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Imaging of Haemorrhagic Stroke
Clinical Radiology (2002) 57: 957±968 doi:10.1053/crad.2002.0954, available online at http://www.idealibrary.com on
Imaging of Haemorrhagic Stroke N . HO G GA R D, I . D . W IL KI NS O N , M . N . I. PA L E Y, P. D. G R IF F I T HS Academic Department of Radiology, University of Sheeld, Royal Hallamshire Hospital, Sheeld, UK Received: 10 July 2001 Revised: 22 October 2001 Accepted: 3 December 2001 Computed tomography (CT) is the reference standard for the imaging of acute non-traumatic intracranial haemorrhage. The sensitivity with which CT detects haemorrhage falls with time and lumber puncture remains mandatory for the exclusion of subarachnoid haemorrhage (SAH). Magnetic resonance (MR) imaging is, however, superior to CT in the subacute and chronic stages after haemorrhage. MR in addition oers pathophysiological information that can help with assessment of both the aetiology of and complications arising from both SAH and intra-parenchymal haemorrhage. Hoggard, N. et al. (2002). Clinical Radiology 57, 957±968. # 2002 Published by Elsevier Science Ltd on behalf of The Royal College of Radiologists Key words: haemorrhage stroke, subarachnoid haemorrhage, parenchymal haemorrhage, MR.
In a previous review article we discussed imaging protocols for patients with ischaemic stroke including new magnetic resonance (MR) methods such as diusion and perfusion weighted imaging [1]. In this article we turn our attention to imaging haemorrhagic stroke. This implies primary, nontraumatic, intracranial haemorrhage (ICH), including lesions such as subarachnoid haemorrhage and parenchymal haematomas as opposed to haemorrhagic transformation in a previously bland, ischaemic stroke. Computed tomography (CT) is currently the imaging investigation of choice for demonstrating or excluding acute ICH of any cause. Despite long-held scepticism, there are increasing data on the value of MR for imaging ICH. This review will give an overview of the imaging of non-traumatic ICH. IMAGING TECHNIQUES
Before discussing the imaging of ICH in detail we will include a brief overview of the physical principals that underpin imaging haemorrhage.
Computed Tomography On CT images dierent X-ray attenuation values are displayed as pixels of dierent intensity. It is the electron density within the voxel that determines the attenuation of X-rays, which, in turn, is dependent on the density of the tissue and the atomic number of the atoms in the voxel. The electron density of blood rises as it clots due to Author for correspondence: Professor P. D. Griths, MRI Department, Floor C, Royal Hallamshire Hospital, Glossop Road, Sheeld S10 2JF, U.K. Fax: 0114 272 4760 0009-9260/02/$35
haemoconcentration and haematomas will have higher attenuation than the lipid rich brain parenchyma [2,3]. In addition, the attenuation of X-rays by a tissue will critically depend upon the energy of the photons and the kV, which can be altered to maximize the contrast in attenuation values between tissues. With time phagocytes lyse the haematoma and the attenuation falls, reducing the sensitivity of CT for its detection. For example, the sensitivity of CT is down to 50% at 1 week and 30% at 2 weeks after aneurysmal subarachnoid haemorrhage (SAH) [4].
CT Angiography CT angiography is performed by a very rapid volume acquisition during the passage of intravenous contrast medium through the cerebral circulation. In the absence of SAH it has been found to have similar sensitivity and interobserver agreement to MR angiography for the detection of cerebral aneurysms over 5 mm [5]. In that study the sensitivity of CT angiography for aneurysms less than 5 mm was 0.57 and 0.35 for time of ¯ight (TOF) MR angiography. However, others have claimed better results for CT angiography in the more dicult situation of imaging patients with SAH. Velthuis et al. detected 90% of all of the aneurysms on CT angiography (91 aneurysms, of which 75 were symptomatic) [6].
Conventional Catheter Angiography Conventional catheter angiography is the reference standard for imaging high ¯ow vascular malformations (aneurysms and arteriovenous malformations (AVMs)). Modern angiographic equipment can produce a matrix of 1024 1024, giving pixel sizes of the order of 0.2 mm.
# 2002 Published by Elsevier Science Ltd on behalf of The Royal College of Radiologists
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Images with a temporal resolution of up to 25/sec can be obtained giving detailed information of ¯ow patterns. This combination of spatial and temporal resolution is not currently possible with any other method of vascular imaging. The risk of permanent clinically detectable neurological de®cits from cerebral angiography was shown to be relatively low in a recent meta-analysis of prospective studies (0.2% for patients with SAH) [7]. The incidence of silent embolism into the cerebral circulation after routine four vessel angiography may be more common [8]. MR diusion weighted imaging showed 42 bright lesions in 23 patients after 23 procedures with a slightly lower incidence in the interventional cases, perhaps related to the use of prophylactic heparin. The rate was higher in those with vascular risk factors, longer or more complex examinations and in those who required multiple catheter changes. The incidence of silent embolic infarction may be even higher in the older population of those with intra-parenchymal haemorrhage (IPH) who undergo angiography. Non-neurological complications are more frequent than overt neurological de®cits, for example groin haematomas occur at a rate of 7.4±8.1% [7,9±11].
Magnetic Resonance Imaging MR imaging has the advantage over CT that it can readily produce multi-planar images allowing anatomical appreciation of haematomas and their complications. Spin echo imaging has not proved as useful for the detection of haemorrhage as gradient echo imaging [12,13]. For gradient echo (GRE) imaging the initial excitation pulse is varied but is less than 908 and no refocusing pulse is used so that the resulting contrast between tissues is complex. As the RF excitation angle is reduced, T1 weighting will fall. As the TE is lengthened, permitting greater loss of spin coherence, the image carries more T2* weighting (rather than T2 because there is no refocusing pulse to remove the eects of stationary ®eld inhomogeneities). The only source of dephasing of the net magnetization that is refocused is magnetic ®eld inhomogeneity due to the imaging gradient. Since none of the other sources of dephasing will be refocused, GRE images are very sensitive to any sort of magnetic ®eld inhomogeneity, for example from haemosiderin or the boundaries of tissues such as the sinuses and the base of the brain [14].
Magnetic Resonance Angiography There are several forms of MR angiography, including TOF, phase contrast and black blood imaging. The most widely employed technique for imaging the cerebral circulation clinically is TOF MR angiography. TOF MR angiography utilizes ¯ow related signal enhancement of a GRE sequence with a short TR. The increase in signal with ¯ow is linear until the blood is completely replaced every TR. The shorter the TR, the greater the background suppression but the faster the ¯ow of incoming unsaturated
spins that is required to obtain the maximum ¯ow related enhancement. TOF angiography may be performed in either 2D or 3D mode. 2D TOF is composed of many thin sections usually acquired one after the other. To maximize in¯ow of unsaturated spins these section are orientated at right angles to the direction of ¯ow in the vessels to be imaged. 3D TOF, as with any other 3D sequence, has multiple partitions that are typically quite thin ( 1 mm) and are contiguous with no inter-slice gap. This increases resolution at the penalty of increasing exposure of the incoming spins to the saturation eects of the RF at each TR, thus limiting the volume that can be covered. This problem has been overcome by using multiple overlapping thin slab acquisition (MOTSA). This utilizes multiple overlapping volumes, a few millimetres or less thick which stacked together to increase anatomical coverage.
ANATOMICAL CLASSIFICATION
Accurate anatomical classi®cation of ICH is important both for relaying information to neurosurgical colleagues and for providing useful dierential diagnoses. ICH is best classi®ed by the intracranial compartment into which the haemorrhage occurs.
Extradural Haematoma There are two leaves of the dura mater, a periosteal leaf and a meningeal leaf. Extradural haematomas occur between these two leaves which, in the acute setting, produces a biconvex shaped haematoma that is usually limited by the cranial sutures. Extradural haematomas are virtually always caused by trauma, usually damage to a branch of the middle meningeal artery often associated with a skull fracture. Diagnosis and surgical management are frequently medical emergencies and CT is ideally suited.
Subdural Haematoma Acute subdural haematomas are usually crescentic in shape on axial sections. The vast majority of subdural haematomas are caused by trauma that disrupts bridging veins crossing the space between the dura and the arachnoid mater. Other causes of subdural haematomas include coagulopathies, ruptured aneurysms ( posterior communicating artery and middle cerebral artery) and haemorrhagic meningeal metastases. Subdural haematomas are sometimes found in children with no history of trauma or with an inappropriate history of trauma. Many of these cases are a result of child abuse. CT should be the ®rst imaging investigation used but MR is an invaluable adjunct in attempting to date the trauma, looking for more than one traumatic event, and identi®es other clinically occult lesions.
