New MR sequences in daily practice: susceptibility weighted imaging. A pictorial essay
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Susceptibility-weighted imaging (SWI) is a relatively new magnetic resonance (MR) technique that exploits the magnetic susceptibility differences of various tissues, such as blood, iron and calcification, as a new source of contrast enhancement. This pictorial review is aimed at illustrating and discussing its main clinical applications.
SWI is based on high-resolution, three-dimensional (3D), fully velocity-compensated gradient-echo sequences using both magnitude and phase images. A phase mask obtained from the MR phase images is multiplied with magnitude images in order to increase the visualisation of the smaller veins and other sources of susceptibility effects, which are displayed at best after post-processing of the 3D dataset with the minimal intensity projection (minIP) algorithm.
SWI is very useful in detecting cerebral microbleeds in ageing and occult low-flow vascular malformations, in characterising brain tumours and degenerative diseases of the brain, and in recognizing calcifications in various pathological conditions. The phase images are especially useful in differentiating between paramagnetic susceptibility effects of blood and diamagnetic effects of calcium. SWI can also be used to evaluate changes in iron content in different neurodegenerative disorders.
SWI is useful in differentiating and characterising diverse brain disorders.
KeywordsBrain Magnetic resonance imaging Susceptibility weighted imaging
Susceptibility weighted imaging (SWI) is a relatively new magnetic resonance (MR) technique that provides innovative sources of contrast enhancement visualising the changes in magnetic susceptibility that are caused by different substances like iron, haemorrhage or calcium. The basic concept of this technique is maintaining phase information into the final image, discarding phase artefacts and keeping just the local phase of interest.
Sensitivity to susceptibility effects increases, progressing from fast spin-echo (SE) to conventional SE to gradient-echo (GE) sequences, from T2-weighting to T2*-weighting, from short to long echo times and from lower to higher field strengths. Before the clinical implementation of SWI, susceptibility imaging relied only on GE sequences. SWI differs significantly from a T2*-weighted GE sequence: it is based on a long echo time (TE) high-resolution, flow-compensated, three-dimensional (3D) GE imaging technique with filtered phase information in each voxel. The combination of magnitude and phase data produces an enhanced contrast magnitude image that is particularly sensitive to haemorrhage, calcium, iron storage and slow venous blood, thus allowing a significant improvement compared with T2* GE sequences. After imaging acquisition, incidental phase variations due to static magnetic field heterogeneities are removed. The phase mask is then multiplied with the magnitude data to enhance the visualisation of vessels or foci with susceptibility effects . SWI is therefore especially helpful in the detection of calcifications and microhaemorrhages, which are both characterised by low signal. The evaluation of the corrected phase images allows the differentiation between the two substances, as calcifications appear bright because of a positive phase shift and haemorrhages appear dark because of a negative phase shift.
A supplementary source of information in SWI is primarily associated with the magnetic susceptibility differences between oxygenated and deoxygenated haemoglobin. SWI represents a technical improvement in “high-resolution blood oxygenation level-dependent venography” (HRBV), originally developed by Reichenbach et al. , which was based on 3D long TE, flow-independent GE sequences and manipulation of the images with the phase data. The paramagnetic properties of deoxyhaemoglobin [BOLD (blood oxygen level dependent) effect] and the prolonged T2* of venous blood were used as an intrinsic contrast agent, leading to a phase difference between vessels containing deoxygenated blood and surrounding brain tissue, resulting in signal intensity cancellation. Thus, deoxyhaemoglobin can behave like a contrast agent with long TEs for differentiating arteries from small veins, which can be as small as 100–200 μm and therefore difficult to detect with conventional MR angiography techniques, such as time of flight (TOF) or phase contrast (PC) . For this reason, the phase-added information that is usually not available in the conventional magnitude image makes SWI well suited for the visualisation of very small vessels such as the caput medusae of venous angiomas and telangiectasias as a result of a combination of slow flow with changes in deoxyhaemoglobin concentration .
Latest advances have allowed the technique to be refined, thereby expanding its clinical applicability to brain imaging as a complementary source of information to conventional T1-weighted and T2-weighted imaging sequences.
This pictorial essay is aimed at showing the most relevant clinical applications of SWI.
