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Neuroimaging
Original research
Evaluation of the perforators of the anterior communicating artery (AComA) using routine cerebral 3D rotational angiography
  1. Stephanie Lescher1,
  2. Maja Zimmermann1,
  3. Jürgen Konczalla2,
  4. Thomas Deller3,
  5. Luciana Porto1,
  6. Volker Seifert2,
  7. Joachim Berkefeld1
  1. 1Institute of Neuroradiology, University Hospital, Goethe University Frankfurt am Main, Frankfurt am Main, Germany
  2. 2Clinic for Neurosurgery, University Hospital, Goethe University Frankfurt am Main, Frankfurt am Main, Germany
  3. 3Institute of Clinical Neuroanatomy, Dr. Senckenberg Anatomy, Neuroscience Center, Goethe-University, Frankfurt am Main, Germany
  1. Correspondence to Dr Stephanie Lescher, Institute of Neuroradiology, Hospital of Goethe University, Schleusenweg 2-16, Frankfurt am Main 60528; Germany; stephanie.lescher{at}kgu.de

Abstract

Background Damage to perforating branches of the anterior communicating artery (AComA) is a known complication of surgical or interventional treatment procedures for AComA aneurysm leading to neurologic deficits. In spite of the clinical relevance of these AComA branches, they have not been systematically analyzed using imaging techniques and most of our knowledge is based on post-mortem injection studies or neurosurgical reports. We therefore analyzed three-dimensional rotational angiography (3DRA) images of the AComA, and propose a first imaging definition of the microvascular structures surrounding the AComA.

Methods Reconstructed 3D data derived from standard-of-care rotational angiography acquisitions (5 s DSA) were retrospectively analyzed. 20 patients undergoing selective cerebral angiography and 3DRA for therapy assessment were included in our study. 3DRA datasets were reconstructed and displayed using the volume rendering technique (VRT). Additionally, multiplanar reformatted CT-like cross-sectional images (MPR) were used to evaluate the number, size, and origin of the perforators of the AComA.

Results Perforating branches of the AComA could be demonstrated in all cases with large interindividual variations in vessel visibility. MPRs appeared to be superior to total VRT volumes in the visualization of the perforating branches of the AComA.

Conclusions 3DRA can be used to visualize perforating branches of the AComA in vivo. Since damage to these perforators may result in neurologic deficits, visualization of these vessels prior to surgery or endovascular aneurysm treatment could help in the planning of therapeutic interventions. Further refinement of current imaging techniques will be necessary, however, to increase the reliability of small vessel angiography.

  • Aneurysm
  • Angiography
  • Angioplasty

https://doi.org/10.1136/neurintsurg-2015-012049

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    Introduction

    Perforating arteries arise from the posterior, posterior-superior, or posterior-inferior surface of the anterior communicating artery (AComA),1–5 but no branches are evident from the anterior aspect of the AComA. With regard to their supplied territories, they can be subdivided into hypothalamic and chiasmatic branches supplying the hypothalamic area, the chiasma, the anterior commissure, the genu of the internal capsule, and the anterior part of the globus pallidus.2–4 Another perforator is the subcallosal artery6 which bilaterally perfuses the subcallosal areas, the columns of the fornix, and the genu of the corpus callosum.6 The perforators are somewhat variable in origin, may be multiple, and their diameter is very small (range 0.1–0.8 mm, average 0.25 mm) and numbering from two to eight (average 4.1).5 ,7

    Precise identification and preservation of the perforating branches of the AComA is key to the treatment of AComA aneurysm,1 but identification is often difficult on preoperative angiograms because of the vascular complexity around the AComA and the small vessel diameter of the perforators. Using an operating microscope, visualization and identification of the perforators is often possible during surgery, but intraoperative visualization of the aneurysm neck and the perforating branches may be difficult if the ipsilateral A1/A2/AComA junction or the A2 as well as the aneurysm itself hides the neck. For interventional treatment procedures of AComA aneurysms, the display of the perforators originating from the AComA and their relation to the aneurysm might be helpful for risk assessment before stenting or angioplasty to avoid perforator strokes.8 ,9

    Injury of the perforating branches of the AComA causes hypothalamic and frontal symptoms such as memory deficits,10 ,11 cognitive dysfunction,12 ,13 cognitive impairment,14 and electrolyte disturbances in the postoperative period, in spite of excellent clinical results.15 Bilateral lesions of the fornix in particular may lead to severe clinical symptoms such as acute confusion due to Korsakoff's syndrome.16

