G

E

D

VKa

b

a

ARA

KACMH

1

mbdswwgeasmcomfe

DG

0h

ARTICLE IN PRESS Model

URR-6135; No. of Pages 10

European Journal of Radiology xxx (2012) xxx– xxx

Contents lists available at SciVerse ScienceDirect

European Journal of Radiology

jo ur n al hom epage: www.elsev ier .com/ locate /e j rad

iagnostic approach to cerebral aneurysms

itor Mendes Pereiraa, Philippe Bijlengab, Ana Marcosa, Karl Schallerb,arl-Olof Lovblada,∗

Division of Diagnostic and Interventional Neuroradiology, Geneva University Hospitals, SwitzerlandDepartment of Neurosurgery, Geneva University Hospitals, Switzerland

r t i c l e i n f o

rticle history:eceived 8 October 2012ccepted 25 October 2012

eywords:neurysmomputed tomographyagnetic resonance imagingemorrhage

a b s t r a c t

Cerebral aneurysms are an important cause of morbidity and mortality due to their causal effect innon-traumatic subarachnoid hemorrhage. Neurosurgical progress in the 20th century helped to improvepatient outcomes greatly. In recent years, techniques such as intravascular treatment by coiling and/orstenting have found an additional place in the management of the disease. With the development of lessand less invasive surgical and endovascular techniques, there has also been a continuous development inimaging techniques that have led to our current situation where we dispose of CT and MR techniques thatcan help improve treatment planning greatly. CT is able to detect and together with its adjunct techniquesCT angiography and CT perfusion, it can allow us to provide the physicians in charge with a detailed image

of the aneurysm, the feeding vessels as well as the status of blood flow to the brain. Angiography hasevolved by becoming the standard tool for guidance during decision making for whatever therapy isbeing envisioned be it endovascular procedures and or surgery and has even progressed more recentlydue to the development of so-called flat panel technology that now allows to acquire CT-like imagesduring and directly after an intervention. Thus nowadays, the diagnostic and interventional techniquesand procedures have become so much entwined as to be considered a whole.

. Introduction

Subarachnoid hemorrhage (SAH) is a well-known cause of highortality and morbidity. As a clinical entity SAH is considered to

e one of the many possible types of stroke or cerebrovasculariseases. Until recent advances in interventional neuroradiology, atrict neurosurgical approach with operation, and mainly clippingas the accepted approach [1]. Initially the approach to aneurysmsas cautious due to its high mortality, but after having known

reat strides in the improvement of surgical techniques, it wasstablished that early operation will prevent re-bleeding, and thusneurysm treatment has become an emergency situation [2]. Whileurgery is the approach which has historically defined the manage-ent since one could evacuate blood and exclude the aneurysm by

lipping, progress in interventional neuroradiology with the devel-pment of coiling and stenting techniques have provided us with

Please cite this article in press as: Pereira VM, et al. Diagnohttp://dx.doi.org/10.1016/j.ejrad.2012.10.014

ore choices for treatment. In most centers, there is a tendencyor the management of aneurysms to become a multidisciplinaryffort that will involve many specialists from the field of clinical

∗ Corresponding author at: Service Neurodiagnostique et Neuro-interventionnelISIM, Hopitaux Universitaires de Genève, 4 rue Gabrielle-Perret-Gentil, 1211eneva, Switzerland. Tel.: +41 22 372 70 33; fax: +41 22 372 70 72.

E-mail address: Karl-olof.lovblad@hcuge.ch (K.-O. Lovblad).

720-048X/$ – see front matter © 2012 Elsevier Ireland Ltd. All rights reserved.ttp://dx.doi.org/10.1016/j.ejrad.2012.10.014

© 2012 Elsevier Ireland Ltd. All rights reserved.

neuroscience beside neurosurgeons such as neuroradiologists(both diagnostic and interventional), neuroanesthesiologists, neu-rointensivists and even neurologists. While the initial bleed willhave an important devastating effect with between 10 and 20%dying initially, the remainder of the patients can benefit fromsurgery or interventional neuroradiology, which will obliterate theaneurysm and evacuate blood.

