Anastomoses Among the Perforating Arteries

Surgery for Cerebral Stroke 25 : 339•`343, 1997

Topic: Anatomy and Imaging of the Cerebral Vessels

Anastomoses among the Perforating Arteries

Slobodan MARINKOVIC, M.D., Ph.D.,1 Hirohiko GIBO, M.D., Ph.D.,2 and Ivana NIKODIJEVIC M.D.3

Summary: Because of their great clinical significance, the authors examined the anastomoses among Keywords: the perforating arteries in twenty injected hemispheres. ・perforating arteries Direct anastomoses were found among the typical perforators of the PCA (65%and 75% of the hemi- ・cerebral arteries spheres), the BA (45%),the VA (40%),and the premammillary artery (35%). The perforators of the ・anaStomoSeS ICA, AChA, MCA and Heubner's artery were connected to the pial arteries in 20%-55%. The anas- ・anatomy tomoses among the hypothalamic branches were present in 90%-95%of the cases. The authors dis- ・vascular occlusions cussed the possible significance of the anastomoses in the cerebrovascular occlusive diseases.

Surg Cereb Stroke (Jpn)25:339-343,1997

of the anterior cerebral artery (ACA) were not found Introduction . On the other hand, the vascular connections among the hypo- Because of a possible great significance of the anas- thalamic branches of the ACA and the anterior communi- tomoses involving the perforating vessels in the occlusive cating artery (ACoA) were present in 95% of the hemi- diseases, we decided to examine the vascular connections spheres (Table 1) (Fig. 1). Direct anastomoses involving the among the perforating branches of all the main cerebral recurrent artery of Heubner were not observed. However, arteries. in 55% of the hemispheres we noted the anastomoses among the olfactory and orbitofrontal branches of the Materials and Methods Heubner's artery, the ACA and the middle cerebral artery The arteries of twenty-six hemispheres were injected occasionally, in the region of the olfactory tract and trigone with india ink and gelatin or with methylmethacrylate. The (Fig. 2). brains injected with india ink were fixed in formalin for Direct anastomoses involving the perforators of the three weeks. The remaining brains were immersed in middle cerebral artery (MCA) were not seen. In 20% of the potassium hydroxide for five days to obtain vascular casts. hemispheres, however, we noted the large perforators to The arteries of the 20 best prepared hemispheres were give off small pial twigs (Fig. 3) which anastomosed with examined under stereoscopic microscope. large leptomeningeal branches of the MCA. Direct anastomoses among the typical perforators of Results the internal carotid artery (ICA) were not present. On the The anastomoses of each group of the perforators will other hand, the connections among the hypothalamic be presented separately. branches of the ICA and the superior hypophyseal artery The anastomoses among the large, typical perforators existed in 95% of the hemispheres (Fig. 4).

1Professor of Anatomy, Institute of Anatomy, Faculty of Medicine, Belgrade, Yugoslavia, 2Assistant Professor of Neurosurgery , Neurosurgical Service, Showa-Inan General Hospital, Komagane City , Japan, and 3Teaching Assistant, Institute of Anatomy, Faculty of Medicine, Belgrade, Yugoslavia (Received May 15, 1997) [Mailing address: Slobodan MARINKOVIC, M.D., Professor of Anatomy, Institute of Anatomy, Subotideva 4/2, Faculty of Medicine, 11000 Belgrade , Yugoslavia] Table 1 Characteristics of the anastomoses among the perforating arteries

Fig. 1 Ventral view of the anterior communicating artery (1), the right (2) and left (3) anterior cerebral arteries, and their hypothalamic branches: the median preoptic arteries (4), the anterior median commissural artery (5), the suprachiasmatic and the left preoptic arteries (6), the supraoptic and optic arteries (7) and the right commissural artery (8). Note a delicate vascular plexus (among arrows) in the midventral part of the lamina terminalis (9). The optic nerves (10) and the optic chiasm (11) were displaced ven- trocaudally. 12-the right internal carotid artery; 13-the posteri- or communicating arteries.

340 脳卒中の外科25:1997 Fig. 2 Ventral view of the left olfactory tract (1) and the Fig. 3 Dorsal view of the right M1 segment (1). Note a orbitofrontal cortex (2) after cutting off the tem- large perforating artery (larger arrow) which poral pole (3), the M1 segment (4) and the Al seg- gives rise to an orbitofrontal branch (smaller ment (5). Note the tiny anastomoses (small arrows). arrows) between the orbitofrontal (6) and olfactory branches (7) of the middle cerebral artery, and the olfactory branches (arrowheads) of the artery of Heubner (8).

Fig. 4 The anastomoses (arrows) among the stalk branches of the tuberoinfundibular artery (1) from the left posterior communicating artery (2), and the stalk branches of the superior hypophyseal artery (3). The pituitary stalk (4) was displaced to the right (curved arrow). 5-the left optic tract, and 6-the internal carotid artery with a ventral view.

The anastomoses involving the perforators of the ante- cal PCoA perforator, known as the premammillary artery, rior choroidal artery (AChA) were practically absent. In was involved in the anastomosing in 35% of the cases 25% of the cases we observed the common origin of the (Table 1). perforators and the uncal or the parahippocampal branch- The anastomoses involved the perforators of the ver- es of the AChA (Fig. 5). tebral artery (VA) and the anterior spinal artery in 40% of The hypothalamic (tuberoinfundibular and mammil- the cases (Table 1). Some of the VA perforators were con- lary) branches of the posterior communicating artery nected to the perforators of the basilar artery. (PCoA) were present frequently (Figs. 4 and 6). The typi- The anastomoses connected the perforators of the

Surgery for Cerebral Stroke 25: 1997 341 basilar artery (BA) among themselves or to the perforators perforators themselves, as well as between them and the of the VA or the posterior cerebral artery (Table 1). Some adjacent branches of the P1 segment (Fig. 7), the BA and/or perforators arose in common with a long pontine artery, the superior cerebellar artery (SCA). which in turn anastomosed with another long pontine The anastomoses involving the thalamogeniculate per- branch. forators of the PCA existed in 65% of the hemispheres The anastomoses involved the interpeduncular perfo- (Table 1). The anastomoses were noted among these per- rators of the posterior cerebral artery (PCA) in 75% of the forators, as well as between them and the adjacent arter- hemispheres. The anastomoses were noted among these ies.