    With recent advances in three-dimensional rotational angiography (3DRA), the ability to determine the anatomy around the AComA and the aneurysm of a patient before surgery or endovascular treatment17 has improved. We therefore retrospectively analyzed 3DRA reconstructions of a consecutive series of 20 patients with aneurysms of the AComA, focusing on the perforating arteries around the aneurysms. Using the latest generation of flat detector neuroangiography, we aimed to evaluate in a proof-of-concept study whether it is at all possible to recognize the perforating branches of the AComA with recent 3DRA.

    Methods

    Patients

    Datasets of 20 patients undergoing selective cerebral angiography and 3DRA for therapy assessment were retrospectively analyzed. All patients needed selective cerebral angiography because of suspected aneurysms in the AComA complex. The origin, size, and number of perforators of the AComA were evaluated retrospectively after reconstruction of the 3DRA datasets.

    3D rotation technique

    All data were obtained on an Axiom Artis zee biplane, software version VC21B, (Siemens, Erlangen, Germany) neuroradiologic angiography system. The angiographic system is equipped with a flat panel detector with an image matrix of 2480×1920 elements and a pixel pitch of 154 µm. In 20 patients with indications for 3DRA of the anterior circulation, we reconstructed the stored projection data of 3D DSA runs. A native 5 s rotational mask run was followed by a contrast-enhanced fill run of 5 s after mechanical intra-arterial injection of 20 mL diluted non-ionic contrast material (Ultravist 240; Bayer-Schering, Berlin, Germany) into the appropriate internal carotid artery (ICA) with a flow rate of 3 mL/s. Injection was started 2 s before the contrast-enhanced fill run. For each rotational acquisition, 133 images were obtained. The spatial resolution of flat detector CT in volumetric images was reported to be approximately 2.2 LP/mm when 2×2 binning of the detector pixels is used for rotational image acquisition, resulting in a best possible resolution of 0.454 mm.18 ,19

    Post-processing and data evaluation

    After transferring the raw data to a dedicated angiographic workstation (syngo XWP; Siemens), the 3DRA datasets were reconstructed using a volume rendering technique (VRT) as well as multiplanar reformatted CT-like cross-sectional images (MPR) with maximum intensity projections (VRT-MIP) with thicknesses between 0.1 and 1.6 mm. The cutting planes were selected by rotation of the total volume.

    The images were retrospectively reviewed by two experienced neuroradiologists, separately and blinded to each other, who determined the number, size, and origin of visible AComA perforating arteries in both the VRT volumes and the corresponding MPRs of the same 3DRA datasets. The reviewers tried to distinguish subcallosal perforators, mostly arising from the posterior or posterior-superior surface, and hypothalamic perforators, arising from the posterior or posterior-inferior surface. Additionally, the presence and origin of the recurrent artery of Heubner (RAH) was described.

    Results

    Clinical data

    The cohort consisted of 10 men and 10 women whose age ranged from 40 to 75 years. The aneurysms of 10 patients (6 men, 4 women) were treated endovascularly (coiling group), nine of which were obstructed by endosaccular coiling and one patient received aneurysm obliteration by implantation of an intrasaccular flow-diverter device (WEB Aneurysm Embolization System; Sequent Medical). Seven patients (4 men, 3 women) underwent surgical aneurysm clipping of the AComA (clipping group). In three cases with incidental findings of aneurysms of the AComA, non-interventional follow-up was favored.

    Eleven aneurysms were ruptured with clinical presentation of subarachnoid hemorrhage prior to intervention, three of whom had additional intracerebral hemorrhage. Secondary aneurysms located in the middle cerebral artery, ICA, or anterior cerebral artery (ACA) were found in eight patients.

    Perforators of the ACoA

    All patients presented with aneurysms at the AComA. The aneurysms were located anterior to the A2 segments in 14 cases and posterior in 5 cases. One patient presented with a giant aneurysm lying just adjacent to the A2 segments.

    The results of the analysis of both complementary reconstruction schemes (VRTs and MPRs with VRT-MIP cuts) of the 3DRA are summarized in table 1.

