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World Journal of Otorhinolaryngology-Head and Neck Surgery (2018) xx, 1e5
Available online at www.sciencedirect.com
ScienceDirect
journal homepage: www.keaipublishing.com/WJOHNS; www.wjent.org
Research Paper
Evaluation of sheep sinonasal endoscopic
anatomy as a model for rhinologic research*
Luis Macias-Valle a,b, Andres Finkelstein-Kulka a,c,
Jamil Manji a,d, Christopher Okpaleke a, Salahuddin Al-Salihi a,
Amin R. Javer a,*
a
St. Paul’s Sinus Centre, Vancouver, British Columbia, Canada
Hospital Español de México, Facultad Mexicana de Medicina Universidad La Salle Mexico City, Mexico
c
Clı´nica Alemana de Santiago, Facultad De Medicina Clı´nica Alemana, Universidad Del Desarrollo, Chile
d
Faculty of Medicine, University of Melbourne, Melbourne, Victoria, Australia
b
Received 7 July 2017; received in revised form 6 April 2018; accepted 2 May 2018
KEYWORDS
Sinus anatomy;
Animal model;
Sinus endoscopy;
Sinus research;
Sinus surgery
Abstract Objectives: Despite many publications describing sheep models for functional
endoscopic sinus surgery (FESS) procedures, accurate endoscopic anatomical studies are lacking. There are no publications correlating computed tomography (CT) and 3D models with
endoscopic anatomical descriptions. This study evaluates and describes the endoscopic anatomy of a sheep model.
Methods: Ten live sheep (20-sides) were included. Two cadaveric specimens, imaged using thin
slice CT for 3D reconstruction correlation were also included. Using endoscopy, anatomical
structures were measured and described. Measurement of the same structures was carried
out using the 3D imaging model.
Results: Three sets of turbinates were identified at 2.3, 5.1 and 8.5 cm from the anterior nasal
sill. Frontal recess and uncinate process were identified at 12.7 cm. The septum has a bony and
cartilaginous component and measures 10.5 cm. The sphenopalatine foramen was measured at
12.1 cm. All anatomical measurements were correlated with the measurements on the CT scan
3D volume-rendering model, thereby allowing for an accurate description of the sheep sinonasal anatomy.
*
Presentation: This study was presented at the 61st, Annual Meeting of the American Rhinologic Society (ARS) on 26th, September, 2015 in
Dallas, TX, USA.
* Corresponding author. St. Paul’s Sinus Centre, St. Paul’s Hospital, Room 2600-1081 Burrard Street, Vancouver, BC, V6Z 1Y6. Canada. Fax:
þ1 (604) 806 9690.
E-mail address: sinusdoc@me.com (A.R. Javer).
Peer review under responsibility of Chinese Medical Association.
Production and Hosting by Elsevier on behalf of KeAi
https://doi.org/10.1016/j.wjorl.2018.05.002
2095-8811/Copyright ª 2018 Chinese Medical Association. Production and hosting by Elsevier B.V. on behalf of KeAi Communications Co.,
Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article in press as: Macias-Valle L, et al., Evaluation of sheep sinonasal endoscopic anatomy as a model for rhinologic
research, World Journal of Otorhinolaryngology-Head and Neck Surgery (2018), https://doi.org/10.1016/j.wjorl.2018.05.002
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2
L. Macias-Valle et al.
Conclusion: This study describes the endoscopic sinonasal anatomical measurements of the
adult sheep. It is the first study to evaluate the sheep CT and endoscopic anatomy in order
to determine its feasibility as an animal model for research in FESS.
