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Branches of the intracavernous internal carotid artery and the blood supply of the intracavernous cranial nerves
ANNALS Of ANATOMY
Branches of the intracavernous internal carotid artery and the blood supply of the intracavernous cranial nerves Ibrahim Tekdemir*, Eray Tiiccar*, Hakan E. Cubuk", Mehmet Ersoy**, Alaittin Elhan* and Haluk Deda***
* Ankara University, Faculty of Medicine, Department of Anatomy, Morfoloji Binasi, 06100 Sihhiye, Ankara, Turkey, ** Ankara UniversityFaculty of Health Education, and *** Ankara University Medicine Faculty, Department of Neurosurgery
Summary. With the increasing frequency of surgical operations to the cavernous sinus greater knowledge of the microanatomy of the cavernous sinus has become necessary. The most frequently seen complications during cavernous sinus surgery involve impairment of cranial nerves. This can occur due to direct damage or ischemia. For these reasons, it is important to know the arterial supplies to the cranial nerves in the cavernous sinus and the anatomy of these branches as well. 15 formaline fixed adult cadavers were used in this study. Before the dissections, the internal carotid artery and vertebral artery were filled with coloured latex on both sides. In this report, the intracavernous branches of internal carotid artery (LLCA.) were identified based on the principles of Nomina Anatomica (1989) and compared with others. In our study we found that the segment of the abducens nerve which lies in Dorello's channel was supplied by the meningeal branch; from the point at which it pierces the cerebellar tentorium, the trochlear nerve is supplied by the tentorial cerebellar artery; the posterior cerebellar artery supplies the proximal segment of the oculomotor nerve that proceeds to the oculomotor triangle. Except for these, all the cranial nerves that were located on the lateral wall of the sinus cavernosus are supplied by the tentorial marginal branch and the branches of the lateral trunk.
Introduction Because of increased interest in the surgical approaches to the cavernous sinus region in recent years, knowledge of the anatomy of the sinus and the related neurovascular structures in the area have become very important (Harris and Rhoton 1970; Parkinson 1974; Lasjaunas 1977). Most of the complications are the cranial nerve injuries that occur either during direct surgical procedures or ischemies that result secondarily to the arterial injuries (Krisht et al. 1994). Therefore, it is important to be familiar with the cavernous branches that supply the cranial nerves in this area. The literature contains many studies concerning the neural and vascular structures of the cavernous sinus. The branches of the LLCA. were examined in detail in previous studies, where several different terms for the cavernous branches of the internal carotid artery (LCA.) were proposed and no uniform classification for identifying those arteries was established (Inoue and Rhoton 1990; Parkinson 1974; Schnurer 1963). Consequently, there are many variations in the terminology used by neurosurgeons and anatomists. This study therefore analyses the distribution and the neural relationships of the cavernous branches of the ICA, and proposes a classification of these branches in keeping with the Nomina Anatomica 1989 and its forthcoming revised edition.
Key words: Internal carotid artery - Cavernous sinus Anatomy
Materials and methods Correspondence to: Ibrahim Tekdemir This work has been supported by the Scientific and Technical Research Council of Turkey (SBAG: 1459)
Ann Anat (1998) 180: 343-348 © Gustav Fischer Verlag
Both sides of 15 formaline fixed adult cadavers were used in the study. Both the LCA. and the vertebral arteries were dissected, canulated and prepared for latex injection. At room tempera-
Fig. 1. Three branches separate from posterior trunk (complete type): the inferior hypophysial artery (i. h. a.), the tentorial basal branch (t. b. b.) and the meningeal branch (m. b.), abducens nerve (a. n.). Fig. 2. Tho branches separate from posterior trunk (incomplete type): the inferior hypophysial artery (i. h. a.) and the meningeal branch (m. b.) Fig. 3. The branches of the lateral trunk which supply the oculomotor nerve, trochlear nerve and ophthalmic nerve on the lateral wall of cavernous sinus. Fig. 4. A large branch from the lateral trunk and its distrubution on the cranial nerves. Fig. 5. Branches from the lateral trunk and their distribution to the cranial nerves. Fig. 6. McConnell's artery separates from inferior hypophysial artery. Fig. 7. Branch from the lateral trunk that supplies abducens nerve. Fig. 8. Three arterial branches arise from a single branch of the lateral trunk.
