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R E S E A R C H Open Access
Angiographic anatomy of the extracranial
and intracranial portions of the internal
carotid arteries in donkeys
Nurul Hayah Khairuddin
1*
, Martin Sullivan
2
and Patrick J. Pollock
3
Abstract
Background: In horses, the extracranial and intracranial pathway of the internal carotid artery has been described. The
extracranial pathway of the internal carotid artery begins at the carotid termination and runs on the dorsal surface of the
medial compartment of the guttural pouch. Thereafter the internal carotid artery passes through the foramen lacerum
to continue intracranially, forming part of the rostrolateral quadrants of the cerebral arterial circle (Circle of Willis). The
objectives of this study were to define and record the anatomy of the carotid arterial tree and the internal carotid artery
in donkeys using angiographic techniques. This is a prospective descriptive study on 26 cadaveric donkeys.
Methods: Twenty six donkey cadavers of mixed, age, sex and use presented for reasons unrelated to disease of the
guttural pouch were subjected to carotid and cerebral angiography using rotational angiography. Rotational
angiographic and 3 dimensional multiplanar reconstructive (3D-MPR) findings were verified with an arterial latex casting
technique followed by dissection and photography.
Results: The following variations of the carotid arterial tree were identified: [1] the internal carotid and occipital arteries
shared a common trunk, [2] the linguofacial trunk originated from the common carotid artery causing the common
carotid artery to terminate as four branches, [3] the external carotid artery was reduced in length before giving rise to
the linguofacial trunk, mimicking the appearance of the common carotid artery terminating in four branches, [4] the
internal carotid artery originated at a more caudal position from the common carotid artery termination.
Conclusion: Veterinarians should be aware that considerable variation exists in the carotid arterial tree of donkeys and
that this variation may differ markedly from that described in the horse.
Keywords: Donkeys, Internal carotid artery, Rotational angiography
Background
In horses, the gross and angiographic anatomy of the
internal carotid artery has been described [1, 2]. The ex-
tracranial pathway of the internal carotid artery begins at
the carotid termination where the internal carotid artery
originates caudal and ventral to the occipital artery and
runs on the dorsal surface of the medial compartment of
the guttural pouch. Thereafter the internal carotid artery
passes through the foramen lacerum to continue intracra-
nially passing through the ventral petrosal sinus and
entering the venous cavernous sinus where the internal
carotid artery forms a sigmoid flexure. After the sigmoid
flexure, the internal carotid artery gives rise to the caudal
intercarotid and caudal communicating arteries before
continuing for a short distance rostrally to terminate as
the rostral and middle cerebral arteries, [2, 3] forming part
of the rostrolateral quadrants of the cerebral arterial circle
(Circle of Willis). The caudal communicating artery,
which turns caudad to join the basilar artery, results in the
formation of the lateral and caudolateral quadrants of the
cerebral arterial circle. The objectives of this study were to
define the angiographic anatomy of the carotid termin-
ation and the internal carotid artery in donkeys; and to
determine the variation of the internal carotid artery be-
tween individual donkeys using rotational angiographic
techniques. To date, carotid and cerebral rotational
* Correspondence: nurul.leman82@gmail.com;nurulhayah@upm.edu.my
1
Department of Farm and Exotic Animal Medicine and Surgery, Faculty of
Veterinary Medicine, Universiti Putra Malaysia, 43400 UPM Serdang, Kuala
Lumpur, Selangor, Malaysia
Full list of author information is available at the end of the article
© The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Khairuddin et al. Irish Veterinary Journal (2017) 70:12
DOI 10.1186/s13620-017-0090-0
angiography with 3D imaging (3D-RA) has not been
described in donkeys.
Methods
Ethics
Ethical approval for this study was granted by the School
of Veterinary Medicine Ethics and Welfare Committee,
University of Glasgow and consent was obtained for the
use of cadaver material.
