sixty-nine anonymized CT scans were imported to MIMICS 10.01 software (Materialise N.V.), and each FS volume was calculated in mm3. There was an absence of significant difference between
right and left FS volume (p = 0.173) and an absence of correlation between age and FS volume (Pearsons test; p = 0.705). Sexual dimorphism
was significantly different (p = 0.001). However, the most discriminant datum for determining sex was found to be the total FS volume (sum
of an individuals right and left FS volumes) with linear discriminant Fishers function coefficients of 2.759 for the male group and 1.275
for the female group. With this model, 72.5% of our sample was correctly classified according to sex.

KEYWORDS: forensic science, forensic anthropology, physical anthropology, frontal sinus volume, sexual dimorphism, identification
Although the interest of frontal sinuses (FSs) has been studied
since the 1920s in radiology and anthropology, their usefulness
in forensic anthropology has recently been highlighted for the
positive identification of corpses (1,2). Indeed, it has been scientifically demonstrated that FSs are unique to each individual and
are unaffected by ancestry (3,4). Their anatomical variations are
the bases for forensic identification (3,57). Nowadays, identification of unidentified bodies using the FS is a reliable technique
that is used when antemortem records exist and could be presented as evidence in a court of law (6,810).
The frontal sinus is a paired, irregularly shaped, pneumatized
cavity located in the frontal bone deep to the superciliary arch
(8). FSs develop as diverticula originating from the lateral nasal
wall around the fourth fetal month following the development of
the frontal recess (9). They are noticeable by the end of the first
year but cannot be detected on radiologic plain film until the age
of 3 years (7). They complete their development at the age of
19 or 20 years (6,7,1013). Some authors have reported that
paranasal sinuses become smaller during life perhaps due to

1
Department of Oto-Rhino-Laryngology - Head and Neck Surgery, University Hospital La Timone, 264 rue St. Pierre, 13385 Cedex 5, Marseille,
France.
2
Unite dAnthropologie Bioculturelle, CNRS-EFS, Faculte de Medecine
Nord, UMR 6578, Aix-Marseille Universite, 51 Boulevard Pierre Dramard,
13916, Marseille, France.
3
Department of Radiology, University Hospital La Timone, 264 rue St.
Pierre, 13385 Cedex 5, Marseille, France.
4
Department of Forensic Medicine, University Hospital La Timone, 264
rue St. Pierre, 13385 Cedex 5, Marseille, France.
*Presented at the 117th Congress of the French Oto-Rhino-Laryngology
Society, October 1618, 2010, in Paris, France.
Received 18 Feb. 2013; and in revised form 20 Nov. 2013; accepted 4
Feb. 2014.

2015 American Academy of Forensic Sciences

pathologic events (10). In clinical practice, chronic sinusitis is


sometimes associated with osteosclerosis of the sinus walls
which leads to decreased sinus volume (11).
The goal of this study was to evaluate the possibility of determining age or sex using FS volume in an adult sample.
Materials and Methods
This retrospective study was performed on anonymized computerized tomography scan (CT scan) images of 69 patients (35
female and 34 male subjects) aged between 16 and 83 years
(mean: 50.2 years), who were referred to the Department of
General Radiology at La Timone University Hospital (Marseille,
France) between November 2009 and January 2010. Mean age
of the female group was 49.97 years (range 1683 years). The
mean age of the male group was 50.47 years (range of
1983 years). Figure 1 shows the distribution of patients by age
and sex. Subjects with any signs of sinus pathology, surgery, or
trauma were excluded from the study. Sinus CT scans were
obtained using two CT scanners (Scanner Siemens Somatom
definition, Siemens Healthcare, Germany or Scanner General
Electric Light speed LS 16 Pro, GE) applying the following
parameters Kv: 120, mAs: 130, 0.3 mm slice every 0.6 mm.
Three-dimensional reconstructions were obtained using MIMICS 10.01 software (Materialise N.V., Leuven, Belgium) on a
Dell computer (Dell XPS M 1330, processor Intel CoreTM 2
Duo CPU T8300 @ 2.40 GHz 2.40 GHz). The procedure was
as follows: anonymized CT-scan transverse images (File IMA)
were imported to MIMICS 10.01, and coronal and sagittal
images were studied to allow thresholding of the region of interest (ROI). The ROI of each FS (right and left) was created using
the CT gray scale (threshold between 1024 and 401 Hounsfield units). This ROI was corrected by the same operator,
1