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ture, latex was mixed with Indian ink, to obtain a suitable mixture. The mixture was liquid prior to but solidified well after injection. We continued injecting latex into the ICA until it flowed out of the vertebral arteries. The vessels exuding latex were clamped, and the perfusion was finished one at a time. This process ensured that all the arteries were filled with latex. After injecting, we waited 24 hours for the latex to solidify before beginning dissection. After removing the calvaria and the brain hemispheres, we made an incision on the anterior-inferior side of the oculomotor triangle in order to visualize the intracavernous branches of the ICA in the cavernous sinus. Afterwards, we drilled and removed the anterior and posterior clinoid processes. The course and the branches of the ICA were dissected and examined at a magnification of 16x using a Zeiss Opmi 1 operating microscope. A Leica M3 camera was used to take the photographs.
rate arteries arose from the ICA and supplied the cranial nerves in the cavernous sinus (Fig. 5). We found no artery arising from the medial side of the ICA, so there was no artery which could be called the medial trunk. In 6 cases (20%), McConnel's artery branched off from the inferior hypohysial artery (Fig. 6). In all cadavers, the ophthalmic artery arose from the ICA outside the cavernous sinus and medial to the anterior clinoid process. We made microdissections of the cranial nerves lying on the lateral wall or in the cavernous sinus in order to clarify the complex arterial supplies. Our results are shown by individually examining the cranial nerves.
Abducens nerve
Results The cavernous portion of the ICA makes two curves within the cavernous sinus, and consists of 5 sections. This classification makes it easier to understand and define origins of the branches of the intracavernous part of the ICA. These branches are evaluated in three different groups; these are the posterior trunk, lateral trunk, and medial trunk.
The section lying in Dorello's channel is supplied by the meningeal branch, whereas the segment lying between the petrous apex and the superior orbital fissure is supplied by the branches of the lateral trunk (Fig. 7).
Ophthalmic Nerve The proximal segment of the ophthalmic nerve lying between trigeminal ganglion and the superior orbital fissure is supplied with the lateral trunk that arises from the ICA as a single trunk or as separate branches (Fig. 8).
The Posterior Truak In 25 of the cases, the posterior trunk arose directly from different points lying between the lateral and medial edges of the second section of the ICA. In 18 cadavers (60%), this trunk gave rise to three branches: the tentorial basal branch (Bernasconi-Cassinari), the meningeal branch, and the inferior hypophysial artery (Fig. 1). In 7 of the cases (23.3%), the posterior trunk gave rise to 2 branches: the meningeal branch and the inferior hypophysial artery (Fig. 2). In the remaining 5 cases (16.6%), the inferior hypophysial artery, the tentorial basal branch and the meningeal branch originated separately from the ICA.
The Lateral Trunk The lateral trunk typically arises from the lateral part of the horizontal segment of the ICA, and it lies over the abducens nerve. In 14 cases (46.6%) the lateral trunk gave rise to all three branches. One of these branches is the marginal tentorial branch, and the others are the branches to nerves. These branches supply the oculomotor, trochlear, abducens and ophthalmic nerves (Fig. 3). In 9 cases (30%) the lateral trunk arose as a large branch from the ICA and spreads out on the lateral wall of the cavernous sinus (Fig. 4). In the remaining 7 cases (23.3%), there was no lateral trunk; instead, 3 or 4 sepa-
Trochlear Nerve This nerve has a close relation with the tentorial basal artery from the point at which it pierces the cerebellar tentorium. Therefore, its proximal segment is supplied by the tentorial basal branch, whereas its distal segment, which lies on the lateral sinus wall, is supplied by the lateral trunk.
Oculomotor Nerve The posterior cerebellar artery supplies the proximal segment of this nerve that proceeds to the oculomotor triangle, where the distal segment, which lies on the lateral wall of the cavernous sinus, is supplied by the large branches originating from the lateral trunk.
Discussion In the classical textbooks, the anatomy of the I.I.c.A. is either not mentioned or analyzed briefly. In addition, there is no agreement on the terminology used for branches of the I.I.c.A. (Snell 1992; Williams 1995). The terminology used by clinicians today is in contradiction to
345