Specimen preparation
Twenty six donkey cadavers were obtained. All donkeys that
died or were euthanized over a 6 month period regardless
of type, age, sex and working purpose were studied. The
head and necks were then disarticulated from the body at
the level of the 3
rd
and 4
th
cervical vertebrae ensuring that
the guttural pouches and the carotid arterial tree remained
intact on both sides. Signalment data were not recorded
during collection of the specimens, but all were adults. The
specimens used in this study were not injected with heparin
prior to death, thus blood clotting in the vessels at post
mortem was to be expected. The muscles surrounding the
cervical vertebrae were stripped off to allow identification of
the point of disarticulation of the neck from the body. Spec-
imens were collected and kept frozen at -20 °C until they
were ready to be transported for the study. Information re-
garding time interval from death to freezing was unavail-
able. The specimens were transported (from frozen) using a
non-refrigerated vehicle and some degree of thawing had
occurred during transportation. Upon arrival the donkey
specimens were immediately stored at -20 °C.
The specimens were thawed before any procedures were
conducted. The left and right common carotid arteries
were identified from the disarticulated region of the neck
and catheterised using a 16Fr male Foley catheter ad-
vanced into each common carotid artery for approximately
5–10 cm. The balloon on the tip of the catheter was in-
flated with 1–2 ml of water and an encircling ligature was
placed caudal to the balloon to prevent the catheter from
becoming dislodged. The arterial system was flushed with
water using a high pressure, manual garden pump via the
catheter until no resistance was met and water could be
seen flowing from the contralateral common carotid artery
(via the Foley catheter). This ensured that all the clotted
blood in the arteries was removed.
Rotational angiography and three dimensional
multiplanar image reconstruction of the carotid and
cerebral vessels
Rotational method of angiography of the carotid and cere-
bral vessels was carried out using a Ziehm Vario 3D mo-
bile fluoroscopic machine equipped with a C-arm unit.
Prior to angiography, the head was placed in left lateral re-
cumbency on a board with two stands to support the
weight of the specimen. To extend the guttural pouch, the
head was pulled cranially from the neck. Utilising this
stand, the specimen was positioned between the X-ray
generator and the image intensifier. A laser-positioning
beam was directed at the centre of the region cranial to
the wings of the atlas, ventral to the ear and caudal to the
vertical ramus of mandible. The laser-positioning device
aided in the aligning and positioning of the C-arm to the
region of interest. A scout radiograph was taken to ensure
correct positioning of the C-arm over the region of the
guttural pouch and approximately, 15–20 mL of contrast
material (Barium sulphate, Baritop ® 100, Sakai Chemical
Industry Company Ltd, Japan) was injected to fill the left
side of the carotid tree to the level of the internal carotid
artery within the cranium. A further 15–20 mL of contrast
material was injected to allow filling of the cerebral vessels
and the contralateral carotid arterial tree. Following injec-
tion of contrast, the Foley catheters on both sides were
clamped to prevent leakage of the contrast agent during
image acquisition. Angiographic images of the carotid ar-
terial tree were obtained immediately after the ipsilateral
injection of the contrast material.
During automatic rotational scanning, the Iso-Cine (for
Cine-Loop function) and 3D operating modes (for 3D-
multiplanar reconstruction) were used. The C-arm move-
ment was motor-driven and could be controlled using a
foot switch, which also controlled exposure. It would take
approximately two minutes for the C-arm to complete a
136 degree rotation scan. Each scan generated 112 sequen-
tial images at different angles, and these could also be
reviewed as a movie using the Cine-Loop function. 3D mul-
tiplanar reconstruction (3D-MPR) of the rotational images
allowed a 3D representation of the vessels to be created.
