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Extracerebral course of the perforating branches of the anterior communicating artery: Microsurgical anatomical study
98
Surg Neural 1991;35:98-104
Extracerebral
Course of the Perforating Branches of the Anterior
Communicating
Artery: Microsurgical Anatomical Study
F. Vincentelli,
M.D.,
G. Lehman,
M.D.,
P. Rabehanta,
M.D.,
and A. Gouaze,
G. Caruso,
M.D.,
F. Grisoli,
M.D.,
M.D.
Neuroanatomical Research Unit U6, INSERM (National Institute for Health and Medical Research), Reseau Inserm, Marseille, and Laboratory of Anatomy, Aix-Marseille University, Tours, France
Vincentelli F, Lehman G, Caruso G, Grisoli F, Rabehanra P, Gouaze A. Extracerebral course of the perforating branches of the anterior communicating artery: microsurgical anatomical study. Surg Neural 1991;35:98-104.
Damage to the perforating branches arising from the anterior communicating artery, because of their blood supply to the septal nuclei and anterior hypothalamus, explains the memory impairment and the electrolyte disturbances that often follow the surgery of aneurysms located in this part of the circle of Willis. The microsurgical anatomy of these branches was studied on 60 fixed human brains, with special attention to their number, caliber, and vascular territory. The direction of the branches was evaluated, measuring the angle formed by them with thepostcommunicating segment of the anterior cerebral artery. The variability of this anatomical region is discussed in light of the literature. KEY
artery;
WORDS:
Perforating
branches;
Anterior
communicating
Aneurysm
The
postoperative morbidity of anterior communicating artery (AcoA) aneurysms is perhaps explained due to the existence of perforating branches at this level. The neurological sequelae are well known; i.e., memclose to Korsakoffs syndrome ory dysfunctions, {1,7,8,11,32,44-46,50,52), and electrolyte disturbances [27,43}. These clinical findings are related to damage of the anterior diencephalon, which is the anterior hypothalamus with the lamina terminalis in its center, the anterior white commissure, and the subcallosal region, The percentages reported in the literature are high. In 1966, Lindquist and Norlen [32] reported a 50% morbidity rate, 15% of which was
Address reprint requests to: F. Vincentelli, M.D., Clinique La Residence du Part, 5 Rue Gaston Berger, 13010 Marseille, France. Received August 28, 1989; accepted April 20, 1990. 0 1991 by Elsevier Science Publishing Co., Inc.
permanent. Microsurgical techniques have been shown to improve the surgical results, and the sequelae are rarely irreversible [49&-5701 15 1,523. However, the high incidence of AcoA aneurysms (37% of all intracranial aneurysms [Sl}) must prompt us to look for the best anatomical definition of this region, with particular regard to the perforating branches of the AcoA.
Material
and Methods
Sixty fixed human brains were taken out of the skull in one piece. Some specimens were injected with a polyester resin dyed with minium. This injection under pressure was administered to the whole body. The technique used was as follows: 1 L of polyester resin (Norsodyne NS) was treated with 10 drops of hardener (liquid cobalt) and 10 cm3 of catalyst (Butanox); 2 kg of minium powder was mixed with acetone until a liquid was obtained; the two substances were mixed and then injected via the femoral artery until coloring of the conjunctiva capillary vessels was reached (an amount of about 2.5 L). Formalin solution was injected intravenously. Some other specimens were injected using another technique in which the whole head was separated from the body. For 24 hours both internal carotid arteries and the jugular veins were flushed with water under pressure; afterward both carotids were injected with 60 cm3 of red latex and both jugulars with 60 cm3 of blue latex. The specimens were then immersed in a 20% formalin solution. Some specimens were injected with China ink, a well-known technique [14,15,41), but this does not permit good dissection of the extracerebral course of the perforators. A surgical microscope was used (M5-APO Wild-Leitz with a camera attached allowing average time exposures of 30 seconds) for the anatomical dissections. Generally, a 16-fold magnification was used, but sometimes a 40fold one was employed. An eyepiece micrometer was available to measure the arterial diameter. 0090.3019/91/$3.50
Extracerebral
Course
Surg Neurol 1991;35:98-104
99
Results The AcoA perforating branches were studied ing their number, caliber, direction, vascular and anatomical relationships.
