Handbook of Practical Medicine Stroke

9781405127660_4_003.qxd 10/13/07 11:11 AM Page 115 3.7 Is it a subarachnoid haemorrhage? 115 headache, meningism, photophobia and fever. How- Intraventricular haemorrhage ever, it can be difficult to distinguish from SAH if the patient is found confused or comatose, with marked neck Intraventricular haemorrhage, which may arise within stiffness and no available history. Clues to the diagnosis the ventricles or from immediately beneath the ependy- of meningitis include a high fever, tachycardia and a mal lining, or by extension from an intracerebral haem- purpuric skin rash (meningococcal meningitis). If the orrhage (i.e. from a caudate haemorrhage or ruptured patient is fully conscious and has no focal neurological subependymal vascular malformation into the intra- signs and if meningitis is suspected, a lumbar puncture ventricular system), may mimic SAH (section 9.1.5). should be done immediately. But if the patient is very ill, Also, intraventricular haemorrhage may occur together antibiotics and steroids should be given at once, i.e. after with SAH, usually from a ruptured aneurysm, most fre- venepuncture for blood cultures but before proceeding quently at the anterior communicating artery complex. to brain CT and then, if no blood or intracranial mass Patients present with sudden severe headache, confu- is seen, a cerebrospinal fluid examination (section 3.7.3). sion, vomiting or collapse with loss of consciousness. 225 Again, brain CT or MR scan is required for diagnosis during life. Cerebellar stroke Cerebellar stroke often gives rise to sudden severe Carotid or vertebral artery dissection headache, particularly if it is haemorrhagic, and also to nausea and vomiting, but is usually accompanied Dissection of the wall of the internal carotid artery may by neurological symptoms and signs, such as vertigo, cause a fairly distinctive headache syndrome, which is dysarthria and unsteadiness, which help distinguish ipsilateral, involving the forehead, periorbital region, it from SAH. However, if the lesion is large, the patient face, teeth or neck, and has a burning or throbbing may present in coma due to direct brainstem compres- quality (section 7.2.1.). The headache may be associated sion or obstruction of cerebrospinal fluid flow from with an ipsilateral Horner’s syndrome or monocular the fourth ventricle, causing hydrocephalus and raised blindness, and with contralateral focal neurological intracranial pressure, or there may be meningism symptoms or signs. Dissection of the wall of the vertebral without signs of definite brainstem dysfunction. In artery generally causes pain in the upper posterior neck a consecutive series of 100 patients with an initial and occiput, usually on one side, and may be asso- diagnosis of subarachnoid haemorrhage, eight had a ciated with symptoms and signs of posterior circulation cerebellar haematoma (and another seven had sup- ischaemia, such as the lateral medullary syndrome. ratentorial intracerebral haemorrhage). 223 Urgent brain Transmural dissection of an intracranial artery can cause CT is required to confirm the diagnosis of cerebellar SAH (section 9.1.3). haematoma, and lumbar puncture should certainly not be done; indeed, lumbar puncture should almost Acute obstructive hydrocephalus always be preceded by brain CT in unconscious patients, even if there are no focal signs of a mass lesion and no Any acute obstruction of the flow of cerebrospinal fluid clinical evidence of raised intracranial pressure (such as causes headache through a rapid increase in intracranial papilloedema). pressure. The headache is commonly bilateral and exacerbated by coughing, sneezing, straining or head movement. Intermittent obstructive hydrocephalus may Intracerebral haemorrhage therefore cause severe paroxysmal headaches. A colloid More than 50% of patients with spontaneous intracere- cyst of the third ventricle is the classical cause of this bral haemorrhage have headache at onset, particularly syndrome; sometimes more than one family member those with superficial lobar haemorrhages, but the is affected. 226 A decreased level of consciousness may headache is generally not as strikingly sudden in onset follow the headache. 227 The outcome can be lethal if a as SAH. 89 Furthermore, focal neurological deficits are diagnosis is not made. 228 Brain CT or MRI usually iden- almost always present, but they can also occur in about tifies the offending lesion (Fig. 3.48). 20–30% of aneurysmal SAHs where there is intraparen- chymal extension of the haemorrhage. 224 Conversely, Migraine some intracerebral haemorrhages, particularly those which are deep, have less prominent focal neurological Migraine headache can sometimes arise suddenly (‘crash’ signs and can easily be mistaken for SAH. CT brain migraine), be severe and prostrating, unilateral or gen- scanning is always required. eralized, and associated with photophobia, irritability, .. ..

