Abstract

Background: The internal carotid artery (ICA) has multiple classification systems; it is essential for brain blood supply, which has bone/neurovascular relationships of wide neurosurgical interest; its anatomy must be known in detail, its angiographic-imaging aspect (endovascular), its ventral aspect (endoscopic endonasal approaches); and its lateral aspect (anterolateral skull base surgery). Our objectives were to identify coincidences/differences between the main classifications of the ICA to improve its surgical-anatomical understanding, unify the terminology of ICA segments, avoid confusion, and carry out a simple description.

Methods: There are differences between classifications; however, these may overlap each other and determine the correspondence between segments, regardless of their purpose. Literature on ICA classifications was reviewed; a cadaver endonasal endoscopic and anterolateral skull base dissection was performed, obtaining representative images of the ICA, as well as angiography. The main terminology of ICA segments was collected, and artistic-anatomical illustrations were created to facilitate the study of ICA.

Results: We compared the endoscopic roadmap to the ICA by Labib/Kassam, the extradural ICA at its lateral aspect by Cherian, and the classic classification by Bouthillier (as well as a small reference to the classification by Gibo/Rhoton). We found the shared characteristics and differences between classifications, with a total of 17 interrelated segments, with a variety of nomenclature and anatomical extension. Initially, we except the extradural ICA by Cherian because it uses almost the same nomenclature that Labib, varying in one segment, which coincides with the nomenclature of Bouthillier and does not change the total summary. The initial and terminal segments were nominative/anatomically equivalent, and there is anatomical nominal variation in the intermediate segments and its relation/correspondence has been easily demonstrated.

Conclusion: Anatomical knowledge of all aspects of ICA using its main classifications, the relation between them, and its diversity of nomenclature is essential to improve its anatomical-surgical understanding and avoid anatomical nominal confusion. It can be achieved through our comparative tables/illustrations.

Keywords: Classifications, Endonasal endoscopy, Internal carotid artery, Lateral skull base

INTRODUCTION

The internal carotid artery (ICA) is a critical structure for cerebral blood supply and has complex bone and neurovascular associations that are of significant interest in neurosurgery.[ 1 , 2 ] Beyond common vascular pathologies such as aneurysms and ICA stenosis,[ 3 , 4 ] the ICA is responsible for supplying key anatomical structures such as the pituitary gland and cranial nerves (Trigeminal V1 and V2).[ 5 , 6 , 10 ] In addition, the craniofacial and upper cervical regions benefit from its anastomotic connections with the external carotid artery.[ 7 ]

Since Fischer’s 1938 classification[ 17 ] based on angiographic features and arterial pathways, numerous segmentation systems have been proposed, ranging from simple to highly detailed, depending on their objectives.[ 8 , 9 , 11 , 12 ] Early classifications by Gibo et al. (1981)[ 21 ] and Rhoton[ 21 ] provided foundational descriptions for microsurgical approaches. However, the 1996 Bouthillier classification significantly streamlined the segmentation system to align with both angiographic observations and microvascular transcranial methods, making it the most widely adopted classification system globally.[ 4 , 22 ]

Advancements in surgical techniques, including skull base surgery and endoscopic endonasal approaches, have introduced new perspectives on the ICA’s anatomy, particularly its ventral aspect.[ 9 , 18 , 19 , 23 - 26 ] Moreover, the application of exoscope technology[ 13 , 14 , 20 ] offers a magnified 3D view, further expanding surgical access to the anterolateral skull base and enhancing the understanding of ICA’s relationships with adjacent structures. These innovations challenge the universality of the Bouthillier classification, as its two-dimensional angiographic framework does not fully encompass the endoscopic or exoscopic perspectives.[ 9 , 27 , 28 ]

Given these developments, neurosurgeons must extend their anatomical expertise beyond traditional classifications to include the lateral and ventral ICA aspects. This study focuses on three key classification systems to minimize confusion: the Bouthillier system, the “Road Map to the ICA” described by Labib and Kassam in 2014,[ 29 - 33 ] and the extradural ICA segmentation in the lateral skull base context, published in 2020.[ 7 ] By correlating these frameworks, the paper aims to simplify the study of ICA anatomy and reduce the terminological and structural ambiguities that can complicate neurosurgical applications.

MATERIALS AND METHODS

There are several differences between the multiple classifications of the ICA; however, we deduced that these may overlap each other and determine the correspondence and variations between their segments, stablishing a relation between them, regardless of their purpose. In a similar way to our “Trinity” title, we divided this research into three steps being the first one, an extensive literature review on ICA classifications; the second one, a cadaver endonasalendoscopic and anterolateral skull base dissection study obtaining representative images; and last one we collected the main terminology of ICA segments and created schematic tables and original artistic anatomical illustrations to facilitate the anatomical surgical study of the ICA.

Literature review on ICA classifications

An extensively literature review on ICA classifications systems was performed, where all the significant classifications and related papers reported since the first description by Fischer[ 17 ] were reviewed [ Table 1 ], but focusing and being emphatic on the three chosen classifications for this paper: (1) the roadmap to the ICA by Labib/Kassam[ 33 ] which fully cover the endonasal endoscopic extended approaches to the ventral cranial base, (2) the classification of Bouthillier[ 4 ] which describe the seven classic segments of the ICA, that it’s strongly consisting with the first historical reported classification in the literature and others,[ 3 ] and fully cover several of the most important anatomical relationships/landmarks useful for the microsurgical/microvascular transcranial approaches and endovascular procedures; and finally (3) the classification described by Cherian[ 7 ] about the extradural ICA segments in relation to the anterolateral skull base, which fully covers bone and neurovascular relationships in the lateral aspect of the ICA (this last one actually is independent related to the first mentioned classification, because due to the similarity of terminology can be easily used also in the endonasal endoscopic view and works as an excellent complementation with each other both classifications) must be noticed that we added small changes to this last classification with the permission of the author and which also resulted in an easy way to understand the lateral triangles of the middle fossa and the vascular supply from the ICA [ Figure 1 ].

