Anatomy of the Feeding Arteries of the Cerebral Arteriovenous Malformations B
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Folia Morphol. Vol. 77, No. 4, pp. 656–669 DOI: 10.5603/FM.a2018.0016 O R I G I N A L A R T I C L E Copyright © 2018 Via Medica ISSN 0015–5659 www.fm.viamedica.pl Anatomy of the feeding arteries of the cerebral arteriovenous malformations B. Milatović1, J. Saponjski2, H. Huseinagić3, M. Moranjkić4, S. Milošević Medenica5, I. Marinković6, I. Nikolić7, S. Marinkovic8 1Centre for Radiology, Clinic of Neurosurgery, Clinical Centre of Serbia, Belgrade, Serbia 2Clinic of Cardiovascular Surgery, Clinical Centre of Serbia, Belgrade, Serbia 3Department of Radiology, Faculty of Medicine, Kallos University, Tuzla, Bosnia and Herzegovina 4Department of Neurosurgery, Faculty of Medicine, Kallos University, Tuzla, Bosnia and Herzegovina 5Centre for Radiology, Clinical Centre of Serbia, Belgrade, Serbia 6Department of Neurology, Helsinki University Central Hospital, Finland 7Clinic for Neurosurgery, Clinical Centre of Serbia, Belgrade, Serbia 8Institute of Anatomy, Faculty of Medicine, University of Belgrade, Belgrade, Serbia [Received: 8 January 2018; Accepted: 30 January 2018] Background: Identification and anatomic features of the feeding arteries of the arteriovenous malformations (AVMs) is very important due to neurologic, radio- logic, and surgical reasons. Materials and methods: Seventy-seven patients with AVMs were examined by using a digital subtraction angiographic (DSA) and computerised tomographic (CT) examination, including three-dimensional reconstruction of the brain vessels. In addition, the arteries of 4 human brain stems and 8 cerebral hemispheres were microdissected. Results: The anatomic examination showed a sporadic hypoplasia, hyperplasia, early bifurcation and duplication of certain cerebral arteries. The perforating arteries varied from 1 to 8 in number. The features of the leptomeningeal and choroidal vessels were presented. The radiologic examination revealed singular (22.08%), double (32.48%) or multiple primary feeding arteries (45.45%), which were dilated and elongated in 58.44% of the patients. The feeders most often originated from the middle cerebral artery (MCA; (23.38%), less frequently from the anterior cerebral artery (ACA; 12.99%), and the posterior cerebral artery (PCA; 10.39%). Multiple feeders commonly originated from the ACA and MCA (11.69%), the MCA and PCA (10.39%), the ACA and PCA (7.79%), and the ACA, MCA and PCA (5.19%). The infratentorial feeders were found in 9.1% of the AVMs. Contribution from the middle meningeal and occipital arteries was seen in 3.9% angiograms. Two cerebral arteries had a saccular aneurysm. The AVM haemorrhage appeared in 63.6% of patients. Conclusions: The knowledge of the origin and anatomic features of the AVMs feeders is important in the explanation of neurologic signs, and in a decision regarding the endovascular embolisation, neurosurgical and radiosurgical treat- ments. (Folia Morphol 2018; 77, 4: 656–669) Key words: angiography, arteriovenous malformations, cerebral arteries, feeding arteries, neuroanatomy, neuroradiology, neurosurgery Address for correspondence: S. Marinković, MD, PhD, Professor of Neuroanatomy, Institute of Anatomy, Faculty of Medicine, Dr. Subotić 4/2, 11000 Belgrade, Serbia, e-mail: [email protected] 656 B. Milatović et al., Feeding arteries of the AVMs INTRODUCTION MATERIALS AND METHODS Each cerebral arteriovenous malformation (AVM) Fifty-seven patients from the Clinic of Neurosur- represents an abnormal vascular network (the nidus) gery of the University of Belgrade were included in this of dilated and tortuous arteries and veins without study, as well as an additional 20 patients from the a capillary bed among them or with some micro- Department of Radiology of the University of Tuzla. vasculature in its nidus [16, 29, 47, 68, 78, 80]. The material regarding these 77 patients was collect- The AVMs receive one or more feeding arteries, and ed in the period from January 2016 to February 2017. contain the intranidal network, as well as one or Each patient had a personal history, as well as several draining veins. serial computerised tomographic (CT) and digital The feeding vessels may originate from the in- subtraction angiographic (DSA) images, while 18 of ternal carotid artery (ICA), and some additional ves- them had an additional neurosurgical report. Most sels occasionally from the external carotid artery of the DSA and CT imaging techniques, including (ECA). More often, however, they arise from the neurosurgical operations, were performed by the anterior (ACA), middle (MCA) or posterior cerebral authors of this study. artery (PCA), and in some cases from the posterior The CT examination was done in a Siemens So- communicating artery (PComA), anterior choroidal matom Definition AS 128-slice scanner (rotation time artery (AChA), or the medial (MPChA) or lateral 0.5 s, pitch 0.5, slice thickness 0.6 mm, 120–140 kV posterior choroidal arteries (LPChA), as well as from interval, manual 260 mA, noise index 3). A CT cerebral the basilar (BA) or vertebral arteries (VA), that