The Perforating
Branches:
DirectionlAngle
Shot
Number,
considerterritory,
Caliber,
Perforating branches were found in 100% of the anatomical specimens. Their average number was 4.1 ? 1.8 (range l-l 1) arising from the AcoA (Figure 1). Regarding their caliber, it was found that 40% of branches ranged from 250 to 500 pm and 607~ of branches were less than 250 pm. The most frequent pattern was that of a larger trunk accompanied by other microbranches. In fact in 5070 of cases, a main trunk was found to divide itself into many small, deep branches, but it was often accompanied by other perforators. In 10 cases an artery of about 1 mm or more in outer diameter was found. Its caliber, direction, and topography pointed out that it was a median callosal artery (Figure 2). On the contrary, we did not find any azygous anterior cerebral artery. This anomaly is described in the literature [2,3,20,30}, with an incidence ranging from 1% to 2%. In our series the angle between the postcommunicating segment of the anterior cerebral artery (A2) and the AcoA perforating branches was measured: its average value was 96” (range 30”-180”), but in 70% of cases this angle ranged only from 90” to 120” (Figure 3). Vascdar
Territory
Whenever possible, taking into account the direction of the AcoA perforators, the vascular territories were divided into four regions in the sagittal plane (Figure 4): (1) lamina terminalis and hypothalamus; (2) anterior commissure, trigone, septum pellucidum, paraolfactory gyrus; (3) subcallosal region, anterior part of the cingulate gyrus; and (4) territory beyond the genu of the corpus callosum. In 12% of cases the AcoA branches supplied only territory 1. Only rarely was this territory extended to supply the optic chiasm too (only one case) (Figure 5). In 88% of cases territory 2 was supplied with these perforators, and in 3 1% of cases they seemed to supply both territory 1 and territory 2 (Figure 6). In 44% of cases the AcoA branches also vascularized the subcallosal region and the anterior part of the cingulate gyrus. In 13% of cases the median callosal artery extended the vascular territory beyond the genu of the corpus callosum. In many instances this artery, even if small in caliber, appeared to lengthen itself abnormally between the two A2s (Figure 6).
B Figure
1. (A) Lateral view showing the perforating branches of AroA and theirposterosuperior direction (black arrowhead). We have found these (B) Microradiogram, perforators in all the examined anatomicalspecimens. with selective injection, confirming tbeposterosuperiovdirection of the AcoA branches (white arrowheads). Their vascular territories are located in a sagittalplane. cc, anteriorcommissure; 44, corpus rallosum; E, opticcbiasm; pg, paraolfartoty gyrus; AL, postcommunicating segment of the anterior Cerebral artery.
Anatomical
Relationships
The anatomical relationships are mostly of surgical interest. The arterial relationships were considered, particularly the above-mentioned A2-AcoA perforators angle. The venous relationships were studied by Duvernoy et al [IG] in connection with the vascularization of the lamina terminalis. The anterior cerebral veins drained the anterior diencephalon: leaving a deep subependymal
Surg Neural 1991;35:98-104
Vincentelli
et al
Figure 2. (A-C) Lateral vieuu showing the fetal t,ype of the anterior circulation. There is a big median callosal artery (black arrowheads). equal in size to the A2 segments (white arrows). but dzfferently directed. In fact, the median callosal artery runs in the subcallosal region perpendicular to A2 (B,C), and it is easy to distinguish it from a trifurcate A2 segment. In A and C the median callosal artery is shown to reach and CYOJJover the genu of the corpus callosum (white awowhead).
B
they joined the deep sylvian veins to form the basilar veins. The relationships with the gyrus rectus (surgical approach) were also studied. Generally, there is no relationship because all the branches are directed upward (Figure l), except for some exceptional chiasmatic branches (Figure 5).
plexus,
Discussion The anatomical aspects of the anterior part of the circle of Willis have been described by many authors C6,7,13,20,21,26,28,27,31,33,34,36,37,37,40,47, 5 1,521, emphasizing the great variability in morphological patterns shown by the AcoA. Knowledge of the embryological development [35] allows us to understand these variations. At Padget stage 5 (embryo of 40 days, 16-18 mm in length) [27}, an arterial plexus appears to join the anterior cerebral arteries. The other
parts of the circle of Willis are already formed at Padget stage 4. At Padget stage 6 (embryo of 45 days, 24 mm) the median callosal artery emerges from this plexiform network. Afterward, this artery regresses or disappears. Piganiol et al [37} have seen that at the 20-mm stage, there is already a median callosal artery, disappearing at the 27-mm stage, with persistance of a residual protrusion on the AcoA. At the same time the involution of the arterial plexus leads to form the AcoA. This short embryological account allows the De Vriese [12) classification to be divided into the following three anatomical patterns, which are determined by the degree of involution of the fetal structures: Fetal type, in which the AcoA is equivalent in caliber to the Al segment and a large median callosal artery is present (Figure 2). Transitional type, corresponding to a smaller AcoA than the Al segment, with a small median callosal artery. Adult type, in which the AcoA caliber is less than one third of that of the Al. The median callosal artery does not exist or only a small protrusion can be found at the AcoA level. This classification permits us to understand the plexiform pathway of some AcoAs, defined “abnormal,” and their multiple anatomical patterns: the inconsistent presence of the median callosal artery; and the possible origin of aneurysms from residual protrusion or arterial dehiscences.
