Original articles Arterial supply of the temporo-medial region of the brain significance for preoperative vascular occlusion testing W. Lüdemann, C. Schneekloth, M. Samii and S. Hussein Department of Neurosurgery, Medical School Hannover, 30625 Hannover, Germany Received September 23, 2000 / Accepted in final form October 01, 2000 Key words: Microsurgical anatomy - Anterior choroidal artery - Posterior cerebral artery - Temporomedial region

Abstract The mesiobasal limbic system is of particular significance in the surgical treatment of temporo-medial tumors and epilepsy. It consists of the uncus, amygdaloid body, hippocampus, dentate gyrus, subiculum, fasciolar gyrus and the parahippocampal gyrus. Knowledge of the vascular microanatomy is a key to the surgical treatment of pathologies in the region. The anterior choroidal artery was selectively injected in fresh brain specimens 50 specimens with a gelatinous ink mixture to demonstrate vascular territories in stereotactic brain slices, and 50 with a Biodur resin to obtain casts for microanatomical evaluation. The cast technique was also applied to 35 specimens injected into the posterior cerebral artery. The rostral third of the temporomedial region is mainly supplied by branches of the anterior choroidal artery. The occipital two thirds are supplied by hippocampal branches, the posteromedial choroidal artery and the inferior temporal branches of the posterior cerebral artery. Important vessel variations with significant implications for the preoperative Wada-test are presented

Vascularisation artérielle de la région temporale médiale. Importance en test d'occlusion vasculaire per-op ératoire Résumé Le système limbique mésio -basal a une importance toute particulière dans le traitement chirurgical des tumeurs temporales médiales et de l'épilepsie. Il est formé par l'uncus, le corps amygdaloïde, l'hippocampe, le gyrus dentatus, le subiculum, le gyrus faciolaris et le gyrus parahippocampal. La connaissance de sa microvascularisation est d'une grande importance pour le traitement chirurgical des pathologies de cette région. L'artère choroïdienne antérieure a été injectée sélectivement sur des cerveaux frais. 50 sujets ont été injectés avec un m élange d'encre gélatineuse pour l'étude des territoires vasculaires à l'aide de coupes stéréotaxiques d'encéphales. 50 autres sujets ont été injectés avec une résine Biodur pour obtenir des moules dans le but de préciser la micro -anatomie. La technique de moulage a été aussi employée sur 35 cerveaux par injection de l'artère cérébrale postérieure. Le tiers rostral de la r égion temporale m édiale était principalement vascularis é par des branches de l'artère choroïdienne antérieure. Les deux tiers occipitaux étaient vascularisés par les branches hippocampales de l'artère choroïdienne postérieure et médiale et par les branches temporales inférieures de l'artère cérébrale postérieure. D'importantes variations vasculaires, présentant un grand int érêt pour le test WADA préopératoire, sont exposées. Knowledge of the arterial supply of the medial part of the temporal lobe is of significance for neurosurgical and neurovascular intervention in this area. Vascular structures, such as branches of the anterior choroidal artery (AChA), could serve as guiding anatomical landmarks during tumour or epilepsy surgery. The vascular supply of the amygdaloid body, dentate gyrus, hippocampal area, parahippocampal gyrus, uncus and subiculum is of particular interest. Ontogenetically these areas were supplied by branches of the AchA, however with their mediobasal movement during expansion of the neocortical areas, their supply has been taken over by the vertebrobasilar circulation [1]. Preoperative endovascular testing with the injection of sodium amytal into the internal carotid artery (Wada -Test) has been used to predict postoperative deficits. Neuropsychological scores are determined before and after injection and patients are excluded from surgery if there is a significant reduction in performance. However, the significance of preoperative endovascular occlusion tests depends on vessel variations in this region.

