Advances in non-invasive imaging of intracranial vascular disease

Ann R Coll Surg Engl 2000; 82:1-5 The Royal College of Surgeons of England Review vances in non-invasive imaging of intracranial vascular disease HR Jdger*t, JP Grievet *Lysholm Radiological Department and tUniversity Department of Neurosurgery, The National Hospitalfor Neurology and Neurosurgery, London, UK Intra-arterial catheter angiography has, in the past, been the mainstay for the investigation of intracranial vascular disease. It is, however, invasive, usually requires in-patients admission, and is associated with a rate of neurological complications between 1% and 3%.1 In recent years, magnetic resonance angiography (MRA) and CT angiography (CTA) have emerged as non-invasive alternatives for imaging blood vessels and have made a significant impact on neuroradiological investigations.2 It is the purpose of this article to explain the basic technical principles of these two methods and to give an overview of their current clinical applications. Technical considerations Both methods are based on the processing of digitally acquired cross-sectional images. There are important differences between MRA and CTA in the acquisition of these data, but the postprocessing methods have a lot in common. Data acquisition magnetic resonance angiography - MRA is performed on a conventional MR scanner and, except for a new technique, contrast-enhanced MRA, does not require the injection of a contrast medium. There are, in principle, two different techniques of MRA: time of flight (TOF) and phase contrast (PC) angiography. Of the time of flight techniques, 3D TOF angiography is used almost exclusively for the examination of intracranial vessels, whilst 2D TOF is more commonly used for neck vessels. In 3D TOF MRA, stationery tissue is saturated by a repetitive radiofrequency pulse and 'fresh spins' from non-saturated flowing blood, which traverse the region of interest, give high signal. Substances that normally have very high Ti signal, such as fat or blood clot, may be incompletely saturated (Ti contamination artifact) and appear as high signal areas. This can interfere with the diagnostic interpretation either by mimicking or by obscuring vascular structures. PC MRA is based on the detection of phase shifts generated by a flow-encoding gradient. The phase Correspondence to: Dr HR Jager, Lysholm Radiological Department, The National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BG, UK. Tel: +44 171 829 8744; Fax: +44 171 278 5122; E-mail: r.jager@ion.ucl.ac.uk Ann R Coll Surg Engl 2000; 82 1 JAGER shift is proportional to the velocity of blood and care must be taken to choose an appropriate 'velocity window' depending on the area studied. Typical velocity parameters are 15 cmn/s for dural sinuses and 50-60 cm/s for major cerebral arteries. With the help of a special software, one can also measure flow velocities in larger blood vessels. This, together with its higher sensitivity to slow flow, represents the major advantages of PC MRA compared to TOF MRA. Its disadvantages are that it can be time consuming, especially if several sequences with different velocity settings have to be performed to encompass the full velocity range of a vascular system. 2D PC is, on the contrary, very quick but provides only a limited amount of angiographic projections. A new technique of contrast-enhanced MRA involves the intravenous injection of a gadolinium-based contrast medium immediately before or during the MRA. The contrast medium shortens the Ti value of blood, which increases the intravascular signal and makes it less dependent on laminar flow. This has the potential of better visualisation of slow flow or flow running in the imaging plane. Intracranial contrast-enhanced MRA has, up to date, mostly used a modified TOF sequence. Data acquisition - CT angiography CT angiography involves the use of ionizing radiation and an iodine-based intravascular contrast medium, which is a disadvantage compared to MRA. Its advantages are that it is quicker and requires less patient cooperation. CT angiography represents essentially a variation of spiral CT scanning. Thin section axial images are acquired during the injection of a contrast medium bolus typically at a rate of 3-4 ml/s. During that period, simultaneous rotation of the CT X-ray tube and movement of the scanning table take place. The speed of the table movement has a bearing on the area coverage and spatial resolution of the CTA. Data postprocessing Axially acquired images from MRA or CTA represent a 3D data set which can be postprocessed in a number of different ways. Maximum intensity projections (MIP) These are two dimensional, projectional images of the 3D data set, which resemble projectional images obtained by conventional angiography. Any overlapping structures of high signal (on MRA) or high density (on CT) in the line of projection have to be 'cut away', otherwise they 2 NON-INVASIVE IMAGING OF INTRACRANIAL VASCULAR DISEASE would obscure the vessels of interest. The projectional images can be rotated in multiple planes, providing a large number of projections from different viewing angles. One can also generate MIP images of targeted subvolumes to show, for example, only the internal carotid circulation of one side. Additional projections can be generated on the computer console at any time after completion of the examination and the patient does not have to be recalled. 