Vous êtes sur la page 1sur 9

Forensic Science International 271 (2017) 126.e1–126.

e9

Contents lists available at ScienceDirect

Forensic Science International


journal homepage: www.elsevier.com/locate/forsciint

Forensic Anthropology Population Data

Applicability and limitations of sex assessment based on foramen


magnum
Zbyšek Seiferta , Lukáš Friedla,* , Kathia Chaumoitreb,c, Jaroslav Bružekd,e


a  , Czech Republic
Department of Anthropology, University of West Bohemia, 30614 Plzen
b
Aix-Marseille Université, 13284 Marseille, France
c
APHM, Hôpital Nord, Medical Imaging Department, 13915 Marseille, France
d
Department of Anthropology and Human Genetics, Charles University in Prague, Prague, Czech Republic
e
UMR5199 PACEA, Université de Bordeaux, Pessac, France

A R T I C L E I N F O A B S T R A C T

Article history:
Received 30 August 2016 Sex assessment of skeletal remains in the context of forensic investigation is one of the most important
Received in revised form 29 November 2016 components when constructing biological profile of the deceased individual since it helps to significantly
Accepted 30 November 2016 narrow down the number of potential victims. Therefore, the number of methods suitable to estimate sex
Available online 8 December 2016 should be as wide as possible, especially for cases of highly fragmented remains. This paper offers a
classification method for sexing human remains based on an area around foramen magnum and tests
Keywords: other similar discriminatory functions published elsewhere on an independent sample from the
Forensic anthropology population data circummediterranean region. We provide discriminant and logistic regression functions for several sets
Sex assessment
of variable combinations derived from head CT images. None of the functions performs reliably enough to
Discriminant analysis
be used in the forensic context. The same holds true for other discriminatory functions published in the
Reliability
Foramen magnum literature. For most of the functions, the failure rate (its inability to successfully assign sex of an unknown
CT imaging individual) reaches 100%. Thus, despite the fact that foramen magnum is sexually dimorphic in most
populations, its use in sexing cranial remains in the forensic context should be limited only to cases in
which we know population affinity of unknown skeletal remains and can provide referential data from
the same population to estimate sex.
© 2016 Elsevier Ireland Ltd. All rights reserved.

1. Introduction this part of the skeleton can be based only on the population
specific quantitative differences in size and shape [6].
Sex diagnosis is one of the most important components in The need for generalized sexing methods is especially evident
evaluating human skeletal remains in the forensic and/or in forensic cases. When working with a large number of human
bioarcheological contexts [1–4]. It can be accomplished due to remains coming from natural disasters, mass graves, or terrorist
the expression of sexual dimorphism in the skeleton or its attacks, we cannot rely on procedures based on regional reference
individual portions. The degree of expression of sexual dimor- samples since the assessment of ancestry is still an anthropological
phism in the skeleton differs between individuals and populations problem [1], and population affinity of most human remains from
because it depends on many biologically relevant variables [5]. The these events will be unknown [2,7]. The need for sex diagnosis
most valued variables used for sexing skeletal remains are those from fragmentary or damaged skeletal material turns the attention
that allow for a reliable sex estimate because they reflect functional of many researchers to other skeletal elements besides the pelvis
differences between the two sexes. Such traits are, however, not and cranium (e.g., to lumbal vertebrae: [8], to the first rib: [9], or to
present on the human cranium and thus, the sex diagnosis from sternum: [10]).
Recently, there has been an increase in the number of
publications on sexing methods based on fragmentary remains
of the basicranium. These methods use, for example, the maximum
transverse diameter [11] together with the antero-posterior
* Corresponding author at: Department of Anthropology, University of West
Bohemia, Sedlá9
ckova 15, 30614 Plzen , Czechia. diameter of foramen magnum (FM) [12–15], some others add the
E-mail address: lukas.friedl@gmail.com (L. Friedl). area of FM [16], its circumference [17], and dimensions of occipital

http://dx.doi.org/10.1016/j.forsciint.2016.11.044
0379-0738/© 2016 Elsevier Ireland Ltd. All rights reserved.
126.e2 Z. Seifert et al. / Forensic Science International 271 (2017) 126.e1–126.e9

Table 1
Overview of methods used for sex assessment based on foramen magnum.

Publication Accuracy Sex Cross-validated Sex bias after Variables Statistical Population N Material Reliability
(%) bias (%) accuracy (%) CV (%) treatment tested

Edwards et al. [16] 67.2 2.9 66.0 0.0 LFM, WFM, AFM DFA Modern Swiss 250 CT
66.4 25.2 – – LFM, WFM, AFM LR

Galdames et al. [12] 66.5 – – – LFM, WFM DFA – Brazilian 211 Dry
skull

Gapert et al. [96] – – 76.7 9.7 LOCsin, WOCdx, DFA Past British 146 Dry
min. skull
iICB

Gapert et al. [15] 70.3 1.0 – – LFM, WFM DFA Past British 158 Dry
skull

Gapert et al. [18] – – 71.9 1.7 WFM, min. iICB, DFA Past British 135 Dry
LOCdx skull
a
– – 81.3 17.5 WOCdx, max. eICB, DFA >50 80
min. iICB
– – 69.1 14.4 Max. eICB, min. DFA <50b 55
iICB

Holland [13] 71.0 – 70.0 – LFM, WFM LR Past American 100 Dry Subsample
skull
90.0 – 85.0 – LFM, WFM, LOC, LR Subsample
WOC, IFB, min.
iICB,
max. eICB, max.
iICB, LBT

Jain et al. [11] 75.7 – 75.7 – 1. WFM; 2. IFM, DFA – Indian 140 CT
AFM

Raghavendra Babu 88.0 – – – LFM, WFM LR – South 90 Dry


et al. [14] Indian skull

Singh and Talwar [19] 70.0 1.6 – – LFM, WFM, max. DFA – Indian 50 Dry
eICB, min. iICB, skull
max. iICB, IFB

Uthman et al. [17] 81.8 17.4 – – LFM, WFM, CFM, DFA Modern Iraqi 88 CT
AFM

CV — cross-validation; DFA — discriminant function analysis; LR — logistic regression; CT — computer tomography.


