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Evaluaon of Morphological Variaons in Tympanic Poron of Temporal Bone in
Dogs
Semra ÇINAR1* , Figen SEVİL-KİLİMCİ1, Mehmet Erkut KARA1
1Department of Anatomy, Faculty of Veterinary Medicine, Aydin Adnan Menderes University, Aydin, Turkey
ABSTRACT
In this study, it was aimed to examine the relaonship between the morphometric-geometric features of the external
acousc meatus, tympanic bulla, and auditory tube and the cranium shape, age, gender, and race characteriscs in
the os temporale region in terms of the clinical-anatomical approach to the outer ear and middle ear regions of the
dog’s skull. A total of 110 dogs’ skulls were used. The bones were photographed in three dierent views with the
camera. The morphometric data on the skull, angle measurements, and index values related to them were calculated
in obtained images. Auditory tube angle and external acousc meatus angle were found to dier stascally among
the age groups. In addion, it was determined that the index values of bulla tympanica, except for the height index,
showed stascal dierences among age groups. When the angle measurements and index values of the skulls of
male and female animals were examined, it was determined that other index values did not dier between female
and male dogs, except for the external acousc meatus angle. As a result, it can be said that age and skull type is more
eecve than gender in the posioning of the tympanic region in dogs. The results of this research are supporve
informaon that can be used in both clinical and zooarchaeological studies on the tympanic bulla region on dogs.
Keywords: Bulla tympanica, dog, morphometry, temporal bone, tuba audiva
Köpeklerde Temporal Kemiğin Pars Tympanica’sındaki Morfolojik Varyasyonların
Değerlendirilmesi
ÖZET
Bu çalışmada, köpeklerin kafatasının dış kulak ve orta kulak bölgelerine anatomik yaklaşım ve klinik açıdan meatus
acuscus externus, bulla mpanica ve tuba audiva’nın morfometrik-geometrik özellikleri ile os temporale
bölgesindeki kafatası şekli, yaş, cinsiyet ve ırk özellikleri arasındaki ilişkinin incelenmesi amaçlanmışr. Çalışmada
toplam 110 adet köpek kafatası üzerinde çalışılmıştır. Kemiklerin üç farklı yönde fotoğraarı çekildi. Elde edilen
görüntülerde kafa ile ilgili bazı morfometrik veriler, açı ölçümleri ve bunlara ilişkin indeks değerleri hesaplandı. Tuba
audiva açısı ve meatus acuscus externus açısı yaş grupları arasında istasksel olarak farklılık görüldü. Ayrıca bulla
mpanika indeks değerlerinin boy indeksi dışında yaş grupları arasında istasksel olarak farklılık gösterdiği belirlendi.
Dişi ve erkek hayvanların kafataslarının açı ölçümleri ve indeks değerleri incelendiğinde, meatus acuscus externus
açısı dışındaki diğer indeks değerlerinin dişi ve erkek hayvanlar arasında farklılık göstermediği belirlendi. Sonuç
olarak köpeklerde mpanik bölgenin pozisyonunda, yaş ve kafa pinin cinsiyeen daha etkili olduğu söylenebilir.
Bu araşrmanın sonuçları köpeklerde bulla mpanica bölgesi ile ilgili hem klinik hem de zooarkeolojik çalışmalarda
kullanılabilecek destekleyici bilgilerdir.
Anahtar kelimeler: Bulla tympanica, köpek, morphome, temporal kemik, tuba audiva
*Corresponding Author: Semra ÇINAR, Department of Anatomy, Faculty of Veterinary Medicine, Aydin Adnan Menderes University, Aydin,
Turkey. e-mail: veterinariansemra@gmail.com
Received Date: 05.10.2021 Accepted Date: 24.11.2021
DOI: 10.53913/aduveterinary.1005009
Animal Health Prod and Hyg (2021) 10 (2) : 39 - 44
Research Arcle
Research Arcle
Çınar et al Morphological Variaons in Tympanic Poron of Temporal Bone in Dogs
.
