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Diagnostic approach to cerebral aneurysms
European Journal of Radiology 82 (2013) 1623–1632
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Diagnostic approach to cerebral aneurysms Vitor Mendes Pereira a , Philippe Bijlenga b , Ana Marcos a , Karl Schaller b , Karl-Olof Lovblad a,∗ a b
Division of Diagnostic and Interventional Neuroradiology, Geneva University Hospitals, Switzerland Department of Neurosurgery, Geneva University Hospitals, Switzerland
a r t i c l e
i n f o
Article history: Received 8 October 2012 Accepted 25 October 2012 Keywords: Aneurysm Computed tomography Magnetic resonance imaging Hemorrhage
a b s t r a c t Cerebral aneurysms are an important cause of morbidity and mortality due to their causal effect in non-traumatic subarachnoid hemorrhage. Neurosurgical progress in the 20th century helped to improve patient outcomes greatly. In recent years, techniques such as intravascular treatment by coiling and/or stenting have found an additional place in the management of the disease. With the development of less and less invasive surgical and endovascular techniques, there has also been a continuous development in imaging techniques that have led to our current situation where we dispose of CT and MR techniques that can help improve treatment planning greatly. CT is able to detect and together with its adjunct techniques CT 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 has evolved by becoming the standard tool for guidance during decision making for whatever therapy is being envisioned be it endovascular procedures and or surgery and has even progressed more recently due to the development of so-called flat panel technology that now allows to acquire CT-like images during and directly after an intervention. Thus nowadays, the diagnostic and interventional techniques and procedures have become so much entwined as to be considered a whole. © 2012 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Subarachnoid hemorrhage (SAH) is a well-known cause of high mortality and morbidity. As a clinical entity SAH is considered to be one of the many possible types of stroke or cerebrovascular diseases. Until recent advances in interventional neuroradiology, a strict neurosurgical approach with operation, and mainly clipping was the accepted approach [1]. Initially the approach to aneurysms was cautious due to its high mortality, but after having known great strides in the improvement of surgical techniques, it was established that early operation will prevent re-bleeding, and thus aneurysm treatment has become an emergency situation [2]. While surgery is the approach which has historically defined the management since one could evacuate blood and exclude the aneurysm by clipping, progress in interventional neuroradiology with the development of coiling and stenting techniques have provided us with more choices for treatment. In most centers, there is a tendency for the management of aneurysms to become a multidisciplinary effort that will involve many specialists from the field of clinical
∗ Corresponding author at: Service Neurodiagnostique et Neuro-interventionnel DISIM, Hopitaux Universitaires de Genève, 4 rue Gabrielle-Perret-Gentil, 1211 Geneva, Switzerland. Tel.: +41 22 372 70 33; fax: +41 22 372 70 72. E-mail address: [email protected] (K.-O. Lovblad). 0720-048X/$ – see front matter © 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejrad.2012.10.014
neuroscience beside neurosurgeons such as neuroradiologists (both diagnostic and interventional), neuroanesthesiologists, neurointensivists and even neurologists. While the initial bleed will have an important devastating effect with between 10 and 20% dying initially, the remainder of the patients can benefit from surgery or interventional neuroradiology, which will obliterate the aneurysm and evacuate blood. Globally, it can be considered that 90% of aneurysms are located on the anterior circulation and 10% in the posterior cerebral circulation. Originally a diagnosis of an aneurysm could be made clinically upon rupture due to the typical signs of thunderclap headache accompanied by neck stiffness and neurological signs, all of which would be confirmed with a lumbar puncture; in a few select cases the aneurysm would cause deficits by pressing on a cranial nerve directly (mostly in cases of giant aneurysms). The initial examination of choice for aneurysms in the acute stage is at the moment clearly still computed tomography (CT). Indeed, its capacity to clearly define newly extravasated blood is still unchallenged by magnetic resonance imaging. Over the last decade, additional CT-based methods such as CT angiography (CTA) and CT perfusion have evolved enough so that they can provide results that can be reliably used in the clinical setting. The referral for a suspicion of cerebral aneurysm can be extremely varied because while many patients arrive acutely with signs of acute headache and deterioration, some will arrive with an “incidental”
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Fig. 1. Patient with typical “warning leak”. He presented with headaches, went to CT which failed to show any clear SAH. However there was a suspicious dilatation of the right MCA (D). On angio-CT an aneurysm was demonstrated (E)–(F).