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Subarachnoid Haemorrhage Subarachnoid haemorrhage (SAH) occurs in the space between the arachnoid and pia mater which is occupied by cerebrospinal ¯uid (CSF). Focal expansions of the subarachnoid space are called cisterns. Because the majority of the cisterns are on the inferior surface of the brain, in gravity-dependent positions, SAH tends to accumulate within them. SAH, because of the anatomy of the subarachnoid space, passes into the cortical sulci and often redistributes into the ventricles. The main causes of SAH are listed in Table 1; they include rupture of cerebral artery aneurysms and vascular malformations. CT is the ®rst line imaging investigation due to its high sensitivity to acute blood. Further assessment is normally with conventional catheter angiography to diagnose or exclude a treatable vascular abnormality.
Parenchymal Haematoma The common causes of intra-parenchymal haemorrhage (IPH) are listed in Table 2. It should be remembered that in many patients there will be a combination of SAH and intra-parenchymal haematoma. At present, CT is the technique used for diagnosis and will often lead to other diagnostic imaging tests to ®nd the cause of the haemorrhage. Cerebral angiography is often required but as many patients are old and have signi®cant carotid atherosclerosis there are higher complications rates. One of the most important research aims in this area is to try to exclude
patients who do not have treatable vascular lesions by noninvasive imaging methods and therefore reduce the number of catheter angiographic studies performed. MR holds some promise here but this remains a dicult radiological problem.
Intraventricular Haemorrhage Intraventricular haemorrhage is often associated with a degree of hydrocephalus as the blood interferes with normal CSF circulation and absorption. It is usually associated with either SAH or IPH and is not considered in isolation any further in this review.
Imaging Parenchymal Haemorrhage Detection The reference standard method for the diagnosis of acute parenchymal haemorrhage is CT rather than MR. On CT, acute haemorrhage causes local mass eect and increased attenuation makes CT very sensitive. There is an increasing literature to suggest that MR may no longer be as poor as previously thought and this is especially important when the dierential diagnosis is ischaemic stroke and thrombolysis, anti-platelet therapy or anticoagulation are being considered. There are many small studies in this area but none of sucient statistical power to draw reliable conclusions. Haemorrhage has been demonstrated in each of a series of nine patients imaged within 6 hours of onset with
Table 1 ± Causes of subarachnoid haemorrhage Cause
Comment
Ruptured aneurysm Benign Perimesencephalic Ruptured vascular malformation Coagulopathy Illicit drug use
(Berry very much more frequent cause than mycotic or malignant aneurysms) (Unknown cause more frequent than penetrating artery infarction) (Cerebral AVM very much more frequent cause than either cavernous angioma, dural AVM) (Iatrogenic, inherited or acquired) (Cocaine and amphetamine, especially in combination, there may often be an underlying structural cause)
Venous thrombosis Others Vasculitis, sickle cell disease, Moyamoya, haemorrhage in super®cial tumours, septicaemia, meningitis
Table 2 ± Causes of intraparenchymal haemorrhage Cause
Comment
Hypertension Amyloid angiopathy Haemorrhagic stroke Ruptured vascular malformation
(Most common cause) (Pathological diagnosis hinted at by history of recurrent bleeds in an elderly person) (Embolic strokes are much more frequent cause than thrombotic) (Cerebral AVM more common cause than cavernous angioma and both are much common causes than either dural AVM or capillary telangectasia) (Frequently in addition to SAH, and may suggest site of aneurysm) (Iatrogenic, inherited or acquired) (Metastases, pituitary adenoma, high grade glioma) (increasingly diagnosed with MR imaging)
Ruptured aneurysm Coagulopathy Tumours Venous infarction Others Vasculitis, Encephalitis, Abcess
(Common in herpes encephalitis imaged on MR. Haemorrhage from an abcess more common in the immunocompromised and when arising from septic emboli)
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CT and MR in a study by Schellinger et al. [15]. Another study has also shown the ability of MR to demonstrate parenchymal haemorrhage 2.5 to 5 hours after onset in six patients and also in all of a series of ®ve patients imaged within 2.5 hours of onset with MR [16]. These small groups suggest that MR appears to have a high sensitivity and similar accuracy when compared with CT [17±19]. However, more clinical data are required, as the volumes of the majority of acute haemorrhages in the clinical series are large (where these have been indicated). As the initial clot resolves, MR becomes increasingly accurate [20]. The imaging of chronic haemorrhage centres on the ability to detect the susceptibility eect of retained haemosiderin deposits on MR [21]. The demonstration of this eect depends not only on the quantity of haemosiderin present but also on the imaging strategy used [22]. Wardlaw and Statham found that 10% of haemorrhages shown on CT at the time of presentation of traumatic parenchymal haematomas were not demonstrated years later with a standard spin echo and proton density weighted images using a 1 T magnet. How often this is true with gradient echo T2*-weighted sequences at dierent ®eld strengths is not clear, although these sequences have been shown to be superior to spin echo sequences for the demonstration of haemosiderin [12].
Complications: Mass Eect Cerebral herniation is caused by mechanical displacement of intracranial contents from one compartment to another. Cerebral herniation is a common secondary eect of expanding intracranial masses such as intraparenchymal or subdural haemorrhage. Those most frequently encountered are sub-falcine and trans-tentorial (see Fig. 1). Secondary brain injury and oedema formation contribute signi®cantly to the morbidity and mortality of parenchymal haemorrhage. The pathogenesis of the process is not well understood but there is a clear early reduction in perfusion
around a haematoma [23,24]. This is likely be an increasingly important aspect of the imaging of the parenchymal haemorrhage as eective treatment strategies emerge.
Investigation of Aetiology For MR imaging of cerebral haemorrhage to be useful clinically it has to deliver information that is not provided on CT, for example detecting haemosiderin. Micro-haemorrhages are detected by MR from their haemosiderin related magnetic susceptibility artifact and may be manifestations of the underlying disease that led to the presenting haemorrhage [25]. Greenberg et al. noted that 80% of patients with a primary parenchymal haemorrhage show other focal areas of signal loss on T2*-weighted imaging consistent with petechial bleeds [26]. In addition, some cerebral haemorrhages do not appear to present clinically so detection by imaging is all the more important [27]. There is histological data associating the occurrence of micro-bleeds and small vessel disease such as hypertensive lipohyalinosis and cerebral amyloid angiopathy [28,29]. Other causes of focal signal loss such as calci®cation, haemorrhage from shear injury or haemangiomas do not carry an increased risk of repeat haemorrhage. In a postmortem study the great majority of focal signal loss using a gradient echo T2* sequence was demonstrated to be related to focal haemosiderin deposits and not to the other causes [29]. Detecting microbleeds has important prognostic implications for patients. The detection of small chronic haemorrhages in IPH indicates that microangiopathy is present and highlights the need for the control of hypertension or other predisposing factors. Work by Greenberg et al. would suggest that patients with an increased number of microbleeds may be at greater risk of rebleeding from cerebral amyloid angiopathy [26]. Patients with microangiopathy as manifest by leucoaraiosis and lacunar infarcts have increased risk of intracerebral haemorrhage in a recent
Fig. 1 ± Caption on p. 961.
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Fig. 1 ± These MR images show the consequences of transtentorial herniation in a patient with an acute subdural haemorrhage (after emergency decompressive surgery). The increased pressure has forced the uncus and the parahippocampal gyrus of the medial temporal lobe medially over the edge of the tentorium cerebelli. This movement tends to eace the suprasellar cistern and at ®rst makes the perimesencephalic cistern on the side of the herniation more prominent. This is an important review area on CT of acute intracranial mass lesions. Contralateral cerebral peduncle compression produces a false localizing contralateral hemiparesis (Kernohan notch) (a±c, T2-weighted axial images that show right posterior cerebral artery territory infarction with contralateral infarction in the inferior thalamus/cerebral peduncle). The infarction produced may be haemorrhagic (d, coronal T1-weighted image showing high signal from methaemoglobin in the inferior left thalamus/cerebral peduncle). Posterior cerebral artery (PCA) is the most common arterial infarction produced by compression (a±c). These PCA infarctions are often haemorrhagic, not evident on this MR examination. Further downward displacement of the brainstem structures may cause tearing of the penetrating arteries from the basiliar and the exiting veins. This leads to infarction and haemorrhage in the midbrain and pons (Duret haemorrhages) (c, T2-weighted axial image, showing high signal in the left cerebral peduncle). (e) This shows a time to peak map of cerebral perfusion. ( f) This shows an inverted cerebral blood volume map (i.e. areas of high cerebral blood volume are showed as darker shades of grey). The time to peak maps show areas of slowed perfusion in the watershed areas adjacent to the posterior cerebral artery territory bilaterally. The area of infarction in the right posterior cerebral artery territory has increased cerebral blood volume, so called luxury perfusion, whereas the left posterior cerebral artery territory has reduced cerebral blood volume indicating that it remains oligaemic at the time of the MR examination.
study of secondary prevention after transient ischaemic attack or mild stroke [30]. Also, the risk : bene®t balance for follow-up cerebral angiography to exclude an underlying AVM in a patient with IPH may be altered if there is evidence for an alternative cause. Although less common than haemorrhage related to hypertensive disease, in the older population cerebral pial arteriovenous malformations and aneurysms remain
important dierential diagnoses because of their propensity for rebleeding and the possibility of curative treatment. Large cerebral AVMs are easily demonstrated on CT and MR, but catheter angiography is needed for smaller AVMs and most aneurysms after acute haemorrhage. Due to technical limitations, MR TOF angiography is not of proven practical value in the assessment of parenchymal haematomas. The T1 shortening produced
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by haemoglobin breakdown products may obscure the ¯owrelated signal arising from an underlying cerebral AVM. There is, however, new interest in the area as recent MR angiography developments progress. Both a group in Japan and our own group have found MRDSA of value since it can be used as a subtraction technique that removes the obscuring eect of the haematoma to reveal the AVM (Fig. 2).
