INTRODUCTION
The development of neuroimaging tech- niques has in part been driven by the need to discover and perfect methods for more rapid and accurate diagnosis of suspected cere- brovascular pathology. As a result, in recent years diagnostic and therapeutic protocols have changed by virtue of theses recent innovations.
In addition, progress in the understanding of cerebral ischaemic pathology has clearified many of the physiopathological mechanisms as- sociated with ischaemic tissue damage, which in turn have made it possible to develop more specific and effective treatment options. The neuroradiological diagnostic techniques avail- able in clinical practice today permit a non-in- vasive and definitive diagnostic evaluation as early as the hyperacute phase of ischaemic stroke, in order to properly select those pa- tients that may best be amenable to treatment with thrombolytic agents (24).
In the neuroimaging diagnostic field, MRI plays a priority role given its many applications and higher sensitivity (82%) as compared to CT (60%) in the early detection of tissue changes caused by an ischaemic event (15).
That said, CT still plays a fundamental diag- nostic and screening role in hyperacute stroke
patients given that it is more sensitive that MRI in demonstrating the presence of haemorrhag- ic foci.
With the perfusion, diffusion, spectroscopy and MR angiographic techniques, MRI repre- sents an important arsenal for studying is- chaemic stroke (within the first six hours) and the tissue changes caused by an occlusive thromboembolic event. The rational integra- tion of the various MRI methods available per- mits a non-invasive, rapidly acquired diagnostic analysis of the patient presenting with signs of cerebral ischaemia, especially when it is aimed at optimally selecting patients for a specific treatment such as thrombolysis (24, 26).
MR angiography (MRA) in particular has won itself a well-defined role in diagnostic protocols evaluating cerebral ischaemia not only as a screening method, but also as an al- ternative to selective digital subtractive an- giography (DSA) of the brachiocephalic and cerebral vessels. At present MRA constitutes an indispensable diagnostic method, which when integrated with basic MRI is the means of choice for studying the cerebral vessels with the aim of locating the site of vascular stenoses and occlusions as well as their effects upon the underlying brain tissue. Collectively the vari- ous MRI techniques are currently able to ac-
1.9
MR ANGIOGRAPHY
A. Carella, P. D’Aprile, A. Tarantino
quire high quality images of the intra- and ex- tracranial cerebral blood vessels that not only supply qualitative data, but also yield informa- tion on the relative velocity and direction of the blood flow.
TECHNIQUES
The techniques used are unenhanced time of flight (TOF) and phase contrast (PC) 2D and 3D (two and three dimensional) MR angiogra- phy and contrast enhanced MR angiography (CE-MRA).
Time of flight (TOF)
The techniques based on the principles of TOF MR angiography are widespread and are easily performed at the same time as the basic MR scan. They are based on “inflow” phenom- ena capable of creating good flow-related con- trast enhancement between the signal of sta- tionary tissues and that of blood protons (i.e., blood) in movement. On entering the imaging volume under examination, the protons have not yet been subject to spatially selective ra- diofrequency pulses and they produce a much higher signal than that given by stationary pro- tons within the imaging volume, which are par- tially saturated by previous radiofrequency (RF) pulses.
The degree of increase in flow signal de- pends on many parameters that are partly spe- cific to the tissues examined (T1 relaxation time) and partly dependent on the acquisition parameters used (TR, TE, flip angle, etc.), the type of flow (velocity, turbulence, etc.) and on the geometry of the acquisition volume in com- parison with the direction of the blood flow (1).
The 3D TOF technique is especially useful in studying the arterial circulation, whereas the 2D technique, which has a lower spatial defini- tion than 3D, is particularly useful in studying slow (venous) flow. TOF techniques can be supplemented by techniques able to improve the suppression of stationary background tissue signal, thus increasing the relative contrast of
the flow signal using an additional “off reso- nance” RF pulse that acts on the stationary pro- tons, saturating them selectively in comparison to those in movement that do not react to this pulse (Magnetization Transfer Contrast: MTC) (4, 6). Other possibilities of accomplishing this are to reduce intravoxel dephasing and satura- tion of the spins with the tilted optimized non saturation excitation (TONE) and multiple overlapping thin slab acquisition (MOTSA) techniques. In the TONE method, the flip an- gle is gradually increased as the flow proceeds towards the centre of the acquisition volume in order to compensate for the reduction in longi- tudinal magnetization of the spins in move- ment, whereas the MOTSA technique uses an acquisition of multiple volumes that interleave with one another (7, 16-18).