JOURNAL OF FORENSIC SCIENCES

We found no significant difference in age distribution between


female and male groups, (Students t-test; p = 0.919) nor
between left and right FS volumes (Students t-test; p = 0.188).
Figures 2 and 3 show the distribution of right and left FS volumes (respectively), according to sex.
Correlations
Pearsons correlation test found an absence of correlation
between age and right or left FS volumes (p = 0.705 and
p = 0.173, respectively).
Linear Discriminant Analysis
FIG. 1Distribution of patients by age and sex.

section by section, in the three space planes. Volume of the ROI


(corresponding to the FS volume) was then calculated by
MIMICS, and results were obtained in cubic millimeters (mm3).
The procedure was conducted twice by the same operator for
each FS. Any pneumatization was accepted as presence of FS.
Results were analyzed using Microsoft Office Excel. Statistical
calculations were performed using IBM SPSS Statistics 18 software. To evaluate the repeatability (intraobserver variations), we
used a Wilcoxon test and the intraclass correlation coefficient
(ICC) (a = 5%) as defined by Fleiss and Shrout (14). Sinus volumes were compared between the sexes. A leftright comparison
was also made. Pearsons correlation test was applied to evaluate
the effect of the age distribution of our sample on the volume of
their FSs. A linear discriminant analysis was used to predict sex
according to FS volume. To create the model, we chose a stepwise discriminant equation using the Wilks lambda method
(F probability to enter fixed at 3.84 and F to exit at 2.71). Prior
probabilities were fixed equal. Sectioning point was defined using
this model and a receiver operating characteristic (ROC) curve.

Results
Repeatability
Wilcoxons test found no significant difference between
results in the first series of FS volume measurements and results
in the second series. We found an intraclass coefficient of correlation between single measurements of 99.5% (95% confidence
interval ranging from 99.1% to 99.7%) and between mean measurements of 99.7% (95% confidence interval (range: 99.6
99.8%). All statistical calculations were performed using results
from the second series of measurements.
Descriptive Statistics
Table 1 shows the results of our FS volume measurements
according to sex and side.

Using a linear discriminant analysis, we found a significant


statistical difference between mean volume according to sex for
right and left sinuses (p = 0.001).
The most discriminant datum for determining sex was found
to be the total FS volume (i.e., the sum of an individuals right
and left FS volumes) with linear discriminant Fishers function
coefficients of 2.759 for the male group and 1.275 for the
female group.
The model was established by Linear Fishers equations as
follows:
F0 (Males) 4:359  104  total FS volume  2:763
F1 (Females) : 2:368  104  total FS volume  1:283
The probability of a patient belonging to the male or female
group was determined as follows:
P0 (Male) : exp(F0)/(exp(F0) + exp(F1))
P1 (Female): exp(F1)/(Exp(f0) + exp(F1)) 1-P1
Using this model, sex determination accuracy was 72.5%. The
sectioning point defined using this model, and a ROC curve
(Fig. 4) was 7050 mm3. Above this sectioning point, the probability of belonging to the male group is higher. The sensitivity
and specificity of this sectioning point were 0.676 and 0.171,
respectively.
Discussion
MIMICS is a powerful, fast, intuitive, and user-friendly tool
for any 3D image-based project. Its reliability has been shown in
many studies in the literature (15,16). In a study published in
May 2010, Varghese et al. (15) compared linear measurements
on spiral CT obtained by MIMICS with cephalometric and
anatomical measurements. They found that measurements
obtained using MIMICS were comparable to anatomical mea-

TABLE 1Minimum, maximum, and mean frontal sinus volumes according to side (right or left) and sex.