Extracerebral
Course
Figure 3. The angle between the A2 segment (CAZ) and the
Surg Neural 1991;35:98-104
AcoAperfora-
tors bad an average value of 96”; it ranges from 30” to 180”, indicating that the branches may arise from the whole circumference of the AcoA. Nevertheless, in 70% of cases this angle ranged only from 90” to 120” (red zone), making it likely to preserve these branches during surgery for A& aneurysms, eoen when it is difficult to reveal them. In fact, the clip application is, on most occasions, made perpendicularly to A2, out of the average direction of the AcoA perforators.
Perforating branches were found in all the AcoAs examined. Their existence has been denied by many authors [9,24,34,38], and many others have reported that the only branch arising from the AcoA is the median callosal artery [17,28,29,37]. The arteries supplying the anterior part of the third ventricle are considered by these authors to be Al or A2 branches. Testut and Latarjet 147) have not described the branches, but they have recognized a central territory at the AcoA. Perforating branches arising from the AcoA have been reported for the first time by Senior [42] in 1923 and The zlascular territo y of the AcoA perforators consists of four regions: (1) lamina terminalis and hypothalamus; (2) anterior commissure, fornix, septum pelhridum, and paraolfacto y gyms (regions 1 and 2 are t~ascularized by AcoA branches in 10070 of cases); (3) subcallosal region and the anterior part of the cyngulate gyrus: and (4) beyond the genu of the
Figure 4.
corpus callosum.
101
Figure 5. This is the only case in our anatomicalseries of vascularization of the cbiasm by AcoA branches (arrow). H, Heubneri- artery; -oc, optic -cbiasm.
by Rubinstein [40] in 1944. The operative findings of Krayenbuhl and Yasargil{25] in 1959 have stressed their surgical interest. Later on many papers mention these branches: In 1969 Duvernoy et al { 161 studied the vascularization of the lamina terminalis, and reported that perforators arise from the AcoA. In 1976 Perlmutter and Rhoton {36] described AcoA branches on 50 injected human brains, without specifying their number. Also in 1976 Dunker and Harris {13J accurately described the Figure 6.
Microradiogram showing both territories 1 and 2 vascularized by AcoA perforators cm). The median callosal artery (arrowhead) is weI/ visualized. This artery arises perpendicular to the A25 and it should not be mistaken for a triplicate A2.
102
Surg Neurol
Vincentelli
et al
1991;35:98-104
topography of these branches on 20 injected human brains. According to these authors, there are never fewer than three branches, except in one case of azygous anterior cerebral artery. This anomaly is to be compared with some examples of an azygous postcommunicating anterior cerebral artery reported in phylogenetic studies [12,29,49}: the median olfactory artery of fish, the frequent fusion of the A2s in rodents, the azygous anterior cerebral artery in the dog, and some primates. In 1977 Crowell and Morawetz [IO] reported the constant presence of perforators arising from the AcoA, ranging from 3 to 13, on 10 injected human brains. In their series the caliber of the branches ranged from 50 to 250 pm, with only one branch measuring 1 mm in outer diameter. In 1978 Tulleken [48] reported from two to four posterosuperior branches on 75 human brains. Regarding the common stem, which we found in 50% of cases and which was often accompanied by other microbranches, Yasargil {Sl] found a single trunk in 65% of examined AcoAs, whereas Dunker and Harris 1131 found at least three AcoA branches. The constant presence of AcoA perforating branches makes the trapping of AcoA aneurysms without a neck dangerous (Figure 7). The morphology and the length of the AcoA do not seem to influence the pattern of origin of the perforators, so when the AcoA is multichanneled, perforators may arise from the different channels. Equally, the AcoA caliber is not related to the number and caliber of its branches {52]. Aneurysms always have their neck on the side of the larger anterior cerebral artery, but no similar lateralization has been found for the perforator site of origin when the AcoA was long enough to evaluate it. In our opinion the surgical interest in the angle of the A2-AcoA branches should be stressed (Figures l-3). Perlmutter and Rhoton [36] have reported that the branches arise from the superior surface of the AcoA in 54% of cases and from the posterior surface in 36% of cases. Considering the initial direction of A2 and of the AcoA branches, this angle ranges from 30” to 180”, but in 70% it is between 90” and 120”. This latter statistical point is encouraging because the clip application for AcoA aneurysms is on most occasions made perpendicularly to A2. In these instances the AcoA perforators are very likely to be preserved, even when it is difficult to reveal them well. In our series these branches supplied the optic chiasm only once (Figure 5), whereas this feature is reported in 21% of cases in the literature [36,39]. The superior chiasmatic arteries are essentially collateral branches of Al { 13, IS]. The lamina terminalis blood supply is of an anastomotic type [lb].The 13vo of examined AcoA perforators have been found to run beyond the genu of the corpus callosum, in accordance with the findings of
Figure 7. Posterolateral view showing an ectasia ofAcoA giving r& to some perforating branches (awows). Keeping in mind this anatomicalpattern, AcoA trapping to treat AcoA aneuvyms without a neck should be considered rl hazardous procedure.
