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Literature Review

Internal Carotid Artery Classification Systems: An Illustrative Review


Jhon E. Bocanegra-Becerra1, Gokhan Canaz2, Cvetina Vatcheva3, Jack Wellington4

Key words The internal carotid artery (ICA) course has been discussed extensively. Several
- Classification systems classification systems have attempted to delineate an accurate and helpful
- ICA
- Internal carotid artery
trajectory for microsurgical and endoscopic guidance, thus allowing a better
- Neuroanatomy neurosurgical performance while avoiding intraoperative complications. Also,
- Nomenclature the practicality of the classification systems has been emphasized for scholarly
Abbreviations and Acronyms
communication among disciplines. Nevertheless, the nomenclature of the ICA
ACA: Anterior cerebral artery remains heterogeneous and confusing for health care professionals, trainees,
CT: Computed tomography and students.
ET: Eustachian tube We present an illustrative review of 8 notable ICA classification systems using
ICA: Internal carotid artery
ILT: Inferolateral trunk
lateral and anterior views as a rapid tool for neuroanatomic consultation. The
MHT: Meningohypophyseal trunk appraisal of the vessel anatomy from different perspectives while recognizing
PCOM: Posterior communicating artery their usefulness and limitations might provide a comprehensive understanding of
PLL: Petrolingual ligament the ICA, optimize the intraoperative performance, and facilitate communication.
From the 1School of Medicine, Universidad Peruana
Cayetano Heredia, Lima, Peru; 2Department of Neurosurgery,
Basaksehir Cam and Sakura City Hospital, Istanbul, Turkey; 8 classification systems proposed by detailed ICA systems to guide the plan-
3
School of Medicine, Eberhard Karls University of Tübingen,
Germany; and 4School of Medicine, Cardiff University, United
Fischer; Gibo, Lenkey, and Rhoton; Las- ning and execution of neurosurgical
Kingdom jaunias et al.; Bouthillier et al.; Ziyal et al.; interventions.
To whom correspondence should be addressed: Shapiro et al.; Labib et al.; and Abdulrauf
Jhon E. Bocanegra-Becerra et al. (Table 1). In addition, illustrations of Gibo, Lenkey, and Rhoton Classification
[E-mail: jhon.bocanegra.b@upch.pe] the anterior and lateral views of the ICA In 1981, Gibo et al. used 50 formalin-fixed
Citation: World Neurosurg. (2022) 163:41-49. are provided in Figures 1 and 2, adult cerebral hemispheres and a colored-
https://doi.org/10.1016/j.wneu.2022.03.116 respectively. based dissection of arteries injected with
Journal homepage: www.journals.elsevier.com/world-
latex or acrylic to propose a new classifi-
neurosurgery
INTERNAL CAROTID ARTERY cation focusing on the supraclinoid region
Available online: www.sciencedirect.com
CLASSIFICATION SYSTEMS of the ICA. Notably, this region was 3 to 40
1878-8750/$ - see front matter ª 2022 Elsevier Inc. All
times magnified to analyze main arteries
rights reserved.
The First Modern Nomenclature System along its course.2
In 1938, with the use of x-ray angiograms of Four ICA segments are described
INTRODUCTION displaced intracranial abnormalities and following the arterial blood flow and
The internal carotid artery (ICA) course cerebral arteries, Fischer published the first topographic correlation with the neck,
has been the subject of different nomen- modern classification of the ICA.1 The goal skull base bones, and cavernous sinus.
clature systems; over time, the vessel tra- was to help localize lesions of the base of These include the C1 or cervical portion,
jectory has been structured based on the skull while considering how their form C2 or petrous portion, C3 or cavernous
distinct aims, materials, and methods. and size affected the ICA segments. The portion, and C4 or supraclinoid portion
Following the introduction of the first description included 5 intracranial (Figures 1B and 2B). The cervical portion
classification by E. Fischer, authors have segments in numeric order and opposite (C1) starts in the common carotid artery
dissected the ICA into a more precise directions to the arterial blood flow. From bifurcation, following its course in the
nomenclature for clinical, research, and C1 to C5: C1 or communicating segment, neck until it reaches the carotid canal.
neuroanatomic purposes. Besides, with C2 or ophthalmic segment, C3 or clinoidal The petrous portion (C2) follows its path
the advent of neuroendoscopy techniques segment, C4 or cavernous segment, and embedded within the petrous part of the
to treat vascular and complex skull base C5 or petrous segment (Figures 1A and 2A). temporal bone until the cavernous sinus
pathologies, special attention has been The practicality of this classification was entry point. Next, the cavernous portion
focused on the systems’ capability to limited by the retrograde fashion of the (C3) travels within the cavernous sinus.
improve operative performance, reduce description, the absent naming of the Then, the supraclinoid portion (C4), an
surgical complications, and facilitate extracranial ICA portion, and the lack of intradural segment, emerges after
communication among disciplines. topographic correlation throughout the crossing the anterior clinoid process
We review the ICA course through an vessel course. Nevertheless, these short- superiorly and terminates at the ICA
illustrative and comparative description of comings motivated the creation of more bifurcation into anterior and middle

