Handbook of Practical Medicine Stroke

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 141 4.2 Cerebral arterial supply 141 arteries from the posterior cerebral artery. The potential minimum and maximum areas of supply are shown in Fig. 4.11. 5 Isolated infarction of the ACA territory is comparat- ively rare, other than when due to ‘vasospasm’ com- plicating subarachnoid haemorrhage (section 14.5.1). Part of the explanation may be that if the proximal ACA is occluded, the distal ACA obtains a blood supply from the other ACA, via the ACoA. Most cases of ACA territory infarction are probably due to either cardioembolism or artery-to-artery embolism from an occluded or stenosed 33 internal carotid artery. Bilateral ACA territory infarction should always prompt a search for an ACoA aneurysm which may have bled recently, although it may also be caused by thromboembolism in patients where both ACAs receive their supply from the same carotid artery via the ACoA, or more rarely when the distal branches cross the midline in the inter-hemispheric fissure. 34 (a) Bilateral anterior cerebral artery territory infarction should always prompt a search for an anterior communicating artery aneurysm which may have bled recently. The motor deficit in the leg usually predominates over that in the arm and is often most marked distally, in con- trast to that from cortical middle cerebral artery infarcts. 35 When the arm is affected, this is usually attributed to extension of the ischaemic area to the internal capsule, although in some cases it may also be a form of motor ‘neglect’ through involvement of the supplementary motor area. 33 There is often no sensory deficit, but even when present it is usually mild. When the motor deficit is bilateral, ACA territory infarction needs to be distin- guished from a lesion in the spinal cord or brainstem. Other frontal lobe features may be present, including urinary incontinence, lack of motivation or, paradoxic- (b) ally, agitation and social disinhibition. Abulia and akin- Fig. 4.10 Selective catheter carotid angiogram of the anterior etic mutism (section 3.3.2) may occur, usually with intracranial circulation: (a) anteroposterior projection bilateral lesions. A grasp reflex may be elicited if the (b) lateral projection. 1 internal carotid artery; 2 middle motor deficit in the hand is not too great. Various apha- cerebral artery and its branches; 3 anterior cerebral artery sic syndromes have been described, and these are usually and its branches; 4 ophthalmic artery; 5 anterior choroidal attributed to involvement of the dominant supple- artery; 6 vestigial stump of the posterior communicating mentary motor area (rather than Broca’s area). Typically, artery (normal variant); 7 lenticulostriate arteries. there will be reduced spontaneous output but preserved repetition. These patients may be mute immediately inter-hemispheric fissure and then continue back- after the onset of the stroke. Occlusion of the ACA can wards as the A3 sections, the anterior pericallosal and result in apraxias and other disconnection syndromes 36 callosomarginal arteries. Other branches include the (section 3.3.3). Interruption of the frontocerebellar tracts orbitofrontal, frontopolar, anterior, middle and post- can result in incoordination of the contralateral limbs erior internal frontal, paracentral and superior and which may mimic cerebellar dysfunction, a fact which inferior parietal arteries. The anterior pericallosal arteries in the pre-CT era occasionally resulted in suboccipital may form anastomoses with the posterior pericallosal explorations looking for cerebellar tumours. 37 When .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 142 142 Chapter 4 Which arterial territory is involved? (a) (b) (c) (d) Fig. 4.11 Ischaemia in the territory of the anterior cerebral artery (ACA). (a) The typical appearance on an axial CT brain scan of ACA territory infarction (arrows). However, there is great inter- individual and inter-hemispheric variability in the area supplied by the ACA (b, c). The dark purple areas show the only part of the cortex on the superolateral surface (b) and the medial surface (c) of the hemisphere, which was always supplied by the ACA in a large pathological study. 230 (van der Zwan 1991). The pale purple represents the maximum extent of the area that may be supplied by the ACA in some patients. (d) There is a similar degree of variability for the intracerebral territory supplied by the ACA. The figure shows the minimum (dark purple) and maximum (pale purple) areas of supply at three levels in the same pathological study. (Reproduced with permission from Dr A. van der Zwan.) there is also a corticospinal deficit, it may mimic the Recurrent artery of Heubner lacunar syndrome of homolateral ataxia and crural paresis (see below). 38 Amnesic disorders are also encountered, This artery is an inconstant branch of the ACA, which, particularly after rupture of an ACoA aneurysm. The if present, usually arises at the junction with or just ‘alien-hand sign’ refers to a variety of dissociative move- beyond the level of the ACoA. 41 It may supply the head ments between right and left hands due to a lesion of the of the caudate, the inferior portion of the anterior limb medial frontal lobe and/or corpus callosum. 39,40 of the internal capsule, and the hypothalamus (Fig. 4.12). .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 143 4.2 Cerebral arterial supply 143 lateral part of the Sylvian fissure (Fig. 4.10). The lenticu- lostriate arteries mostly arise from the proximal part of the MCA mainstem (see below). Atheroma may develop in situ, but this is uncommon in whites but perhaps more frequent in people from east Asia (section 6.3.1). Therefore, in whites the mechanism of occlusion tends to be either impaction of an embolus, extension of a more proximal thrombus (e.g. from the internal carotid artery), or less commonly intracranial dissection. 46–48 As far as we know, occlusion of the MCA mainstem is nearly always symptomatic, although some young patients with very good cortical collateral supply may have remarkably few symptoms. In most cases, the occlusion occurs in the proximal mainstem, thereby involving the lenticulostriate arteries, and consequently there is ischaemia of both the deep and superficial territories of the MCA. Typically, this presents as a contralateral hemimotor and sensory deficit, with a homonymous hemianopia and aphasia or visuospatial disturbance depending on which hemisphere is affected. If the cortical collateral supply from the anterior cerebral artery (ACA) and posterior cerebral artery (PCA) is good, the brunt of the ischaemia tends to fall on the sub- cortical structures, resulting in a striatocapsular infarct Fig. 4.12 A CT brain scan showing the typical area of (see below). If the occlusion is more distal in the main- infarction (arrow) resulting from occlusion of the recurrent stem and there is no ischaemia in the lenticulostriate artery of Heubner. territory, the leg may be relatively spared because most fibres to the leg originate in cortical areas usually sup- The characteristic deficit from unilateral occlusion was plied by the ACA and these descend medially in the said to be weakness of the face and arm, often with corona radiata adjacent to the lateral ventricle. 49 dysarthria. 35 However, more recent work suggests that the motor deficit may actually be due to involvement of Middle cerebral artery: deep perforating arteries the medial striate arteries (see below). 42–44 The syndromes (lenticulostriate) of akinetic mutism or abulia (section 3.3.2) may occur but are usually associated with bilateral lesions. Arising from the main MCA mainstem, there are usually between 6 and 12 lenticulostriate arteries, most of which emerge at right angles to their parent artery to enter Anterior cerebral artery: deep perforating arteries the anterior perforated substance. Three groups can be (medial striate) identified – medial, middle and lateral. These may sup- A variable number of small branches from the A1 seg- ply the lentiform nucleus, lateral head of the caudate ment of the ACA and ACoA enter the anterior perforated nucleus, anterior limb of the internal capsule, part of the substance and may supply the anterior striatum, the globus pallidus and lower parts of the internal capsule superior anterior limb of the internal capsule and the (Fig. 4.13). Some, particularly those in the lateral group, anterior commissure. They may also supply the optic have their origins from a cortical branch of the MCA, or chiasm and tract. 45 Occlusion of the medial striate from either the superior or inferior divisions of the MCA. 50 arteries cause weakness of the face and arm. When a thrombus or embolus in the MCA mainstem lies over the origins of all of the lenticulostriate arteries a ‘comma’-shaped infarct (when viewed in the axial Middle cerebral artery: mainstem plane) may develop – a so-called striatocapsular infarct The midle cerebral artery (MCA) is traditionally divided (Fig. 4.14 and see Fig. 6.20) (section 6.7.2). About one- into sections. The first section (M1) passes laterally third to one-half of cases will have a potential cardiac between the upper surface of the temporal lobe and the source of embolism, one-third stenotic or occlusive inferior surface of the frontal lobe until it reaches the disease of the ICA, and one-third stenosis or occlusion .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 144 144 Chapter 4 Which arterial territory is involved? It should be stressed that ‘lacunar infarction’ is a patho- logical term, and for clarity the radiological equivalent is best referred to as a ‘small, deep infarct’. 53 Based on early pathological studies, most occlusions of single, deep per- forating arteries from the MCA mainstem were thought to be caused by local in situ small-vessel disease rather than embolism, although the number of pathologically verified cases was very small. However, more recent pathological and radiological studies have suggested that at least some lacunar infarcts may be caused by a disturbance of blood–brain barrier permeability 54,55 (section 6.4). There is considerable inter-individual variation in the number of lenticulostriate arteries, and in general the largest area is supplied by the most lateral branch. Additionally, the volume of an individual infarct will depend on the actual site of occlusion, i.e. the more proximal the occlusion of the deep perforating artery, the larger the lacune. The tendency for studies not to consider small, deep infarcts greater than 1.5 m diameter as the radiological equivalent of lacunes prob- ably leads to under-reporting, this cut-off size emanating originally from pathological studies. 56 When the results of acute imaging and subsequent autopsy have been compared directly, the lesion at autopsy was signific- antly smaller than that seen on brain imaging. 57 Single lacunes may present with one of the classical ‘lacunar syndromes’ (section 4.3.2) or, rarely, with isolated move- ment disorders, such as hemiballismus. However, the majority of lacunes (80%) are clinically silent (or at least clinically unrecognized), occurring most frequently in Fig. 4.13 Postmortem demonstration of the deep perforating the lentiform nucleus. 56 arteries arising from the mainstem of the middle cerebral artery (arrow). Lacunar infarction is a pathological term, and for clarity the radiological equivalent should probably be confined to the MCA mainstem. 51,52 Angiographic stud- referred to as a ‘small, deep infarct’. ies have shown that MCA mainstem occlusion of this type may be relatively short-lived, presumably due to Multiple supratentorial lacunes, also referred to as état fragmentation of the embolus. 