Globally, it can be considered that 90% of aneurysms are locatedon the anterior circulation and 10% in the posterior cerebral circula-tion. Originally a diagnosis of an aneurysm could be made clinicallyupon rupture due to the typical signs of thunderclap headacheaccompanied by neck stiffness and neurological signs, all of whichwould be confirmed with a lumbar puncture; in a few select casesthe aneurysm would cause deficits by pressing on a cranial nervedirectly (mostly in cases of giant aneurysms).

The initial examination of choice for aneurysms in the acutestage is at the moment clearly still computed tomography (CT).Indeed, its capacity to clearly define newly extravasated blood isstill unchallenged by magnetic resonance imaging. Over the lastdecade, additional CT-based methods such as CT angiography (CTA)and CT perfusion have evolved enough so that they can provide

stic approach to cerebral aneurysms. Eur J Radiol (2012),

results that can be reliably used in the clinical setting. The refer-ral for a suspicion of cerebral aneurysm can be extremely variedbecause while many patients arrive acutely with signs of acuteheadache and deterioration, some will arrive with an “incidental”

ARTICLE IN PRESSG Model

EURR-6135; No. of Pages 10

2 V.M. Pereira et al. / European Journal of Radiology xxx (2012) xxx– xxx

F CT whr

diattabroi

1

sitailbefottcoaisc7snweaa

ig. 1. Patient with typical “warning leak”. He presented with headaches, went to

ight MCA (D). On angio-CT an aneurysm was demonstrated (E)–(F).

iscovery of an aneurysm having usually occurred during imag-ng (CT or MRI) for headache or something completely differentt times. Also, one population that is very important to identify ishat of patients who will have suffered a so-called warning leak:hese hemorrhages are known to have occurred in between 20nd 35% of patients [3,4]; if correctly identified, the patients couldenefit from CT and CTA in order to identify a not yet completelyuptured aneurysm that could be treated quickly (Fig. 1). The aimf this paper is to discuss the state-of-the-art diagnostic workuprrespective of the treatment modality chosen.

.1. Computed tomography

Blood at least in the early stage is seen as a hyperdensity (i.e. atructure more “white” than the adjacent brain parenchyma) ands very easily detected with CT. The most common case of SAH israumatic (85%), but most cases of non-traumatic SAH are due toneurysms. In the situation of traumatic SAH very often, a traumas known, but in some cases it must be suspected if the blood isocated in locations less typical for aneurysms (e.g. subarachnoidlood on the convexity of the brain) or if radiologically there arevident signs of an external traumatic event. CT is also the pre-erred method for imaging whenever a trauma to the head is knownr suspected. However in 15–20% of cases of non traumatic SAHhere is no aneurysm to be found and 2/3 of these cases are dueo peri-mesencephalic SAH. Peri-mesencencephalic SAH, which isharacterized by the presence of blood in the basal cisterns in frontf the mesencephalon mainly is usually not of aneurysmatic originnd has a good prognosis (Fig. 2). Cerebral angiography after thenitial clinical event was the technique that would allow to demon-trate or exclude a cause of the symptoms. All of this was drasticallyhanged when computed tomography (CT) appeared in the early0’s and one could see the contents of the skull and its differenttructures; one was thus able to directly visualize the subarach-oid blood. Initially, even with CT displaying blood, angiography

Please cite this article in press as: Pereira VM, et al. Diagnohttp://dx.doi.org/10.1016/j.ejrad.2012.10.014

as necessary until only just a decade ago; indeed, CT has evolvednormously since its development: it is no longer simply used as

tool to rule out hemorrhage, but can in itself be used for verydvanced imaging and pre-therapeutic purposes.

ich failed to show any clear SAH. However there was a suspicious dilatation of the

Blood accumulation on the scanner is graded according to theFisher classification [5] with a grade 1 being no blood visible and agrade 4 with diffuse or no subarachnoid blood but intraventricularor intraparenchymal clot (Figs. 3–5).