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cerebral arteries. Note that the C4 portion trigeminal artery.3 From this, the authors Although this classification was beauti-
divides into 3 parts: ophthalmic, derived an embryologic classification fully engineered based on embryology and
communicating, and choroidal segments. based on ICA development dependent on anatomic correlation, it did not achieve
The ophthalmic segment extends from the third aortic arch and dorsal aorta. extensive use.
the origin of the ophthalmic artery to the The ICA was divided into 7 segments,
origin of the posterior communicating demarcated by the origin of arterial A Classification Suitable for Clinical Use
artery (PCOM). Then, the communicating branches along its course and correlating In 1996, Bouthillier et al. proposed a new
segment follows until the origin of the the embryologic origin with regional classification including contributions from
anterior choroidal artery. Lastly, the anatomical entities (Figures 1C and 2C). their predecessors but with a more accu-
choroidal segment continues until the These consisted of the following rate delineation of the ICA. This, com-
terminal ICA bifurcation. landmarks: the first segment of the ICA bined with a more considerate approach to
The magnification of the C4 portion analogous to the third aortic arch (the looking at its course, namely, in the di-
allowed a millimetric description of its cervical ICA in an adult) with proximal rection of blood flow, created a more
trajectory. For example, the average di- and distal limits of the carotid bulb and practical system for clinical use than the
ameters at its origin and terminal bifur- ICA cervical-petrous junction, respec- previous versions.4
cation were 5.0 mm and 4.1 mm, tively. The second: dorsal aorta amid sec- The description was based on 20 speci-
respectively. The total C4 portion length ond and third aortic arches (distal portion mens from 10 cadaveric heads, 7 fixed with
ranged from 14 to 25 mm (average 19 corresponding to the hyoid and car- formalin, and 3 fresh unembalmed. Colored
mm), with the ophthalmic segment being oticotympanic arteries in an embryo and silicone rubber was injected into the inter-
the longest and the communicating adult, respectively), with proximal and nal jugular veins and ICA, which was
segment the shortest. Although beyond distal limits of the ICA cervical-petrous microscopically examined throughout its
the scope of our review, the authors also junction and caroticotympanic artery, course. Furthermore, additional observa-
included technical notes in the treatment respectively. The third: dorsal aorta amid tions were done during surgical procedures
of tumors and intracranial aneurysms of first and second aortic arches (segment that involved the skull base, the cavernous
the supraclinoid region based on perfo- relates to between the hyoid and mandib- sinus, and ophthalmic segment carotid an-
rating branches arising in the three seg- ular, and caroticotympanic and vidian ar- eurysms. The analysis of 20 dry human
ments of C4 (e.g., the superior teries, in an embryo and adult, skulls allowed a detailed description of bony
hypophyseal arteries). respectively), with proximal and distal structures, including the foramen lacerum
limits of the caroticotympanic and vidian and anterior clinoid process. In addition, 4
An Embryologic Classification arteries, respectively. The fourth: dorsal cadaveric pieces involving the skull base
In 1984, Lasjaunias et al. published an aorta amid first aortic arch and trigeminal portion of the ICA, from the entrance into
embryologic methodology to identify artery origin (segment relates to between the carotid canal to its supraclinoid posi-
anatomic variants alongside segmental vidian artery and meningohypophyseal tion, were removed en bloc and underwent
agenesis of the ICA. This system focuses on trunk [MHT] with respect to an adult), with histologic examination.
2 main aspects: (1) individual segments of proximal and distal limits of the vidian From C1 to C7, the ICA divides into 7
the ICA possess conspicuous embryologic artery and MHT, respectively. The fifth: segments in ascending fashion, following
determinants, and (2) regression of subse- dorsal aorta amid origins of trigeminal and the direction of blood flow and consid-
quent segments of the ICA may be a primitive dorsal ophthalmic arteries ering neighboring anatomical structures
consequence of proximal agenesis to 1 (segment relates to horizontal cavernous (Figures 1D and 2D). The cervical segment
segment. Such embryologic data may be segment amid MHT and inferolateral trunk or C1 starts from the common carotid
applied to understand and differentiate [ILT] in respect to an adult), with proximal artery bifurcation, running within the
congenital versus acquired modifications to and distal limits of the MHT and ILT, carotid sheath along the internal jugular
the ICA, with the clinician recognizing what respectively. The sixth: segment amid vein, the vagus nerve, a venous plexus,
is considered a normal or aberrant ICA.3,10 origin and anastomosis of the primitive and postganglionic sympathetic nerves
The classification was designed with the dorsal and ventral ophthalmic arteries, until it reaches the carotid canal. Then,
retrospective analysis of a single case study respectively (corresponds to the clinoid the petrous segment or C2 travels within
reporting a 35-year-old woman with a 4- segment amid origins of the ILT and the periosteum of the carotid canal,
month history of generalized epilepsy. Her ophthalmic artery in an adult). Proximal surrounded by a venous plexus and
past medical history included a cutaneous and distal limits involved the ILT and postganglionic sympathetic nerve, and
mandibular angioma treated with radio- ophthalmic artery, respectively. The sev- ends at the posterior edge of the
therapy at the age of 4 years and a thyroid- enth: segment amid anastomosis of the foramen lacerum. Note that the ICA does
ectomy at the age of 26 years. A meningioma primitive ventral ophthalmic artery and not pass through the foramen lacerum
of the anterior clinoid process was diag- carotid bifurcation (relates to the supra- but crosses over it. Also, C2 subdivides
nosed through histology and selective ca- clinoid portion of the ICA from origins of into 3 smaller parts, which refer to the
rotid angiography. However, such findings ophthalmic and PCOM arteries in an adult, planes on which it courses—a vertical
from the ICA angiography revealed the ophthalmic segment), proximal and portion, a bend (ICA posterior loop), and
segmental agenesis of the ICA alongside distal limits involve the ophthalmic and a horizontal portion that courses
intracavernous revascularization via a PCOM arteries.3,10 anteromedially.