46,47 The deficit in the lacunaire, may present as a pseudobulbar palsy, with or limbs tends to be motor rather than sensory and is often without marche à petits pas. This abnormality of gait similarly severe in the arm and leg. In about 70% there superficially resembles that of Parkinson’s disease, but are symptoms of cortical dysfunction, although these debate continues as to whether a true Parkinsonian syn- may be mild and resolve rapidly. The pathogenesis of the drome can occur from lacunes in the basal ganglia. 58–62 cortical symptoms is much debated but seems most It is important to distinguish état lacunaire from the likely to be due to cortical ischaemia, which is not imaged dilatations of perivascular spaces (état criblé) that are by CT or MR, although it may be detected by functional often present in the basal ganglia of hypertensive indi- imaging, such as position emission tomography (PET) viduals, and which may be difficult to differentiate on and single-photon emission CT (SPECT). 51 The alterna- MR scans 63 (Fig. 4.16). These are not due to infarction tive explanations include deafferentation of the cortex, and have not been convincingly associated with any direct interruption of subcortical–cortical pathways, or particular clinical presentation. involvement of subcortical structures which subserve language functions. Hemianopia is unusual. Middle cerebral artery: cortical branches Occlusion of a single lenticulostriate artery results in a ‘lacunar infarct’ (Fig. 4.15), there being no functional In the sylvian fissure, the M2 section of the MCA usu- anastomoses between adjacent perforating arteries. 50 ally bifurcates into superior and inferior divisions. The .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 145 4.2 Cerebral arterial supply 145 (a) (c) Fig. 4.14 Striatocapsular infarction. (a) The typical appearance of a right striatocapsular infarct on a CT brain scan, axial views (arrows). (b) A T2-weighted axial MR scan, showing a left striatocapsular infarct (arrows) and an MR angiogram (c) from the same patient, showing lack of flow in the proximal segment of the left middle cerebral artery (broad arrow). Normal flow is seen in the right middle cerebral artery (narrow arrow). The patient had had a recent anterior myocardial infarction, and it was presumed that an embolus had lodged in the proximal (b) left middle cerebral artery. (See also Fig. 6.20e) superior division generally gives rise to the orbitofrontal, The branches of the MCA are not often affected by prefrontal, pre-Rolandic, Rolandic, anterior parietal and local atherosclerotic disease although they can be affected posterior parietal branches, while the inferior division by vasculitis, amyloid angiopathy and mycotic aneurysms. usually gives rise to the angular, temporo-occipital, pos- Therefore, the main causes of MCA branch ischaemia terior temporal, middle temporal, anterior temporal and are probably embolism, or low flow, secondary to more temporopolar branches. However, there are many vari- proximal vascular lesions. 46,64 The usual clinical syn- ations in this pattern. The potential minimum and drome resulting from occlusion of the superior division maximum area of supply of these branches is shown is much the same as for the MCA mainstem, but in 5 in Fig. 4.17. At their origins, the luminal diameter of general the motor and sensory deficits are greater in the these vessels is usually about 1 mm, but by the time they face and arm than in the leg. Occlusion of the inferior anastomose with the cortical branches of the anterior division usually causes a homonymous hemianopia or and posterior cerebral arteries, they are usually less than superior quadrantanopia and fluent aphasia (in the dom- 0.2 mm in diameter. 13 There is almost no collateral con- inant hemisphere) but relatively mild problems in the nection between individual branches of the MCA. limbs, although higher-level discriminatory sensory .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 146 146 Chapter 4 Which arterial territory is involved? (a) (a) Lacunar infarct Internal capsule Ventricles Middle cerebral artery Lenticulostriate arteries arising from the middle cerebral artery Anterior cerebral artery Internal capsule (b) Fig. 4.15 Lacunar infarction. (a) The typical appearance of a small, deep infarct confined to the territory of a single, (b) deep perforating artery on a T1-weighted, coronal MR scan Fig. 4.16 The appearance of état criblé: (a) on a T2-weighted (curved arrow). (b) A diagrammatic representation of the case, MR brain scan (arrows); (b) in a pathological specimen. demonstrating the likely underlying vascular process (coronal brain section); one of the lenticulostriate arteries is occluded (broken line). .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 147 4.2 Cerebral arterial supply 147 (a) (b) Fig. 4.17 Ischaemia in the territory of the middle cerebral artery (MCA). (a) The typical appearance on a CT brain scan of extensive MCA territory infarction (arrows) in a patient who had an occluded mainstem of the MCA. (b) The typical appearance on a T2-weighted MR scan of MCA branch occlusion (arrows). (c) The patient whose scan is shown in (b) was a young man with dissection of the proximal internal carotid artery (ICA) (arrow) in a road accident. The intra-arterial digital subtraction catheter angiogram shows a smooth, tapering, complete occlusion of the proximal ICA, typical of dissection. (c) functions may be affected. A similar pattern can, how- reports do not deal with deficits in the acute phase of ever, occur with occlusion of the posterior cerebral artery stroke. (section 4.2.3). The area of infarcted cortex may be very small, so small that the distinction on CT from cortical Middle cerebral artery: medullary perforating arteries atrophy can be difficult (section 5.4.2). As a result, some very restricted clinical deficits occur. For example, it has Medullary perforating arteries arise from distal branches been shown that isolated arm weakness is more likely to of the middle cerebral artery (MCA) on the surface of occur from a cortical than a subcortical lesion. 65–67 the hemispheres. They are usually 20–50 mm in length Although there is a large volume of classical neuro- and descend to supply the subcortical white matter (i.e. logical literature correlating various restricted ‘MCA’ centrum semiovale), converging centripetally towards syndromes (most of which include some disturbance of the lateral ventricle 70 (Fig. 4.18). These are functional higher cortical function) with ischaemia or haemorrhage end-arteries, and their distal fields are part of the internal in specific areas of brain parenchyma, the inter-individual boundary zone (section 4.2.4). variability of the vascular anatomy means that it is virtu- Isolated, acute infarcts of the centrum semiovale ally impossible to link them reliably with occlusions of are thought to be uncommon but are probably being particular MCA branches. 68,69 Furthermore, many of the recognized more often with the greater use of MR .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 148 148 Chapter 4 Which arterial territory is involved? (d) (e) Fig. 4.17 (continued) (d) However, there is great inter-individual and inter-hemispheric variability in the area of brain supplied by the MCA. The dark purple area shows the only part of the cortex on the lateral surface of the hemisphere which was always supplied by the MCA in a large pathological study. 230 (e) There is a similar degree of variability for the intracerebral territory supplied by the MCA. The figure shows the minimum (dark purple) and maximum (light purple) areas of supply at three levels in the same pathological study. (Reproduced with permission of Dr A. van der Zwan.) diffusion-weighted imaging. 71,72 The majority are small 4.2.3 Posterior (vertebrobasilar) system (<1.5 cm in diameter) and probably arise from occlusion of a single medullary perforating artery, although this The vertebrobasilar (VB) system develops quite separ- has never been verified pathologically. The spectrum ately from the carotid system and is subject to many of clinical presentation is similar to that of single more changes during gestation. It is this that probably deep MCA perforating artery (i.e. lenticulostriate artery) accounts for the much greater variation in arterial occlusions, with the classical lacunar syndromes of pure configuration within the VB than in the carotid sys- motor stroke, sensorimotor stroke and ataxic hemiparesis tem, and this may contribute to the development of predominating. In such cases, there is rarely evidence of ischaemia. 74 large-vessel disease or cardioembolism. Larger infarcts in this area present with a syndrome similar to more exten- Extracranial vertebral artery sive MCA cortical infarction, with weakness/sensory loss which is more marked in the face and arm than leg, The right vertebral artery (VA) arises as the first branch aphasia or visuospatial disturbance and, if the optic of the right subclavian artery (which arises from the radiation is involved, a visual field defect. These are innominate artery), while the left VA arises as the first more often associated with large-vessel disease (internal branch of the left subclavian artery (which arises directly carotid artery/MCA occlusion or stenosis). However, from the aortic arch) (Figs 4.3 and 4.19). The course of such infarcts may in fact be in the internal boundary the VA is traditionally divided into sections. The V1 sec- zone, particularly when there are multiple lesions. 72,73 tion is from the origin to the transverse foramen at either The explanations for deficits of ‘cortical’ modalities C5 or C6. The V2 section is within the transverse for- are similar to those for striatocapsular infarction, i.e. amina from the C5/6 level to C2. The V3 section circles ischaemia without necrosis, deafferentation of the cor- the arch of C1 and passes between the atlas and occiput. tex, or involvement of subcortical structures subserving The major branch outside the skull is the single, midline ‘cortical’ functions, but there is little evidence to support anterior spinal artery, formed by a contribution from any of them. both VAs. .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 149 4.2 Cerebral arterial supply 149 The origin of the VA can be affected by atheroma, either within the VA itself or by overlying plaque in the innominate or subclavian arteries, and may be the site of occlusion or a source of emboli. 75,76 It may also be involved in inflammatory disorders, such as Takayasu’s arteritis (section 7.3.2) and be the site of arterial dis- section) (section 7.2.1). Trapping of the VA by cervical spondylosis is frequently cited as a cause of symptoms attributed to ‘vertebrobasilar insufficiency’, but in real- ity, both the symptoms (which are generally non-focal) and the X-ray changes of cervical spondylosis are very common in older people, and rarely is there a convinc- ing cause-and-effect relationship (section 7.1.5). How- ever, thrombus may form in the VA after prolonged or unusual neck posturing. 77,78 Intracranial vertebral artery The V4 section of the vertebral artery (VA) is intracranial, until the two arteries unite to form the midline basilar artery at the pontomedullary junction (Fig. 4.19). As the VAs pierce the dura, there is a decrease in the thickness of the adventitial and medial layers, with marked reduction in both medial and external elastic laminae. There may be branches which supply the medulla. As with the ICA, occlusion of a VA may be asymp- tomatic. At the other extreme, there may be extensive infarction of the lateral medulla and inferior cerebellar Fig. 4.18 Pathological demonstration of the medullary hemisphere. Atheroma is a common cause of stenosis perforating arteries arising from the cortical surface (courtesy or occlusion. 