InvestIgatIons

Neuroradiology
J v Byrne

Whats new?
new multislice Ct scanners are used for Ct angiography, which is rapidly replacing catheter angiography Diffusion-weighted MRI enables reliable, ultra-fast diagnosis of ischaemic stroke there is an increasing trend to tailor MRI sequences to specific pathologies

Abstract
advances in neuroradiology, like most medical imaging specialties, are driven by technical improvements and clinical refinements of investigation paradigms. technically, the emphasis has always been to improve image quality whilst reducing the use of ionizing radiation. this has led to a greater reliance on computer post-processing of the images and use of modalities that do not involve ionizing radiation, such as MRI and Doppler ultrasound. In the last few years sub-specialization of neuroradiologists has occurred with specialists in paediatric neuroradiology, head and neck imaging, and interventional neuroradiologists emerging from a reducing number of generalists. this chapter describes in detail the main imaging modalities used in clinical practice. the intention is to show how each technology is deployed for investigations and treatments. the emphasis is on helping the reader to understand which is the most appropriate type of imaging in different circumstances,when contrast enhancement of scans is needed (and when it is not) and how different modalities frequently complement each other. the more infrequently used techniques are set in context within neuroradiology and specialist functional imaging and research imaging are briefly described.

Computer reconstructions of digitalized MRI and radiographic images provide on-screen displays in three dimensions

CT
Since its introduction in the mid-1970s, CT has been the mainstay of neuroradiological diagnosis. Its role has evolved in the last decade with the introduction of faster multislice scanners, which generate considerably more data than previous machines, allowing better-quality three-dimensional (3D) image displays. Technique The basic principle of CT involves rotating an X-ray source and a series of detectors around the patient and making multiple measurements of radiation attenuation. The measured attenuation (amount of radiation absorbed) by small volume-elements (voxels) of the subject is calculated by computer and used to build a two-dimensional (2D) picture composed of a matrix of pixels. Each pixel is assigned a grey-scale value (in Hounsfield units), which is based on the measured attenuation and therefore reflects the density of the scanned tissue. Hounsfield units, named after the inventor of CT, are scaled with the attenuation value of water set at zero and maximum density +1000 and minimum density 1000. High-density structures (e.g. bone or calcification) are depicted in white and low-density tissues (e.g. air) in black; intermediate densities are depicted in grey. By this means, the inherent contrast resulting from density differences between tissues is displayed on a cross-sectional image (Figure 1). In order to obtain non-axial views it was previously necessary either to alter the patients position or angle the scanner gantry. The extent to which the latter can be achieved was limited by the engineering of the scanner. The problem has been solved by spiral scanning and the introduction of multiple detector systems. The original scanners collected data for each 2D slice in a single 360 rotation using a single detector. Multiple 2D images could be re-assembled by computer reconstruction to obtain images in 3D displays but the quality was relatively poor. Current scanners move the X-ray source and patient simultaneously, and scan in a helical pattern to produce volume data images in seconds. These speeds are achieved using multiple detectors, which collect data as they move. Current multidetector scanners employ up to 64 detectors and can scan the entire brain in less than 3060 seconds. These speeds reduce artefacts caused by the patient moving and are fast enough to scan during the first pass of a bolus of intravascular radiographic contrast media. This has been a major advance for neuroradiology.
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Keywords angiography; computerized tomography; magnetic resonance

imaging Doppler ultrasound; myelography; perfusion imaging; positron emission tomography; radionuclide scanning

Neuroradiology uses planar scanning, i.e. computerized tomography (CT) and magnetic resonance imaging (MRI), alone or in combination, to identify most central nervous system (CNS) pathologies. Traditional radiographic techniques (e.g. plain radiography, myelography and angiography) are now secondline modalities. Skull radiography has a role in the emergency department, but not in general medical or neurology out-patient departments. Myelography with intrathecal injection of radiographic contrast media is now reserved for patients who are unable to undergo MRI because of implants (e.g. cardiac pacemakers) or extreme claustrophobia, and is generally used in combination with CT. Techniques such as Doppler ultrasound (carotid, transcranial and intra-operative), radionuclide scanning and functional MRI have specific indications and are important research tools with limited roles in routine practice.