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Table 1. Summary of Internal Carotid Artery Classification Systems
Study Fischer1 Gibo, Lenkey and Rhoton2 Lasjaunias et al.3 Bouthillier et al.4

Publication 1938 1981 1984 1996


year
Material and Based on x-ray angiograms of Based on 50 formalin-fixed brain hemispheres, and the Based on retrospective analysis of a single case study Based on the ICA microscopic description of 10
A

methods intracranial arterial injection of latex or acrylic into arteries. reporting a meningioma of the anterior clinoid process cadaveric heads, description of bony
3A 35 3A3 (
3

abnormalities. and segmental agenesis of the ICA alongside relationships from 20 dry human skulls, and
intracavernous revascularization via a trigeminal artery. histological examination of the ICA in the skull
D E3

base.
Number of 5 4 7 7
C /

segments
G D 2 A 3

Nomenclature C1 - Communicating C1 - cervical 1. Cervical C1 - Cervical


(segments) C2 - Ophthalmic C2 - petrous 2. Ascending intrapetrous C2 - Petrous
A C

C3 - Clinoidal C3 - cavernous 3. Horizontal intrapetrous C3 - Lacerum


C4 - Cavernous C4 - supraclinoid: 4. Ascending foramen lacerum C4 - Cavernous
C5 - Petrous Ophthalmic 5. Horizontal intracavernous C5 - Clinoid
CA D
2 E A CG ,D353 3 3A3 5 )

Communicating 6. Clinoid C6 - Ophthalmic


Choroidal 7. Terminal C7 - Communicating
Main features It was intended to help localize The C4 portion described several important perforating Segments are in between branches of the ICA. It merges previous classifications with accurate
3DC A 3 I ) GA

skull base lesions and correlate branches (e.g., superior hypophyseal arteries) for Provides embryological methodology identifying delineation of segments.
their position with the ICA intraoperative consideration. anatomical variants alongside segmental agenesis of the More practical for clinical use than their
segments. It included technical notes for treating intracranial ICA clinically. predecessors.
The extracranial ICA description tumors and aneurysms of the supraclinoid region. Focuses on individual segments of the ICA possessing It is helpful for surgeries with a transcranial
was excluded. It is helpful for surgeries with a transcranial distinct embryological determinants and the regression microscopic approach.
microscopic approach of subsequent ICA segments as a consequence of

ICA CLASSIFICATION SYSTEMS: AN ILLUSTRATIVE REVIEW


C

proximal agenesis to one segment.