Imaging of Subarachnoid Haemorrhage Detection CT is taken to be the reference standard for diagnosing acute SAH and has been shown to be a reliable technique [31]. Infrequently SAH may be dicult to dierentiate from subdural blood on CT but it should be remembered that subdural collections do not track into cortical sulci. There are a number of reasons why SAH may be missed on CT.
First misinterpretation, or second, the anatomical location of the SAH may not be included ( for example, SAH from a posterior interior cerebellar artery (PICA) aneurysm or a spinal arteriovenous malformation). Third, the timing of the CT examination is critical to its sensitivity. On the day of SAH, intracranial blood is detected in about 98% of patients. This proportion declines to 90% after day one, 80% after 5 days and 50% after 1 week [4,32]. Exclusion of SAH on CT requires careful attention to several review areas. These include the basal cisterns, especially in the interpendular fossa and suprasellar cistern, in the dependent portions of the lateral ventricles (occipital horns), the inter-hemispheric ®ssure and also an overall assessment of the symmetry of CSF spaces (Fig. 3). In comparison to CT, all patients with SAH will have xanthochromia of their CSF between 12 hours after and 2 weeks after the haemorrhage [33]. Therefore lumbar puncture is mandatory if CT is negative. Unfortunately, this simple doctrine is frequently overlooked or not
Fig. 2 ± Caption on p. 7.
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Fig. 2 ± MR images from a patient with a subacute parietal parenchymal haematoma. The high signal on the T1 weighted image (a) is consistent with the presence of methaemoglobin in a subacute haemorrhage from the adjacent cluster of abnormal vessels that imply the presence of a cerebral AVM. The T2-weighted image (b) suggests that there is a mixture of intra- and extra-cellular methaemoglobin surrounded by oedema. On the paired diusion weighted images and ADC maps (c) and (d), the surrounding oedema is associated with increased diusion from vasogenic, not cytotoxic oedema. The nidus of an underlying cerebral AVM is visualized on the MRDSA images (e) and ( f), but very poorly on the SLINKY TOF shown in (g).
understood. A recent audit at our institution (unpublished) showed that 24% of patients investigated for possible SAH and normal CT did not have CSF studies. Similar ®ndings have been presented from Cardi [34] and these underline the need for improved education of clinical colleagues by radiologists. The role of MR for SAH remains controversial. It is generally accepted that acute SAH is dicult to detect with conventional MR imaging [35,36]. There are a number of studies suggesting that ¯uid attenuated inversion-recovery (FLAIR) or turbo-FLAIR imaging can detect SAH reliably and is superior to CT for subacute SAH [13,37±42]. The inversion time of water, or CSF, is dependent on its protein content. Once the CSF protein content is above a threshold (determined by the imaging parameters), FLAIR imaging will demonstrate subarachnoid haemorrhage and disease but in a non-speci®c manner [43]. Similarly, protein concentrations also aect CT appearances, for example colloid cysts of the third ventricle are hyperdense because of the high electron density from their proteinaceous contents.
Noguchi has reported 100% detection of acute SAH with FLAIR imaging and a 63% detection rate for chronic SAH [37]. The same group compared CT with MR for subacute and chronic SAH ®nding a CT detection rate of 46% for 37 cases [38,39]. Turbo-FLAIR imaging has been shown to be more sensitive than CT in the detection for small amounts of fresh blood diluted by CSF [44]. This study found that a haematocrit of 27% was required to raise the Houns®eld number suciently for the haemorrhage to be denser than cortical grey matter, whereas a haematocrit of only 22.4% blood was required with an eective TE of 120 ms for the mixture to be more hyperintense than normal cortical grey mater on turbo-FLAIR images. This fell to 9% if the TE was increased to 160 ms. A limitation of SAH imaging with FLAIR sequences is artifactual CSF hyperintensity. Artifactual CSF hyperintensity is prominent in the ventricular system, around the foramina of Munro, the fourth ventricle and basal cisterns, and is due to in¯ow of non-nulled CSF into sections due to
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high CSF ¯ow rates [45]. CSF that moves into a section of the volume to be imaged during the TI interval on a turboFLAIR sequence will not be exposed the inversion pulse, thus producing high CSF signal intensity. Section-selective inversion pulses with a broad bandwidth and the use of cardiac synchronization are some techniques that reduce these artifacts. Regions in which haemorrhage is demonstrated by CT will not necessarily correspond to those observed on MR imaging. The physical state of the haematoma is important as it has dierent consequences for the sensitivity of an investigation to the haemorrhage [46]. It is interesting to note that the use of gradient echo T2* imaging has been reported to be superior to the use of FLAIR alone and the combination of the two was superior to either alone for subacute haemorrhage [13,47]. The regions of abnormal signal on images tended to dier, which may have re¯ected
Fig. 3 ± Images of a 44-year-old man with a sudden onset severe headache with photophobia and nuchal stiness. (a) Unenhanced CT of the head shows high attenuation subarachnoid haemorrhage particularly in the occipital pole of the right lateral ventricle but also in the anterior part of the inter-hemispheric ®ssure. (b) A FLAIR image from an MR examination performed 4 days later shows haemorrhage in both of the lateral ventricles, detected as loss of the normal CSF signal suppression. (c) T2*-weighted image shows the haemorrhage not only in the occipital poles of the lateral ventricles but also in the third ventricle as areas of signal loss. Haemorrhage in the anterior aspect of the inter-hemispheric ®ssure is dicult to appreciate on this section. This example illustrates how the MR sequences can be complementary for detecting SAH.
not just dierent local biochemical changes but also localized dierences in physical state of the haemorrhage, especially in the acute cases. Again this study con®rmed the superiority of MR imaging to CT in the subacute and chronic periods after SAH, but with the two investigations being of comparable sensitivity in patients with acute SAH.
Vasospasm It is likely that vasospasm after SAH is a result of periarterial blood clot. In 1980, Fisher et al. showed that the amount and the location of subarachnoid blood seen on the initial CT is a strong predictor of vasospasm [48]. Angiographic vasospasm is found in 60±70% of patients with heavy cisternal accumulations of blood at 10±12 days after SAH. However, angiographic vasospasm does not always correlate with symptoms and tissue perfusion
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Fig. 4 ± MR images from a 69-year-old patient with a 13-day history of headache presenting with left sided weakness. (a) A fast spin echo T2-weighted image fails to demonstrate any haemorrhage. (b) A T1-weighted image shows subtle raised signal in the right Sylvian ®ssure. The haemorrhage is con®rmed in the gradient echo T2*-weighted image (c) and the FLAIR image (d). The DWI image (e) shows more extensive, bilateral watershed infarction. Oligaemia is shown in the prolonged time to peak in the perfusion map ( f).
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depends on small arteries and arterioles not imaged on angiography [49]. There are several techniques for the evaluation of cerebral blood ¯ow. Transcranial Doppler is easily repeatable, noninvasive and without the complications of cerebral angiography, but many studies have demonstrated the low sensitivity of the technique [50]. The 133Xe technique has been validated and provides reliable measurements [51±53]. The problems of Xe/CT include a relatively high radiation exposure, limited anatomical coverage and diculties arising from the degree of co-operation required from patients. CT perfusion using intravenous iodinated contrast media has also been advocated and prospectively assessment for monitoring vasospasm. Its anatomical coverage is more limited than CT, though clearly multi-slice CT is advantageous compared to single-slice systems [54,55]. Both SPECT and PET have been used to assess vasospasm and appear sensitive [56,57]. In particular, technetium-99m hexamethylpropylene amine oxime (HMPAO) SPECT scanning is widely available and has been used to monitor progression of vasospasm and the eects of therapeutic intervention [58]. Diusion and perfusion weighted MR imaging abnormalities related to vasospasm are present in 64% of SAH cases as early as 4±7 days after haemorrhage [13] (Fig. 4). The use of cerebral perfusion to help determine and monitor clinical management is being explored for Xe/CT by Yonas and others [59].