Very rarely a calcified aneurysm can be seen on the conventionalX-ray image (Fig. 6) as a calcified crescent: this is nowadays muchbetter seen on the CT and CTA images.

In a study using multi-slice CTA, Wintermark et al. founda sensitivity of 94.8%; this study was done in the early stagesof multi-slice imaging: i.e. with scanners with 8 and 16 detec-tor rows; with subsequent actual advances the number of rowsallowing simultaneous acquisition has increased even more [6,7].CTA was also found to be sufficient to exclude aneurysms inpatients with subarachnoid hemorrhage in cases with patternsof peri-mesencephalic SAH with a sensitivity of 96.4%. It stillremains important to go though and look at all axial slices (Fig. 7),before using the reconstructions. While reconstructions using moresophisticated software packages will often enhance the anatomicdetail (Figs. 8–13), very often simple maximum intensity projection(MIP) type reconstructions will be very useful in a first evaluation.

CTA is even believed to be able to exclude SAH with more than99% in a recent publication [8].

Perfusion CT: even though CT perfusion techniques had beenaround for quite some time [9], they were also only implementedclinically recently due to advances in multi-slice techniques. XenonCT had initially been done but this technique had not found a vastacceptance [9]. CT perfusion protocols have been used with greatsuccess in the diagnosis and management of acute stroke. In thecase of patients with aneurysms, it has been restricted mostly to thestudy of vasospasm or more rarely ischemia that may occur aftervessel occlusion (Fig. 13). Vasospasm, which usually occurs duringthe two weeks after SAH, if severe enough may cause ischemia andthe so-called delayed neurological deficits that may even cause sig-nificant morbidity progress to death. Sanelli et al. found the use ofCBF and MTT to bring the most useful information [10]

stic approach to cerebral aneurysms. Eur J Radiol (2012),

When using all these CT techniques together, conventional CT,CTA and CTP the idea is to maximally orient the clinician by demon-strating, hemorrhage, eventual tissular damage as well as preparefor intervention by providing maximum resolution imaging in 3 D

ARTICLE IN PRESSG Model

EURR-6135; No. of Pages 10

V.M. Pereira et al. / European Journal of Radiology xxx (2012) xxx– xxx 3

F o aneh

(omu

ogb

1

n

ig. 2. Patient with perimesencephalic blood on the CT (A). On subsequent MRA nemorrhage.

Fig. 14). CTP will usually not be performed in the initial evaluationf the patient with a suspicion of SAH and aneurysm but will beore used in the follow-up period after treatment has been done

sually.For follow-up studies however, whenever a metallic device (coil

r clip) has been implanted, beam hardening artifacts appear thatreatly diminish the visibility of the vessel and the surroundingrain structures.

Please cite this article in press as: Pereira VM, et al. Diagnohttp://dx.doi.org/10.1016/j.ejrad.2012.10.014

.2. Conventional angiography

While cerebral angiography remains the gold standard exami-ation and is still the one that is preformed in most cases where

Fig. 3. Fisher 2 grade SAH: subarachnoid blood can be seen

urysm can be seen (B). This was a typical case of perimesencephalic subarachnoid

an intervention is being planned, in the acute setting at least fordiagnostic purposes it has been replaced by the CT scanner. In aprospective series, Willinsky et al. found a rate of 1.3% of neurologiccomplications due to cerebral angiography [11] but have been aslow as 0.34% in the series of Dawkins [12] in a more selected series ofpatients. This low occurrence has been reproduced for high-volumeacademic centers [13]. Despite developments in technology, whenconfronted with SAH that may be due to an aneurysm, based onabsence of trauma or location, angiography is still advised because

stic approach to cerebral aneurysms. Eur J Radiol (2012),

remaining superior to both CTA and MRA [14].After treatment however, CT and or MRA can be done to assess

vessel patency and aneurysms occlusion [15–17]. Angiography alsoremains the technique of choice to really demonstrate the presence

as thin hyperdense layer in the right sylvian fissure.