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3. G

Limitations The ICA portions are numbered Limited utility for endoscopic endonasal approach. It is unsuitable for most surgical interventions, as it does Limited utility for endoscopic endonasal
against the direction of blood It disregards the clinoid segment, which possibly not consider any topographical anatomical relationships approach, although DePowell et al.5 still found it
flow. creates a blind spot when differentiating between or any surgical or endoscopic experience. helpful.
A
E A

It does not consider any extradural and intradural abnormalities. The clinoid segment can only be localized
E A

anatomical relations to the The subdivision of the supraclinoid segment into microsurgically, as it does not appear on any
artery but rather its ophthalmic, communicating, and choroidal uses clinically available imaging modalities.
5

displacement due to intracranial specific branching points as a reference. Their high The lacerum segment could be misleading since
3A

abnormalities. variability makes them unreliable anatomical the ICA does not typically cross the lacerum
5 A

It disregards some key landmarks. foramen but passes above it.


anatomical landmarks, such as
the petrous and the cervical
A
03A3 D

portions of the ICA.


AE35

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JHON E. BOCANEGRA-BECERRA ET AL.


Study Ziyal et al.6 Shapiro et al.7 Labib et al.8 Abdulrauf et al.9

Publication 2005 2014 2014 2016


www.SCIENCEDIRECT.com

year
Material and Based on 15 cadaveric head dissections using Based on cross-sectional studies and cerebral Based on bilateral endoscopic endonasal Based on cadaveric dissections of the ICA in 5
methods different surgical approaches, 5 dry skulls and 10 angiograms showing patterns of aneurysm formation dissections of 33 cadaveric specimens, along heads and CT angiography of 648 internal
bilateral angiograms from normal patients. and growth. with analysis of anatomic correlations. carotid arteries.
A

Number of 5 7 6 8
3A 35 3A3 (
3

segments
D E3

Nomenclature C1 - Cervical Cervical Parapharyngeal Cervical


(segments) C2 - Petrous Petrous Petrous Cochlear
C3 - Cavernous Cavernous Paraclival Petrous
C /
G D 2 A 3

C4 - Clinoidal Paraophthalmic Parasellar Gasserian-Clival


C5 - Cisternal Posterior communicating Paraclinoid Sellar
Anterior choroidal Intradural Sphenoid
A C

Terminus Ring
Cisternal
CA D

Main features Proposed as a classification suitable for clinical An endovascular and angiographic A description of the course of the ICA through a It may be applied uniformly to all skull base
2 E A CG ,D353 3 3A3 5 )

practice with minimal affection by anatomical description of the ICA. ventral perspective and with the help of key surgical approaches, including lateral
variations. anatomical landmarks as reference points. microsurgical and ventral endoscopic
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It is specifically designed to cater to the needs approaches.


3DC A 3 I ) GA

of endoscopic approaches. It highlights clinical information and surgical


risk to embedded structures in the
nomenclature.
Limitations Uses the PLL and distal dural ring as anatomical It uses branching points such as the PCOM and the Limited utility in transcranial microscopic It is the most numerous classification and
landmarks, which cannot be found in clinical ACA, making the classification susceptible to surgeries. introduces new terminology.
imaging. anatomical variations and unreliable for clinical use. It introduces new terminology for the

ICA CLASSIFICATION SYSTEMS: AN ILLUSTRATIVE REVIEW


C
3. G

It is based on cerebral angiograms, which lack the description of the ICA, making it potentially
microsurgical precision needed to define each confusing.
segment’s boundaries properly.
A
E A