Investigation of Cause In patients with proven SAH the source of the haemorrhage must be sought and this is usually investigated by catheter angiography. The majority of cases arise from rupture of an intracranial aneurysm, with a minority arising from AVMs. The reference standard for demonstration of the intracranial circulation is conventional selective fourvessel catheter digital subtraction angiography. Although MR angiography methods continue to improve, even highresolution techniques fail to reliably demonstrate aneurysms less than 2 mm, even in the absence of haemorrhage [6,59, 60]. CT angiography also fails to match the resolution of angiography, although good results using the technique have been published [61]. The technique becomes much less reliable for aneurysms less than 5 mm in diameter [5,62]. Part of the information that is ordinarily obtainable from angiography is temporal, for example increased circulation time in cases of vasospasm after SAH or reduced circulation time because of the presence of an arteriovenous shunt. Some steps to temporally resolved MR angiography are being made with magnetic resonance digital subtraction angiography (MRDSA) and other similar techniques, for example time-resolved imaging of contrast kinetics (TRICKS) [63,64]. These techniques are still being developed but cannot currently match either the temporal or the spatial resolution of conventional catheter angiography. About 80% of patients with SAH have a ruptured cerebral aneurysm as the cause demonstrated on the initial four-vessel angiogram, that is 15±20% will have negative angiography [65,66]. In a study to evaluate spiral CT
angiography, 15 of 134 patients had structural causes demonstrated on subsequent imaging not identi®ed on the initial conventional cerebral angiogram [67]. This is 12% (15/128) of those with a structural cause identi®ed by all diagnostic measures and including a post mortem diagnosis. There is a 5.8±11% chance of either an aneurysm or AVM being demonstrated on a repeat angiogram and performing a second angiogram remains standard practice in most institutions [68,69]. There is now a role for MR after repeated angiography or even before the second angiogram for perimesencephalic SAH as in a proportion associated infarcts of perforator territory are demonstrated [70]. There is also evidence that CT angiography is a useful investigation for perimesencephalic haemorrhage and should be used before conventional cerebral angiography is employed [71]. CONCLUSION
CT remains the investigation of choice for the imaging of acute non-traumatic intracranial haemorrhage. For SAH there is also some evidence that CT angiography may be useful, but it is inferior in quality to conventional catheter angiography. For the subacute and chronic stages of SAH, that is 3±4 days after onset, MR imaging including FLAIR and gradient echo T2*-weighted sequences should be used when available. However, delayed lumbar puncture remains mandatory if both CT and MR fail to demonstrate SAH. Diusion and perfusion weighted MR imaging to assess ischaemia and oligaemia may be helpful where the capability exists, Xe/CT or HMPAO/SPECT can be used to similar eect for the assessment of cerebral perfusion. The approach to imaging subacute and chronic IPH is not so clear. The value of a T2*-weighted sequence is proved, but evidence for the use of MR angiography or indeed CT angiography without conventional angiography is still lacking, nor is the clinical role of diusion and perfusion imaging in IPH established. REFERENCES 1 Hoggard N, Wilkinson ID, Griths PD. The imaging of ischaemic stroke. Clin Radiol 2001;56:171±183. 2 New PF, Aronow S. Attenuation measurements of whole blood and blood fractions in computed tomography. Radiology 1976;121: 635±640. 3 Brooks RA, DeChiro G, Patronas N. MR imaging of cerebral haematoma at dierent ®eld strengths: theory and applications. J Comp Asst Tomogr 1989;13:194±206. 4 van Gijn J, van Dongen KJ. The time course of aneurysmal haemorrhage on computed tomograms. Neuroradiology 1982;23: 153±156. 5 White PM, Teasdale EM, Wardlaw JM, Easton V. Intracranial aneurysms: CT angiography and MR angiography for detection prospective blinded comparison in a large patient cohort. Radiology 2001;219:739±749. 6 Velthuis BK, Rinkel GJ, Ramos LM, et al. Subarachnoid hemorrhage: aneurysm detection and preoperative evaluation with CT angiography. Radiology 1998;208:423±430. 7 Cloft HJ, Joseph GJ, Dion JE. Risk of cerebral angiography in patients with subarachnoid haemorrhage, cerebral aneurysm and arteriovenous malformation a meta analysis. Stroke 1999;30: 317±320.
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32 Adams HP, Kassell NF, Torner JC, Sahs AL. CT and clinical correlations in recent aneurysmal subarachnoid haemorrhage: a preliminary report of the Cooperative Aneurysm Study. Neurology 1983;33:981±988. 33 Vermeulen M, Hasan D, Blijenberg BG, Hijdra A, Van Gijn J. Xanthochromia after subarachnoid hemorrhage needs no revisitation. J Neurol Neurosurg Psychiatry 1989;52:826±828. 34 Sadiq S, Jenkins S, Hourihan M. An audit of lumbar puncture procedures following a normal CT scan in patients suspected of having subarachnoid haemorrhage. BJR Congress series. Proceedings of the UK Radiological Congress, 2001, May 21±23, Wembley, U.K. London: British Institute of Radiology, 2001; 50. 35 Atlas SW. MR imaging is highly sensitive for acute subarachnoid hemorrhage not. Radiology 1993;186:319±322. 36 Bradley WG, Schmidt PG. Eect of methemoglobin formation on the MR appearance of subarachnoid hemorrhage. Radiology 1985;156:99±103. 37 Noguchi K, Ogawa T, Inugami A, Toyoshima H, Okudera T, Uemura K. MR of acute subarachnoid hemorrhage: a preliminary report of ¯uid-attenuated inversion-recovery pulse sequences. Am J Neuroradiol 1994;15:1940±1943. 38 Noguchi K, Ogawa T, Inugami A, et al. Acute subarachnoid hemorrhage: MR imaging with ¯uid-attenuated inversion recovery pulse sequences. Radiology 1995;196:773±777. 39 Noguchi K, Ogawa T, Seto H, et al. Subacute and chronic subarachnoid hemorrhage: diagnosis with ¯uid-attenuated inversion-recovery MR imaging. Radiology 1997;203:257±262. 40 Singer MB, Atlas SW, Drayer BP. Subarachnoid space disease: diagnosis with ¯uid-attenuated inversion-recovery MR imaging and comparison with gadolinium-enhanced spin-echo MR imaging± blinded reader study. Radiology 1998;208:417±422. 41 Ogawa T, Inugami A, Fujita H, et al. MR diagnosis of subacute and chronic subarachnoid hemorrhage: comparison with CT. Am J Roentgenol 1995;165:1257±1262. 42 Chrysikopoulos H, Papanikolaou N, Pappas J, et al. Acute subarachnoid haemorrhage: detection with magnetic resonance imaging. Br J Radiol 1996;69:601±609. 43 Melhem ER, Jara H, Eustace S. Fluid-attenuated inversion recovery MR imaging: identi®cation of protein concentration thresholds for CSF hyperintensity. AJR Am J Roentgenol 1997;169:859±862. 44 Noguchi K, Seto H, Kamisaki Y, Tomizawa G, Toyoshima S, Watanabe N. Comparison of ¯uid-attenuated inversion-recovery MR imaging with CT in a simulated model of acute subarachnoid hemorrhage. Am J Neuroradiol 2000;21:923±927. 45 De Coene B, Hajnal JV, Gatehouse P, et al. MR of the brain using ¯uid-attenuated inversion recovery (FLAIR) pulse sequences. Am J Neuroradiol 1992;13:1555±1564. 46 Ogawa T, Inugami A, Shimosegawa E, et al. Subarachnoid hemorrhage: evaluation with MR imaging. Radiology 1993;186: 345±351. 47 Griths PD, Wilkinson ID, Mitchell P, et al. Multimodality magnetic resonance imaging detects hemodynamic changes and cerebral ischaemia in patients with subarachnoid hemorrhage. Am J Neuroradiol 2001;22: 690±697. 48 Fisher C, Kistler J, Davis J. Relation of cerebral vasospasm to subarachnoid haemorrhage visualised by computerized tomographic scanning. Neurosurgery 1980;6:1±9. 49 Heros R, Zervas N, Varsos V. Cerebral vasospasm after subarachnoid hemorrhage: an update. Ann Neurol 1983;14: 599±608. 50 Sloan M, Haley EC Jr, Kassell NF, et al. Sensitivity and speci®city of transcranial Doppler ultrasonography in the diagnosis of vasospasm following subarachnoid haemorrhage. Neurology 1989;39:1514±1518. 51 Yamakami I, Isobe K, Yamaura A, Nakamura T, Makino H. Vasospasm and regional cerebral blood ¯ow (rCBF) in patients with ruptured intracranial aneurysm: serial studies with the xenon133 inhalational method. Neurosurgery 1983;13:394±401. 52 Yonas H, Sekhar L, Johnson D, Gur D. Determination of irreversible ischaemia by xenon-enhanced computed tomographic monitoring of cerebral blood ¯ow in patients with symptomatic vasospasm. Neurosurgery 1989;24:368±372.