79 Dissection of the intracranial VA may of Dr Nigel Hyman, Taunton, UK). present with subarachnoid haemorrhage ( sections 7.2.2 Fig. 4.19 Angiographic demonstration of the vertebrobasilar arterial system. (a) Anteroposterior projection of an MR angiogram, showing the extracranial vertebral arteries. The numbers refer to the segments of the artery; (0) the origin; (1) the precanal portion; (2) the intracanalicular part; (3) the horizontal part. The large arrow shows an intravertebral disc. (b) Lateral projection of an intra-arterial catheter angiogram, showing (1) the distal vertebral artery; (2) the posterior inferior cerebellar artery; (3) the basilar artery; (4) the anterior inferior cerebellar artery; (5) the superior cerebellar artery; (6) the posterior cerebral artery. (a) (b) .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 150 150 Chapter 4 Which arterial territory is involved? and 9.1.3). The subclavian steal syndrome, as memor- direct branches from the VA originating between the able as it is rare, occurs when there is haemodynamically origin of the PICA and the basilar artery. 81 There are significant stenosis of the subclavian artery proximal to medial and lateral branches of the PICA, the medial the origin of the VA. In this situation, the direction of branch usually supplying the cerebellar vermis and adja- blood flow is normal in the contralateral VA but reversed cent cerebellar hemisphere and the lateral branch the in the ipsilateral VA, with blood passing into the axillary cortical surface of the cerebellar tonsil and suboccipital artery from the VA. The blood pressure will be lower in cerebellar hemisphere. the affected arm. Exercise of the ipsilateral arm increases Historically, occlusion of the PICA has been linked the flow away from the brainstem, which may cause to lateral medullary infarcts, causing Wallenberg’s syn- neurological symptoms. However, it is noteworthy that drome. This consists of an ipsilateral Horner’s syndrome reversed flow in VA is a common finding on ultrasound (descending sympathetic fibres), loss of spinothalamic and angiographic studies in patients with no neuro- function over the contralateral limbs (spinothalamic logical symptoms at all. 80 tract) and ipsilateral face (descending trigeminal tract), vertigo, nausea, vomiting and nystagmus (vestibular Reversed flow in one vertebral artery is a common nuclei), ipsilateral ataxia of limbs (inferior cerebellar finding in patients with no neurological symptoms – it peduncle) and ipsilateral paralysis of palate, larynx and is very rare to find a patient who has symptoms of the pharynx (nucleus ambiguus), resulting in dysarthria, subclavian steal syndrome. dysphonia and dysphagia. As with other ‘classical’ eponymous brainstem syndromes, the complete form of Wallenberg’s syndrome is relatively infrequent in Posterior inferior cerebellar artery clinical practice. Indeed, syndromes which do not The posterior inferior cerebellar arteries (PICAs) usu- involve the lateral medulla but only the cerebellum ally arise from the intracranial vertebral arteries (VA), are now recognized as being more frequent. These although one may be absent in up to 25% of patients usually present with vertigo, ataxia (of gait and limbs), (Figs 4.19 and 4.20). Also, the VA may terminate in the nystagmus and headache. Another striking symptom PICA, i.e. there is no distal connection with the basilar is ipsilateral axial lateropulsion, which seems to the artery. Small branches from the PICA may supply the patient like lateral displacement of their centre of gravity lateral medulla, but more frequently it is supplied by or being pushed to one side, although this can also Internal carotid Anterior cerebral artery Temporal lobe artery Middle cerebral artery Posterior communicating artery Fig. 4.20 Arterial supply of the cerebellum. The brainstem, cerebellum and inferior surface of Superior cerebellar Posterior cerebral artery the temporal and occipital lobes viewed from artery anteroinferiorly. The cerebellum, on the left- hand side of the drawing, has been cut away to Pons reveal the inferior temporal and occipital lobes. Three major pairs of arteries supply the cerebellum: the superior cerebellar, the anterior Basilar inferior cerebellar (both branches of the basilar) artery and the posterior inferior cerebellar arteries Perforating (branch of the vertebral arteries). Perforating arteries branches of the basilar artery supply the pons. The medial parts of the medulla are supplied by the anterior spinal artery and the lateral parts by branches of the vertebral arteries. The posterior cerebral arteries supply the posteromedial Occipital lobe Anterior inferior temporal lobes and the occipital lobes. The cerebellar artery superior surface of the cerebellum (not shown) Vertebral artery Anterior spinal Posterior inferior is predominantly supplied by the superior artery cerebellar artery cerebellar arteries. .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 151 4.2 Cerebral arterial supply 151 occur with ischaemia in the territories of the anterior Sometimes the basilar artery becomes elongated (and inferior and superior cerebellar arteries. 82 Isolated therefore tortuous) and dilated (Figs 4.21 and 6.5). This is vertigo has been reported in cases of PICA territory known as dolichoectasia, and its importance may have infarction but it is difficult if not impossible to distin- been underestimated 90–92 (sections 6.3.6 and 9.1.4). guish the few cases of vertigo due to cerebellar stroke There are five potential consequences: from the many more commoner causes of vestibular • the dilated artery may directly compress the brain- dysfunction unless the patient remains ataxic after stem, resulting in a mixture of cranial nerve and long any rotational component has settled, and there is an tract signs; appropriate infarct on brain imaging 81,83,84 (section • the disruption of laminar flow predisposes to in situ 3.3.7). Infarcts restricted to the territory of either the thrombosis, which may occlude the origins of the medial or lateral branches of the PICA usually cause less paramedian or long circumferential branches; impairment. 82,85 • there may be distal embolization from areas of in situ thrombosis; • the changes in contour of the basilar artery may result in Basilar artery distortion around the origins of the perforating arteries; The general pattern of branching from the basilar artery • the artery may rupture causing a subarachnoid is of short paramedian (perforating) branches, which haemorrhage. supply the base of the pons to either side of the midline and also the paramedian aspects of the pontine teg- Anterior inferior cerebellar artery mentum. The lateral aspects of the base of the pons and the tegmentum are supplied by pairs of short and long The anterior inferior cerebellar arteries (AICAs) arise circumferential arteries, which also supply the cerebellar from the proximal basilar artery (Figs 4.19 and 4.20) and hemispheres. The frequency of infarction from occlu- give off branches to the upper medulla and base of the sion of such perforating arteries has probably been pons before supplying the anterior cerebellar structures. underestimated, partly because of the difficulty of imag- In most people, they also give rise to the internal audi- ing such infarcts in the pre-MRI era. tory arteries, but these may come directly from the Occlusion of a single paramedian artery, resulting in basilar artery or, occasionally, the superior or posterior a restricted infarct in the brainstem, can present with inferior cerebellar arteries. The internal auditory arteries any of the classical lacunar syndromes (section 4.3.2). are effectively end-arteries. Disturbances of eye movement (either nuclear or inter- The internal auditory arteries supply the seventh and nuclear) may also occur from such lesions, either in eighth cranial nerves within the auditory canal and, on isolation or in addition to pure motor deficits (e.g. entering the inner ear, divide into the common cochlear Weber’s syndrome). 86,87 Unlike the anterior circulation, and anterior vestibular arteries. The common cochlear where intrinsic disease of the anterior cerebral or middle artery then divides into the main cochlear artery, which cerebral artery mainstem is uncommon, occlusion of supplies the spiral ganglion, the basilar membrane the mouth of a single perforating artery by a plaque structures and the stria vascularis, while the posterior of atheroma in the parent basilar artery needs to be vestibular artery supplies the inferior part of the saccule considered alongside intrinsic small-vessel disease as the and the ampulla of the semicircular canal. The anterior underlying mechanism. 88 The ‘locked-in syndrome’ vestibular artery supplies the utricle and ampulla of the occurs with bilateral infarction, or haemorrhage, of the anterior and horizontal semicircular canals. 93 base of the pons (section 3.3.2). Isolated occlusion of the AICA is probably relatively The ‘top of the basilar syndrome’ is a constellation of uncommon, but when it does occur there is almost symptoms and signs that may occur when an embolus always infarction in both the cerebellum and pons. 94 impacts in the distal basilar artery, resulting in bilateral Symptoms tend to be tinnitus, vertigo and nausea, with ischaemia of upper brainstem structures and of the an ipsilateral Horner’s syndrome, an ipsilateral nuclear posterior cerebral artery territories. 89 The syndrome con- facial palsy, dysarthria, nystagmus, ipsilateral trigeminal sists of altered pupillary responses, supranuclear paresis sensory loss, cerebellar ataxia (in the ipsilateral limbs) of vertical gaze, ptosis or lid retraction, somnolence, and sometimes a contralateral hemiparesis (i.e. similar hallucinations, involuntary movements such as hemi- to the lateral medullary syndrome with the seventh ballismus, visual abnormalities such as cortical blind- and eighth nerve lesions replacing those of the ninth ness (from involvement of the occipital lobes), and an and tenth nerves and a hemiparesis). Ischaemia in the amnesic state (from involvement of the temporal lobes territory of the internal auditory artery is probably an or thalamus). under-recognized cause of sudden unilateral deafness, .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 152 152 Chapter 4 Which arterial territory is involved? which may occur in isolation, as may vertigo 95,96 (sec- tion 3.3.7). Occlusion of the AICA is probably most often secondary to atherothrombosis in the basilar artery. Superior cerebellar artery The superior cerebellar arteries (SCAs) arise from the basilar artery immediately before its terminal bifurcation (Figs 4.19 and 4.20). They usually supply the dorsolateral midbrain and have branches to the superior cerebellar peduncle and superior surface of the cerebellar hemi- spheres. The ‘classical’ syndrome of occlusion of the whole territory of the SCA includes an ipsilateral Horner’s (a) syndrome, limb ataxia and intention tremor, with con- tralateral spinothalamic sensory loss, contralateral upper motor neurone type facial palsy and sometimes a con- tralateral fourth nerve palsy. In its pure form, it is rare. However, it is often associated with other infarcts in the distal territory of the basilar artery, and may have a poor prognosis. 97 Infarcts that only involve the cerebellar territory of the SCA, on the other hand, have a better prognosis. 98,99 In these cases, headache, limb and gait ataxia, dysarthria, vertigo and vomiting are most pro- minent, but cases with some of these deficits in isola- tion have been reported, due to occlusion of the distal branches. 100 Vertigo is much less common in SCA than posterior or anterior inferior cerebellar artery territory infarction. 