9781405127660_4_003.qxd 10/13/07 11:11 AM Page 116 116 Chapter 3 Is it a vascular event and where is the lesion? ‘Exploding head’ syndrome Clusters of attacks characterized by a sensation of sudden noise in the head and terror, rather than pain, can strike individuals over the age of 50 years, particularly during the twilight of sleep. 232,233 The cause is uncertain. Cough headache Idiopathic cough headache is defined as head pain brought on by coughing or other Valsalva manoeuvres, but not by prolonged physical exercise, in the absence of any intracranial disorder. 234,235 It is probably caused by distension of venous structures in the brain. It is a sudden-onset headache and lasts from 1 s to 30 min, tends to be bilateral and posterior, does not begin earlier than the fifth decade of life, is more frequent in men, is not accompanied by other neurological mani- festations and often responds to indomethacin. These clinical characteristics allow its differential diagnosis from posterior fossa lesions, especially herniation of the cerebellar tonsils (Chiari-I malformation), even though a craniocervical magnetic resonance imaging study is useful to rule this out. Fig. 3.48 CT brain scan showing a tumour in the third Hypnic headache ventricle (arrow) at the foramen of Monro, causing obstructive hydrocephalus. This type of headache has only been recognized recently. 236,237 It wakes patients up in the middle of the night, 2–6 h after sleep onset; it is usually diffuse mild confusion, anorexia, mild fever, extraocular muscle and bilateral, or in the neck. It occurs almost exclusively palsy (ophthalmoplegic migraine) or symptoms of brain- in middle age, twice as often in women as in men. stem disturbance (basilar migraine) and thus be mis- Patients usually get out of bed and walk around until the taken for SAH. However, migraineurs generally have a pain subsides, within 10 min to 3 h. Typically the attacks past or, less diagnostically helpful, a family history of are recurrent, from once a week to 6 times per night. migraine and the headache is commonly unilateral and There are no known precipitating factors, there is no throbbing, not so rapid in onset and of shorter duration photophobia, phonophobia or nausea and there are than the headache of SAH. 86 Vomiting tends to start well no concomitant autonomic features, such as in cluster into the migraine attack, in contrast to SAH, in which it headache or chronic paroxysmal hemicrania. commonly occurs at or soon after onset of the headache. Post-traumatic headache Idiopathic stabbing headache Immediately after a head injury there is often headache; Three specific varieties of sudden sharp stabbing head- this may be pulsating and made worse by head move- ache have been described: ice-pick-like pains, ‘jabs and ment, jolting, coughing, sneezing and straining. 229 jolts syndrome’ and ophthalmodynia. 229,230 The pains Normally the headache gradually disappears as the soft are mostly at the temples or orbits but on occasion are and any bony tissue damage resolves. In a series of 200 elsewhere in the head. 231 Migraineurs are particularly patients admitted to hospital with head injury only susceptible. 231 Precipitants – which are seldom present 83 still had a headache by a day or so afterwards; only 22 – may be postural change, physical exercise, or head of those 83 (11% of all patients) complained spon- motion. As these pains are transient and lancinating, taneously, and only three required an analgesic. 238 they are unlikely to be confused with the headache of The diagnosis of post-traumatic headache should not SAH. The mechanism is unknown. be confused with SAH if there is a history of head injury, .. ..

9781405127660_4_003.qxd 10/13/07 11:11 AM Page 117 3.7 Is it a subarachnoid haemorrhage? 117 but the patient may be amnesic and there may be no Phaeochromocytoma witness, in which case acute head injury with secondary bleeding into the subarachnoid space can be confused Patients with a phaeochromocytoma experience acute with spontaneous SAH. pressor reactions; in about 80% of attacks they complain of headache 241,242 often in combination with palpita- If the circumstances of a traumatic head injury are tions or sweating. 243 The headache is usually of sudden unclear, and there is a reasonable chance that onset, bilateral, severe and throbbing. It appears to be spontaneous intracranial haemorrhage was the cause related to a rapid increase in blood pressure and lasts less of the accident and so the head injury, then brain CT than an hour in about 75% of patients, but it may last should be done as soon as the patient’s condition from a few minutes to a few hours. Some patients may allows, regardless of the severity of the head injury. collapse with loss of consciousness or develop focal neurological signs during the episode, as a result of cere- bral oedema or sometimes haemorrhage. Attacks may be Benign orgasmic cephalalgia and benign exertional provoked by exertion, straining, emotional upset, worry headache 242 or excitement. Acute, severe, explosive occipital or generalized head- The diagnosis depends on clinical suspicion being ache, usually occurring at the moment of sexual orgasm aroused when the history is first taken (which can be or during strenuous exercise (benign orgasmic cephalal- difficult because the condition is so rare) and is con- gia and benign exertional headache, respectively) may firmed by finding increased excretion of catecholamines mimic SAH. 196,239,240 The history of onset during sexual (metanephrine and vanillylmandelic acid) in three 24-h intercourse (or masturbation) may not be forthcoming specimens of urine, or raised plasma free metanephrine without specific and sensitive enquiry. Points in favour or normetanephrine levels during the attack. 