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53 Fukui M, Johnson D, Yonas H, Sekhar L, Latchaw R, Pentheny S. Xe/CT cerebral blood ¯ow evaluation of delayed symptomatic cerebral ischemia after subarachnoid hemorrhage. Am J Neuroradiol 1992;13:265±270. 54 Nabavi DG, Cenic A, Craen RA, et al. CT assessment of cerebral perfusion: experimental validation and initial clinical experience. Radiology 1999;213:141±149. 55 Nabavi DG, LeBlanc LM, Baxter B, et al. Monitoring cerebral perfusion after subarachnoid haemorrhage using CT. Neuroradiology 2001;43:7±16. 56 Hasan D, Peski J, Loeve I, Krenning E, Vermeulen M. Single emission computed tomography in patients with acute hydrocephalus or with cerebral ischemia after subarachnoid hemorrhage. J Neurol Neurosurg Psych 1991;54:490±493. 57 Powers W, Grubb R, Baker R, Mintun M, Raichle M. Regional cerebral blood ¯ow and metabolism in reversible ischaemia due to vasospasm. J Neurosurg 1985;62:539±546. 58 Lewis DH, Eskridge JM, Newell DW, et al. Brain SPECT and the eect of cerebral angioplasty in delayed ischaemia due to vasospasm. J Nucl Med 1992;33:1789±1796. 59 Firlik AD, Kaufmann AM, Jungreis CA, Yonas H. Eect of transluminal angioplasty on cerebral blood ¯ow in the management of symptomatic vasospasm following aneurysmal subarachnoid hemorrhage. J Neurosurg 1997;86:830±839. 60 Blatter DD, Parker DL, Ahn SS, et al. Cerebral MR angiography with multiple overlapping thin slab acquisition. Part II. Early clinical experience. Radiology 1992;183:379±389. 61 Matsumoto M, Sato M, Nakano M, et al. Three-dimensional computerized tomography angiography-guided surgery of acutely ruptured cerebral aneurysms. J Neurosurg 2001;94:718±727. 62 Pedersen HK, Bakke SJ, Hald JK, et al. CTA in patients with acute subarachnoid haemorrhage: a comparative study with selective,
63 64 65
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digital angiography and blinded, independent review. Acta Radiol 2001;42:43±49. Strecker R, Scheer K, Klisch J, et al. Fast functional MRA using time-resolved projection MR angiography with correlation analysis. Magn Reson Med 2000;43:303±309. Korosec FR, Frayne R, Grist TM, Mistretta CA. Time-resolved contrast-enhanced 3D MR angiography. Magn Reson Med 1996;36: 345±351. Mayberg MR, Batjer HH, Dacey R, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 1994;25: 2315±2328. Schwartz TH, Solomon RA. Perimesencephalic nonaneurysmal subarachnoid hemorrhage: review of the literature. Neurosurgery 1996;39:433±440. Hashimoto H, Iida J, Okada M, Sakaki T. Use of spiral computerized tomography in patients with subarachnoid hemorrhage in whom subtraction angiography did not reveal cerebral aneurysms. J Neurosurg 2000;92:278±283. Juul R, Fredriksen TA, Ringkjob R. Prognosis in subarachnoid hemorrhage of unknown etiology. J Neurosurg 1986;64:359±362. Forster DM, Steiner L, Hakanson S, Bergvall U. The value of repeat pan-angiography in cases of unexplained subarachnoid hemorrhage. J Neurosurg 1978;48:712±716. Rogg JM, Smeaton S, Doberstein C, Goldstein JH, Tung GA, Haas RA. Assessment of the value of MR imaging for examining patients with angiographically negative subarachnoid haemorrhage. Am J Roentol 1999;172:201±206. Ruigrok YM, Rinkel GJ, Buskens E, Velthuis BK, van Gijn J. Perimesencephalic hemorrhage and CT angiography: a decision analysis. Stroke 2000;31:2976±2983.
Imaging of Haemorrhagic Stroke N . HO G GA R D, I . D . W IL KI NS O N , M . N . I. PA L E Y, P. D. G R IF F I T HS Academic Department of Radiology, University of Sheeld, Royal Hallamshire Hospital, Sheeld, UK Received: 10 July 2001 Revised: 22 October 2001 Accepted: 3 December 2001 Computed tomography (CT) is the reference standard for the imaging of acute non-traumatic intracranial haemorrhage. The sensitivity with which CT detects haemorrhage falls with time and lumber puncture remains mandatory for the exclusion of subarachnoid haemorrhage (SAH). Magnetic resonance (MR) imaging is, however, superior to CT in the subacute and chronic stages after haemorrhage. MR in addition oers pathophysiological information that can help with assessment of both the aetiology of and complications arising from both SAH and intra-parenchymal haemorrhage. Hoggard, N. et al. (2002). Clinical Radiology 57, 957±968. # 2002 Published by Elsevier Science Ltd on behalf of The Royal College of Radiologists Key words: haemorrhage stroke, subarachnoid haemorrhage, parenchymal haemorrhage, MR.
In a previous review article we discussed imaging protocols for patients with ischaemic stroke including new magnetic resonance (MR) methods such as diusion and perfusion weighted imaging [1]. In this article we turn our attention to imaging haemorrhagic stroke. This implies primary, nontraumatic, intracranial haemorrhage (ICH), including lesions such as subarachnoid haemorrhage and parenchymal haematomas as opposed to haemorrhagic transformation in a previously bland, ischaemic stroke. Computed tomography (CT) is currently the imaging investigation of choice for demonstrating or excluding acute ICH of any cause. Despite long-held scepticism, there are increasing data on the value of MR for imaging ICH. This review will give an overview of the imaging of non-traumatic ICH. IMAGING TECHNIQUES
Before discussing the imaging of ICH in detail we will include a brief overview of the physical principals that underpin imaging haemorrhage.
Computed Tomography On CT images dierent X-ray attenuation values are displayed as pixels of dierent intensity. It is the electron density within the voxel that determines the attenuation of X-rays, which, in turn, is dependent on the density of the tissue and the atomic number of the atoms in the voxel. The electron density of blood rises as it clots due to Author for correspondence: Professor P. D. Griths, MRI Department, Floor C, Royal Hallamshire Hospital, Glossop Road, Sheeld S10 2JF, U.K. Fax: 0114 272 4760 0009-9260/02/$35
haemoconcentration and haematomas will have higher attenuation than the lipid rich brain parenchyma [2,3]. In addition, the attenuation of X-rays by a tissue will critically depend upon the energy of the photons and the kV, which can be altered to maximize the contrast in attenuation values between tissues. With time phagocytes lyse the haematoma and the attenuation falls, reducing the sensitivity of CT for its detection. For example, the sensitivity of CT is down to 50% at 1 week and 30% at 2 weeks after aneurysmal subarachnoid haemorrhage (SAH) [4].
CT Angiography CT angiography is performed by a very rapid volume acquisition during the passage of intravenous contrast medium through the cerebral circulation. In the absence of SAH it has been found to have similar sensitivity and interobserver agreement to MR angiography for the detection of cerebral aneurysms over 5 mm [5]. In that study the sensitivity of CT angiography for aneurysms less than 5 mm was 0.57 and 0.35 for time of ¯ight (TOF) MR angiography. However, others have claimed better results for CT angiography in the more dicult situation of imaging patients with SAH. Velthuis et al. detected 90% of all of the aneurysms on CT angiography (91 aneurysms, of which 75 were symptomatic) [6].
Conventional Catheter Angiography Conventional catheter angiography is the reference standard for imaging high ¯ow vascular malformations (aneurysms and arteriovenous malformations (AVMs)). Modern angiographic equipment can produce a matrix of 1024 1024, giving pixel sizes of the order of 0.2 mm.