85 Embolism (either cardiac or artery-to-artery) is considered the most frequent cause of both complete and partial SCA territory infarcts. The arterial supply of the cerebellum The cerebellum is supplied by the three long circum- ferential arteries described above: posterior inferior cerebellar artery (PICA), anterior inferior cerebellar artery (AICA) and superior cerebellar artery (SCA). The PICA usually supplies the inferior surface, the AICA the anterior surface and the SCA the superior, tentorial sur- face (Fig. 4.20). Territorial infarction is considered most likely to be caused by thromboembolism, particularly from the heart or the basilar artery. However, these arterial systems also have perforating arteries. Cortical (b) infarction in the cerebellum is of two types: infarction Fig. 4.21 (a) An axial CT brain scan, showing dolichoectasia perpendicular to the cortical rim at the boundary zone of the basilar artery extending into the cerebellopontine between perforating arteries (which lack anastomoses); angle (curved arrow). At this stage, the patient presented with and infarction that parallels the cortical rim and is the trigeminal neuralgia. (b) Postmortem demonstration of the boundary zone between the SCA and PICA. Small, deep vertebral artery (closed arrows) and basilar artery (open arrow) in the same patient 2 years later, after massive infarction of the infarcts occur within the deep white matter of the cere- brainstem and cerebellum. bellar hemispheres, usually around the deep boundary zones. Unlike other small, deep infarcts, the predomin- ant cause may be low flow without acute occlusion as a result of large-vessel atherothrombosis 101 (Fig. 4.22). .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 153 4.2 Cerebral arterial supply 153 (a) (b) (d) (c) Fig. 4.22 A montage of MR scans and one CT scan, showing (medial branch of PICA). (c) A cortical infarct in the left PICA various cerebellar infarcts (arrows). (a) Small cerebellar cortical territory . (d) A left cerebellar cortical infarct (lateral branch of infarcts in the posterior inferior cerebellar artery (PICA) superior cerebellar artery). territories. (b) A unilateral small right cerebellar cortical infarct .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 154 154 Chapter 4 Which arterial territory is involved? (e) (f) Fig. 4.22 (continued) (e) An infarct in the left brainstem just CT scan, showing a left superior cerebellar infarct (medial inferior to the pons (perforating branch of basilar artery). (f) A branch of the superior cerebellar artery). choroidal artery (PChA), both of which supply the thala- Cerebellar infarction may be misdiagnosed as mus. Once the PCA has passed around the free medial ‘labyrinthitis’, or even upper gastrointestinal disease if edge of the tentorium, it usually divides into two, with a nausea and vomiting are prominent. total of four main branches. The anterior division gives rise to the anterior and posterior temporal arteries, while Posterior cerebral artery from the posterior division the calcarine and parieto- The two posterior cerebral arteries (PCAs) are usually the occipital arteries arise. The posterior pericallosal arteries terminal branches of the basilar artery (Figs 4.19 and 4.20) are usually branches of the parieto-occipital arteries, and and their course is traditionally described in sections. pass anteriorly to form a potential anastomosis with the The precommunicating (i.e. before the posterior com- anterior pericallosal arteries from the anterior cerebral municating artery; PCoA) P1 section of the PCA passes artery. The potential minimum and maximum areas of around the cerebral peduncle and comes to lie between supply of these branches are shown in Fig. 4.23. 230 During the medial surface of the temporal lobe and the upper early fetal development, the internal carotid artery (ICA) brainstem. From this section, small paramedian mesen- supplies most of the posterior aspect of the cerebral cephalic arteries and the thalamic–subthalamic arteries hemispheres and brainstem through the PCoA. In some arise to supply the medial midbrain, the thalamus and adults this pattern persists, with only a vestigial basilar part of the lateral geniculate body. In about 30% of indi- artery–PCA connection, and in about 30% one or both viduals, these vessels arise from a single pedicle and PCAs are supplied from the ICA, via the PCoA 29,30 (sec- therefore bilateral midbrain infarction can result from tion 4.2.2). a single PCA occlusion. After the PCoA (from which the Occlusions of the PCA origin are probably most often polar arteries to the thalamus usually arise), there are embolic from the heart or proximal arterial atheroma, usually the thalamogeniculate arteries and the posterior and they are also due to the arrest of an embolus at the .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 155 4.2 Cerebral arterial supply 155 (a) (b) (c) Fig. 4.23 Ischaemia in the territory of the posterior cerebral artery (PCA). (a) The typical appearance on a T2-weighted MR scan of (d) PCA territory infarction (arrows). However, there is great inter-individual and inter- hemispheric variability in the area supplied by the PCA (b, c). The dark purple areas show the only part of the cortex on the lateral surface (b) and the medial surface (c) of the hemisphere, which was always supplied by the PCA in a large pathological study. 230 The pale purple represents the maximum extent of the area which may be supplied by the PCA in some patients. (d) There is a similar degree of variability for the intracerebral territory supplied by the PCA. The figure shows the minimum (dark purple) and maximum (pale green) areas of supply at three levels in the same pathological study. (Reproduced with permission of Dr A. van der Zwan.) .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 156 156 Chapter 4 Which arterial territory is involved? basilar bifurcation which then fragments. 89,102,103 As Caudate nucleus with occlusion of the mainstem of the middle cerebral artery (MCA), ischaemia can occur in both the deep and superficial territory of the PCA. Occlusion of the Lateral ventricles Lentiform nucleus deep perforating branches results in ischaemia of the thalamus and upper brainstem, as described below. Such patients may have a hemiparesis in addition to their Anterior Posterior communicating visual defects and so mimic extensive MCA territory artery infarction. 104–106 Visual field defects are the most com- b monly encountered syndrome from PCA infarction. A Medial Lateral macular-sparing homonymous hemianopia is explained To other by collateral flow from the MCA supplying the occipital thalamus pole. 107 More restricted infarcts can result in small Posterior homonymous sectoranopias. Bilateral occipital infarc- a c d tion may result in cortical blindness. When visual func- tion is less severely affected, disorders of colour vision To midbrain (discrimination, naming) may be apparent. Transient Posterior cerebral artery ischaemia in the PCA territory may sometimes give ‘pos- itive’ visual phenomena which are very similar to those Basilar artery of classical migraine. 108 Visual perseverations, such as seeing an object several times despite continued fixa- Fig. 4.24 Diagrammatic representation of the arterial supply of the thalamus, showing the anterior, medial, lateral and tion, and continuing to see an object as an after-image posterior nuclei. The branches are: (a) thalamic–subthalamic (palinopsia) can also occur. 109 Disorders of language (paramedian, thalamoperforating, posterior internal optic) function can also arise from PCA territory infarction, arteries (in addition to the thalamus, branches supply the probably due to involvement of the thalamus (see below) midbrain, and in about 30% the branches to the thalamus or its projection fibres. Alexia, with or without agraphia, in the other hemisphere arise from a common pedicle); results from a dominant hemisphere PCA occlusion (b) polar (tuberothalamic, anterior internal optic) arteries; (section 3.3.3). Amnesic disorders occur because of direct (c) thalamogeniculate arteries; (d) posterior choroidal arteries. involvement of the temporal lobes, the thalamus, or the mamillothalamic tract 110 (section 3.3.3). Typically, there is marked amnesia for recent events. Non-dominant In addition to supplying the thalamus, branches also hemisphere PCA territory infarcts may result in disorders go to the upper midbrain. In 30% of people, the of visuospatial function. branches to both sides of the thalamus have a common pedicle from just one PCA. 113 They supply the postero- medial thalamus, including the nucleus of the medial Arterial supply of the thalamus longitudinal fasciculus, the posterior dorsomedial nucleus The thalamus is involved in about one-quarter of all and the intralaminar nuclei. The typical syndrome of posterior circulation ischaemic strokes, either in isola- unilateral infarction is of acute reduction of conscious tion following perforating artery occlusion, or in com- level, neuropsychological disturbances such as apathy, bination with other structures following large artery disorientation and memory dysfunction, and impaired thrombosis or artery-to-artery embolism. 111 The blood upgaze, with little or no motor or sensory disturbance. supply to the thalamus comes from four groups of arter- The neuropsychological abnormalities are difficult to ies, which over the years have, confusingly, been called distinguish from cortical syndromes and they also have a by several different names 112 (Fig. 4.24). Unlike other wide non-stroke differential diagnosis. The symptoms lacunar infarcts, those in the thalamus are associated resulting from bilateral infarcts due to occlusion of a with a wide range of clinical syndromes, which can make common vascular pedicle are similar to those from uni- clinical localization difficult. lateral infarction, but are usually much more severe. Hypersomnolence can persist for many weeks, presumably due to involvement of the intralaminar nuclei and rostral thalamic–subthalamic arteries (also known fibres of the reticular activating system. Additionally, as paramedian, thalamoperforating and the syndrome of akinetic mutism can occur (section posterior internal optic arteries) These arise from the proximal posterior cerebral artery 3.3.2). Amnesic syndromes are most likely to occur when (PCA). They are usually 200–400 µm in luminal diameter. there is involvement of the dorsomedial nucleus, and .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 157 4.2 Cerebral arterial supply 157 mood disturbances may mimic frontal lobe syndromes. proprioceptive loss. The Déjerine–Roussy syndrome is Thalamic dementia consists of impaired attention, slowed caused by more extensive lateral thalamic infarction and responses, apathy, poor motivation and amnesia. is sometimes referred to as the syndrome of the thalamo- geniculate pedicle. 120,121 It consists of a mild hemipare- The neuropsychological abnormalities caused by sis, marked hemianaesthesia, hemiataxia, astereognosis ischaemia in the territory of the thalamic–subthalamic and frequently paroxysmal pain/hyperaesthesia (often arteries are difficult to distinguish from cortical of delayed onset) and choreoathetotic movements, all syndromes and they also have a wide non-stroke contralateral to the lesion. The original cases had exten- differential diagnosis. sion of the infarcts into the internal capsule and towards the putamen, although most of the features of this syn- drome result from involvement of the ventroposterior polar arteries (also known as tuberothalamic nucleus and ventrolateral nucleus of the thalamus. and anterior internal optic arteries) These usually arise from the posterior communicating Finally, there is the supply from the medial and lateral artery, although in about 30% of people the artery is posterior choroidal arteries (PChAs), which also arise absent and the blood supply comes from the thalamic– from the posterior cerebral artery. These supply the subthalamic arteries. The polar arteries supply the pulvinar and posterior thalamus, the geniculate bodies anteromedial and anterolateral areas, including the and the anterior nucleus. Involvement of the PChA dorsomedial nucleus, the reticular nucleus, the mamillo- presents typically with visual field deficits (upper or thalamic tract and part of the ventrolateral nucleus. lower homonymous quadrantanopia, and rarely homo- These nuclei have substantial connections with the nymous horizontal sectoranopia), with or without frontal lobes, and the dorsomedial nuclei link with hemisensory loss. Some cases have associated neuro- medial temporal lobe structures. The deficits from polar psychological deficits such as transcortical aphasia and infarcts are mainly neuropsychological; patients tend disturbance of memory function. 