Dunker and Harris 1131, who reported 1070 of cortical pericallosal territories for these branches. The AcoA branches are, in our opinion, located in a sagittal plane, and laterally directed branches, similar to the recurrent artery of Heubner [19,23,26,48], are never found. The sagittal pathway has been confirmed by our microangiograms (Figures 1 and 6) and by the studies of Dunker and Harris [13]. The AcoA branches are directed upward and posteriorly toward the anterior commissure and the anterior part of the trigone, which they vascularize in 100% of cases [22]. The branches show a lateral inflection toward that part of the paraolfactory gyrus where the septal nuclei in humans are located. It is impossible to determine the importance of these branches in the blood supply to the hypothalamus, because its anatomy is not precisely defined. Although its location is classically subcommissural, there are some cells or nuclei, functionally close to the hypothalamus, which are situated above the anterior commissure [4,5]. However, in our opinion, the AcoA perforators are better qualified as septocommissural arteries rather than anterior hypothalamic. The damage of the septal nuclei is perhaps responsible for the frequent postoperative
Extracerebral
problems in patients with AcoA aneurysms: endocrine dysfunction due to their connection to the hypothalamus and memory impairment, because the same septal nuclei belong to the limbic system.
22. Haymaker W. Blood supply of the human hypothalamus. maker W, Andersen E, Nauta J, eds. The hypothalamus. field, Ill: CC Thomas, 1969:210-8.
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communicating
9. Critchley
M. The anterior 1930;53:120-65.
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11. Damasio A, Graff-Redford NR, Eslinger N. Amnesia following basal forebrain 1985;42:263-71.
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Heubner JBO. Zur topographie zelnen hirnarterien. Zentralbl
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Kaplan HA. The lateral perforating branches of the anterior middle cerebral arteries. J Neurosurg 1965;23:305-10.
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Krayenbuhl H, Yasargil MG. Etude clinique. In: Krayenbuhl H, ed. L’anevrisme de l’artere communicante anterieure. Paris: Masson, 1959:57-70.
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H. Disturbances of the 27. Landolt AM, Yasargil MG, Krayenbuhl serum electrolytes after surgery of intracranial arterial aneurysms. J Neurosurg 1972;37:210-8. centrale 28. Lazorthes G, Gaubert J, Poulhes J. La distribution corticale de I’artere cerebrale anterieure. Etude anatomique incidences neurochirurgicales. Neurochirurgie 1956;2:237-53. 29. Lazorthes G, Gouaze A, Salamon G. Vascularisation de I’encephaIe, vol 1. Paris: Masson, 1976:8-12.
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G, Norlen G. Korsakoff s syndrome after operation on aneurysm of the anterior communicating artery. Acta Stand 1966;42:24-34.
S, Milisavljevic M, Kovacevic M. Anatomical bases 33. Marinkovic for surgical approach to the initial segment of the anterior cerebral artery. Surg Radio1 Anatomy 1986;8:7-18. 34. Ostrowski AZ, Webster JE, Gurdjian ES. The proximal anterior cerebral artery: an anatomic study. Arch Neurol 1960;3:661-4.