J V Byrne FRCS FRCR is Consultant Neuroradiologist at the John Radcliffe Hospital and Professor of Neuroradiology at the University of Oxford, UK. His specialist interests are cerebrovascular disease and interventional neuroradiology. Competing interests: none declared.

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Frontal horn

Cyst

Cyst Calcification Figure 1

Axial CT scan without contrast, showing calcification in an oligodendroglioma that was found to be partially cystic at surgery. The calcification was not evident on MRI

CT with contrast media A water-soluble iodine-containing agent is injected intravenously and accumulates in areas of bloodbrain barrier breakdown. Contrast agents are used to highlight tumours and areas of inflammation (e.g. meningitis, abscesses). The effect of uptake by a lesion is to increase its density so that it appears brighter (relative to the surrounding brain). This is termed enhancement and reflects the vascularity of the tissues, i.e. it is increased in vascular tumours and reduced in areas of infarction. Contrast media can also be injected into arteries as well as veins to show vessels, i.e. angiography, or intrathecally by lumbar puncture to show the spinal cord, i.e. myelography. CT is then used to image the structures outlined by the density differences within the injected body compartment. This is the principle of traditional radiographic myelography which CT has replaced because it is more sensitive than X-ray film and CT angiography (CTA). The images are acquired as digital 3D data, which makes their interpretation easier (Figure 2).

Fast scanning during injections allows the rate of contrast uptake by a tissue to be measured and is the basis of perfusion scanning. This technique is used to estimate blood flow and blood volume within tissues by comparing time/density curves between different parts of the brain. It is used to identify areas of under-perfusion after stroke.

MRI
MRI is now the modality of choice for the investigation of most neurological disease because it does not use ionizing radiation and is extremely sensitive to small changes in tissue water content (Table 1). Principles of MRI In MRI, imaging is based on the phenomenon of magnetic resonance, in which elements with an odd number of subatomic particles (protons and electrons) can be induced to resonate
Nidus of arteriovenous malformation (AVM) Draining veins Haematoma Anterior cerebral arteries displaced by haematoma Middle cerebral artery

Enlarged middle cerebral artery and branches supplying AVM A coronal view of the frontal lobes (computed tomography angiography) showing a haematoma and the nidus of a brain arteriovenous malformation (AVM). The scan is performed during the passage of a bolus of radiographic contrast so that the arteries are enhanced and reconstructed by computer to produce this display. Figure 2

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InvestIgatIons

when placed in a strong magnetic field. Clinical MRI is performed at the resonance frequency of hydrogen nuclei because they are abundant in biological tissue. Resonating hydrogen protons are perturbed by electromagnetic energy, applied as a radiofrequency pulse. This causes the protons to emit a weak signal, which is detected, amplified and, after computer processing, used to construct an image. Different tissues contain different amounts of hydrogen (largely in water) in various molecular environments; the appearance of the image depends principally on the concentration and molecular environment of the perturbed hydrogen protons and the applied radiofrequency pulse.

The appearance of the image can be changed by manipulating the radio-frequency pulse, using electronic protocols (termed sequences). The parameters commonly measured are T1, T2 and T2* relaxation times (Figure 3), Images relying principally on contrast produced by T1 relaxation are termed T1-weighted (T1 W) and show cerebrospinal fluid (CSF) darker than the brain. These sequences are designed to show the anatomical detail of the brain and spinal cord. They are used with contrast enhancement for similar indications to CT. The contrast medium used in MRI is a paramagnetic substance, such as gadolinium, which alters the

Head of caudate nucleus Lentiform nucleus (comprising putamen, globus, pallidius) White matter of frontal lobe Frontal horn of lateral ventricle Subcutaneous fat Sulci of Sylvian fissure

Head of caudate nucleus External capsule Internal capsule Lentiform nucleus

External capsule

Sylvian fissure

Thalamus Third ventricle

Thalamus

Trigone region of lateral ventricle Interhemispheric fissure and falx Posterior partition of lateral ventricle (trigone)

a Axial T2W and b T1W MRI showing the basal ganglia.