ARTICLE IN PRESSG Model

EURR-6135; No. of Pages 10

4 V.M. Pereira et al. / European Journal of Radiology xxx (2012) xxx– xxx

F mora

osco

tgCdtatte

Ft

ig. 4. SAH Fisher grade 3: diffuse blood in the basal cisterns. The blood is locatedneurysm (B).

f vasospasm that occurs a few days after SAH in cases of moreevere bleeding. Again, once the catheter is in situ the physician mayhoose to either perform mechanical dilatation or to give some kindf intra-arterial vasodilator drug (papaverine, nimodipine,etc).

However, the development of flat panel technology has allowedhese angiography units to develop axial imaging capabilities thato well beyond angiography with now CT angiography as well asT perfusion images being possible to acquire in addition to simpleiagnostic images [18–21]. Indeed this will allow the interven-ional neuroradiologist to not just assess the presence of blood but

Please cite this article in press as: Pereira VM, et al. Diagnohttp://dx.doi.org/10.1016/j.ejrad.2012.10.014

lso to determine if any significant changes have occurred sincehe CT done usually just prior to intervention (Fig. 15). In additiono providing these yet slightly low quality CT images but that arenormously helpful, flat panel techniques also allow to perform

ig. 5. Patient with an anterior cerebral artery aneurysm having caused diffuse SAH, therhe left (A). This corresponds to a Fisher grade 4. The aneurysm is demonstrated on the C

e in the right basal cistern (A). CT angiography reveals a small right-sided carotid

ultra-high resolution images of the vessels with the device in situ(Figs. 16–18)

1.3. Magnetic resonance imaging

Magnetic resonance imaging mostly has a role in the follow-upof aneurysms after treatment. While sequences such as diffusionand perfusion imaging can be of great help in order to detect lesionsthat may are established, MRI still remains slightly more difficultto assess regarding the presence of acute bleeding, especially in

stic approach to cerebral aneurysms. Eur J Radiol (2012),

the subarachnoid regions. Indeed, the presence of pulsation arti-facts sometimes renders the exact evaluation of sequences such asFLAIR difficult to the novice. In the early stages MRI was problem-atic due to the fact that the patient could initially not (or not well

e is also blood in the ventricles as well as in the parenchyma of the frontal lobe onTA (B).

ARTICLE IN PRESSG Model

EURR-6135; No. of Pages 10

V.M. Pereira et al. / European Journal of Radiology xxx (2012) xxx– xxx 5

Fig. 6. Patient with calcified aneurysm. This can be identified on the skull X ray as a crescent of calcification (arrow). On unenhanced CT the ring-like calcification at the endof the left carotid is well seen and CTA shows the filling of the structure corresponding to the aneurysm.

s (A). T

esats

Fig. 7. Carotid aneurysm, on the right side, oriented inward

nough) be monitored and had to remain very calm inside the MR

Please cite this article in press as: Pereira VM, et al. Diagnohttp://dx.doi.org/10.1016/j.ejrad.2012.10.014

canner; then, with the development of faster scanning methodsnd more and more MRI compatible hardware (clips, coils, moni-oring equipment), the technique has become feasible even in lesstable patients.

Fig. 8. MCA bifurcation aneurysm with sagittal MIP

his is seen better in the coronal MIP projection (arrow) (B).

Indeed while FLAIR can sometimes demonstrate hyperinten-

stic approach to cerebral aneurysms. Eur J Radiol (2012),

sities in the sulci that corresponds to blood, it may be difficultto distinguish from other phenomena such as CSF pulsations[22] Mohamed found few true positive cases in a limited series[23], however FLAIR was infrequently positive when CT showed

(A) and volume rendering reconstructions (B).