ACA, anterior cerebral artery; ICA, internal carotid artery; CT, computed tomography; PLL, petrolingual ligament; PCOM, posterior communicating artery.
E A
5
3A
5 A
A
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The lacerum segment or C3 extends carotid angiograms from 10 normal patients the carotid foramen. Then, the “petrous
from the end of the carotid canal, where it and 1 where the ophthalmic artery arose segment” follows within the temporal
further goes above the exocranial foramen from the cavernous segment. bone and partially above the foramen lac-
lacerum, creating the lateral loop of the This classification includes 5 ICA seg- erum, containing the caroticotympanic
ICA and running upwards towards the ments, from C1 to C5, delimited by the ca- and vidian branches. Notably, Shapiro
posterior cavernous sinus. C3 ends at the rotid foramen, carotid canal, the PLL, and et al. disregarded the lacerum segment of
superior margin of the petrolingual liga- the proximal and distal dural rings the Bouthillier et al.4 classification after
ment (PLL), a continuation of the perios- (Figures 1F and 2F). First, the cervical obtaining data from the pattern
teum of the carotid canal. segment (C1) extends from the carotid formation and extension of nontraumatic
The cavernous segment or C4 begins common bifurcation to the carotid temporal bone aneurysms in such area
from the superior margin of the PLL, foramen. Then, it continues in an (those lesions either extended into the
accompanied by a venous plexus and intraosseous horizontal course as the petrous or cavernous segments but were
postganglionic sympathetic nerves. It is petrous segment (C2) until it reaches the not focal to the lacerum segment). The
subdivided into 4 smaller portions: a ver- superior border of the PLL. Importantly, “cavernous segment” starts after crossing
tical portion, a posterior bend (medial the authors reported that none of the the estimated margin of PLL and
loop of the ICA), a horizontal portion, and analyzed ICA specimens passed through following its course until the
an anterior bend. The cavernous segment the foramen lacerum, alluding to the name approximated location of the proximal
terminates at the proximal dural ring. attributed by Bouthillier et al.,4 which they dural ring. The cavernous segment is
From this point, the clinoid segment or C5 considered a misleading term. The further divided into a proximal ascending
forms the anterior loop of the ICA and superior margin of the PLL marks the segment, proximal genu, horizontal
ends at the distal dural ring (intradural entry point of the ICA into the cavernous segment, distal genu, and distal
segment of the ICA). Then, the sinus as it moves towards the proximal ascending segment—the MHT originates
ophthalmic segment or C6 follows, from dural ring, thus constituting the cavernous mainly from the posterior genu;
which 2 major arterial branches arise: the segment (C3). The clinoidal segment (C4), meanwhile, the ILT arises from the
ophthalmic and superior hypophyseal ar- a wedge-shaped portion, follows in be- horizontal segment.
teries. C6 terminates at the origin of the tween the proximal and distal dural rings The “paraophthalmic segment” extends
PCOM artery, which marks the beginning and is surrounded by the carotid collar. from the estimated distal border of the
of the communicating segment or C7—the Finally, the cisternal segment (C5) con- cavernous segment to the ostium of the
anterior choroidal artery arises from this tinues inside the subarachnoid space and PCOM artery, which in turn demarcates
portion. Lastly, C7 ends at the terminal terminates at the ICA bifurcation into the the beginning of the “posterior commu-
bifurcation of the ICA. anterior and middle cerebral branches. The nicating segment.” The latter extends to-
main branches of the C5 segment include wards the anterior choroidal artery. The
An Anatomic Study With Angiographic the superior hypophyseal, ophthalmic, “anterior choroidal segment” is delimited
Interpretation PCOM, and anterior choroidal arteries. around the choroidal ostium, and ulti-
In 2005, Ziyal et al. noticed that systems mately, the “terminus segment” surges
relying on the arterial blood flow without An Endovascular Classification System beyond the choroidal ostium and finishes
considering anatomical variations could The need for an optimized endovascular in the terminal ICA bifurcation.
mislead the ICA nomenclature. For perspective of the ICA drove Shapiro et al.
example, the ophthalmic artery had been to publish a new nomenclature in 2014. An Endoscopic Perspective of the ICA
reported to be originated in the clinoidal The authors proposed a system based on The emerging use of the endoscopic
segment, the cavernous segment, and, cerebral angiograms (depicting the aneu- endonasal approach to treat lesions in the
rarely, in the middle meningeal ar- rysm formation and growth patterns in the median sagittal and paramedian plane
tery.2,11-13 Therefore, they aimed to ICA) and cross-sectional studies from the inspired authors to contemplate a more
establish a nomenclature with clinical New York University Langone Medical comprehensive ICA nomenclature from
utility and minimal affection by Center and associated hospitals.7 this standpoint. On the other hand, the
anatomical variations, based on constant The system divides the ICA into 7 seg- limited attributions of the endoscope op-
anatomical structures such as bone, ments without an alphanumeric order tics, namely, bidimensional view and
dura, and dural/periosteal folds.6 following the arterial blood flow: cervical, barrel-type spatial distortion, made it
Ziyal et al. dissected the ICA course in 15 petrous, cavernous, paraophthalmic, pos- challenging to extrapolate microsurgical
cadaveric heads with microfilm examina- terior communicating, anterior choroidal, anatomy into the ventral view of the ICA
tion under the pterional, orbitozygomatic, and terminus segments (Figures 1G and under the endoscope.
subtemporal, subtemporal-infratemporal, 2G). Due to angiography limitations to Labib et al. conceived a reliable system
petrosal, transsphenoidal, transbasal, and visualize the PLL and dural ring, some of attending the endoscopic issues regarding
transfacial approaches. Also, 5 dry skulls the hallmark points for segmentation the distortion of distance and perspective
allowed the bilateral study of bone land- had to be estimated based on previous concerning the vessel course.8 Although
marks, including the foramen lacerum, microsurgical classifications. not a pioneered system from the
sphenoid, petrous, and occipital bones. First, the “cervical segment” extends endonasal endoscopic approach, the
Moreover, the ICA trajectory was revised in from the common carotid bifurcation to previous efforts had lacked accuracy and