PJ, Damasio H, Kassel lesions. Arch Neural
and anatomy. 35. Padget DH. The circle of Willis: its embryology In: Dandy WE, ed. Intracranial aneurysms. Ithaca: Comstock, 1945:67-90.
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13. Dunker RO, Harris AB. Surgical anatomy of the proximal anterior artery.
26. Kribs M, KIeihues P. The recurrent artery logical study of the blood supply of the normal and pathological conditions. In: circulation and stroke. Berlin: Springer,
der hein1.
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H, Delon S, Vannson JL. The vascularization 15. Duvernoy human cerebellar cortex. Brain Res Bull 1983;11:419-80. 16. Duvernoy H, Koritke JG, Monnier G. Sur la vascularisation lame terminale humaine. 2 Zellforsch 1969;102:49-77.
of the de la
17. Farnarier P, Michotey P, Moskow N, Salamon G. Etude anatomique et radiologique des branches corticales de l’artere cerebrale anterieure. Ann Radio1 1977;20:203-21. 18. Gibo H, Lenkey C, Rhoton AL. Microsurgical anatomy of the supraclinoid portion of the internal carotid artery. J Neurosurg 1981;55:560-74. 19. Gomes F, Dujovny M, Umanski F, Ausman JI, Diaz FG, Ray WJ, Mirchandani HG. Microsurgical anatomy of the recurrent artery of Heubner. J Neurosurg 1984;60: 130-9. M, Umanski F, Kim Berman 20. Gomes F, Dujovny Ausman JI, Mirchandani HG, Ray WJ. Microanatomy rior cerebral artery. Surg Neurol 1986;26:129-41. 21. Grisoli J, Piganiol G, Sedan R. L’artere cerebrale anterieure. CR Assoc Anat 1957;99:349.
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36. Perlmutter D, Rhoton AL. Microsurgical cerebral-anterior communicating-recurrent Neurosurg 1977;45:259-72.
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Salamon G. Atlas de la vascularisation I’homme. Paris: Sandoz, 1973.
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Surg Neural 1991;35:98-104
Extracerebral
Course of the Perforating Branches of the Anterior
Communicating
Artery: Microsurgical Anatomical Study
F. Vincentelli,
M.D.,
G. Lehman,
M.D.,
P. Rabehanta,
M.D.,
and A. Gouaze,
G. Caruso,
M.D.,
F. Grisoli,
M.D.,
M.D.
Neuroanatomical Research Unit U6, INSERM (National Institute for Health and Medical Research), Reseau Inserm, Marseille, and Laboratory of Anatomy, Aix-Marseille University, Tours, France
Vincentelli F, Lehman G, Caruso G, Grisoli F, Rabehanra P, Gouaze A. Extracerebral course of the perforating branches of the anterior communicating artery: microsurgical anatomical study. Surg Neural 1991;35:98-104.
Damage to the perforating branches arising from the anterior communicating artery, because of their blood supply to the septal nuclei and anterior hypothalamus, explains the memory impairment and the electrolyte disturbances that often follow the surgery of aneurysms located in this part of the circle of Willis. The microsurgical anatomy of these branches was studied on 60 fixed human brains, with special attention to their number, caliber, and vascular territory. The direction of the branches was evaluated, measuring the angle formed by them with thepostcommunicating segment of the anterior cerebral artery. The variability of this anatomical region is discussed in light of the literature. KEY
artery;
WORDS:
Perforating
branches;
Anterior
communicating
Aneurysm
The
postoperative morbidity of anterior communicating artery (AcoA) aneurysms is perhaps explained due to the existence of perforating branches at this level. The neurological sequelae are well known; i.e., memclose to Korsakoffs syndrome ory dysfunctions, {1,7,8,11,32,44-46,50,52), and electrolyte disturbances [27,43}. These clinical findings are related to damage of the anterior diencephalon, which is the anterior hypothalamus with the lamina terminalis in its center, the anterior white commissure, and the subcallosal region, The percentages reported in the literature are high. In 1966, Lindquist and Norlen [32] reported a 50% morbidity rate, 15% of which was
Address reprint requests to: F. Vincentelli, M.D., Clinique La Residence du Part, 5 Rue Gaston Berger, 13010 Marseille, France. Received August 28, 1989; accepted April 20, 1990. 0 1991 by Elsevier Science Publishing Co., Inc.
permanent. Microsurgical techniques have been shown to improve the surgical results, and the sequelae are rarely irreversible [49&-5701 15 1,523. However, the high incidence of AcoA aneurysms (37% of all intracranial aneurysms [Sl}) must prompt us to look for the best anatomical definition of this region, with particular regard to the perforating branches of the AcoA.