Figure 1:

Extradural internal carotid artery (ICA) anterolateral skull base classification (Cherian): segmentation of the ICA in this classification, which uses anatomical relationships to name each segment and follows the contrary direction to the blood flow, clarifying this order according to the fact that since the neurosurgeon performs many cranial approaches, he is usually more familiar first with the terminal segments and lastly with the proximal segments “For the neurosurgeon the brain comes first” referring to ICA terminal segments (Personal communication) and also being consistent with the chosen direction in the first historical classification,[ 18] with a total of six segments (Parapharyngeal, petrous, paraclival, cavernous, paraclinoid, and intradural), and mainly describe the extradural ICA and surgical landmarks at its lateral aspect, usefulness for all extradural anterolateral skull base approaches. (a) The vertical segments (“Tubes”/Odds) in green, and the horizontal segments (“Suppliers”/Evens) in red are shown; the direction of each segment can also be seen in relation to the depth and anteroposterior aspect (arrows); O: Ophthalmic artery, SP: Superior pituitary artery, McC: McConell capsular arteries, ILT: Inferolateral trunk, MHT: Meningohypophyseal trunk, CTp: Carotid tympanic artery, V: Vidian artery. (b) Bone and ligament relationships (anterior and posterior) of the ICA (Clivus and cochlea are in the same sagittal plane of the corresponding segment, and the rest of the structures are lateral to the ICA. Anterior clinoid process (ACP); posterior clinoid process (PCP). (c) Extension of the cavernous sinus (shaded in blue) covering the distal part of the paraclival segment, the entire cavernous segment, and the proximal part of the paraclinoid segment; level of the proximal (PDR) and distal (DDR) dural rings (blue dotted lines in the distal part of the paraclinoid segment) and arrangement of the cranial nerves: oculomotor (III) in the roof of the cavernous sinus (RCS), trochlear (IV), trigeminal (V) and its ophthalmic (V1), maxillary (V2) and mandibular (V3) branches. The lateral wall of the cavernous sinus (LCS) includes cranial nerves IV, V1, and V2; the greater superficial petrosal nerve (GSPN) predicts the direction of the petrosal segment. (d) Representation of the triangles of the anterolateral skull base, highlighting the delimitation of the edges corresponding to the nervous structures; Dolenc (1); Supratrochlear (2); Parkinson (3); Mullan (4); Anterolateral (5); Kawase (6); and Glasscock (7). The limits of each segment are detailed in Table 3. C2 (intradural), C3 (paraclinoid), C4 (cavernous), C5 (paraclival), C6 (petrous), C7 (parapharyngeal).

Table 1:

Some of the main classifications of the ICA described by different authors over the years and its

Cadaver dissection study

We performed cadaver dissection in a total of 4 cadavers in two different laboratories of surgical anatomy. In one of the laboratories, the endoscopic endonasal approaches were performed in two injected cadaver specimens obtaining relevant pictures of the dissection of the ventral aspect of the ICA considered the segmentation by Labib/Kassam.[ 9 , 33 ] The approaches of the anterolateral skull base and middle fossa triangles were realized separately in another laboratory of surgical anatomy in two more injected cadaver specimens, taking into consideration the description of the extradural ICA by Cherian.[ 7 ] It should be noted that for the corresponding aspect to the Bouthillier[ 4 ] classification, no cadaver dissection was performed, but we used just original illustrations and an angiographic image (obtained and modified with permission of the author from the National Service of Radioneurosurgery of the Occidental National Medical Center in Guadalajara City, Mexico) what it is described in [ Figure 2 ].

Figure 2:

Bouthillier classification: Segmentation of the ICA in this classification, which uses an alpha numerical system and follows the direction of the blood flow, with a total of 7 segments (C1: Cervical, C2: Petrous, C3: Lacerum, C4: Cavernous, C5: Clinoidal, C6: Ophthalmic and C7: Communicating), being consistent with the first classification of the ICA (Fischer) and considering vascular and bone-ligament landmarks for the delimitation and name of each segment. (a) Angiography and ascending catheterization of the ICA, where its course and loops “knees” are shown, and the extension of the corresponding segments is delimited; (b) Schematic illustration of the ICA, delimiting each of the segments of the ICA according to this classification. ICA: Internal carotid artery.

The first part of the cadaveric dissections corresponding to the endonasal endoscopic dissection for the ventral aspect of the ICA was performed in the Laboratory of Surgical Neuroanatomy of the Faculty of Medicine of La Salle University in México City, taking advantage of the facilities and the special endoscopic instrumental available provided by the professor of the skull base fellowship course. We performed fully extended approaches to the ventral cranial base in two cadavers, these had been previously preserved by formalin fixation and injected intravascularly with colored silicon (red for arteries and blue for veins). Specific endoscopic instruments were used (endoscopes with 0° and 30° lens cameras, and special endoscopic instruments such as drills and microdissectors, etc.) to approach from cephalic to caudal, the cribiform plate, floor of the sela, optic carotid recesses, upper, middle and lower clival and paraclival regions, the petrous apex, the pterygopalatine and infratemporal fosses and the odontoid process. The cadavers were fully endonasal endoscopically dissected, managing to obtain a great panoramic billaterally “landscape” exposureof the full extradural trajectory of the ICA in its ventral aspect, and representative images were taken, to delimitate the segments described by Labib/Kassam,[ 33 ] managing to highlight some of the most important surgical landmarks in this aspect [ Figure 3 ].