TOF techniques have limitations that are mainly characterized by two situations: the first source of error is caused by the presence in the acquisition volume of stationary tissues that can appear hyperintense (e.g., gadolinium enhance- ment, meta-haemoglobin, fat and oily sub- arachnoid contrast media) and that can there- fore be wrongly interpreted as blood flow sig- nal; the second source of error considers the possibility that vascular structures may appear isointense and therefore not emit blood flow signal using certain acquisition parameters.
This latter situation can depend on a series of technical factors (e.g., TE, TR, flip angle, direc- tion of blood flow, thickness of the acquisition layer and acquisition volume). For example, the inadvertent use of a high TE value can be one of the main causes of a lack of vascular signal;
fortunately, many MR systems only allow a vari- ation in TE values within narrow limits.
It should also be stressed that in 3D-TOF ac- quisitions, the anatomical structure of interest must be correctly positioned within the acquisi- tion volume, in other words in the lower third of the slab (where the inflow effect is highest).
Phase Contrast (PC)
This technique capitalizes upon the phase
effects that occur when protons move along the
direction of a magnetic field gradient. PC MR angiography techniques allow the quantifica- tion of flow velocity and volume as well as the direction of the blood flow. In general, this method entails long acquisition times with wide fields of view, and it is therefore the technique of choice in the study of arteriovenous fistulas and AVM’s. In fact, PC and TOF MR angiog- raphy are complementary and provide for a more accurate diagnosis when combined.
Contrast Enhancement (CE)
Dynamic MR angiographic techniques use the intravascular phase of a bolus of paramag- netic contrast medium (e.g., gadolinium) inject- ed intravenously, in association with the acqui- sition of ultrafast sequences dependent on T1 relaxation times (9, 19, 22). The use of intra- venous contrast medium causes a significant re- duction in the T1 relaxation time of the blood with a considerable increase in the intensity of the blood flow signal as well as the relative con- trast between blood and the stationary tissues.
It goes without saying that in order for the con- trast medium to have a maximum effect, it re- quires an optimal choice of the time interval be- tween the intravenous injection of the contrast medium bolus and image acquisition.
The main drawback of this technique is an increase in stationary tissue signal and the si- multaneous opacification of the veins. However, this limitation can be reduced by the use of very short scanning times (e.g., a partial K space technique as in “key-hole” sequences) and by rapidly administering the contrast medium as a bolus during data acquisition in order to ac- quire the images when the contrast medium reaches its greatest intravascular concentration.
MR ANGIOGRAPHY
OF THE SUPRAAORTIC VESSELS Technique
In recent years MRA has enabled an accurate and non-invasive diagnostic analysis of the
supraaortic vessels, which together with Doppler ultrasound studies in the presurgical phase has limited the use of invasive conventional DSA to selected cases.
Although PC MR angiography can be uti- lized to examine the supraaortic vessels, TOF techniques are more commonly employed. Gen- erally speaking, for studies of the carotid bifur- cation a transverse acquisition plane with a 3D- TOF technique is used to reduce the saturation effects, however, this technique has certain lim- itations due to its long acquisition times and consequently the associated motion artefacts (14). The proposal made by Prince in 1994 (19) was therefore accepted with enthusiasm; the proposal involved using contrast-enhanced 3D MR angiography to capture the passage of a bo- lus of paramagnetic contrast material through the inaging volume in order to study the supraaortic vessels. This led to the perfection of a technique capable of examining the extracra- nial vessels including the aortic arch, the origins of the supraaortic vessels and the neck vessels (13, 23). In particular, extremely fast volumet- ric acquisitions are used directly in the coronal plane during the injection of the contrast medi- um bolus, over acquisition times of approxi- mately 15-30 seconds. In this technique, given that the signal is produced mainly by the ad- ministered contrast agent, it is mandatory to syn- chronize the image acquisition with the injec- tion of the contrast agent in order to obtain maximum arterial filling during the central por- tion of acquisition. The advantage of this method lies in the speed of the examination and in the possibility of now covering the entire length of the brachiochephalic vessels from their origins through their proximal intracranial seg- ments (Figs. 1.87, 1.88).
Clinical applications
The cervical carotid and vertebral arteries
were the first vascular segments for the applica-
tion of MR angiography. Numerous studies of
MRA show its high sensitivity in detecting
carotid stenoses, 92-100%, with a specificity of
64-100% (2, 5, 14).
Slow and turbulent flow can cause a signal drop-out within the vessel under study, with a consequent overestimation of the degree of stenosis. This represents an important limita- tion in the use of standard 2D- and 3D-TOF MR angiographic techniques.
