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Round table: Giant intracranial aneurysms

Imaging of giant cerebral aneurysms Imagerie des anévrysmes cérébraux géants E. Tollard a,∗ , G. Perot a , E. Clavier a , E. Gerardin a,b a b

Department of Neuroradiology, Rouen University Hospital, 1, rue de Germont, 76031 Rouen cedex, France INSERM U982, Rouen University Hospital, Rouen, France

a r t i c l e

i n f o

Article history: Received 28 April 2013 Received in revised form 5 October 2013 Accepted 19 October 2013 Keywords: Digital subtraction angiography Magnetic resonance imaging Computed tomography Giant aneurysms Diagnosis

a b s t r a c t The aim of this study was to review the different imaging techniques for analysing giant intracranial aneurysms (digital subtraction angiography [DSA], magnetic resonance imaging [MRI], computed tomography [CT]) imaging and explain their respective contribution to the understanding of the characteristics of these complex aneurysms. Giant aneurysms have a complex pathology with multiple stages of evolution and consequences. Therefore, complex imaging is mandatory to enhance the understanding of these parameters and to plan an often complicated treatment strategy. DSA remains the gold standard for analysing aneurysms, but non-invasive sectional imaging (CT, MRI) also provides essential information in the specific case of giant aneurysms. © 2014 Elsevier Masson SAS. All rights reserved.

r é s u m é Mots clés : Angiographie numérisée Imagerie par résonance magnétique Scanner Anévrysmes géants Diagnostic

L’objectif de cet article est de faire le point sur les différentes techniques d’imagerie utilisées pour l’étude des anévrysmes géants : angiographie digitalisée, imagerie par résonance magnétique, scanner; et, d’expliquer leur contribution respective dans la compréhension et l’exploration des caractéristiques spécifiques de ces formations anévrysmales complexes. Les anévrysmes géants sont des malformations complexes présentant de multiples types d’évolution et de complications. Un bilan d’imagerie complet est obligatoire afin de mieux évaluer toutes les caractéristiques de la malformation et permettre de planifier la stratégie d’une thérapeutique souvent complexe. Si l’angiographie numérisée reste l’examen diagnostique de référence, les examens non invasifs tels que tomodensitométrie crânio-encéphalique et imagerie en résonance magnétique procurent aussi des informations essentielles dans le cas particulier de ces malformations anévrysmales géantes. © 2014 Elsevier Masson SAS. Tous droits réservés.

1. Introduction In the last two decades, major improvements in non-invasive (without injection), or minimally invasive (with intravenous injection), angiographic techniques have changed modalities in imaging aneurysms. Digital subtraction angiography (DSA) remains the gold standard [1], despite being an invasive technique with intra-arterial injection after supra-aortic catheterisation. However, computed tomography angiography (CTA) and magnetic

∗ Corresponding author. E-mail addresses: [email protected], [email protected] (E. Tollard).

resonance angiography (MRA) have made vascular intracranial examination both easier and more widespread. A recent review [2] compared the spatial resolution of current imaging techniques (0.6–1 mm for MRA, 0.4–0.7 mm for CTA, 0.2 mm for DSA and, 0.15 mm for 3D rotational angiography) and assessed their important role in imaging aneurysms. Depicting a small size aneurysm is not the primary concern in imaging giant aneurysms, however 3D reconstruction, which requires good spatial resolution, may be useful with these different imaging modalities. Giant aneurysms have specific morphological and physiological characteristics requiring further exploration than vascular examination alone. The thrombosed portion, mass effect, inflammatory wall and, hypoperfusion of the downstream parenchyma necessitate exploration by computed tomography (CT) and