Figure 3

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Differential diagnosis using MRI

Multifocal white matter (high-signal) lesions on T2-weighted sequences Multiple sclerosis Infections progressive multifocal leucoencephalopathy, Lyme disease, opportunist infections Inflammatory acute disseminated encephalomyelitis, sarcoidosis, chronic inflammatory polyneuritis Cerebrovascular disease migraine, toxaemia of pregnancy, subacute atherosclerotic encephalomyelitis vasculitis granulomatous, systemic necrotizing, rheumatoid neoplasm metastasis toxic pontine myelinolysis, postradiation change

Materials returning high signal on T1-weighted sequences

Fat (including fat-containing tumour products) subacute haematoma (methaemoglobin) Melanomas (melanin is paramagnetic) Flowing blood on some sequences Paramagnetic contrast agents (e.g. gadolinium)

magnetic properties of blood and appears brighter on T1 W images (Figure 4). Water (and therefore CSF) appears white on T2-weighted (T2 W) images. T2 W images are very sensitive to increases in cerebral water, which occur in most inflammatory and neoplastic diseases of the CNS. Cerebral white and grey matter can be distinguished because of differences in their water and fat content. T2 star (T2*) is the term used to describe the effects on the scan of molecules with inherent magnetic properties. The best example is the iron contained in haemoglobin (Hb). After acute haemorrhage, the magnetic resonance signal from a blood clot is affected by the extravasated Hb. The magnetic effect, termed susceptibility, causes local differences (inhomogeneities) in the magnetic gradient and loss of signal. T2*-weighted sequences are sensitive to any magnetic field inhomogeneity and are best at showing the effects of both acute and chronic cerebral haemorrhage (Figure 5). Hydrogen protons in bone or in areas of calcification return little signal and therefore appear dark on both T1 W and T2 W sequences. MRI is not as sensitive to brain calcification as CT. MRI sequences and techniques A typical brain scan comprises several sequences designed to image the brain in three orthogonal planes using a combination of sequence types. The spine is imaged in the sagittal plane with axial scans at levels of interest. Any plane of scan can be designated on MRI (unlike CT). Contrast medium (e.g. gadolinium)

Table 1

Trigone of lateral ventricle

Enhanced lateral sinus a

Enhancing component of cerebellar tumour

Non-enhancing cystic element of cerebellar tumour a Saggital T1-weighted MRI after administration of intravenous gadolinium. A cystic cerebellar tumour shows partial enhancement. b Magnetic resonance angiography enhanced with gadolinium and reconstructed in the axial plane. The tumour is only moderately vascular. This was confirmed at surgery; histological examination revealed a cerebellar astrocytoma rather than a more vascular haemangioblastoma.

Basilar artery Jugular bulb

Posterior communicating artery Internal carotid artery Posterior cerebral artery

Sigmoid sinus Lateral sinus Torcula

Tumour in cerebellar hemisphere without evidence of vessel hypertrophy

Figure 4

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Vasogenic oedema surrounding haematoma Signal loss due to magnetic effect of acute haematoma

Third ventricle containing cerebrospinal fluid Internal cerebral veins

Early low signal rim to haematoma due to haemosiderin Vasogenic oedema Bright centre of subacute/chronic haematoma Anterior cerebral arteries

Falx

b a Axial T2 W MRI showing an acute haematoma in the frontal lobe. The centre of the haematoma contains deoxyhaemoglobin which distorts the magnetic field locally and reduces the signal return. This results in a dark area on the image. b is the same patient scanned 2 weeks later when the effect has reduced as the clot breaks down and the centre now returns a higher (brighter) signal. Figure 5

is administered intravenously to highlight tumour and inflammatory lesions that have interrupted the bloodbrain barrier (Figures 4 and 6). CSF signal-suppressing sequences: Since T2 W sequences are best for demonstrating focal lesions causing increases in cerebral water, lesions in the periventricular brain (e.g. multiple sclerosis) may be obscured by the high signal returned by adjacent CSF. A fluid low-attenuation inversion recovery (FLAIR) sequence was developed to show periventricular plaques because it produces a T2 W image with dark CSF but has proved to have wider uses including tumour follow-up (Figure 7). It is usually included in a standard brain scan protocol.
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Fat-suppression sequences: Fat appears bright on standard T1 W and T2 W sequences. Sequences that suppress the fat signal are used to investigate suspected fat-containing tumours and lesions in areas containing fat (e.g. the orbit, Figure 8). Diffusion-weighted MRI: Physiological and pathological changes in the Brownian motion of water in the cellular and extracellular compartments of tissue can be distinguished by diffusionweighted MRI. These movements are detected on ultra-fast scans which measure the rate and direction of water diffusion. Acute cell swelling after ischaemic stroke (due to cytotoxic oedema) restricts normal diffusion. DWI scanning can demonstrate this change and can demonstrate hyperacute infarction (Figure 9),