244 The of the diagnosis are a history of similar previous sexual blood sugar is usually raised at the time of the attack, a or exertional headaches, no alteration in consciousness, useful distinction from hypoglycaemic attacks, which short duration of the headache (minutes to hours) and may simulate phaeochromocytoma because of second- no signs of meningeal irritation such as neck stiffness, or ary release of adrenaline in response to low blood sugar. low back pain, and nor sciatica in the ambulant patient. The tumour may arise at any point along the line of These headaches can occur at any time in life and do not development of the sympathetic chain from the neck to necessarily occur every time the patient experiences the pelvis and scrotum. orgasm, or exercises strenuously. If patients present soon Headache may also reflect idiopathic surges of hyper- after their first-ever sudden orgasmic headache, it is not tension, not associated with phaechromocytoma or any possible to exclude SAH without brain CT and lumbar other identifiable condition. 245 puncture. If a patient presents after recurrent attacks, and the history is characteristic, investigation is seldom Occipital neuralgia necessary. Occipital neuralgia is characterized by an aching or paroxysmal jabbing pain in the posterior neck and Reaction to monoamine oxidase inhibitor drugs occipital region in the distribution of the greater or lesser People taking classic monoamine oxidase inhibitors occipital nerves (Fig. 3.49). It may rarely present quite (MAOIs), of which phenelzine and tranylcypromine dramatically, like SAH, 246 but there is usually diminished are the most commonly used, may experience sudden sensation or dysaesthesiae of the affected area (C2 dis- severe headache after ingesting sympathomimetic tribution), focal tenderness over the point where the agents, red wine or foods with a high tyramine content, greater occipital nerve trunk crosses the superior nuchal such as mature cheese, pickled herrings, game and yeast line, and a therapeutic response to infiltration of local extract. This is because MAOIs irreversibly block the anaesthetic near the tender area on the nerve trunk. ability of both MAO isoforms (A and B) to metabolize dietary tyramine in the liver (A) and gut wall (B). The Benign ‘thunderclap headache’ combination of a classic MAOI and oral tyramine can provoke dangerous hypertension. The headache tends ‘Thunderclap headache’ is not a true disease entity, but a to be over the occipital region of the head and is asso- convenient term to describe unclassifiable varieties of ciated with a rapid rise in blood pressure. It can be sudden-onset, severe, generalized pain in the head, some- relieved by the alpha noradrenergic blocking agent, times with vomiting. 247 It may last up to a day or so. phentolamine. Clinically, the syndrome cannot be reliably distinguished .. ..

9781405127660_4_003.qxd 10/13/07 11:11 AM Page 118 118 Chapter 3 Is it a vascular event and where is the lesion? Greater occipital nerve Lesser occipital nerve Fig. 3.49 Diagram showing the anatomical distribution of the sensory innervation of the greater and lesser occipital nerves. from SAH, but the chances of aneurysmal SAH are • the site of any SAH or intracerebral or intraventricular increased in the presence of female gender, epileptic haemorrhage and therefore the likely cause (section seizures, loss of consciousness at onset, focal neuro- 9.4.1 and Fig. 3.50); logical symptoms (e.g. diplopia), vomiting or exertion • the presence of any complications, such as preceding the onset of headache. 194 The diagnosis is hydrocephalus; therefore made by exclusion, mainly of SAH. About 50% • any contraindications to lumbar puncture such as of these patients have a history of typical migraine or cerebral oedema or haematoma with brain shift, or a tension-type headache (with gradual onset). large cerebellar infarct, when there is no blood evident The prognosis is benign; a 3-year follow-up of 71 on CT; patients seen in hospital found identical recurrences in • and whether there is any other intracranial ab- 12, again without evidence of SAH, whereas nearly 50% normality that may account for the symptoms and developed episodes of more obvious migraine or tension signs. headache. 248 Of 93 such patients identified in general The sensitivity of CT in SAH depends on the amount practice and followed up for a median of 5 years, again of subarachnoid blood, the resolution of the scanner, the none suffered SAH; recurrent attacks of ‘thunderclap skills of the radiologist and the timing of the CT after headache’ occurred in eight patients, and 13 developed symptom onset. The sensitivity is greatest in the first few new tension headache or migraine. 249 days and falls thereafter, as blood in the subarachnoid space is resorbed (Fig. 9.19). In fact, the term ‘resorp- Headache is common in clinical practice, but tion’ may not always be appropriate to describe this ‘thunderclap’ headache is not. No physical sign can process, diffusion and sedimentation being other expla- definitely exclude subarachnoid haemorrhage if a nations. CT evidence of subarachnoid blood can dis- sudden onset headache persists for a few hours. appear very rapidly. If brain CT is done within 1–2 days after SAH onset, extravasated blood will be demon- strated in more than 95% of patients. 202 But the chance 3.7.3 Investigations to confirm the diagnosis of of finding subarachnoid blood on brain CT then subarachnoid haemorrhage decreases sharply, to 50% on day 7, 20% on day 9, and Investigations are essential in making the diagnosis of almost nil after 10 days. 251,252 subarachnoid haemorrhage (SAH), given the clinical features are relatively non-specific. 250 If brain CT is done within 1–2 days after subarachnoid haemorrhage onset, extravasated blood will be demonstrated in more than 95% of patients. Brain CT scan All patients presenting with a suspected recent SAH (i.e. Of course, minute amounts of subarachnoid blood within the last few days) should initially have an urgent may be overlooked by the uninitiated (Fig. 3.51). Depend- brain CT to determine: ing on the amount of blood in the cisterns and the • whether there is blood in the subarachnoid space; delay before scanning, an ‘absent’ or ‘missing’ (isodense) .. ..