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magnetic resonance imaging (MRI) as would any tissular brain lesion [1]. The aim of this chapter was to present the different available techniques and emphasize their essential role in understanding giant aneurysms, in order to ensure optimum patient management. Many references from the literature, quoted in this section, refer to giant serpentine aneurysms, however the techniques can be extended to any type of giant aneurysm (saccular, fusiform or serpentine). 2. What needs to be analyzed? The giant aneurysm and its subsequent consequences, which occur on the surrounding brain structure such as parenchymal, parent and distal arteries, perforating arteries should be analysed. 2.1. The aneurysm A giant aneurysm is still an aneurysm and is defined as localized, pathological, blood-filled dilatation of a blood vessel caused by a disease or weakening of the vessel’s wall. Therefore, it is essential to understand the circulating portion, comprising neck, depth and diameter, as well as the related arteries, which is made up of the parent artery and efferent arteries. When it contains a thrombosed part, this must also be analysed for size and inflammation within the wall, using peripheral enhancement. 2.2. Consequences on surrounding brain structure These aneurysms tend to manifest with a mass effect or embolic episodes. Thus, the aneurysm may be located in a bone canal, such as the petrous segment of the internal carotid artery, requiring exploration of the skull base. Alternatively, the aneurysm may be located on branches of the circle of Willis, requiring exploration of the brain parenchyma, meningeal structures, cranial nerves and ventricular system. This is especially the case for giant aneurysms of the posterior fossa, which can compress the fourth ventricle. When containing a thrombosed portion, some clots may migrate, occlude arterial branches and cause ischaemia. The size of the brain infarction varies depending on the size of the branch: from punctate lesions, when micro thrombi occlude very distal branches, to a major stroke, when an arterial trunk is occluded. This is usually tolerated in giant serpentine aneurysms where slow flow induces collateral development [2–4]. Similar to other aneurysms, giant aneurysms may bleed and be responsible for subarachnoid hemorrhage and/or intra-parenchymal haematoma. Usually the onset of acute symptoms leads to an emergency diagnosis. 3. Which examinations are used? Different well-known imaging techniques (X-ray, MRI) are performed in order to diagnose and analyse aneurysms, mainly digital subtraction angiography (DSA), CT and MRI. The aim of this section was to describe the different patterns of giant aneurysms for each examination modality. 3.1. Digital subtraction angiography The common carotid, internal carotid and verterbral arteries, were selectively catheterised through arterial access (primarily femoral) using the Seldinger technique. Then, intra-arterial injection of an iodine contrast agent (ICA) was administered while cranial radiographs were taken at regular time intervals (usually two per second for intra-cranial aneurysms). DSA remains the

gold standard for imaging aneurysms since spatial and time resolutions are excellent. As a result, we were able to obtain precise images of circulating vessels and important dynamic information. However, DSA does not explore non-circulating elements, i.e. the thrombosed section, the wall and the surrounding brain parenchyma. To assess the size and morphology of the circulating portion, we used plain 2D radiographs and 3D rotational angiography, which is not always useful in the case of major flow disturbances within a large circulating portion. Fanning et al. [5] described sinusoidal angiographic appearance as the Pretzel sign in serpentine aneurysms (Fig. 1b). To understand the quality of vascularisation of the aneurysm, we used 2D angiographic series searching for: • dynamic study of the filling of arteries located after the aneurysm; • presence of collateral arterial network in distal territory. Therefore, it is important to selectively catheterise the common carotid and vertebral arteries one after the other, and sometimes also to catheterise internal and external carotid arteries. In cases of very slow flow within the aneurysm, recruitment of pial collaterals from nearby distal cerebral arteries is possible, as well as the development of trans-dural anastomosis between meningeal arteries and distal pial branches (Fig. 2f). Balloon test occlusion (BTO) of the parent artery may also be performed, entailing occlusion of the parent artery of the aneurysm while injecting the other axis, to evaluate the efficient collaterals and confirm if the parent artery is occluded. A BTO is considered positive when collateral arteries vascularise the occluded territory with less than one second delay on the venous phase, compared to the side of the injected artery. 3.2. CT scan 3.2.1. Non-enhanced CT (NECT) scans The first examination for any neurological symptom is most often a NECT scan of the brain. It is of paramount importance to be able to differentiate between a vascular and non-vascular lesion, especially when presenting with mass effect, due to surrounding oedema (hypodensity), which may lead to a misdiagnosis of the neoplasm ([6–9]). The giant intracranial aneurysm is a wellcircumscribed lesion with heterogeneous density: • high density for the acute thrombosed section; • lower density for the circulating channel; • low density for the chronic thrombosed section. There may also be a peripheral rim of calcification (high density), indicating the chronic nature of the lesion [1,6,8]. A NECT scan can also be used to evaluate the degree of mass effect (midline shift, loss of cortical sulcus and basal cisterna) and the presence of acute hydrocephalus (enlargement of ventricles, transependymal resorption), which can both lead to severe intracranial hypertension requiring emergency treatment (Fig. 3a, b). Bone filter reconstruction, enables analysis of skull base deformation, which occurs primarily in giant carotid aneurysms. In emergency cases, a ruptured aneurysm can be diagnosed with hyperdensity related to blood collection either in the subarachnoid space (subarachnoid haemorrhage) or within the brain parenchyma (intra-cerebral haematoma). 3.2.2. Post contrast CT (PCCT) scan The PCCT scan is a brain scan performed a few minutes after injection of ICA, which infiltrates the brain parenchymal structures,