LFM — length of foramen magnum (FM); WFM — width of FM; AFM — area of FM; CFM — circumference of FM; IFM — index of FM.
LOC — length of occipital condyle (OC); WOC — width of OC; ICB — intercondylar breadth (internal or external); IFB — inter (postcondylar) foramina breadth, LBT — length of
basilar tubercle.
sin — left; dx — right.
a
Subgroup of individuals under 50 years of age at death.
b
Subgroup of individuals over 50 years of age at death.

condyles [13,15,18,19]. Table 1 provides basic overview of these The aim of this study is to evaluate the applicability of the
methods together with their accuracy. published sexing methods based on FM in recent French
It is generally accepted that the methods of sex classification population, and to compare discrimination power of individual
show high population specificity (e.g., Refs. [20,21]). Moreover, measurements of FM through computing our own discriminant
populations are not stationary in time and that influences the and logistic regression functions. General aim of this study is to
applicability of the methods due to secular trends, which can critically evaluate the significance of FM dimensions for sex
rapidly result in size changes in the skeleton or its respective parts estimation in the forensic context.
[22]. Several studies use only morphometric or typological
analyses of FM without any efforts to create classification models 2. Materials and methods
whose outputs would include statistics describing natural varia-
tion within a population (e.g., mean and range values for the FM 2.1. Samples
dimensions or shape group affiliation) using modern reference
sample [23–29] and past reference samples or anatomical The material consists of 109 CT images of the head of patients of
collections [30–39]. Faculté de Médecine, Aix Marseille Université, France. The sample
The methods that are supposed to be used in the forensic includes heterogeneous individuals from the circummediterra-
context should be as accurate and reliable (internally and nean area and comprises of 54 adult males (mean age = 52 years,
externally valid) as possible but at the same time they should SD = 17 years) and 55 females (mean age = 58 years, SD = 17 years).
have low rate of misclassification [40,41]. Therefore, such studies These data were collected and anonymized with the approval of
should report an error rate [7,42] and a sex bias [43]. The lower the ethics committee of Aix-Marseille Université: Faculté de
limit for reliability of these sexing methods should be at least 95% Médicine. Scans were captured using Siemens© Sensation 64
(of correctly classified individuals) [44,45]. scanner (Erlangen, Germany) at Department of Radiology — North
Z. Seifert et al. / Forensic Science International 271 (2017) 126.e1–126.e9 126.e3

Hospital in Marseille, France. The tomograph was configured as length, breadth, height, and cranial base length) to identify internal
follows: 120 kV, 36–350 mA s, 1.5 mm pitch. Sorting the individuals variability of the sample (Table 2). All of these variables together
into age categories was considered neither necessary nor beneficial represent simplified spatial relationships between FM area and the
because there are no statistically significant changes in dimensions rest of the skull.
of skull throughout life [46]. The patients’ skulls were free of The linear dimensions were obtained from raw landmark
pathologies or injuries around the FM, and if a head injury was coordinates by means of Euclidean Distance Matrix Analysis [51] in
present in other parts of the skull, it did not interfere with PAST [52]. FM area and circumference were acquired with a
landmark positioning. specific software function of automatic outline tracing in FijiJ using
a two-dimensional projection of the FM outline on a plane.
2.2. Morphometric procedures
2.3. Statistical treatment
Every individual’s DICOM scan set was visually enhanced,
manually segmented, and a 3D surface model was created using Intra-observer error, assessing the level of measurement
FijiJ software [47]. The model was then cleaned and smoothed [48] accuracy when performed by one observer, was evaluated using
in MeshLab [49]. Nine landmarks (Fig. 1) were labeled on a 3D Mean Percentage Absolute Difference (MAD%) that was calculated
model in Morphome3cs [50] to allow for gathering of the as a ratio of mean of absolute differences between the first and
dimensional data. Labeling was done by one of the authors (ZS) second measurement divided by the mean value of the two
with experience in morphometrics. ZS first labeled one orbitale and measurements [53–55].
both porions, which allow for defining the transversal Frankfurt Assumptions of multivariate analyses were tested by means of
horizontal plane (TP). Corresponding sagittal (SP) and coronal one-way ANOVA, Shapiro–Wilk’s, Kruskal–Wallis’ and Levene’s
planes (CP) were also constructed. These planes were then used to tests. Discriminant Function Analysis (DFA) as an extensively
properly set the landmarks, i.e. vertex by moving TP superiorly, employed technique for discriminating sex was used for classifying
opisthocranion by moving CP posteriorly, foraminolaterale and individuals into groups by maximizing the differences between
euryon by moving SP laterally. Midsagittal plane was used for sexes [56,57]. Logistic Regression Analysis (LRA) was also applied
placing medial landmarks (i.e., nasion, vertex, opisthocranion, because it provides considerably better discriminating power in
opisthion and basion) along the midline. some cases [41,58]. Jackknife and bootstrap validation methods were
Four variables were specified to define the foramen magnum applied to statistically validate the results [57,59]. Accuracy is a rate
area (length, width, circumference, and area), and four auxiliary of correct classification within a sample used to generate a
variables to define parameters of a whole skull (maximum cranial classification model. The term reliability defines the rate of correct

Fig. 1. Location of landmarks used in this study (ba — basion; eu — euryon; fol — foraminolaterale; n — nasion; o — opisthion; op — opisthocranion; or — orbitale; po — porion;
v — vertex).
126.e4 Z. Seifert et al. / Forensic Science International 271 (2017) 126.e1–126.e9

Table 2
Variables used in this study. Martin’s numbers and Howells’ abbreviations refer to the particular definition in Knußmann [97] and Howells [98].

Variable Martin Howells Definition


Ba-o M7 FOL Foramen magnum length; distance basion-opisthion
Fol-fol M16 Foramen magnum breadth; distance foraminolaterale-foraminolaterale
AFM Area of foramen magnum; automatic function in FijiJ software
CFM Circumference of foramen magnum; automatic function in FijiJ software
Ba-n M5 BNL Skull base length; distance basion-nasion
Ba-v M17(1) Maximum cranial height; distance basion-vertex
N-op M1d NOL Maximum cranial length; distance nasion-opisthocranion
Eu-eu M8 XCB Maximum cranial breadth; distance euryon-euryon perpendicular to sagittal plane and parallel to transverse plane