Arterial latex casting, dissection and photography
Angiographic findings were verified using an arterial
latex casting technique followed by dissection and pho-
tography. For this technique, the arterial system was
injected with embalming material (Cambridge formula-
tion, Vickers Laboratory, Pudsey, West Yorkshire, LS28
6QW, UK) via the catheterised common carotid arteries
and once the arterial injection was completed, the ca-
daver was left at ambient temperature for approximately
48 hours to allow the fixative to take effect. Trylon latex
(Trylon Ltd, Bury Close, Higham Ferrers Nothants,
NN10 8HQ, UK) was used to produce a cast of the
carotid arterial tree. After the arterial latex injection, the
cadaver was carefully placed in a large heavy-duty con-
tainer inside a store. The temperature of the storeroom
usually depended on the surrounding environmental
temperature as the storeroom was not equipped with
heating or cooling equipment. Improved air movement
in the room was achieved with a fan. Air changes were
not monitored. The cadaver was left to allow the latex to
Khairuddin et al. Irish Veterinary Journal (2017) 70:12 Page 2 of 7
cure for 10–14 days. Typically after 10 days, the cadaver
was ready for dissection. Photographs of the carotid
termination and the extracranial internal carotid artery
were taken using a digital camera (Nikon D60 D-SLR)
and compared with the angiographic findings.
Results
Angiographic variations of the extracranial portion of the
internal carotid artery
The common/standard anatomical pattern of the extra-
cranial portion of the internal carotid artery and its
pathway in donkeys was similar to that observed in the
horse (Fig. 1). Rotational angiography of bilateral carotid
trifurcation and internal carotid artery was performed
on 26 donkeys, producing 52 angiograms. Thirty nine
angiograms demonstrated a pattern common to that
found in horses [1] and 13 had anatomical variations.
Where there were differences in the angiographic
appearance in comparison to horses, these variations
affected the termination of the common carotid artery.
Sharing of a common trunk with the occipital and the
internal carotid arteries was observed unilaterally in one
donkey (Fig. 2). Five angiograms demonstrated the
linguofacial trunk originating from the common carotid
artery (Fig. 3). In another five angiograms, it appeared
that the linguofacial trunk shared a common origin with
the external carotid artery (Fig. 4).
Another interesting finding in two angiograms was
that the internal carotid artery originated much more
Fig. 1 Lateral angiogram (left) of the common pattern of the carotid
trifurcation and the internal carotid artery of a donkey. 1 common
carotid artery; 2 external carotid artery; 3 internal carotid artery; 4
occipital artery; 5 cranial branch of occipital artery; 6 caudal branch
of occipital artery; 7 linguofacial trunk
Fig. 2 Lateral angiogram of the left carotid arterial tree of a donkey
shows variation from the common pattern of this structure where
the occipital and the internal carotid arteries share a common trunk
(black arrow). 1 common carotid artery; 2 external carotid artery; 3
internal carotid artery; 4 occipital artery
Fig. 3 Lateral angiogram of the left carotid arterial tree of a donkey
shows variation from the common pattern of this structure. The
origin of the linguofacial trunk (black arrow) is directly from the
common carotid artery. 1 common carotid artery; 2 external carotid
artery; 3 internal carotid artery; 4 occipital artery; 5 linguofacial trunk
Khairuddin et al. Irish Veterinary Journal (2017) 70:12 Page 3 of 7
caudal to the occipital artery (Fig. 5), compared to the
common anatomical pattern. The distance of the in-
ternal carotid artery origin from the common carotid
artery was neither measured nor recorded during angi-
ography, but was measured during dissection. Bilateral
variations were noted in one donkey, and unilateral vari-
ations in 11 donkeys. Of 13 angiograms with variations
at the termination of the carotid arterial tree, it was
noted that nine variations were on the left side and four
were on the right.
Angiography of the intracranial portion of the internal
carotid artery and the cerebral arterial circle
In the region of the intracranial portion of the internal ca-
rotid artery, the presence of the caroticobasilar arteries
could be appreciated in 20 donkeys, either unilaterally
(10) or bilaterally (10). Figure 6 shows an example of the
unilateral presence of this artery and Fig. 7 a bilateral ex-
ample. However, several eccentric connections were seen
in addition to this artery in a number of donkeys (3/26).