ARTICLE IN PRESSG Model

EURR-6135; No. of Pages 10

6 V.M. Pereira et al. / European Journal of Radiology xxx (2012) xxx– xxx

Fig. 9. Carotid aneurysm seen both in the coronal MIP CTA reconstruction (A) as well as on the contrast-enhanced MR angiography (B).

n the a

nasiatw

tlo

pbb

Fig. 10. A Com aneurysm of the anterior communicating artery, seen o

othing [24]. Also, while from a theoretical point of view, MRI using combination of T2*, FLAIR and T2 techniques should be clearlyuperior to CT, very often most radiologists feel more at easy tonterpret blood still using CT. Regarding chronic deposits of sub-rachnoid blood for example in the sulci, MRI, especially using T2*echniques or even better susceptibility-weighted imaging (SWI)ill better demonstrate these areas of cortical signal drop.

As with most intracerebral lesions and structures, “conven-ional” MRI sequences will be most suited to demonstrate the finalesion that will explain the eventual neurological or neuropsychol-gical deficit in a given patient [25].

Magnetic resonance angiography has at least from a theoretical

Please cite this article in press as: Pereira VM, et al. Diagnohttp://dx.doi.org/10.1016/j.ejrad.2012.10.014

erspective the advantage of being able to produce images of therain vasculature [26] without the use of contrast material: this cane done either with the time-of-flight technique or phase contrast

Fig. 11. Basilar artery aneurysm demonstrated in bo

xial image (A) but much better seen on the coronal reconstruction (B).

technique. Usually, TOF techniques are more commonly used eventhough they are very susceptible to flow direction.

For the follow-up of patients with aneurysms, the use ofMRA based on time-of-flight techniques has become the standardapproach. Indeed, while initial worries regarding the use of the highmagnetic fields with either clips or coils or even stents have provenunfounded, at least with current generations of devices that are pro-duced to be MR compatible [27]; however improvements have beenmade with the continuous development of contrast – enhanced MRangiography methods: Pierot found that while contrast-enhancedMRA could better depict aneurysm remnant after treatment, coilvisibility itself was better on TOF type images [28]. Stented arteries

stic approach to cerebral aneurysms. Eur J Radiol (2012),

can also be visualized both with CTA and MRA techniques [19,29]Again as with CT perfusion, techniques using diffusion and per-

fusion MR have been proven of interest in cases with aneurysmal

th sagittal (A) and coronal MIP projections (B).

ARTICLE IN PRESSG Model

EURR-6135; No. of Pages 10

V.M. Pereira et al. / European Journal of Radiology xxx (2012) xxx– xxx 7

atom

Stawbat

Fig. 12. Left sided MCA aneurysm with small intraparenchymal hem

AH. Sometimes, the use of diffusion will reveal a small lesion dueo ischemia [30]; perfusion techniques, like those we know from CTre not as easy to use because while MR perfusion does cover the

Please cite this article in press as: Pereira VM, et al. Diagnohttp://dx.doi.org/10.1016/j.ejrad.2012.10.014

hole brain, the changes found in early stages of vasospasm maye easily missed; in later stages one will again find the presence oflterations in blood flow parameters in the region vascularized byhe spastic vessel.

Fig. 13. Patient with SAH and vasospasm: CT perfusion shows alterations in

a (A, B) with an aneurysm being seen on the CT angiograms (C, D).

2. Discussion

Cerebral aneurysms are a treatable cause of severe disabil-

stic approach to cerebral aneurysms. Eur J Radiol (2012),

ity; this has been made possible due to parallel advances overmany decades in both diagnostic (imaging) and in therapeu-tic modalities. While it is still associated with high rates ofinitial mortality, treatment options have evolved from simple

the right MCA territory whereas angio-CT shows vessel irregularities.