122 to be rather apathetic and lack spontaneity. Typically, The thalamic arteries were traditionally considered to left-sided infarcts result in an aphasia that is non-fluent, be end-arteries, but functional anastomoses probably do with poor naming but preserved comprehension and occur. 111 It is perhaps for this reason that the vascular repetition, and impaired learning of verbal material. 114 pathology underlying thalamic infarcts is much more Right-sided infarcts result in hemineglect syndromes variable than that of other lacunar infarcts. and impaired visuospatial processing. Polar infarcts, par- ticularly if bilateral, may result in acute amnesia. 115 4.2.4 Arterial boundary zones Arterial boundary zones may be defined as those areas of thalamogeniculate arteries These are the five or six small branches arising from the the brain where the distal fields of two or more adjacent more distal posterior cerebral artery, equivalent to the arteries meet (section 6.7.5). The potential clinical rel- lenticulostriate arteries of the middle cerebral artery evance is that one might predict that these areas would and are usually 400–800 µm in luminal diameter. They be particularly vulnerable to haemodynamic stresses, supply the ventrolateral thalamus, including the ventro- such as hypotension and low focal or global cerebral per- postero-lateral (VPL) and ventro-postero-medial (VPM) fusion pressure. There are two types of boundary zone: nuclei, i.e. the specific relay nuclei for motor and sen- • those where there are functional anastomoses between sory functions. Pure sensory stroke is a typical lateral the two arterial systems, e.g. on the pial surface thalamic deficit due to ischaemia in the territory of a between the major cerebral arteries, and to a lesser thalamogeniculate artery (section 4.3.2). There may be extent at the base of the brain between the choroidal a full hemianaesthesia or partial syndromes such as circulations; 13 hand and mouth (cheiro-oral), hand, foot and mouth • those at the junction of the distal fields of two non- (cheiro-podo-oral) and pseudoradicular sensory loss 116,117 anastomosing arterial systems, e.g. deep perforating (section 3.3.5). The deficit can involve all modalities, and pial medullary perforating arteries in the centrum or spare pain and temperature sensation. 118 If there is semiovale. 123 extension to the internal capsule, a sensorimotor stroke With the former, the boundary zone will occur at occurs 119 (section 4.3.2). Hemiataxia is also a typical fea- points of equal pressure between the two arterial sys- ture of involvement of the contralateral ventrolateral tems. Consequently, changes in arterial pressure in one nucleus, because of interruption of fibres in the dentato- of the systems may result in a shift of the boundary zone rubro-thalamic pathway. The clinical features are rather towards the compromised artery (Figs 4.11, 4.17, 4.23). like cerebellar dysfunction and are not explained by With the latter, the boundary zone is likely to be more or .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 158 158 Chapter 4 Which arterial territory is involved? Fig. 4.25 Variability of the internal boundary zones. The purple shaded areas represent the minimum areas of intracerebral supply at three levels of the anterior, middle and posterior cerebral arteries in a large pathological study, 230 as shown individually in Figs 4.11d, 4.17e and 4.23d. The adjacent unshaded areas represent the areas of variation within which the boundaries between these territories were found. (Reproduced with permission of Dr A. van der Zwan.) less fixed in the cerebral hemisphere (Fig. 4.25). Both flow), it is in fact the deep or internal boundary zone that types of boundary zone are present in the cerebellum. is most vulnerable to low blood flow. 123,124 However, The impression that might be gained from the clinico- whereas with cortical infarcts the differential diagnosis is radiological literature is that the major boundary zones from distal field embolism, in the subcortical region the occur at symmetrical, predictable sites in the hemi- differential is from intrinsic disease of the perforating 3 spheres (e.g. Damasio ). Consequently, in some classi- arteries, and there are just as many problems with the fications of stroke, imaged infarcts in these areas are anatomical localization of the boundary zones in indi- considered most likely to be haemodynamic rather than vidual patients. 5,72,73 embolic in origin, i.e. due to low flow rather than acute arterial occlusion. But, as has been shown in Figs 4.11, 4.17, 4.23 and 4.25, for both types of boundary zone, there is considerable inter-individual and intra-individual 5 variation. More recent maps of arterial territories have 4.3 Clinical subclassification of stroke taken account of this work. 8,10 Lang et al. 10 used the minimum and maximum areas of middle cerebral artery 5 supply from van der Zwan et al. to assess whether 4.3.1 Introduction imaged areas of infarction distal to a haemodynamic- ally significant internal carotid artery lesion should be Having taken the history and performed a physical regarded as being territorial infarcts or boundary zone examination, the physician should have established infarcts. Using the minimum area of supply, two-thirds which brain functions have been affected by the stroke were considered as boundary zone infarcts, but when the (or, with more difficulty, the transient ischaemic attack). maximum area of supply was considered only one-fifth These clinical findings then need to be used to identify were classified in the same way. We do not believe it is groups of patients in a manner which will bring together always possible to identify ‘typical’ CT or MR patterns the brain and vascular anatomy. The traditional teach- associated with boundary zone infarction, given the ing of cerebrovascular neurology is based on the general very real difficulty of identifying where they are in vivo assumption that particular symptoms and signs arise (section 6.7.5). from restricted areas of damaged brain, which, in turn, receive their vascular supply in a reasonably predictable We do not believe it always is possible to identify manner. This has its origins in the large classical liter- ‘typical’ CT or MR patterns associated with boundary ature describing patterns of neurological deficit which zone infarction. were linked (usually at a later postmortem) with particu- lar vascular lesions, a process that produced a myriad It has been suggested that while cortical boundary of eponymous clinical syndromes. Although these were zone infarcts may have many causes (and not just low of value to those interested in exploring the subtleties .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 159 4.3 Clinical subclassification of stroke 159 of cerebral localization before the advent of PET and Despite being well known, many of the ‘classical’ fMRI, and remain the stock in trade of many neuro- vascular syndromes occur rather infrequently in logists’ clinical demonstrations, most of these ‘classical’ routine clinical practice. vascular syndromes occur infrequently (at least in their pure forms), and even when they do occur they rarely Early clinically based classifications distinguished have a particularly distinctive cause. The sensitivity, anterior (carotid) circulation strokes and posterior (verte- specificity and generalizability of many of the clinico- brobasilar) circulation strokes. 125 It seems reasonable to anatomical correlations have rarely been tested on large, retain this division, because certain investigations (e.g. unselected groups of patients with stroke and they are of carotid duplex) and treatments (e.g. carotid endarterec- limited practical value to most clinicians. Additionally, tomy) are only appropriate to the carotid circulation – the descriptions nearly always relate to ischaemic rather while recognizing that for a number of reasons there can than haemorrhagic strokes and, although one might be considerable overlap of symptoms between the two argue that this is perfectly acceptable in the context of territories (Table 4.3). In terms of the intracranial circula- a high proportion of patients having brain CT or MR tion (both anterior and posterior), there are striking scans, unfortunately there remain a large number of differences between the structure, anastomotic poten- clinicians worldwide who do not have ready access to tial, vascular pathology and functional areas of the brain such technology to make the distinction with certainty. perfused by the main stems of the parent arteries, the Table 4.3 Which arterial territory are the Likely arterial territory neurological problems in? Anterior Either Posterior Dysphasia + Monocular visual loss + Unilateral weakness* + Unilateral sensory disturbance* + Dysarthria† + Ataxia† + Dysphagia† + Diplopia† + Vertigo† + Bilateral simultaneous visual loss + Bilateral simultaneous weakness + Bilateral simultaneous sensory disturbance + Crossed sensory/motor loss + *Usually assumed to be ‘anterior’, but see under lacunar syndromes (section 4.3.2). †In isolation, these symptoms are not normally regarded as indicating a cerebrovascular event (section 3.2.1) Note: whether the neurological symptoms are transient or persistent, and irrespective of whether there are abnormal neurological signs, it can be all but impossible to be sure of which arterial territory is involved, because so often the symptoms are not entirely specific for one particular arterial territory. This is because of individual variation in arterial anatomy and the pattern of any arterial disease affecting the collateral circulation, and because one function can be distributed through both arterial territories (e.g. the corticospinal tract is supplied in the cerebral hemispheres by the anterior circulation and then, in the brainstem, by the posterior circulation). Sometimes brain imaging can help if one particularly recent lesion is found in a relevant place (e.g. if a patient with a hemiplegia has just one infarct in the contralateral pons on MRI, then it is more likely to have been due to posterior than anterior ischaemia, particularly if the infarct looks of an appropriate age). Arterial imaging is unhelpful, because so often a symptomatic lesion in one artery is associated with asymptomatic lesions in other arteries. Arterial bruits are unhelpful for the same reason. .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 160 160 Chapter 4 Which arterial territory is involved? cortical branch arteries and the small, deep perforating occur in areas such as the lentiform nucleus and do arteries (Table 4.2). not present as stroke syndromes, but nonetheless are There is also good evidence that the prognosis of these an important cause of cognitive decline. 