Cerebral revascularization model in a swine

6 Springer-Verlag 2005 Printed in Austria

Cerebral revascularization model in a swine

M. Reinert 1, C. Brekenfeld2, P. Taussky1, R. Andres1, A. Barth1, and R. W. Seiler1

1Department of Neurosurgery, University Hospital of Bern, Bern, Switzerland 2Department of Neuroradiology, University Hospital of Bern, Bern, Switzerland

Summary

The purpose of this study was to analyze the suitability of the cerebral vasculature of the pig regarding a revascularization proce- dure.

In two 60 kg pigs the femoral artery was exposed and canulated for selective angiography and interventional procedures. After the angiography, the pigs were brought to the animal OR for craniot- omy and analysis of the intracranial cerebral arteries and the surgical exposure of the carotid arteries under the microscope.

Angiography demonstrated the presence of a true internal-, exter- nal carotid artery and vertebral arteries. Both the vertebral and inter- nal carotid arteries are feeding a rete mirabilis both at the cranial base and the cranio-cervical junction. At these sites further advance- ment of the angiography catheter was not possible. Out of these rete mirabilis, an intracranial carotid artery and an intracranial vertebral artery were formed, respectively. The intracranial cerebral vessels were of the dimension of 1 mm and less. The extracranial portion of the internal carotid artery was 2.5 mm of diameter.

From these findings, we conclude that a direct cerebral revascula- rization procedure of the intracranial vessels is not possible in the swine. However, a global revascularization procedure on the extrac- ranial portion of the internal carotid artery is thus feasible, both using a low- and high-flow anastamosis technique.

Keywords: Cerebral revascularization; model; pig; angiography;

anatomy.

Introduction

Cerebral revascularization is being performed in patients with moyamoya disease by using a direct extracranial-intracranial (EC-IC) anastomosis tech- nique [7]. Further cerebral revascularization is indi- cated in patients su¤ering of large blood vessels anomalies such as aneurysms or carotid occlusion [6, 10]. In these patients a direct high-flow anastomosis technique may be necessary by using a technique with- out any temporary occlusion. The development of new diagnostic techniques such as the

O

extraction method in the positron emission tomography (PET)

has led to the analysis of patients having a hemody- namic compromise. Patients with clinical symptomatic carotid occlusion and increased hemispheric oxygen extraction fraction (OEF) > 1.130 may benefit of a surgical revascularization procedure [1, 2, 9]. In ongo- ing multicenter studies in Japan (Japanese Carotid Atherosclerosis Study: JCST) [2] and the United States (carotid occlusion surgery study: COSS) [2] [4] patients are being recruited. The recent reports of the interim analysis in both studies are in favour for the combined surgically and medically treated group [8].

The possibility of measuring the OEF prior and after a revascularization procedure has led to the idea of comparing two surgical procedures, such as a stan- dard EC-IC bypass and an excimer laser assisted non- occlusive anastomosis (ELANA)-technique, which is basically an immediate high-flow anastomosis without any temporary occlusion [5]. An appropriate animal model is thus necessary. The literature of the cerebral vasculature of the pig was however not conclusive on the exact anatomy and blood flow territory of the internal carotid artery [3] and the role of the rete mira- bilis at the cranial base.

Prior to starting any PET and revascularization study, the exact anatomical situation and possible operative and interventional approaches need to be defined.

Materials and methods

Two 60 kg pigs were sedated with atropine, xylazine and ket- amine. An intravenous line was placed in the ear. Anesthesia was initiated with thiopentone and the animals were then intubated and ventilated. Anesthesia was maintained with fentanyl and thio- pentone. The femoral artery was surgically exposed and canulated with a 6 french catheter sheath for selective angiography and inter-

ventional procedures. Thereafter, the animals were transported to the angiography-suite (CAS500, Toshiba Ltd. Japan, Matrix 1024
1024, biplanar).

The following procedures were performed in Pig 1 Selective angiography of the truncus bicaroticus, common carotid, right internal and external artery, left internal and external carotid artery was performed.

Thereafter, both vertebral arteries were selectively canulated. The animal was then transported to the an- imal operating theatre. A right sided craniectomy to the skull base was performed. The dura was opened and the brain was exposed. From the cranial base, the intracranial portion of the internal carotid artery, fol- lowing the rete mirabilis, was exposed and followed to the first bifurcation.

The following procedures were performed in Pig 2 After selective angiography with a microcatheter, the left internal carotid artery was occluded with coils up to the rete mirabilis. Thereafter a left external ca- rotid angiogram was performed, followed by canula- tion of the right internal carotid artery and occlusion with coils. The occlusion was documented and collat- erals from the external carotid artery were assessed by a control angiogram of the common carotid artery.

Next, the vertebral artery was catheterized and a verte- brobasilar angiogram was performed. The animal was then brought to the animal operating theatre. On both sides the common carotid, internal and external ca- rotid arteries were exposed. Finally, the arteries were excised including the intravascular coils.

Intraoperativ images were performed using a digital camera (Sony DSC-T1 and Nikon Coolpix 990). The images were processed using Corel Draw2 (Corel- Draw 9.0, Ottawa, Canada).

Results

The pig has a truncus bicaroticus which splits into a left and right common carotid artery. The common carotid artery divides into an internal and external carotid artery. The internal carotid arteries supply the major part of the brain except the brain stem and the cerebellum. The extracranial portion of the internal carotid artery ends in a rete mirabilis, which is a sort of vascular sponge out of which forms the intracranial portion of the internal carotid artery.