Material
and Methods
Sixty fixed human brains were taken out of the skull in one piece. Some specimens were injected with a polyester resin dyed with minium. This injection under pressure was administered to the whole body. The technique used was as follows: 1 L of polyester resin (Norsodyne NS) was treated with 10 drops of hardener (liquid cobalt) and 10 cm3 of catalyst (Butanox); 2 kg of minium powder was mixed with acetone until a liquid was obtained; the two substances were mixed and then injected via the femoral artery until coloring of the conjunctiva capillary vessels was reached (an amount of about 2.5 L). Formalin solution was injected intravenously. Some other specimens were injected using another technique in which the whole head was separated from the body. For 24 hours both internal carotid arteries and the jugular veins were flushed with water under pressure; afterward both carotids were injected with 60 cm3 of red latex and both jugulars with 60 cm3 of blue latex. The specimens were then immersed in a 20% formalin solution. Some specimens were injected with China ink, a well-known technique [14,15,41), but this does not permit good dissection of the extracerebral course of the perforators. A surgical microscope was used (M5-APO Wild-Leitz with a camera attached allowing average time exposures of 30 seconds) for the anatomical dissections. Generally, a 16-fold magnification was used, but sometimes a 40fold one was employed. An eyepiece micrometer was available to measure the arterial diameter. 0090.3019/91/$3.50
Extracerebral
Course
Surg Neurol 1991;35:98-104
99
Results The AcoA perforating branches were studied ing their number, caliber, direction, vascular and anatomical relationships.
The Perforating
Branches:
DirectionlAngle
Shot
Number,
considerterritory,
Caliber,
Perforating branches were found in 100% of the anatomical specimens. Their average number was 4.1 ? 1.8 (range l-l 1) arising from the AcoA (Figure 1). Regarding their caliber, it was found that 40% of branches ranged from 250 to 500 pm and 607~ of branches were less than 250 pm. The most frequent pattern was that of a larger trunk accompanied by other microbranches. In fact in 5070 of cases, a main trunk was found to divide itself into many small, deep branches, but it was often accompanied by other perforators. In 10 cases an artery of about 1 mm or more in outer diameter was found. Its caliber, direction, and topography pointed out that it was a median callosal artery (Figure 2). On the contrary, we did not find any azygous anterior cerebral artery. This anomaly is described in the literature [2,3,20,30}, with an incidence ranging from 1% to 2%. In our series the angle between the postcommunicating segment of the anterior cerebral artery (A2) and the AcoA perforating branches was measured: its average value was 96” (range 30”-180”), but in 70% of cases this angle ranged only from 90” to 120” (Figure 3). Vascdar
Territory
Whenever possible, taking into account the direction of the AcoA perforators, the vascular territories were divided into four regions in the sagittal plane (Figure 4): (1) lamina terminalis and hypothalamus; (2) anterior commissure, trigone, septum pellucidum, paraolfactory gyrus; (3) subcallosal region, anterior part of the cingulate gyrus; and (4) territory beyond the genu of the corpus callosum. In 12% of cases the AcoA branches supplied only territory 1. Only rarely was this territory extended to supply the optic chiasm too (only one case) (Figure 5). In 88% of cases territory 2 was supplied with these perforators, and in 3 1% of cases they seemed to supply both territory 1 and territory 2 (Figure 6). In 44% of cases the AcoA branches also vascularized the subcallosal region and the anterior part of the cingulate gyrus. In 13% of cases the median callosal artery extended the vascular territory beyond the genu of the corpus callosum. In many instances this artery, even if small in caliber, appeared to lengthen itself abnormally between the two A2s (Figure 6).
B Figure
1. (A) Lateral view showing the perforating branches of AroA and theirposterosuperior direction (black arrowhead). We have found these (B) Microradiogram, perforators in all the examined anatomicalspecimens. with selective injection, confirming tbeposterosuperiovdirection of the AcoA branches (white arrowheads). Their vascular territories are located in a sagittalplane. cc, anteriorcommissure; 44, corpus rallosum; E, opticcbiasm; pg, paraolfartoty gyrus; AL, postcommunicating segment of the anterior Cerebral artery.