40
Introducon
Morphometric studies of the skull can be done to
determine species, race or sex characteriscs (Onar,
1999; Onar and Gunes, 2003; Schmidt et al., 2011), as
well as to form the basis of clinical approaches in various
regions (Fox, 1964; Schmidt et al., 2011; Schmidt et al.,
2013) is important. One of the most common ailments
of dogs seen in veterinary medicine is ear disease. About
15%-20% of all canine paents have ear problems, which
can range from mild erythema to severe os media
(Louis, 2004). The temporal bone, which parcipates in
the formaon of a part of the lateral and base wall of the
cavum cranii, is an important bone in terms of clinical
applicaons, as some important vessels and nerves pass
through it, arculates with the mandible, and forms the
bony roof of the ear. In the middle of pars tympanica of
the os temporale external hole of the meatus acouscs
externus osseous is located. External acousc meatus
(external ear canal) is a tubular path which it is extending
from concha auriculare to membrana tympanica and
obliquely in dog (Evans, 1993; König, 2007; Njaa et al.,
2012). The membrana tympanica at the end of external
acousc meatus is located at an angle of approximately
45 degrees to the horizontal central axis of the external
acousc meatus in dogs, however, this angle may dier
according to dog breeds (Njaa et al., 2012). External
acousc meatus is closed in newborn kiens and
puppies. For this reason, although newborn puppies can
perceive some sounds, they cannot hear them properly.
Generally, the external ear canal opens between the 6th
and 14th days and the puppies begin to hear in the 3rd
week aer they are born (Samsar and Akın, 2006). Bony
enlargement called tympanic bulla located on the ventral
aspect of the pars tympanica is a structure that contains
the middle ear (Bahadır and Yıldız, 2004). The space in
the middle ear is called tympanic cavity and this space
is in conjuncon with the pharynx through the auditory
tube (Eustachian tube). Since the posion of the osseous
roof of the external auditory canal, mastoid part of
middle ear, and auditory tube, which is the funconal
unit of the ear, is related to various clinical approaches.
Many studies are conducted on the morphometric and
geometric features of the region (Mann et al., 1979;
Albiin, 1984; Djeric and Savic, 1985; Sadler-Kimes et
al., 1989; Kemaloğlu et al., 1996; Judkins and Li, 1997;
Sırıkçı et al., 2001). In clinical applicaons, posion of
the external auditory canal for otoscope applicaon and
locaon of the tympanic membrane during cleaning of
the ear canal must be taken into account (Njaa et al.,
2012). For example, the dorso-rostral border of the
external acousc meatus and the shape of the zygomac
process of the os temporale and the angle of the skull
to the long axis may show variaons in dierent skull
types of dogs. This is important in terms of placing the
autoendoscope deeper during video otoscope use in
procedures such as myringotomy (Njaa et al., 2012). In
addion, regarding the angle of the external auditory
canal with the tympanic annulus; provides an advantage
in washing the external ear, inserng and passing the
catheter into the horizontal ear canal, and collecng
the washing soluon and serum physiology without
damaging the tympanic membrane (Njaa et al., 2012).
Auditory tubeposion is considered to be the main cause
of middle ear inammaons (Mawson, 1974; Kemaloğlu
et al., 1996). The po sion of the Tympanic bulla and
auditory tube changes depending on age (Takeuchi ve
ark., 1980; Bluestone and Doyle, 1988; Kemaloğlu et al.,
1996)
Due to the common middle ear inammaons in
children, there are many studies on this subject both in
humans and animals (Sadler-Kimes, 1989; Judkins and
Li, 1997). For this reason, os temporale measurements
and their raos to ossa cranii measurements have gained
importance. Considering the changes in development
process of the studied measurements, it is seen that the
os temporale connues to develop together with the
ossa faciei unl it reaches maturity (Takeuchi ve ark.,
1980) and it has been revealed that the growth process
of the skull signicantly aects funcon of the auditory
tube (Mann et al., 1979). In these studies, change in the
shape, size and posion of the auditory tube with age
was also invesgated (Mann et al., 1979; Takeuchi et al.,
1980; Todd and Marn, 1988).
