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THE ANATOMICAL RECORD 300:1609–1617 (2017)

Frontal Sinus Development and


Juvenile Age Estimation
KAITLIN MOORE* AND ANN ROSS
Sociology & Anthropology, North Carolina State University, North Carolina

ABSTRACT
Assessment of development is an important component of age estima-
tion in juveniles. One area that has not been fully investigated as a possi-
ble aging method is the development of the frontal sinus. The frontal
sinuses form when the ectocranial table of the frontal bone separates
from the endocranial table forming an air pocket in the bone. The endo-
cranial table ceases growth with the brain, while the ectocranial table is
displaced anteriorly as the facial bones continue growth. In order to
examine growth and the utility of the frontal sinuses for age estimation,
392 radiographs were examined ($5159 and #5233) from the Juvenile
Radiograph Database at North Carolina State University and the Patricia
Database from Mercyhurst University. The sample included individuals
who ranged in age from 0 to 18 years. Anterior view (or AP) radiographs
were examined and were grouped based upon the presence or absence of
the frontal sinus. Individuals were grouped into four age categories. A
one-way ANOVA was performed to test whether developmental phase was
related to age. Results from the ANOVA show that developmental phase
is significantly related to age (P <.0001). An ordinal logistic regression
was conducted to examine whether developmental phase could be used to
predict age. The results of the logistic regression suggest that develop-
mental phase is an accurate indicator of age (P <.0001, df 5 1, Chi-
Squared 5 537.2428); however, the age ranges can be quite wide and
should be utilized alongside other established methods of age estimation.
Anat Rec, 300:1609–1617, 2017. V C 2017 Wiley Periodicals, Inc.

Key words: frontal sinus; development; age estimation;


juvenile

The frontal sinus is an air filled cavity located on the as young as two years of age; however, they often are not
frontal bone of the skull. It consists of bilateral sinuses visible radiographically until approximately six years of
separated by a bony septum, which is located in the pos- age (Enlow and Hans, 1996; Dixon et al., 1997; Tatlisu-
terior portion of the supercilliary ridge between the mak et al., 2008; da Silva et al., 2009; Verma et al., 2015).
endocranial and ectocranial tables of the frontal bone Growth continues through puberty, extending beyond the
(Elnow and Hans, 1996; Dixon et al., 1997; Standring, middle part of the supercilliary ridge and towards the
2008). The frontal sinus is lined with a moist mucosal
membrane that acts as a humidifier to warm air as it is
breathed in (McLaughlin et al., 2001; Verma et al., *Correspondence to: Kaitlin M. Moore, North Carolina State
2015). University, Sociology and Anthropology, 10 Current Drive Cam-
Unlike the other sinuses, the frontal sinus is absent at pus Box 8107, Raleigh, North Carolina 27695. E-mail:
birth (Enlow and Hans, 1996; Ponde et al., 2003; Standr- kmmoor10@ncsu.edu
ing, 2008; Tatlisumak et al., 2008; da Silva et al., 2009; Received 10 May 2016; Revised 8 December 2016; Accepted
Tabor et al., 2009). The frontal sinus begins to form as two 20 December 2016.
small pea shaped pockets located above the orbits on DOI 10.1002/ar.23614
either side of the osteometric point glabella (Gagliardi Published online 19 May 2017 in Wiley Online Library
et al., 2004). The sinuses can begin forming in individuals (wileyonlinelibrary.com).

C 2017 WILEY PERIODICALS, INC.


V
1610 MOORE AND ROSS

Fig. 1. Radiograph depicting an individual with frontal sinuses that are absent (birth to 5 years). Radiograph from Patricia (Pediatric Radiology
Interactive Atlas).
FRONTAL SINUS DEVELOPMENT IN JUVENILE 1611

Fig. 2. Radiograph of an individual during the initial stage of frontal sinus development (age 6–7). The sinuses are circled in red. Radiograph
from Patricia (Pediatric Radiology Interactive Atlas).

medial portion of the orbital roof (Ponde et al., 2003; Mar- regulated. Development is influenced by both brain
ques et al., 2014; Verma et al., 2015). Growth ceases at expansion and the growth of the midfacial region (Enlow
about 20 years of age, when the shape and size of the and Hans, 1996; Dixon et al., 1997). The skull grows
sinus become stable (Tabor et al., 2009). rapidly from birth to age seven in order to compensate
The mechanisms that are responsible for the develop- for rapid brain growth (Standring, 2008). During this
ment and expansion of the frontal sinus are highly time, the endocranial table of the frontal bone is
1612 MOORE AND ROSS