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Fig. 1. Seventy-seven-year-old woman with fast cognitive impairment revealing a giant serpentine aneurysm of the right middle cerebral artery (MCA). Frontal digital subtraction angiography (DSA) permitted a dynamic study of the flow within aneurysm with arterial time (a), parenchymal time (b) and venous time (c). The parent artery (arrow) and the slow circulating channel (large arrow) within the thrombosed part were clearly identifiable, forming the pretzel sign. During MRI examination, 3D TOF (d) and 3D T1 post-gadolinium (e) sequences were performed and reconstructed using a volume rendering technique. MCA (arrow) was visible on both, but the circulating channel within the thrombosed part was barely visible on 3D TOF, which usually depicts arterial flow. Enhanced analysis of the circulating channel was achieved after an injection of gadolinium (large arrow). Femme de 77 ans avec rapide détérioration cognitive révélant un anévrisme serpentin géant de l’artère cérébrale moyenne droite. L’angiographie de face a permis une étude dynamique du flux dans l’anévrisme au temps artériel (a), parenchymateux (b) et veineux (c). L’artère porteuse (flèche) et le flux ralenti dans le chenal circulant (flèche large) à l’intérieur de la partie thrombosée sont clairement identifiés, formant le signe du bretzel. Au cours de l’IRM, le 3D TOF (d) et le 3D T1 après gadolinium (e) ont été acquis et reconstruits selon la technique du rendu de volume. L’artère cérébrale moyenne était visible sur les deux (flèche), mais le chenal circulant au sein de la partie thrombosée était faiblement visible sur le 3D TOF, qui visualise surtout les flux artériels. Une meilleure analyse du chenal circulant était réalisée après injection de gadolinium (flèche large).

filling all vascular structures (arterial and venous). It must be differentiated from a CTA (technique described below), which explores intra-cranial arteries. A PCCT scan is usually performed to analyse non-vascular brain lesions, however giant aneurysms may present radiologically and clinically as tumours. A PCCT scan provides a bright enhancement of the circulating channel with a higher density than the acute thrombosed section. Although the thrombus is not enhanced, there is a peripheral enhancement of the aneurysm due to inflammation in the wall of the aneurysm.

The result is a target sign described by Kricheff as central hyperdensity of the circulating channel, intermediate hypodensity of the thrombus and peripheral hyperdensity of the wall [10]. 3.2.3. CTA CTA acquisition is performed after a bolus injection of ICA with bolus tracking to avoid venous infusion. CTA explores intracranial arteries with a very good spatial resolution, allowing multiplanar reconstructions (MPR) and different post treatment techniques,

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Fig. 2. Male patient, aged 20 years, with chronic headaches revealing a giant serpentine aneurysm of the right middle cerebral artery. Frontal digital subtraction angiography (DSA) views of the right common carotid injection (a, b, c), showing slow filling of the aneurysm with opacification of the sylvian branches (arrow heads) after the external carotid territories (large arrow on the superficial temporal artery) and the right posterior cerebral artery territory (dotted arrow) infused by a patent right posterior communicating artery. Frontal views of a selective right external carotid injection (d, e, f), showing increased meningeal vascularisation (small arrows), which could contribute to transdural anastomosis with the underlying right middle cerebral artery territory. Homme de 20 ans, présentant des céphalées chroniques amenant à la découverte d’un anévrisme géant serpentin de l’artère cérébrale moyenne droite. Angiographie : vue frontale de l’artère carotide commune droite (a, b, c) montrant un remplissage lent de l’anévrisme avec opacification des branches de l’artère sylvienne (têtes de flèche) après les branches de la carotide externe (artère temporale superficielle, flèche large) et de l’artère cérébrale postérieure droite (flèche en pointillés) alimentée par l’artère communicante postérieure. Vue frontale après injection sélective de l’artère carotide externe droite (d, e, f) montrant une majoration de la vascularisation méningée (petites flèches) qui contribue au développement d’anastomoses transdurales avec le territoire sous-jacent de l’artère cérébrale moyenne droite.