At our institution, MR imaging (MRI) is performed by using a 1.5-T system (Magnetom Avanto; Siemens, Erlangen, Germany) with a 12-channel head coil. SWI is obtained with a long-TE, fully flow-compensated 3D GE sequence with the following parameters: repetition time (TR)/TE, 49/40 ms; flip angle, 15°; rectangular field of view (FOV), 7/8; matrix size, 280 × 320; slice thickness, 1.6 mm (80 slices in a single slab matrix size); iPAT factor, 2; acquisition time, 5 min. Images are acquired in the axial plane parallel to the bicommissural line.
SWI sequences have some intrinsic disadvantages, which are mainly represented by artefacts caused by undesirable sources of magnetic susceptibility that occur at air–tissue interfaces, therefore limiting the investigation of areas next to paranasal sinuses and temporal bone. The “blooming artefact”, useful in most cases, might also not be needed in some situations, producing normal tissue signal cancellation and loss of anatomical borders. The sequence acquisition time on a 1.5-T system ranges from 5 to 8 min, depending on the spatial resolution and the coverage of the brain needed, leading to an increased incidence of movement artefacts.
Imaging at a high field strength has some advantages over 1.5 T in the delineation of even smaller vessels belonging to the venous network, with shorter imaging times because of the higher signal-to-noise ratio, higher spatial resolution and increased susceptibility effects . However susceptibility-based signal loss and severe image distortion caused by air–tissue interfaces or other sources of local field heterogeneity are much more severe at higher fields, thus reducing SWI’s usefulness in the evaluation of the posterior fossa and skull base.
Cerebral amyloid angiopathy
Sporadic cerebral amyloid angiopathy (CAA) is a common small-vessel disease associated with ageing, dementia and Alzheimer’s disease, that can only be diagnosed histopathologically following biopsy or at post-mortem examination. It consists of deposition of amyloid protein within the small and medium-sized cerebral arteries, which is likely responsible for increased vessel fragility and it is one of the major causes of lobar intraparenchymal haemorrhages in the elderly .
Computed tomography (CT) and conventional MR techniques are usually unable to show cerebral microbleeds (CMBs), which can be frequently observed on T2*-weighted gradient-echo MRI and have a typical lobar distribution . Recent findings indicate that CMBs in the general elderly population are relatively common and are even more frequently observed in patients with AD .
CAA is also characterised by white matter hyperintensities on conventional MRI sequences, which have been associated with cognitive impairment . Vascular amyloid deposition is believed to be involved in the pathophysiological mechanisms that determine white matter hypoperfusion through either vessel stenosis or vascular dysfunction .
CAA should also be suspected in elderly patients with clinical signs of a progressive encephalopathy syndrome with seizures, in which extensive white matter abnormalities are discovered in brain MRI together with multiple CMBs with lobar and subcortical distribution (Fig. 2). It has been recently reported that this combination of MR findings should be interpreted as CAA-related inflammation, which can be treated with steroid therapy with a prompt resolution of the symptoms . In those cases, the demonstration of an APoE ɛ4ɛ4 genotype can definitely support the neuroradiological diagnosis. Hypertensive encephalopathy and especially posterior reversible encephalopathy syndrome (PRES), when the signal abnormalities of the white matter are more symmetrical and located in parieto-occipital regions, should be taken into consideration for differential diagnosis.
Iron deposition increases in the brain as a function of age, primarily in the form of ferritin and particularly in oligodendrocytes, but also in neurons and microglia. Typical sites of iron deposition include the globus pallidum, substantia nigra, and red and dentate nuclei. Ferritin is paramagnetic and produces strong susceptibility effects on T2*-weighted images. SWI filtered-phase images are particularly suitable for showing increased iron content in the brain (. Abnormally elevated iron levels are evident in many neurodegenerative disorders, including Parkinson’s disease, Alzheimer’s disease, Huntington’s disease and amyotrophic lateral sclerosis.
The ability to measure the amount of ferritin in the brain can be used for a better understanding of the progression of the disease and is also helpful in predicting the treatment outcome.
Phase images allow a better distinction between the pars compacta and the pars reticulata of the substantia nigra, which contains iron (Fig. 1). As in patients with idiopathic Parkinson’s disease, there is evidence of increased iron in the substantia nigra , SWI sequences can be proposed as a useful imaging tool to identify iron deposition as a biomarker for disease progression, although longitudinal studies are required to support the usefulness of this specific application . Accurate localisation of the subthalamic nucleus can also be achieved in the SWI phase maps at 3 T, allowing safe direct targeting for placement of electrodes in the treatment of Parkinson’s disease .