the Nomina Anatomica, making evident the rational and universal insufficiency of today's terminology (Inoue and Rhoton 1990; Jimenez 1993; Lang 1995; Nuza 1990; TranDihn 1987). As the surgical approaches to the cavernous sinus have increased, a clearer understanding of the region has become important and necessary. The branches of the ICA arising within the cavernous sinus have been studied by many neurosurgeons. The meningohypophysial trunk was found in all cases that Parkinson (1974) examined. He described the three branches of this trunk as the dorsal elival artery, tentorial artery, and the inferior hypophysial artery. He also described the artery that emerged from the horizontal portion of the ICA as the inferior cavernous sinus artery and found it in 80% of his dissections. He defined a capsular artery that emerged from the medial side of the ICA but did not state a percentage. Inoue et al. (1990) identified the meningohypophysial trunk in all of their dissections and found two types of the artety. They found that 70% of the arteries were of the complete type that gave rise to all the dorsal clival, the tentorial and the inferior hypophysial arteries. Of all cases, 30% were of the incomplete type, in which one or two of the three branches arose directly from the carotid artery. The dorsal meningeal artery was the most frequent branch to arise directly from the ICA. The artery of the inferior cavernous sinus arose from the horizontal segment and passed above the abducens nerve in 96% of sinuses and below it in 4%. In 4% of the cases, there was a duplication of the artery of the inferior cavernous sinus. All the arteries we examined passed above the abducens nerve after branching from the horizontal segment of the ICA. Jimenez et al. (1993) stated that the meningohypophysial trunk gave off all three branches in 63% of their case material. In 80% of these cases, the artery of the inferior cavernous sinus was the second branch of the ICA. The dorsal meningeal artery originated from the meningohypophysial trunk in all cases except one, where it originated as an independent artery from the ICA. In 76.6% of their cases, the superior (anterior) capsular artery had
an intracavernous origin, and in 6.6% of the cases, the superior capsular artery emerged extracavemously. The results of Nuza and Taner (1990), Parkinson and Shields (1974) and Inoue et al. (1990) are quite similar from studies in which they used the same terminology. 'Iran-Dinh (1987) has examined the confusion in terminology, and referred to the Nomina Anatomica (1989) as the main source for comparing the terminology, used to define the branches of the ICA in the cavernous sinus. This study points out that the points of emergence from the ICA and the area that these arteries irrigate must be considered in naming these branches. Tran-Dinh recommends naming the arteries the posterior trunk, the lateral trunk and the medial group instead of using names such as meningohypophysial trunk or the artery of the inferior cavernous sinus. Tran-Dinh named the arteries branching from these main groups the hypophysial artery, basal tentorial artery, marginal tentorial artery, clival branch, capsular branch, nervous branch, osseous branch, meningeal branch and anastomotic branch. Unfortunately, they did not combine their definitions with the corresponding arteries used by other clinicians in previous studies. Based on the findings from our dissections and the nomenclature used in the Nomina Anatomica (1989), we made a classification of the branches of the ICA in the cavernous sinus (Tables 1 and 2). We found that the inferior hypophysial artery, the tentorial basal branch (tentorial artery, Bernasconi-Cassinari) and the meningeal branch (dorsal meningeal artery, clival artery) arose from the posterior trunk (dorsal main stem, meningohypophysial trunk, posterior caroticocavemous trunk). The tentorial marginal branch and the branches to nerves (artery of the inferior cavernous sinus, lateral caroticocavernous trunk, lateral main stem, inferolateral trunk) arose from the lateral trunk, whereas the cavernous branch (McConnell's capsular artery) arose from the medial group of the 1.C.A. Posterior, lateral and medial groups have not been described in the Nomina Anatomica, but the authors suggest the primary branches of the I.I.c.A. be named according to their origins.
Table 1. Chronologie comparative termsfor intracavemous branches of the ICA Author(s) Year
Name Given to the ArterialBranches
McConnell, 1953 Schnurer and Stattin, 1963 Parkinson, Shields, 1974 Tran Dinh, 1987 Inoue, Rhoton et al., 1990 Nuza, Taner, 1990 Jimenez, Carmora et al., 1993 Krisht et al., 1994 Lang, 1995 Nomina Anatomica, 1989 In the presentstudy
Inferior hypophysial artery Dorsalmainstem Meningohypophysial trunk Posterior trunk Meningohypophysial trunk Meningohypophysial trunk Meningohypophysial trunk Meningohypophysial trunk Posterior caroticocavemous trunk
Lateralmainstem Artery of the inferior CS Lateral trunk Artery of the inferior CS Artery of the inferior CS Artery of the inferior CS Inferolateral trunk Lateralcaroticocavemous trunk
Posterior trunk
Lateraltrunk
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Capsular arteries Capsular arteries Medial group Capsular arteries Capsular arteries Capsular arteries Capsular arteries Medial group
Table 2. Comparative terms for the branches that arose from posterior trunk of the ICA Branches of main trunk
Author(s) Year
Main trunk
McConnell, 1953
Inferior hypophysial artery
Schnurer and Stattin, 1963
Dorsal main stem
Parkinson, Shields 1974
Meningohypophysial trunk:
Inferior hypophysial artery Dorsal meningeal artery Tentorial artery
Tran Dinh, 1987
Posterior trunk:
Inferior hypophysial artery Marginal tentorial artery Clival artery
Inoue, Rhoton et al., 1990
Meningohypophysial trunk:
Inferior hypophysial artery Dorsal meningeal artery Tentorial artery
Nuza, Taner, 1990
Meningohypophysial trunk
Inferior hypophysial artery Dorsal meningeal artery Tentorial artery
Jimenez, Carmona et al., 1993
Meningohypophysial trunk:
Inferior hypophysial artery Dorsal meningeal artery Tentorial artery
Krisht et al., 1994
Meningohypophysial trunk
Inferior hypophysial artery Tentorial basal branch Meningeal branch
Lang, 1995
Posterior caroticocavemous trunk
Inferior hypophysial artery Posterior clival artery Inferior hypophysial artery Tentorial basal branch Meningeal branch
Nomina Anatomica, 1989
In the present study
Inferior hypophysial artery Tentorial basal branch Meningeal branch
Posterior trunk
The McConnell's capsular artery arises from the medial side of the horizontal segment of the intracavernous lC.A., and it irrigates the pituitary gland. Inoue and Rhoton found this artery in only 8% of their case material. Tran-Dinh (1987) reported an incidence of 28.1%. Nuza (1990) found the capsular artery in 30% of the cases, and that the inferior capsular artery originated from the ICA in 5 cases and from the inferior hypophysial artery in 4 cases. Jimenez et al. (1993) reported that the McConnell's capsular artery had inferior and superior branches. The superior branch (anterior) was seen in 76.6% while the inferior capsular artery was found in 90%. In our study no artery originated from the medial group. In 6 of our dissections (20%), we saw the McConnell's capsular artery originating from the inferior hypophysial artery. Hayreh (1974) reported an incidence of 7% for the cavernous origin of the ophthalmic artery, where Harris and Rhoton (1970) reported 8%, and Tran-Dinh 15.6%. In contrast to these previous studies the present study did not find the ophthalmic artery arising from the intracavernous segment of the ICA. In their detailed study on the blood supply of the intracavernous cranial nerves, Krisht et al. (1994) stated that all the cranial nerves were supplied by the inferolateral
trunk with the exception of the proximal segment of the abducens nerve, as it is supplied by branches from the dorsal clival artery. In our study, we found that the abducens nerve lying between Dorello's channel and the petrosal apex is supplied by branches from the meningeal branch. The trochlear nerve lying between the point at which it enters the cerebellar tentorium and the superior orbital fissure is supplied by branches from the tentorial basal artery (Bernasconi-Cassinari). The proximal segment of the oculomotor nerve, that is, the segment before it reaches the oculomotor triangle, is supplied by branches from the posterior cerebellar artery. All the other segments of these nerves were supplied by the tentorial marginal branch and the branches that arise from the lateral trunk. In conclusion, we can state that (a) the Nomina Anatomica, revised every 5 years, must be a guide for anatomists and clinicians in order to provide a universally accepted terminology and avoid disagreement on the descriptions and nomenclature, and (b) given that cranial nerve deficits are the most common complications of cavernous sinus surgery, better understanding of the blood supply to these nerves as well as choosing the correct surgical approach may help to prevent such complications.
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References Hayreh SS (1974) The ophthalmic artery. In: Newton TH, Potts DG (eds) Radiology of the skull and brain. Angiography, Vol 2. St. Louis, CV Mosby, pp 1333-1350 Harris FS, Rhoton AL Jr (1970) Anatomy of the cavernous sinus: A microsurgical study. J Neurosurg 45: 169-180 Inoue T, Rhoton AL Jr, Theele D, Barry ME (1990) Surgical approaches to the cavernous sinus: A microsurgical study. Neurosurgery 26: 903-932 Jimenez Castellanos J, Carmona A, Catalina-Herrera CJ (1993) Anatomical study of the branches emerging along the intracavernous course of the internal carotid artery in humans. Acta Anat 148: 57-61 Krisht A, Barnett DW, Barrow DL, Bonner G (1994) The blood supply of the intracavernous cranial nerves: An anatomic study. Neurosurgery 34: 275-279 Lang J (1995) Skull base and related structures. Schattauer, Stuttgart New York, pp 179-191 Lasjauninas P, Moret J, Manelfe C, Theron J, Hasso T, Seeger J (1977) Arterial anomalies at the base of the skull. Neuroradiol 13: 267-272
McConnell EM (1953) The arterial blood supply of the human hypophysis cerebri. Anat Rec 115: 175-201 Nomina Anatomica (1989), Sixth Edition, Churchill Livingstone, London Nuza AB, Taner D (1990) Anatomical variations of the intracavernous branches of the internal carotid artery with reference to the relationship of the internal carotid artery and sixth cranial nerve. A microsurgical study. Acta Anat 138: 238-245 Parkinson D, Shields CB (1974) Persistent trigeminal artery: Its relationship to the normal branches of the cavernous carotid artery. J Neurosurgery 40: 244-248 Schnurer LB, Stattin S (1963) Vascular supply of intracranial dura from the internal carotid artery with special reference to its angiographic significance. Acta Radiol (Diagn) (Stockh) 1: 441-450