Anatomical
Relationships
The anatomical relationships are mostly of surgical interest. The arterial relationships were considered, particularly the above-mentioned A2-AcoA perforators angle. The venous relationships were studied by Duvernoy et al [IG] in connection with the vascularization of the lamina terminalis. The anterior cerebral veins drained the anterior diencephalon: leaving a deep subependymal
Surg Neural 1991;35:98-104
Vincentelli
et al
Figure 2. (A-C) Lateral vieuu showing the fetal t,ype of the anterior circulation. There is a big median callosal artery (black arrowheads). equal in size to the A2 segments (white arrows). but dzfferently directed. In fact, the median callosal artery runs in the subcallosal region perpendicular to A2 (B,C), and it is easy to distinguish it from a trifurcate A2 segment. In A and C the median callosal artery is shown to reach and CYOJJover the genu of the corpus callosum (white awowhead).
B
they joined the deep sylvian veins to form the basilar veins. The relationships with the gyrus rectus (surgical approach) were also studied. Generally, there is no relationship because all the branches are directed upward (Figure l), except for some exceptional chiasmatic branches (Figure 5).
plexus,
Discussion The anatomical aspects of the anterior part of the circle of Willis have been described by many authors C6,7,13,20,21,26,28,27,31,33,34,36,37,37,40,47, 5 1,521, emphasizing the great variability in morphological patterns shown by the AcoA. Knowledge of the embryological development [35] allows us to understand these variations. At Padget stage 5 (embryo of 40 days, 16-18 mm in length) [27}, an arterial plexus appears to join the anterior cerebral arteries. The other
parts of the circle of Willis are already formed at Padget stage 4. At Padget stage 6 (embryo of 45 days, 24 mm) the median callosal artery emerges from this plexiform network. Afterward, this artery regresses or disappears. Piganiol et al [37} have seen that at the 20-mm stage, there is already a median callosal artery, disappearing at the 27-mm stage, with persistance of a residual protrusion on the AcoA. At the same time the involution of the arterial plexus leads to form the AcoA. This short embryological account allows the De Vriese [12) classification to be divided into the following three anatomical patterns, which are determined by the degree of involution of the fetal structures: Fetal type, in which the AcoA is equivalent in caliber to the Al segment and a large median callosal artery is present (Figure 2). Transitional type, corresponding to a smaller AcoA than the Al segment, with a small median callosal artery. Adult type, in which the AcoA caliber is less than one third of that of the Al. The median callosal artery does not exist or only a small protrusion can be found at the AcoA level. This classification permits us to understand the plexiform pathway of some AcoAs, defined “abnormal,” and their multiple anatomical patterns: the inconsistent presence of the median callosal artery; and the possible origin of aneurysms from residual protrusion or arterial dehiscences.
Extracerebral
Course
Figure 3. The angle between the A2 segment (CAZ) and the
Surg Neural 1991;35:98-104
AcoAperfora-
tors bad an average value of 96”; it ranges from 30” to 180”, indicating that the branches may arise from the whole circumference of the AcoA. Nevertheless, in 70% of cases this angle ranged only from 90” to 120” (red zone), making it likely to preserve these branches during surgery for A& aneurysms, eoen when it is difficult to reveal them. In fact, the clip application is, on most occasions, made perpendicularly to A2, out of the average direction of the AcoA perforators.
Perforating branches were found in all the AcoAs examined. Their existence has been denied by many authors [9,24,34,38], and many others have reported that the only branch arising from the AcoA is the median callosal artery [17,28,29,37]. The arteries supplying the anterior part of the third ventricle are considered by these authors to be Al or A2 branches. Testut and Latarjet 147) have not described the branches, but they have recognized a central territory at the AcoA. Perforating branches arising from the AcoA have been reported for the first time by Senior [42] in 1923 and The zlascular territo y of the AcoA perforators consists of four regions: (1) lamina terminalis and hypothalamus; (2) anterior commissure, fornix, septum pelhridum, and paraolfacto y gyms (regions 1 and 2 are t~ascularized by AcoA branches in 10070 of cases); (3) subcallosal region and the anterior part of the cyngulate gyrus: and (4) beyond the genu of the
Figure 4.
corpus callosum.
101
Figure 5. This is the only case in our anatomicalseries of vascularization of the cbiasm by AcoA branches (arrow). H, Heubneri- artery; -oc, optic -cbiasm.
by Rubinstein [40] in 1944. The operative findings of Krayenbuhl and Yasargil{25] in 1959 have stressed their surgical interest. Later on many papers mention these branches: In 1969 Duvernoy et al { 161 studied the vascularization of the lamina terminalis, and reported that perforators arise from the AcoA. In 1976 Perlmutter and Rhoton {36] described AcoA branches on 50 injected human brains, without specifying their number. Also in 1976 Dunker and Harris {13J accurately described the Figure 6.