classification within an independent sample. The misclassification 3. Results


bias (error of classification) is a probability given by the classification
model that the sex of an unknown individual is estimated incorrectly, All variables show statistically significant differences of means
i.e., a ratio of falsely classified cases within the respective subgroup of between sex groups (P < 0.001 and P < 0.002 in case of cranial
same sexed individuals [e.g., classifying 10 males and 90 females as breadth). The values of MAD% ranged from 0.07% to 0.53%
females in a test sample give us an error rate (misclassification) of implying very low level of intra-observer error. The descriptive
10% when classifying an unknown individual as a female]. We then statistics of eight studied variables for 109 individuals is
use the term failure rate, which refers to a probability of failure when presented in Table 3. All multivariate analysis requirements were
assessing sex of an unknown individual, calculated as a sum of met with the exception for cranial height in males and cranial
individuals classified incorrectly and individuals with undetermined breadth in females, which were not normally distributed.
sex relative to the number of all individuals in a group/subgroup. It is Nevertheless, the deviation is small and DFA is robust enough
applicable when the posterior probability of classification is higher to deal with slight violations. The coefficients, test statistics, and
than 0.5. The sex bias [43] is a difference in correct classifications sex classification accuracy results of seven discriminant functions
between the subgroups of males and females (i.e., [sex bias] = [male (DF1–7) are presented in Table 4. The smallest Wilk’s lambda of
accuracy] [female accuracy]). 0.67 indicates the greatest classification power of DF7, neverthe-
There are two decisive criterions used in this study to assess less, this means that the variables used explain only about 30% of
possible extent of usability of FM variables in sex estimation method. observed variation. DF1 and DF7 show the highest classification
(1) A traditional approach of (correct) discrimination of sexes, which accuracy rate of 72.2% (males) and 74.5% (females) at a posterior
is based on the accuracy of separating groups of males and females by probability (PP) level of 0.5. The sex bias is low, except in cases of
a sectioning point that equals the posterior probability threshold of DF4 and DF5 where it is slightly over 6%. Not a single discriminant
0.5 (accuracy 1). In this case, significant number of individuals is function created that used only the FM dimensions reached
found in the overlapping areas of uncertainty (expressed through accuracy better than 70%. However, the use of four cranial
misclassification and sex biases). (2) A reliable discrimination of dimensions together with the FM area (DF7) helped to improve
sexes, which reflects the percentage of individuals extremely distant the score only slightly.
from sectioning point and out of the interval of uncertainty (accuracy When considering the reliable classification with PP of 0.95, the
2). Arbitrarily, the posterior probability threshold for this reliable accuracy drops in DF1 to 67% and 50%, respectively. In DF7 there is
discrimination is set to 0.95 [2,60,61]. We use the term accuracy quite an opposite trend with the accuracy increasing to 100% and
(accuracy 1) when expressing the correct classification rate with 80%, respectively. However, the majority of cases remain undeter-
posterior probability threshold 0.5, and then, we use the term mined (due to a stricter threshold) as we may recognize with the
reliable accuracy (accuracy 2) which refers to only those cases with help of the failure rate that is more indicative of the true
posterior probability higher than 95%. classification power. This means that an unknown individual
In the next step, we used our data to validate the discriminant or would be sexed, using these equations, with the extremely high
logistic regression formulae provided by several authors in their probability of failure.
publications [11,13–17]. We test the reliability of presented In a similar way, Table 5 presents coefficients, statistics, and
classification models on our French sample, which in these results of the LRA. It is noteworthy that LRA performs slightly
instances serves as an independent sample. The data were treated better than DFA in terms of classification accuracy and sex bias,
and analyses performed in Microsoft Excel and Real Statistics with 77.8% of correctly classified males and 76.4% females (DF7),
Resource Pack [62], PAST 3 [52], and SPSS Statistics 22. and the highest sex bias of 4.3% at PP threshold of 0.5. Increasing

Table 3
Descriptive statistics of the variables used for groups of males and females supplemented by the P value of the Student’s t-test of means.

Variable M (n = 54) F (n = 55) P

Minimum Maximum Mean SD Minimum Maximum Mean SD


Ba-o (mm) 28.98 41.91 36.79 2.77 29.92 40.51 35.00 2.22 0.000
Fol-fol (mm) 27.02 37.09 30.97 2.10 23.89 35.07 29.25 2.28 0.000
AFM (mm2) 619.35 1116.46 851.70 113.12 532.13 1040.11 760.28 98.44 0.000
CFM (mm) 89.50 121.20 105.73 7.18 86.15 117.57 100.09 6.41 0.000
Ba-n (mm) 94.18 117.19 105.52 4.84 91.04 109.16 101.19 4.58 0.000
Ba-v (mm) 118.54 151.53 141.23 5.71 123.67 154.15 135.69 5.91 0.000
Eu-eu (mm) 131.60 155.74 145.20 5.43 134.35 159.81 141.99 5.05 0.002
N-op (mm) 167.88 196.21 184.77 6.76 164.33 199.15 178.55 6.54 0.000
Z. Seifert et al. / Forensic Science International 271 (2017) 126.e1–126.e9 126.e5

Table 4
Unstandardized coefficients for each discriminant function and an overview of DFA results at different posterior probability (PP) levels.

DF Variable Coefficient Wilk’s l Cross-validated accuracy Sex bias (%) Mean error rate (%) Reliable accuracy Sex bias (%) Mean failure rate (%)
(accuracy 1)* (%) (accuracy 2)** (%)

M F M F
1 Ba-n 0.059 0.710 72.2 74.5 2.3 26.6 67.0 50.0 17.0 97.3
Ba-v 0.063
N-op 0.067
Eu-eu 0.079
Constant 37.977

2 Ba-o 0.190 0.844 63.0 67.3 4.3 34.9 0.0 0.0 0.0 100.0
Fol-fol 0.299
Constant 15.830

3 Ba-o 0.058 0.842 61.1 65.5 4.3 36.7 0.0 0.0 0.0 100.0
Fol-fol 0.209
CFM 0.071
Constant 15.611

4 Ba-o 0.001 0.836 63.0 69.1 6.1 33.9 0.0 0.0 0.0 100.0
Fol-fol 0.135
AFM 0.007
Constant 9.748

5 Ba-o 0.135 0.832 57.4 63.6 6.2 39.4 0.0 0.0 0.0 100.0
Fol-fol 0.183
CFM 0.204
AFM 0.016
Constant 2.482

6 CFM 0.131 0.838 63.0 65.5 2.5 35.8 0.0 0.0 0.0 100.0
AFM 0.018
Constant 0.742

7 Ba-n 0.074 0.674 72.2 74.5 2.3 26.6 100.0 80 20 92.7


Ba-v 0.025
N-op 0.053
Eu-eu 0.068
Ba-o 0.098
Fol-fol 0.163
CFM 0.141
AFM 0.008
Constant 30.635

DF — discriminant function; CFM — the circumference of foramen magnum; AFM — the area of foramen magnum.
*
PP > 0.5.
**
PP > 0.95.

PP threshold to 0.95, LRA performs similarly when comparing to standards, nonetheless, may not be set easily since particular
DFA with no truly significant success. A reliability test of the results depend on varying quality of medical images influenced by
already published sexing formulae (Table 6) yielded 32.9% and the scanner used, an individual to be scanned, specific scanning
68.7% of correct classification on an independent sample at PP of protocol [65], and also on subjective adjustment of images by the
0.5, and an alarmingly high sex bias up to 100%. researchers. Even though researches are reporting about optimal
threshold intervals of the given tissue, e.g. from 110 to 320 Houns-
4. Discussion field units for bone [66], a universal global threshold cannot be set
because any tissue shows characteristic but not specific values and
It is generally accepted that in cases where human skull shows the interval can be very wide and overlapping for different tissue
better preservation than pelvis, the basicranium and specifically [65], and setting the final threshold value is a matter of
the area around foramen magnum can be used for sexing an professional experience, knowledge of human anatomy, and more
unknown individual. It is especially relevant for highly fragmented or less of an instinct. Besides manual thresholding, there are other
remains when the cranial base preserves well due to large mass of methods of semi or fully automatic procedures based on various
soft tissue and ligaments surrounding it [63,64]. Nevertheless, it is algorithms [67–73]. The promising approach uses Half-Maximum-
necessary to follow established standards (or to try to improve Height algorithm proposed by Spoor et al. [74] and introduced in
them) for sex assessment to make a study trustworthy. However, in 3D segmentation and surface reconstruction by Dutailly et al. [75].
the case of foramen magnum area there are no well-established Most often employed technique of surface model generation is
methods, at least when one considers CT and other medical called “marching cubes” [76] but there are alternatives [77]. The
material as a source of data. With such sources, standards for (1) reconstruction process creates staircase artifacts but they can be
medical images processing and 3D surface model generation (i.e. reduced by smoothing without the loss of information [48,78].
adjusting the contrast, noise, and other features of images, and According to Richards and Jabour [79] there are four clear
segmenting regions of interest), and (2) proper definitions of problems with taking measurements of foramen magnum and
cranial landmarks on virtual skull should be developed. Such adjacent anatomical structures out of CT data: (1) similar tissue
126.e6 Z. Seifert et al. / Forensic Science International 271 (2017) 126.e1–126.e9

Table 5
Coefficients for each logistic regression function and an overview of LRA results at different posterior probability (PP) levels.