9781405127660_4_003.qxd 10/13/07 11:12 AM Page 119 3.7 Is it a subarachnoid haemorrhage? 119 Fig. 3.50 Brain CT scan (a) showing a 2- or 3-week-old catheter angiography (b) revealed an anterior communicating intracerebral haemorrhage in the frontal lobes (arrow) of a artery aneurysm (arrow) which had ruptured and bled into the patient who presented with an acute behavioural disorder and frontal lobes. was misdiagnosed as being a hysterical alcoholic. Subsequent cistern, or absent cortical sulci, may be the only clue to the presence of subarachnoid blood (Fig. 3.52). If subarachnoid haemorrhage is suspected and yet the brain CT scan appears normal, look carefully at the interpeduncular cistern, ambient cisterns, quadrigeminal cistern, the region of the anterior communicating artery and posterior inferior cerebellar artery, the posterior horns of the lateral ventricles and the cortical sulci. If blood is present in these sites, it may be isodense or slightly hyperdense, and hence the normally hypodense cisterns and sulci may be difficult to see and seem ‘absent’. Haemorrhage from an intracranial aneurysm can result not only in SAH but also in an intracerebral hae- morrhage, which is easily seen on plain CT and generally persists for longer than subarachnoid blood, because the resorption of intraparenchymal blood, as seen on CT, occurs over several days to weeks rather than a few days. 251 However, small intracerebral haemorrhages can also resolve very quickly, within days (section 5.4.1). Fig. 3.51 CT brain scan showing a subtle amount of subarachnoid blood in the anterior part of the About one-quarter of unselected patients who reach interhemispheric fissure (arrow), from a ruptured aneurysm hospital alive after aneurysmal haemorrhage have an of the anterior communicating artery. intracerebral haemorrhage on CT. 224,251 .. ..

9781405127660_4_003.qxd 10/13/07 11:12 AM Page 120 120 Chapter 3 Is it a vascular event and where is the lesion? Fig. 3.52 Brain CT scan of a patient with subarachnoid haemorrhage showing isodense blood in the cortical sulci giving the appearance of ‘absent’ sulci. In particular, the sylvian fissures are not seen because they are filled with just enough blood to raise the density of the cerebrospinal fluid to that of brain parenchyma. False positive evidence of SAH on CT scans Fig. 3.53 Brain CT scan of a patient who is brain dead from A false positive diagnosis of SAH may be made on the CT general hypoxia. There is generalized oedema, with effacement brain scan, for example in patients who are comatose of the cisternal cerebrospinal fluid spaces. These spaces appear and brain dead (i.e. have no cerebral blood flow at the hyperdense, through venous stasis, which may falsely suggest time of the scan). The CT scan not only shows cerebral subarachnoid haemorrhage. oedema, but hyperdense material in the subarachnoid space which represents blood in congested subarachnoid blood vessels 253–255 (Fig. 3.53). Increased density of the Always do a lumbar puncture if the history is tentorium and basal cisterns as a false positive sign of suggestive of subarachnoid haemorrhage and the CT SAH on an unenhanced CT scan has also been described scan (performed early, within a few days) is normal. in polycythaemia, 256 purulent meningitis, 257 subdural Frequently, the cerebrospinal fluid will be normal haematoma, 258,259 gliomatosis cerebri 260 and spontane- too, but occasionally in this setting an abnormal ous intracranial hypotension. 261 cerebrospinal fluid will provide the only evidence of subarachnoid haemorrhage. Lumbar puncture Lumbar puncture without prior brain CT is potentially According to a consecutive series from the Netherlands, dangerous in patients with an intracerebral haemor- the negative predictive value of CT scanning performed rhage. 262 Brain herniation may occur even in patients within 12 h of onset of sudden headache is 97%. 202 without focal signs or a decreased level of consciousness. 263 In other words, there is an important small minority Once the decision has been taken to do a lumbar punc- (of about 3%) with sudden headache and normal CT ture, the next requirement is to do it well. This is more within 12 h who do have xanthochromia in the cere- difficult than it seems. Before drawing cerebrospinal brospinal fluid, and in whom angiography subsequently fluid, the first rule is to wait until at least 6 and preferably confirms a ruptured aneurysm. Therefore a lumbar punc- 12 h have elapsed after the headache onset. This delay ture is necessary in any patient with sudden headache is absolutely essential because if cerebrospinal fluid and a normal CT scan, even though the results will be obtained earlier turns out to be blood-stained, it is abso- normal in most patients. lutely and irrevocably impossible to distinguish between .. ..