    View this table:
    Table 1

    Basic pattern of perforators of the anterior communicating artery (AComA) in three-dimensional rotational angiograph reconstructions using the volume rendering technique (VRT) and multiplanar reformatted CT-like cross-sectional images (MPR)

    On average, 2.15 perforators were observed per subject (range 1–5 branches). The subcallosal artery was the largest branch of the perforators arising from the posterior or posterior-superior aspect of the AComA and could be detected in all cases in MPRs with VRT-MIP cuts (20/20 patients) and in 18 of 20 patients in the VRT reconstructions of the total volume. The mean diameter of the subcallosal artery was 0.67 mm (range 0.49–0.96 mm) in the VRT-MIP cuts and 0.64 mm (range 0.48–0.94 mm) in the VRT reconstructions (figures 1 and 2). Owing to their smaller diameter, the hypothalamic perforators could only be displayed in MPRs and were visible in 12 of the 20 patients (mean number 1 (range 0–4) and mean size 0.53 mm (range 0.45–0.76 mm)). It was not possible to recognize any of the hypothalamic perforators with VRT reconstructions (figure 3).

    Figure 1
    Figure 1

    Volume rendering technique (VRT) images in translucent reconstruction mode (A) and multiplanar reformatted CT-like cross-sectional images (MPRs) with VRT-maximum intensity projection cuts (B and C) of the anterior circulation show an anterior communicating artery (AComA) aneurysm (*) with a subcallosal artery (arrows) originating from the AComA complex close to the neck of the aneurysm.

    Figure 2
    Figure 2

    Volume rendering technique (VRT) images (A) and multiplanar reformatted CT-like cross-sectional images (MPRs) with VRT-maximum intensity projection cuts (B and C) of the anterior circulation showing an anterior communicating artery (AComA) aneurysm with two recurrent arteries of Heubner (arrows), a perforator with an anteriorly-inferiorly route (*) and the subcallosal artery (ellipse) originating from the AComA complex close to the aneurysm.

    Figure 3
    Figure 3

    Volume rendering technique (VRT) images (A) and multiplanar reformatted CT-like cross-sectional images (MPRs) with VRT-maximum intensity projection cuts (B and C) of the anterior circulation in a patient with an anterior communicating artery (AComA) aneurysm (*) showing hypothalamic perforators (ellipse) arising posteriorly of the AComA and a recurrent artery of Heubner (arrows) with its typical reversed course along the proximal anterior cerebral artery.

    In three patients, orbitofrontal branches with anteroinferior directions originating from the lateral aspect of the AComA at the junction with the A1/A2 segment were seen (figure 4).

    Figure 4
    Figure 4

    Volume rendering technique images (A) of a giant anterior communicating artery (AComA) aneurysm adjacent to the A2 segments and two orbitofrontal perforators with anteriorly-inferiorly direction (white asterisks) arising from the A1/A2 junction. Surgical view through the operating microscope before (B) and after (C) positioning of two clips shows the perforators (asterisks) in relation to the aneurysmal neck and its preservation after clipping.

    Venous contamination was widely excluded with early start and short durations of the 3DRA scans and visual proof that small arteries originate directly from the AComA. To avoid misinterpretation of streak artifacts as perforators, various window settings and reconstruction modes (VRTs and MIP reconstructions including corresponding MPRs) with different angulations were used to identify perforators originating directly from the AComA or the aneurysm itself.

    MPRs appeared to be superior to total VRT volumes in the visualization of the perforating branches of the AComA (figure 2). The small diameter of the AComA perforators reported by others5 ,6 ,20 can be well appreciated by comparing the 3DRA images with the perforating branches arising from the AComA in an immersion fixed post-mortem brain (figure 5).

    Figure 5
    Figure 5

    Anterior part of the circle of Willis in an autopsy of the brain. The optic nerves and chiasm, internal carotid arteries, A1 and A2 segments as well as the anterior communicating artery (AComA) with associated recurrent artery of Heubner and small perforators with posterior and inferior directions are indicated.

    RAH (distal medial striate artery)

    The RAH (distal medial striate artery) was found in all but two cases. In two cases Heubner arteries were found originating from the A2 segment and the remaining 16 patients had RAHs arising from the A1/A2 junction, one of which presented with a hyperplastic RAH and three with a single hypoplastic RAH (figures 2 and 3).