3-Dimensional images The most frequently used 3-dimensional postprocessing method is surface shaded display (SSD). This is frequently used for CTA images. In its simplest form, vascular structures are separated from surrounding structures by thresholding of CT numbers. The vascular images are then shown as 3D objects that can be viewed from different angles using a virtual light source. Because of a partial overlap of the CT numbers for vessels and bone these structures a frequently shown together. More complex methods of postprocessing, such as erosion and dilation, allow separation of vessels from bone or other high density structures such as aneurysm dips. Clinical applications Cerebral aneurysms There have now been several blinded multi-reader studies comparing the sensitivity of MRA in detecting aneurysms previously diagnosed by DSA.4' Sensitivities for detecting aneurysms larger than 5 mm ranged from 77% to 94 % with variations between observers depending on their experience in reading MRA studies. The sensitivities dropped to between 10% and 60% for aneurysms smaller than 5 mm. Some of the prospectively missed aneurysms could be detected retrospectively and the critical size for retrospective detection appears to be 2-3 mm. Performing 3D TOF MRA in patients with acute subarachnoid haemorrhage has some specific pitfalls: intraparenchymal blood clot, which is of high signal, can obscure aneurysms and vasospasm may prevent visualisation of flow in more distal vessels. On the other hand, there have been a number of case reports of patients with acute SAH which described aneurysms detected by MRA and missed by catheter angiography. In our experience of MRA in 34 patients with acute subarachnoid haemorrhage, MRA detected two surgically confirmed aneurysms, which were missed on DSA. The superiority of MRA in these Ann R Coll Surg Engi 2000; 82 NON-INVASIVE IMAGING OF INTRACRANIAL VASCULAR DISEASE JAGER instances is chiefly due to the much larger number of projections available with MRA compared to DSA where each projection necessitates separate contrast injections (with the exception of biplane systems). In view of these findings, MRA and DSA have to be viewed as complementary in the investigation of SAH. An MRA preceding the DSA study may also be useful in identifying the optimal projection angles for demonstration of aneurysms on the latter.7 Giant aneurysms represent another challenge for MRA. On 3D TOF MRA, these are rarely visualized in their full extent because of slow flow and turbulent flow in their fundus. Gadolinium-enhanced MRA is likely to provide a better delineation of giant aneurysms. CTA has a similar detection rate to MRA for cerebral aneurysms, with reported sensitivities for detection of aneurysms between 85% and 90% in a mixed patient population,89 and in patients with SAH.'0 This figure falls to 50%9 and 79%8 for aneurysms smaller then 3 mm and 5 mm, respectively. Apart from its size, the location of an aneurysm also influences its detectability on CTA: infraclinoid aneurysms of the internal carotid artery which are intimately related to the bony structures of the skull base are more easily missed. Although CTA data are usually displayed as surface shaded reconstruction some authors found that targeted MIP projections and inspection of axial source images increase the sensitivity of CTA." In CTA, the vascular lumen is directly opacified by contrast medium and there is no signal drop out due to complex flow patterns in giant aneurysms, as in 3D TOF MRA. CTA is, therefore, useful for accurate delineation of larger aneurysm. aneurysms. GDC coils, which are mainly composed of platinum, and not titanium, create large beam hardening artifact. Platinum coils create, however, very little artifact on MRA which is able to show incomplete coiling with a residual neck or flow signal in the interstices between loops of coils.'4 Treated cerebral aneurysms Modern titanium aneurysm clips no longer represent a contra-indication for MR scanning, however local safety policies may vary according to experience. Titanium is not ferromagnetic and, as a result, these clips are not deflected and do not cause geometric filed distortion. We have shown, in a recent study,'2 that there is, however, a small focal signal drop out around the clip due to magnetic susceptibility effects which precludes screening for a residual neck of the clipped aneurysm. MRA may, however, still have a role in the screening for vasospasm (see below) or non-invasive follow up of coincidental unruptered aneurysms. On CTA studies, there is less artifact surrounding the clip. According to our own experience and that of others,'3 a residual aneurysm neck following surgery can be demonstrated with this method. CTA is, however, totally unsuitable for the follow-up of coiled Ann R Coll