Males
Right frontal sinus
Left frontal sinus
Females
Right frontal sinus
Left frontal sinus

Minimum
(mm3)

Maximum
(mm3)

Mean
(mm3)

Confidence Interval
95% (mm3)

Standard
Deviation (mm3)

Mean Standard
Error (mm3)

94.35
188.12

12,935.35
12,737.05

4513.89
5035.09

3415.185612.59
3858.176212

3098.57
3274.6

539.39
561.59

31.05
41.64

6483.47
9407.89

2424.4
2644.48

1833.643015.15
1948.983339.99

1719.76
2024.69

290.69
342.24

MICHEL ET AL.

FIG. 2Distribution of right frontal sinus volumes according to sex.

FIG. 3Distribution of left frontal sinus volumes according to sex.

surements. Results for repeatability have shown that our method


using CT-scanner 3D reconstructions is reliable using the very
high intraclass coefficient of correlation. Moerenhout et al. (16),
in their study on the reliability of cephalometric measurements
performed with MIMICS, found a very high degree of repeatability of facial measurements obtained using MIMICS software, with an intraclass coefficient of correlation of 1000, which
is comparable to our results. Moreover, they evaluated interobserver reliability, which was not significantly different (16).
We decided to perform calculations using the second series of
measurements because we estimated that the operator was better
trained, even though the differences between the two series were
not significantly different.
Computerized tomography scans of the sinus have superseded
X-ray radiographs in routine medical practice. According to the
French medical guidelines, there is almost no indication for
using X-ray radiographs for the diagnosis of sinus pathology
(17). In forensic anthropology, this change in medical practice

FRONTAL SINUS 3D RECONSTRUCTIONS

FIG. 4Receiving operator characteristic (ROC) curve used to define the


sectioning point to determine sex according to total frontal sinus volume.

has resulted in fewer patients receiving X-ray radiographs and


more patients undergoing sinus CT scans. Consequently, some
studies have started to evaluate the use of FS CT scans for identifying unidentified bodies (1821). According to these studies,
which took only two-dimensional measurements of the FS and
compared antemortem and postmortem images, sinus CT scans
provide very precise data and offer a new field of research.
A similar shift can be seen in the anthropological literature, and
studies have shown that the use of CT scans for morphometric
investigations of the FS is easy and reliable for antemortem/postmortem comparison (18,20). We found only a few morphometric
studies in the literature using 3D-reconstructions of the frontal
sinus (2224). Nevertheless, 3D-reconstructions are an important
part of virtual anthropology and have dramatically enhanced the
potential for qualitative and quantitative morphological analysis
(25). They allow anthropologists to take into consideration morpho-functional ensembles that were impossible to study in classical anthropology. Currently, tridimensional reconstructions of
the paranasal sinuses are often used in radiology. Radiologists
have developed virtual endoscopy techniques to explore the
paranasal cavities (23). These reconstructions can also be used
to study airflow in the nasal and paranasal cavities (22).
Some published data claimed that the left FS was bigger than
the right FS (20,26). Ponde et al. (26) conducted a study on 100
macerated skulls and concluded there was a significant difference regarding sex and location of the sinus, with predominance
of the left side in males. Tatlisumak et al. (20) analyzed 300
paranasal CT scans and concluded that measurements were different the left side being larger in both sexes. Our results
showed that the male left side is larger. However, unlike the
other studies, our results did not yield a significant difference.
Likewise, Emirzeoglu et al. (18), in a volumetric study of paranasal sinuses using 77-CT scans, found no significant left/right
difference for FS volume. These nonconcording studies use different methods as linear measurements and volume calculations
do not provide the same results. We believe that 3D reconstructions of the FS provide more reliable data (e.g., volume) than
2D measurements. The size of an anatomical structure such as
a FS must, whenever possible, be evaluated using three-dimensional measurements.