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Figure 1. Lateral view of the internal carotid artery (ICA) Labib et al.8 (H); Abdulrauf et al.9 (I). ACA, anterior cerebral
classification systems. Basal illustration showing anatomical artery; ILT, inferolateral trunk; MHT, meningohypophyseal trunk;
landmarks and branches of the ICA (E). ICA classification Oph, ophthalmic artery; PCOM, posterior communicating artery;
systems: Fischer1 (A); Gibo, Lenkey and Rhoton2 (B); Lasjaunias PLL, petrolingual ligament.
et al.3 (C); Bouthillier et al.4 (D); Ziyal et al.6 (F); Shapiro et al.7 (G);

46 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2022.03.116

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Figure 2. Anterior view of the internal carotid artery (ICA) Labib et al.8 (H); Abdulrauf et al.9 (I). ACA, anterior cerebral
classification systems. Basal illustration showing anatomical artery; ILT, inferolateral trunk; MHT, meningohypophyseal trunk;
landmarks and branches of the ICA (E). ICA classification Oph, ophthalmic artery; PCOM, posterior communicating artery;
systems: Fischer1 (A); Gibo, Lenkey and Rhoton2 (B); Lasjaunias PLL, petrolingual ligament.
et al.3 (C); Bouthillier et al.4 (D); Ziyal et al.6 (F); Shapiro et al.7 (G);

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relied on highly variable anatomic superior limit of the medial petrous apex structures: the styloid process, cochlea,
structures.14 Hence, this novel system and the upper edge of the petroclival the ET, PLL, abducens nerve, trigeminal
aimed to understand the ICA anatomy fissure up to the level of the proximal nerve, Gasserian ganglion, the MHT, the
from a ventral endonasal perspective, dural ring of the ICA. The sellar floor is trochlear nerve, and the oculomotor nerve.
provide a relevant classification to the highlighted as a key landmark. Radiologically, 324 (648 sides) adult
expanded endoscopic approaches, and The paraclinoid segment originates consecutive axial computed tomography
identify landmarks for each ICA from the proximal to the distal dural ring. angiography images (excluding cases with
segment. Thus, helping to improve The bony landmarks in this short segment noted pathology) from the author’s
technical dexterity and diminishing the include the lateral tubercular recess, the respective institutional radiology database
risk of ICA injury. medial opticocarotid recess, the distal in conjunction with the skeletal associa-
The course of the ICA was carefully osseous arch, and the lateral opticocarotid tions of the ICA to the styloid process
observed through bilateral endoscopic recess. Importantly, these osseous pa- base, clivus, sella, vidian canal, cochlea,
endonasal dissections of 33 cadaveric rameters are crucial during the resection and sphenoid sinus were analyzed. Studies
specimens. Morphometric analyses were of intradural lesions. with limited image quality for analysis
made in 24 ICAs. The common carotid Finally, the intradural segment of the were excluded.
arteries, vertebral arteries, and internal ICA travels from the distal dural ring, The ICA was divided into 8 segments
jugular veins were injected with colored within the subarachnoid space, and ends according to cadaveric and radiologic im-
siloxane/silicone material. As a result, the at the bifurcation into the anterior and aging findings. Such segments were
ICA was divided into 6 segments in the medial cerebral arteries. identified according to anatomical land-
direction of blood flow, starting from the Although this system brought a clear marks that correlated to each ICA por-
bifurcation of the carotid artery and understanding of the ICA anatomy under tion’s origin and termination (Figures 1I
ending at the distal dural ring. The an endoscopic perspective, it also created and 2I). Thus, the cervical segment
nomenclature referred to cranial base new terminology. In parallel, DePowell constitutes the first subdivision and