such as maximum intensity projection and, volume rendering, which result in angiographic views. The role of CTA is to analyze the circulating channel of the giant aneurysm. When the flow is homogeneous and fast (arterial time), complete filling of the circulating channel is obtained, then size and relationship with the parent artery and nearby branches can be analysed clearly. When the circulating channel is wide and with flow disturbances, there may be only partial filling and a consequent difficulty in assessing its size and the arteries involved. 3.3. MRI Over the past 20 years, MRI has greatly improved the meaning of giant aneurysm and the evaluation of its parenchymal complications [1,6,9,11–13]. 3.3.1. Aneurysm and its vessels On T1 and T2 spin echo weighted images (including FLAIR sequences), high flow circulating vessels are black (no signal)

due to the flow void effect: high velocity protons, as in arteries or large veins, have a low transit time, leave the imaging plane before receiving the signal and are replaced by nonexcited protons. The thrombosed part of the aneurysm is heterogeneous, a combination of hypointense and hyperintense, because of signal differences in time evolution of blood products (Table 1). On T2* (gradient echo) images, which are very sensitive to magnetic susceptibility artefacts, blood product as well as calcifications appear as a strong hypointensity the size of which is overestimated (for instance: a small amount of blood will look much larger than it actually is) because of the artefacts. To evaluate circulating channel and the nearby vessels, two techniques can be used: • a flow depiction technique (3D time of flight [TOF] sequence); • a filling depiction technique (post contrast 3D T1 weighted sequence).

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Fig. 3. Same patient as in Fig. 1. Axial head NECT scan (a, b) showing an important, heterogenous, right temporal lesion, with arcuate calcifications (arrow head), surrounding edema (large arrow) and responsible for midline shift (dotted arrow). The MRI exam with axial FLAIR (c) and 3D T1 post-gadolinium (d) sequences allows a better visualization of this giant serpentine aneurysm of the middle cerebral artery with a small circulating portion (stars) inside a large round thrombosed part. There is surrounding edema (large arrow) clearly visible on the axial FLAIR and a peripheral enhancement (arrow) after gadolinium injection. Même patiente qu’à la Fig. 1. Les coupes axiales du scanner cérébral sans injection (a, b) montrent une importante lésion temporale droite, hétérogène, avec des calcifications arciformes (tête de flèche), de l’œdème périlésionnel (flèche large) et un engagement sous-falcoriel (flèche en pointillés). L’IRM en axial FLAIR (c) et en 3D T1 après injection de gadolinium permet de mieux visualiser cet anévrisme serpentin géant de l’artère cérébrale moyenne droite, avec une petite portion circulante (étoiles) au sein d’une large partie thrombosée. Il existe un œdème périlésionnel (large flèche) bien visible en FLAIR et un rehaussement périphérique (flèche) après injection de gadolinium.

The 3D TOF sequence is usually set as an arterial flow sequence: slow flow, i.e. venous circulation, is saturated so as not to interfere with analysing the arterial network. This is a widespread and very interesting sequence for visualising intra-cranial arteries and characterising aneurysms. The problem with giant aneurysms is that its flow is very often heterogeneous in a wide circulating channel. Therefore, the blood flow within and downstream from the aneurysm is often slower than regular arterial flow and this sequence can underestimate the circulating portion as well as miss

some arterial efferent branches (Fig. 1d). Although it can be a drawback for morphological characterisation it can at the same time provide interesting functional information: if the branches located downstream of the aneurysm are not visible and there is no sign of brain ischaemia, that might be an indication of possible collateral artery development. The post contrast 3D T1 weighted sequence will show all intracranial vascular structures because the gadolinium contrast product fills arteries and veins (Fig. 1e). Therefore, it provides