Fig. 3. Radiograph depicting an individual during the initial stage of frontal sinus expansion (age 8–10). The sinus is circled in red. Radiograph
from Patricia (Pediatric Radiology Interactive Atlas).
FRONTAL SINUS DEVELOPMENT IN JUVENILE 1613
signaled by surrounding tissue to grow to provide space years of age. For this study, only juveniles under the age
for the expansion of the brain (Enlow and Hans, 1996). of 18 were considered. This database can also be
The tables of the frontal bone begin to separate. When accessed via the web at http://math.mercyhurst.edu/
brain growth slows, at approximately six years of age, ~sousley/databases/radiographic_database/.
the endocranial table of the frontal bone ceases to grow Several radiographs were received directly from the
and adopts the general shape of the brain (Enlow and North Carolina Office of the Chief Medical Examiner in
Hans, 1996; Dixon et al., 1997). This growth period Raleigh, North Carolina. These radiographs were
accounts for the beginning stages of frontal sinus obtained to increase the sample size of individuals
development. between the age of five and ten years, all of which were
A second period of rapid growth in the skull takes from cases prior to 2013.
place at the onset of puberty (Standring, 2008). While Radiographs were considered for inclusion in this
there is growth in every direction of the skull, this study if they were anterior views and if there was no
period is generally associated with rapid growth of the trauma to the frontal bone. Both males and females
midfacial region (Standring, 2008). During this time, the were considered for inclusion, as were individuals of
nasomaxillary complex of the face is remodeled and dis- varying ancestral origins. Radiographs were excluded if
placed anteriorly and inferiorly, and the ectocranial table the image was overexposed, making it difficult to distin-
of the frontal bone is similarly displaced (Enlow and guish between anatomical structures. A total of 392 indi-
Hans, 1996; Dixon et al., 1997; Standring, 2008). This viduals were included from these three sources (# 5 233,
displacement causes further separation between the two $ 5 159).
tables of bone. The medullary bone between the tables is The radiographs that were selected for this study first
resorbed, allowing for the growth of the sinus (Enlow underwent a visual assessment. The age, sex, and ances-
and Hans, 1996). Expansion continues until the sinus tral groups were recorded as were the presence or
occupies all the space between the two tables of bone absence of the frontal sinus. If the frontal sinus was pre-
that was not being functionally utilized (Enlow and sent, the shape and extent of the expansion of the sinus,
Hans, 1996). both laterally and superiorly, were recorded. The radio-
Frontal sinus shape is unique to each individual graphs were then scored numerically based on the size
(Schuller, 1921). Many studies have examined the and shape of the frontal sinus.
uniqueness of its shape, all of which have concluded Individuals with no sign of frontal sinus development
that no two are alike (Schuller, 1921; Tang et al., 2009). were scored as a 0. Radiographs from these individuals
Studies including monozygotic twins have also found had frontal bones that appeared solid and uniform with
that the frontal sinus shape differs considerably (Uth- no areas of radiolucency visible above the orbits (Fig. 1).
man et al., 2010). One study examined the size and The ages of these individuals ranged from birth to age
shape of the frontal sinus among kin groups and found five.
that less than 2% of the individuals had similarly Individuals in the first stage of frontal sinus develop-
shaped frontal sinuses (Chaiyasate et al., 2007; Camer- ment also had frontal bones that appeared solid and uni-
iere et al., 2008; Tabor et al., 2009). form, but with two small, kidney bean shaped areas of
Though much research has been done on the heritabil- radiolucency on the medial portion of the superior bor-
ity of and identification from frontal sinus shape, little der of the orbits near the anatomical landmark glabella.
research has been done examining frontal sinus develop- This stage of development was scored as 1 and appeared
ment and its association with age. Research that does in individuals between six and seven years of age (Fig.
exist tends to focus on volume of the frontal sinus in 2).
relation to age and utilizes adults rather than juveniles. Individuals between the ages of eight and ten years
The purpose of this study is to more fully explore the old were in the initial stage of frontal sinus expansion.
development of the frontal sinus and to test whether it In these individuals, the two areas of radiolucency had
could be a skeletal parameter for juvenile age expanded medially and laterally, but were still in the
estimation. glabella region of the frontal bone (Fig. 3). These indi-
viduals were scored as 2.
MATERIALS AND METHODS The final stage of development encompassed individu-
als from 11 to 18 years of age. Individuals in this stage
Radiographs from three different locations were uti- showed fully formed frontal sinuses and were scored as
lized for this study. The samples from the North Caro- 3. The sinus was larger and more cavernous and
lina State University Juvenile Radiographic Database expanded laterally and superiorly on the frontal bone
(NIJ 2010-DN-BX0K214) were comprised of radiographs (Fig. 4).
obtained from the North Carolina Office of the Chief
Medical Examiner. The database contains individuals
Statistical Analysis
from birth to 18 years of age who died between 1974 and
2002. The database was amassed by the second author A one-way analysis of variance (ANOVA) was per-
and the data are freely available at https://sites.google. formed on the sample with phase as the independent
com/a/ncsu.edu/radiograph-database-project/. variable and age as the dependent variable. In addition,
The Patricia database (Pediatric Radiology Interactive a Tukey-Kramer adjustment for multiple comparisons
Atlas), compiled by Mercyhurst University, was also uti- was used to determine if the mean ages of each phase
lized for this study (NIJ 2008-DN-BX-K152). This data- category were significantly different from one another.
base includes radiographs from over 20 locations across Finally, the data were fit in a logistic regression to
the country, including two clinical locations. Patricia assess if developmental phase was an accurate predictor
contains radiographs of individuals from birth to 21 of age. A logistic regression was utilized because it can
1614 MOORE AND ROSS