In two donkeys, a small vessel originating from the second
curve of the sigmoid flexure of the left internal carotid ar-
tery was noted to be connected to the caudal intercarotid
artery (Fig. 8). In another donkey, an eccentric connection
was seen on the left side where a vessel originating from
the second curve of the sigmoid flexure was observed to
join the caudal communicating artery before that artery
joined the basilar artery to form the caudolateral
Fig. 4 Lateral angiogram of the left carotid arterial tree of a donkey
shows variation from the common pattern of this structure. The
linguofacial trunk shares the same origin with the external carotid
artery (black arrow). 1 common carotid artery; 2 external carotid
artery; 3 internal carotid artery; 4 occipital artery; 5 linguofacial trunk
Fig. 5 Lateral angiogram of the left carotid arterial tree of a donkey
shows variation from the common pattern of this structure. The left
internal carotid artery (red open arrow) originates very caudal to the
common carotid artery termination. 1 common carotid artery; 2
external carotid artery; 3 internal carotid artery; 4 occipital artery; 5
linguofacial trunk
Fig. 6 Dorsoventral angiogram of the cerebral arterial circle of a
donkey. The basilar artery was not straight and leaning more to the
right side. Note the presence of the right caroticobasilar artery
(arising from the second curve of the internal carotid artery). 1
internal carotid artery; 2 intercarotid artery; 3 caudal communicating
artery; 4 basilar artery; 5 caroticobasilar artery
Khairuddin et al. Irish Veterinary Journal (2017) 70:12 Page 4 of 7
quadrants of the cerebral arterial circle (Fig. 9). Unfortu-
nately, it was difficult to determine whether this was a true
vessel or superimposition with other vessel. In one don-
key, it was thought that the caudal intercarotid artery was
absent; however its presence was confirmed with repeated
views using the Cine-Loop function.
Dissection of the latex casted specimens
Dissections were carried out on 26 donkey specimens
that had been subjected to latex casting of the carotid
arterial tree confirming the angiographic findings in all
the specimens at the level of extracranial part of the
carotid arterial tree. In the 26 donkeys where bilateral
carotid arterial tree latex casting was attempted, only
two satisfactory casts of the carotid arterial tree were ob-
tained out of 52 casts. Where the casting technique was
unsuccessful, it appeared that the embalming fluid and
latex failed to fill the arterial lumen satisfactorily, resulting
in shrinking of the samples (25 casts). However, partially
filled casts were nevertheless dissected as in some cases
they retained enough shape to be of value (3 casts). Twenty
two latex casts from non-embalmed specimens were not
harvested. An immediate anatomical observation on these
specimens was made and recorded during dissections.
Discussion
In the donkey, the angiographic appearance of the ca-
rotid trifurcation and the internal carotid artery has been
reported to have a similar pattern to that of the horse
Fig. 7 Dorsoventral angiogram of the common pattern of the
internal carotid arteries and formation of the cerebral arterial circle
of a donkey. Note the bilateral presence of caroticobasilar arteries
(red arrows). 1 internal carotid artery; 2 intercarotid artery; 3 caudal
communicating artery; 4 basilar artery
Fig. 8 Dorsoventral angiogram of the cerebral arterial circle of a
donkey. A peculiar connection is seen (red arrow) from the second
curve of sigmoid flexure of the internal carotid artery to the caudal
intercarotid artery. 1 internal carotid artery; 2 intercarotid artery; 3
caudal communicating artery; 4 basilar artery
Fig. 9 Dorsoventral angiogram of the cerebral arterial circle of
a donkey. A connection is seen from the second curve of the
right internal carotid artery to the caudal communicating artery
(red arrow). 1 internal carotid artery; 2 caudal communicating artery;
3 external carotid artery
Khairuddin et al. Irish Veterinary Journal (2017) 70:12 Page 5 of 7
[4]. However, one major difference was that the common
carotid artery may terminate as four branches instead of
three, where the linguofacial trunk (external maxillary
artery) arises directly from the common carotid artery
and not as a branch of the external carotid artery [4].
Another difference noted was that the occipital artery of
donkeys was larger than in horses [4].