    Complications due to perforator territories

    Infarctions of the genu of the corpus callosum according to perforator territories were identified in one patient in each of the coiling and clipping groups (figure 6).

    Figure 6
    Figure 6

    Infarctions of the genu of the corpus callosum due to compromise of the perforating subcallosal branch are shown in one patient in each of the coiling (upper row) and the clipping group (lower row) in diffusion-weighted images (A and D) and in the ADC maps (B and E). Diffusion restriction due to bleeding was ruled out in the CCT (C) or on T2* weighted (F). ADC, apparent diffusion coefficient; CCT, cerebral computer tomography.

    Discussion

    Perforating arteries of the AComA can be detected using modern neuroangiographic imaging. Volume rendering and CT-like reconstructions of 3DRA datasets have the potential to identify the perforating branches of the AComA and can reveal the origin and anatomical course of these arteries. A basic pattern with up to five perforators originating from the AComA could be found in all patients, with a median of 2.15 branches per patient. Neurosurgeons and interventional neuroradiologists may use this technique to identify critical structures prior to vascular surgery or intervention.

    However, the incidence and location of perforator origin in relation to the aneurysm neck has received little attention in previous publications. Anatomical cadaver and intraoperative neurosurgical studies have reported perforating arteries arising from the dorsal and inferior surface of the AComA.1–5 They can be subdivided into subcallosal, hypothalamic, and chiasmatic branches supplying the subcallosal and hypothalamic area, the chiasma, the anterior commissure, the genu of the internal capsule, and the anterior part of the globus pallidus. Lazorthes et al21 examined these arteries and noted their possible importance in AComA aneurysms, but in modern neurosurgical literature they have received little attention despite an increasing number of operations for AComA aneurysms in the past decades. Yasargil et al1 stressed the surgical and clinical importance of these vessels, naming them ‘the hypothalamic arteries’ since they perfuse the infundibulum, optic chiasm, subcallosal area, and preoptic areas of the hypothalamus. Other authors have remarked that the AComA perforators are quite regular features of the human brain.22–24 Serizawa et al5 classified the perforating branches into the following three groups according to their vascular territories: subcallosal, hypothalamic, and chiasmatic branches. The diameter, number, site, and origin of these branches were substantially different.5 The number ranged from 2 to 8 (average 4.1) and the diameter varied from 0.1 to 0.8 mm (average 0.25 mm). The subcallosal branch was observed to be single and the largest branch with a diameter ranging from 0.4 to 0.8 mm (average 0.5 mm), followed by the hypothalamic branches with a mean diameter of 0.19 mm and the chiasmatic branches were the smallest with a mean diameter of 0.1 mm.5 In the current series, the subcallosal artery was identified based on its posterior/posterior-superior direction in all cases (20/20 patients) within the MPRs of the 3DRA datasets. Hypothalamic arteries were identified based on their posterior/posterior-inferior location in 12 of the 20 patients. Owing to the limited spatial resolution of the recent neuroangiography system, it was expected that only perforators of diameters larger than 0.454 mm would be sufficiently visible. Not every branch is likely to be seen in the images, especially chiasmatic branches with an estimated diameter of 0.1 mm.

    MPRs provide more reliable detection of small vessels, as previously reported in the literature.25

    Compromise of the perforating branches from the AComA region during surgery or endovascular treatment may result in major neurologic deficits with cognitive alterations26 ,27 and/or electrolyte disturbances18 after treatment. In the current series, unilateral infarctions of the genu of the corpus callosum due to possible compromise of the perforating subcallosal branch were obvious in one patient in the coiling group and in one patient in the clipping group. Amnesia and other memory deficits were not obvious in the clinical follow-up visits of either patient after treatment. Further infarctions due to compromise of territories of the perforating branches other than the subcallosal artery were not found. The preservation of the perforating arteries around the aneurysms of the AComA complex might be especially challenging when the perforating branches directly originate from the aneurysmal neck. In 3 of 22 cases in this series (14%), the perforating arteries were adherent to the neck or the dome of the aneurysm, which was retrospectively evaluated by the authors and which would be very helpful to know prior to surgery or endovascular procedure. With regard to perforators that apparently arise from the aneurysm neck, there is a tendency for 3D reconstructed images to appear to fuse or merge vascular structures that are closely opposed to one another. This may lead to the false interpretation that a perforator arises from the surface or base of the aneurysm. Different projections and various reconstruction modes of the 3DRA were therefore obtained to exclude vessel overlap and to clearly identify the origins of the vessels.