Copyright ª 2018 Chinese Medical Association. Production and hosting by Elsevier B.V. on
behalf of KeAi Communications Co., Ltd. This is an open access article under the CC BY-NCND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Introduction
Animal models are living organisms with an inherited, naturally acquired, or induced pathological process that, in one
way or another, resembles the same phenomenon in man.1
There is an ongoing need to find an animal model to study
new treatment modalities in humans. These include pharmaceutical and toxicology research (where animal models
can be used to determine effect, efficacy, effective dose,
toxicity profile, and patho-medications)1 and functional
endoscopic sinus surgery (FESS) research and training.2,3
Many different animal models have been used in FESSrelated research, including rabbits,4 sheep,5 and swine.6
Among these animal models, the sheep model has been
demonstrated to be favorable for FESS-related research. Even
though rabbits are readily available and easy to breed, their
nasal cavities are too small to accommodate even the smallest
diameter sinonasal endoscopes (2.7 mm pediatric endoscope)
for endoscopic maneuvers.7 Although the configuration of the
sheep’s head is different to that of a human, the nasal cavity
appears to be quite similar and, as noted from computed tomography (CT) scans, the major sinuses (maxillary, ethmoidal
and frontal) lie in approximately the same orientation as in
humans. Furthermore, the model itself is spacious enough to
accommodate standard instruments, affordable, easily
obtainable and of good tissue quality.3
Despite many publications describing sheep models for
FESS procedures, accurate endoscopic anatomical studies
are lacking. Furthermore, there are no publications correlating computed tomography (CT) and 3D models with
endoscopic anatomical descriptions. In this study, we aim
to evaluate and accurately describe the endoscopic anatomy of a live sheep model using CT and 3D models.
specimens. Axial, coronal and sagittal planes were obtained
using a GE low-dose volume CT (VCT, General Electric,
Fairfield, CT, USA). Images of both specimens were evaluated independently by 3 rhinologists (ARJ, LMV, and AFK) to
identify similarities and differences from human sinonasal
anatomy. The evaluation was carried out using OsiriX 2
software (version 8, 32-bits for Mac OS). The orientation of
sinonasal outflow tracts, identification of superior, middle
and inferior turbinates, and the potential area encompassing the sphenopalatine foramen were also evaluated.
Measurements and volume evaluations were obtained using
an electronic ruler and protocols from the software
mentioned previously (Fig. 1).
Image 3D rendering for measurements
OsiriX 2 (ver 8 32-bits for Mac OS) was used to render 3D
images from an axial CT scan of each sheep cadaver model.
Using a logarithmic table for opacity and a different setting
of linear table values for bone density and soft tissue
density, a 3D model was created (Fig. 2).8 Using the same
algorithm for density values, a virtual endoscopic reconstruction was formulated for cross checking distances of
anatomical references between the cadaver model, live
model and the 3-D reconstruction model (Fig. 3).
Material and methods
Our group chose Dorset cross strain sheep (Ovies aries) as a
candidate for an animal model. We obtained 10 live sheep
for endoscopic evaluation and 2 sheep cadaver heads for
imaging and 3D reconstruction, for a total of 24 sides. All 10
live specimens were female, with a mean age of 12 months
and mean weight of 70 kg (SD Z 9 kg). Sheep were procured
by the Centre for Comparative Medicine at the University of
British Columbia. Animal ethics approval was obtained from
the University of British Columbia Research Ethics Board
(#A14-0172).
Anatomic evaluation through CT images
Routine image guided CT protocol for sinonasal procedures
was ordered and performed on two sheep cadaver
Fig. 1 An axial cut of the cadaveric specimen showing the
electronic ruler function, ROI (region of interest) shows the
predicted area of the sphenopalatine foramen at 12.18 cm
from nasal sill (green circle).
Please cite this article in press as: Macias-Valle L, et al., Evaluation of sheep sinonasal endoscopic anatomy as a model for rhinologic
research, World Journal of Otorhinolaryngology-Head and Neck Surgery (2018), https://doi.org/10.1016/j.wjorl.2018.05.002
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Sheep sinonasal endoscopic anatomy
3
temperature. A steady state of anesthesia was reached
prior to beginning surgery.
With the specimen in prone position, the head was
elevated to approximately 30 . Rigid sinonasal endoscopy
was performed utilizing standard endoscopes used in FESS
(4.0-mm 0-degree and 30-degree 18 cm Hopkins telescope
Karl Storz, Endoscopy, Tuttlingen, Germany) on the anaesthetized sheep. Systematic evaluation and measurement of
pertinent intranasal structures was obtained for all 10
sheep and analyzed as 20 discrete nasal cavities. All sheep
were extubated satisfactorily after the procedure and
returned to their individual pens for postoperative
observation.