In literature review on the subject, detailed data
on various ear diseases in dogs and temporal bone
morphometry, which is important in terms of
examinaon, and variaons of this region depending on
race, age, gender, and skull shape were not found. In this
study, it was aimed to examine the relaonship between
the morphometric and geometric features of the external
acousc meatus, tympanic bulla and auditory tube and
the cranium shape, age, and gender characteriscs in the
os temporale region in terms of the clinical-anatomical
approaches to the outer ear and middle ear regions of
the dog’s skull.
Materials and Methods
In this study, dog skull bones obtained from the archive of
Adnan Menderes University Veterinary Faculty Anatomy
Department Osteometry Laboratory were used. A total
of 110 dogs (48 female, 59 male, 3 non-gendered)
were studied. In the absence of age records of the
animals (n:16), the approximate age of the animals was
determined according to the condion of their teeth and
sutures (Dyce et al. 2002; Thrall and Robertson, 2011;
Mihelic et al., 2013; Schmidt et al., 2013). Accordingly,
animals with an approximate age range of 1.5 months to
168 months were used.
In order to demonstrate the reliability of the method, the
cranium of a randomly selected dog was photographed
ve mes and all measurements were taken repeatedly
on these ve images of the same skull to calculate the
coecients of variaon (Özdamar, 2004).
Aer checking the validity and reliability of the
measurement method, photographic images of the
bones, which were placed on a at plaorm with the
Çınar et al Morphological Variaons in Tympanic Poron of Temporal Bone in Dogs
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41
help of play dough, were taken from the dorsal, lateral
and basal face with a Canon EOS 350D camera. A ruler
was placed during photographing for calibraon of the
images. Photographs were taken perpendicular to the
bone and focusing on the midpoint of the bone for all
posions. All obtained photos were transferred to the
computer in “.jpeg” format. Aer calibraon of the
transferred images in the “ImageJ” program, all the
measurements of skull bones were taken using necessary
commands in the “ImageJ” program”,
whose reference points were already
dened. (Figure 1-3, Table 1).
Stascal analyzes were performed
with the SPSS 19.0 program, and
normal distribuon of the data was
checked with the “Shapiro-Wilk
test”. In age and gender groups, an
intergroup comparison was checked
for independent variables by t-test.
The results were checked with the
Mann-Whitney test, which is a non-
parametric test for parameters that
did not show normal distribuon,
and the signicant (p) values were
wrien according to the results of
this test. Pearson correlaon analysis
method was used to determine
whether there was a correlaon
between the cranium index values
in the bones used and the index
and angle values obtained from the
pars tympanica region the data were
presented as the number of animals
in the group (n), mean value (MV),
and standard deviaon (SD) in tables.
The signicance level in the study
was accepted as p<0.05. Checking
the reliability of the measurement
method, the coecient of variaon
(%CV) of measurements was
calculated using the formula,
“(standard deviaon/mean value) x
100” (Özdamar, 2004).
Results
When the coecients of variaon
calculated for the measurement
method in the study were examined,
the lowest coecient of variaon
was found to be 0.18% in facial length
and skull width measurements, and
the highest coecient of variaon
was 1.96% in the measurement of
auditory tube angle.
Angle measurements and index
values of the young and adult age
groups are presented in Table 2.
Auditory tube angle and external
acousc meatus angle were found
to dier stascally between two
groups. In addion, it was determined that the index
values of bulla tympanica, except for the height index,
showed stascal dierences among age groups.
Angle measurements and index values of the skulls
of male and female animals are presented in Table 3.
According to these results, it was determined that other
index values did not dier between female and male
animals, except for the external acousc meatus angle.