LR Variable Coefficient (B) Nagelkerke R2 Bootstrapped accuracy Sex bias (%) Mean error rate (%) Reliable accuracy Sex bias (%) Mean failure rate (%)
(accuracy 1)* (%) (accuracy 2)** (%)

M F M F
1 Ba-n 0.07 0.381 74.1 76.4 2.3 24.8 67.0 50.0 17.0 97.3
Ba-v 0.09
N-op 0.08
Eu-eu 0.09
Constant 47.37

2 Ba-o 0.16 0.209 64.8 67.3 2.5 34.0 0.0 0.0 0.0 100.0
Fol-fol 0.27
Constant 13.93

3 Ba-o 0.06 0.211 64.8 69.1 4.3 33.0 0.0 0.0 0.0 100.0
Fol-fol 0.20
CFM 0.06
Constant 13.79

4 Ba-o 0.01 0.220 66.7 69.1 2.4 32.1 0.0 0.0 0.0 100.0
Fol-fol 0.13
AFM 0.01
Constant 8.87

5 Ba-o 0.15 0.228 68.5 67.3 1.2 32.1 100.0 0.0 100.0 98.3
Fol-fol 0.19
CFM 0.22
AFM 0.02
Constant 1.35

6 CFM 0.14 0.218 66.7 67.3 0.6 33.0 0.0 0.0 0.0 100.0
AFM 0.02
Constant 0.29

7 Ba-n 0.09 0.424 77.8 76.4 1.4 22.9 80.0 100.0 20.0 93.6
Ba-v 0.04
N-op 0.07
Eu-eu 0.09
Ba-o 0.03
Fol-fol 0.19
CFM 0.09
AFM 0.01
Constant 44.11

LR — logistic regression; CFM — the circumference of foramen magnum; AFM — the area of foramen magnum.
*
PP > 0.5.
**
PP > 0.95.

Table 6
Validation of reliability of sex classification methods published by other authors (cited along with the reference material) using their discriminant or logistic regression
functions on our sample data.

Material Used variables Statistical analysis Accuracy (%)a Sex bias (%) Reliability (%)b Sex bias (%) Mean error rate (%)

M F Mean M F Mean
Modern Swiss [16] LFM, WFM, AFM LR 66.0 66.0 66.0 0.0 44.0 21.8 32.9 22.2 66.9
DF 77.1 51.9 64.5 25.2 59.3 78.2 68.7 18.9 31.3
Past British [15] LFM, WFM LR 66.0 70.0 68.0 4.0 100.0 0.0 50.0 100.0 50.0
DF 69.5 67.1 68.3 2.4 0.0 100.0 50.0 100.0 50.0
Past American [13] LFM, WFM LR – – 70.0 – 0.0 100.0 50.0 100.0 50.0
(Past) Indian [11] LFM, WFM DF – – 75.0 – 100.0 0.0 50.0 100.0 50.0
(Past) South Indian [14] LFM, WFM LR – – 88.0 – 18.5 65.5 42.0 46.9 58.0
Modern Iraqi [17] LFM, WFM, CFM, AFM DF 90.7 73.3 82.0 17.4 100.0 0.0 50.0 100.0 50.0

LFM — length of foramen magnum (FM); WFM — width of FM; AFM — area of FM; CFM — circumference of FM; IFM — index of FM.
LR — logistic regression; DF — discriminant function.
a
Accuracy declared by the author; using cross-validated results if available.
b
Accuracy achieved by using the published function on our study sample.

density of ligaments and bones, (2) sample orientation, (3) from 3D models based on CT data was already adequately
craniometric landmarks selection and definition, and (4) various explored by Stull et al. [80]. Measurements taken from virtual
methods of image processing, especially for detecting bone edges. models were also analyzed in general by Richard et al. [81].
Once all these problems are sufficiently controlled for, one has Hallgrimson et al. [82] also noted, that for the full use of
to make sure the researcher gathers the data reliably. Inter- geometric morphometrics it is crucial for reliable comparison of
observer error, associated to gathering cranial measurements data to have standardized procedures when digitizing landmarks.
Z. Seifert et al. / Forensic Science International 271 (2017) 126.e1–126.e9 126.e7