ARTICLE IN PRESSG Model

EURR-6135; No. of Pages 10

8 V.M. Pereira et al. / European Journal of Radiology xxx (2012) xxx– xxx

Fig. 14. CT showing SAH, more widely distributed on the left. Angiography demonstrated a left-sided posterior communicating artery aneurysm which was subsequentlycoiled. DSA shows the lateral projection before and after coiling. Also antero-posterior skull view showing the coil in situ.

stctitii

Ft

urgery (originally carotid ligation) to more advanced clippingechniques using microneurosurgery to now encompass endovas-ular methods such as coiling and even stenting. Very often all ofhese techniques are used in combination and not alone. Imag-ng of aneurysms rests to a great extent on the use of computed

Please cite this article in press as: Pereira VM, et al. Diagnohttp://dx.doi.org/10.1016/j.ejrad.2012.10.014

omography for diagnosis and angiography for confirmation ornformation that may lead to a procedure. Angiography, whichs the gold standard reference method for the demonstration

ig. 15. CT images reconstructed from rotation images acquired on the angiographyable.

of an aneurysmal change, is today more and more used as anadvanced planning tool in order to prepare for what may mostlyturn out to be an endovascular approach. This, together with thedevelopment of so-called flat panel detector techniques has ush-ered in a real period of multi-modal imaging with axial imagingbeing performed at the same time. Also this allows combinedapproaches to be developed in cases where surgery as well asendovascular navigation is necessary: in addition to being to fullycombined techniques, it is possible to use one technique to com-plement the other in case of need. MR technology is also nowcoming of age so that it can be incorporated into this patientoriented approach and where the physicians can benefit fromthe increased insight into not just pathology and anatomy butinto pathophysiology in order to improve and predict patientoutcomes.

For follow-up purposes, MR techniques are becoming themethod of choice: on the one hand the do not subject the patient toadditional radiation and on the other hand they can better demon-strate the post-therapeutic vessel: by using contrast-enhancedtime-of-flight MRA techniques, it is possible to obtain at 1.5 T and3.0 T images of the vessel adjacent to the coiled vessel that willallow to continue follow-up with this technique. If on follow-upexaminations there is a suspicion of aneurysm re-growth, one maythen decide to proceed at first to angiography in order to decidewhether to re-treat.

Also MRI can better the presence of small ischemic changesthat may have been induced by the bleeding itself, the opera-tion/intervention or even vasospasm. Also when one considerspatients having been treated either with coils or clips, MRI, while

stic approach to cerebral aneurysms. Eur J Radiol (2012),

having central signal drops at the location of the device, is stillbetter tan CT where very often very impressive “stellate” beam-hardening artifacts sometimes render image interpretation difficultif not impossible.

Please cite this article in press as: Pereira VM, et al. Diagnostic approach to cerebral aneurysms. Eur J Radiol (2012),http://dx.doi.org/10.1016/j.ejrad.2012.10.014

ARTICLE IN PRESSG Model

EURR-6135; No. of Pages 10

V.M. Pereira et al. / European Journal of Radiology xxx (2012) xxx– xxx 9

Fig. 16. High-resolution CT reconstruction of a stent.

Fig. 17. DSA showing coiled carotid aneurysm. A Leo stent has been put in place.

Fig. 18. CTA with reconstructions through a giant aneurysm. The volume rendering image shows the giant carotid artery aneurysm whereas the high-resolution CTangiography demonstrates the stent in situ.

ING Model

E

1 rnal o

3

CascsRawitTbui

R

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

ARTICLEURR-6135; No. of Pages 10

0 V.M. Pereira et al. / European Jou

. Conclusions

The usual work-up of aneurysms includes an initial CT withT angiography: this will demonstrate or not hemorrhage as wells an underlying aneurysm. Angiography has remained the goldtandard for objectification of an underlying vascular process; itan also provide invaluable information in planning the eventualurgical and/or endovascular treatment as well as to perform it.ecent technological advances allow angiography equipment tocquire axial Imaging as well with perfusion and anatomic images,hich may be invaluable tools for the monitoring of treatment dur-

ng and directly after the procedure. MR imaging is preferred forhe follow-up of aneurysms, especially using contrast-enhancedOF MR angiography. However combined MR-angio suites are alsoecoming available that will challenge the more traditional sett-ps we have today where diagnosis and treatment are merging

nto one single activity.

eferences

[1] Krayenbühl HA, Yas argil MG, Flamm ES, Tew Jr JM. Microsurgical treatment ofintracranial saccular aneurysms. Journal of Neurosurgery 1972;37(December(6)):678–86.