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Anterior falx

Tumour Optic tract Mid-brain

Enhancement of tumour

Corpus callosum Straight sinus (enhanced)

Tumour arising from planum sphenoidale Mid-brain Pituitary gland Pons c Sphenoid air sinus

Axial T1W a and b and sagittal c MRI showing a tumour which enhances after intravenous gadolinium injection b and c. This is a meningioma which has grown from the anterior margin of the pituitary fossa. Note how the pituitary gland is bright c because it is outside the bloodbrain barrier and, therefore, also enhances. Figure 6

before changes are detectable on CT. It is also used to distinguish brain abscesses from tumours since pus in the former is associated with restricted diffusion, which is not seen in areas of tumour-induced vasogenic cerebral oedema. Functional MRI: Sequences that allow production of images in less than 1 second can be used to perform dynamic scanning and real-time imaging. Fast-scanning techniques such as echoplanar
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imaging can show areas of increased brain activity and are used in functional MRI for research and to locate eloquent areas of the brain in patients before neurosurgery. Perfusion imaging techniques (i.e. scanning immediately after an intravenous injection of contrast medium) is used with DWI so that reduced perfusion (i.e. contrast uptake) can be compared with areas of restricted diffusion on DWI to identify ischaemic brain that is potentially salvagable brain after stroke.

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Demyelination CSF in frontal sulci

Lateral ventricle

Lateral ventricle Demyelination Demyelination

CSF in interhemispheric fissure

a Sagittal T2-weighted and b axial fluid low-attenuation inversion recovery MRI in a patient with multiple sclerosis. In a, plaques of demyelination return high signal (bright), as does CSF. The sequence used in b is designed to show plaques as high-signal lesions, but with low signal returned by CSF. The resulting image clearly shows areas of demyelination, against dark CSF in the adjacent ventricles.

Figure 7

Magnetic resonance spectroscopy (MRS): Since the MR signal reflects the chemical composition of tissue it can measure cerebral metabolites. This is done by producing a display showing the frequency spectrum of chemical composition of an area of tissue. MRS is used in various specific clinical situations (e.g. to distinguish radionecrosis from recurrent neoplasms) and to assay cerebral levels of drugs (e.g. lithium). Despite its theoretical potential, its clinical role has proved limited. Magnetic resonance angiography (MRA): Because moving hydrogen atoms in flowing blood return different signals from those in static tissue, sequences have been designed to capitalize on the effect of blood flow and highlight vessels. There are
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two types of sequence in clinical use: time-of-flight and phasecontrast. Both rely on computer post-processing of images to produce an angiogram (i.e. images showing blood vessels). They can selectively demonstrate arteries (MR arteriography) or veins (MR venography), based on the velocities and direction of blood flow, and can be used to demonstrate the patency of intracranial vessels. No injected contrast is needed, but MRA is increasingly performed after injection of gadolinium to improve the resolution of vessels and to obtain the temporal dimension. Fast scanning allows the use of 3D data collection and is now used extensively for the diagnosis and follow-up of treated vascular lesions such as aneurysms and arteriovenous malformation, and to show tumour vasculature and vessel occlusions (Figure 4).

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Frontal lobe Anterior hemispheric fissure

Orbital optic nerve surrounded by external ocular muscles Middle concha Inferior concha Maxillary sinus

Cortical grey matter Anterior corpus callosum White matter of frontal lobe Frontal horn of lateral ventricle Trigone of lateral ventricle Third ventricle Infarct in centrum semiovale

Coronal MRI of the orbits obtained with a T2-weighted sequence (hence bright CSF), showing the orbital optic nerves. The external ocular muscles can also be seen, contrasted against the low signal returned by fat on this sequence. The right optic nerve (arrow) returns the bright signal characteristic of optic neuritis. (By courtesy of P Pretorius). Figure 8

Axial diffusionweighted MRI at the level of lateral ventricles. Anatomical detail is vague compared with T1-weighted images (e.g. Figure 4b), CSF appears dark, and grey matter is lighter than white matter (note the crossing fibres of the anterior corpus callosum). This scan shows restricted water diffusion caused by infarction in the left centrum semiovale, it was performed within hours of the onset of hemiplegia.