Fig. 4. Radiograph of an individual with a fully formed frontal sinus (age 11–18). The sinus is circled in red. Adapted from Patricia (Pediatric
Radiology Interactive Atlas).
FRONTAL SINUS DEVELOPMENT IN JUVENILE 1615
TABLE 1. Distribution of sample by sex and ancestry TABLE 2. Classification matrix of actual phase by
predicted phase
Ancestry Male Female Total
Actual Phase Predicted
European Americans 114 84 198
African Americans 68 45 113 0 1 2 3
Hispanic Americans 31 16 47 0 98% 0.74% 0.74% 0.37%
Native Americans 6 5 11 1 43% 33% 23% 0%
Asian Americans 3 2 5 2 12.50% 33% 50% 0
Indian Americans 1 0 1 3 0 0 2.38% 97.60%
Unknown 10 7 17
Total 233 159 392

TABLE 3. Prediction profile results showing the prob-


abilities of age and phase
Probability of Phase by age
Age 0 1 2 3
0–1 100%
2–4 95%
5 83% 15%
6 61% 32%
7 37% 46% 18%
8 15% 44% 36%
9 11% 28% 55%
10 12% 58% 28%
11 42% 53%
12 22% 76%
13 9% 90%
14 96%

Only ages 0–14 are presented.

These individuals spanned different ages and different


ancestral groups.
Fig. 5. Box plot depicting the spread and mean ages for each In this sample, there were 271 individuals who had
developmental phase. no signs of frontal sinus development, 21 individuals in
the beginning stages of growth, 16 showing the initial
spread of the frontal sinus, and 84 individuals with fully
be applied to both continuous and categorical variables
formed frontal sinuses. Figure 5 depicts a box plot of the
and does not require an underlying assumption of nor-
age distribution for each developmental phase.
mality to be met (Fournier and Ross, 2015).
The ANOVA procedure indicated a statistically signifi-
The data were first fit with an ordinal logistic regres-
cant relationship between the age and the development
sion with both sex and age as dependent variables and
stage of the frontal sinus (df 5 2, SS 5 13420.032,
developmental phase as the independent variable. Sex
4473.33, F Ratio 5 1325.666, Prob > F <.0001).
was not found to have a significant effect on the develop- The Tukey-Kramer adjustment showed that phase 0 is
mental phase, so the model was refit, excluding sex as a significantly different than phases 1–3 (P-value5
parameter. All statistical analyses were performed in <.0001). However, phase 1 is not significantly different
JMP Pro 12.0.1 (SAS 2015). than phase 2 (P -value 5 0.1179), but it is significantly
different from phase 0 and phase 3 (P-value 5 <.0001),
and phase 3 is significantly different from phase 0–2
RESULTS
(P-value 5 <.0001).
Simple statistics were calculated using Microsoft The logistic regression showed that sex did not have a
Excel VR (Table 1). Bilateral absence of the frontal sinus, significant effect on developmental phase (P-val-
or absence of both sides of the sinus, was observed in ue 5 0.9310). The model was refit, excluding sex as a
eight individuals who were over age six. Seven of these parameter. The logistic regression results suggested that
individuals were between the ages of six and eight this model is useful for predicting age in juvenile indi-
years. Because it is generally agreed upon that frontal viduals (ChiSq 5 537.24, df 5 1, P-value <.0001). The
sinuses become visible in radiographs around age six, area under the Receiver Operating Characteristic (ROC)
the absence of the sinus could not be confirmed in these curve was .99 for each of the developmental phases, indi-
seven individuals as they could have been developmen- cating a strong separation between the phases. The mis-
tally delayed. However, one individual was well into classification rate for the model was 0.07%. Table 2
their teens and thus, was the only individual in which presents the classification matrix, which shows that for
bilateral absence of the frontal sinus could be confirmed. phase 0 the misclassification rate is 0.01%, for phase 3 it
Unilateral absence of the frontal sinus was observed is 0.02% with the highest misclassification rates falling
in 0.2% of the sample (nine individuals). In all nine of in phases 1 and 2, which is most likely because of the
these individuals, the right side of the sinus was absent. relatively small sample size in these two phases.
1616 MOORE AND ROSS