9781405127660_4_003.qxd 10/13/07 11:12 AM Page 121 3.7 Is it a subarachnoid haemorrhage? 121 blood that was there before (genuine SAH) and blood to measure the cerebrospinal fluid pressure, because that was introduced by the needle (a bloody tap). With sudden headache may be a first manifestation of intra- pre-existing blood in the cerebrospinal fluid, bilirubin cranial venous thrombosis. After you have withdrawn will have been formed in the interval from SAH onset, the needle, had it properly disposed of and made sure from the breakdown of erythrocytes in the cerebrospinal your patient is comfortable, take a good look at the cere- fluid (see below), but of course not with a traumatic tap. brospinal fluid. There are roughly four possibilities: A false positive diagnosis of SAH can be almost as damag- • the cerebrospinal fluid is blood-stained; ing as a missed one, because insurance companies are • it is colourless but not clear; bound to remain wary, despite negative investigations • it is clear but there is some colour (mostly yellowish or for an aneurysm. Never believe a colleague, however pink); senior, who tells you that ‘the tap went so smoothly, it is • or it is crystal-clear. impossible that the blood was traumatic’. Even the So there are essentially two qualities to the fluid: smoothest puncture can hit a vein. Also the ‘three-tube colour and clarity. Clarity refers only to whether one can test’ (a decrease in red blood cells in consecutive tubes) is see through the tube, irrespective of the colour (a good notoriously unreliable. 264 Immediately proceeding with glass of Bourgogne rouge is red but clear). CT or MR angiography in all patients with bloodstained Each cerebrospinal fluid specimen should be sent to cerebrospinal fluid is not a good idea either, despite the clinical chemistry laboratory. If it is colourless, the some people advocating this way of circumventing cells should be counted. If there are no or only a few the ‘bloody tap’ problem: a small (<5 mm) unruptured (<100) red cells, a recent SAH has been ruled out. And if aneurysm can be expected in every 50th adult and there are no white cells and the pressure is normal, the should in most cases be left untreated. patient can be sent home. If the cerebrospinal fluid is blood-stained, ask the laboratory to spin it down imme- It is a widely held myth that the distinction diately at appropriate speed and to call you when they between subarachnoid haemorrhage and a traumatic have done so. It is perhaps unconventional but abso- ‘bloody’ tap can be made reliably by collecting the lutely essential that you go to the laboratory yourself to cerebrospinal fluid in three consecutive test tubes have a look at the supernatant after centrifugation and and counting the number of red cells in each tube. to compare it in bright light with water in a similar test tube, against a white background. If the supernatant is Keeping patients in the emergency department or yellow, the diagnosis of subarachnoid haemorrhage is admitting them to hospital until 6–12 h after sym- certain – though the cause of course still needs to be ptom onset may be a practical problem. However, there determined. is no other option. If red cells have entered the cere- brospinal fluid during the headache episode, sufficient Blood-stained cerebrospinal fluid should be lysis will take place during that time for bilirubin and immediately centrifuged; if the supernatant is yellow oxyhaemoglobin to be formed. 205 These pigments give this proves haemorrhage. Xanthochromia is almost the cerebrospinal fluid a yellow tinge after centrifugation invariably found between 12 h and 2 weeks after (xanthochromia), a critical feature in the distinction subarachnoid haemorrhage. from a traumatic tap; these pigments are almost invari- ably detectable until at least 2 weeks later. 265 Bilirubin is Of course the presence of bilirubin can be confirmed the most important pigment of the two, since it can be by spectrophotometry the next day. This test should cer- formed only in vivo, whereas haemoglobin can be broken tainly be performed if one is in any doubt and perhaps down to oxyhaemoglobin in a test tube that has been left even if the supernatant seems crystal-clear, although unattended for too long. many neurologists can confidently exclude xantho- chromia by visual inspection alone. 266 The specimen Lumbar puncture should be done after a negative CT should be stored in darkness, preferably wrapped in scan, but not until at least 6–12 h have elapsed since tinfoil because the ultraviolet components of daylight the onset of headache. can break down bilirubin – not only in icteric newborns but also in test tubes. At least two test tubes should be filled with cere- Spectrophotometry can confirm the presence of brospinal fluid, with an extra tube for the microbiology bilirubin. 267 In most cases this is accompanied by laboratory if the fluid is not blood-stained but somewhat oxyhaemoglobin, but the presence of oxyhaemoglobin opaque (meningitis, after all?) while the tube is filling alone is irrelevant to the diagnosis of SAH. Although up. If the cerebrospinal fluid seems clear do not forget the sensitivity and specificity of spectrophotometry have .. ..