Snell RS (1992) Clinical Anatomy for medical students. Little, Brown and Company. 4th edition, pp 824-826 'Iran-Dinh H (1987) Cavernous branches of the internal carotid artery: Anatomy and nomenclature. Neurosurgery 20: 205-210 WilliamsPL, Warwick R (1995) Gray's Anatomy. London: Churchill Livingstone (38th edition), pp 1525-1526 Accepted March 25, 1998
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Branches of the intracavernous internal carotid artery and the blood supply of the intracavernous cranial nerves Ibrahim Tekdemir*, Eray Tiiccar*, Hakan E. Cubuk", Mehmet Ersoy**, Alaittin Elhan* and Haluk Deda***
* Ankara University, Faculty of Medicine, Department of Anatomy, Morfoloji Binasi, 06100 Sihhiye, Ankara, Turkey, ** Ankara UniversityFaculty of Health Education, and *** Ankara University Medicine Faculty, Department of Neurosurgery
Summary. With the increasing frequency of surgical operations to the cavernous sinus greater knowledge of the microanatomy of the cavernous sinus has become necessary. The most frequently seen complications during cavernous sinus surgery involve impairment of cranial nerves. This can occur due to direct damage or ischemia. For these reasons, it is important to know the arterial supplies to the cranial nerves in the cavernous sinus and the anatomy of these branches as well. 15 formaline fixed adult cadavers were used in this study. Before the dissections, the internal carotid artery and vertebral artery were filled with coloured latex on both sides. In this report, the intracavernous branches of internal carotid artery (LLCA.) were identified based on the principles of Nomina Anatomica (1989) and compared with others. In our study we found that the segment of the abducens nerve which lies in Dorello's channel was supplied by the meningeal branch; from the point at which it pierces the cerebellar tentorium, the trochlear nerve is supplied by the tentorial cerebellar artery; the posterior cerebellar artery supplies the proximal segment of the oculomotor nerve that proceeds to the oculomotor triangle. Except for these, all the cranial nerves that were located on the lateral wall of the sinus cavernosus are supplied by the tentorial marginal branch and the branches of the lateral trunk.
Introduction Because of increased interest in the surgical approaches to the cavernous sinus region in recent years, knowledge of the anatomy of the sinus and the related neurovascular structures in the area have become very important (Harris and Rhoton 1970; Parkinson 1974; Lasjaunas 1977). Most of the complications are the cranial nerve injuries that occur either during direct surgical procedures or ischemies that result secondarily to the arterial injuries (Krisht et al. 1994). Therefore, it is important to be familiar with the cavernous branches that supply the cranial nerves in this area. The literature contains many studies concerning the neural and vascular structures of the cavernous sinus. The branches of the LLCA. were examined in detail in previous studies, where several different terms for the cavernous branches of the internal carotid artery (LCA.) were proposed and no uniform classification for identifying those arteries was established (Inoue and Rhoton 1990; Parkinson 1974; Schnurer 1963). Consequently, there are many variations in the terminology used by neurosurgeons and anatomists. This study therefore analyses the distribution and the neural relationships of the cavernous branches of the ICA, and proposes a classification of these branches in keeping with the Nomina Anatomica 1989 and its forthcoming revised edition.
Key words: Internal carotid artery - Cavernous sinus Anatomy
Materials and methods Correspondence to: Ibrahim Tekdemir This work has been supported by the Scientific and Technical Research Council of Turkey (SBAG: 1459)
Ann Anat (1998) 180: 343-348 © Gustav Fischer Verlag
Both sides of 15 formaline fixed adult cadavers were used in the study. Both the LCA. and the vertebral arteries were dissected, canulated and prepared for latex injection. At room tempera-
Fig. 1. Three branches separate from posterior trunk (complete type): the inferior hypophysial artery (i. h. a.), the tentorial basal branch (t. b. b.) and the meningeal branch (m. b.), abducens nerve (a. n.). Fig. 2. Tho branches separate from posterior trunk (incomplete type): the inferior hypophysial artery (i. h. a.) and the meningeal branch (m. b.) Fig. 3. The branches of the lateral trunk which supply the oculomotor nerve, trochlear nerve and ophthalmic nerve on the lateral wall of cavernous sinus. Fig. 4. A large branch from the lateral trunk and its distrubution on the cranial nerves. Fig. 5. Branches from the lateral trunk and their distribution to the cranial nerves. Fig. 6. McConnell's artery separates from inferior hypophysial artery. Fig. 7. Branch from the lateral trunk that supplies abducens nerve. Fig. 8. Three arterial branches arise from a single branch of the lateral trunk.