Figure 9

When to use CT or MRI

During CT the patient is more accessible and overall scanning is quicker, thus CT is safer after recent trauma and for imaging in very ill patients.For almost all other indications brain and spine scanning uses MRI because of the absence of ionizing radiation, high sensitivity to CNS pathology and the ability to image in any plane directly. The last is especially useful when imaging the spine (Figure 10) The strong magnetic fields used in MRI can affect cardiac pacemakers and may disturb metal implants. Patients with pacemakers, some types of aneurysm clips or retained metallic foreign bodies (particularly in the eye) cannot be scanned and so they are imaged with CT. Other problems that limit the use of MRI are the claustrophobic nature of the scanner and the need for patients to remain quite still during scanning. For these reasons, sedation or general anaesthesia may be required to scan children and patients who suffer claustrophobia. Monitoring patients under general anaesthesia is more complicated during MRI than CT.
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CT is better at showing intracranial calcification (Figure 1), bone and recent intracranial haemorrhage (Figure 11), particularly subarachnoid haemorrhage, though it seems likely that the capabilities of MRI will continue to expand. Recent technical improvements in 3D scanning with CT have increased its use for angiography, especially after spontaneous intracranial haemorrhage. CT angiography has replaced emergency catheter angiography in many departments and its complementary role assures it a place in neuroradiology for the foreseeable future.

Radiographic angiography
Technique Cerebral intra-arterial angiography is usually performed by selective catheterization of the carotid or vertebral artery. Following percutaneous femoral or brachial artery puncture, a catheter is positioned under fluoroscopic control and radio-opaque contrast medium is injected rapidly. Passage of the contrast bolus through tissues from artery to vein is recorded by a series of

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L2 vertebral body

Lipoma in lumbar canal Fat-containing tract to skin dimple Dark cerebrospinal fluid S1 vertebral body

Low spinal cord

Lipoma in lumbar canal Tethered cord and filum White cerebrospinal fluid in expanded lumbo-sacral canal

b Figure 10

Sagittal T1W (dark CSF) and T2W MRI (bright CSF) of the lumbar canal in a patient with spina bifida. a A tract between the spinal canal and skin surface containing fat (therefore bright on the image) is best seen. b The spinal cord extends low into the lumbar canal and is tethered in the region of the bony defect (L5/S1).

radiographic exposures timed to show the maximum opacification of each component of the vascular tree. Subtraction of each digitized image from a baseline image (obtained before the arrival of intravascular contrast) is performed electronically, i.e. by digital subtraction angiography (DSA). This process removes details of the baseline image (i.e. cranial bone) from subsequent images so they show only the opacified vessels. Because digitized systems are sensitive to lower concentrations of contrast medium, images can be obtained following both intravenous (IV-DSA) and intra-arterial (IA-DSA) injection. Improved computer reconstruction techniques now allow 3D image post-processing in DSA. To acquire enough data for 3D displays, a technique called rotational angiography is used. This involves rotating the X-ray gantry in a similar way to CT during the injection of contrast medium. Pros and cons IA-DSA carries a risk of arterial damage caused by the catheter or inadvertent introduction of emboli. IV-DSA is therefore attractive
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because it is less likely to cause stroke, but it lacks the precision of IA-DSA. It has been replaced by CTA and MRA. MRA can provide images of adequate diagnostic quality without exposing patients to the risks associated with ionizing radiation and radiographic contrast agents. However, CT angiography is more robust, provides better bone detail and is quicker in acutely ill patients. Along with the general shift to less invasive imaging, CT and MR angiography are replacing catheter angiography for diagnosis and IA-DSA is increasingly performed only during endovascular embolization procedures for the treatment of brain arteriovenous malformations and aneurysms (Figures 2 and 12).