Figure 3:

Endonasal endoscopic classification (Labib/Kassam): Segmentation of the ICA in this classification, which uses anatomical relationships for name each segment and follows the direction of the blood flow, with a total of 6 segments (Parapharyngeal, Petrous, Paraclival, Parasellar, Paraclinoid and Intradural), and mainly describe the extradural ICA and surgical landmarks at its ventral aspect, usefulness for all the endonasal endoscopic approaches. (a) Inferior segments of the right ICA: Parapharyngeal, Petrous (After removal of the carotid canal), and proximal paraclival segment (Equivalent to C3/Lacerum segment) and its relations with the cartilaginous portion of the Eustachian tube . (b) Superior segments of the right ICA: Distal paraclival segment, parasellar segment and paraclinoid segment and its relations with the clivus and the sellar region. (c) Panoramic endonasal endoscopic view of the dissection showing both ICA, highlighting each of its extradural segments and its extension (right ICA) and pointing out some of the most relevant landmarks; optic nerve impression (ONI); lateral opticocarotid recess (LOCR); medial opticocarotid recess (MOCR); opticocarotid point (1); caroticosellar point (2); Divisions of the clivus (dotted white lines); distal dural ring (purple dotted line) in the left ICA; proximal dural ring (green dotted line) in the left ICA. (d) Bottom of the right infratemporal fossa, showing the parapharyngeal ICA showing its relationship with the lower cranial nerves, noted the XI and XII cranial nerves medial to the ICA, and the IX cranial nerve, internal jugular vein (IJV), and styloid process (SP) lateral to the ICA. (e) the vagus nerve is observed posterior to the ICA, as it is medially mobilized. ICA:Internal carotid artery.

The second part was performed in the Aesculap Academy, Cadaver Laboratory of Neurosurgery at the Institute of Neurosciences, Krishna Vishwa Vidyapeeth in Karad, under magnification of a surgical microscope and using customized microsurgical instruments from the laboratory for the dissection, two cadavers previously fixed and injected with colored liquid latex, red color for arteries and blue color for veins, were surgically dissected at the anterolateral skull base; Dolenc approach, Dolenc modified approach, trans cavernous, and Kawase approaches were fully performed using microsurgical instruments and high speed motorized drill, uncovering the whole anatomy of the lateral skull base and the relation between bone structures, cranial nerves and other landmark nerves, as well as the triangles of the middle fossa related to the extradural segments of the ICA described by Cherian, obtaining representative images of the mentioned anatomy in a simulation of surgical approaches, as well as a courtesy from one of the authors (Prof. Gervith Reyes); we count with images of full cadaver dissection of the course of the ICA and its relation with the cranial nerves that were modified with his permission [ Figure 4 ].

Figure 4:

Extradural internal carotid artery (ICA) anterolateral skull base cadaver dissections: (a) colored picture of the extradural surgical dissection of the lateral wall of the left cavernous sinus with the trochlear, ophthalmic, and maxillary nerves (IV, V1, and V2) and the relation with the ICA medial to the nerves (Cavernous segment), superiorly can be seen the III cranial nerve in the roof of the cavernous sinus, and superior to the ICA the optic nerve (II) and inferiorly and lateral to the ICA can be seen the Gasserian ganglion (GG) and its mandibular branch (V3). (b) Sequential photograph added representation of the course of the left ICA (red, bright shadow) and the alpha numeric segments in relation to the lateral aspect according to the classification of figure 3; intradural (C2), paraclinoid (C3), cavernous (C4), paraclival (C5), and petrous (C6); *Distal dural ring. (c) Full dissection of anterolateral skull base cadaveric specimen with injected ICA, showing the optic, oculomotor, trochlear, and ophthalmic (II, III, IV, and V1, respectively) going in the direction of the optic canal and into the orbit, together with the abducens nerve (VI) of which its trajectory is shown highlighted in yellow, including its passage through the Dorello’s canal (*) also can be seen the triangles (highlighted with a light green shade) that are in direct relation to the ICA: posterior to the ICA and its anterior edge being the petrosal segment, the Kawase triangle with the facial nerve (VII) inside; lateral and posterior to the ICA the Parkinson’s and the supratrochlear (Spt) triangles, containing the cavernous segment and the abducens nerve; and anterior and medial to the paraclinoid segment is the clinoid triangle (Clin). (d) Sequential figure, the trigeminal nerve, and gasser ganglion have been sectioned and reflected anteriorly, exposing the complete path of the ICA from the petrous segment (C6), passing through the paraclival (C5), cavernous (C4), and paraclinoid (C3) segment, to the intradural segment. The cranial nerves are highlighted in yellow and the petrosphenoidal ligament has been exposed (*). Note that the facial nerve has been exposed, and its trajectory can be observed in the direction of the stylomastoid foramen. (e) An overview of the extradural dissection of the lateral wall of the cavernous sinus in transcavernous approaches in cadaver, showing the rest of the triangles of the lateral aspect and the disposition of the cranial nerves from the optic to the facial and vestibulocochlear nerves inside of the Kawase triangle. Notice that this classification and approach does not usually reach the parapharyngeal segment and the lower cranial nerves, as shown below in the ventral by the endoscopic endonasal approach to the bottom of the subtemporal fossa in Figures d and e. Therefore, both classifications can be used perfectly in a complementary manner to determine the positions of all cranial nerves (except the olfactory nerve) with respect to the ICA among other relevant surgical landmarks.

Main terminology of the ICA and creation of comparative tables and original illustrations

Looking for the coincidences and differences of the segments of the ICA (nominatively and anatomically), the terminology of three main classifications was collected (Gibo and Rhoton,[ 21 ] Bouthillier[ 4 ] and Labib/Kassam[ 33 ]); initially and to avoid confusion, we did not include the extradural ICA described by Cherian et al.,[ 7 ] due to its terminology similarity with the segmentation proposed by Labib et al.[ 33 ] which did not affect the total sum of segments). We put and organize all the information together in a schematic table with color code (red, blue, and yellow shaded), looking for the specific extension of each segment in each classification and comparing it with the others, finding relevant data, and simplifying the information. We use the original illustrations with color code for each classification to make easier the understanding of each segment in the comparison of the classifications [ Figure 5 ]; a new version of the illustration for the anterolateral aspect of the ICA at the skull base was created, taking as a reference the original schematic illustration of the work by Cherian et al.[ 7 ] preserving the simplicity and facility of the original version, but changing with permission of the author, the color code, the orientation of the names of each segment according to its anatomical direction, and a new complementary system called “tube and suppliers” was added to this classification [ Figure 1 ] were the “tube” correspond to the vertical segments and doesn’t provide branches, and the “suppliers” correspond to the horizontal segments and provide branches as follows: petrous segment provides vidian and carotid tympanic arteries; cavernous segment provides meningohypophyseal and inferolateral trunks, and the McConell capsular arteries; and the intradural segment provides the ophthalmic and the superior pituitary arteries.