All these studies, including the one presented here, nevertheless approaches bears more value, it is critical to validate the sexing
show that the data can be reliably gathered and provide robust formulae on independent samples. Such approach has, nonethe-
results. less, not been vigorously applied in all the published studies.
Sexual dimorphism of the human skeleton shows statistically Our approach to sex diagnosis based on FM incorporated two
significant differences in almost all linear measurements due to levels of posterior probability (accuracy 1 with the decision rule
differences in size between the sexes due to genetic and hormonal being equal to 0.5 and accuracy 2 with the decision rule being equal
regulation during ontogeny. The difference in size between males to 0.95). The stricter criterion than P = 0.5 is preferred even in
and females can sum up to 20% in a relatively homogeneous studies by Franklin et al. [61] and Kranioti et al. [93], who also
population but also with a wide area of overlapping values [44,83– prefer the PP of 0.95. We opted for such approach specifically to
86]. test whether FM can be used reliably in the forensic context where
When evaluating the foramen magnum, the issue of individual’s a much higher certainty about the sex of a deceased individual is
age seems not to be of major concern, as Gapert et al. [18] or required. As we have shown, using such a strict (but needed)
Coquegniot and Le Minor [85] have already shown that there are no posterior probability renders any application of the estimation
significant changes in its dimensions during one’s life once the formulae almost impossible since the failure rates reach almost
ossification of this area in early childhood is completed. 100% for most of the equations. The only situation for which the
Our results indicate agreement with other authors that foramen method would be applicable is when the most inclusive formula is
magnum area is sexually dimorphic and that the difference is also used on individuals who lie on the extreme ends of their
statistically significant. However, that does not mean the area is distributions, i.e. small females and big males respectively. Overall,
suitable to be used in sex assessment. The reasons are multiple. the presented research showed that any sex estimation based on
First, there are underlying issues with reference samples, which foramen magnum is highly susceptible to fail in following Daubert
are often outdated as referential to contemporary populations due criteria, mainly due to unacceptable error rates [94,95].
to secular trends, which themselves greatly influence metric
features observed in populations during time [64,88,89]. Secular
5. Conclusions
trends have been addressed in general by Wescott and Jantz [22] or
Ubelaker [87], and specifically for foramen magnum by Gruber et al.
Estimating sex on the basis of metric evaluation of the
[63] or Saini et al. [64].
basicranium or cranial base is possible since general size
Second, according to our accuracy and reliability results
dimorphism is reflected even in this region of the cranium.
(Tables 4–6) of all the methods, they cannot be considered as
However, our results and the test of reliability of previously
practically applicable sex assessment methods. Even when we
published sexing methods gave us quite conclusive evidence that
consider the methods as being population specific, they are still not
population specificity is a key complication in applying any
powerful enough to give us confidence acceptable in the forensic
discriminant function or logistic regression formulae to samples
context besides as only a supportive evidence. Unacceptable sex
other than the one on which these functions have been created. In
bias up to 100% was produced by the reliability testing of
other words, DFA and LRA based on foramen magnum dimensions
discriminant and logistic regression functions presented by few
have very poor classification power in independent population
other authors [11,13–17] reaching far beyond 6% threshold of
samples. Moreover, the applicability of these formulae is further
bearable bias as proposed by Walker [43].
hindered in the forensic context due to a rather strict decisive
From a theoretical perspective, one isolated cranial structure
criterion (high posterior probability). Further development of
(FM) cannot express the same level of sexual dimorphism as the
population specific sex assessment methods based on foramen
cranium as a whole [2,90]. Sjøvold [91] already stated that based on
magnum does not have a justification due to the lack of
one trait we cannot accurately estimate the sex of a skeleton and
standardized protocols, strong population specificity, secular
our results confirm that FM alone is not sufficient for such effort.
trends of cranial dimensions, and overall low accuracy due to
Therefore, we support Edwards et al.’s [16] notion that FM should
inadequately expressed sexual dimorphism. Therefore, any
be used only in cases when there is insufficient preservation of the
application of discriminant functions presented here can only
skeleton in general or cranium in particular, and under the
be recommended if other, more suitable skeletal elements are
assumption that we know (or can reliably estimate) the population
unavailable for the sex assessment and if the victims come from
affinity of an individual. The accuracy of methods presented by
the same population on which the functions have been created.
other authors oscillate around 70–80% [15,16,19], which is very low
and unacceptable according to the legal rules of evidence awaiting
at least 95% [44,45]. In fact, even a complete skull used for sex Acknowledgments
assessment produces, on average, an accuracy ranging from 80 to
90% [7]. Use of the CT images sample for research purposes was
Classification methods like DFA, LRA, and others became approved by Faculté de Médecine, Aix Marseille Université in
integral parts of many statistical packages available today and France. This research was supported by the Grant Agency of the
this allows for a very fast data processing and analysis. Such speed University of West Bohemia (grant number: SGS-2015-010). The
is reflected in the amount of publications devoted to sex estimation authors would like to thank two anonymous reviewers for helpful
based on FM in recent years with divided suggestions about suggestions to improve the manuscript.
applicability in forensic practice [15,17,26,28,92]. In our view, plain
statement of statistically significant differences cannot be mis- References
placed for practical significance.
Among the above mentioned studies, there are contrasting [1] M.Y. Iscan, M. Steyn, The Human Skeleton in Forensic Medicine, Charles C.
Thomas, Springfield, 2013.
opinions on the applicability of FM to sex estimation. Gapert et al. [2] J. Bruzek, P. Murail, Methodology and reliability of sex determination from the
[15], for example, consider the metric assessment of FM as well skeleton, in: A. Schmitt, E. Cunha, J. Pinheiro (Eds.), Forensic Anthropology and
applicable to sexing the crania, while Edwards et al. [16], do not Medicine: Complementary Sciences From Recovery to Cause of Death,
Humana Press, Totowa, 2006, pp. 225–242.
recommend using FM for such purposes or if the need rises due to [3] D.C. Dirkmaat, A Companion to Forensic Anthropology, John Wiley & Sons, 2012.
preservation issues, the methods based on this area should be used [4] I. Gama, D. Navega, E. Cunha, Sex estimation using the second cervical
with caution. However, in order to decide which of these two vertebra: a morphometric analysis in a documented Portuguese skeletal
126.e8 Z. Seifert et al. / Forensic Science International 271 (2017) 126.e1–126.e9