Plain radiography and myelography

The chest radiograph is the most important plain radiograph in neuroradiology. Spinal radiography has a limited role as a primary investigation, except after trauma. Radiographic tomography and myelography have largely been replaced by planar scanning.

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High-density haemorrhage in frontal lobe

Calcification in pineal Part of left lateral ventricle

Haemorrhage in the frontal lobe Cerebrospinal fluid in left lateral ventricle Haemorrhage in the right lateral ventricle Falx

Axial CT scan showing an acute haematoma in the right frontal lobe a. The clot is hyperdense and so appears whiter than the brain. It has extended into the adjacent ventricle b. Figure 11

Radionuclide scanning
Brain and spine scanning for the diagnosis of tumours, using radionuclides such as technetium-99m, has been generally replaced by CT and MRI. The principle of radionuclide scanning is that tissues and neoplasms concentrate a substance labelled with a radioactive isotope (i.e. a radiotracer) and the patient is scanned at a suitable interval after its injection. The technique is most commonly used to identify sites of metastatic tumour but tissue metabolism and blood flow can also be assessed with positron emission tomography (PET) and single-photon emission computerized tomography (SPECT).
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Techniques Positron emission tomography (PET) involves the detection of two high-energy photons emitted by the annihilation of a positron from a radiotracer. The radionuclides used have short halflives and a cyclotron is required to produce them; this, and the need for a dedicated detector, has previously limited its availability, but the recent introduction of networked radionuclide production and systems that are combined with a CT scanner (i.e. PET-CT) has seen an expansion in its use in oncology. Single-photon emission computerized tomography (SPECT) uses gamma ray-emitting radionuclides and can be performed using a standard gamma camera. Technetium-99m-labelled

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Pericallosal artery Aneurysm Anterior cerebral artery Middle cerebral artery Internal cerebral artery a b

Coils in aneurysm Microcatheter at the internal cerebral artery termination

2D a and c and 3D b digital subtraction angiography frontal views showing an aneurysm of the anterior communicating artery before a and c and during treatment by coil embolization. The 3D view is obtained by rotating the X-ray source during intra-arterial contrast injection and is used for pre-operative evaluation of the aneurysm and anatomy.

Figure 12

hexamethylpropylene amine oxime (HMPAO) is commonly used for scanning the brain. This substance is lipophilic and crosses the intact bloodbrain barrier to bind to unspecified receptors. Its distribution reflects cerebral blood flow and remains stable for about 1 hour, during which scanning is performed. Uses Both techniques are used to measure cerebral blood flow, but PET provides unique information about cerebral metabolism of oxygen and glucose, using oxygen-15 and fluorine-18 respectively. They are used to investigate patients with seizure disorders, dementia, neoplasms or ischaemic disease. PET research has been beneficial in the development of SPECT, and both are used to complement and validate functional MRI.

analysis and is used to evaluate the cervical carotid arteries. The Doppler principle is used to determine the velocity of blood flow based on frequency changes in a continuous sonic signal. This technique has been refined by the addition of colour to the displayed images, and high-power instruments are now available for transcranial use, which are capable of estimating blood flow velocity in intracranial arteries. Uses Transcranial ultrasonography is used to evaluate hydrocephalus and neonatal haemorrhage in young children. It is simple to use, but less simple to interpret. Duplex scanning has replaced angiography for screening patients with suspected carotid bifurcation stenosis. It may be combined with MRA, and most vascular surgeons use the combination for preoperative imaging, instead of IA-DSA.

Ultrasonography
Technique Ultrasonography is based on the transmission and detection of reflected sound from tissue planes within the body. Because bone is relatively impervious to sound, ultrasonography is useful in the CNS only when performed through a bone defect (e.g. an open fontanelle) or after laminectomy. Duplex ultrasonography combines high-resolution real-time imaging with Doppler flow
FURTheR ReADINg Demaerel P, ed. Recent advances in diagnostic neuroradiology. Berlin: springer-verlag, 2001. grossman RI, Yousem DM. neuroradiology: the requisities (requisites in radiology). oxford: Mosby, 2003. osborn a, Blaser s, salzman K, et al. Diagnostic imaging: brain, 1st edn. amirys, 2004.

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