Figure 5:

Total sum of segments of three classifications. (a) Rhoton and Gibo Classification: 1. cervical, 2. petrous, 3. cavernous, 4. supraclinoid; (b) Labib and Kassam classification: 5. parapharyngeal, 6. petrous, 7. paraclival, 8. parasellar, 9. paraclinoid, and 10. intradural; (c) Bouthillier classification: 11. cervical, 12. petrous, 13. lacerum, 14 cavernous, 15. paraclinoid, 16. ophtalmic, and 17. communicating. Notice that the initial segments (1, 5, 11) and the terminal segments (4, 10, 17) are extensively equal in all the classifications, and the terminal segments correspond to the intradural portion of the internal carotid artery.

Finally, a complex schematic anatomical illustration of the lateral aspect of the ICA was created, including the main anatomical details, bone and neurovascular relationships, and surgical landmarks of the ICA, resulting in the limits of the triangles of the middle fossa, managing to combine the main elements of each classification for the final understanding of the vessel.

RESULTS

We compared the endoscopic roadmap to the ICA by Labib/Kassam,[ 33 ] the extradural ICA at its lateral aspect by Cherian,[ 7 ] and the classic classification by Bouthillier,[ 4 ] with a brief reference to Gibo/Rhoton’s[ 21 ] classification. Our analysis identified 17 interrelated segments with notable variations in nomenclature and anatomical extension [ Figure 5 and Table 2 ]. While the extradural ICA classification by Cherian et al.[ 7 ] shows nominal variation in one segment compared to Labib et al.,[ 33 ] it aligns with Bouthillier[ 4 ] in the same segment without affecting the results.

Table 2:

Trinity of the internal carotid artery

We found the initial and terminal segments to be anatomically and nominatively equivalent across classifications [ Table 2 ]. Two interrelated names for the initial segment, cervical and parapharyngeal, share identical anatomical boundaries (from the common carotid bifurcation to the external carotid canal) [ Table 3 ]. For the terminal segment, three interrelated names, supraclinoid, intradural, and communicating, were equivalent in anatomical extension, making “Intradural” a practical term for consistent use across classifications. Its proximal boundary (entry into the dura after the distal dural ring) and distal boundary (ICA bifurcation into terminal branches) remain constant [ Table 3 ]. Excluding the initial and terminal segments, we observed variations in intermediate segments, which were clearly illustrated with color-coded tables [ Tables 2 and 3 ]. Using Gibo and Rhoton’s classification as the base, we assigned Labib = 1, Bouthillier = 2, and Cherian = 3. Key findings include: C2 (Rhoton): covers the petrous and paraclival carotid in Classifications 1 and 3, comparable to segments C2 and C3 (lacerum/proximal paraclival) in Classification 2. C3 (Rhoton): covers the parasellar and paraclinoid carotid in Classification 1, segments C4, C5, and C6 in Classification 2, and the cavernous and parasellar/paraclinoid segments in Classification 3.

Table 3:

Trinity of the internal carotid artery

Nomenclature and anatomical overlap were observed between intermediate segments in Classifications 1 and 3, particularly petrous, paraclival, parasellar, and paraclinoid segments. Pure nominative coincidence was seen in the cavernous segment across Rhoton, Bouthillier, and Cherian classifications. The petrous segment was the only universally constant segment, anatomically and nominatively, across all classifications, although Rhoton’s petrous segment had a greater extension [ Table 3 ].

Furthermore, we established that cranial nerves associated with the parapharyngeal ICA in the ventral aspect (Classification 1) [ Figure 3 ] complement those related to the extradural ICA segments in Classification 3 [ Figures 1 and 4 ]. This demonstrates that the classifications, rather than competing, function as complementary systems, enhancing surgical landmarks for neural, vascular, and bony structures, including ligaments, the cavernous sinus (CS), and lateral middle fossa triangles [ Figure 6 ]. This integrated approach provides valuable anatomical and surgical insights.

Figure 6:

The lateral aspect of the right internal carotid artery (ICA) shows vital relationships with the upper and middle cranial nerves, cavernous sinus, pituitary gland, clinoid processes, optic strut, sella turcica, petrolingual ligament, petrous bone, clivus, internal jugular vein, and lower cranial nerves. The annulus of Zinn and its contents, marked by green dotted oval lines, frame key anatomical landmarks. Endonasal endoscopic segmentation highlights neural, vascular, and bony relationships, including the carotid plexus joining the greater superficial petrosal nerve (GSPN) to form the vidian nerve. Trigeminal structures (Gasserian ganglion, Meckel’s cave and branches V1, V2 and V3) are also closely associated. The abducens nerve (dotted yellow line) is the only one intracavernous nerve, and the proximal and distal dural rings (PDR, DDR) define the ICA’s dural boundaries for, critical for surgical precision.

Transitional carotid and carotid collar

The term “Transitional carotid,” though not officially part of the three classifications in this work, is often used to describe the carotid segment between the proximal and distal dural rings [ Table 3 , Figures 1 and 6 ], especially in relation to aneurysms (e.g., transitional aneurysms).[ 1 , 12 , 16 , 44 ] It corresponds to parts of the paraclinoid and parasellar segments in Classifications 1 and 3 and the clinoid segment in Classification 2, aiding in locating aneurysms in this region, also called the “Carotid collar.”[ 59 , 62 ] Another transitional segment is described by other authors,[ 41 , 42 , 68 ] though these details exceed the scope of this work.