discovery of an aneurysm having usually occurred during imaging (CT or MRI) for headache or something completely different at times. Also, one population that is very important to identify is that of patients who will have suffered a so-called warning leak: these hemorrhages are known to have occurred in between 20 and 35% of patients [3,4]; if correctly identified, the patients could benefit from CT and CTA in order to identify a not yet completely ruptured aneurysm that could be treated quickly (Fig. 1). The aim of this paper is to discuss the state-of-the-art diagnostic workup irrespective of the treatment modality chosen. 1.1. Computed tomography Blood at least in the early stage is seen as a hyperdensity (i.e. a structure more “white” than the adjacent brain parenchyma) and is very easily detected with CT. The most common case of SAH is traumatic (85%), but most cases of non-traumatic SAH are due to aneurysms. In the situation of traumatic SAH very often, a trauma is known, but in some cases it must be suspected if the blood is located in locations less typical for aneurysms (e.g. subarachnoid blood on the convexity of the brain) or if radiologically there are evident signs of an external traumatic event. CT is also the preferred method for imaging whenever a trauma to the head is known or suspected. However in 15–20% of cases of non traumatic SAH there is no aneurysm to be found and 2/3 of these cases are due to peri-mesencephalic SAH. Peri-mesencencephalic SAH, which is characterized by the presence of blood in the basal cisterns in front of the mesencephalon mainly is usually not of aneurysmatic origin and has a good prognosis (Fig. 2). Cerebral angiography after the initial clinical event was the technique that would allow to demonstrate or exclude a cause of the symptoms. All of this was drastically changed when computed tomography (CT) appeared in the early 70’s and one could see the contents of the skull and its different structures; one was thus able to directly visualize the subarachnoid blood. Initially, even with CT displaying blood, angiography was necessary until only just a decade ago; indeed, CT has evolved enormously since its development: it is no longer simply used as a tool to rule out hemorrhage, but can in itself be used for very advanced imaging and pre-therapeutic purposes.
Blood accumulation on the scanner is graded according to the Fisher classification [5] with a grade 1 being no blood visible and a grade 4 with diffuse or no subarachnoid blood but intraventricular or intraparenchymal clot (Figs. 3–5). Very rarely a calcified aneurysm can be seen on the conventional X-ray image (Fig. 6) as a calcified crescent: this is nowadays much better seen on the CT and CTA images. In a study using multi-slice CTA, Wintermark et al. found a sensitivity of 94.8%; this study was done in the early stages of multi-slice imaging: i.e. with scanners with 8 and 16 detector rows; with subsequent actual advances the number of rows allowing simultaneous acquisition has increased even more [6,7]. CTA was also found to be sufficient to exclude aneurysms in patients with subarachnoid hemorrhage in cases with patterns of peri-mesencephalic SAH with a sensitivity of 96.4%. It still remains important to go though and look at all axial slices (Fig. 7), before using the reconstructions. While reconstructions using more sophisticated software packages will often enhance the anatomic detail (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 than 99% in a recent publication [8]. Perfusion CT: even though CT perfusion techniques had been around for quite some time [9], they were also only implemented clinically recently due to advances in multi-slice techniques. Xenon CT had initially been done but this technique had not found a vast acceptance [9]. CT perfusion protocols have been used with great success in the diagnosis and management of acute stroke. In the case of patients with aneurysms, it has been restricted mostly to the study of vasospasm or more rarely ischemia that may occur after vessel occlusion (Fig. 13). Vasospasm, which usually occurs during the two weeks after SAH, if severe enough may cause ischemia and the so-called delayed neurological deficits that may even cause significant morbidity progress to death. Sanelli et al. found the use of CBF and MTT to bring the most useful information [10] When using all these CT techniques together, conventional CT, CTA and CTP the idea is to maximally orient the clinician by demonstrating, hemorrhage, eventual tissular damage as well as prepare for intervention by providing maximum resolution imaging in 3 D
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Fig. 2. Patient with perimesencephalic blood on the CT (A). On subsequent MRA no aneurysm can be seen (B). This was a typical case of perimesencephalic subarachnoid hemorrhage.
(Fig. 14). CTP will usually not be performed in the initial evaluation of the patient with a suspicion of SAH and aneurysm but will be more used in the follow-up period after treatment has been done usually. For follow-up studies however, whenever a metallic device (coil or clip) has been implanted, beam hardening artifacts appear that greatly diminish the visibility of the vessel and the surrounding brain structures. 1.2. Conventional angiography While cerebral angiography remains the gold standard examination and is still the one that is preformed in most cases where
an intervention is being planned, in the acute setting at least for diagnostic purposes it has been replaced by the CT scanner. In a prospective series, Willinsky et al. found a rate of 1.3% of neurologic complications due to cerebral angiography [11] but have been as low as 0.34% in the series of Dawkins [12] in a more selected series of patients. This low occurrence has been reproduced for high-volume academic centers [13]. Despite developments in technology, when confronted with SAH that may be due to an aneurysm, based on absence of trauma or location, angiography is still advised because 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 also remains the technique of choice to really demonstrate the presence
Fig. 3. Fisher 2 grade SAH: subarachnoid blood can be seen as thin hyperdense layer in the right sylvian fissure.
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Fig. 4. SAH Fisher grade 3: diffuse blood in the basal cisterns. The blood is located more in the right basal cistern (A). CT angiography reveals a small right-sided carotid aneurysm (B).
of vasospasm that occurs a few days after SAH in cases of more severe bleeding. Again, once the catheter is in situ the physician may choose to either perform mechanical dilatation or to give some kind of intra-arterial vasodilator drug (papaverine, nimodipine,etc). However, the development of flat panel technology has allowed these angiography units to develop axial imaging capabilities that go well beyond angiography with now CT angiography as well as CT perfusion images being possible to acquire in addition to simple diagnostic images [18–21]. Indeed this will allow the interventional neuroradiologist to not just assess the presence of blood but also to determine if any significant changes have occurred since the CT done usually just prior to intervention (Fig. 15). In addition to providing these yet slightly low quality CT images but that are enormously helpful, flat panel techniques also allow to perform
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-up of aneurysms after treatment. While sequences such as diffusion and perfusion imaging can be of great help in order to detect lesions that may are established, MRI still remains slightly more difficult to assess regarding the presence of acute bleeding, especially in the subarachnoid regions. Indeed, the presence of pulsation artifacts sometimes renders the exact evaluation of sequences such as FLAIR difficult to the novice. In the early stages MRI was problematic due to the fact that the patient could initially not (or not well
Fig. 5. Patient with an anterior cerebral artery aneurysm having caused diffuse SAH, there is also blood in the ventricles as well as in the parenchyma of the frontal lobe on the left (A). This corresponds to a Fisher grade 4. The aneurysm is demonstrated on the CTA (B).