9781405127660_4_003.qxd 10/13/07 11:12 AM Page 122 122 Chapter 3 Is it a vascular event and where is the lesion? not yet been confirmed in a series of patients with case reports cited above, migraine might explain both suspected SAH and a negative CT scan, 268 it is the best the headache and the arterial narrowing (‘vasospasm’). technique currently available. Segmental and fully reversible vasospasm has been demonstrated in patients with severe headache but with- out an aneurysm, 273 and even in a patient with benign Late presentation with a history of sudden headache 274 exertional headache. ‘Thunderclap headache’ does It is not uncommon in clinical practice to encounter not warrant the potentially dangerous procedure of patients who describe having had a severe headache of catheter angiography if both the CT scan and the cere- sudden onset 3 weeks (or more) ago, sounding very brospinal fluid are normal within 1 week of the event; much like an SAH, which resolved after a few hours or CT angiography or MR angiography in ‘late patients’ days. If patients present 2 weeks or more after an episode should be reserved for those with a convincing history, of sudden headache, the diagnostic value of a normal e.g. having spent a few days in bed because of the CT scan is very limited. A lumbar puncture showing headache. crystal-clear cerebrospinal fluid with no bilirubin on spectrophotometry will generally suffice to exclude SAH, If a patient presents with a sudden severe headache provided the interval is not more than 1 week. With and the CT scan and lumbar puncture are carried out an initially positive CT scan, the cerebrospinal fluid is in less than 1 week and are completely normal, with invariably xanthochromic for 2 weeks, 265 but the point no evidence of intracranial haemorrhage, then has been made that xanthochromia may not last as cerebral catheter angiography is not indicated; CT long in the 5% of patients with SAH in whom early CT or MR angiography should not be performed scanning is negative. 268 Indeed there is a report of a indiscriminately. patient with aneurysmal rupture in whom not only CT scanning was normal on day 7, but also the cerebro- spinal fluid, on the next day. 269 In a patient presenting late, if there has been asso- ciated loss of consciousness, or if the patient has been References severely ill for several days, the probability of a ruptured aneurysm is considerable, and there is a good case for 1 Hankey GJ, Slattery JM, Warlow CP. The prognosis of angiography, at least CT angiography (section 9.4.4). The hospital-referred transient ischaemic attacks. J Neurol issue of distinguishing patients with non-haemorrhagic Neurosurg Psychiatry 1991; 54(9):793–802. ‘thunderclap headache’ from those with ruptured 2 Hankey GJ, Warlow CP. Transient Ischaemic Attacks. aneurysms has been unnecessarily complicated by a few London: W.B. Saunders Company Ltd, 1994. case reports of impressive but rare events. There is one 3 Ferro JM, Canhao P, Bousser MG, Stam J, report of fatal aneurysmal rupture in which the presence Barinagarrementeria F. Cerebral vein and dural sinus of iron-containing macrophages was interpreted as evid- thrombosis in elderly patients. Stroke 2005; 36(9):1927–32. 4 van Gijn J. Cerebral venous thrombosis: pathogenesis, ence of an earlier haemorrhage, in a patient with a pre- presentation and prognosis. J R Soc Med 2000; 93(5):230–3. ceding episode of headache. 270 This interpretation is 5 Dennis MS, Bamford JM, Sandercock PA, Warlow CP. A questionable, as the patient survived the second episode comparison of risk factors and prognosis for transient for a few days. A second type of case report, exemplified ischemic attacks and minor ischemic strokes. The by two patients from different sources, relates that an Oxfordshire Community Stroke Project. Stroke 1989; aneurysm can be found on cerebral angiography in 20(11):1494–9. patients with sudden headache and negative findings 6 Dennis MS, Bamford JM, Sandercock PA, Warlow CP. on CT as well as on lumbar puncture, accompanied Incidence of transient ischemic attacks in Oxfordshire, by arterial narrowing. 271,272 At operation no evidence of England. Stroke 1989; 20(3):333–9. haemorrhage around the aneurysm was found in 7 Koudstaal PJ, van Gijn J, Frenken CW, Hijdra A, Lodder J, either case, but it was claimed that the aneurysm Vermeulen M et al. TIA, RIND, minor stroke: a continuum, or different subgroups? Dutch TIA Study Group. J Neurol had suddenly enlarged, without rupturing. Although a Neurosurg Psychiatry 1992; 55(2):95–7. growing aneurysm may occasionally cause headache, a 8 Johnston SC, Sidney S, Bernstein AL, Gress DR. A much more probable explanation is that in the course of comparison of risk factors for recurrent TIA and stroke in life a few per cent of all adults develop asymptomatic patients diagnosed with TIA. Neurology 2003; 60(2):280–5. aneurysms and that indiscriminate use of angiography 9 Rothwell PM, Buchan A, Johnston SC. Recent advances in is bound to reveal some of them (section 15.2.1). If it is management of transient ischaemic attacks and minor assumed that the aneurysm was incidental in the two ischaemic strokes. Lancet Neurol 2006; 5(4):323–31. .. ..