[2] Ljunggren B, Säveland H, Brandt L, Zygmunt S. Early operation and overalloutcome in aneurysmal subarachnoid hemorrhage. Journal of Neurosurgery1985;62(April (4)):547–51.

[3] Ostergaard JR. Warning leak in subarachnoid haemorrhage. BMJ 1990;301(July(6745)):190–1.

[4] Jakobsson KE, Säveland H, Hillman J, et al. Warning leak and managementoutcome in aneurysmal subarachnoid hemorrhage. Journal of Neurosurgery1996;85(December (6)):995–9.

[5] Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoidhemorrhage visualized by computerized tomographic scanning. Neurosurgery1980;6:1–9.

[6] Wintermark M, Uske A, Chalaron M, et al. Multislice computerized tomogra-phy angiography in the evaluation of intracranial aneurysms: a comparisonwith intraarterial digital subtraction angiography. Journal of Neurosurgery2003;98(April (4)):828–36.

[7] Binaghi S, Colleoni ML, Maeder P, et al. CT angiography and perfusion CT incerebral vasospasm after subarachnoid hemorrhage. AJNR American Journal ofNeuroradiology 2007;28(April (4)):750–8.

[8] McCormack RF, Hutson A. Can computed tomography angiography of the brainreplace lumbar puncture in the evaluation of acute-onset headache after a neg-ative noncontrast cranial computed tomography scan? Academic EmergencyMedicine 2010;17(April (4)):444–51.

[9] Drayer BP, Wolfson SK, Reinmuth OM, Dujovny M, Boehnke M, Cook EE. Xenonenhanced CT for analysis of cerebral integrity, perfusion, and blood flow. Stroke1978;9(March–April (2)):123–30.

10] Sanelli PC, Ugorec I, Johnson CE, et al. Using quantitative CT perfusion forevaluation of delayed cerebral ischemia following aneurysmal subarachnoidhemorrhage. AJNR American Journal of Neuroradiology 2011;32(December

Please cite this article in press as: Pereira VM, et al. Diagnohttp://dx.doi.org/10.1016/j.ejrad.2012.10.014

(11)):2047–53.11] Willinsky RA, Taylor SM, TerBrugge K, Farb RI, Tomlinson G, Montanera W.

Neurologic complications of cerebral angiography: prospective analysis of2899 procedures and review of the literature. Radiology 2003;227(May (20)):522–8.

[

PRESSf Radiology xxx (2012) xxx– xxx

12] Dawkins AA, Evans AL, Wattam J, et al. Complications of cerebral angiogra-phy: a prospective analysis of 2924 consecutive procedures. Neuroradiology2007;49(September (9)):753–9.

13] Fifi JT, Meyers PM, Lavine SD, et al. Complications of modern diagnostic cerebralangiography in an academic medical center. Journal of Vascular and Interven-tional Radiology 2009;20(April (4)):442–7.

14] White PM, Teasdale FRCR, Wardlaw EM, Easton JMV. Intracranial aneurysms:CT angiography and MR angiography for detection – prospective blinded com-parison in a large patient cohort. Radiology 2001;June (219):739–49.

15] Walace RC, Karis JP, Partovi S, Fiorella D. Noninvasive imaging of treatedcerebral aneurysms. Part II: CT angiographic follow-up of surgically clippedaneurysms. AJNR American Journal of Neuroradiology 2007;28(August(7)):1207–12.