sample, Int. J. Leg. Med. 129 (2015) 365–372, doi:http://dx.doi.org/10.1007/ [32] C. Manoel, F.B. Prado, P.H.F. Caria, F.C. Groppo, Morphometric analysis of the
s00414-014-1083-0. foramen magnum in human skulls of Brazilian individuals: its relation to
[5] D.W. Frayer, M.H. Wolpoff, Sexual dimorphism, Annu. Rev. Anthropol. 14 gender, Braz. J. Morphol. Sci. 26 (2009) 104–108.
(1985) 429–473. [33] P. Chethan, K.G. Prakash, B.V. Murlimanju, K.U. Prashanth, L.V. Prabhu, V.V.
[6] _
M. Steyn, M.Y. Işcan, Sexual dimorphism in the crania and mandibles of South Saralaya, A. Krishnamurthy, M.S. Somesh, C.G. Kumar, Morphological analysis
African whites, Forensic Sci. Int. 98 (1998) 9–16. and morphometry of the foramen magnum: an anatomical investigation, Turk.
[7] D.A. Komar, J.E. Buikstra, Forensic Anthropology: Contemporary Theory and Neurosurg. 22 (2012) 416–419, doi:http://dx.doi.org/10.5137/1019-5149.
Practice, Oxford University Press, Oxford, 2008. JTN.4297-11.1.
[8] K.R. Ostrofsky, S.E. Churchill, Sex determination by discriminant function [34] Y. Günay, M. Altinkök, The value of the size of foramen magnum in sex
analysis of lumbar vertebrae, J. Forensic Sci. 60 (2015) 21–28, doi:http://dx.doi. determination, J. Clin. Forensic Med. 7 (2000) 147–149, doi:http://dx.doi.org/
org/10.1111/1556-4029.12543. 10.1054/jcfm.2000.0430.
[9] A.M. Kubicka, J. Piontek, Sex estimation from measurements of the first rib in a [35] U. Ukoha, O.A. Egwu, I.J. Okafor, A.E. Anyabolu, G.U. Ndukwe, I. Okpala, Sexual
contemporary Polish population, Int. J. Leg. Med. 130 (2016) 265–272, doi: dimorphism in the foramen magnum of Nigerian adult, Int. J. Biol. Med. Res. 2
http://dx.doi.org/10.1007/s00414-015-1247-6. (2011) 878–881.
[10] P. Garcia-Parra, A. Perez Fernandez, M. Djorojevic, M. Botella, I. Aleman, Sexual [36] S.G. Kalthur, S. Padmashali, C. Gupta, A.S. Dsouza, Anatomic study of the
dimorphism of human sternum in a contemporary Spanish population, occipital condyle and its surgical implications in transcondylar approach, J.
Forensic Sci. Int. 244 (2014) 313.e1–313.e9, doi:http://dx.doi.org/10.1016/j. Craniovertebr. Junction Spine 5 (2014) 71–77, doi:http://dx.doi.org/10.4103/
forsciint.2014.06.019. 0974-8237.139201.
[11] D. Jain, O.P. Jasuja, S. Nath, Evaluation of foramen magnum in sex [37] N. Coskun, M. Sindel, The morphometric analysis of inferior clivus and
determination from human crania by using discriminant function analysis, foramen magnum and its importance in surgical approaches, Ann. Med. Sci. 13
Mednifico J. 2 (2014) 88–92. (2004) 36–39.
[12] I.C.S. Galdames, P.P. Russo, D.A.Z. Matamala, R.L. Smith, Sexual dimorphism in [38] P. Loyal, K. Ongeti, A. Pulei, P. Mandela, J. Ogeng’o, Gender related patterns in
the foramen magnum dimensions, Int. J. Morphol. 27 (2009) 21–23. the shape and dimensions of the foramen magnum in an adult Kenyan
[13] T.D. Holland, Sex determination of fragmentary crania by analysis of the cranial population, Anat. J. Africa 2 (2013) 138–141.
base, Am. J. Phys. Anthropol. 70 (1986) 203–208, doi:http://dx.doi.org/ [39] K. Saini, A mophometric study of foramen magnum in dry adult human skull,
10.1002/ajpa.1330700207. Int. J. Curr. Res. Rev. 7 (2015) 14.
[14] Y.P. Raghavendra Babu, T. Kanchan, Y. Attiku, P.N. Dixit, M.S. Kotian, Sex [40] C.R. Grivas, D.A. Komar, Kumho, Daubert, and the nature of scientific inquiry:
estimation from foramen magnum dimensions in an Indian population, J. implications for forensic anthropology, J. Forensic Sci. 53 (2008) 771–776, doi:
Forensic Leg. Med. 19 (2012) 162–167, doi:http://dx.doi.org/10.1016/j. http://dx.doi.org/10.1111/j.1556-4029.2008.00771.x.
jflm.2011.12.019. [41] F. Santos, P. Guyomarc’h, J. Bruzek, Statistical sex determination from
[15] R. Gapert, S. Black, J. Last, Sex determination from the foramen magnum: craniometrics: comparison of linear discriminant analysis, logistic regression,
discriminant function analysis in an eighteenth and nineteenth century British and support vector machines, Forensic Sci. Int. 245C (2014) 204.e1–204.e8,
sample, Int. J. Leg. Med. 123 (2009) 25–33, doi:http://dx.doi.org/10.1007/ doi:http://dx.doi.org/10.1016/j.forsciint.2014.10.010.
s00414-008-0256-0. [42] L.L. Klepinger, Fundamentals of Forensic Anthropology, John Wiley & Sons,
[16] K. Edwards, M.D. Viner, W. Schweitzer, M.J. Thali, Sex determination from the New Jersey, 2006.
foramen magnum, J. Forensic Radiol. Imaging 1 (2013) 186–192, doi:http://dx. [43] P.L. Walker, Sexing skulls using discriminant function analysis of visually
doi.org/10.1016/j.jofri.2013.06.004. assessed traits, Am. J. Phys. Anthropol. 136 (2008) 39–50, doi:http://dx.doi.org/
[17] A.T. Uthman, N.H. Al-Rawi, J.F. Al-Timimi, Evaluation of foramen magnum in 10.1002/ajpa.20776.
gender determination using helical CT scanning, Dentomaxillofac. Radiol. 41 [44] M.L. Lewis, The Bioarchaeology of Children Perspectives from Biological and
(2012) 197–202, doi:http://dx.doi.org/10.1259/dmfr/21276789. Forensic Anthropology, Cambridge University Press, Cambridge, 2007.
[18] R. Gapert, S. Black, J. Last, Test of age-related variation in the craniometry of the [45] L. Scheuer, Application of osteology to forensic medicine, Clin. Anat. 15 (2002)
adult human foramen magnum region: implications for sex determination 297–312.
methods, Forensic Sci. Med. Pathol. 9 (2013) 478–488, doi:http://dx.doi.org/ [46] E. Nikita, Age-associated variation and sexual dimorphism in adult cranial
10.1007/s12024-013-9437-3. morphology: implications in anthropological studies, Int. J. Osteoarchaeol. 24
[19] G. Singh, I. Talwar, Morphometric analysis of foramen magnum in human skull (2014) 557–569, doi:http://dx.doi.org/10.1002/oa.2241.
for sex determination, Hum. Biol. Rev. 2 (2013) 29–41. [47] J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S.
[20] M.K. Spradley, R.L. Jantz, Sex estimation in forensic anthropology: skull versus Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D.J. White, V.
postcranial elements, J. Forensic Sci. 56 (2011) 289–296, doi:http://dx.doi.org/ Hartenstein, K. Eliceiri, P. Tomancak, A. Cardona, Fiji: an open-source platform
10.1111/j.1556-4029.2010.01635.x. for biological-image analysis, Nat. Methods 9 (2012) 676–682, doi:http://dx.
[21] E. Gualdi-Russo, Sex determination from the talus and calcaneus measure- doi.org/10.1038/nmeth.2019.
ments, Forensic Sci. Int. 171 (2007) 151–156, doi:http://dx.doi.org/10.1016/j. [48] J. Vollmer, R. Mencl, H. Müller, Improved Laplacian smoothing of noisy surface
forsciint.2006.10.014. meshes, Eurographics 18 (1999) 1–8.
[22] D.J. Wescott, R.L. Jantz, Assessing craniofacial secular change in American [49] P. Cignoni, M. Callieri, M. Corsini, M. Dellepiane, F. Ganovelli, G. Ranzuglia,
blacks and whites using geometric morphometry, in: D.E. Slice (Ed.), Modern MeshLab: an open-source mesh processing tool, Eurographics (2008) 1–8.
Morphometrics in Physical Anthropology, Kluwer Academic/Plenum Publish- [50] CGG MFF UK, Morphome3cs II, Charles University in Prague, Czech Republic,
ers, New York, 2005, pp. 231–246. 2015. http://www.morphome3cs.com.
[23] P. Radhakrishnan, G. Chandhi, K. Sandeep, A.S. D’souza, A morphometric [51] S. Lele, J.T. Richtsmeier, Euclidean distance matrix analysis: a coordinate-free
analysis of the foramen magnum and variations in its shape: a computerized system approach for comparing biological shapes using landmark data, Am. J.
tomographic study, Nov. Sci. Int. J. Med. Sci. 1 (2012) 281–285. Phys. Anthropol. 86 (1991) 415–427, doi:http://dx.doi.org/10.1002/
[24] K.A. Murshed, A.E. Cicekcibasi, I. Tuncer, Morphometric evaluation of the ajpa.1330860307.
foramen magnum and variations in its shape: a study on computerized [52] Ø. Hammer, D.A.T. Harper, P.D. Ryan, PAST: paleontological statistics software
tomographic images of normal adults, Turk. J. Med. Sci. 33 (2003) 301–306. package for education and data analysis, Palaeontol. Electron. 4 (2001) 9.
[25] G. Kanodia, V. Parihar, Y.R. Yadav, P.R. Bhatele, D. Sharma, Morphometric [53] J.M. Bland, D.G. Altman, Statistical methods of assessing agreement between
analysis of posterior fossa and foramen magnum, J. Neurosci. Rural Pract. 3 two methods of clinical measurement, Lancet 1 (8476) (1986) 307–310.
(2012) 261–266, doi:http://dx.doi.org/10.4103/0976-3147.102602. [54] V. Sladek, M. Berner, P. Galeta, L. Friedl, S. Kudrnova, Technical note: the effect
[26] S. Sukumar, S. Yadav, H.B. Manju, 3D reconstruction computer tomography of of midshaft location on the error ranges of femoral and tibial cross-sectional
foramen magnum and frontonasal junction for sex determination in south parameters, Am. J. Phys. Anthropol. 141 (2010) 325–332, doi:http://dx.doi.org/
Indian population, Int. J. Pharm. Biol. Sci. 3 (B) (2012) 615–619. 10.1002/ajpa.21153.
[27] S. Makaju, Study of Morphometric Evaluation of Dimension and Shape of [55] P. Galeta, J. Bruzek, M. Lázni9cková-Galetová, Is sex estimation from handprints
Foramen Magnum: A Study on Computerized Tomographic in Nepalese in prehistoric cave art reliable? A view from biological and forensic
Population, (2013) . anthropology, J. Archaeol. Sci. 45 (2014) 141–149, doi:http://dx.doi.org/
[28] F.H. Erdil, V. Sabanciogullari, M. Çimen, O. Işik, Morphometric analysis of the 10.1016/j.jas.2014.01.028.
foramen magnum by computed tomography, Erciyes Med. J. 32 (2010) 167– [56] E. Giles, Statistical techniques for sex and race determination. Some comments
170. in defense, Am. J. Phys. Anthropol. 25 (1966) 85–86.
[29] D. Damiani, N.S. Borelli, H.J.F. Melo, R.S. Lima, L. Nobeschi, Morphometry and [57] M. Pietrusewsky, Metric analysis of skeletal remains: methods and applica-
spatial correlation of the foramen magnum and spinal cord through the tions, in: M.A. Katzenberg, S.R. Saunders (Eds.), Biological Anthropology of
magnetic resonance in normal young adults — anatomical and clinical aspects, Human Skeleton, John Wiley & Sons, Hoboken, 2007, pp. 487–532.
 