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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 end of the left carotid is well seen and CTA shows the filling of the structure corresponding to the aneurysm.
Fig. 7. Carotid aneurysm, on the right side, oriented inwards (A). This is seen better in the coronal MIP projection (arrow) (B).
enough) be monitored and had to remain very calm inside the MR scanner; then, with the development of faster scanning methods and more and more MRI compatible hardware (clips, coils, monitoring equipment), the technique has become feasible even in less stable patients.
Indeed while FLAIR can sometimes demonstrate hyperintensities in the sulci that corresponds to blood, it may be difficult to 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
Fig. 8. MCA bifurcation aneurysm with sagittal MIP (A) and volume rendering reconstructions (B).
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Fig. 9. Carotid aneurysm seen both in the coronal MIP CTA reconstruction (A) as well as on the contrast-enhanced MR angiography (B).
Fig. 10. A Com aneurysm of the anterior communicating artery, seen on the axial image (A) but much better seen on the coronal reconstruction (B).
nothing [24]. Also, while from a theoretical point of view, MRI using a combination of T2*, FLAIR and T2 techniques should be clearly superior to CT, very often most radiologists feel more at easy to interpret blood still using CT. Regarding chronic deposits of subarachnoid blood for example in the sulci, MRI, especially using T2* techniques or even better susceptibility-weighted imaging (SWI) will better demonstrate these areas of cortical signal drop. As with most intracerebral lesions and structures, “conventional” MRI sequences will be most suited to demonstrate the final lesion that will explain the eventual neurological or neuropsychological deficit in a given patient [25]. Magnetic resonance angiography has at least from a theoretical perspective the advantage of being able to produce images of the brain vasculature [26] without the use of contrast material: this can be done either with the time-of-flight technique or phase contrast
technique. Usually, TOF techniques are more commonly used even though they are very susceptible to flow direction. For the follow-up of patients with aneurysms, the use of MRA based on time-of-flight techniques has become the standard approach. Indeed, while initial worries regarding the use of the high magnetic fields with either clips or coils or even stents have proven unfounded, at least with current generations of devices that are produced to be MR compatible [27]; however improvements have been made with the continuous development of contrast – enhanced MR angiography methods: Pierot found that while contrast-enhanced MRA could better depict aneurysm remnant after treatment, coil visibility itself was better on TOF type images [28]. Stented arteries can also be visualized both with CTA and MRA techniques [19,29] Again as with CT perfusion, techniques using diffusion and perfusion MR have been proven of interest in cases with aneurysmal
Fig. 11. Basilar artery aneurysm demonstrated in both sagittal (A) and coronal MIP projections (B).
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Fig. 12. Left sided MCA aneurysm with small intraparenchymal hematoma (A, B) with an aneurysm being seen on the CT angiograms (C, D).
SAH. Sometimes, the use of diffusion will reveal a small lesion due to ischemia [30]; perfusion techniques, like those we know from CT are not as easy to use because while MR perfusion does cover the whole brain, the changes found in early stages of vasospasm may be easily missed; in later stages one will again find the presence of alterations in blood flow parameters in the region vascularized by the spastic vessel.
2. Discussion Cerebral aneurysms are a treatable cause of severe disability; this has been made possible due to parallel advances over many decades in both diagnostic (imaging) and in therapeutic modalities. While it is still associated with high rates of initial mortality, treatment options have evolved from simple
Fig. 13. Patient with SAH and vasospasm: CT perfusion shows alterations in the right MCA territory whereas angio-CT shows vessel irregularities.
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Fig. 14. CT showing SAH, more widely distributed on the left. Angiography demonstrated a left-sided posterior communicating artery aneurysm which was subsequently coiled. DSA shows the lateral projection before and after coiling. Also antero-posterior skull view showing the coil in situ.
surgery (originally carotid ligation) to more advanced clipping techniques using microneurosurgery to now encompass endovascular methods such as coiling and even stenting. Very often all of these techniques are used in combination and not alone. Imaging of aneurysms rests to a great extent on the use of computed tomography for diagnosis and angiography for confirmation or information that may lead to a procedure. Angiography, which is the gold standard reference method for the demonstration
Fig. 15. CT images reconstructed from rotation images acquired on the angiography table.