The recent introduction of CE 3D-TOF MRA has resolved certain problems concerning the correct estimation of the degree of vascular stenosis and the evaluation of the origins of the supraaortic vessels (Fig. 1.89). Recent studies have shown the CE 3D-TOF technique to be more accurate than standard 2D- and 3D-TOF acquisitions (14, 23).
Stenotic-occlusive atheromatous pathology The 3D-TOF MR angiographic technique is currently considered the best available method for defining the morphology of stenotic-occlu- sive lesions of the carotid and vertebral arteries.
To avoid problems with the progressive satura- tion of the spins when using 2D- and 3D-TOF techniques, one should preferably use an acqui- sition plane perpendicular to the longitudinal axis of the vessel being examined; consequent- ly, both the carotid and the vertebral arteries must be examined in the axial plane (Fig. 1.90).
The 3D-TOF technique can also be used with a bolus injection of a contrast agent (gadolini- um), using rapid volumetric acquisitions in the coronal plane (Fig. 1.91). The disadvantage of this technique is in its slightly invasive nature (linked to the intravascular administration of gadolinium) and in its limited spatial resolution as compared to the traditional 3D-TOF method utilizing a transverse plane acquisition.
For stenoses greater than 70%, a signal drop- out at the stenotic segment is described in both the 2D- and 3D-TOF MR angiographic tech- niques. In cases of preocclusive high grade
Figs. 1.87-1.88 - Dynamic MRA scan of the epiaortic vessels acquired in the coronal plane with high definition ultrafast T1 sequences (AT: 28 seconds); note the excellent demarcation from the emergence of the epiaortic vessels.
stenosis, the 2D-TOF technique may prove more effective than the 3D because its sensitivi- ty to slow flow makes it possible to identify residual flow distal to the narrowing, whereas the 3D technique can give an erroneous picture of occlusion with a complete absence of distal flow signal.
Vascular dissections
Stenotic-occlusive pathology of the internal carotid artery and the vertebrobasilar vessels is being increasingly seen as cases presenting as neurological and neuroradiological emergen- cies. With regard to ischaemic strokes, particu- lar attention must be paid to the role of dissec-
tion of the cervical arteries. These dissections are often under recognized as they typically af- fect young patients who commonly lack the usual vascular risk factors (2%).
Increased diagnostic suspicion is often sug- gested by the appearance of headache, stiff neck, neck pain, Horner’s syndrome and dizzi- ness in the dissection of the vertebral artery.
Carotid and vertebral dissections can be diag- nosed with relative ease using simple MR and MRA acquisitions (Fig. 1.92) (20). Levy et al (12) reported a sensitivity and specificity of 95% and 98%, respectively, for the detection of cervical internal carotid dissection.
Both T1- and T2-weighted spin echo (SE) images and the single partitions of 3D-TOF MRA permit the detection of the character- istic findings of vascular dissection, includ- ing the presence of a flow void in the resid- ual lumen and haemoglobin hyperintensity within the subintimal haematoma. An alter- native to the TOF method is a combination of PC MRA and a comparative T1-weighted SE study with suppression of the fat signal for the effective visualization of the intramu- ral thrombus.
With regard to dissections of the vertebral artery, although MR angiography is less sensitive than that of the internal carotid artery, it is felt to be preferable to invasive selective conven- tional DSA as the double lumen caused by the subintimal dissection can cause the detachment of emboli in patients undergoing catheteriza- tion.
MR angiography plays an important role in the follow-up of these lesions, which usually successfully heal after treatment with anticoag- ulants.
INTRACRANIAL VESSELS Technique
The most frequently used technique for studying the intracranial vessels is 3D-TOF MRA. The acquisition volume is oriented trans- versally and covers the vessels of the circle of Willis and the proximal segments of the major
Fig. 1.89 - Dynamic CE MRA: presents a serrated stenosis of the right subclavian artery and a stenosis on the bifurcation of the right carotid artery.
Fig. 1.90 - Dynamic MRA: a) panoramic study of the epiaortic vessels; b) selective reconstruction of the left carotid bifurca- tion, which appears normal; c) selective reconstruction of the right carotid bifurcation in which one can observe the pres- ence of an atheromasic plaque at the beginning of the right in- ternal carotid artery. d) comparative study of the right carotid bifurcation with 3D-TOF technique and axial acquisitions:
note a reduction in flow signal by the plaque; echo-Doppler finding: soft stenosing plaque at the origin of the right internal carotid artery.
a
c
d
b
cerebral arteries; in order to obtain good spatial and contrast resolution, the thickness of the in- dividual scans must be relatively small (0.8 - 1.5 mm). Optimal intravascular contrast is ob- tained using the variable flip angle technique
(TONE) coupled with transverse magnetiza- tion transfer (MTC) overlay for better suppres- sion of the perivascular stationary tissue signal (4, 16). For the separate study of the arterial and venous systems, it is necessary to correctly position prespatial saturation bands proximal to the flow signal to be eliminated.