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Pseudosubarachnoid haemorrhage in subdural 242 Lance JW, Hinterberger H. Symptoms of haematoma. J Neurol Neurosurg Psychiatry 2003; pheochromocytoma, with particular reference to 74(8):1131–2. headache, correlated with catecholamine production. 260 Belsare G, Lee AG, Maley J, Kirby P, St Louis EK, Follett K. Arch Neurol 1976; 33(4):281–8. Pseudo-subarachnoid hemorrhage and cortical visual 243 Baguet JP, Hammer L, Mazzuco TL, Chabre O, Mallion JM, impairment as the presenting sign of gliomatosis cerebri. Sturm N et al. Circumstances of discovery of Semin Ophthalmol 2004; 19(3–4):78–80. phaeochromocytoma: a retrospective study of 41 261 Schievink WI, Maya MM, Tourje J, Moser FG. Pseudo- consecutive patients. Eur J Endocrinol 2004; 150(5):681–6. subarachnoid hemorrhage: a CT-finding in spontaneous 244 Lenders JW, Keiser HR, Goldstein DS, Willemsen JJ, intracranial hypotension. Neurology 2005; 65(1):135–7. Friberg P, Jacobs MC et al. Plasma metanephrines in the 262 Duffy GP. 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9781405127660_4_004.qxd 10/13/07 11:09 AM Page 131 4 Which arterial territory is involved? Using arterial and brain anatomy to develop a clinically based method of subclassification 4.1 Introduction 131 4.2 Cerebral arterial supply 133 4.3 Clinical subclassification of stroke 158 4.4 Subclassification based on aetiology 171 Much of the recent focus in the medical literature has 4.1 Introduction been on classifications which depend on knowing the underlying cause of the stroke. While it is clearly logical to try to establish the cause of every individual stroke, Once the diagnosis of a cerebrovascular (vs non-vascular) since it is with this knowledge that rational treatments event has been made in someone presenting with an for limiting the acute damage and secondary prevention acute stroke syndrome (Chapter 3), the clinician then will be developed, tested and deployed, as will be seen, needs a framework on which to base the further sub- this is not always possible to achieve in a timely manner classification of that event. Although in the past, time- even in well-financed healthcare systems. based schemes of subclassification were promoted, we The subclassification of stroke has the potential to have seen already that the distinction between stroke refine the practice of various different healthcare profes- and transient ischaemic attack (TIA) is arbitrary, does sionals, many of whom are more interested in the clin- not have any rational pathophysiological basis (sec- ical deficits and functional consequences resulting from tion 3.2), and is of little value to the physician seeing a the brain lesion (e.g. nursing and rehabilitation) rather patient with persisting symptoms within minutes or than the underlying cause. There are also many other hours after onset. Similarly, there is no evidence to sug- reasons for subclassifying patients with strokes and TIAs gest that a distinction between ‘major stroke’ and ‘minor which, while not all of immediate value to the individual stroke’ (defined as symptoms lasting more or less than patient or their relatives, may be helpful when consider- 1 week respectively) or with reversible ischaemic neuro- ing the general management of cerebrovascular disease logical deficit (RIND) – variously defined as cases in and the overall burden to the community (Table 4.1). which symptoms resolve in less than 1 week or 3 weeks – This diversity of need perhaps explains why there is still conveys any useful aetiological information. Indeed, the no universal method of subclassification used equally by tendency for some physicians to use the terms ‘minor’ stroke physicians, therapists, health service managers and ‘major’ as a type of shorthand to describe the level of and others. residual disability simply leads to confusion. If a method of subclassification is going to be applic- able to all patients during life, irrespective of age, dis- ability and geographical location, clinical data must be used as the core component because they are available to Stroke: practical management, 3rd edition. C. Warlow, J. van Gijn, every clinician; subsequently obtained investigative data M. Dennis, J. Wardlaw, J. Bamford, G. Hankey, P. Sandercock, G. Rinkel, P. Langhorne, C. Sudlow and P. Rothwell. Published appropriate to the individual situation can then be used 2008 Blackwell Publishing. ISBN 978-1-4051-2766-0. to refine that clinical subclassification. After the clinical 131 ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 132 132 Chapter 4 Which arterial territory is involved? Table 4.1 Potential benefits of subclassifying patients with 100% sensitive and specific, although there is a tendency strokes and transient ischaemic attacks. for the results of investigations to be perceived, almost automatically, as the ‘gold standard’. This fact may par- Aid cost-effective and timely search for the cause of the tially explain the trend for the literature to overemph- stroke or transient ischaemic attack asize the exceptions to general clinical rules, although Aid planning of immediate supportive care and even the most sophisticated images have to be inter- rehabilitation programme preted (just like symptoms and signs) with the potential Improve prognostication for survival, functional outcome, for both inter-observer and intra-observer variability and and recurrence Stratify entry to clinical trials to reduce heterogeneity and significant numbers of false positives and false negat- therefore have the best chance of demonstrating ives. There are always going to be exceptions to the rules, treatment benefit in a subgroup if such a benefit is present and one definition of clinical acumen is the ability to Help put the results of clinical trials into the context of an sense when such exceptions are likely. Thus, anyone individual physician’s own practice using any system of classification must be blessed with a Provide more sensitive assessment of case mix in individual healthy dose of realism. units, for comparative audit and contracting purposes Aid audit of management One should not presume that the results of investigations will necessarily be any more sensitive history and examination, the clinician will have some or specific than the clinical findings. Investigations information about the site of the brain lesion, the vascu- contribute most to the diagnostic process when set lar territory affected and possibly some clues as to