# 2002 Published by Elsevier Science Ltd on behalf of The Royal College of Radiologists
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Images with a temporal resolution of up to 25/sec can be obtained giving detailed information of ¯ow patterns. This combination of spatial and temporal resolution is not currently possible with any other method of vascular imaging. The risk of permanent clinically detectable neurological de®cits from cerebral angiography was shown to be relatively low in a recent meta-analysis of prospective studies (0.2% for patients with SAH) [7]. The incidence of silent embolism into the cerebral circulation after routine four vessel angiography may be more common [8]. MR diusion weighted imaging showed 42 bright lesions in 23 patients after 23 procedures with a slightly lower incidence in the interventional cases, perhaps related to the use of prophylactic heparin. The rate was higher in those with vascular risk factors, longer or more complex examinations and in those who required multiple catheter changes. The incidence of silent embolic infarction may be even higher in the older population of those with intra-parenchymal haemorrhage (IPH) who undergo angiography. Non-neurological complications are more frequent than overt neurological de®cits, for example groin haematomas occur at a rate of 7.4±8.1% [7,9±11].
Magnetic Resonance Imaging MR imaging has the advantage over CT that it can readily produce multi-planar images allowing anatomical appreciation of haematomas and their complications. Spin echo imaging has not proved as useful for the detection of haemorrhage as gradient echo imaging [12,13]. For gradient echo (GRE) imaging the initial excitation pulse is varied but is less than 908 and no refocusing pulse is used so that the resulting contrast between tissues is complex. As the RF excitation angle is reduced, T1 weighting will fall. As the TE is lengthened, permitting greater loss of spin coherence, the image carries more T2* weighting (rather than T2 because there is no refocusing pulse to remove the eects of stationary ®eld inhomogeneities). The only source of dephasing of the net magnetization that is refocused is magnetic ®eld inhomogeneity due to the imaging gradient. Since none of the other sources of dephasing will be refocused, GRE images are very sensitive to any sort of magnetic ®eld inhomogeneity, for example from haemosiderin or the boundaries of tissues such as the sinuses and the base of the brain [14].
Magnetic Resonance Angiography There are several forms of MR angiography, including TOF, phase contrast and black blood imaging. The most widely employed technique for imaging the cerebral circulation clinically is TOF MR angiography. TOF MR angiography utilizes ¯ow related signal enhancement of a GRE sequence with a short TR. The increase in signal with ¯ow is linear until the blood is completely replaced every TR. The shorter the TR, the greater the background suppression but the faster the ¯ow of incoming unsaturated
spins that is required to obtain the maximum ¯ow related enhancement. TOF angiography may be performed in either 2D or 3D mode. 2D TOF is composed of many thin sections usually acquired one after the other. To maximize in¯ow of unsaturated spins these section are orientated at right angles to the direction of ¯ow in the vessels to be imaged. 3D TOF, as with any other 3D sequence, has multiple partitions that are typically quite thin ( 1 mm) and are contiguous with no inter-slice gap. This increases resolution at the penalty of increasing exposure of the incoming spins to the saturation eects of the RF at each TR, thus limiting the volume that can be covered. This problem has been overcome by using multiple overlapping thin slab acquisition (MOTSA). This utilizes multiple overlapping volumes, a few millimetres or less thick which stacked together to increase anatomical coverage.
ANATOMICAL CLASSIFICATION
Accurate anatomical classi®cation of ICH is important both for relaying information to neurosurgical colleagues and for providing useful dierential diagnoses. ICH is best classi®ed by the intracranial compartment into which the haemorrhage occurs.
Extradural Haematoma There are two leaves of the dura mater, a periosteal leaf and a meningeal leaf. Extradural haematomas occur between these two leaves which, in the acute setting, produces a biconvex shaped haematoma that is usually limited by the cranial sutures. Extradural haematomas are virtually always caused by trauma, usually damage to a branch of the middle meningeal artery often associated with a skull fracture. Diagnosis and surgical management are frequently medical emergencies and CT is ideally suited.
Subdural Haematoma Acute subdural haematomas are usually crescentic in shape on axial sections. The vast majority of subdural haematomas are caused by trauma that disrupts bridging veins crossing the space between the dura and the arachnoid mater. Other causes of subdural haematomas include coagulopathies, ruptured aneurysms ( posterior communicating artery and middle cerebral artery) and haemorrhagic meningeal metastases. Subdural haematomas are sometimes found in children with no history of trauma or with an inappropriate history of trauma. Many of these cases are a result of child abuse. CT should be the ®rst imaging investigation used but MR is an invaluable adjunct in attempting to date the trauma, looking for more than one traumatic event, and identi®es other clinically occult lesions.
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IMAGING OF HAEMORRHAGIC STROKE
Subarachnoid Haemorrhage Subarachnoid haemorrhage (SAH) occurs in the space between the arachnoid and pia mater which is occupied by cerebrospinal ¯uid (CSF). Focal expansions of the subarachnoid space are called cisterns. Because the majority of the cisterns are on the inferior surface of the brain, in gravity-dependent positions, SAH tends to accumulate within them. SAH, because of the anatomy of the subarachnoid space, passes into the cortical sulci and often redistributes into the ventricles. The main causes of SAH are listed in Table 1; they include rupture of cerebral artery aneurysms and vascular malformations. CT is the ®rst line imaging investigation due to its high sensitivity to acute blood. Further assessment is normally with conventional catheter angiography to diagnose or exclude a treatable vascular abnormality.
Parenchymal Haematoma The common causes of intra-parenchymal haemorrhage (IPH) are listed in Table 2. It should be remembered that in many patients there will be a combination of SAH and intra-parenchymal haematoma. At present, CT is the technique used for diagnosis and will often lead to other diagnostic imaging tests to ®nd the cause of the haemorrhage. Cerebral angiography is often required but as many patients are old and have signi®cant carotid atherosclerosis there are higher complications rates. One of the most important research aims in this area is to try to exclude
patients who do not have treatable vascular lesions by noninvasive imaging methods and therefore reduce the number of catheter angiographic studies performed. MR holds some promise here but this remains a dicult radiological problem.
Intraventricular Haemorrhage Intraventricular haemorrhage is often associated with a degree of hydrocephalus as the blood interferes with normal CSF circulation and absorption. It is usually associated with either SAH or IPH and is not considered in isolation any further in this review.
Imaging Parenchymal Haemorrhage Detection The reference standard method for the diagnosis of acute parenchymal haemorrhage is CT rather than MR. On CT, acute haemorrhage causes local mass eect and increased attenuation makes CT very sensitive. There is an increasing literature to suggest that MR may no longer be as poor as previously thought and this is especially important when the dierential diagnosis is ischaemic stroke and thrombolysis, anti-platelet therapy or anticoagulation are being considered. There are many small studies in this area but none of sucient statistical power to draw reliable conclusions. Haemorrhage has been demonstrated in each of a series of nine patients imaged within 6 hours of onset with
Table 1 ± Causes of subarachnoid haemorrhage Cause
Comment
Ruptured aneurysm Benign Perimesencephalic Ruptured vascular malformation Coagulopathy Illicit drug use
(Berry very much more frequent cause than mycotic or malignant aneurysms) (Unknown cause more frequent than penetrating artery infarction) (Cerebral AVM very much more frequent cause than either cavernous angioma, dural AVM) (Iatrogenic, inherited or acquired) (Cocaine and amphetamine, especially in combination, there may often be an underlying structural cause)
Venous thrombosis Others Vasculitis, sickle cell disease, Moyamoya, haemorrhage in super®cial tumours, septicaemia, meningitis
Table 2 ± Causes of intraparenchymal haemorrhage Cause
Comment
Hypertension Amyloid angiopathy Haemorrhagic stroke Ruptured vascular malformation
(Most common cause) (Pathological diagnosis hinted at by history of recurrent bleeds in an elderly person) (Embolic strokes are much more frequent cause than thrombotic) (Cerebral AVM more common cause than cavernous angioma and both are much common causes than either dural AVM or capillary telangectasia) (Frequently in addition to SAH, and may suggest site of aneurysm) (Iatrogenic, inherited or acquired) (Metastases, pituitary adenoma, high grade glioma) (increasingly diagnosed with MR imaging)
Ruptured aneurysm Coagulopathy Tumours Venous infarction Others Vasculitis, Encephalitis, Abcess
(Common in herpes encephalitis imaged on MR. Haemorrhage from an abcess more common in the immunocompromised and when arising from septic emboli)
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CT and MR in a study by Schellinger et al. [15]. Another study has also shown the ability of MR to demonstrate parenchymal haemorrhage 2.5 to 5 hours after onset in six patients and also in all of a series of ®ve patients imaged within 2.5 hours of onset with MR [16]. These small groups suggest that MR appears to have a high sensitivity and similar accuracy when compared with CT [17±19]. However, more clinical data are required, as the volumes of the majority of acute haemorrhages in the clinical series are large (where these have been indicated). As the initial clot resolves, MR becomes increasingly accurate [20]. The imaging of chronic haemorrhage centres on the ability to detect the susceptibility eect of retained haemosiderin deposits on MR [21]. The demonstration of this eect depends not only on the quantity of haemosiderin present but also on the imaging strategy used [22]. Wardlaw and Statham found that 10% of haemorrhages shown on CT at the time of presentation of traumatic parenchymal haematomas were not demonstrated years later with a standard spin echo and proton density weighted images using a 1 T magnet. How often this is true with gradient echo T2*-weighted sequences at dierent ®eld strengths is not clear, although these sequences have been shown to be superior to spin echo sequences for the demonstration of haemosiderin [12].