344
ture, latex was mixed with Indian ink, to obtain a suitable mixture. The mixture was liquid prior to but solidified well after injection. We continued injecting latex into the ICA until it flowed out of the vertebral arteries. The vessels exuding latex were clamped, and the perfusion was finished one at a time. This process ensured that all the arteries were filled with latex. After injecting, we waited 24 hours for the latex to solidify before beginning dissection. After removing the calvaria and the brain hemispheres, we made an incision on the anterior-inferior side of the oculomotor triangle in order to visualize the intracavernous branches of the ICA in the cavernous sinus. Afterwards, we drilled and removed the anterior and posterior clinoid processes. The course and the branches of the ICA were dissected and examined at a magnification of 16x using a Zeiss Opmi 1 operating microscope. A Leica M3 camera was used to take the photographs.
rate arteries arose from the ICA and supplied the cranial nerves in the cavernous sinus (Fig. 5). We found no artery arising from the medial side of the ICA, so there was no artery which could be called the medial trunk. In 6 cases (20%), McConnel's artery branched off from the inferior hypohysial artery (Fig. 6). In all cadavers, the ophthalmic artery arose from the ICA outside the cavernous sinus and medial to the anterior clinoid process. We made microdissections of the cranial nerves lying on the lateral wall or in the cavernous sinus in order to clarify the complex arterial supplies. Our results are shown by individually examining the cranial nerves.
Abducens nerve
Results The cavernous portion of the ICA makes two curves within the cavernous sinus, and consists of 5 sections. This classification makes it easier to understand and define origins of the branches of the intracavernous part of the ICA. These branches are evaluated in three different groups; these are the posterior trunk, lateral trunk, and medial trunk.
The section lying in Dorello's channel is supplied by the meningeal branch, whereas the segment lying between the petrous apex and the superior orbital fissure is supplied by the branches of the lateral trunk (Fig. 7).
Ophthalmic Nerve The proximal segment of the ophthalmic nerve lying between trigeminal ganglion and the superior orbital fissure is supplied with the lateral trunk that arises from the ICA as a single trunk or as separate branches (Fig. 8).
The Posterior Truak In 25 of the cases, the posterior trunk arose directly from different points lying between the lateral and medial edges of the second section of the ICA. In 18 cadavers (60%), this trunk gave rise to three branches: the tentorial basal branch (Bernasconi-Cassinari), the meningeal branch, and the inferior hypophysial artery (Fig. 1). In 7 of the cases (23.3%), the posterior trunk gave rise to 2 branches: the meningeal branch and the inferior hypophysial artery (Fig. 2). In the remaining 5 cases (16.6%), the inferior hypophysial artery, the tentorial basal branch and the meningeal branch originated separately from the ICA.
The Lateral Trunk The lateral trunk typically arises from the lateral part of the horizontal segment of the ICA, and it lies over the abducens nerve. In 14 cases (46.6%) the lateral trunk gave rise to all three branches. One of these branches is the marginal tentorial branch, and the others are the branches to nerves. These branches supply the oculomotor, trochlear, abducens and ophthalmic nerves (Fig. 3). In 9 cases (30%) the lateral trunk arose as a large branch from the ICA and spreads out on the lateral wall of the cavernous sinus (Fig. 4). In the remaining 7 cases (23.3%), there was no lateral trunk; instead, 3 or 4 sepa-
Trochlear Nerve This nerve has a close relation with the tentorial basal artery from the point at which it pierces the cerebellar tentorium. Therefore, its proximal segment is supplied by the tentorial basal branch, whereas its distal segment, which lies on the lateral sinus wall, is supplied by the lateral trunk.
Oculomotor Nerve The posterior cerebellar artery supplies the proximal segment of this nerve that proceeds to the oculomotor triangle, where the distal segment, which lies on the lateral wall of the cavernous sinus, is supplied by the large branches originating from the lateral trunk.
Discussion In the classical textbooks, the anatomy of the I.I.c.A. is either not mentioned or analyzed briefly. In addition, there is no agreement on the terminology used for branches of the I.I.c.A. (Snell 1992; Williams 1995). The terminology used by clinicians today is in contradiction to
345