127–130 Other groups differs (section 10.2). A case can therefore be lacunes, however, occur at strategic sites such as in the made for further subdividing strokes into those that are: internal capsule and pons, where clinically ‘eloquent’ • restricted to deep, subcortical areas (supplied by small ascending and descending neural tracts are concen- perforating arteries); trated, with the result that an extensive clinical deficit • restricted to superficial cortical areas (supplied by can occur from an anatomically small lesion (sections small pial branch arteries); and finally 3.3.4 and 3.3.5). However, these lesions are much less • those that involve both deep and cortical structures likely to cause an acute disturbance of higher cognitive (implicating the whole area of supply of the parent or visual function than those involving the cortex. cerebral artery). Initially, a small number of clinical syndromes were However, this is likely to be easier and more robust for correlated with relevant lacunes at subsequent post- anterior than posterior circulation events. Next, one mortem. 131–134 These came to be regarded as the ‘clas- needs to consider whether these subgroups can be iden- sical’ lacunar syndromes, and to varying degrees the tified clinically with reasonable reliability. The greatest sensitivity and specificity of these relationships have been amount of information is available for the group of tested using CT/MRI. Since then many other syndromes strokes due to ischaemia in the territory of a single, deep have been reported in association with CT/MR imaged perforating artery, and these will be considered first. small, deep infarcts but rare associations, perhaps due to idiosyncratic individual variations in the vascular anatomy, are of little practical use to clinicians. 87,135 4.3.2 Lacunar syndromes Consequently, the standard classification of subcortical infarction states that the term ‘lacunar syndrome’ should The clinical syndrome be restricted to a clinical situation in which the likely Ischaemia in the territory of a single, deep perforating mechanism of infarction ‘involves transient or perman- artery can cause a restricted area of infarction known as ent occlusion of a single perforating artery with a high a ‘lacune’ (section 6.4) (Fig. 4.26). Technically, it should degree of probability’ – i.e. that this mechanism is the be described as an ischaemic lacune because similar usual cause of a particular syndrome 53 (section 6.7.3). sized areas of tissue destruction can be caused by small haemorrhages. 126 The term ‘lacune’ is a pathological one pure motor stroke and if only cross-sectional imaging is available, the term The association of pure motor deficits and lacunes was ‘small, deep infarct’ is preferred, with the presumption noted early in the 20th century. 63,136 Pure motor strike that the imaged area of infarction is within the territory (PMS) will be described in detail since it is the most fre- of a single perforating artery. 53 In fact, most lacunes quently encountered of all lacunar syndromes (LACS) and exemplifies many of their core features. The clinical ‘rules’ for diagnosing PMS were set out by Fisher and Curry who defined the syndrome as ‘A paralysis com- plete or incomplete of the face, arm and leg on one side unaccompanied by sensory signs, visual field defect, aphasia, or apractagnosia. In the case of brainstem lesions the hemiplegia will be free of vertigo, deafness, tinnitus, diplopia, cerebellar ataxia, and gross nystagmus.’ 131 This definition allowed sensory symptoms but not signs to be present. This puts into clinical terminology the funda- mental neuroanatomical concepts of LACS (Table 4.4). For a patient to present with symptoms and signs that fulfil the above criteria, it is likely that the stroke has been caused by a lesion in an area where the motor tracts are closely packed together, since a lesion of the motor cortex sufficiently extensive to involve the face, arm and leg areas of the homunculus would almost certainly Fig. 4.26 Postmortem demonstration of a lacune (closed arrow) also affect neural pathways subserving higher cognitive in the internal capsule (open arrow) of a coronal brain slice. or visual functions. It was stressed that the definition .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 161 4.3 Clinical subclassification of stroke 161 Table 4.4 Lacunar syndromes. hemiplegia. 57,140 It should be stressed that the definitions used stated that the whole of the arm or leg should be Definition affected, something one suspects is often overlooked. Maximum deficit from a single vascular event The infarcts were in the corona radiata or the junctional No visual field deficit zone between it and the internal capsule, where nerve No new disturbance of higher cerebral function fibres are relatively more dispersed than in the capsule or No signs of brainstem disturbance* pons. 57 Cases with these more restricted deficits are prob- Categories ably best described as ‘partial’ rather than ‘classical’ Pure motor stroke LACS but they still seem most likely to be associated Pure sensory stroke with small, deep infarcts, although many large studies Ataxic hemiparesis (including dysarthria–clumsy hand that have reported on the sensitivity and specificity of syndrome and homolateral ataxia and crural paresis) Sensorimotor stroke clinicoanatomical correlations have combined the two groups. 135,141 To be acceptable as a pure motor, sensory or sensorimotor Although one might go even further and include any stroke, the relevant deficit must involve at least two out of three areas of the face, arm and leg, and, with particular case with a pure motor deficit no matter how anatom- reference to the arm, should involve the whole limb and ically restricted as a PMS, in practice the more restricted not just the hand. a deficit, the more likely it is to arise from a cortical lesion. In most studies of isolated upper or lower limb *Some brainstem syndromes may be caused by lacunar motor deficit, less than a quarter were caused by lacunar infarcts. infarcts although lacunar infarcts may be more likely to cause an isolated facial weakness. 65–67,142 applied to the maximum deficit in the acute phase of a single stroke, a particularly important point in the Only deficits involving the whole of the arm and face context of current hyperacute assessment, but also it did (brachio-facial), or the whole of the arm and leg not apply to less recent strokes where other signs were (brachio-crural), should be accepted as partial lacunar present to begin with but had subsequently resolved. syndromes, not more restricted deficits (e.g. hand only) that are more likely to be of cortical origin. Patients with lacunar syndromes should have no aphasia, no visuospatial disturbance, no visual field pure sensory stroke defect, no clear disturbance of brainstem function and Pure sensory stroke (PSS), the sensory counterpart of no drowsiness at any time after their stroke, unless pure motor stroke, in terms of the anatomical distribu- caused by a coexisting non-vascular condition. tion of the deficit, is encountered much less frequently. Although the definition in the original paper suggested In the original report of nine autopsied cases, six of the that there should be objective sensory loss, in a later lacunes were in the internal capsule and three in the paper Fisher noted that there could be cases with per- pons, which emphasizes the point that the same clinical sistent sensory symptoms in the absence of objective syndrome may occur with occlusion of a perforating signs. 132,143 A single case of a partial PSS has been verified artery arising from the middle cerebral artery (anterior pathologically. 144 As noted in section 3.3.5, lesions circulation) or the basilar artery (posterior circulation). within the thalamus can give characteristic, restricted Since then, cases of PMS have been reported with lacunes syndromes such as hand and mouth (cheiro-oral), and at other sites along the cortico-spinal tract, including the hand, mouth and foot (cheiro-oral-pedal), and although corona radiata, the cerebral peduncle and the medullary the whole of the limb is not affected, these are most pyramid. 137 Although the anatomical distribution of often caused by lacunar infarcts. Overall, most lesions lesions in large series is broadly similar to the original causing PSS are in the thalamus, in keeping with the pathological observations, diffusion tensor imaging is original pathological studies and are the smallest of the beginning to provide more detailed information about symptomatic small, deep infarcts. 145 the impact and possibly prognosis of lacunar infarcts on different parts of the corticospinal tract. 138,139 homolateral ataxia and crural paresis, In the early 1980s, series of cases with slightly more dysarthria–clumsy hand syndrome and restricted pure motor deficits (e.g. weakness of just the ataxic hemiparesis face and arm, or arm and leg) associated with small, deep These syndromes are less generally accepted as ‘classical infarcts on CT were reported – hence our preference LACS’, unlike pure motor stroke and pure sensory stroke, for the term PMS rather than the original pure motor although they were all described at about the same time. .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 162 162 Chapter 4 Which arterial territory is involved? This may be because of the difficulty of interpreting sensorimotor stroke some physical signs and the fact that the syndromes are The inclusion of sensorimotor stroke (SMS) as a classical less common. The original patients with homolateral lacunar syndrome (LACS) is based on a single patient ataxia and crural paresis were described as having weak- with a postmortem, reported almost a decade after the ness of the lower limb, especially the ankle and toes, other classical LACS. 119 This case was due to a lacune a Babinski sign and ‘striking dysmetria of the arm and in the ventroposterior nucleus of the thalamus, but leg on the same side’. 133 In the dysarthria–clumsy hand there was also pallor of the adjacent internal capsule. syndrome, although the deficit was described as being Although there were marked sensory and motor signs ‘chiefly of dysarthria and clumsiness of one hand’, two which persisted, the onset of the sensory symptoms pre- of the three original patients had signs suggestive of ceded the motor ones. There is also postmortem support pyramidal dysfunction in the ipsilateral leg, and both for the view that an infarct primarily within the internal had an ataxic gait. 134 In a later paper, Fisher reported capsule can cause an SMS. 128 A similar syndrome was three further patients who had prominent vertical reported after a small haemorrhage in the same place. 151 nystagmus as well as pyramidal weakness and cerebellar These authors made the point that a sensory deficit can signs, and suggested that a new term, ‘ataxic hemipare- occur from lesions of the posterior limb of the internal sis’, should be used for these cases and those with homo- capsule, presumably by interruption of the thalamo- lateral ataxia and crural paresis. 146 The relevant lacunes cortical pathways. In an MR study, the infarcts in cases of were all in the pons, and he attributed the variable distri- SMS were larger than in other LACS, although they were bution of the weakness in different cases to the involve- still thought to be within the territory of a single per- ment of motor fibres where they are relatively dispersed forating artery. 86 This supported an earlier CT study by the pontine nuclei. It has been reported that if ‘rigid’ which reported that the infarcts in SMS were slightly clinical criteria for dysarthria–clumsy hand syndrome larger and extended more medially than in patients with are used, the syndrome predicts a lesion in the contra- pure motor stroke (PMS), abutting the posterolateral lateral pons but a more recent study which used MR as aspect of the thalamus. 152 In the Stroke Data Bank, in well as CT reported that 40% were in the internal which SMS was the second most frequent LACS after capsule. 147,148 On the other hand, others have suggested PMS, 31% had a lesion in the posterior limb of the inter- that true homolateral ataxia and crural paresis may be nal capsule, 22% had a lesion in the corona radiata, 7% caused most frequently by territorial infarcts in the ante- in the genu of the capsule, 6% in the anterior limb of the rior cerebral artery territory. 