compartments surrounding the ICA as et al. re-examined Bouthillier et al.‘s follows the analog course of previous
viewed from a ventral perspective. Named classification,4 which had already achieved microsurgical classification systems.
from proximal to distal: the para- widespread use, under the transnasal Then, the cochlear segment (the
pharyngeal, petrous, paraclival, parasellar, endoscopic approach to preserve the ascending segment of the ICA in the
paraclinoid, and intradural segments existing terminology and expand its temporal bone) starts from the base of
(Figures 1H and 2H). universal application. Upon testing their the styloid process towards the ET. The
First, the parapharyngeal segment ari- hypothesis, the authors suggested the petrous segment (the horizontal segment
ses from the common carotid artery preservation of the terminology could be of the ICA in the temporal bone) begins
bifurcation, runs within the carotid extrapolated to the endoscopic approach at the crossing of the ET superolateral to
sheath, and ends at the external orifice of and avoid new terms.5 the ICA turn, from vertical to horizontal
the carotid canal of the petrous bone. at the genu. The Gasserian-Clival
Corresponding surgical landmarks include A System With Potential Use in segment (the ascending segment of ICA
the eustachian tube (ET), the fossa of Microsurgical and Endoscopic in the cavernous sinus) starts at the
Rosenmüller, and levator veli palatini. Approaches proximal portion of the PLL and ends at
The petrous segment extends from the Abdulrauf et al. provided a clinical meth- the MHT. The sellar segment (the medial
external orifice of the carotid canal, travels odology to the uniform application of skull loop of ICA in the cavernous sinus) starts
vertically, and continues on 3 planes: base surgical approaches, including lateral at MHT. Then, the sphenoid segment (the
posterior-to-anterior, inferior-to-superior, microsurgical and ventral endoscopic lateral loop of ICA within the cavernous
and lateral-to-medial towards the postero- procedures. Additionally, this nomencla- sinus) continues after crossing the troch-
lateral edge of the exocranial surface of the ture proposes the extrapolation of clinical lear nerve on the lateral aspect of the
foramen lacerum. Along with this segment, information to potential surgical injuries cavernous ICA located directly lateral to
key landmarks include the pterygoid wedge, involving structures proximal to the ICA.9 the sphenoid sinus. The ring segment,
the mandibular division of the trigeminal Anatomic and radiologic aspects were composed between the 2 dural rings,
nerve, and the vidian nerve/artery. considered. Anatomically, the authors starts at the crossing of the oculomotor
The paraclival segment extends from used 5 human head cadaveric dissections nerve on the lateral aspect of the ICA.
the posterolateral aspect of the foramen of the ICA (10 sides in total), which un- Finally, the cisternal segment continues at
lacerum to the superior limit of the medial derwent formalin fixation. Visualization of the distal dural ring.
petrous apex. This segment has 5 surfaces: arterial and venous systems was enhanced
anterior, medial, posterior, lateral, and via red and blue latex inoculation via the
inferior. Important landmarks include the cervical segment of the ICA and internal DISCUSSION
ICA sock, the roof of the fossa of Rose- jugular vein at vertebral level C6. Micro- This illustrative review described the his-
nmüller, paraclival protuberance, and fo- scopy aided in the inspection and demar- torical attempts to create a unified
ramen rotundum. cation of the ICA anatomical course. nomenclature version of the ICA.
The parasellar segment, embedded in Associations between the ICA were Although the pioneered ICA system from
the cavernous sinus, extends from the appraised against the following landmark Fischer had anatomical limitations and