A prediction profiler, which measures the predictive periods experience the highest rates of homicides, they
response as one variable is changed (in this case age) make up the bulk of the radiographs in this sample.
while the other (phase) is held constant, was also used Juveniles aged 6 to 12 years have homicide rates lower
in the logistic regression to provide probabilities for each than any other subset of the US population (Finkelhor
age being a specific phase (Table 3). The prediction pro- and Ormrod, 2001). Because this age range has the low-
filer showed that juveniles do not develop frontal sinuses est homicide rates, there were very few postmortem
between 0 and 4 years of age. They begin to develop a radiographs from this group included in this study
frontal sinus between 5 and 6, they transition from sample.
phase 0 to 3 between 7 and 9 years of age. At 10 years Future directions would include radiographs or medi-
of age they transition between phase 1 and 3 and transi- cal scans of clinical data. This would increase the sample
tion between phase 2 and 3 between the ages of 11 and size overall, but more importantly would increase the
13. Finally there is a 96% probability that the frontal number of radiographs for the 6 to 12 year old age
sinus is fully developed by age 14. range. A larger sample size would allow for a more in
depth analysis of the age ranges and perhaps would
DISCUSSION allow for the identification of more phases of develop-
ment with narrower associated age ranges.
Frontal sinus development and growth is strongly
Although the results of this study indicate that frontal
associated with specific age related periods of skull
sinus development can be an accurate indicator of age,
growth. These periods of growth are detectable with the
phases of frontal sinus development as examined in this the ranges observed in this study span several years.
study. Frontal sinus absence of phase 0 was observed Stages 1 and 2 provide the narrowest age ranges, span-
after birth and during the initial growth period of the ning two and three years, respectively. The largest age
skull. Though the endocranial table of the frontal bone range is seen in stage 3, which spans eight years. This
was being remodeled to support brain expansion, the may limit the usefulness of frontal sinus development as
sinus was not radiographically visible. The sinus only an age indicator in juveniles older than 11. However,
became visible in radiographs towards the end of the this study does show that by age 14 the frontal sinuses
first period of skull growth. Coincidentally, this is the are fully formed in this sample and the older age bracket
time when the endocranial table ceases growing and con- could be tightened.
forms to the general shape of the brain. This first phase The primary use of the frontal sinus in medico-legal
of development was not observed in individuals younger contexts has been the identification of unknown individ-
than six years of age, which conforms to what most of uals. In this arena, it has proven to be extremely useful,
the clinical literature reported about frontal sinuses not boasting up to 100 percent accuracy in identifying indi-
being visible in radiographs of juveniles younger than viduals (Besana and Rogers, 2010). However, the growth
six years of age (Enlow and Hans, 1996; Dixon et al., of the frontal sinus and its link to age has largely been
1997; da Silva et al., 2009; Verma et al., 2015). ignored. This study shows that frontal sinus develop-
The second phase of frontal sinus development as ment can be utilized to accurately predict age in suba-
defined in this study coincides to the timespan between dults. This may prove useful in cases of fragmented or
the primary and secondary periods of skull growth. This incomplete remains that make traditional methods of
occurs in the years leading up to puberty, during a time age estimation difficult. Until further work can be done
in which frontal sinus growth is slow and steady (Ponde to narrow the age ranges associated with each develop-
et al., 2003). mental stage, this method should be used with caution
The third phase of development, fully formed frontal and alongside existing methods of juvenile age
sinuses, occurs when an individual enters puberty. As estimation.
this is the period of time when much of the facial growth
occurs, this phase shows the most dramatic change ACKNOWLEDGMENTS