Cavernous segment in the trinity of ICA

To establish a clear relationship between the CS extension and specific segments of the ICA across classifications, we utilized cadaveric dissection [ Figures 3 , 4 and 7 ]. This analysis demonstrated that the cavernous segment is fully encompassed by the CS, with equivalency observed between Cherian’s cavernous segment,[ 7 ] Labib’s parasellar segment,[ 33 ] and Bouthillier’s cavernous segment.[ 4 ] In our study, the CS extended caudally to the distal paraclival segment and cephalically to the proximal paraclinoid segment in Classifications 1 and 3. Schematic details of this relationship are provided in Figures 1 and 6 . The CS itself spans from the superior orbital fissure anteriorly to the petrous portion of the temporal bone posteriorly.[ 37 , 43 ]

Figure 7:

The endonasal endoscopic view of the ventral skull base at the level of the sellar floor reveals both internal carotid arteries (ICAs) extending from the paraclival to the paraclinoid segments. A blue-shaded rectangle highlights the cavernous sinus extension, which spans the distal paraclival segment proximal paraclinoid segment and fully covers the parasellar segment (right ICA) as described in Labib’s classification. This corresponds to the cavernous segment (C4 horizontal segment) of Cherian’s classification for the left ICA. Below the sella, the clivus is visible, while superior to the sella, the tuberculum and planum can be observed, providing critical anatomical landmarks for endoscopic approaches.

Given the complexity of this segment, we chose to focus on its study while avoiding excessive detail on other segments to maintain our objective of simplifying the information. Notably, there are even comprehensive works dedicated to single ICA segments.[ 2 , 44 - 47 , 68 , 69 ] Variations in distances and angulations within the cavernous segment can be observed even in the same individual.[ 67 ]

McConell’s capsular arteries (only) Anterior and inferior capsular arteries (only 28% constant)[ 23 ]

Intracavernous branches may exhibit variability or be inconstant,[ 23 , 66 ] yet they play a critical role in supplying blood to the cranial nerves of the lateral wall of the CS,[ 5 , 48 ] the pituitary gland, its anterior capsule, the sella dura mater, and the CS walls.[ 27 , 47 , 49 , 51 , 64 ] These branches may also be involved in the vascularization of tumors in the sellar region.[ 52 ] In addition, this segment has anatomical relationships with the sphenoid sinus,[ 32 , 48 , 53 , 54 ] which further emphasizes its surgical importance.

DISCUSSION

Multiple classifications of the ICA have been proposed over the past century, each offering a unique perspective with specific objectives [ Table 1 ]. These range from embryological segmentation,[ 35 , 55 ] various angiographic aspects,[ 3 , 22 , 56 , 57 , 70 ] and endovascular considerations,[ 58 ] to anatomical and surgical relationships relevant to transcranial and endonasal endoscopic approaches.[ 7 , 33 , 34 ] However, as Poblet e et al. highlight, excessive neuroanatomical detail, unclear clinical application, inconsistent or overly complex schematic drawings, and poor-quality dissections can hinder rather than enhance understanding.[ 49 ] This surplus of variable data and inconsistent nomenclature risks creating confusion, which, in the worst cases, could result in significant surgical errors.

To address this, we have established a simplified relationship between ICA classifications, presenting three key frameworks and consolidating their elements into tables and original illustrations. Using color-coded diagrams, we streamlined the diverse nomenclature into a single document, creating what we term the “Trinity of the Internal Carotid Artery” [ Figure 8 ]. This integrates an anatomical foundation with three primary classifications,[ 4 , 7 , 33 ] presenting the ICA’s complexity in an accessible manner. We strongly encourage readers to explore the original works of these classifications, as well as comparative studies and discussions on nomenclature.[ 2 , 8 , 38 , 39 , 47 , 60 , 62 ]

Figure 8:

The triangulation of classifications for the internal carotid artery (ICA) integrates historical and modern perspectives to offer a comprehensive anatomical-surgical framework. Rhoton and Gibo’s classification serves as the anatomical base, while Bouthillier’s system provides a consistent, angiographic, and microsurgical approach for open procedures. Labib’s classification focuses on the ventral aspect of the ICA, tailored for endonasal endoscopic approaches, and Cherian’s classification addresses the lateral aspect, ideal for anterolateral skull base surgeries. Together, these complementary systems ensure a complete understanding of the ICA, enhancing precision and adaptability in diverse neurosurgical techniques.

We firmly believe that in modern medicine, a dogmatic approach is no longer appropriate. The rapid evolution of technology and surgical techniques demands adaptability and continuous learning. These advancements include minimally invasive anterior skull base endonasal surgery with novel techniques,[ 9 , 18 , 19 , 56 , 59 , 65 ] progress in endovascular neurosurgery,[ 6 , 12 , 22 , 28 ] 3D enhanced exoscope use,[ 16 , 53 , 63 ] robotic-assisted surgery,[ 61 ] and innovations in augmented reality, virtual reality, 3D modeling,[ 15 ] and digital reconstruction for neurosurgical applications. Given this pace of innovation, relying on a single universal ICA classification is inadequate.

This document is not intended as a definitive or dogmatic guide but as a practical, demonstrative, and educational tool for neurosurgeons. While perfect uniformity among classifications is unattainable due to their varied objectives and the ICA’s anatomical variations ranging from bifurcation levels[ 35 , 36 ] to segmental agenesis and course differences observed in angiographic and cadaveric studies,[ 3 , 66 ] this work serves as a valuable guide with academic and surgical utility. These variations emphasize the need for individualized approaches, considering not only interpatient differences but also variability between the ICAs of a single patient. Thus, each surgical case and approach must remain personalized.

We have demonstrated how three major ICA classifications[ 4 , 7 , 33 ] can complement, relate to, and overlap with one another. For example, the classifications by Labib et al.[ 33 ] and Cherian et al.[ 7 ] effectively integrate the relationships of the ICA with the upper, middle, and lower cranial nerves from the medial ventral to lateral perspectives and vice versa. They also align with critical surgical landmarks essential in both endoscopic endonasal and anterolateral skull base approaches, as shown in [ Tables 2 and 3 ; Figures 5 , 6 and 7 ]. This document aims to serve as a robust clinical and neurosurgical tool in an era where understanding multiple approaches, perspectives, and methodologies is essential. Relying solely on a single classification for the ICA is insufficient, given the complexity of modern neurosurgery.

We acknowledge that this information will require updates and reorganizations as advancements in medicine and neurosurgery emerge, yet its foundation will remain relevant since anatomical structures are constant. This work should be viewed as a tool for achieving a comprehensive surgical understanding of the ICA while encouraging openness to well-founded innovations and meaningful changes in the field.