SWI has been demonstrated to be very useful in the acute phase of stroke for several reasons. First of all, it is very sensitive to the presence of CMBs, whose early identification is believed to predict the probability of potential haemorrhagic transformation after thrombolytic treatment . It has also been hypothesised that CMBs can represent a link between cerebral haemorrhage and ischaemia .
SWI is also capable of identifying the acute intravascular clot in the main and distal branches of the cerebral arteries .
Cerebral venous sinus thrombosis
Cerebral vascular malformations
Cerebral arteriovenous malformations (AVMs) are easily displayed by conventional MRI and MR angiography because of their characteristic high flow, whereas venous malformations such as cavernomas, developmental venous anomalies and capillary telangiectasias cannot be adequately visualised without contrast medium administration and GE sequences, as they mainly consist of slow-flow small vessels. MR angiography techniques are often inadequate for visualising small vessels with slow flow. On the contrary, SWI sequences are well suited for the visualisation of very small vessels, such as the caput medusae of venous angiomas and telangiectasias as a result of a combination of slow flow with changes in deoxyhaemoglobin concentration . The combined information derived from both phase and magnitude images is responsible for enhanced visualisation of such lesions.
SWI plays a substantial role in the identification and characterisation of cerebral vascular malformations, first of all improving their detection rate. On the other hand, allowing simultaneous visualisation of the different compartments of cerebral AVMs and of the relationship with one another and with the brain parenchyma, it is particularly valuable for therapeutic planning. The clinical usefulness of a similar technique, BOLD MR venography, was first demonstrated by Essig et al. .
Concerning slow-flow vascular malformations (i.e. cavernomas, developmental venous anomalies and capillary telangiectasias) the phase information contained in SWI is responsible for an artefactual enhancement that dramatically improves MRI sensitivity to these pathological conditions. Without SWI, small vascular malformations could be entirely missed by conventional imaging techniques .
Capillary telangiectasias are asymptomatic venous vascular malformations, which are smaller and less common than cavernomas and can sometimes occur in mixed cavernoma/telangiectasia lesions. These may occur sporadically or may be infrequently associated with syndromes, like hereditary haemorrhagic telangiectasia or ataxia telangiectasia. They may also manifest as a result of endothelial injury, such as radiation-induced vascular injury, particularly in children who have received cranial irradiation.
Traumatic brain injuries
Brain MRI predictors of tumour grade include contrast enhancement, oedema, mass effect, cyst formation or necrosis, haemorrhage, metabolic activity and cerebral blood volume. It is well known that the growth of solid tumours, such as gliomas, is dependent on the angiogenesis of pathological vessels. SWI can provide a thorough assessment of the internal angioarchitecture of brain tumours (increased microvascularity inside and beyond the tumour margins), together with the identification of foci of haemorrhage and calcification, thus representing an additional tool in the neuroradiological grading of cerebral neoplasms. The administration of a contrast agent (CE-SWI) allows discrimination among those three entities, as only blood vessels will change their signal intensity, while calcifications and regions of inactive haemorrhage (which can be differentiated from each other by the evaluation of phase images, as described above) will not. The clinical potential of contrast-enhanced BOLD MR venography at 3 T and 1.5 T for the study of brain tumours was first reported by Barth et al. , who demonstrated variable venous patterns in various types of tumours and in different parts of the lesions (oedema, contrast-enhancing areas, necrosis), which might represent increased blood supply and particular vascular patterns around fast-growing malignant tumours.
Pinker et al.  demonstrated a correlation between intratumoural susceptibility effects, positron emission tomography (PET) results and histopathological grading. SWI has been proposed in the evaluation of clinical response to anti-angiogenetic drugs and in the differential diagnosis with pseudo-progression after chemo- and radiotherapy . A correlation with MR PWI has also been attempted . However, larger comparative studies of PWI and SWI are still needed to determine a more precise role of the new techniques in the grading of cerebral neoplasms.
SWI, which is a combination of GE techniques with phase information, represents a useful tool for the identification and characterisation of vascular malformations and for a better understanding of cerebrovascular diseases. Despite some inherent limitations, SWI has increasing indications for neuroradiology and should be included in the routine imaging protocols of trauma and vascular abnormalities. Further investigation is still needed into its extensive clinical application in neurodegenerative diseases and tumoural pathological conditions.
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