of an aneurysmal change, is today more and more used as an advanced planning tool in order to prepare for what may mostly turn out to be an endovascular approach. This, together with the development of so-called flat panel detector techniques has ushered in a real period of multi-modal imaging with axial imaging being performed at the same time. Also this allows combined approaches to be developed in cases where surgery as well as endovascular navigation is necessary: in addition to being to fully combined techniques, it is possible to use one technique to complement the other in case of need. MR technology is also now coming of age so that it can be incorporated into this patient oriented approach and where the physicians can benefit from the increased insight into not just pathology and anatomy but into pathophysiology in order to improve and predict patient outcomes. For follow-up purposes, MR techniques are becoming the method of choice: on the one hand the do not subject the patient to additional radiation and on the other hand they can better demonstrate the post-therapeutic vessel: by using contrast-enhanced time-of-flight MRA techniques, it is possible to obtain at 1.5 T and 3.0 T images of the vessel adjacent to the coiled vessel that will allow to continue follow-up with this technique. If on follow-up examinations there is a suspicion of aneurysm re-growth, one may then decide to proceed at first to angiography in order to decide whether to re-treat. Also MRI can better the presence of small ischemic changes that may have been induced by the bleeding itself, the operation/intervention or even vasospasm. Also when one considers patients having been treated either with coils or clips, MRI, while having central signal drops at the location of the device, is still better tan CT where very often very impressive “stellate” beamhardening artifacts sometimes render image interpretation difficult if not impossible.
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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 CT angiography demonstrates the stent in situ.
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3. Conclusions The usual work-up of aneurysms includes an initial CT with CT angiography: this will demonstrate or not hemorrhage as well as an underlying aneurysm. Angiography has remained the gold standard for objectification of an underlying vascular process; it can also provide invaluable information in planning the eventual surgical and/or endovascular treatment as well as to perform it. Recent technological advances allow angiography equipment to acquire axial Imaging as well with perfusion and anatomic images, which may be invaluable tools for the monitoring of treatment during and directly after the procedure. MR imaging is preferred for the follow-up of aneurysms, especially using contrast-enhanced TOF MR angiography. However combined MR-angio suites are also becoming available that will challenge the more traditional settups we have today where diagnosis and treatment are merging into one single activity. References [1] Krayenbühl HA, Yas¸argil MG, Flamm ES, Tew Jr JM. Microsurgical treatment of intracranial saccular aneurysms. Journal of Neurosurgery 1972;37(December (6)):678–86. [2] Ljunggren B, Säveland H, Brandt L, Zygmunt S. Early operation and overall outcome in aneurysmal subarachnoid hemorrhage. Journal of Neurosurgery 1985;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 management outcome in aneurysmal subarachnoid hemorrhage. Journal of Neurosurgery 1996;85(December (6)):995–9. [5] Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 1980;6:1–9. [6] Wintermark M, Uske A, Chalaron M, et al. Multislice computerized tomography angiography in the evaluation of intracranial aneurysms: a comparison with intraarterial digital subtraction angiography. Journal of Neurosurgery 2003;98(April (4)):828–36. [7] Binaghi S, Colleoni ML, Maeder P, et al. CT angiography and perfusion CT in cerebral vasospasm after subarachnoid hemorrhage. AJNR American Journal of Neuroradiology 2007;28(April (4)):750–8. [8] McCormack RF, Hutson A. Can computed tomography angiography of the brain replace lumbar puncture in the evaluation of acute-onset headache after a negative noncontrast cranial computed tomography scan? Academic Emergency Medicine 2010;17(April (4)):444–51. [9] Drayer BP, Wolfson SK, Reinmuth OM, Dujovny M, Boehnke M, Cook EE. Xenon enhanced CT for analysis of cerebral integrity, perfusion, and blood flow. Stroke 1978;9(March–April (2)):123–30. [10] Sanelli PC, Ugorec I, Johnson CE, et al. Using quantitative CT perfusion for evaluation of delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. AJNR American Journal of Neuroradiology 2011;32(December (11)):2047–53. [11] Willinsky RA, Taylor SM, TerBrugge K, Farb RI, Tomlinson G, Montanera W. Neurologic complications of cerebral angiography: prospective analysis of 2899 procedures and review of the literature. Radiology 2003;227(May (20)): 522–8.
[12] Dawkins AA, Evans AL, Wattam J, et al. Complications of cerebral angiography: a prospective analysis of 2924 consecutive procedures. Neuroradiology 2007;49(September (9)):753–9. [13] Fifi JT, Meyers PM, Lavine SD, et al. Complications of modern diagnostic cerebral angiography in an academic medical center. Journal of Vascular and Interventional 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 comparison in a large patient cohort. Radiology 2001;June (219):739–49. [15] Walace RC, Karis JP, Partovi S, Fiorella D. Noninvasive imaging of treated cerebral aneurysms. Part II: CT angiographic follow-up of surgically clipped aneurysms. AJNR American Journal of Neuroradiology 2007;28(August (7)):1207–12. [16] Kwee TC, Kwee RM. MR angiography in the follow-up of intracranial aneurysms treated 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 cerebral aneurysms, part I: MR angiographic follow-up of coiled aneurysms. AJNR American Journal of Neuroradiology 2007;28(June–July (6)):1001–8. [18] Söderman M, Babic D, Holmin S, Andersson T. Brain imaging with a flat detector C-arm: technique and clinical interest of XperCT. Neuroradiology 2008;50(October (10)):863–8. [19] Clarenc¸on F, Piotin M, Pistocchi S, Babic D, Blanc R. Evaluation of stent visibility 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 VasoCT in the treatment of intracranial aneurysm with flow-diverter stents. Journal of Neurosurgery 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-attenuated inversion recovery imaging: reduced CSF artifacts and enhanced sensitivity and specificity for subarachnoid hemorrhage. AJNR American Journal of Neuroradiology 2011;32(December (11)):2054–60. [23] Mohamed M, Heasly DC, Yagmurlu B, Yousem DM. Fluid-attenuated inversion