J. Morphol. Sci. 29 (2012) 87–90. [58] P. Chánová, Uživatelské srovnání ruzných klasifika9 cních nástroju multivaria9cní
[30] E. Osunwoke, G. Oladipo, Morphometric analysis of the foramen magnum and statistické analýzy aplikovaných ve forenzní antropologii k odhadu pohlaví
jugular foramen in adult skulls in southern Nigerian population, Am. J. Sci. Ind. podle kostry, Západo9 ceská univerzita v Plzni, 2012.
Res. 3 (2012) 446–448, doi:http://dx.doi.org/10.5251/ajsir.2012.3.6.446.448. [59] J. Hendl, Prehled statistických metod: analýza a metaanalýza dat, Portál, Praha,
[31] K. Natsis, M. Piagkou, G. Skotsimara, G. Piagkos, P. Skandalakis, A 2012.

morphometric anatomical and comparative study of the foramen magnum [60] P. Murail, J. Bružek, F. Houët, E. Cunha, DSP: a tool for probabilistic sex
region in a Greek population, Surg. Radiol. Anat. 35 (2013) 925–934, doi:http:// diagnosis using worldwide variability in hip-bone measurements, Bull.
dx.doi.org/10.1007/s00276-013-1119-z. Mémoires La Société d’Anthropologie Paris 17 (2005) 167–176.
Z. Seifert et al. / Forensic Science International 271 (2017) 126.e1–126.e9 126.e9

[61] D. Franklin, A. Cardini, A. Flavel, A. Kuliukas, Estimation of sex from cranial [82] B. Hallgrimson, M.L. Zelditch, T.E. Parsons, E. Kristensen, N.M. Young, S.K. Boyd,
measurements in a Western Australian population, Forensic Sci. Int. 229 Morphometrics and biological anthropology in the postgenomic age, in: M.A.
(2013) 158.e1–158.e8, doi:http://dx.doi.org/10.1016/j.forsciint.2013.03.005. Katzenberg, S.R. Saunders (Eds.), Biological Anthropology of Human Skeleton,
[62] C. Zaiontz, Real Statistics Resource Pack, (2015) . http://www.real-statistics.com. John Wiley & Sons, Hoboken, 2007, pp. 207–236.
[63] P. Gruber, M. Henneberg, T. Boni, F.J. Ruhli, Variabilityof human foramen magnum [83] C. Dawson, D. Ross, X. Mallett, Sex determination, in: S.M. Black, E. Ferguson
size, Anat. Rec. 292 (2009) 1713–1719, doi:http://dx.doi.org/10.1002/ar.21005. (Eds.), Forensic Anthropology from 2000 to 2010, Taylor & Francis, Boca Raton,
[64] V. Saini, R. Srivastava, S.N. Shamal, T.B. Singh, V. Kumar, P. Kumar, S.K. Tripathi, 2011, pp. 61–94.
Temporal variations in basicranium dimorphism of North Indians, Int. J. Leg. [84] F.P. Schulter-Ellis, L.C. Hayek, D.J. Schmidt, Determination of sex with a
Med. 128 (2013) 699–707, doi:http://dx.doi.org/10.1007/s00414-013-0957-x. discriminant analysis of new pelvic bone measurements: part II, J. Forensic Sci.
[65] W. Bilkfelner, Applied Medical Image Processing. A Basic Course, 2nd ed., (1985) 178–185.
Taylor & Francis, Boca Raton, 2014. [85] H. Coqueugniot, J.-M. Le Minor, Fermeture des synchondroses intra-
[66] N. Sugano, T. Sasama, Y. Nakajima, Y. Sato, T. Nishii, T. Iida, K. Nakagawa, K. Ono, occipitales: implication dans la configuration du foramen magnum, C. R.
S. Nishihara, S. Tamura, K. Yonenobu, T. Ochi, Effects of CT threshold value to Palevol. 1 (2002) 35–42.
make a surface bone model on accuracy of shape-based registration in CT- [86] S.R. Saunders, Juvenile skeletons and growth-related studies, in: M.A.
based navigation system for hip surgery, Int. Congr. Ser. 1230 (2001) 319–324. Katzenberg, S.R. Saunders (Eds.), Biological Anthropology of Human Skeleton,
[67] S. Acton, N. Ray, Biomedical Image Analysis: Segmentation, Synthesis Lectures John Wiley & Sons, Hoboken, 2007, pp. 117–147.
on Image, Video, and Multimedia Processing, vol. 4(2009), pp. 1–108, doi: [87] D.H. Ubelaker, Issues in forensic anthropology, in: C.S. Larsen (Ed.), A
http://dx.doi.org/10.2200/S00133ED1V01Y200807IVM009. Companion to Biological Anthropology, 2010, pp. 412–426.
[68] S.N. Bhadoria, P. Aggarwal, C.G. Dethe, R. Vig, Comparison of segmentation [88] P. Guyomarc’h, J. Velemínská, P. Sedlak, M. Dobisíková, I. Švenkrtová, J.