Figure 1. Dorsal view of the skull and the measurements
Figure 2. Lateral view of the skull and the measurements
Figure 3. Basal view of the skull and the measurements
Çınar et al Morphological Variaons in Tympanic Poron of Temporal Bone in Dogs
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42
The correlaon coecients between cranial index values
and angle values measured from the pars tympanica
region are presented in Table 4. In parcular, it was
observed that there was a correlaon between the angle
of the auditory tube and the all skull indices. External
acousc meatus angle was found to have correlaon
only with bulla tympanica indices
Discussion
Before starng the study, ve images were taken from
the skull of an animal to the demonstrate reliability of
the method used and the measurements taken, and all
measurements were taken again from these images. It is
seen that the highest coecient of variaon was 1.96%
in the angle of Tuba audiva. According to these data,
since all coecients were below 5% value, it was seen
that the measurement method used in the study was
reliable (Özdamar 2004).
When index values of the tympanic bulla measurements
were examined, it was noted that the width and length of
the bulla were larger compared to the skull size in young
animals, but the height rao did not change with age. In
addion, it was determined that the angle of the auditory
Parameter Method Source
Lenght Values (mm)
Facial length FL Between nasion and prosthion EVANS (1993)
Cranial length CL Between Inion and nasion EVANS (1993)
Cranial width CW The widest interparietal width EVANS (1993)
Cranial height CH Lateral side from base of occipital condyle to highest point
of head EVANS (1993)
Skull width SW The widest interzygomac distance EVANS (1993)
Skull length SL FL+CL EVANS (1993)
Width of Bulla tympanica 1 BTW1 The largest diamater of the Bulla tympanica DRIESCH
(1976)
Width of Bulla tympanica 2 BTW2 The narrowest diamater of Bulla tympanica DRIESCH
(1976)
Heigth of Bulla tympanica BTH
The distance between the upper border of the porus acus-
cus externus and the ground contacng part of the bulla
tympanica
-
Angle
Values
(o)
Angle of tuba audiva TAA Angle of tuba audiva with transversal plane -
Angle of meatus acuscus externus MEA The angle between ventral border of porus acuscus exter-
nus and the transversal axis ALBIIN (1984)
Index Values (%)
Skull index SI SW x 100 /SL EVANS (1993)
Cranial index CI CW x 100 /CL EVANS (1993)
Facial index FI SW x 100 /FL EVANS (1993)
Width of Bulla tympanica 1 index BWI1 BTW1x100/SL -
Width of Bulla tympanica 2 index BWI2 BTW2x100/SW -
Heigth of Bulla tympanica index BHI BTHx100/CH -
Table 1. Idencaon of abbreviaons in the study
Young Adult p
Angular values (o) N MV±SD NMV±SD
Angle of tuba audiva 39 43.81±7.38 69 53.50±5.65 0.000***
Angle of meatus acuscus externus 39 48.34±5.32 69 45.75±5.86 0.021*
Index values (%)
Skull index 41 57.90±4.09 69 56.38±9.51 0.004**
Cranial index 41 75.69±10.02 69 57.90±10.67 0.000***
Facial index 41 156.67±27.05 69 126.69±26.80 0.000***
Width of bulla tympanica 1 index 41 16.86±4.411 69 12.28±1.34 0.000***
Width of bulla tympanica 2 index 41 13.44±4.02 69 8.93±1.10 0.000***
Heigth of bulla tympanica index 41 19.17±4.76 69 20.92±2.09 0.114
Table 2: Angular measurements and calculated index values of the skulls of animals in dierent age groups
p<0.05 * , p<0.01** , p<0.001***
Çınar et al Morphological Variaons in Tympanic Poron of Temporal Bone in Dogs
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43
tube with the transversal plane was approximately 18%
higher in adults than in young animals. The angle that
the porus acuscus externus makes with the transversal
axis is approximately 5% greater in young animals
than in adults. In this case, it is seen that the long axis
of the tympanic bulla rotates more rostro-medially
in the horizontal plane depending on age. While the
suturae-shaped secons of the occipital bone, which
largely surround the tympanic bone secons in the
skull posteriorly and laterally, are mostly closed by the
age of six months, the sphenoid bone and associated
synchondrosis type juncons anteriorly close aer one
year of age (Evans, 1993; Thrall and Robertson, 2011;
Schmidt et al., 2013). Since the facial bones connue to
grow at the front during these periods, it can be said that
the posion of the tympanic bone may show age-related
changes in this way.