JOURNAL OF FORENSIC SCIENCES

It is commonly acknowledged that FSs reach their maximum


size at 20 years old and then remain stable until death (excluding pathological phenomena) (6,7,1013). Tatlisumak et al. (20)
conducted a study on 300 paranasal CT scans and found that
maximum size of FS was reached between 30 and 40 years old
and that FS volume decreased thereafter. We found no correlation between age and FS volume. In Fig. 1, we can see a disparity in some age brackets (mainly between 40 and 49 years).
Nevertheless, age distribution in our data was statistically
homogenous between sexes. This observation demonstrates that
the difference in FS volumes observed between females and
males is not biased by age distribution.
In accordance with the literature (8,18,20,21,26), our data
revealed a significant difference in FS volume between females
and males. These results may be correlated to the overall skull
size difference between males and females, which still exists in
modern humans and could also be correlated to the anterior projection of the glabella, which is a male characteristic. In this
study, we validated our protocol for determining sinus volume
and the parameters studied. Our results showed that sex was the
most discriminating factor in regard to volume differences
between individuals. In a prospective study, we will correlate
paranasal sinus volume with other cranial measurements (maximum skull length and biparietal distance) to define a weighting
factor. In 2010, Uthman et al. (21) measured FS size on 90 paranasal CT scans (45 females and 45 males) and found a model for
sex prediction based on left sinus height, with an overall accuracy
of 76.9%. This result, based on two-dimensional measurements,
is comparable to our prediction model based on total FS volume
(three-dimensional measurements), which had an overall accuracy
of 72.5%. Uthman et al. (21) improved their prediction model by
combining left sinus height with maximum skull length, which
gave an overall sex classification accuracy of 85.9%. A more
recent study involving the frontal sinus enabled correct sex identification in 60% of cases using multivariate logistic regression
equations (29). Our results are consistent with published data.
Regarding FS features, we found no absence of FS in our
sample. In four patients, we found a hypoplasic FS (volume
inferior to 100 mm3). One (1.4%) of these four patients had
bilateral hypoplasia. In the literature, results for absence of FS
(also called agenesis or aplasia) were very variable (range:
050%). Typically, this occurs approximately in 5% of cases
(6,8,20,21,26,30). Variability in FS absence may be linked to the
sample used to evaluate FS features: FS absence seemed to be
more prevalent in some populations, such as Eskimos, with
extreme living conditions (13). However, it may also be linked
to the technique used to evaluate presence or absence of FS.
X-ray photographs seemed to augment the number of FS
absences. FS is a dynamic component of the fronto-ethmoidal
complex and it may be difficult to confirm its presence by X-ray
imaging when pneumatization is low (13). The difference
between aplasia and hypoplasia cannot be evaluated using X-ray
photographs. We used CT scans to evaluate FS volume and systematically found a pneumatized FS. Another important feature is
FS morphology, which shows very high interindividual variability. The uniqueness of the FS is the basis of a number of forensic
identification methods (3,6,8,21,28). We also found a very high
degree of variability between the individuals in our sample.
Conclusion
We proposed a new protocol to evaluate the variability of the
FS in an adult population. Using this protocol, we validated the

high feasibility of this technique in addition to the very high reliability of our results. Thus, we were able to demonstrate the
absence of significant differences between right and left FS volume, the absence of correlation between age and FS volume,
and the existence of a sexual dimorphism of FS volume, which
are foreground problems in the fields of physical anthropology
and forensic anthropology aimed at establishing the biological
profile of an individual. We found that there was an absence of
correlation between age and FS volume in our data but that it
was possible to predict sex with 72.5% of accuracy. This study
also opens up new avenues of research which could lead to the
formal identification of an individual by exploiting the very high
degree of morphological variability observed in FS CT-scan 3D
reconstructions used to perform antemortem and postmortem
comparisons.
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Additional information and reprint requests:
Justin Michel, M.D., M.Sc.
Department of Oto-Rhino-Laryngology - Head and Neck Surgery
University Hospital La Timone
264 rue St. Pierre
13385 Cedex 5
Marseille
France
E-mail: justin.michel@univ-amu.fr
justin.michel@ap-hm.fr

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