Surg Engl 2000; 82 Cerebral arteriovenous malformations 3D TOF MRA is well suited for demonstrating high velocity flow in the major feeding vessels and nidus of a cerebral arteriovenous malformations (AVMs). Slower flow within compartments of the nidus and in draining veins may remain undetected. It is, therefore, often not possible to show all the components of an AVM with this technique. Contrast-enhanced MRA has been shown to improve the visibility of the slow flow components of AVMs. This can also be achieved with PC MRA, which is, however, more time consuming. It may be necessary to repeat the PC MRA sequence a number of times with different velocity windows to show arterial and venous components equally well. Additional information about the direction and velocity of flow in an AVM can be obtained from PC MRA using special programmes. CTA has, so far, not been widely used for the investigation of cerebral AVMs. This may be due to the fact that a relatively large area of the cranium needs to be studied to depict larger AVMs and for complete evaluation of the venous drainage. By doubling the table speed and injecting 150 ml instead of 100 ml of contrast medium we have managed complete coverage of most AVMs with an acceptable spatial resolution. We have now studied over 20 patients with cerebral AVMs and found a good correlation between catheter angiography and CTA in the detection of feeding vessels, nidus structure and draining vein. Postprocessing using 3D surface shaded display and advanced reconstruction methods requires, however, operator experience to produce reliable and reproducible results. With CTA, it is also possible to calculate the volume of an AVM nidus and to identify and quantify embolic material within it. The role of CTA in AVMs is not yet certain but it might well prove useful as an adjunct to DSA in the treatment planning and in the non-invasive follow-up of treated lesions. Intracranial stenosis and occlusion Arteriosclerotic disease Both MRA and CTA have been used in the investigation of intracerebral ischaemic vascular disease. A 3 JAGER recent study15 showed that 3D TOF MRA is more sensitive than 3D PC MRA and has also a higher negative predictive value. The length and degree of intracranial vascular stenoses can, however, be overestimated because of complex flow patterns around stenoses. This can be helped to some degree by the use of contrast-enhancement.16'17 It is of note that a number of flow and susceptibility related artifacts could mimic the presence of a stenosis in a normal intracranial circulation, particularly in the proximal intracranial ICA. CTA has also been shown to be feasible and potentially useful in the diagnosis of middle cerebral artery stenosis.18 It may well become a useful adjunct to an emergency CT examination in acute stroke. In this context, it could be used to identify the level of occlusion and help selecting patients suitable for intracranial thrombolysis. Vasospasm MRA can be used to show cerebral vasospasm but a recent comparative study with DSA showed relatively disappointing figures for sensitivity and specificity with 46% and 70%, respectively.19 CT has been used to demonstrate vasospasm following subarachnoid haemorrhage,20 but further investigations are still needed for this application. Tumour encasement We demonstrated that MRA can be used to assess vascular compromise by skull base tumours such as meningiomas and pituitary macroadenomas.21 3D TOF MRA shows readily displacement and narrowing of blood vessels by surrounding tumour. Contrastenhanced MRA shows up some background enhancement of these extra-axial tumours and can, therefore, demonstrate vascular encasement in the absence of vascular narrowing which is an advantage over conventional angiography. Venous occlusion 2D phase contrast MR angiography is a well established and rapid (as opposed to 3D PC MRA) method of diagnosing thrombotic or tumoural occlusion of the major dural sinuses. 3D TOF MRA can also be used but an acute or subacute thrombus can produce high signal, which can mimic flow. More recently, CTA has been shown to be at least as effective.' Conclusion MRA and CTA have already made a huge impact on patient management. They can be used as a first line 4 NON-INVASIVE IMAGING OF INTRACRANIAL VASCULAR DISEASE investigation in many clinical situations thereby reducing the overall patient morbidity. Their use for other clinical indications will need to be clarified by future studies. In addition, continued development in hardware and software will contribute to further improvement of the image quality of CTA and MRA. References 1. Heiserman JE, Dean BL, Hodak JA, Flom RA, Bird CR, Drayer BP. Neurologic complication of cerebral angiography. 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Cerebral venography: comparison of CT and MR projection venography. Am J Roentgenol 1997; 169:1699-707. See cover picture CT angiogram Left antero-superior view of a colour surface shaded display of a large arteriovenous malformation with associated anterior communicating artery aneurysm and large venous pouches. Ann R Coll Surg Engl 2000; 82 5