Several studies on the microsurgical anatomy have been performed [2, 3, 5, 7, 8, 10, 11, 12, 14, 15, 17, 20], whereas there have been no injection studies demonstrating the extent of individual vascular territories in the temporo-medial region. Material and methods One hundred and thirty human brains without macroscopic pathological signs were obtained 6-12 hours post-mortem. After initial fixation in 10% formalin for 3 hours, the anterior choroidal artery was selectively injected. Fifty specimens were injected with a gelatinous ink mixture (0.1 ml saturated ink combined with 0.5 ml saturated ink with 7% gelatine at 30˚ C) to permit evaluation of vascular territories in stereotactic brain slices. A further 50 specimens were injected with a Biodur resin (0.3 -1 ml of 66% Biodur E20 (Biodur Heidelberg, Germany), 28% Biodur E22 (Biodur Heidelberg, Germany) and 10% methylketon) to obtain casts for microanatomical evaluation. The cast technique was also applied to 35 specimens injected into the posterior cerebral artery (PCA). After fixation for 6 weeks in 10% formaline the cast specimens were subjected to microanatomical dissection. To determine the vascular territories (Fig. 2) the ink -injected specimens were sliced for stereotactically -orientated evaluation according to Schaltenbrand and Wahren [19]. For this purpose the brains were embedded in 3% agar-agar and cut using a special designed device (Fig. 1) with a section thickness of 0.4 mm.

Fig. 1 Sectioning-device designed for the production of stereotactically-orientated brain slices. The whole brain is embedded in agar-agar and is cut after orientation in this device using ventriculographic detection of the connecting line between anterior and posterior commissures as baseline. A, fixation plate

Fig. 2 Stereotactically-orientated brain slice (Fp 9.0 according to Schaltenbrand and Wahren, posterior view) for evaluation of vascular territory after selective ink injection (blue staining) into both anterior choroidal arteries Results Microanatomical dissection Anastomosing arteries between the proximal part of the anterior choroidal (Table 1) and posterior cerebral arteries ( Table 2) were demonstrated in 52% of specimens (Fig. 3). Further connections between both vessel territories were regularly observed

along the lateral geniculate body and the choroidal plexus of the temporal horn (Fig. 4 ). Anastomoses between the anterior choroidal and middle cerebral arteries (MCA) were demonstrated in 12% of specimens, being in the uncal area between the uncohippocampal branches of the anterior choroidal artery and the uncal branches arising from the middle cerebral artery. Anastomoses between the anterior choroidal and posterior communicating arteries (PcoA) were demonstrated in 14% of specimens in 2.5% the anterior choroidal artery originated from the posterior communicating artery. Anastomosing branches from the internal carotid artery were demonstrated in 5% of specimens along the optic tract.

Fig. 3 Basal microscopic view of the crural cistern demonstrating the course of the Biodur-injected anterior choroidal artery (AchA ) and the hippocampal branch ( hb). An anastomotic branch (arrow ) to the posterior cerebral artery (P2) runs from the hippocampal sulcus (arrowheads) to the origin of the posterior lateral choroidal branch (PLchb). Cc , crus cerebri III, oculomotor nerve

Fig. 4 Basal microscopic view of the crural cistern demonstrating the course of the Biodur-injected anterior choroidal artery (AChA ) and the hippocampal branches ( hb). This specimen shows a different anastomotic connection between posterior cerebral artery (P2) and the AChA (see text) when compared with Fig. 3. Note the difference in caliber of the two arteries

Table 1. Branches of the anterior choroidal artery (AChA) for the blood supply of the temporo-medial region

Table 2. Branches of the posterior cerebral artery (PCA) for the blood supply of the temporo-medial region Evaluation of vascular territories After selective injection of ink into the anterior choroidal artery staining was seen in the amygdaloid body in 91% of specimens (Table 3 ) 59% of the hippocampal formations and 56% of the uncus were also stained. Staining was demonstrated in the dentate gyrus in 41% of specimens, in the subiculum in 37% and in the parahippocampal area in 34%.