    For the sake of completeness, the authors also looked at the RAH. Heubner described a recurrent artery which originated from the ACA and then reversed its course to run back along the proximal ACA to the anterior perforated substance. Variations in the origin of this artery have been described in detail in previous studies.7 ,8 ,28 The artery supplies the anterior part of the caudate nucleus, the anterior one-third of the putamen, and the anterior limb of the internal capsule. Occlusions of the recurrent artery can result in infarctions with clinical syndromes of aphasia, hemiparesis, and paralysis of the face and tongue. In our case series, the RAH was detectable in 18 of 20 patients and mainly arose from the A1/A2 junction.

    Recent advances in 3DRA provide a sensitive technique to characterize aneurysm geometry and to obtain information about the surgical anatomy around the AComA complex and aneurysms before surgery.17 Using an operating microscope, the origin and relation of the perforators to the aneurysm neck can also be visualized, but the visualization of them prior to surgery using high-quality 3D angiography has not yet been implemented routinely in the clinic. To the authors’ knowledge, this is the first study of the feasibility of visualizing the small perforating arteries of the AComA complex using modern angiographic equipment. Unfortunately, due to the retrospective character of the study, the intraoperative benefit of having this information preoperatively remains unclear and future studies should focus on whether this knowledge alters treatment delivery and the potential outcome. The authors believe that the ability to demonstrate the AComA perforators on imaging prior to any treatment is a valuable asset for aneurysms located in the AComA and may aid intraoperative or interventional decision-making and potentially prevent complications.

    Study limitations

    With the existing angiographic techniques and reconstruction tools, it is possible to show many but not all perforating arteries of the AComA due to its spatial resolution with a minimum of 0.454 mm. Therefore, this study did not aim to give an exact and complete anatomic definition of this region. Incomplete or delayed filling of perforators with contrast material and technical limitations in the spatial resolution of smaller branches may contribute to these limitations. Although general improvements in the technology of flat detector CT such as 3DRA in full resolution and an increased read-out rate of flat detectors has been introduced in recent years, further technological refinement will be needed to increase the reliability of small vessel angiography. Statements describing the origin and course of the perforating branches in this region therefore remain approximate attempts of definition.

    The retrospective nature of this study involves further limitations: (1) under ideal circumstances, a comparison between 3DRA and features seen at surgery would have established whether perforators seen at surgery were identified preoperatively; and (2) the question remains whether occlusion of any of these perforators results in clinical or radiological evidence of ischemia. A detailed comparison between imaging and clinical findings was not the focus of this proof-of-concept study and was therefore not attempted. The authors analyzed the 3D datasets retrospectively after the patients had undergone surgery or endovascular treatment. Information about the perforators was not provided prior to surgery or the treatment procedure. The authors therefore could not provide a comparison group in whom surgery/endovascular treatment was performed without preoperative visualization of the AComA perforators using this technique to determine whether there was a difference in the surgical or clinical outcome. This should be addressed in future studies.

    Conclusion

    3DRA can be used to visualize perforating branches of the AComA in vivo. Since damage to these perforators may result in neurologic deficits, visualization of these vessels prior to surgery or endovascular aneurysm treatment could help in the planning of therapeutic interventions. However, further refinement of current imaging techniques is needed to increase the reliability of small vessel angiography for risk assessment prior to aneurysm treatment.

    Acknowledgments

    The authors thank Dr Udo Rüb, Anatomical Institute II, Goethe University Frankfurt am Main, Germany for his help with the post-mortem analysis of the AComA.

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    Footnotes

    • Contributors SL: concept, design, data analysis and interpretation, manuscript writing and preparation. MZ, JK, LP, TD, VS: data analysis, critical review of manuscript. JB: concept, data interpretation, critical review of manuscript.

    • Competing interests JB: consulting fee or honorarium: proctor for WEB, Sequent Medical and member of the scientific advisory board of Acandis. There is a permanent scientific cooperation between Siemens Healthcare AG and the Institute of Neuroradiology and travel expenses for presentation of projects are covered by the company. The other authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article.

    • Ethics approval Ethics approval was obtained from the local ethics committee.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Data sharing statement All data are included in the study.