the Nomina Anatomica, making evident the rational and universal insufficiency of today's terminology (Inoue and Rhoton 1990; Jimenez 1993; Lang 1995; Nuza 1990; TranDihn 1987). As the surgical approaches to the cavernous sinus have increased, a clearer understanding of the region has become important and necessary. The branches of the ICA arising within the cavernous sinus have been studied by many neurosurgeons. The meningohypophysial trunk was found in all cases that Parkinson (1974) examined. He described the three branches of this trunk as the dorsal elival artery, tentorial artery, and the inferior hypophysial artery. He also described the artery that emerged from the horizontal portion of the ICA as the inferior cavernous sinus artery and found it in 80% of his dissections. He defined a capsular artery that emerged from the medial side of the ICA but did not state a percentage. Inoue et al. (1990) identified the meningohypophysial trunk in all of their dissections and found two types of the artety. They found that 70% of the arteries were of the complete type that gave rise to all the dorsal clival, the tentorial and the inferior hypophysial arteries. Of all cases, 30% were of the incomplete type, in which one or two of the three branches arose directly from the carotid artery. The dorsal meningeal artery was the most frequent branch to arise directly from the ICA. The artery of the inferior cavernous sinus arose from the horizontal segment and passed above the abducens nerve in 96% of sinuses and below it in 4%. In 4% of the cases, there was a duplication of the artery of the inferior cavernous sinus. All the arteries we examined passed above the abducens nerve after branching from the horizontal segment of the ICA. Jimenez et al. (1993) stated that the meningohypophysial trunk gave off all three branches in 63% of their case material. In 80% of these cases, the artery of the inferior cavernous sinus was the second branch of the ICA. The dorsal meningeal artery originated from the meningohypophysial trunk in all cases except one, where it originated as an independent artery from the ICA. In 76.6% of their cases, the superior (anterior) capsular artery had
an intracavernous origin, and in 6.6% of the cases, the superior capsular artery emerged extracavemously. The results of Nuza and Taner (1990), Parkinson and Shields (1974) and Inoue et al. (1990) are quite similar from studies in which they used the same terminology. 'Iran-Dinh (1987) has examined the confusion in terminology, and referred to the Nomina Anatomica (1989) as the main source for comparing the terminology, used to define the branches of the ICA in the cavernous sinus. This study points out that the points of emergence from the ICA and the area that these arteries irrigate must be considered in naming these branches. Tran-Dinh recommends naming the arteries the posterior trunk, the lateral trunk and the medial group instead of using names such as meningohypophysial trunk or the artery of the inferior cavernous sinus. Tran-Dinh named the arteries branching from these main groups the hypophysial artery, basal tentorial artery, marginal tentorial artery, clival branch, capsular branch, nervous branch, osseous branch, meningeal branch and anastomotic branch. Unfortunately, they did not combine their definitions with the corresponding arteries used by other clinicians in previous studies. Based on the findings from our dissections and the nomenclature used in the Nomina Anatomica (1989), we made a classification of the branches of the ICA in the cavernous sinus (Tables 1 and 2). We found that the inferior hypophysial artery, the tentorial basal branch (tentorial artery, Bernasconi-Cassinari) and the meningeal branch (dorsal meningeal artery, clival artery) arose from the posterior trunk (dorsal main stem, meningohypophysial trunk, posterior caroticocavemous trunk). The tentorial marginal branch and the branches to nerves (artery of the inferior cavernous sinus, lateral caroticocavernous trunk, lateral main stem, inferolateral trunk) arose from the lateral trunk, whereas the cavernous branch (McConnell's capsular artery) arose from the medial group of the 1.C.A. Posterior, lateral and medial groups have not been described in the Nomina Anatomica, but the authors suggest the primary branches of the I.I.c.A. be named according to their origins.
Table 1. Chronologie comparative termsfor intracavemous branches of the ICA Author(s) Year
Name Given to the ArterialBranches
McConnell, 1953 Schnurer and Stattin, 1963 Parkinson, Shields, 1974 Tran Dinh, 1987 Inoue, Rhoton et al., 1990 Nuza, Taner, 1990 Jimenez, Carmora et al., 1993 Krisht et al., 1994 Lang, 1995 Nomina Anatomica, 1989 In the presentstudy
Inferior hypophysial artery Dorsalmainstem Meningohypophysial trunk Posterior trunk Meningohypophysial trunk Meningohypophysial trunk Meningohypophysial trunk Meningohypophysial trunk Posterior caroticocavemous trunk
Lateralmainstem Artery of the inferior CS Lateral trunk Artery of the inferior CS Artery of the inferior CS Artery of the inferior CS Inferolateral trunk Lateralcaroticocavemous trunk
Posterior trunk
Lateraltrunk
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Capsular arteries Capsular arteries Medial group Capsular arteries Capsular arteries Capsular arteries Capsular arteries Medial group
Table 2. Comparative terms for the branches that arose from posterior trunk of the ICA Branches of main trunk
Author(s) Year
Main trunk
McConnell, 1953
Inferior hypophysial artery
Schnurer and Stattin, 1963
Dorsal main stem
Parkinson, Shields 1974
Meningohypophysial trunk:
Inferior hypophysial artery Dorsal meningeal artery Tentorial artery
Tran Dinh, 1987
Posterior trunk:
Inferior hypophysial artery Marginal tentorial artery Clival artery
Inoue, Rhoton et al., 1990
Meningohypophysial trunk:
Inferior hypophysial artery Dorsal meningeal artery Tentorial artery
Nuza, Taner, 1990
Meningohypophysial trunk
Inferior hypophysial artery Dorsal meningeal artery Tentorial artery
Jimenez, Carmona et al., 1993