recovery MR imaging and subarachnoid hemorrhage: not a panacea. AJNR American Journal of Neuroradiology 2004;25(April (4)):545–50. [24] Shimoda M, Hoshikawa K, Shiramizu H, Oda S, Matsumae M. Problems with diagnosis by fluid-attenuated inversion recovery magnetic resonance imaging in patients with acute aneurysmal subarachnoid hemorrhage. Neurologia Medico-Chirurgica (Tokyo) 2010;50(7):530–7. [25] Romner B, Sonesson B, Ljunggren B, Brandt L, Säveland H, Holtås S. Late magnetic resonance imaging related to neurobehavioral functioning after aneurysmal subarachnoid hemorrhage. Neurosurgery 1989;25(September (3)):390–6. [26] Maeder PP, Meuli RA, de Tribolet N. Three-dimensional volume rendering for magnetic resonance angiography in the screening and preoperative workup 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 clips made of titanium: magnetic characteristics and artifacts in MR. AJNR American Journal of Neuroradiology 1997;18(May (5)):939–44. [28] Pierot L, Portefaix C, Boulin A, Gauvrit JY. Follow-up of coiled intracranial aneurysms: comparison of 3D time-of-flight and contrast-enhanced magnetic resonance angiography at 3T in a large, prospective series. European Radiology 2012;22(October (10)):2255–63. [29] Lövblad KO, Yilmaz H, Chouiter A, et al. Intracranial aneurysm stenting: follow-up with MR angiography. Journal of Magnetic Resonance Imaging 2006;24(August (2)):418–22. [30] Lövblad KO, el-Koussy M, Guzman R, et al. Diffusion-weighted and perfusionweighted MR of cerebral vasospasm. Acta Neurochirurgica Supplement 2001;77:121–6.
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Diagnostic approach to cerebral aneurysms Vitor Mendes Pereira a , Philippe Bijlenga b , Ana Marcos a , Karl Schaller b , Karl-Olof Lovblad a,∗ a b
Division of Diagnostic and Interventional Neuroradiology, Geneva University Hospitals, Switzerland Department of Neurosurgery, Geneva University Hospitals, Switzerland
a r t i c l e
i n f o
Article history: Received 8 October 2012 Accepted 25 October 2012 Keywords: Aneurysm Computed tomography Magnetic resonance imaging Hemorrhage
a b s t r a c t Cerebral aneurysms are an important cause of morbidity and mortality due to their causal effect in non-traumatic subarachnoid hemorrhage. Neurosurgical progress in the 20th century helped to improve patient outcomes greatly. In recent years, techniques such as intravascular treatment by coiling and/or stenting have found an additional place in the management of the disease. With the development of less and less invasive surgical and endovascular techniques, there has also been a continuous development in imaging techniques that have led to our current situation where we dispose of CT and MR techniques that can help improve treatment planning greatly. CT is able to detect and together with its adjunct techniques CT 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 has evolved by becoming the standard tool for guidance during decision making for whatever therapy is being envisioned be it endovascular procedures and or surgery and has even progressed more recently due to the development of so-called flat panel technology that now allows to acquire CT-like images during and directly after an intervention. Thus nowadays, the diagnostic and interventional techniques and procedures have become so much entwined as to be considered a whole. © 2012 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Subarachnoid hemorrhage (SAH) is a well-known cause of high mortality and morbidity. As a clinical entity SAH is considered to be one of the many possible types of stroke or cerebrovascular diseases. Until recent advances in interventional neuroradiology, a strict neurosurgical approach with operation, and mainly clipping was the accepted approach [1]. Initially the approach to aneurysms was cautious due to its high mortality, but after having known great strides in the improvement of surgical techniques, it was established that early operation will prevent re-bleeding, and thus aneurysm treatment has become an emergency situation [2]. While surgery is the approach which has historically defined the management since one could evacuate blood and exclude the aneurysm by clipping, progress in interventional neuroradiology with the development of coiling and stenting techniques have provided us with more choices for treatment. In most centers, there is a tendency for the management of aneurysms to become a multidisciplinary effort that will involve many specialists from the field of clinical
∗ Corresponding author at: Service Neurodiagnostique et Neuro-interventionnel DISIM, Hopitaux Universitaires de Genève, 4 rue Gabrielle-Perret-Gentil, 1211 Geneva, Switzerland. Tel.: +41 22 372 70 33; fax: +41 22 372 70 72. E-mail address: [email protected] (K.-O. Lovblad). 0720-048X/$ – see front matter © 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejrad.2012.10.014
neuroscience beside neurosurgeons such as neuroradiologists (both diagnostic and interventional), neuroanesthesiologists, neurointensivists and even neurologists. While the initial bleed will have an important devastating effect with between 10 and 20% dying initially, the remainder of the patients can benefit from surgery or interventional neuroradiology, which will obliterate the aneurysm and evacuate blood. Globally, it can be considered that 90% of aneurysms are located on the anterior circulation and 10% in the posterior cerebral circulation. Originally a diagnosis of an aneurysm could be made clinically upon rupture due to the typical signs of thunderclap headache accompanied by neck stiffness and neurological signs, all of which would be confirmed with a lumbar puncture; in a few select cases the aneurysm would cause deficits by pressing on a cranial nerve directly (mostly in cases of giant aneurysms). The initial examination of choice for aneurysms in the acute stage is at the moment clearly still computed tomography (CT). Indeed, its capacity to clearly define newly extravasated blood is still unchallenged by magnetic resonance imaging. Over the last decade, additional CT-based methods such as CT angiography (CTA) and CT perfusion have evolved enough so that they can provide results that can be reliably used in the clinical setting. The referral for a suspicion of cerebral aneurysm can be extremely varied because while many patients arrive acutely with signs of acute headache and deterioration, some will arrive with an “incidental”
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Fig. 1. Patient with typical “warning leak”. He presented with headaches, went to CT which failed to show any clear SAH. However there was a suspicious dilatation of the right MCA (D). On angio-CT an aneurysm was demonstrated (E)–(F).