48 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2022.03.116

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LITERATURE REVIEW
JHON E. BOCANEGRA-BECERRA ET AL. ICA CLASSIFICATION SYSTEMS: AN ILLUSTRATIVE REVIEW

lacked broad clinical applicability, it which is important for marking the tran- 5. Depowell JJ, Froelich SC, Zimmer LA, et al. Seg-
ments of the internal carotid artery during endo-
motivated the subsequent development of sition from intradural to extradural space.
scopic transnasal and open cranial approaches:
nomenclatures addressing different It has also been neglected since it is not can a uniform nomenclature apply to both? World
radiographic, endovascular, and neuro- visible on any clinical imaging modalities Neurosurg. 2014;82:S66-S71.
endoscopic needs. At the same time, the and only localized microsurgically,
6. Ziyal IM, Özgen T, Sekhar LN, Özcan OE,
sophistication of neurosurgical technology requiring additional research sources Çekirge S. Proposed classification of segments of
has shaped the ICA anatomy from other than radiologic imaging. These as- the internal carotid artery: anatomical study with
different perspectives, which has resulted pects are some of the considerations that angiographical interpretation. Neurol Med Chir
(Tokyo). 2005;45:184-190.
in heterogeneous denominations and should made when using the different ICA
confusion among health care pro- classifications. Further potential issues 7. Shapiro M, Becske T, Riina HA, et al. Toward an
fessionals, trainees, and students. that could arise when applying each ICA endovascular internal carotid artery classification
While the classifications mentioned classification are listed in Table 1. system. Am J Neuroradiol. 2014;35:230-236.
above offer unique and invaluable insight
8. Labib MA, Prevedello DM, Carrau R, et al. A road
into the structure and path of the ICA, map to the internal carotid artery in expanded
they also meet with some difficulties in CONCLUSIONS endoscopic endonasal approaches to the ventral
finding the best method to subdivide it Our graphical description of multiple ICA cranial base. Neurosurgery. 2014;10(Suppl 3):
448-471.
into segments in a way that is anatomically systems provides a rapid neuroanatomic
accurate, physiologically meaningful, consultation tool and highlights the 9. Abdulrauf SI, Ashour AM, Marvin E, et al. Pro-
clinically applicable to more than 1 surgi- importance of effective communication in posed clinical internal carotid artery classification
system. J Craniovertebr Junction Spine. 2016;7:161-170
cal approach, as well as reliable in cases of academic settings. We also believe the
[Published correction appears in J Craniovertebr
anatomic variations. Fischer’s numerical future application of augmented reality Junction Spine. 2017;8:84.].
segmentation of the ICA against the di- software for improved visuospatial orien-
rection of blood flow, the disregard for tation of the ICA systems might help in 10. Lasjaunias P, Berenstein A. Arterial anatomy:
introduction. In: Surgical Neuroangiography: Func-
topographic relations to the artery, and the providing a more entertaining learning tional Anatomy of Craniofacial Arteries. Berlin:
limited source of information he used to experience, although useful 3-dimensional Springer-Verlag; 1987:1-32.
create the first ICA classification have only models are already available.15
marked a small number struggles that Ultimately, the knowledge of the ICA 11. Kyoshima K, Oikawa S, Kobayashi S. Interdural
origin of the ophthalmic artery at the dural ring of
future author would encounter. Another anatomy based on a single system may be the internal carotid artery. Report of two cases.
significant point for concern has proven to both convenient and suboptimal; however, J Neurosurg. 2000;92:488-489.
be the limited application of the classifi- understanding it through our comparative
12. Liu Q, Rhoton AL Jr. Middle meningeal origin of
cations from Gibo et al., Bouthillier et al., description will help to sum up the
the ophthalmic artery. Neurosurgery. 2001;49:
and Ziyal et al. as they do not consider the strengths of each nomenclature for better 401-407.
ICA anatomy through a ventral perspec- anatomic appraisal, operative perfor-
tive, nor do they account for the differ- mance, and easier communication. 13. Renn WH, Rhoton AL Jr. Microsurgical anatomy
of the sellar region. J Neurosurg. 1975;43:288-298.
ences in the view through a microscope
and an endoscope such as the altered ACKNOWLEDGMENTS 14. Alfieri A, Jho HD. Endoscopic endonasal
depth-perception and the barrel type cavernous sinus surgery: an anatomic study.
spatial distortion created by the bi- We would like to thank “Cura Canaz Neurosurgery. 2001;48:827-836 [discussion: 836-
dimensional view of an endoscope. This Medical Arts” for its essential and indis- 837].

makes the previously mentioned classifi- pensable role in illustrating this work.
15. Melé MV, Puigdellívol-Sánchez A, Mavar-
cations inapplicable to endoscopic endo- Haramija M, et al. Review of the main surgical and
nasal surgical approaches and limits them REFERENCES angiographic-oriented classifications of the course
of the internal carotid artery through a novel
to be only relevant to transcranial micro- 1. Fischer E. The positional deviations of the anterior interactive 3D model. Neurosurg Rev. 2018;43:
surgical approaches. On the other hand, cerebral artery in angiograms [Die Lageabwei- 473-482.
chungen der vorderen hirnarterie im crefassbild].
the ICA classifications from Labib et al. Zentralbl Neurochir. 1938;3:300-313.
and Shapiro et al. were explicitly designed
Conflict of interest statement: Dr. G. Canaz is affiliated with
to be applicable to endoscopic surgeries, 2. Gibo H, Lenkey C, Rhoton AL Jr. Microsurgical “Cura Canaz Medical Arts.” The authors declare no other
as those were primarily based on endo- anatomy of the supraclinoid portion of the inter- conflict of interest.
nal carotid artery. J Neurosurg. 1981;55:560-574.
scopic endonasal dissections and cerebral Received 19 January 2022; accepted 26 March 2022
angiograms, which in turn made them not 3. Lasjaunias P, Santoyo-Vazquez A. Segmental Citation: World Neurosurg. (2022) 163:41-49.
precise enough to be used in transcranial agenesis of the internal carotid artery: angio- https://doi.org/10.1016/j.wneu.2022.03.116
surgical interventions. graphic aspects with embryological discussion. Journal homepage: www.journals.elsevier.com/world-
Furthermore, some ICA classifications Anat Clin. 1984;6:133-141. neurosurgery
have failed to recognize essential land- Available online: www.sciencedirect.com
4. Bouthillier A, Van Loveren HR, Keller JT. Seg-
marks for their description of the ICA ments of the internal carotid artery: a new clas- 1878-8750/$ - see front matter ª 2022 Elsevier Inc. All
course, such as the clinoid segment, sification. Neurosurgery. 1996;38:425-433. rights reserved.

WORLD NEUROSURGERY 163: 41-49, JULY 2022 www.journals.elsevier.com/world-neurosurgery 49

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