Meningohypophysial trunk:
Inferior hypophysial artery Dorsal meningeal artery Tentorial artery
Krisht et al., 1994
Meningohypophysial trunk
Inferior hypophysial artery Tentorial basal branch Meningeal branch
Lang, 1995
Posterior caroticocavemous trunk
Inferior hypophysial artery Posterior clival artery Inferior hypophysial artery Tentorial basal branch Meningeal branch
Nomina Anatomica, 1989
In the present study
Inferior hypophysial artery Tentorial basal branch Meningeal branch
Posterior trunk
The McConnell's capsular artery arises from the medial side of the horizontal segment of the intracavernous lC.A., and it irrigates the pituitary gland. Inoue and Rhoton found this artery in only 8% of their case material. Tran-Dinh (1987) reported an incidence of 28.1%. Nuza (1990) found the capsular artery in 30% of the cases, and that the inferior capsular artery originated from the ICA in 5 cases and from the inferior hypophysial artery in 4 cases. Jimenez et al. (1993) reported that the McConnell's capsular artery had inferior and superior branches. The superior branch (anterior) was seen in 76.6% while the inferior capsular artery was found in 90%. In our study no artery originated from the medial group. In 6 of our dissections (20%), we saw the McConnell's capsular artery originating from the inferior hypophysial artery. Hayreh (1974) reported an incidence of 7% for the cavernous origin of the ophthalmic artery, where Harris and Rhoton (1970) reported 8%, and Tran-Dinh 15.6%. In contrast to these previous studies the present study did not find the ophthalmic artery arising from the intracavernous segment of the ICA. In their detailed study on the blood supply of the intracavernous cranial nerves, Krisht et al. (1994) stated that all the cranial nerves were supplied by the inferolateral
trunk with the exception of the proximal segment of the abducens nerve, as it is supplied by branches from the dorsal clival artery. In our study, we found that the abducens nerve lying between Dorello's channel and the petrosal apex is supplied by branches from the meningeal branch. The trochlear nerve lying between the point at which it enters the cerebellar tentorium and the superior orbital fissure is supplied by branches from the tentorial basal artery (Bernasconi-Cassinari). The proximal segment of the oculomotor nerve, that is, the segment before it reaches the oculomotor triangle, is supplied by branches from the posterior cerebellar artery. All the other segments of these nerves were supplied by the tentorial marginal branch and the branches that arise from the lateral trunk. In conclusion, we can state that (a) the Nomina Anatomica, revised every 5 years, must be a guide for anatomists and clinicians in order to provide a universally accepted terminology and avoid disagreement on the descriptions and nomenclature, and (b) given that cranial nerve deficits are the most common complications of cavernous sinus surgery, better understanding of the blood supply to these nerves as well as choosing the correct surgical approach may help to prevent such complications.
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References Hayreh SS (1974) The ophthalmic artery. In: Newton TH, Potts DG (eds) Radiology of the skull and brain. Angiography, Vol 2. St. Louis, CV Mosby, pp 1333-1350 Harris FS, Rhoton AL Jr (1970) Anatomy of the cavernous sinus: A microsurgical study. J Neurosurg 45: 169-180 Inoue T, Rhoton AL Jr, Theele D, Barry ME (1990) Surgical approaches to the cavernous sinus: A microsurgical study. Neurosurgery 26: 903-932 Jimenez Castellanos J, Carmona A, Catalina-Herrera CJ (1993) Anatomical study of the branches emerging along the intracavernous course of the internal carotid artery in humans. Acta Anat 148: 57-61 Krisht A, Barnett DW, Barrow DL, Bonner G (1994) The blood supply of the intracavernous cranial nerves: An anatomic study. Neurosurgery 34: 275-279 Lang J (1995) Skull base and related structures. Schattauer, Stuttgart New York, pp 179-191 Lasjauninas P, Moret J, Manelfe C, Theron J, Hasso T, Seeger J (1977) Arterial anomalies at the base of the skull. Neuroradiol 13: 267-272
McConnell EM (1953) The arterial blood supply of the human hypophysis cerebri. Anat Rec 115: 175-201 Nomina Anatomica (1989), Sixth Edition, Churchill Livingstone, London Nuza AB, Taner D (1990) Anatomical variations of the intracavernous branches of the internal carotid artery with reference to the relationship of the internal carotid artery and sixth cranial nerve. A microsurgical study. Acta Anat 138: 238-245 Parkinson D, Shields CB (1974) Persistent trigeminal artery: Its relationship to the normal branches of the cavernous carotid artery. J Neurosurgery 40: 244-248 Schnurer LB, Stattin S (1963) Vascular supply of intracranial dura from the internal carotid artery with special reference to its angiographic significance. Acta Radiol (Diagn) (Stockh) 1: 441-450
Snell RS (1992) Clinical Anatomy for medical students. Little, Brown and Company. 4th edition, pp 824-826 'Iran-Dinh H (1987) Cavernous branches of the internal carotid artery: Anatomy and nomenclature. Neurosurgery 20: 205-210 WilliamsPL, Warwick R (1995) Gray's Anatomy. London: Churchill Livingstone (38th edition), pp 1525-1526 Accepted March 25, 1998
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