Results
Fig. 2 Volume rendering of the CT scan images was done,
obtaining a model with a reconstruction of sinonasal landmarks
for measurement and comparison with the endoscopic model.
Live endoscopic sinonasal model
Sheep were induced with propofol at 46 mg/kg IV through a
catheter placed in the cephalic vein. Orotracheal intubation was then performed under direct vision and anesthesia
was maintained using isoflurane (45% to start and 23% for
maintenance).
After intubation, an orogastric tube was placed in position to prevent bloat. Monitoring took place with standard
monitoring equipment including heart rate, electrocardiogram, non-invasive blood pressure, expired carbon dioxide,
inspired and expired isoflurane, oxygen saturation and
Imaging and virtual endoscopy model
Numerous intranasal structures were consistently observed
and measured during the CT evaluation. The nasal septum
has both a cartilaginous and bony component with a mean
anterior to posterior distance of 10.5 cm. Three different
sets of turbinates were easily identified and found to be
consistently at a mean distance of 2.3, 5.1 and 8.5 cm from
the anterior nasal sill. Turbinates appear to have larger
mucosal surface in the form of concentric semicircular
architecture.
A natural bony dehiscence is encountered on the lateral
nasal wall at 12.1 cm from the nasal sill and 1.5 cm from the
floor of the nose. Within this foramen, both vascular and
muscular contents were identified; this area was identified
most closely to resemble the human sphenopalatine artery
(SPA) foramen. The frontal recess area and uncinate
Fig. 3 Superior images: Axial and coronal cuts used for the reconstruction of the virtual endoscopy model (lower left image),
comparison of the same area in the cadaveric model dissection (lower right image) showing the area of the sphenopalatine foramen, accurately predicted with the 3D model previously.
Please cite this article in press as: Macias-Valle L, et al., Evaluation of sheep sinonasal endoscopic anatomy as a model for rhinologic
research, World Journal of Otorhinolaryngology-Head and Neck Surgery (2018), https://doi.org/10.1016/j.wjorl.2018.05.002
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4
process were identified at 12.7 cm from the nasal sill and
1.8 cm from the floor of the nose, respectively.
The nasal septum did not extend to the full length of the
nasal cavity and ended significantly short of the nasopharynx. The distance between the posterior boundary of
the nasal septum and the posterior wall of the nasopharynx
was found to be 13.8 cm with a mean area of 3.8 cm2. This
posterior gap allowed visualization of the contralateral
lateral nasal wall using angled scopes. All measurements
were corroborated using virtual endoscopy, which was
developed from the axial cuts of the CT scan as noted
previously (Fig. 4). All anatomical measurements were
compared in triplicate between the endoscopic, tomographic and 3D models to improve accuracy (Table 1).
Discussion
Although publications already exist describing the sheep
model for evaluation of surgical competency in FESS9 and
basic research,10 there is scarce literature regarding
anatomical description of the identifiable anatomical
structures in a sheep model. Furthermore, the use of
cadaveric models for surgical competency has the limitation of not having real life conditions (i.e. no bleeding) to
contribute to the acquisition of surgical skill.11
Many animal models have been tested for research in
rhinology, including rabbits,4 swine7 and sheep.5 As
described by the authors, swine is not suitable for surgical
manipulation due to insufficient intranasal space.7 Similar
restrictions apply to the rabbit model, although both have
been used successfully for in vivo research in chronic rhinosinusitis (CRS).12 Based on our measurements and experience with live endoscopy of the sheep nasal cavity, the
sheep model seems very appropriate for endoscopic surgical manipulation. Interestingly, the anatomical characteristics of the septum allow visualization of the contralateral
nasal wall, opening the possibility of bi-nostril instrumentation and a two surgeon, four-handed training model.This
model has also been proven viable for CRS research.13
The importance of the sheep model for pharmaceutical
trials and for evaluation of new biomedical devices has also
been proven in recent studies. Yaniv et al recently trialed a
Fig. 4 Virtual endoscopy of the left nasal cavity of the
sheep, based on the information obtained with the axial cuts
from the CT scan. The cross (þ) shows the nasal septum, the
inferior turbinate (*) and the nasal floor are also depicted.