38 They also make the point capsule and only 9% in the thalamus. 150 The lesions in that many other cases reported with similar-sized the corona radiata were on average almost twice as large infarcts of the corona radiata on CT have had much as those in the capsule, but both were larger than the more extensive deficits. Another possible explanation corresponding lesions in the PMS group. MR scanning for the syndromes is that there is a second, non-imaged has disclosed that in some CT-negative cases the lesion lesion. The data from detailed MRI studies argue against can be in the medial part of the medulla. 153 this being common. In one study, only 5 of 26 patients (19%) with ataxic hemiparesis had more than one small, The brain lesion deep infarct on imaging, but the figure for patients with PMS in the same study was similar, with 6 of 33 (18%). 86 Table 4.5 summarizes the large studies of the clinico- Another study reported that 10% of patients with ataxic radiological correlations for the various lacunar syn- hemiparesis had a ‘double lesion’. 149 Additionally, in the dromes (LACS) and imaged small, deep infarcts. Overall, Stroke Data Bank study, a history of previous, clinically it must be recognized that about 10% of patients present- apparent stroke was no more common in the ataxic ing with a LACS will have a relevant lesion other than hemiparesis/dysarthria–clumsy hand syndrome group a small, deep infarct or haemorrhage on a scan, which than in those with other LACS. 150 Sensory variants of might explain the neurological symptoms. The propor- ataxic hemiparesis have been reported, but there is no tion of such ‘atypical’ patients does seem to be higher evidence that the anatomical and clinical issues raised for SMS than for the other syndromes, and particular are significantly different from those between PMS and care should therefore be taken with this group. So most sensorimotor stroke (see below). LACS are caused by small deep infarcts or haemorrhages, but not all of them. This inconsistency may be because Limb ataxia does not necessarily imply a cerebellar additional deficits were not recognized by the clinicians stroke in the presence of ipsilateral pyramidal (e.g. visual inattention, visuospatial disturbance) or had signs, but may be caused by a lacunar infarct or resolved by the time of assessment, or because the relev- haemorrhage in the basal ganglia or pons. ant lesion was misclassified on imaging, particularly in .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 163 4.3 Clinical subclassification of stroke 163 Table 4.5 Clinicoradiological correlations of lacunar syndromes. Syndrome, studies Setting Mean time Imaging Number of Non-lacunar infarct on to scan patients imaging (n, %) Pure motor stroke Bamford et al. 214 Community CT 49 1 (2) Hommel et al. 86 Hospital MR 35 0 (0) Melo et al. 215 Hospital CT 121 6 (5) Norrving & Staaf 216 * Hospital CT 123 0 (0) Norrving & Staaf 216 † Hospital CT 52 5 (9) Gan et al. 217 Hospital CT/MR 101 7 (7) Arboix et al. 138 Hospital CT/MR 222 33 (15) Pure sensory stroke Bamford et al. 214 Community CT 7 0 (0) Hommel et al. 86 Hospital MR 12 1 (8) Gan et al. 217 Hospital CT/MR 15 0 (0) Arboix et al. 145 Hospital CT/MR 99 7 (7) Ataxic hemiparesis Bamford et al. 214 Community CT 9 0 (0) Hommel et al. 86 Hospital MR 28 2 (7) Gan et al. 217 Hospital CT/MR 41 1 (1) Sensorimotor stroke Bamford et al. 214 Community CT 43 2 (5) Huang et al. 229 Hospital CT 37 8 (21) Hommel et al. 86 Hospital MR 8 1 (12) Landi et al. 218 Hospital CT 34 3 (11) Lodder et al. 219 Hospital CT 47 5 (11) Arboix & Marti-Vilalta 220 Hospital CT/MR 42 8 (19) Gan et al. 217 Hospital CT/MR 46 1 (2) All lacunar syndromes Wardlaw et al. 183 Hospital CT 19 2 (11) Boiten & Lodder 191 Hospital CT 109 11 (10) Ricci et al. 221 Community CT 56 2 (4) Samuelsson et al. 222 Hospital MR 91 8 (11) Anderson et al. 179 ‡ Community CT 69 12 (17) Kappelle et al. 223 Hospital CT 78 5 (6) All lacunar syndromes: studies using MR DWI Schonewille et al. 224 Hospital 53 h DWI 43 1 (2) Lindgren et al. 225 Hospital 33 h DWI 23 2 (9) Lee et al. 226 Hospital 32 h DWI/MRA 19 4 (21) Gerraty et al. 9 Hospital 9 h DWI/PWI/MRA 19 13 (68) *Classical or †partial pure motor stroke. ‡Retrospective classification from records. MR, magnetic resonance; DWI, diffusion-weighted imaging; PWI, perfusion-weighted imaging. studies performed without the benefit of MR diffusion- territory of single perforating arteries, except in a hand- weighted imaging. ful of cases. Based on the results of postmortem studies, it has traditionally been considered that asymptomatic (smaller) lacunes are probably most often the conse- The vascular lesion quence of occlusion by thickened vessel walls (lipo- Any of the lacunar syndromes (LACS) may be caused by hyalinosis), when the usual diameter of the vessel is less a small haemorrhage, and this accounts for about 5% than 100 µm, while the larger symptomatic lacunes are of cases in community studies. 137 There is no direct probably most often the result of vessel occlusion due to information about the cause of the ischaemia in the complex small-vessel disease or microatheroma, when .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 164 164 Chapter 4 Which arterial territory is involved? the vessel diameter is around 400 µm 127,154 (section 6.4). Table 4.6 Posterior circulation syndromes. Some cases, particularly those in the pons with occlusion of a basilar perforating artery, may be caused by obstruc- At time of maximum deficit, any of: tion of the mouth of the perforating artery by an athero- Ipsilateral cranial nerve (III–XII) palsy (single or multiple) matous plaque within the parent artery. 155 Although an with contralateral motor and/or sensory deficit Bilateral motor and/or sensory deficit embolic mechanism is possible, epidemiological evidence Disorder of conjugate eye movement (horizontal or vertical) suggests that there is a low frequency of severe carotid Cerebellar dysfunction without ipsilateral long tract stenosis or cardiac sources of embolism 156–164 (section deficit (as seen in ataxic hemiparesis) 6.4). More recent pathology and MR studies have sug- Isolated hemianopia or cortical blindness gested that oedema secondary to endothelial dysfunc- tion and the breakdown of the blood–brain barrier may Note that disorders of higher cerebral function (e.g. aphasia, also have a role. 54,55,165 agnosias) may be present in addition to the above features if From the above, it can be seen that a LACS does not the posterior cerebral artery territory is involved. reliably distinguish whether the brain lesion relates to the anterior or posterior systems, although in older series and some schemes of classification it seems likely that vascular surgery. 167 Consequently, at the present time, it would always have been considered as an anterior one must recognize that the posterior circulation syn- circulation stroke (e.g. Rochester, Minnesota). 125,166 It dromes (POCS) are a relatively crude grouping, which has been recognized that small, deep infarcts are the from both a topographic and aetiological perspective usual cause of certain brainstem syndromes (usually encompasses a heterogeneous group of strokes (sec- a pure motor stroke plus a cranial nerve palsy or eye tion 6.7.4). movement disorder) but before simply accepting these The clinical deficits that point to the lesion being in alongside the classical LACS, the even greater paucity the distribution of the posterior circulation are shown of pathological studies should be recognized. 86 As in Table 4.6. Other symptoms and signs that may be noted above, the vascular lesion may be different, with present but are not of any particular localizing value atheroma overlying the mouth of the perforating artery include Horner’s syndrome (which can occur in both being more frequent than in the anterior circulation. 155 carotid and vertebrobasilar strokes), nystagmus, vertigo Consequently, these types of deficit are not generally (which in isolation is rarely due to a stroke), dysarthria included in studies reporting the prognosis of patients (which can occur from lesions anywhere in the motor with LACS, but this position may need to be reviewed in pathways) and hearing disturbance. 168,169 Occasionally, the light of future MR studies. an otherwise typical POCS may be associated with distur- bance of higher cerebral function, e.g. aphasia, agnosias. This should not come as a surprise, given the variable 4.3.3 Posterior circulation syndromes supratentorial territory supplied by the posterior cerebral arteries, and these cases should still be considered as The clinical syndromes 104,105,170 POCS (section 4.2.3). Although there are some clinical syndromes due to well- When diagnosing POCS at the bedside it is useful to localized lesions within the posterior circulation which, consider whether there is involvement of the: along with their eponymous names, are an integral • distal territory, i.e. beyond the top of the basilar artery part of ‘classical neurology’ (e.g. Weber, Millard–Gubler, (visual field defects, higher cerebral dysfunction); Wallenberg), in practice such syndromes are rarely seen • middle territory, i.e. the basilar artery (motor deficits, in their pure form. Indeed, the clinical consequences of cranial nerves III–VII palsies); a given vascular lesion are generally less predictable • proximal territory, i.e. the vertebral arteries (crossed than for arteries in the anterior circulation because of the motor and sensory deficits, lower cranial nerve palsies), greater frequency of developmental vascular anomalies since the mechanisms of stroke in the three areas may and the greater variability of the territory supplied by well differ. 79,170–173 The involvement of more than one individual arteries. Additionally, until the advent of territory, particularly if sequential and/or associated with MRI, clinicoradiological correlation was difficult because fluctuating level of arousal, should raise the suspicion of the poorer performance of CT in the posterior fossa of occlusion of the basilar artery, which may in turn lead compared with the supratentorial compartment, and to consideration of thrombolytic therapy. 174–176 There catheter angiography was also performed much less fre- is probably a tendency for POCS to be underdiagnosed quently than for anterior circulation strokes because in non-specialist centres. In our view, this most often it rarely led to any change in management, such as results from a failure to appreciate that truncal or gait .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 165 4.3 Clinical subclassification of stroke 165 Table 4.7 Clinicoradiological correlations Study Number Appropriate No lesion Inappropriate of posterior circulation syndromes. infarct infarct Bamford 177 * 81 19 (23%) 60 (74%) 2 (2%) Lindgren et al. 178 * 32 12 (37%) 20 (62%) 0 Anderson et al. 179 * 36 16 (44%) 16 (44%) 4 (11%) Wardlaw et al. 183 † 13 8 (62%) 5 (38%) 0 Al-Buhairi et al. 227 † 71 32 (45%) 39 (55%) 0 Mead et al. 228 † 212 105 (50%) 86 (41%) 21 (10%) *Community-based study, first-ever strokes. †Hospital-based study, first-ever and recurrent strokes. ataxia is present, because no one bothers to have the resulting from occlusion of a single perforating artery patient sit or stand up. in the anterior circulation are most likely to be due to intrinsic disease of those vessels, in the posterior circula- tion atheromatous disease in the parent artery may cause The brain lesion a similar brain lesion by occluding the origin of a single In community-based studies between 10% and 18% of perforating artery – a process referred to as ‘basilar branch patients presenting with POCS had an intracerebral occlusion’ (section 4.3.2). It seems likely that, because of haemorrhage. 