Angiography of the extracranial portions of the internal
carotid artery
Previously published angiographic studies of the carotid
arterial tree of the donkey, described the origin of the
linguofacial trunk as the common carotid artery, and not
as a branch of the external carotid artery, as is the case
in the horse [4]. However, this observation was based on
a single donkey, thus this finding cannot be regarded as
conclusive. Based on the study presented here, it appears
that the carotid trifurcation of the donkey is similar to
that of the horse (based on 39/52 angiograms). However,
a number of the donkey cadavers (13/52) showed the
following variations:
1. The internal carotid artery and occipital artery
shared a common trunk (1/13 angiograms)
2. The linguofacial trunk was present as a branch of
the common carotid artery, rather than as a branch
of the external carotid artery (5/13 angiograms)
3. The linguofacial trunk shared a common trunk with the
origin of the external carotid artery (5/13 angiograms)
4. The internal carotid artery originated more caudally,
than the usual pattern, from the common carotid
artery termination (2/13 angiograms)
In this study, the origin of the internal carotid artery was
observed to be commenced more caudal than the com-
monly understood anatomical pattern of this structure in
two of the cadavers. Usually, the internal carotid artery
originated very close to the occipital artery. In donkeys that
have a linguofacial trunk originating from the common ca-
rotid artery and an internal carotid artery originating very
caudal to the termination of the common carotid, there
may be confusion in identifying the internal carotid artery,
given the assumption that the common carotid artery ter-
minates in three branches. One may mistakenly think that
the internal carotid artery was absent, or worse, identify
the occipital artery as the internal carotid artery.
The anatomical arrangement of the linguofacial trunk
may create confusion in terms of where exactly this ves-
sel originates. We speculate that if the linguofacial trunk
is given off close to the origin of the external carotid ar-
tery it may appear angiographically, that the two vessels
share a common origin.
In this study, a number of anatomical variations present
in the donkeys have been previously described in horses
as well. However, interestingly, aberrant branches of the
internal carotid artery, as noted in horses [1, 4–6], were
not observed in any of the donkeys in this study.
Angiography of the intracranial portions of the internal
carotid artery
There is a paucity of published literature relating to the
internal carotid artery and the cerebral arterial circle of
donkeys. In one report [7] it was argued that the internal
carotid artery bifurcates intracranially into caudal com-
municating and rostral cerebral arteries, with the middle
cerebral artery branching from the rostral cerebral artery
and not from the internal carotid artery. Contrary to
what has been described in the horse, the internal
carotid artery was considered to give off the caudal
communicating artery and continue for a short distance
rostrally to terminate as the rostral and middle cerebral
arteries [2]. In other words, the rostral cerebral artery
starts after the origin of the middle cerebral artery.
A rostral intercarotid artery was observed in the cere-
bral arterial circle in one donkey [7]. This was described
as a thin vessel originating from the extension of the
internal carotid artery (perhaps more correctly described
as the rostral cerebral artery) at the level where the in-
ternal carotid artery gives off the caudal communicating
artery. The rostral intercarotid artery formed a connection
to the contralateral vessel.
The description given for the caudal communicating
artery in the horse, is that the artery turns caudal after
coming off the intracranial portion of internal carotid
artery, and then joins the basilar artery to form the
lateral and caudolateral quadrants of the cerebral arterial
circle [2]. In this study, generally the arrangement of the
caudal communicating giving rise to the basilar artery
followed this pattern. However in some donkeys, it was
observed that there were some indirect fine branches at
the terminal end of the caudal communicating arteries,
and generally the continuation to the basilar artery was
not easy to determine. The junction of the distal seg-
ment of the caudal communicating artery with the basi-
lar artery is created by a rete or plexus of the terminal
branches of the basilar artery as recognised by Sisson
(1910). According to Nanda [2], a rostral cerebellar
artery originates from the terminal portion of the basilar
artery, of which there can be either two or three on
either side. Where a plexus or rete can be seen before
the basilar artery joins the caudal communicating artery,
the rostral cerebellar artery may leave this plexus in a
variable and asymmetrical manner [2].