The intracranial portion of the internal carotid ar- tery then divides into the caudal communicating artery and the end-segment of the internal carotid artery. The first branch leaving the internal carotid artery is the caudal communicating artery. The internal carotid artery then turns rostrally to give o¤ several smaller middle cerebral arteries. From this point, the artery is called rostral cerebral artery (Figs. 1 and 2).

The extracranial vertebral artery also ends in a caudal rete mirabilis just at the cranio-caudal junction before entering the dura. This caudal rete mirabilis is, however, not as prominent as the rostral one. Out of this caudal rete mirabilis results an intracranial verte- bral artery which then gives rise to the basilar artery together with the contralateral vertebral artery (Fig.

1d).

Selective angiography of the extracranial portion of the internal carotid artery showed ‘‘primitive’’ arteries between the internal carotid arteries and the basilar artery (Fig. 1b).

Angiographic dimensions of the extracranial and intracranial vessels

The extracranial internal carotid artery measured 2.5 mm in diameter at the bifurcation. Before entering the rete mirabilis the internal carotid artery measured 2 mm. The internal carotid artery following the rete mirabilis was of the dimension of 1 mm in diameter (Fig. 1b). The diameter of the rostral artery and the caudal communicating artery was of 0.5 mm and 0.4 mm respectively. The intracranial vertebral artery and basilar artery diameters were below 1 mm.

Coil occlusion of the internal carotid arteries

After occlusion of the left internal carotid artery

with coils, a strong collateralization via the rete mira-

bilis from the right side was seen (Fig. 1c). After occlu-

sion of both internal carotid arteries, the vertebral an-

giography showed a fine contrast filling in the anterior

circulation via the caudal communicating artery. The

external carotid angiogram showed that it is not in-

volved in the perfusion of the brain except with a tiny

contrast filling over an ethmoidal anastomosis. The

ophthalmic artery splits o¤ from the external carotid

artery. Selective injection of the vertebral artery after

occlusion of both internal carotid arteries leads to a

contrast filling of the caudal communicating arteries

Fig. 1. (a) Lateral left internal carotid angiogram showing the rete mirabilis, the caudal communicating artery and the intracranial carotid artery. (b) Anterior-posterior left internal carotid artery angiogram showing the primitive artery, the rete mirabilis and the middle cerebral ar- tery branches. (c) Anterior-posterior right common carotid angiogram after coiling of the left internal carotid artery: showing the cross-flow over the rete mirabilis. (d) Anterior-posterior right vertebral angiogram after coiling of both internal carotid arteries: showing the right verte- bral artery, the anterior spinal artery, the basilar artery, the caudal communicating artery and the internal carotid artery

and thus the middle and anterior cerebral arteries (Fig.

1d).

Intraoperative situs

Rightsided craniectomy

The craniectomy or craniotomy is a laborious bony work, to finally reach the dura. After opening of the dura under the operating microscope and retraction of the brain, the intracranial carotid artery was dem- onstrated, as well as its branches. These vessels were

extremely fine, with a diameter of 1 mm for the intra- cranial carotid artery (Fig. 2a).

Preparation of the carotid arteries

The preparation of the carotid arteries was techni- cally achieved without any complications. The com- mon carotid artery was 3.2 mm in diameter, depend- ing of manipulation and thus vasospasm. The internal carotid artery at the bifurcation site was 2.5 mm in diameter (Fig. 2b).

Discussion

The purpose of this study was to find out if a swine model is suitable for a cerebral revascularization pro- cedure. The specific aim was to assess the swine as a possible model to test the di¤erence between two by- pass techniques: the standard EC-IC bypass and the Excimer laser assisted non-occlusive anastamosis tech- nique (ELANA). Therefore, this study of the intracra- nial blood vessel situation and dimensions was per- formed as the situation could not be clarified from the accessible literature.

Four new findings were observed in this study, which were previously not expressly stated. First, the rete mirabilis can not be passed by a selective angio- graphic microcatheter. Second, the external carotid artery does not participate in the cerebral perfusion.

The third finding is that the intracranial anatomical situation is such that a microvascular anastomosis technique is at the limit of the technically possible, and certainly not suitable for an ELANA-Bypass pro- cedure. The fourth finding is the di¤erence of the diam- eters of the internal carotid artery prior to and after the rete mirabilis, eventhough there were no other vessels leaving the rete mirabilis. We hypothesize that this may only be possible if the rete mirabilis has a sort of balloon function, where a pulsatile blood flow con- verges into a more continuous blood flow. A higher flow rate could also be possible but is less probable to our view since the blood pressure decrease over the rete mirabilis must be considerable.

An experimental revascularization procedure can, however, still be considered in the swine, by perform- ing a bypass on the extracranial portion of the internal carotid artery. By doing this we could test the di¤er- ence in OEF using a low-flow versus a high-flow by- pass technique. The practicability of this new setup will be tested in another series of pigs.

Fig. 2. (a) Intraoperative view of the internal carotid splitting into the caudal communicating artery and the end-segment of the internal carotid artery. (b) Operative exposure of the common carotid, inter- nal and external carotid arteries. This exposure is suitable for per- forming a high flow anastomosis, using for example the excimer laser assisted high-flow anastomosis technique. The schematic bypass is shown in green. In this exposure, the occlusion of the carotid artery is induced by coiling of the vessel lumen

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Correspondence: Michael Reinert, Klinik fu¨r Neurochirurgie, Inselspital Bern, Universita¨t Bern, 3010 Bern, Switzerland. e-mail:

michael.reinert@neurochirurgie-bern.ch