Fig. 5 Medial and slightly dorsal view of the perforating branches (1 to 3) of the right anterior choroidal artery (4). 5-the internal carotid artery. Note one perforator (smaller arrow) to arise by a common trunk (larger arrow) with the uncal branch (6) of the AChA. 7-the posterior communicating artery.

Fig. 7 Rostral and slightly dorsal view of the basilar bifurcation site (smaller arrow). Note an anastomotic channel (arrowheads) between an interpeduncular perforator (middle- Fig. 6 Ventral view of the caudal hypothalamus. Note the anasto- sized arrows), arising by a large common moses (arrow) between the mammillary branch (1) of the left trunk (larger arrow) with the other perfo- posterior communicating artery (2) and the mammillary rators, and a peduncular branch (open branch (3) of the right posterior communicating artery (4). 5- arrows). 1-the opposite perforator which the right and left P1 segments; 6-the mammillary bodies; 7- gives off a large peduncular branch (2); 3- the median eminence; 8-the pituitary stalk. the left, and 4-the right P1 segments.

342 脳卒中の外科25:1997 Heubner, and further (through the intracerebral anasto- Discussion moses) the perforators of the ICA and the MCA.

It is obvious from our results, and the other reports, 3)5)9) that the anastomoses are more fre References quent among the hypothalamic branches than among the typical perforating 1) Adams RD, Victor M: Cerebrovascular diseases. In, Adams arteries. Direct connections did not involve the typical per- RD, Victor M (eds): Principles of Neurology. McGraw-Hill Information Services Company, New York, 1989,pp 617-692 forators of the ACA, the Heubner's artery, the MCA, the 2) Duvernoy HM: Human Brainstem Vessels. Springer-Verlag, ICA and, practically, the AChA. Only Gomes et a1.4) and Berlin, 1978,pp 5-25 Rosner et al.") have found the anastomoses among some 3) Duvernoy H, Koritke JG, Monnier G: Sur la vascularisation of these perforators in rare cases. On the other hand, the du tuber posterieur choez l'homme et sur les relations vas- culares tubero-hypophysaires. J Neuro-Visc Relat 32: 112- anastomoses are often present among the perforators of 142, 1971 the vertebrobasilar arterial system.2)7)8)10) Some of the lat- 4) Gomes F, DujovnyM, Umansky F, et al: Microsurgical anato- ter vascular connections are so frequent and large in size my of the recurrent artery of Heubner. J Neurosurg 60: 130- 139, 1984 (Table 1) that they might play an important role in the 5) Haymaker W: Blood supply of the human hypothalamus. In, cerebrovascular occlusive diseases.1) Nauta WHJ, Haymaker W, Anderson E (eds): Hypothalamus. Unlike the extracerebral segments of the ACA, the Charles C Thomas, Springfield, 1976, pp 210-218 MCA, the ICA and the AChA perforators, their intracere- 6) Kodama N, SuzukiJ: Cerebrovascular moyamoya disease, 3rd bral segments are always interconnected.6) Although these report. The study on the aging of the perforating branches and the possibility of collateral pathway. Neurol Med Chir intracerebral anastomoses are only between 20 ƒÊm and 30 15: 55-67, 1975 μm in size, they are very important part of the collateral 7) Marinkovid S, Gibo H: The surgical anatomy of the perfo- circulation in the moyamoya disease.12) rating branches of the basilar artery. Neurosurgery 33: 80- The "indirect" anastomoses involving the typical per- 87, 1993 forators are manifested in two ways. First, by their com- 8) Marinkovid S, Milisavljevid M, Kovacevic M: Anastomoses among the thalamoperforating branches of the posterior mon origin with certain pial branches (Fig. 3). Second, by cerebral artery. Arch Neurol 43: 811-814,1986 the anastomoses between the pial branches of the perfo- 9) Marinkovid S, MilisavljevidM, Marinkovid Z: Microanatomy rators and the pial branches of the main cerebral arteries and possible clinical significance of anastomoses among the hypothalamic arteries. Stroke 20: 1341-1352,1989 (Fig. 2). The latter anastomoses are probably the anatom- 10) Milisavljevid M, Marinkovid S, Gibo H, et al: The thalamo- ic basis for development of the "ethmoidal moyamoya ves- geniculate perforators of the posterior cerebral artery: The sels."12) Namely, tiny anastomotic channels are present microsurgical anatomy. Neurosurgery 28: 523-530,1991 between the ethmoidal arteries (from the ophthalmic 11) Rosner SS, Rhoton AL, Ono M, et al: Microsurgical anato- artery) and the olfactory branches in the region of the my of the anterior perforating arteries. J Neurosurg 61: 468- 485, 1984 olfactory bulb and tract. Thus, the blood in the moyamoya 12) Suzuki J, Kodama N: Cerebrovascular "moyamoya"disease , patients could flow from the ethmoidal branches to the 2nd report. Collateral routes to forebrain via ethmoid and ACA, the Heubner's artery and, occasionally, to the MCA. superior nasal meatus. Angiology 22: 223-236,1971 In this way, the blood could fill the ACA and the artery of

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