Microradiogram showing both territories 1 and 2 vascularized by AcoA perforators cm). The median callosal artery (arrowhead) is weI/ visualized. This artery arises perpendicular to the A25 and it should not be mistaken for a triplicate A2.
102
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et al
1991;35:98-104
topography of these branches on 20 injected human brains. According to these authors, there are never fewer than three branches, except in one case of azygous anterior cerebral artery. This anomaly is to be compared with some examples of an azygous postcommunicating anterior cerebral artery reported in phylogenetic studies [12,29,49}: the median olfactory artery of fish, the frequent fusion of the A2s in rodents, the azygous anterior cerebral artery in the dog, and some primates. In 1977 Crowell and Morawetz [IO] reported the constant presence of perforators arising from the AcoA, ranging from 3 to 13, on 10 injected human brains. In their series the caliber of the branches ranged from 50 to 250 pm, with only one branch measuring 1 mm in outer diameter. In 1978 Tulleken [48] reported from two to four posterosuperior branches on 75 human brains. Regarding the common stem, which we found in 50% of cases and which was often accompanied by other microbranches, Yasargil {Sl] found a single trunk in 65% of examined AcoAs, whereas Dunker and Harris 1131 found at least three AcoA branches. The constant presence of AcoA perforating branches makes the trapping of AcoA aneurysms without a neck dangerous (Figure 7). The morphology and the length of the AcoA do not seem to influence the pattern of origin of the perforators, so when the AcoA is multichanneled, perforators may arise from the different channels. Equally, the AcoA caliber is not related to the number and caliber of its branches {52]. Aneurysms always have their neck on the side of the larger anterior cerebral artery, but no similar lateralization has been found for the perforator site of origin when the AcoA was long enough to evaluate it. In our opinion the surgical interest in the angle of the A2-AcoA branches should be stressed (Figures l-3). Perlmutter and Rhoton [36] have reported that the branches arise from the superior surface of the AcoA in 54% of cases and from the posterior surface in 36% of cases. Considering the initial direction of A2 and of the AcoA branches, this angle ranges from 30” to 180”, but in 70% it is between 90” and 120”. This latter statistical point is encouraging because the clip application for AcoA aneurysms is on most occasions made perpendicularly to A2. In these instances the AcoA perforators are very likely to be preserved, even when it is difficult to reveal them well. In our series these branches supplied the optic chiasm only once (Figure 5), whereas this feature is reported in 21% of cases in the literature [36,39]. The superior chiasmatic arteries are essentially collateral branches of Al { 13, IS]. The lamina terminalis blood supply is of an anastomotic type [lb].The 13vo of examined AcoA perforators have been found to run beyond the genu of the corpus callosum, in accordance with the findings of
Figure 7. Posterolateral view showing an ectasia ofAcoA giving r& to some perforating branches (awows). Keeping in mind this anatomicalpattern, AcoA trapping to treat AcoA aneuvyms without a neck should be considered rl hazardous procedure.
Dunker and Harris 1131, who reported 1070 of cortical pericallosal territories for these branches. The AcoA branches are, in our opinion, located in a sagittal plane, and laterally directed branches, similar to the recurrent artery of Heubner [19,23,26,48], are never found. The sagittal pathway has been confirmed by our microangiograms (Figures 1 and 6) and by the studies of Dunker and Harris [13]. The AcoA branches are directed upward and posteriorly toward the anterior commissure and the anterior part of the trigone, which they vascularize in 100% of cases [22]. The branches show a lateral inflection toward that part of the paraolfactory gyrus where the septal nuclei in humans are located. It is impossible to determine the importance of these branches in the blood supply to the hypothalamus, because its anatomy is not precisely defined. Although its location is classically subcommissural, there are some cells or nuclei, functionally close to the hypothalamus, which are situated above the anterior commissure [4,5]. However, in our opinion, the AcoA perforators are better qualified as septocommissural arteries rather than anterior hypothalamic. The damage of the septal nuclei is perhaps responsible for the frequent postoperative
Extracerebral
problems in patients with AcoA aneurysms: endocrine dysfunction due to their connection to the hypothalamus and memory impairment, because the same septal nuclei belong to the limbic system.
22. Haymaker W. Blood supply of the human hypothalamus. maker W, Andersen E, Nauta J, eds. The hypothalamus. field, Ill: CC Thomas, 1969:210-8.
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