177–179 The correlation between the clinical the shape of the vertebrobasilar system, emboli are most syndrome and brain imaging in patients with ischaemic likely to arrest either in the distal part of the vertebral stroke is shown in Table 4.7. The ‘inappropriate’ lesions artery or in the upper part of the basilar artery. included a number of supratentorial small, deep infarcts. Given that most of the studies were based on CT, it is 4.3.4 Total anterior circulation syndrome possible that these patients had a further and perhaps therefore relevant infarct in the brainstem that was The clinical syndrome not visible. With the increasing use of MRI, it has become clear that certain brainstem syndromes are usu- The clinical features of the total anterior circulation ally associated with small, deep infarcts, compatible with syndrome (TACS) (Table 4.8) are a hemiplegia (usually ischaemia in the territory of a single basilar perforating with an ipsilateral hemisensory loss), a visual field artery. 86 Of 93 cases of isolated homonymous hemi- deficit on the same side and a new disturbance of higher anopia associated with a vascular lesion, 80 (96%) were cerebral function referable to the same cerebral hemi- attributed to posterior cerebral artery occlusion. 180 sphere. ‘Total’ is used in this context to signify that all the major aspects of supratentorial cerebral function have been affected, and it does not imply necessarily The vascular lesion that there has been infarction in the whole of the anter- Traditionally, pathological series have suggested that ior circulation territory. TACS is very much the equi- within the anterior circulation the ratio of embolism to valent of the terms ‘full house’ and ‘complete middle in situ thrombosis is about 3 : 1, while in the posterior cerebral artery syndrome’ which have been used in other circulation this ratio is reversed. 181 In vivo studies have classifications. 125,152 Some impairment of consciousness questioned this, and it seems likely that at least some is often present, which can make formal testing of higher of the difference is the result of the inevitable selection cortical and visual function difficult. bias that occurs in pathological series. 75,103,172,182 In a large hospital-based registry, 32% of posterior circula- Table 4.8 Total anterior circulation syndrome. tion infarcts were associated with large-artery occlusion, 14% were attributed to artery-to-artery emboli, 24% to At time of maximum deficit, all of: embolism from the heart and 14% to perforating artery Hemiplegia or severe hemiparesis contralateral to the disease. 172 It is important to note that, in whites at least, cerebral lesion atheroma of the intracranial portion of the vertebral Hemianopia contralateral to the cerebral lesion arteries and the basilar artery is much more common New disturbance of higher cerebral function (e.g. dysphasia, visuospatial disturbance) than in the intracranial carotid or middle cerebral arter- +/– sensory deficit contralateral to the cerebral lesion ies. Thus, as noted above, while small deep infarcts .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 166 166 Chapter 4 Which arterial territory is involved? Table 4.9 Clinicoradiological correlations Study Number Appropriate No lesion Inappropriate of total anterior circulation syndromes. infarct infarct Bamford 177 * 55 52 (95%) 0 3 (5%) Lindgren et al. 178 * 54 35 (65%) 15 (28%) 4 (7%) Anderson et al. 179 * 68 44 (65%) 10 (15%) 12 (18%) Wardlaw et al. 183 † 33 31 (94%) 0 2 (6%) Al-Buhairi et al. 227 † 64 40 (62%) 15 (23%) 9 (14%) Mead et al. 228 † 94 69 (73%) 7 (7%) 18 (19%) *Community-based study, first-ever strokes. †Hospital-based study, first-ever and recurrent strokes. was presumed to be because of effective leptomeningeal The brain lesion collaterals (section 6.7.1). This is a similar argument to In community-based studies between 19% and 25% of that relating to striatocapsular infarction (section 4.2.2). patients presenting with TACS had an intracerebral An early angiographic study reported that of 20 pat- haemorrhage. 177–179 The correlation between the clinical ients with extensive hemispheric infarction as judged by syndrome and brain imaging in patients with ischaemic CT, 14 had MCA occlusion and the other 6 had either stroke is shown in Table 4.9. Perhaps the biggest ‘catch’ occlusion or more than 75% stenosis of the ipsilateral is the well-described ability of posterior cerebral artery internal carotid artery (ICA). 46 Later studies of patients (PCA) territory ischaemia to produce a TACS; 104–106,183 with non-haemorrhagic TACS who had an early carotid the patients generally have a relatively mild hemiparesis duplex examination reported that more than one-third but marked aphasia (not always fluent) and a visual field had either occlusion or a high-grade stenosis of the ICA deficit. The motor deficit occurs because of involvement ipsilateral to the cerebral lesion, and many of the others of the small, perforating arteries arising from the proxi- had a major cardiac source of embolism. 160,164 In the mal PCA, which supply the upper midbrain (section Lausanne Stroke Registry, in which the topographically 4.2.3). Although the original definition of TACS simply defined large MCA territory infarcts would be broadly used the word ‘hemiparesis’, in fact the vast majority of equivalent to TACS, 41% of patients had occlusion of the patients in the Oxfordshire Community Stroke Project ipsilateral ICA and 33% had a major source of cardiac who were classified as having TACS were either hemiplegic embolism. 48 or had a severe hemiparesis that would certainly have been incompatible with walking. 184 Therefore, it is worth 4.3.5 Partial anterior circulation syndromes bearing in mind the aphorism ‘beware the walking TACS – the patient may have a posterior circulation syn- The clinical syndrome drome’. The volume of infarction in patients with TACS, as judged by CT, is, not surprisingly, significantly greater The final group of syndromes have less extensive deficits than in patients with lesser deficits 152,178 (section 4.3.7). than a total anterior circulation syndrome and yet do not fulfil the specific criteria for a lacunar syndrome, Occasionally, a total anterior circulation syndrome either because of the presence of higher cortical deficits results from occlusion of the posterior cerebral artery. or because the motor/sensory deficit is too restricted in In such cases, there is often a relatively mild anatomical terms. These would be broadly similar to a hemiparesis but marked aphasia and visual field loss – combination of the superficial middle cerebral artery ‘beware the walking TACS’. and anterior cerebral artery syndromes in other classi- fications. 125 The clinical features of partial anterior circulation syndromes (PACS) are set out in Table 4.10. The vascular lesion From the early pathological studies, the TACS pattern of The brain lesion deficit was linked with occlusion of the proximal main- stem of the middle cerebral artery (MCA) and infarction In community-based studies between 6% and 13% of in both the deep and superficial territories. 68 It was also patients presenting with a partial anterior circulation recognized that, on occasion, the extent of infarction in syndrome had an intracerebral haemorrhage. 177–179 The the superficial territory was not as extensive, and this correlation between the clinical syndrome and brain .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 167 4.3 Clinical subclassification of stroke 167 Table 4.10 Partial anterior circulation syndromes. PACS (isolated anterior cerebral artery infarcts being relatively uncommon), 28% of patients had greater than At time of maximum deficit, any of: 50% stenosis of the ipsilateral ICA, and 33% had a major Motor/sensory deficit + hemianopia 48 source of cardiac embolism. Motor/sensory deficit + new higher cerebral dysfunction New higher cerebral dysfunction + hemianopia Pure motor/sensory deficit less extensive than for lacunar 4.3.6 Syndromes of uncertain origin syndromes (e.g. monoparesis) For a variety of reasons, the physician will occasionally New higher cerebral dysfunction alone (e.g. aphasia) have difficulty allocating cases with confidence on When more than one type of deficit is present, they must all clinical grounds to one of the four stroke syndromes. For reflect damage in the same cerebral hemisphere. example, the patient may have had a previous stroke, be demented, or have had a limb amputated for peripheral imaging in patients with ischaemic stroke is shown in vascular disease. In such cases, it may be unclear what Table 4.11. Most of the patients with ‘inappropriate’ new neurological deficits have arisen from the current infarcts had either multiple small, deep infarcts, which stroke. There are also patients, who are often very elderly, may or may not have been relevant to the clinical syn- in whom it can be difficult to decide whether they drome, or what appeared to be isolated posterior cerebral should be classified as having a partial anterior circula- artery (PCA) territory infarction. Although PCA territory tion syndrome (PACS) or a total anterior circulation syn- infarction is usually considered to be due to embolism drome (TACS), usually because of uncertainty about the from the vertebrobasilar arteries, there will be up to 15% presence of new higher cerebral dysfunction or a visual of patients whose PCAs are supplied by the carotid sys- field deficit. If one is not certain about a deficit, it is usu- tem, because of developmental variation in the circle of ally best to consider it absent, and therefore the majority Willis (section 4.2.2). should be considered as having a PACS. The exception is if the patient is drowsy, which – if due to the cerebral lesion rather than any metabolic disturbance – would be The vascular lesion indicative of an extensive supratentorial lesion with the In an angiographic study of 25 patients with medium patient being classified as having a TACS, or of a major (1.5–3.0 cm) areas of infarction on CT, 14 were found to brainstem stroke with the patient being classified as a have middle cerebral artery (MCA) occlusion, 6 had posterior circulation syndrome. At the other end of the internal carotid artery (ICA) occlusion, and 5 had no spectrum, one should be quite rigid about applying the significant angiographic lesion 46 (section 6.7.2). Later rules describing the extent of a motor or sensory deficit studies of patients with non-haemorrhagic partial anter- which ought to be present before diagnosing LACS ior circulation syndromes (PACS) who had an early (i.e. only when there is involvement of the face, arm and carotid duplex examination reported that about a quar- leg; or the whole of the face and arm; or the whole of the ter had either occlusion or high-grade stenosis of the ICA arm and leg). At the end of the day, however, there is ipsilateral to the cerebral lesion, and up to half the other some evidence that making a ‘best guess’ on the basis of patients had a major cardiac source of embolism. 160,164 the evidence available to you is probably a reasonably In the Lausanne Stroke Registry, in which the topo- accurate strategy. 185 graphically defined limited superficial MCA territory The results of any brain imaging may well assist the infarcts would be broadly equivalent to the majority of primary classification, i.e. point towards the most likely Table 4.11 Clinicoradiological Study Number Appropriate No lesion Inappropriate correlations of partial anterior circulation infarct infarct syndromes. Bamford 177 * 106 47 (44%) 56 (53%) 3 (3%) Lindgren et al. 178 * 61 21 (34%) 24 (39%) 16 (26%) Anderson et al. 179 * 75 25 (33%) 31 (41%) 19 (25%) Wardlaw et al. 183 † 43 29 (67%) 7 (16%) 7 (16%) Al-Buhairi et al. 227 † 121 78 (64%) 39 (32%) 4 (3%) Mead et al. 228 † 441 213 (48%) 143 (32%) 85 (19%) *Community-based study, first-ever strokes. †Hospital-based study, first-ever and recurrent strokes. .. ..