Complications: Mass Eect Cerebral herniation is caused by mechanical displacement of intracranial contents from one compartment to another. Cerebral herniation is a common secondary eect of expanding intracranial masses such as intraparenchymal or subdural haemorrhage. Those most frequently encountered are sub-falcine and trans-tentorial (see Fig. 1). Secondary brain injury and oedema formation contribute signi®cantly to the morbidity and mortality of parenchymal haemorrhage. The pathogenesis of the process is not well understood but there is a clear early reduction in perfusion
around a haematoma [23,24]. This is likely be an increasingly important aspect of the imaging of the parenchymal haemorrhage as eective treatment strategies emerge.
Investigation of Aetiology For MR imaging of cerebral haemorrhage to be useful clinically it has to deliver information that is not provided on CT, for example detecting haemosiderin. Micro-haemorrhages are detected by MR from their haemosiderin related magnetic susceptibility artifact and may be manifestations of the underlying disease that led to the presenting haemorrhage [25]. Greenberg et al. noted that 80% of patients with a primary parenchymal haemorrhage show other focal areas of signal loss on T2*-weighted imaging consistent with petechial bleeds [26]. In addition, some cerebral haemorrhages do not appear to present clinically so detection by imaging is all the more important [27]. There is histological data associating the occurrence of micro-bleeds and small vessel disease such as hypertensive lipohyalinosis and cerebral amyloid angiopathy [28,29]. Other causes of focal signal loss such as calci®cation, haemorrhage from shear injury or haemangiomas do not carry an increased risk of repeat haemorrhage. In a postmortem study the great majority of focal signal loss using a gradient echo T2* sequence was demonstrated to be related to focal haemosiderin deposits and not to the other causes [29]. Detecting microbleeds has important prognostic implications for patients. The detection of small chronic haemorrhages in IPH indicates that microangiopathy is present and highlights the need for the control of hypertension or other predisposing factors. Work by Greenberg et al. would suggest that patients with an increased number of microbleeds may be at greater risk of rebleeding from cerebral amyloid angiopathy [26]. Patients with microangiopathy as manifest by leucoaraiosis and lacunar infarcts have increased risk of intracerebral haemorrhage in a recent
Fig. 1 ± Caption on p. 961.
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Fig. 1 ± These MR images show the consequences of transtentorial herniation in a patient with an acute subdural haemorrhage (after emergency decompressive surgery). The increased pressure has forced the uncus and the parahippocampal gyrus of the medial temporal lobe medially over the edge of the tentorium cerebelli. This movement tends to eace the suprasellar cistern and at ®rst makes the perimesencephalic cistern on the side of the herniation more prominent. This is an important review area on CT of acute intracranial mass lesions. Contralateral cerebral peduncle compression produces a false localizing contralateral hemiparesis (Kernohan notch) (a±c, T2-weighted axial images that show right posterior cerebral artery territory infarction with contralateral infarction in the inferior thalamus/cerebral peduncle). The infarction produced may be haemorrhagic (d, coronal T1-weighted image showing high signal from methaemoglobin in the inferior left thalamus/cerebral peduncle). Posterior cerebral artery (PCA) is the most common arterial infarction produced by compression (a±c). These PCA infarctions are often haemorrhagic, not evident on this MR examination. Further downward displacement of the brainstem structures may cause tearing of the penetrating arteries from the basiliar and the exiting veins. This leads to infarction and haemorrhage in the midbrain and pons (Duret haemorrhages) (c, T2-weighted axial image, showing high signal in the left cerebral peduncle). (e) This shows a time to peak map of cerebral perfusion. ( f) This shows an inverted cerebral blood volume map (i.e. areas of high cerebral blood volume are showed as darker shades of grey). The time to peak maps show areas of slowed perfusion in the watershed areas adjacent to the posterior cerebral artery territory bilaterally. The area of infarction in the right posterior cerebral artery territory has increased cerebral blood volume, so called luxury perfusion, whereas the left posterior cerebral artery territory has reduced cerebral blood volume indicating that it remains oligaemic at the time of the MR examination.
study of secondary prevention after transient ischaemic attack or mild stroke [30]. Also, the risk : bene®t balance for follow-up cerebral angiography to exclude an underlying AVM in a patient with IPH may be altered if there is evidence for an alternative cause. Although less common than haemorrhage related to hypertensive disease, in the older population cerebral pial arteriovenous malformations and aneurysms remain
important dierential diagnoses because of their propensity for rebleeding and the possibility of curative treatment. Large cerebral AVMs are easily demonstrated on CT and MR, but catheter angiography is needed for smaller AVMs and most aneurysms after acute haemorrhage. Due to technical limitations, MR TOF angiography is not of proven practical value in the assessment of parenchymal haematomas. The T1 shortening produced
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by haemoglobin breakdown products may obscure the ¯owrelated signal arising from an underlying cerebral AVM. There is, however, new interest in the area as recent MR angiography developments progress. Both a group in Japan and our own group have found MRDSA of value since it can be used as a subtraction technique that removes the obscuring eect of the haematoma to reveal the AVM (Fig. 2).
Imaging of Subarachnoid Haemorrhage Detection CT is taken to be the reference standard for diagnosing acute SAH and has been shown to be a reliable technique [31]. Infrequently SAH may be dicult to dierentiate from subdural blood on CT but it should be remembered that subdural collections do not track into cortical sulci. There are a number of reasons why SAH may be missed on CT.
First misinterpretation, or second, the anatomical location of the SAH may not be included ( for example, SAH from a posterior interior cerebellar artery (PICA) aneurysm or a spinal arteriovenous malformation). Third, the timing of the CT examination is critical to its sensitivity. On the day of SAH, intracranial blood is detected in about 98% of patients. This proportion declines to 90% after day one, 80% after 5 days and 50% after 1 week [4,32]. Exclusion of SAH on CT requires careful attention to several review areas. These include the basal cisterns, especially in the interpendular fossa and suprasellar cistern, in the dependent portions of the lateral ventricles (occipital horns), the inter-hemispheric ®ssure and also an overall assessment of the symmetry of CSF spaces (Fig. 3). In comparison to CT, all patients with SAH will have xanthochromia of their CSF between 12 hours after and 2 weeks after the haemorrhage [33]. Therefore lumbar puncture is mandatory if CT is negative. Unfortunately, this simple doctrine is frequently overlooked or not
Fig. 2 ± Caption on p. 7.
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Fig. 2 ± MR images from a patient with a subacute parietal parenchymal haematoma. The high signal on the T1 weighted image (a) is consistent with the presence of methaemoglobin in a subacute haemorrhage from the adjacent cluster of abnormal vessels that imply the presence of a cerebral AVM. The T2-weighted image (b) suggests that there is a mixture of intra- and extra-cellular methaemoglobin surrounded by oedema. On the paired diusion weighted images and ADC maps (c) and (d), the surrounding oedema is associated with increased diusion from vasogenic, not cytotoxic oedema. The nidus of an underlying cerebral AVM is visualized on the MRDSA images (e) and ( f), but very poorly on the SLINKY TOF shown in (g).
understood. A recent audit at our institution (unpublished) showed that 24% of patients investigated for possible SAH and normal CT did not have CSF studies. Similar ®ndings have been presented from Cardi [34] and these underline the need for improved education of clinical colleagues by radiologists. The role of MR for SAH remains controversial. It is generally accepted that acute SAH is dicult to detect with conventional MR imaging [35,36]. There are a number of studies suggesting that ¯uid attenuated inversion-recovery (FLAIR) or turbo-FLAIR imaging can detect SAH reliably and is superior to CT for subacute SAH [13,37±42]. The inversion time of water, or CSF, is dependent on its protein content. Once the CSF protein content is above a threshold (determined by the imaging parameters), FLAIR imaging will demonstrate subarachnoid haemorrhage and disease but in a non-speci®c manner [43]. Similarly, protein concentrations also aect CT appearances, for example colloid cysts of the third ventricle are hyperdense because of the high electron density from their proteinaceous contents.