discovery of an aneurysm having usually occurred during imaging (CT or MRI) for headache or something completely different at times. Also, one population that is very important to identify is that of patients who will have suffered a so-called warning leak: these hemorrhages are known to have occurred in between 20 and 35% of patients [3,4]; if correctly identified, the patients could benefit from CT and CTA in order to identify a not yet completely ruptured aneurysm that could be treated quickly (Fig. 1). The aim of this paper is to discuss the state-of-the-art diagnostic workup irrespective of the treatment modality chosen. 1.1. Computed tomography Blood at least in the early stage is seen as a hyperdensity (i.e. a structure more “white” than the adjacent brain parenchyma) and is very easily detected with CT. The most common case of SAH is traumatic (85%), but most cases of non-traumatic SAH are due to aneurysms. In the situation of traumatic SAH very often, a trauma is known, but in some cases it must be suspected if the blood is located in locations less typical for aneurysms (e.g. subarachnoid blood on the convexity of the brain) or if radiologically there are evident signs of an external traumatic event. CT is also the preferred method for imaging whenever a trauma to the head is known or suspected. However in 15–20% of cases of non traumatic SAH there is no aneurysm to be found and 2/3 of these cases are due to peri-mesencephalic SAH. Peri-mesencencephalic SAH, which is characterized by the presence of blood in the basal cisterns in front of the mesencephalon mainly is usually not of aneurysmatic origin and has a good prognosis (Fig. 2). Cerebral angiography after the initial clinical event was the technique that would allow to demonstrate or exclude a cause of the symptoms. All of this was drastically changed when computed tomography (CT) appeared in the early 70’s and one could see the contents of the skull and its different structures; one was thus able to directly visualize the subarachnoid blood. Initially, even with CT displaying blood, angiography was necessary until only just a decade ago; indeed, CT has evolved enormously since its development: it is no longer simply used as a tool to rule out hemorrhage, but can in itself be used for very advanced imaging and pre-therapeutic purposes.
Blood accumulation on the scanner is graded according to the Fisher classification [5] with a grade 1 being no blood visible and a grade 4 with diffuse or no subarachnoid blood but intraventricular or intraparenchymal clot (Figs. 3–5). Very rarely a calcified aneurysm can be seen on the conventional X-ray image (Fig. 6) as a calcified crescent: this is nowadays much better seen on the CT and CTA images. In a study using multi-slice CTA, Wintermark et al. found a sensitivity of 94.8%; this study was done in the early stages of multi-slice imaging: i.e. with scanners with 8 and 16 detector rows; with subsequent actual advances the number of rows allowing simultaneous acquisition has increased even more [6,7]. CTA was also found to be sufficient to exclude aneurysms in patients with subarachnoid hemorrhage in cases with patterns of peri-mesencephalic SAH with a sensitivity of 96.4%. It still remains important to go though and look at all axial slices (Fig. 7), before using the reconstructions. While reconstructions using more sophisticated software packages will often enhance the anatomic detail (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 than 99% in a recent publication [8]. Perfusion CT: even though CT perfusion techniques had been around for quite some time [9], they were also only implemented clinically recently due to advances in multi-slice techniques. Xenon CT had initially been done but this technique had not found a vast acceptance [9]. CT perfusion protocols have been used with great success in the diagnosis and management of acute stroke. In the case of patients with aneurysms, it has been restricted mostly to the study of vasospasm or more rarely ischemia that may occur after vessel occlusion (Fig. 13). Vasospasm, which usually occurs during the two weeks after SAH, if severe enough may cause ischemia and the so-called delayed neurological deficits that may even cause significant morbidity progress to death. Sanelli et al. found the use of CBF and MTT to bring the most useful information [10] When using all these CT techniques together, conventional CT, CTA and CTP the idea is to maximally orient the clinician by demonstrating, hemorrhage, eventual tissular damage as well as prepare for intervention by providing maximum resolution imaging in 3 D
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Fig. 2. Patient with perimesencephalic blood on the CT (A). On subsequent MRA no aneurysm can be seen (B). This was a typical case of perimesencephalic subarachnoid hemorrhage.
(Fig. 14). CTP will usually not be performed in the initial evaluation of the patient with a suspicion of SAH and aneurysm but will be more used in the follow-up period after treatment has been done usually. For follow-up studies however, whenever a metallic device (coil or clip) has been implanted, beam hardening artifacts appear that greatly diminish the visibility of the vessel and the surrounding brain structures. 1.2. Conventional angiography While cerebral angiography remains the gold standard examination and is still the one that is preformed in most cases where
an intervention is being planned, in the acute setting at least for diagnostic purposes it has been replaced by the CT scanner. In a prospective series, Willinsky et al. found a rate of 1.3% of neurologic complications due to cerebral angiography [11] but have been as low as 0.34% in the series of Dawkins [12] in a more selected series of patients. This low occurrence has been reproduced for high-volume academic centers [13]. Despite developments in technology, when confronted with SAH that may be due to an aneurysm, based on absence of trauma or location, angiography is still advised because 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 also remains the technique of choice to really demonstrate the presence
Fig. 3. Fisher 2 grade SAH: subarachnoid blood can be seen as thin hyperdense layer in the right sylvian fissure.