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Table 1 Magnetic resonance different signals of blood products of varying age. Signal du sang en IRM en fonction du temps. Time

T1 weighted images

T2 weighted images

T2* weighted images

Intra cellular Oxy Hb

< 6 hours

Iso or hypo intense

Hyper intense

Strongly hypo intense

Intra cellular Deoxy Hb

6–36 hours

Iso or hypo intense

Hyper intense

Strongly hypo intense

Intra cellular Met Hb

3–7 days

Hyper intense

Hyper intense

Strongly hypo intense

Extra cellular Met Hb

1–4 weeks

Hyper intense

Hyper intense

Strongly hypo intense

Hemosiderin

> 1 month

Iso or hypo intense

Hyper intense

Strongly hypo intense

Osborn AG. Diagnostic Imaging: Brain, Amirsys – Elsevier Sanders, 2004.

Fig. 4. Male patient, aged 59 years, presenting with progressive right hemiparesia and diplopia, revealing an almost completely thrombosed giant termino-basilar aneurysm. Two MRI examinations were performed: at diagnosis (a, b, c) and 3 months after embolization of the small circulating portion (d, e, f). On the first axial FLAIR images (a, b, c), the hyperintense edema surrounding the hypointense aneurysm had almost completely disappeared at follow-up examination (d, e, f) whereas the aneurysmal sac remained the same. The disappearance of the vasogenic edema, associated with clinical improvement, is probably secondary to the anti-inflammatory effect of embolization. Homme de 59 ans présentant une hémi-parésie droite et une diplopie progressive révélant un anévrysme géant de la terminaison du tronc basilaire presque totalement thrombosé. Deux IRM ont été réalisées : au cours du diagnostic (a, b, c) et trois mois après l’embolisation du chenal circulant (d, e, f). Sur les premières coupes axiales FLAIR (a, b, c), l’anévrisme en hyposignal est entouré d’un œdème en hypersignal, qui, sur les coupes en post-embolisation (d, e, f), va avoir quasiment disparu alors que le sac anévrismal reste inchangé. Cette disparition s’est accompagnée d’une amélioration clinique et était probablement secondaire à l’effet anti-inflammatoire de l’embolisation.

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Figure 5. Sixteen-year-old girl with progressive loss of right visual acuity and recent episodes of headaches. A cerebral MR exam was performed and diagnosed a right giant carotido-ophtalmic aneurysm. These coronal T2 Fat Sat weighted images show the circulating aneurysmal sac (star) without edema of the surrounding brain parenchyma but a mass effect that medially shift the optic chiasma and the right optic nerve (arrow) which explains the optic nerve atrophy (large arrow). Jeune femme de 16 ans ayant une baisse progressive de l’acuité visuelle et des céphalées récentes. L’IRM cérébrale a diagnostiqué un anévrisme géant carotido-ophtalmique droit. La séquence coronale T2 Fat Sat montre le sac anévrismal circulant (étoile) sans œdème du parenchyme cérébral adjacent mais avec un effet de masse sur le nerf optique droit (flèche) et le chiama optique refoulés vers la gauche, ce qui explique l’atrophie du nerf optique (flèche large).