Noguchi has reported 100% detection of acute SAH with FLAIR imaging and a 63% detection rate for chronic SAH [37]. The same group compared CT with MR for subacute and chronic SAH ®nding a CT detection rate of 46% for 37 cases [38,39]. Turbo-FLAIR imaging has been shown to be more sensitive than CT in the detection for small amounts of fresh blood diluted by CSF [44]. This study found that a haematocrit of 27% was required to raise the Houns®eld number suciently for the haemorrhage to be denser than cortical grey matter, whereas a haematocrit of only 22.4% blood was required with an eective TE of 120 ms for the mixture to be more hyperintense than normal cortical grey mater on turbo-FLAIR images. This fell to 9% if the TE was increased to 160 ms. A limitation of SAH imaging with FLAIR sequences is artifactual CSF hyperintensity. Artifactual CSF hyperintensity is prominent in the ventricular system, around the foramina of Munro, the fourth ventricle and basal cisterns, and is due to in¯ow of non-nulled CSF into sections due to
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high CSF ¯ow rates [45]. CSF that moves into a section of the volume to be imaged during the TI interval on a turboFLAIR sequence will not be exposed the inversion pulse, thus producing high CSF signal intensity. Section-selective inversion pulses with a broad bandwidth and the use of cardiac synchronization are some techniques that reduce these artifacts. Regions in which haemorrhage is demonstrated by CT will not necessarily correspond to those observed on MR imaging. The physical state of the haematoma is important as it has dierent consequences for the sensitivity of an investigation to the haemorrhage [46]. It is interesting to note that the use of gradient echo T2* imaging has been reported to be superior to the use of FLAIR alone and the combination of the two was superior to either alone for subacute haemorrhage [13,47]. The regions of abnormal signal on images tended to dier, which may have re¯ected
Fig. 3 ± Images of a 44-year-old man with a sudden onset severe headache with photophobia and nuchal stiness. (a) Unenhanced CT of the head shows high attenuation subarachnoid haemorrhage particularly in the occipital pole of the right lateral ventricle but also in the anterior part of the inter-hemispheric ®ssure. (b) A FLAIR image from an MR examination performed 4 days later shows haemorrhage in both of the lateral ventricles, detected as loss of the normal CSF signal suppression. (c) T2*-weighted image shows the haemorrhage not only in the occipital poles of the lateral ventricles but also in the third ventricle as areas of signal loss. Haemorrhage in the anterior aspect of the inter-hemispheric ®ssure is dicult to appreciate on this section. This example illustrates how the MR sequences can be complementary for detecting SAH.
not just dierent local biochemical changes but also localized dierences in physical state of the haemorrhage, especially in the acute cases. Again this study con®rmed the superiority of MR imaging to CT in the subacute and chronic periods after SAH, but with the two investigations being of comparable sensitivity in patients with acute SAH.
Vasospasm It is likely that vasospasm after SAH is a result of periarterial blood clot. In 1980, Fisher et al. showed that the amount and the location of subarachnoid blood seen on the initial CT is a strong predictor of vasospasm [48]. Angiographic vasospasm is found in 60±70% of patients with heavy cisternal accumulations of blood at 10±12 days after SAH. However, angiographic vasospasm does not always correlate with symptoms and tissue perfusion
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Fig. 4 ± MR images from a 69-year-old patient with a 13-day history of headache presenting with left sided weakness. (a) A fast spin echo T2-weighted image fails to demonstrate any haemorrhage. (b) A T1-weighted image shows subtle raised signal in the right Sylvian ®ssure. The haemorrhage is con®rmed in the gradient echo T2*-weighted image (c) and the FLAIR image (d). The DWI image (e) shows more extensive, bilateral watershed infarction. Oligaemia is shown in the prolonged time to peak in the perfusion map ( f).
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depends on small arteries and arterioles not imaged on angiography [49]. There are several techniques for the evaluation of cerebral blood ¯ow. Transcranial Doppler is easily repeatable, noninvasive and without the complications of cerebral angiography, but many studies have demonstrated the low sensitivity of the technique [50]. The 133Xe technique has been validated and provides reliable measurements [51±53]. The problems of Xe/CT include a relatively high radiation exposure, limited anatomical coverage and diculties arising from the degree of co-operation required from patients. CT perfusion using intravenous iodinated contrast media has also been advocated and prospectively assessment for monitoring vasospasm. Its anatomical coverage is more limited than CT, though clearly multi-slice CT is advantageous compared to single-slice systems [54,55]. Both SPECT and PET have been used to assess vasospasm and appear sensitive [56,57]. In particular, technetium-99m hexamethylpropylene amine oxime (HMPAO) SPECT scanning is widely available and has been used to monitor progression of vasospasm and the eects of therapeutic intervention [58]. Diusion and perfusion weighted MR imaging abnormalities related to vasospasm are present in 64% of SAH cases as early as 4±7 days after haemorrhage [13] (Fig. 4). The use of cerebral perfusion to help determine and monitor clinical management is being explored for Xe/CT by Yonas and others [59].
Investigation of Cause In patients with proven SAH the source of the haemorrhage must be sought and this is usually investigated by catheter angiography. The majority of cases arise from rupture of an intracranial aneurysm, with a minority arising from AVMs. The reference standard for demonstration of the intracranial circulation is conventional selective fourvessel catheter digital subtraction angiography. Although MR angiography methods continue to improve, even highresolution techniques fail to reliably demonstrate aneurysms less than 2 mm, even in the absence of haemorrhage [6,59, 60]. CT angiography also fails to match the resolution of angiography, although good results using the technique have been published [61]. The technique becomes much less reliable for aneurysms less than 5 mm in diameter [5,62]. Part of the information that is ordinarily obtainable from angiography is temporal, for example increased circulation time in cases of vasospasm after SAH or reduced circulation time because of the presence of an arteriovenous shunt. Some steps to temporally resolved MR angiography are being made with magnetic resonance digital subtraction angiography (MRDSA) and other similar techniques, for example time-resolved imaging of contrast kinetics (TRICKS) [63,64]. These techniques are still being developed but cannot currently match either the temporal or the spatial resolution of conventional catheter angiography. About 80% of patients with SAH have a ruptured cerebral aneurysm as the cause demonstrated on the initial four-vessel angiogram, that is 15±20% will have negative angiography [65,66]. In a study to evaluate spiral CT
angiography, 15 of 134 patients had structural causes demonstrated on subsequent imaging not identi®ed on the initial conventional cerebral angiogram [67]. This is 12% (15/128) of those with a structural cause identi®ed by all diagnostic measures and including a post mortem diagnosis. There is a 5.8±11% chance of either an aneurysm or AVM being demonstrated on a repeat angiogram and performing a second angiogram remains standard practice in most institutions [68,69]. There is now a role for MR after repeated angiography or even before the second angiogram for perimesencephalic SAH as in a proportion associated infarcts of perforator territory are demonstrated [70]. There is also evidence that CT angiography is a useful investigation for perimesencephalic haemorrhage and should be used before conventional cerebral angiography is employed [71]. CONCLUSION
CT remains the investigation of choice for the imaging of acute non-traumatic intracranial haemorrhage. For SAH there is also some evidence that CT angiography may be useful, but it is inferior in quality to conventional catheter angiography. For the subacute and chronic stages of SAH, that is 3±4 days after onset, MR imaging including FLAIR and gradient echo T2*-weighted sequences should be used when available. However, delayed lumbar puncture remains mandatory if both CT and MR fail to demonstrate SAH. Diusion and perfusion weighted MR imaging to assess ischaemia and oligaemia may be helpful where the capability exists, Xe/CT or HMPAO/SPECT can be used to similar eect for the assessment of cerebral perfusion. The approach to imaging subacute and chronic IPH is not so clear. The value of a T2*-weighted sequence is proved, but evidence for the use of MR angiography or indeed CT angiography without conventional angiography is still lacking, nor is the clinical role of diusion and perfusion imaging in IPH established. REFERENCES 1 Hoggard N, Wilkinson ID, Griths PD. The imaging of ischaemic stroke. Clin Radiol 2001;56:171±183. 2 New PF, Aronow S. Attenuation measurements of whole blood and blood fractions in computed tomography. Radiology 1976;121: 635±640. 3 Brooks RA, DeChiro G, Patronas N. MR imaging of cerebral haematoma at dierent ®eld strengths: theory and applications. J Comp Asst Tomogr 1989;13:194±206. 4 van Gijn J, van Dongen KJ. The time course of aneurysmal haemorrhage on computed tomograms. Neuroradiology 1982;23: 153±156. 5 White PM, Teasdale EM, Wardlaw JM, Easton V. Intracranial aneurysms: CT angiography and MR angiography for detection prospective blinded comparison in a large patient cohort. Radiology 2001;219:739±749. 6 Velthuis BK, Rinkel GJ, Ramos LM, et al. Subarachnoid hemorrhage: aneurysm detection and preoperative evaluation with CT angiography. Radiology 1998;208:423±430. 7 Cloft HJ, Joseph GJ, Dion JE. Risk of cerebral angiography in patients with subarachnoid haemorrhage, cerebral aneurysm and arteriovenous malformation a meta analysis. Stroke 1999;30: 317±320.
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