In general, contrast agents are not used for studying the cerebral vessels, with the excep- tion of certain cases where the intracranial pathology demands that intravascular contrast material be specifically used for the study of slow vascular flow.
CLINICAL APPLICATIONS Stenotic-occlusive pathology
In recent years the development and clini- cal application of MRI in the study of is- chaemic stroke patients has provided much in- formation on cerebral perfusion (perfusion MR), metabolic integrity (spectroscopy MR), variations in cerebral diffusion coefficients (DWI) and information on the morphology of the intra- and extracranial vessels using MR angiography (2, 25).
In cases of ischaemic stroke, MR angiography plays a potentially important role. In the hypera- cute phase of cerebral ischaemia, integrating the morphological and metabolic imaging informa- tion in cases of vascular stenosis or occlusion provides all the data required to make specific therapeutic choices (Figs. 1.93, 1.94).
MR angiography provides a good represen- tation of the first and second order vessels of the circle of Willis, but has limitations in the study of smaller vessels (Figs. 1.95, 1.96, 1.97, 1.98). In addition to spatial definition, limita- tions include an accurate estimation of the de- gree of high grade stenoses and the accurate distinction between high grade stenoses and frank occlusions (8, 11).
The carotid siphon can benefit from an MR angiographic evaluation, although care must be taken to avoid errors in overestimation of the pathological changes due to the reduction in flow signal as a result of turbulence. Another problem is posed in some cases by the flow tur-
Fig. 1.91 - Dynamic MRA scan of the epiaortic vessels: a) steno- sis on the bifurcation of the right carotid artery and occlusion at the start of the left internal carotid artery; b) the specific study using the 3D-TOF technique better demarcates the pres- ence and entity of the stenosis at the start of the right external carotid artery.
a
b
bulence present at vascular bifurcations, which can erroneously be interpreted as stenoses. The administration of contrast media (gadolinium) has been used to resolve these problems of par- tial signal loss.
Collateral pathways to the circle of Willis can be evaluated using the 3D-TOF technique by means of an appropriate arrangement of the selective prespatial saturation pulse; an alterna- tive is the PC method that provides informa- tion on the direction of blood flow (25).
Occlusive venous pathology
With suspected venous thrombosis, MR venography is the diagnostic examination of choice. This technique is used together with the conventional SE MR scan, which permits the detection of associated parenchymal abnormal- ities (e.g., venous infarction) as well as the ab- normal signal of vascular thrombosis or the ab-
Fig. 1.91 - (cont.) – c) Another case, medium grade stenosis on the right carotid bifurcation and serrated stenosis with presence of plaque at the beginning of the left internal carotid artery; d and e) selective reconstruction of the carotid bifurcations.
c
d
e
Fig. 1.92 - Dissection of the left vertebral artery. a) Basic SE T2 MR scan: left cerebellum ischaemic lesion; b and c) MRA: ab- sence of signal in the last stretch of the left vertebral artery;
d) single base partition: presence of hypointense parietal thrombus, in acute phase, at the vertebral artery; e) check-up MRA (15 days later): partial recanalization of the vessel.
a
b
c
d
e
Fig. 1.92 - (cont.) f) Comparison with DSA.
f
a
b
c
Fig. 1.93 - Hyperacute phase ischaemia. a) Basic SE T2 MRI:
negative finding; b) DW MR image; ischaemic lesion in left insu- lar-parietal location; c) MRA of the vessels of the circle of Willis:
occlusion of the bifurcation of the left Sylvian artery.
sence of normal signal void within the dural ve- nous sinuses. Toward this same aim, T2-weight- ed SE images acquired perpendicular to the dural venous sinuses are recommended for a more accurate supplemental study.
In MR angiography, the high signal of the thrombus can give false negative results; in such cases a comparative study using T1- and T2-weighted SE images and the application of presaturation bands, as well as use of the PC tech-
Fig. 1.94 - Hyperacute phase ischaemia. a) and b) TSE-HASTE images, a blurred swelling caused by the oedema of the cortex in a right parasagittal frontal position with small hyperintensities near the signal; c and d) DW images: widespread ischaemic focus in the territory of the right anterior cerebral artery.
c
d a
b
nique are in combination typically able to dis- pel diagnostic doubts (17).