Studies of sexual dimorphism in the closure of skull
sutures have shown that dierences in suture closure
can be seen in both male and female (Sahni et al., 2005;
Vijay et al., 2013; Alhadi et al., 2019). Since dierences
between males and females occur at dierent points
in the life cycle, a gender-related dierence in the
posion of tympanic region can also be expected due to
dierences in suture closure. However, according to the
results of this study, it was determined that other angle
and index values did not dier between female and male
animals, except for a small dierence in the external
acousc meatus angle in the dog.
It has been stated that the closure me of synchondrosis
type unions, which has the most important eect on
the longitudinal growth of the skull-shape, may vary
according to the skull-shape type or race (Schmidt et
al., 2013). The auditory tube angle measurement is
approximately the angle of the tympanic bulla long axis
with the transversal plane. It can be said that the long
axis of tympanic bulla may be more medially oriented in
dogs with longer head type, as this angle has negave
correlaons with skull indices. In addion, the medial
posion of the tympanic bulla increases as the bulla
height increases.
The most important limitaon of this study is the
insucient exact age informaon of the animals. For
this reason, animals esmated under one year of age,
which are considered to be young, could not be divided
into subgroups. The neurocranium (cranium) region of
the skull, in which it is located in the temporal bone,
has largely completed its development and this region
changes less. However, the splanchnocranium (facies)
region adjacent to the temporal bone develops and
changes much more rapidly unl about one year of
age (Evans, 1993; Thrall and Robertson, 2011; Schmidt
et al., 2011). Therefore, if the younger group could be
further divided into subgroups, age-related changes
could be seen more prominently. In addion, due to the
lack of pedigree records of all dogs used, breed-related
evaluaons could not be made. Instead, skull indices
were used to evaluate head type-related changes.
In conclusion, it can be said that age and skull type
is more eecve than gender in the posion of the
tympanic region in dogs. The results of this research are
supporve informaon that can be used in both clinical
and zooarchaeological studies on the tympanic bulla
region in dogs.
Acknowledgement
This study is a part of the project supported by TUBITAK
(2209-University Students Research Projects Support
Table 3: Angular measurements and calculated index values of the skulls of animals of dierent sexes
p<0.05 *
FEMALE MALE
Angular values (o) NMV±SD NMV±SD p
Angle of tuba audiva 48 49.83±6.79 57 50.03±8.80 0.616
Angle of meatus acuscus externus 48 45.48±4.73 57 47.77±6.51 0.040*
Index values (%)
Skull index 48 57.22±10.94 59 56.77±4.63 0.608
Cranial index 48 66.57±15.02 59 62.92±12.37 0.201
Facial index 48 137.43±31.1 59 138.95±30.36 0.735
Width of bulla tympanica 1 index 48 14.21±2.51 59 13.87±4.41 0.066
Width of bulla tympanica 2 index 48 10.83±2.62 59 10.47±3.98 0.146
Heigth of bulla tympanica index 48 20.78±3.23 59 19.83±3.63 0.176
SI CI FI BWI1 BWI2 BHI
TAA -0,273** -0,581** -0,524** -0,454** -0,528** 0,265**
MEA -0,120 0,127 0,061 0,220*0,212* -0,110
Table 4: Correlaon coecients between cranial index values and the angle values on the pars tympanica
p<0.01**
Çınar et al Morphological Variaons in Tympanic Poron of Temporal Bone in Dogs
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44
Program/1919B011301511)
The rst results of this study XVII. Presented at the
Internaonal Veterinary Medicine Students Scienc
Research Congress (Istanbul).
Conict of interest
The authors declare that they have no conict of interest
in this study.
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