We also emphasize the indispensable value of cadaveric dissections[ 19 , 33 , 45 , 50 , 56 ] in anatomical studies, which remain essential despite technological advances that may be inaccessible to many.

This study highlights the importance of cadaveric dissection in understanding ICA classifications and envisions future opportunities to combine endonasal endoscopic and extradural anterolateral skull base approaches on a single cadaver. This will enable a more cohesive anatomical correlation between the ventral and lateral ICA aspects.

CONCLUSION

Detailed knowledge of the ICA anatomy is critically important from a neurosurgical perspective, as well as for related fields such as otorhinolaryngology and maxillofacial surgery. Given the complexity of the ICA and its proximity to key anatomical structures, efforts should be made to simplify its study. Understanding its main classifications, their interrelationships, and the diverse nomenclature is essential to avoid anatomical and nominal confusion. This clarity can be achieved through comparative tables and illustrations that enhance the anatomical surgical comprehension of the ICA.

We conclude that studying the triangulation of classifications, referred to here as “The Trinity of the Internal Carotid Artery” (encompassing the three main classifications discussed in this work), provides readers with the foundational surgical knowledge of the ICA required by modern neurosurgery and skull base surgery. We strongly encourage readers to study the original works of the authors of these classifications to deepen their understanding and achieve a comprehensive grasp of this complex vessel. Finally, we extend our heartfelt gratitude to the authors of the various ICA classifications throughout history and to the colleagues who contributed to this paper.

Ethical approval:

The research/study is approved by the Institutional Ethics Committee at the Faculty of Medicine, UNAM, under protocol ID: UNAM-FM/DI/083-2023 ,Approval Date: 11-12-2023.

Declaration of patient consent:

Patient’s consent was not required as there are no patients in this study.

Financial support and sponsorship:

Nil.

Conflicts of interest:

There are no conflicts of interest.

Use of artificial intelligence (AI)-assisted technology for manuscript preparation:

The author confirms that there was no use of artificial intelligence (AI)-assisted technology for assisting in the writing or editing of the manuscript and no images were manipulated using AI.

Disclaimer

The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Journal or its management. The information contained in this article should not be considered to be medical advice; patients should consult their own physicians for advice as to their specific medical needs.

References

1. Al-Rodhan NR, Piepgras DG, Sundt TM. Transitional cavernous aneurysms of the internal carotid artery. Neurosurgery. 1993. 33: 993-8

2. Alikhani P, Sivakanthan S, Van Loveren H, Agazzi S. Paraclival or cavernous internal carotid artery: One segment but two names. J Neurol Surg B Skull Base. 2016. 77: 304-7

3. Bonasia S, Smajda S, Ciccio G, Bojanowski MW, Robert T. Proposed new classification for internal carotid artery segmental agenesis based on embryologic and angiographic correlation. Surg Radiol Anat. 2023. 45: 375-87

4. Bouthillier A, Van Loveren HR, Keller JT. Segments of the internal carotid artery: A new classification. Neurosurgery. 1996. 38: 425-33

5. Charlick M, Das JM, editors. Anatomy, Head and Neck: Internal Carotid Arteries. [Updated 2023 Jul 24]. StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; Jan- 2025. p. Available from: https://www.ncbi.nlm.nih.gov/books/NBK556061/

6. Campos JK, Lin LM, Beaty NB, Bender MT, Jiang B, Zarrin DA. Tandem cervical carotid stenting for stenosis with flow diversion embolisation for the treatment of intracranial aneurysms. Stroke Vasc Neurol. 2018. 4: 43-7

7. Cherian I, Burhan H. A simple and practical approach to understanding the extradural carotid segments related to both open and endoscopic skull base. J Neurosurg Neurol Kazajstan. 2020. 58: 7-16

8. Chmielewski R, Ciszek B. Internal carotid artery classification systems. Polish J Aviat Med Bioeng Psychol. 2020. 24: 27-35

9. Chin OY, Ghosh R, Fang CH, Baredes S, Liu JK, Eloy JA. Internal carotid artery injury in endoscopic endonasal surgery: A systematic review. Laryngoscope. 2016. 126: 582-90

10. Capo H, Kupersmith MJ, Berenstein A, Choi IS, Diamond GA. The clinical importance of the inferolateral trunk of the internal carotid artery. Neurosurgery. 1991. 28: 733-7 discussion 737-8

11. De Boer M, Shiraev TP, Loa J. Successful management of a large internal carotid artery aneurysm via open resection. Am J Case Rep. 2021. 22: e935009

12. Ducruet AF, Kellner CP, Connolly ES, Meyers PM. Endovascular occlusion of a ruptured transitional aneurysm associated with a developmental venous anomaly. Case report. Neurosurg Focus. 2009. 26: 1-4

13. De Jesus Encarnacion Ramirez M, Peralta I, Ramirez I, Dauly V, Mainer G, Nurmukhametov R. Development of a novel low-cost exoscope to expand access to microneurosurgical care in low-and middle-income countries. World Neurosurg. 2022. 163: 5-10

14. Encarnacion Ramirez M, Peralta Baez I, Nurmukhametov R, Goncharov E, Efe IE, Sufianov A. Comparative survey study of the use of a low cost exoscope vs. microscope for anterior cervical discectomy and fusion (ACDF). Front Med Technol. 2023. 4: 1055189

15. Encarnacion Ramirez M, Ramirez Pena I, Barrientos Castillo RE, Sufianov A, Goncharov E, Soriano Sanchez A. Development of a 3D printed brain model with vasculature for neurosurgical procedure visualisation and training. Biomedicines. 2023. 11: 330

16. Fernandes ST, Doria-Netto HL, Alves RV, Lapate RL, Ferreira NP, Teixeira MJ. The diagnostic accuracy of MRI in determining the relations between paraclinoid aneurysms and the cavernous sinus. Neuroradiology. 2022. 64: 1175-85

17. Fischer E. Die Lageabweichungen der vorderen hirnarterie im gefassbild. Zentralblatt Neurochir. 1938. 3: 300-12

18. Fernandez-Miranda JC, Gardner PA, Rastelli MM, PerisCelda M, Koutourousiou M, Peace D. Endoscopic endonasal transcavernous posterior clinoidectomy with interdural pituitary transposition. J Neurosurg. 2014. 121: 91-9