reliable information about the size of the circulating portion and patency of collateral branches. It also depicts peripheral enhancement of the aneurysm (Fig. 3d). 3.3.2. The brain parenchyma The oedema surrounding the aneurysm will appear as hypointense on T1 weighted images and hyperintense on T2 weighted images (including FLAIR sequence). It is a vasogenic oedema mainly involving the white matter and not corresponding to vascular territory (Fig. 3a, c). It is difficult to differentiate between what is due to mass effect or to inflammation, especially because both components exist in giant aneurysms (Fig. 4). Sometimes the oedema is visible in the cortical and sub cortical areas, or in the vascular territory downstream from the aneurysm. It is also hypointense on T1 weighted images and hyperintense on T2 weighted images (including FLAIR sequence) but is more likely a cytotoxic oedema due to ischaemia (low flow, embolic, etc.). During the 10-day acute phase, diffusion weighted images make the difference because a cytotoxic oedema appears with restricted diffusion whereas vasogenic oedema has increased diffusion. In the chronic phase, locating the defined vascular territory will make the difference. After a haemorrhage, blood products within subarachnoid spaces will appear hyperintense on FLAIR sequence (and sometimes hypointense on T2 * sequence, when the clot is thick). If the haematoma is located within the brain parenchyma, it will be heterogeneous on T1 and T2 sequences and strongly hypointense on T2* sequences. The intensity of the haematoma varies with time (Table 1). MRI is also the best technique for visualizing cranial nerve lesions due to the mass effect of giant aneurysms. It can show compression and also sometimes atrophy of the nerve (Fig. 5). 4. Conclusion Giant aneurysms have a complex pathology with multiple stages of evolution and consequences. Therefore, complex imaging is mandatory for better understanding of these parameters and to plan an often complicated treatment strategy. DSA remains the gold standard for analyzing aneurysms, but sectional imaging (CT, MRI) also provides essential information in the specific case of giant

aneurysms. As imaging modalities are improving very quickly, in the future new sequences, such as brain perfusion or functional imaging, may be added to routine examination of patients. To date, imaging modalities remain relatively undocumented regarding giant aneurysms. Disclosure of interest The authors declare that they have no conflicts of interest concerning this article. Acknowledgement The authors are grateful to Nikki Sabourin-Gibbs, from Rouen University Hospital, for reviewing the manuscript in English. References [1] Türe U, Elmaci I, Ekinci G, Pamir MN. Totally thrombosed giant P2 aneurysm: a case report and review of literature. J Clin Neurosci 2003;10(1):115–20. [2] Hacein-Bey L, Provenzale JM. Current imaging assessment and treatment of intracranial aneurysms. AJR 2011;196(1):32–44. [3] Van Rooij WJ, Sluzewski M, Beute GN. Endovascular treatment of giant serpentine aneurysms. AJNR 2008;29:1418–9. [4] Hacein-Bey L, Connolly Jr ES, Mayer SA, Young WL, Pile-Spellman J, Solomon RA. Complex intracranial aneurysms: combined operative and endovascular approaches. Neurosurgery 1998;43:1304–13. [5] Fanning NF, Kelleher MO, Ryder DQ. The Pretzel sign: angiographic pattern of tortuous intra-aneurysmal blood flow in giant serpentine aneurysm. Br J Neurosurg 2003;17:67–71. [6] Christiano LD, Gupta G, Prestigiacomo CJ, Gandhi CD. Giant serpentine aneurysms. Neurosurg Focus 2009;26(5):E5. [7] Patel DV, Sherman IC, Hemmati M, Ferguson RJ. Giant serpentine intracranial aneurysm. Surg Neurol 1981;16:402–7. [8] Mawad ME, Klucznik RP. Giant serpentine aneurysms: radiographic features and endovascular treatment. AJNR 1995;16:1053–60. [9] Belec L, Cesaro P, Brugieres P, Gray F. Tumor-simulating giant cerebral aneurysm of the posterior cerebral artery. Surg Neurol 1988;29:210–5. [10] Kricheff II. Intracranial aneurysms and arteriovenous malformations. Chicago: In Refresher Course 408, 64th Scientific Assembly and Annual Meeting of the RSNA; 1978. [11] Aletich VA, Debrun GM, Monsein LH, Nauta HJ, Spetzler RF. Giant serpentine aneurysms: a review and presentation of five cases. AJNR 1995;16:1061–72. [12] Coley SC, Hodgson TJ, Jabukowski J. Coil embolization of giant serpentine aneurysms: report of two cases arising from the posterior cerebral artery. Br J Neurosurg 2002;16:43–7. [13] Sari A, Kandemir S, Kuzeyli K, Dine H. Giant serpentine aneurysm with acute spontaneous complete thrombosis. AJNR 2006;27:766–8.

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Imaging of giant cerebral aneurysms.

The aim of this study was to review the different imaging techniques for analysing giant intracranial aneurysms (digital subtraction angiography [DSA]...
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