between the developmental phases.
While this study provides valuable information The authors would like to thank the North Carolina
regarding the use of the frontal sinuses to estimate age, Office of the Chief Medical Examiner and specifically
there were some shortcomings. Mr. Clyde Gibbs for providing the radiographs used in
The sources used for this study obtained the majority this study. And we thank Dr. Beth Murnane, the second
of their radiographs through medical examiners, indicat- author’s son’s pediatrician, for fruitful discussions of
ing that these individuals were either homicide victims frontal sinus development in children.
or experienced death under suspicious circumstances.
According to the Crimes Against Children Research Cen-
ter, there are two major periods in life during which LITERATURE CITED
juveniles experience a high risk of homicide. In young Besana JL, Rogers TL. 2010. Personal identification using the fron-
children, individuals under the age of one year have the tal sinus*. J Forensic Sci 55:584–589.
highest homicide rate with a slight decline until age six Cameriere R, Ferrante L, Molleson T, Brown B. 2008. Frontal sinus
accuracy in identification as measured by false positives in kin
(Finkelhor and Ormrod, 2001). These homicides are usu-
groups. J Forensic Sci 53:1280–1282.
ally committed by family members. The second period of Chaiyasate S, Baron I, Clement P. 2007. Analysis of paranasal sinus
high homicide rates in juveniles begins at age 12 with a development and anatomical variations: A CT genetic study in
steep increase during the late teen years (Finkelhor and twins. Clin Otolaryngol 32:93–97.
Ormrod, 2001). High rates of homicide in teens are asso- da Silva RF, Prado FB, Caputo IGC, Devito KL, de Luscena Botelho
ciated with poverty, gang activity, and drug-related vio- T, Junior ED. 2009. The forensic importance of frontal sinus
lence (Finkelhor and Ormrod, 2001). As these time radiographs. J Forensic Leg Med 16:18–23.
FRONTAL SINUS DEVELOPMENT IN JUVENILE 1617
Dixon AD, Hoyte DA, Ronning O. 1997. Fundamentals of craniofa- Schuller A. 1921. Das rontgenogram der stirnhohle: ein hilfsmittel
cial growth. Boca Raton: CRC Press f€
ur die identit€atsbestimmung von schadeln. Monatsschr Ohren-
Enlow DH, Hans MG. 1996. Essentials of facial growth. Philadel- heilkd Laryngorhinol 5:1617–1620.
phia: Saunders. Standring S. 2008. Gray’s Anatomy: The basis of clinical practice.
Finkelhor D, Ormrod R. 2001. Homicides of Children and Youth. Edinburgh: Churchill Livingstone/Elsevier.
US Department of Justice Office of Juvenile Justice and Delin- Tabor Z, Karpisz D, Wojnar L, Kowalski P. 2009. An automatic rec-
quency Prevention. ognition of the frontal sinus in x-ray images of skull. IEEE Trans
Fournier NA, Ross AH. 2015. Sex, ancestral, and pattern type vari- Biomed Eng 56:361–368.
ation of fingerprint minutiae: A forensic perspective on anthropo- Tang J, Hu D, Jiang F, Yu X. 2009. Assessing forensic applications
logical dermatoglyphics. Am J Phys Anthropol 160: 625–632. of the frontal sinus in a chinese han population. Forensic Sci Int
Gagliardi A, Winning T, Kaidonis J, Hughes T, Townsend G. 2004. 183:104. e1–104. e3.
Association of frontal sinus development with somatic and skele- Tatlisumak E, Ovali GY, Asirdizer M, Aslan A, Ozyurt B, Bayindir
tal maturation in aboriginal australians: A longitudinal study. P, Tarhan S. 2008. CT study on morphometry of frontal sinus. Cli-
HOMO 55:39–52. nAnat 21:287–293.
Marques JAM, de Oliveira Musse J, Gois BC, Galv~ ao LCC, Paranhos Uthman AT, Al-Rawi NH, Al-Naaimi AS, Tawfeeq AS, Suhail EH.
LR. 2014. Cone-beam computed tomography analysis of the frontal 2010. Evaluation of frontal sinus and skull measurements using
sinus in forensic investigation. Int J Morphol 32:660–665. spiral CT scanning: An aid in unknown person identification.
McLaughlin RB, Rehl RM, Lanza DC. 2001. Clinically relevant frontal Forensic Sci Int 197:124. e1–124. e7.
sinus anatomy and physiology. Otolaryngol Clin North Am 34:1–22. Verma P, Verma KG, Khosa R, Kumar S, Basavaraju S,
Ponde JM, Metzger P, Amaral G, Machado M, Prandini M. 2003. Patwardhan N. 2015. Combined use of frontal sinus and nasal
Anatomic variations of the frontal sinus. Minim Invasive Neuro- septum patterns as an aid in forensics: A digital radiographic
surg 46:29–32. doi:10.1055/s-2003-37956 [doi] study. North Am J Med Sci 7:47.

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