tools for multiple modalities in medical imaging, J. Adv. Inf. Technol. 3 (2012) Bružek, Impact of secular trends on sex assessment evaluated through
197–205, doi:http://dx.doi.org/10.4304/jait.3.4.197-205. femoral dimensions of the Czech population, Forensic Sci. Int. 262 (2016)
[69] J.S. Suri, D. Wilson, S. Laxminarayan, Handbook of Biomedical Image Analysis 284.e1–284.e6, doi:http://dx.doi.org/10.1016/j.forsciint.2016.02.042.
II, Springer Science & Business Media, 2005. [89] A. Kote rová, J. Velemínská, J. Dupej, H. Brzobohatá, A. Pilný, J. Bru žek,
[70] K. Rathnayaka, T. Sahama, M.A. Schuetz, B. Schmutz, Effects of CT image Disregarding population specificity: its influence on the sex assessment
segmentation methods on the accuracy of long bone 3D reconstructions, Med. methods from the tibia, Int. J. Leg. Med. (2016) 1–11, doi:http://dx.doi.org/
Eng. Phys. 33 (2011) 226–233, doi:http://dx.doi.org/10.1016/j.medeng- 10.1007/s00414-016-1413-5.
phy.2010.10.002. [90] S.D. Ousley, R.L. Jantz, Fordisc 3 and statistical methods for estimating sex and
[71] T.M. Nassef, New segmentation approach to extract human mandible bones ancestry, in: D.C. Dirkmaat (Ed.), A Companion to Forensic Anthropol, 1st ed.,
based on actual computed tomography data, Am. J. Biomed. Eng. 2 (2012) 197– Blackwell Publishing, 2012, pp. 311–321.
201, doi:http://dx.doi.org/10.5923/j.ajbe.20120205.01. [91] T. Sjøvold, Geschlechtsdiagnose am skelett, in: R. Knussman (Ed.), Anthro-
[72] M. Salas, S. Maddock, A 3D MRI Skull Segmentation Method Based on pologie. Handbuch der vergleichenden Biologie des Menschen, Band 1; 1. Tl,
Deformable Models, Department of Computer Science Research Memoran- Gustav Fisher Verlag, Stuttgart, 1988, pp. 444–480.
dum CS-09-10, University of Sheffield, 2009. [92] C. Shanthi, S. Lokanadham, Morphometric study on foramen magnum of
[73] H. Scherf, R. Tilgner, A new high-resolution computed tomography (CT) human skulls, Med. Sci. Int. Med. J. 2 (2013) 792–798, doi:http://dx.doi.org/
segmentation method for trabecular bone architectural analysis, Am. J. Phys. 10.5455/medscience.2013.02.8079.
Anthropol. 140 (2009) 39–51, doi:http://dx.doi.org/10.1002/ajpa.21033. [93] E. Kranioti, J. García-Donas, H. Langstaff, Sex estimation of the Greek mandible
[74] F.C. Spoor, F.W. Zonneveld, G.A. Macho, Linear measurements of cortical bone with the aid of discriminant function analysis and posterior probabilities, Rom.
and dental enamel by computed tomography: applications and problems, Am. J. Leg. Med. 22 (2014) 101–104.
J. Phys. Anthropol. 91 (1993) 469–484, doi:http://dx.doi.org/10.1002/ [94] K.M. Lesciotto, The impact of Daubert on the admissibility of forensic
ajpa.1330910405. anthropology expert testimony, J. Forensic Sci. 60 (2015) 549–555, doi:http://
[75] B. Dutailly, H. Coqueugniot, P. Desbarats, S. Gueorguieva, R. Synave, 3D surface dx.doi.org/10.1111/1556-4029.12740.
reconstruction using HMH algorithm, 16th IEEE International Conference on [95] A.R. Klales, S.D. Ousley, J.M. Vollner, A revised method of sexing the human
Image Processing (ICIP) (2009) 2505–2508. innominate using Phenice’s nonmetric traits and statistical methods, Am. J.
[76] W.E. Lorensen, H.E. Cline, Marching cubes: a high resoluion 3D surface Phys. Anthropol. 149 (2012) 104–114, doi:http://dx.doi.org/10.1002/
construction algorithm, ACM Siggraph Comp. Graph. 21 (4) (1987) 163–169. ajpa.22102.
[77] Y. Sahillioglu, Marching Rhombic Dodecahedra, (2008) . [96] R. Gapert, S. Black, J. Last, Sex determination from the occipital condyle:
[78] T. Moench, S. Adler, B. Preim, Staircase-Aware Smoothing of Medical Surface discriminant function analysis in an eighteenth and nineteenth century British
Meshes, (2010), doi:http://dx.doi.org/10.2312/VCBM/VCBM10/083-090. sample, Am. J. Phys. Anthropol. 138 (2009) 384–394, doi:http://dx.doi.org/
[79] G.D. Richards, R.S. Jabbour, Foramen magnum ontogeny in Homo sapiens: a 10.1002/ajpa.20946.
functional matrix perspective, Anat. Rec. 294 (2011) 199–216, doi:http://dx. [97] R. Knußmann, Anthropologie, Band I: Wesen und Methoden der Anthro-
doi.org/10.1002/ar.21319. pologie. 1. Teil: Wissenschaftstheorie, Geschichte, morphologische Methoden.
[80] K.E. Stull, M.L. Tise, Z. Alie, D.R. Fowler, Accuracy and reliability of Handbuch der vergleichenden Biologie des Menschen, G. Fischer Verlag,
measurements obtained from computed tomography 3D volume rendered Stuttgart, 1988.
images, Forensic Sci. Int. 238 (2014) 133–140, doi:http://dx.doi.org/10.1016/j. [98] W.W. Howells, Cranial Variation in Man. A Study by Multivariate Analysis of
forsciint.2014.03.005. Patterns of Differences Among Recent Human Populations, (1973) Papers of
[81] A.H. Richard, C.L. Parks, K.L. Monson, Accuracy of standard craniometric Peabody Museum Cambridge, MA.
measurements using multiple data formats, Forensic Sci. Int. 242 (2014) 177–
185, doi:http://dx.doi.org/10.1016/j.forsciint.2014.06.015.