Table 3 . Results from evaluation of the vascular territory after selective ink injection into the anterior choroidal artery (see Figure 1). The mean stained area is given as a percentage (n = 50) Variations In 5.8% of specimens no hippocampal branches from the PCA were demonstrable, thus the arterial supply of the hippocampal formation was dominated by the AChA. In 2 specimens (4%) the AChA territory was observed to extend towards the occipital cortical area (Fig. 5). A similar reciprocal supply was noted in the uncal area with the uncal branches from the MCA and the uncohippocampal branches of the AChA.

Fig. 5 Basal view of a brain specimen after selective injection of the anterior choroidal artery (arrowheads) demonstrating an important variation. The long course of the AchA with extension into the collateral sulcus and supply of the posterior cerebral artery territory was demonstrated in two specimens (4%) Discussion The present study has shown the highly variable arterial supply of the temporo-medial region, being most striking for the hippocampal formation where the territories of PCA and AChA are closely connected, and proximal (52%) and distal anastomoses are regularly demonstrable [8, 14]. Selective injection into the AChA demonstrated a 59% supply of the hippocampal formation, but in 5.8% of specimens no hippocampal branches from the PCA were observed. This variable extension of the AChA territory has its origin in the embryological development of the PCA [1] its mediobasal movement with expansion of the neocortical areas leads to domination by the vertebrobasilar system in this area. The AChA is the dominating artery in the early stages of development [9, 13] with a large telencephalic territory and the variations described (Fig. 5) representing some conservation of this early developmental stage. Descriptions of this artery as the PCA are therefore wrong [4]. In fact the AChA shows few variations in its origin [16 , 18] (97.5% ICA 2.5% PcoA in this series) related to the early developmental anlage. In contrast, the anastomotic network between the AChA and the later developing MCA, and especially the PCA, is highly variable. Another region with a reciprocal relationship between two vascular territories is the uncal area and, to a lesser extent, the amygdaloid body. The blood supply of the amygdaloid body was of AChA origin in 91% of specimens in the present study the remaining 9% most probably being supplied by branches of the MCA. With a missing anterior inferior temporal branch from the PCA in 8% (Table 2 ) the temporo-polar cortical region was probably also supplied by branches from the MCA [8]. The variable extent of the AChA territory [1] and the medial perforating branches, with their peduncular, capsulothalamic

and optic supply [14], are the main reasons for difficulties in treating arteriovenous malformations [6] and aneurysms [21] arising from the AChA. It is considered to be the most dangerous artery for surgical and interventional procedures [9]. It should be noted that pre-surgical neurovascular tests may lead to uncertain results, even when using selective injection techniques with catheterization of specific arterial branches instead the ICA itself [8]. If the PCA is injected prior to a selective amygdalohippocampectomy (Fig. 6), there is a 5.8% risk of an underdeveloped PCA supplying the region of interest.

Fig. 6 Schematic drawing of the hippocampus (asterisk) demonstrating the involved vessels for presurgical evaluation prior to hippocampectomies (selective Wada - Test). As demonstrated here, one possible route is the selective catheterization of the P2 segment of the posterior cerebral artery via the basilar artery (BA) and filling of the posterior lateral choroidal branches (PLchb). Superselective catheterization of the anterior choroidal artery (AchA ) via the internal carotid artery ( ICA) is another possibility With regards to the reported observations neuropsychological testing should be performed with occlusion of both the AChA and PCA. Conclusion The vascular supply of the temporo-medial region arises from the MCA, AChA and PCA, with the uncal area being supplied by both MCA and AChA branches. The supply of the amygdaloid body and the rostral third of the hippocampus is dominated by branches from the AChA. In general, the occipital two thirds of the hippocampal formation are supplied by PCA branches, but vessel variations with extension of the AChA territory with an underdeveloped PCA are not uncommon. These findings are of important clinical significance and insecure the evaluation of presurgical occlusion tests.

References

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