16] Kwee TC, Kwee RM. MR angiography in the follow-up of intracranial aneurysmstreated with guglielmi detachable coils: systematic review and meta-analysis.Neuroradiology 2007;49(September (9)):703–13.

17] Wallace RC, Karis JP, Partovi S, Fiorella D. Noninvasive imaging of treated cere-bral aneurysms, part I: MR angiographic follow-up of coiled aneurysms. AJNRAmerican Journal of Neuroradiology 2007;28(June–July (6)):1001–8.

18] Söderman M, Babic D, Holmin S, Andersson T. Brain imaging with a flatdetector C-arm: technique and clinical interest of XperCT. Neuroradiology2008;50(October (10)):863–8.

19] Clarenc on F, Piotin M, Pistocchi S, Babic D, Blanc R. Evaluation of stent visi-bility by flat panel detector CT in patients treated for intracranial aneurysms.Neuroradiology 2012. February [Epub ahead of print].

20] Kizilkilic O, Kocer N, Metaxas GE, Babic D, Homan R, Islak C. Utility of VasoCTin the treatment of intracranial aneurysm with flow-diverter stents. Journal ofNeurosurgery 2012;117(July (1)):45–9.

21] Lövblad KO, Flat panel detector CT. CT angiography, and CT perfusion in stroke.AJNR American Journal of Neuroradiology 2010;31(September (8)):1470.

22] Lummel N, Schoepf V, Burke M, Brueckmann H, Linn J. 3D fluid-attenuatedinversion recovery imaging: reduced CSF artifacts and enhanced sensitivityand specificity for subarachnoid hemorrhage. AJNR American Journal of Neu-roradiology 2011;32(December (11)):2054–60.

23] Mohamed M, Heasly DC, Yagmurlu B, Yousem DM. Fluid-attenuated inver-sion recovery MR imaging and subarachnoid hemorrhage: not a panacea. AJNRAmerican Journal of Neuroradiology 2004;25(April (4)):545–50.

24] Shimoda M, Hoshikawa K, Shiramizu H, Oda S, Matsumae M. Problems withdiagnosis by fluid-attenuated inversion recovery magnetic resonance imag-ing in patients with acute aneurysmal subarachnoid hemorrhage. NeurologiaMedico-Chirurgica (Tokyo) 2010;50(7):530–7.

25] Romner B, Sonesson B, Ljunggren B, Brandt L, Säveland H, Holtås S. Latemagnetic resonance imaging related to neurobehavioral functioning afteraneurysmal subarachnoid hemorrhage. Neurosurgery 1989;25(September(3)):390–6.

26] Maeder PP, Meuli RA, de Tribolet N. Three-dimensional volume render-ing for magnetic resonance angiography in the screening and preoperativeworkup of intracranial aneurysms. Journal of Neurosurgery 1996;85(December(6)):1050–5.

27] Wichmann W, Von Ammon K, Fink U, Weik T, Yasargil GM. Aneurysm clipsmade of titanium: magnetic characteristics and artifacts in MR. AJNR AmericanJournal of Neuroradiology 1997;18(May (5)):939–44.

28] Pierot L, Portefaix C, Boulin A, Gauvrit JY. Follow-up of coiled intracranialaneurysms: comparison of 3D time-of-flight and contrast-enhanced magneticresonance angiography at 3T in a large, prospective series. European Radiology2012;22(October (10)):2255–63.

29] Lövblad KO, Yilmaz H, Chouiter A, et al. Intracranial aneurysm stenting:

stic approach to cerebral aneurysms. Eur J Radiol (2012),

follow-up with MR angiography. Journal of Magnetic Resonance Imaging2006;24(August (2)):418–22.

30] Lövblad KO, el-Koussy M, Guzman R, et al. Diffusion-weighted and perfusion-weighted MR of cerebral vasospasm. Acta Neurochirurgica Supplement2001;77:121–6.