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Fig. 4. SAH Fisher grade 3: diffuse blood in the basal cisterns. The blood is located more in the right basal cistern (A). CT angiography reveals a small right-sided carotid aneurysm (B).
of vasospasm that occurs a few days after SAH in cases of more severe bleeding. Again, once the catheter is in situ the physician may choose to either perform mechanical dilatation or to give some kind of intra-arterial vasodilator drug (papaverine, nimodipine,etc). However, the development of flat panel technology has allowed these angiography units to develop axial imaging capabilities that go well beyond angiography with now CT angiography as well as CT perfusion images being possible to acquire in addition to simple diagnostic images [18–21]. Indeed this will allow the interventional neuroradiologist to not just assess the presence of blood but also to determine if any significant changes have occurred since the CT done usually just prior to intervention (Fig. 15). In addition to providing these yet slightly low quality CT images but that are enormously helpful, flat panel techniques also allow to perform
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-up of aneurysms after treatment. While sequences such as diffusion and perfusion imaging can be of great help in order to detect lesions that may are established, MRI still remains slightly more difficult to assess regarding the presence of acute bleeding, especially in the subarachnoid regions. Indeed, the presence of pulsation artifacts sometimes renders the exact evaluation of sequences such as FLAIR difficult to the novice. In the early stages MRI was problematic due to the fact that the patient could initially not (or not well
Fig. 5. Patient with an anterior cerebral artery aneurysm having caused diffuse SAH, there is also blood in the ventricles as well as in the parenchyma of the frontal lobe on the left (A). This corresponds to a Fisher grade 4. The aneurysm is demonstrated on the CTA (B).
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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 end of the left carotid is well seen and CTA shows the filling of the structure corresponding to the aneurysm.
Fig. 7. Carotid aneurysm, on the right side, oriented inwards (A). This is seen better in the coronal MIP projection (arrow) (B).
enough) be monitored and had to remain very calm inside the MR scanner; then, with the development of faster scanning methods and more and more MRI compatible hardware (clips, coils, monitoring equipment), the technique has become feasible even in less stable patients.
Indeed while FLAIR can sometimes demonstrate hyperintensities in the sulci that corresponds to blood, it may be difficult to 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
Fig. 8. MCA bifurcation aneurysm with sagittal MIP (A) and volume rendering reconstructions (B).
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Fig. 9. Carotid aneurysm seen both in the coronal MIP CTA reconstruction (A) as well as on the contrast-enhanced MR angiography (B).
Fig. 10. A Com aneurysm of the anterior communicating artery, seen on the axial image (A) but much better seen on the coronal reconstruction (B).
nothing [24]. Also, while from a theoretical point of view, MRI using a combination of T2*, FLAIR and T2 techniques should be clearly superior to CT, very often most radiologists feel more at easy to interpret blood still using CT. Regarding chronic deposits of subarachnoid blood for example in the sulci, MRI, especially using T2* techniques or even better susceptibility-weighted imaging (SWI) will better demonstrate these areas of cortical signal drop. As with most intracerebral lesions and structures, “conventional” MRI sequences will be most suited to demonstrate the final lesion that will explain the eventual neurological or neuropsychological deficit in a given patient [25]. Magnetic resonance angiography has at least from a theoretical perspective the advantage of being able to produce images of the brain vasculature [26] without the use of contrast material: this can be done either with the time-of-flight technique or phase contrast
technique. Usually, TOF techniques are more commonly used even though they are very susceptible to flow direction. For the follow-up of patients with aneurysms, the use of MRA based on time-of-flight techniques has become the standard approach. Indeed, while initial worries regarding the use of the high magnetic fields with either clips or coils or even stents have proven unfounded, at least with current generations of devices that are produced to be MR compatible [27]; however improvements have been made with the continuous development of contrast – enhanced MR angiography methods: Pierot found that while contrast-enhanced MRA could better depict aneurysm remnant after treatment, coil visibility itself was better on TOF type images [28]. Stented arteries can also be visualized both with CTA and MRA techniques [19,29] Again as with CT perfusion, techniques using diffusion and perfusion MR have been proven of interest in cases with aneurysmal
Fig. 11. Basilar artery aneurysm demonstrated in both sagittal (A) and coronal MIP projections (B).
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Fig. 12. Left sided MCA aneurysm with small intraparenchymal hematoma (A, B) with an aneurysm being seen on the CT angiograms (C, D).
SAH. Sometimes, the use of diffusion will reveal a small lesion due to ischemia [30]; perfusion techniques, like those we know from CT are not as easy to use because while MR perfusion does cover the whole brain, the changes found in early stages of vasospasm may be easily missed; in later stages one will again find the presence of alterations in blood flow parameters in the region vascularized by the spastic vessel.