Aneurysms
In the acute stage of subarachnoid haemor- rhage, the examination of choice is CT, followed by invasive conventional selective DSA to reveal the presence of one or more aneurysms and to visualize the anatomy of the individual aneurysms; MRI and MRA have sec- ondary roles during this acute phase.
MRA is the examination technique of choice for screening patients with family histories of
such potentially heritable pathology as the aneurysms associated with polycystic kidney disease, or in cases where there is a relatively high association of aneurysms such as aortic coarctation (21). Studies performed thus far show that MRA is able to detect 3-4 mm aneurysms with approximately 86-90% sensi- tivity, and with 100% specificity (3, 10) (Fig.
Fig. 1.94 - (cont.) e and f) MRA of the vessels of the circle of Willis: occlusion at the start of the right anterior cerebral artery and serrated stenosis in segment M2 of the right Sylvian artery.
Fig. 1.95 - Left insular-temporal-parietal ischaemic lesion: a) ba- sic SE T2 MRI; b) 3D-TOF MRA of the vessels of the circle of Willis; occlusion in segment M2 of the left Sylvian artery.
e
f
b
a
1.99). Smaller aneurysms are often not visible due to MR angiography’s limited spatial resolu- tion and because of the irregular flow dynamics within small aneurysms. And, when studying giant aneurysms the slow and turbulent flow can reduce the intraluminal signal and cause an
underestimation of the dimensions of the lu- men of the aneurysm.
3D-TOF MRA has recently been used in studying aneurysms treated with Guglielmi’s
Fig. 1.96 - Left temporooccipital ischaemia: a) basic SE T2 MRI;
b) MRA of the vessels of the circle of Willis: occlusion in the P1 segment of the left posterior cerebral artery.
Fig. 1.97 - Right parietal ischaemia: a) basic SE T2 MRI; b) 3D- TOF MRA of the vessels of the circle of Willis: absence of flow signal in the right carotid siphon with partial revascularization of the right Sylvian artery through the circle vessels.
b a a
b
Fig. 1.97 (cont.) - c) MRA of neck vessels: occlusion at the be- ginning of the right internal carotid artery.
Fig. 1.98 - a) Basic SE T2 MRI; blurred signal hyperintensity in right occipital location; b) SE T1 image after gadolinium: non- homogeneous contrast enhancement due to blood-brain barri- er damage caused by the presence of an acute ischaemic area;
c) MRA of the vessels of the circle of Willis: stenosis in the proximal segment of the right posterior cerebral artery.
c
a
b
c
detachable embolization coils. This has shown a good correspondence between MRA and se- lective DSA with regard to the evaluation of aneurysms occluded with coils. It has in fact been possible to evaluate any residual aneurysm neck and flow within the residual aneurysmatic sack if present. However, to be fair, certain vascular details are obviously less easy to evaluate in the single MRA partitions.
Arteriovenous malformations
Generally speaking, MRA used in combina- tion with MRI is sufficient for the detection of most cerebral arteriovenous malformations.
The TOF MRA technique gives good documen- tation of the major arterial feeding arteries (Fig.
1.100). Venous drainage and the central nidus are better studied using PC MRA. The use of in- travenous gadolinium improves visualization of the venous vascular components of AVM’s.
MRA also permits in-depth studies of the nidus, its dimensions and its relationship with the surrounding neural tissue, which are im- portant elements for treatment planning. This technique is also useful during follow-up after therapy; invasive selective DSA is nevertheless required in order to obtain precise images of the exact anatomical architecture and the dy- namic aspects of the AVM.
CONCLUSIONS
MRA is an important non-invasive method for studying the brachiocephalic and cerebral blood vessels. Its main application in neuro- radiological emergencies is for the evaluation
Fig. 1.99 - 3D TOF MRA of the vessels of the circle of Willis:
presence of an aneurysm on the anterior communicating artery.
b a
Fig. 1.100 - AVM: a) basic SE T2 MRI: numerous serpigenous images with signal void in the left temporoparietal region; b) 3D TOF MRA: presence of a large AVM, supplied by branches orig- inating from the Sylvian artery and left posterior cerebral artery.
of cerebral circulation in suspected cases of ischaemic stroke or thrombosis of the dural venous sinuses. In such cases, MRA can be performed together with conventional MRI aimed at obtaining a rapid and complete di- agnostic analysis of the problem, thereby al- lowing optimal specific treatment choices to be made. It is also widely used to screen for cerebral aneurysms in high risk groups, and more recently to monitor aneurysms follow- ing treatment with Gugielmi’s detachable em- bolization coils.
It is important to underline the importance of having access to high performance MRI sys- tems that allow the rapid execution of both the static conventional imaging as well as the an- giographic acquisitions.
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