19. Fortes FS, Pinheiro-Neto CD, Carrau RL, Brito RV, Prevedello DM, Sennes LU. Endonasal endoscopic exposure of the internal carotid artery: An anatomical study. Laryngoscope. 2012. 122: 445-51

20. Garneau JC, Laitman BM, Cosetti MK, Hadjipanayis C, Wanna G. The Use of the exoscope in lateral skull base surgery: Advantages and limitations. Otol Neurotol. 2019. 40: 236-40

21. Gibo H, Lenkey C, Rhoton AL. Microsurgical anatomy of the supraclinoid portion of the internal carotid artery. J Neurosurg. 1981. 55: 560-74

22. Gao F, Sun X, Guo X, Li D, Xu GD, Miao ZR. Endovascular recanalization of symptomatic nonacute intracranial internal carotid artery occlusion: Proposal of a new angiographic classification. AJNR Am J Neuroradiol. 2021. 42: 299-305

23. Harris FS, Rhoton AL. Anatomy of the cavernous sinus. A microsurgical study. J Neurosurg. 1976. 45: 169-80

24. Iwanaga J, Anand MK, Camacho A, Rodriguez F, Watson C, Caskey EL. Surgical anatomy of the internal carotid plexus branches to the abducens nerve in the cavernous sinus. Clin Neurol Neurosurg. 2020. 191: 105690

25. Ismail M, Darwish M, Gomma M, Herzallah IR, El Tahan AE. Endoscopic orientation of juxta-pituitary carotid in transsphenoidal approaches: Critical considerations for clinical applications. Indian J Otolaryngol Head Neck Surg. 2021. 73: 461-6

26. Internal carotid artery - Radiology Reference Article. Available from: https://radiopaedia.org/articles/internal-carotid-artery-1?lang=gb [Last accessed on 2024 Apr 14].

27. Joo W, Funaki T, Yoshioka F, Rhoton AL. Microsurgical anatomy of the carotid cave. Neurosurgery. 2012. 70: 300-11 discussion 311-2

28. Jafar PP, Huang PK, Nelson M, Shapiro T, Becske HA, Riina E. Toward an endovascular internal carotid artery classification system. Am J Neuroradiol. 2014. 35: 230-6

29. Kurbanov A, Zimmer LA, Theodosopoulos PV, Leach JL, Keller JT. An Endoscopic roadmap of the internal carotid artery. Neurosurgery. 2015. 77: E153-4

30. Kassam AB, Vescan AD, Carrau RL, Prevedello DM, Gardner P, Mintz AH. Expanded endonasal approach: Vidian canal as a landmark to the petrous internal carotid artery. J Neurosurg. 2008. 108: 177-83

31. Kassam A, Labib MA, Prevedello DM, Carrau R. In Reply: An endoscopic roadmap of the internal carotid artery. Neurosurgery. 2015. 77: E154-5

32. Kang YJ, Cho JH, Kim DH, Kim SW. Relationships of sphenoid sinus pneumatization with internal carotid artery characteristics. PLoS One. 2022. 17: e0273545

33. Labib MA, Prevedello DM, Carrau R, Kerr EE, Naudy C, AlShaar HA. A road map to the internal carotid artery in expanded endoscopic endonasal approaches to the ventral cranial base. Neurosurgery. 2014. 10: 448-70

34. Labib MA, Abramov I, Houlihan LM, Srinivasan VM, Scherschinski L, Prevedello DM. Combined subtarsal contralateral transmaxillary retroeustachian and endoscopic endonasal approaches to the infrapetrous region. J Neurosurg. 2023. 139: 1-10

35. Lasjaunias P, Santoyo-Vazquez A. Segmental agenesis of the internal carotid artery: Angiographic aspects with embryological discussion. Anat Clin. 1984. 6: 133-41

36. Lasjaunias P. Surgical neuroangiography. Functional anatomy of craniofacial arteries. 1: Available from: https://www.osti.gov/biblio/5235774 [Last accessed on 2024 Apr 13]

37. Massa RN, Minutello K, Mesfin FB, editors. Neuroanatomy, cavernous sinus. Anatomy of the eyelid, orbit, and lacrimal system. A dissection manual. Germany: Springer; 2023. p. 27-37

38. Melé MV, Puigdellívol-Sánchez A, Mavar-Haramija M, JuanesMéndez JA, Román LS, De Notaris M. Review of the main surgical and angiographic-oriented classifications of the course of the internal carotid artery through a novel interactive 3D model. Neurosurg Rev. 2020. 43: 473-82

39. Newman H, Milne N, Lewis SB. Neurosurgical anatomy of the internal carotid artery: Magnetic resonance imaging study of the sellar region. World Neurosurg. 2020. 133: e711-5

40. Najera E, Ibrahim B, Muhsen BA, Ali A, Sanchez C, Obrzut M. Blood supply of cranial nerves passing through the cavernous sinus: An anatomical study and its implications for microsurgical and endoscopic cavernous sinus surgery. Front Oncol. 2021. 11: 702574

41. Nomina anatomica, editors. 6th ed: Authorised by the Twelfth International - Google Books. p. Available from: https://books.google.co.uk/books/about/nomina_anatomica_sixth_edition.html?id=bfmjsweacaaj&redir_esc=y [Last accessed on 2024 Apr 14]

42. Nikolenko VN, Fomkina OA. Deformation-strength parameters of arteries of the brain in the ii period of mature age. Sechenov Med J. 2019. 10: 41-6

43. Osawa S, Rhoton AL, Tanriover N, Shimizu S, Fujii K. Microsurgical anatomy and surgical exposure of the petrous segment of the internal carotid artery. Neurosurgery. 2008. 63: 210-38 discussion 239

44. Ohmoto T, Yabuno N, Date I. Surgical treatment of transitional internal carotid aneurysms. J Clin Neurosci. 1997. 4: 373-7