2. Discussion Cerebral aneurysms are a treatable cause of severe disability; this has been made possible due to parallel advances over many decades in both diagnostic (imaging) and in therapeutic modalities. While it is still associated with high rates of initial mortality, treatment options have evolved from simple
Fig. 13. Patient with SAH and vasospasm: CT perfusion shows alterations in the right MCA territory whereas angio-CT shows vessel irregularities.
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Fig. 14. CT showing SAH, more widely distributed on the left. Angiography demonstrated a left-sided posterior communicating artery aneurysm which was subsequently coiled. DSA shows the lateral projection before and after coiling. Also antero-posterior skull view showing the coil in situ.
surgery (originally carotid ligation) to more advanced clipping techniques using microneurosurgery to now encompass endovascular methods such as coiling and even stenting. Very often all of these techniques are used in combination and not alone. Imaging of aneurysms rests to a great extent on the use of computed tomography for diagnosis and angiography for confirmation or information that may lead to a procedure. Angiography, which is the gold standard reference method for the demonstration
Fig. 15. CT images reconstructed from rotation images acquired on the angiography table.
of an aneurysmal change, is today more and more used as an advanced planning tool in order to prepare for what may mostly turn out to be an endovascular approach. This, together with the development of so-called flat panel detector techniques has ushered in a real period of multi-modal imaging with axial imaging being performed at the same time. Also this allows combined approaches to be developed in cases where surgery as well as endovascular navigation is necessary: in addition to being to fully combined techniques, it is possible to use one technique to complement the other in case of need. MR technology is also now coming of age so that it can be incorporated into this patient oriented approach and where the physicians can benefit from the increased insight into not just pathology and anatomy but into pathophysiology in order to improve and predict patient outcomes. For follow-up purposes, MR techniques are becoming the method of choice: on the one hand the do not subject the patient to additional radiation and on the other hand they can better demonstrate the post-therapeutic vessel: by using contrast-enhanced time-of-flight MRA techniques, it is possible to obtain at 1.5 T and 3.0 T images of the vessel adjacent to the coiled vessel that will allow to continue follow-up with this technique. If on follow-up examinations there is a suspicion of aneurysm re-growth, one may then decide to proceed at first to angiography in order to decide whether to re-treat. Also MRI can better the presence of small ischemic changes that may have been induced by the bleeding itself, the operation/intervention or even vasospasm. Also when one considers patients having been treated either with coils or clips, MRI, while having central signal drops at the location of the device, is still better tan CT where very often very impressive “stellate” beamhardening artifacts sometimes render image interpretation difficult if not impossible.
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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 CT angiography demonstrates the stent in situ.
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3. Conclusions The usual work-up of aneurysms includes an initial CT with CT angiography: this will demonstrate or not hemorrhage as well as an underlying aneurysm. Angiography has remained the gold standard for objectification of an underlying vascular process; it can also provide invaluable information in planning the eventual surgical and/or endovascular treatment as well as to perform it. Recent technological advances allow angiography equipment to acquire axial Imaging as well with perfusion and anatomic images, which may be invaluable tools for the monitoring of treatment during and directly after the procedure. MR imaging is preferred for the follow-up of aneurysms, especially using contrast-enhanced TOF MR angiography. However combined MR-angio suites are also becoming available that will challenge the more traditional settups we have today where diagnosis and treatment are merging into one single activity. References [1] Krayenbühl HA, Yas¸argil MG, Flamm ES, Tew Jr JM. Microsurgical treatment of intracranial saccular aneurysms. Journal of Neurosurgery 1972;37(December (6)):678–86. [2] Ljunggren B, Säveland H, Brandt L, Zygmunt S. Early operation and overall outcome in aneurysmal subarachnoid hemorrhage. Journal of Neurosurgery 1985;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 management outcome in aneurysmal subarachnoid hemorrhage. Journal of Neurosurgery 1996;85(December (6)):995–9. [5] Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 1980;6:1–9. [6] Wintermark M, Uske A, Chalaron M, et al. Multislice computerized tomography angiography in the evaluation of intracranial aneurysms: a comparison with intraarterial digital subtraction angiography. Journal of Neurosurgery 2003;98(April (4)):828–36. [7] Binaghi S, Colleoni ML, Maeder P, et al. CT angiography and perfusion CT in cerebral vasospasm after subarachnoid hemorrhage. AJNR American Journal of Neuroradiology 2007;28(April (4)):750–8. [8] McCormack RF, Hutson A. Can computed tomography angiography of the brain replace lumbar puncture in the evaluation of acute-onset headache after a negative noncontrast cranial computed tomography scan? Academic Emergency Medicine 2010;17(April (4)):444–51. [9] Drayer BP, Wolfson SK, Reinmuth OM, Dujovny M, Boehnke M, Cook EE. Xenon enhanced CT for analysis of cerebral integrity, perfusion, and blood flow. Stroke 1978;9(March–April (2)):123–30. [10] Sanelli PC, Ugorec I, Johnson CE, et al. Using quantitative CT perfusion for evaluation of delayed cerebral ischemia following aneurysmal subarachnoid hemorrhage. AJNR American Journal of Neuroradiology 2011;32(December (11)):2047–53. [11] Willinsky RA, Taylor SM, TerBrugge K, Farb RI, Tomlinson G, Montanera W. Neurologic complications of cerebral angiography: prospective analysis of 2899 procedures and review of the literature. Radiology 2003;227(May (20)): 522–8.
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