is, angiography (CTA) was performed as well, using Ul- from their corresponding branches: the superior travist 370 as a contrast medium (bolus 100 mL, flow cerebellar (SCA), anterior inferior cerebellar (AICA), of contrast 4 mL/s). Multiplanar reconstruction and and posterior inferior cerebellar arteries (PICA), as volume rendering were made of the skull and blood well as from the small medullary and pontine twigs vessels to get three-dimensional (3D) CTA images. [16, 18, 24, 26, 78]. One or more of the mentioned The DSA in all patients was performed by the vessels may supply a single AVM, either from the Seldinger’s method, i.e. by a transfemoral cathe- same or different sources. terisation followed by an automatic injection of the A precise identification of the feeding vessels was contrast substance (Omnipaque) in a bolus of 5–8 mL performed only sporadically by neuroradiologists and per each sequence, in order to obtain a four vessel neurosurgeons [16, 18, 24, 27, 46, 78]. In general, cerebral angiography. In addition, a 3D vascular re- the parent arteries were determined, and rarely their construction was made in several patients. This was branches which directly supplied certain AVMs. In done by using a monoplane DSA unit with rotational fact, there are no articles in the available literature capabilities (Siemens Healthcare, Axiom Artis). Typ- dealing systematically with the feeding arteries. Yet, ically, 6–10 mL of Ultravist 370 was applied, when the anatomic knowledge of the feeders is clinically one anteroposterior, one lateral, and one or two very important for several reasons. Firstly, the involve- oblique angiograms were made of the carotid and ment of certain feeders and location of their AVMs vertebrobasilar systems. The field of view was 38-cm2 can usually explain neurologic signs and symptoms for the anteroposterior images, and 30-cm2 for the in patients. Secondly, feeders are used during the lateral and oblique images, whilst a 1024 × 1024 endovascular interventional radiologic procedure matrix was used. The spatial resolution was 0.32 [16, 50–53, 80]. Thirdly, some feeders are the site of × 0.32 mm. The 3D DSA typically involved a 1–3 sec- neurosurgical intervention [14, 18, 24, 27, 45, 69, 78]. ond delay, followed by a 2.5 mL/s injection of a total Finally, they can be the site of arterial aneurysms 12–15 mL. The images were reconstructed in a 256 [1, 10, 16, 19, 54, 56]. × 256 matrix. The rotational angiographic data were Accordingly, the aim of our study was, firstly, to transferred to an independent workstation (Siemens identify each single feeding vessel of the AVMs and Healthcare, Leonardo Workplace) for the generation its parent artery in our patients. Secondly, to deter- of 3D reformatted images. mine the anatomic features of the feeders, and their The obtained images of each patient were ana- relationship with a local AVM and the brain region lysed by one group, and then independently by anoth- involved. And thirdly, to consider the therapeutic er group of the authors, in order to identify the parent implications of the obtained anatomic facts. and feeding arteries. The appearance of each feeder 657 Folia Morphol., 2018, Vol. 77, No. 4 Figure 1. The leptomeningeal (pial) branches of the main cerebral arteries. A. Branches of the anterior and posterior cerebral arteries on the medial and inferior surface of the cerebral hemisphere. 1 — the A2 segment. Note the medial orbitofrontal artery (2), frontopolar (3), perical- losal (4), callosomarginal (5), the anterior (6), middle (7) and posterior internal frontal (8), paracentral (9), superior parietal (10), and the pre- cuneal arteries (11). Also note the P2 segment of the posterior cerebral artery (12), the parieto-occipital (13), calcarine (14), and the posterior temporal (15), middle temporal (16) and anterior temporal arteries (17). B. The leptomeningeal branches of the middle cerebral artery on the superolateral surface of the hemisphere. Note the prefrontal arteries (1), precentral (2), central (3), anterior parietal (4), posterior parietal (5), angular gyrus (6), temporo-occipital (7), and the posterior temporal (8), middle temporal (9) and anterior temporal arteries (10). was then examined carefully. The mentioned imaging As regards the supraclinoid (C4) segment of the procedures were approved by the authorities of the ICA, it always gave rise to the typical side and the ter- Clinic of Neurosurgery, Department of Radiology, and minal branches, i.e. the PComA, AChA, ACA and MCA, the Ethics Committee of the University Clinical Centre. but also occasionally to the uncal branch (12.5%), and Statistically, the frequencies of the feeders and their 1–4 perforating twigs in all the cases. parent arteries were counted. The ACA had, more or less, a typical appearance Finally, the arteries of 4 brain stems and 8 cerebral in the examined specimens. In only 1 case a hypo- hemispheres, taken from routine autopsies, were plasia of its proximal (A1) segment was observed. washed out with a 10% saline solution and perfused This segment gave off 1–3 perforating twigs, as well with a 10% mixture of India ink and gelatine.