45. Ovalle Torres CS, Mora AE, Campero A, Cherian I, Sufianov A, Sanchez EF. Enhancing microsurgical skills in neurosurgery residents of low-income countries: A comprehensive guide. Surg Neurol Int. 2023. 14: 437

46. Paullus WS, Pait TG, Rhoton AL. Microsurgical exposure of the petrous portion of the carotid artery. J Neurosurg. 1977. 47: 713-26

47. Prasad KC, Gupta A, Induvarsha G, Anjali PK, Vyshnavi V. Microsurgical anatomy of the internal carotid artery at the skull base. J Laryngol Otol. 2022. 136: 64-7

48. Peris-Celda M, Kucukyuruk B, Monroy-Sosa A, Funaki T, Valentine R, Rhoton AL. The recesses of the sellar wall of the sphenoid sinus and their intracranial relationships. Neurosurgery. 2013. 73: ons117-31 discussion ons131

49. Poblete T, Casanova D, Soto M, Campero A, Mura J. Microsurgical anatomy of the anterior circulation of the brain adjusted to the neurosurgeon’s daily practice. Brain Sci. 2021. 11: 519

50. Pérez-Cruz JC, Macías-Duvignau MA, Reyes-Soto G, GascaGonzález OO, Baldoncini M, Miranda-Solís F. Latex vascular injection as method for enhanced neurosurgical training and skills. Front Surg. 2024. 11: 1366190

51. Quisling RG, Rhoton AL. Intrapetrous carotid artery branches: Radioanatomic analysis. Radiology. 1979. 131: 133-6

52. Rhoton AL, Saeki N, Perlmutter D, Zeal A. Microsurgical anatomy of common aneurysm sites. Clin Neurosurg. 1979. 26: 248-306

53. Rubini A, Di Gioia S, Marchioni D. 3D exoscopic surgery of lateral skull base. Eur Arch Otorhinolaryngol. 2020. 277: 687-94

54. Reyes-Soto G, Pérez-Cruz JC, Delgado-Reyes L, Castillo-Rangel C, Cacho Diaz B, Chmutin G. The Vertebrobasilar trunk and its anatomical variants: A Microsurgical anatomical study. Diagnostics (Basel). 2024. 14: 534

55. Ramirez MJ, Chaddad-Neto F, Montemurro N, Ramirez Pena IJ, Rosario Rosario A, Catillo-Rangel C. Decibel decisions: The concept of intracranial aneurysm surgery with a decibel meter on two surgical cases. Cureus. 2023. 15: e48993

56. Rindler RS, Leonel LC, Graepel S, Agosti E, Kerezoudis P, Pinheiro-Neto CD. The endonasal midline inferior intercavernous approach to the cavernous sinus: Technical note, cadaveric step-by-step illustration, and case presentation. Acta Neurochir (Wien). 2022. 164: 2573-80

57. Ramirez MJ, Nurmukhametov R, Musa G, Barrientos Castillo RE, Encarnacion VL, Soriano Sanchez JA. Three-dimensional plastic modeling on bone frames for cost-effective neuroanatomy teaching. Cureus. 2022. 14: e27472

58. Ramirez MD, Musa G, Castillo RE, Cherian I, Sufianov A, Lafuente J. Three-dimensional cerebrovascular bypass training. A new low-cost home-made model. Front Med Case Rep. 2021. 2: 1-10

59. Rhoton AL. The cavernous sinus, the cavernous venous plexus, and the carotid collar. Neurosurgery. 2002. 51: S375-410

60. Salaud C, Decante C, Ploteau S, Hamel A. Implication of the inferolateral trunk of the cavernous internal CAROTID artery in cranial nerve blood supply: Anatomical study and review of the literature. Ann Anat. 2019. 226: 23-8

61. Stumpo V, Staartjes VE, Klukowska AM, Golahmadi AK, Gadjradj PS, Schröder ML. Global adoption of robotic technology into neurosurgical practice and research. Neurosurg Rev. 2021. 44: 2675-87

62. Seoane E, Rhoton AL, De Oliveira E. Microsurgical anatomy of the dural collar (carotid collar) and rings around the clinoid segment of the internal carotid artery. Neurosurgery. 1998. 42: 869-86

63. Sufianov RA, Garifullina NA, Magomedova AS, Hevor MG, Ramirez MJ, Sufianov AA. Endoscopically assisted exoscopic surgery for microvascular decompression of the trigeminal nerve with intraoperative use of indocyanine green. Surgeries. 2024. 5: 172-83

64. Surgical neuroanatomy by Álvaro Campero. Available from: https://www.edicionesjournal.com/papel/9789874922243/neuroanatom%c3%ada+quir%c3%bargica [Last accessed on 2024 Apr 14].

65. Vajkoczy P, Draf W, Carrau RL, Bockmül U, Kassam AB, editors. Endonasal endoscopic surgery of skull base tumors: An interdisciplinary approach Chapter 7. 2015. p. 160-171 United States: Thieme

66. Willinsky R, Lasjaunias P, Berenstein A. Intracavernous branches of the internal carotid artery (ICA). Comprehensive review of their variations. Surg Radiol Anat. 1987. 9: 201-15

67. Wang C, Xie J, Cui D, Cheng Y, Zhang S. A new classification of cavernous segment of the internal carotid artery. J Craniofac Surg. 2013. 24: 1418-22

68. Zimmer LA, Marcati E, Andaluz N, Froelich SC, Leach JL, Fernandez Miranda JC. Paratrigeminal, paraclival, precavernous, or all of the above? A circumferential anatomical study of the C3-C4 transitional segment of the internal carotid artery. Oper Neurosurg (Hagerstown). 2018. 14: 432-40

69. Zhou W, Fang X, Di G, Jiang X. The anatomy of the parapharyngeal segment of the internal carotid artery for endoscopic endonasal approach. Neurosurg Rev. 2020. 43: 1391-401

70. Ziyal IM, Ozgen T, Sekhar LN, Ozcan OE, Cekirge S. Proposed classification of segments of the internal carotid artery: anatomical study with angiographical interpretation. Neurol Med Chir (Tokyo). 2005. 45: 184-90 discussion 190-1