L. Macias-Valle et al.
Table 1 Measurement of identifiable intranasal anatomical structures (nZ24).
Sinonasal structure
Measurement (SD)
Head of the inferior turbinate
Posterior wall of nasopharynx
Posterior edge of septum
Uncinate process and frontal recess area
Area of the sphenopalatine Foramen
2.3 cm (0.3 cm)
24.3 cm (1.2 cm)
10.5 cm (0.4 cm)
12.7 cm (1.3 cm)
12.1 cm (1.8 cm)
new generation of composite removable stents using a live
sheep model to test their results.14 A recent publication
from our group demonstrated the utility of the live sheep
model to measure the efficacy of a novel self propelling
hemostatic agent, upon creating a mucosal injury to the
inferior turbinate and subsequent bleeding.15
We found an adequate and acceptable correlation in
measurements between all three sheep models. The study
revealed that the sinonasal anatomy of the sheep exhibits
many similarities to human sinus anatomy. The identification of natural ostia of the sinuses and their outflow tracts,
as well as areas of neurovascular contents such as the SPA
foramen, opens the possibility for multiple research projects in the future.
The possibility of teaching surgical techniques under
conditions resembling live operative experience could
impact the way rhinology training is currently undertaken.
The skillset obtained through surgical simulation using animal models has proven to be successfully transferrable to
the operating theatre.16 Sheep heads have been found
useful to assess and teach surgical techniques in rhinology.11 However, the potential application of introducing a
live bleeding model may further enhance the learning
experience and allow for better evaluation of surgical
competency.
The sheep model meets the anatomic feasibility criteria
we set out at the start of the study by making it a suitable
animal model for rhinologic research. To our knowledge,
this is the first study to verify, measure and correlate
sinonasal landmarks accurately in the sheep model using
CT3D reconstruction, virtual endoscopy and live endoscopy.
We understand that the measurement of a particular
breed of sheep with specific phenotypical characteristics
might not be extrapolated to other sheep models. However,
we feel it is important to report measurements and descriptions of anatomical landmarks for facilitating and
standardizing results for future studies using these types of
animal models.
Another limitation of our study is the setting required for
live surgery in the sheep model. The facilities, equipment,
and staff necessary to perform this type of research may
not be easily available for all research centers. Nevertheless, the benefit of having an animal model resembling the
actual surgical experience of FESS may be invaluable for
training programs.
Finally, considerations should be made with regards to
some of the differences between sheep and human anatomy. Although the sheep model is proven to be adequate
for certain endoscopic surgical procedures, limitations due
to length of instruments and depth of structures should be
Please cite this article in press as: Macias-Valle L, et al., Evaluation of sheep sinonasal endoscopic anatomy as a model for rhinologic
research, World Journal of Otorhinolaryngology-Head and Neck Surgery (2018), https://doi.org/10.1016/j.wjorl.2018.05.002
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Sheep sinonasal endoscopic anatomy
taken into account. Certain authors have resorted to the
resection of the anterior section of the sheep muzzle in
cadaveric models to adjust for the working distances of
standardized instruments.17 It should also be noted that the
spatial orientation and topographic characteristics of
important landmarks related to complications in FESS, such
as the orbit or the skull base, are different in the sheep
model when compared to human anatomy.
Conclusion
This study describes endoscopic sinonasal anatomical
landmarks and their measurements in an adult sheep
model. This is the first study to compare both sheep CT and
sinonasal endoscopic anatomy. These findings support the
feasibility of using a sheep model for research in Rhinology.
Financial support and funding
There is no funding or financial disclosure to declare with
respect to this manuscript.
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Edited by YU-Xin Fang
Please cite this article in press as: Macias-Valle L, et al., Evaluation of sheep sinonasal endoscopic anatomy as a model for rhinologic
research, World Journal of Otorhinolaryngology-Head and Neck Surgery (2018), https://doi.org/10.1016/j.wjorl.2018.05.002
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