The odd arrangement of the caudolateral quadrants of
the cerebral arterial circle has also been reported [8]. It
was suggested that the caudal communicating artery
should not be named as such because of the presence of
various fine branches interconnected with the basilar
Khairuddin et al. Irish Veterinary Journal (2017) 70:12 Page 6 of 7
artery, which were arranged in an odd manner similar to
the primitive patterns observed in other lower mammals
and submammals (fishes, amphibians and reptiles).
Perhaps in view of the results described here, the varia-
tions in arrangement of these fine vessels might be
regarded as variant anastomoses of the cerebral arterial
circle. Based on the observations herein, the rete was
seen as various anastomotic fine vessels interconnecting
the basilar artery, not only to the caudal communicating
but also to the caudal intercarotid arteries, as also seen
in the angiographic findings of the donkeys studied here.
Due to the complex three dimensional structures of the
cerebral arterial circle and its connections, the best way
to verify the continuation of these eccentric vessels is by
viewing its three dimensional display using the 3D-MPR
function. However, due to the fact that the 3D-MPR
representations faced some limitations of its own,
further investigation on these eccentric vessels could not
be carried out accordingly.
Conclusion
The findings described here, provide additional informa-
tion regarding the pathway of the extracranial and intra-
cranial internal carotid artery pathway. The intracranial
internal carotid and the cerebral arterial circle could be
observed angiographically and these findings comple-
ment the anatomical study of the blood supply to the
brain of donkeys.
Abbreviations
3D- MPR: 3 dimensional multiplanar reconstructive; 3D- RA: 3 dimensional
rotational angiography
Acknowledgement
The authors would like to thank The Donkey Sanctuary, UK, for their
generous support in this study. We also wish to thank Richard Irvine and
Michael McGuigan from the post mortem unit, School of Veterinary
Medicine, Prof. Shaw Dunn and Gordon Redford from School of Life
Sciences, University of Glasgow, for their assistance with the preparation of
the specimens for arterial latex casting.
Funding
This study was funded by the Ministry of Higher Education of Malaysia, grant
number KPT(BS)820626-05-****.
Availability of data and materials
The data that support the findings of this study are available from the
corresponding author upon reasonable request.
Authors’contribution
NH carried out the processing of the cadaveric material in preparation for
angiographic work, performed the angiographic work and data analysis. MS
participated in the angiographic data analysis and helped to draft the
manuscript. PJP participated in coordination of the research work, involved
in identification of the cerebral and carotid vessels, and its association with
the guttural pouches and helped to draft the manuscript. All authors read
and approved the final manuscript.
Competing interest
None of the authors have any competing interests in the written manuscript.
Consent for publication
This manuscript does not contain any individual person’s data.
Ethics approval
Ethical approval for this study was granted by the School of Veterinary
Medicine Ethics and Welfare Committee, University of Glasgow and consent
was obtained for the use of cadaver material. This work was a cadaveric
study of donkey heads. The donkeys were not euthanised for the purposes
of the study, but the result of euthanasia of animals because of health or
welfare reasons or had died of natural causes. The work was approved by
the School Research Ethics Committee, on which sits a UK Home Office
Inspector. The Home Office governs and sanctions all animal research in the
UK. Euthanasia of the donkeys met The Animals (Scientific Procedures) Act
1986 (Appropriate Methods of Humane Killing) Order 1996.
Publisher’sNote
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
Author details
1
Department of Farm and Exotic Animal Medicine and Surgery, Faculty of
Veterinary Medicine, Universiti Putra Malaysia, 43400 UPM Serdang, Kuala
Lumpur, Selangor, Malaysia.
2
Small Animal Clinical Sciences, School of
Veterinary Medicine, University of Glasgow, Glasgow, UK.
3
Weipers Centre
Equine Hospital, School of Veterinary Medicine, University of Glasgow,
Glasgow, UK.
Received: 1 February 2017 Accepted: 10 April 2017
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