the in a proper clinical context and when they take the potential aetiology (e.g. the presence of atrial fibrillation). pre-test probability of the disorder to be diagnosed This information needs to be organized in a manner that into account. facilitates a modular and hierarchical approach to sub- classification – i.e. additional but complementary levels Many clinicians had anticipated that the advances of subclassification can be used in any particular situation in neuroimaging would have made any clinically based to suit individual requirements and facilities. Thus, the classification redundant long ago. Superficially, a method basic scheme needs to provide a skeleton on which these of subclassification based on the imaged site of brain fragments of information about an individual patient damage (i.e. a topographical classification) and then can be hung in an orderly manner so as to orientate fur- describing this in terms of the likely vascular territory ther management. Ideally, such a ‘core’ clinical skeleton, involved is attractive. Developments such as diffusion- usable in everyday practice, could be built on by both weighted MR imaging (section 5.5.2) have certainly clinicians and researchers according to their access to, aided the identification of brain lesions; however, not all and the applicability of, various investigations. Used in infarcts are visible even on DWI and the nature of the this way, a system of classification should also facilitate DWI ‘lesion’ does not appear to give additional prognostic the integration and application of research findings from information to clinical data. 1,2 There remains, therefore, the university centres into everyday practice. an illogicality of basing a system on imaging ‘holes in Traditional neurological teaching has always focused the brain’, when the current thrust of acute treatments on first determining the site of the lesion within the ner- is to prevent such holes appearing by very early thera- vous system, since this nearly always narrows the range peutic intervention. So, although imaging has certainly of possible underlying causes. It would seem logical, been useful in the subclassification of intracerebral therefore, to attempt to identify groups of stroke patients haemorrhage and subarachnoid haemorrhage (Chap- with broadly similar brain and arterial lesions, since ters 5, 8 and 9), it has so far failed on its own to provide a these are likely to be caused by broadly similar types of useful framework for classification of ischaemic stroke vascular disease. Following on from this, such groups and TIA, let alone the entity of ‘brain attack’. The reasons might be expected to have certain nursing and rehabilita- for this include the following: tion needs, and also a distinctive prognosis. As will be • the surprising inter-individual and intra-individual seen, such an approach to subclassification, based initi- variability of the pattern of the vascular supply to the ally on an analysis of the brain damage, is in fact entirely brain (section 4.2); complementary to the aetiological classifications which • the current limitations of even the most sophisticated usually have both clinical syndromes and the results of imaging technology to produce reliable results in all cross-sectional imaging as core components. patients with stroke – particularly within hours of At the outset it is very important to recognize the onset (section 5.5); limitations of both the clinical findings and the invest- • the variations in technology between centres and over igations that are used to subclassify patients; none will be time – even different researchers have different machines; .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 133 4.2 Cerebral arterial supply 133 • the problems with generalizability of such a system, with the localization of the arterial lesion have begun to even if appropriate images were available (as they may take this variability into account. 7,8 But even then, there well be in the future), given current problems with the has to be a lesion on the scan to localize – this is some- funding of healthcare worldwide; thing that is actually becoming less frequent with very • the current lack of data correlating cross-sectional early scanning, unless the latest MR techniques are used imaging with outcome. although these are not infallible; and even when lesions 9 In section 4.2, we will review the relevant vascular are visible, their size may change with time (Fig. 4.1). anatomy, and then in section 4.3 describe a system Not surprisingly, this all means that attributing an infarct linking this with the features of the clinical examination to a particular underlying pathogenesis on the basis of its of patients with ‘brain attack’ or stroke that assist lesion site and size is often incorrect. 10–12 One important conse- localization, as discussed in Chapter 3. Finally, in section quence of the above is that at the level of the individual 4.4 we will see how this provides a basis for a commonly patient, the occlusion of a specific artery may present used aetiological classification. clinically in different ways. Nevertheless, in this chapter, we have attempted to relate each part of the vascular anatomy to the symptoms and signs commonly, but not always, encountered in clinical practice. 4.2 Cerebral arterial supply The pathogenesis of a cerebral infarct cannot be determined purely on the basis of its site and size. The cerebral vascular anatomy can be described in two 4.2.1 Introduction main parts: the anterior (carotid) and posterior (vertebro- For the information from the clinical history and exam- basilar, VB) systems. With the exception of the basilar, ination to be formulated in a manner that will have as anterior communicating and innominate arteries, the much relevance as possible to the underlying vascular precerebral and intracerebral arteries are paired although lesion, the clinician needs to have a working knowledge only one artery will be described in each section unless of the cerebral blood supply. This will also be required for there is significant side-to-side variation. planning and interpreting the results of investigations, For each system, there are three components: the extra- and assessing the relevance of possible treatments. How- cranial arteries, the major intracranial arteries and the ever, the general assumption that the vascular supply small (in terms of diameter) superficial and deep perforat- of the brain follows an entirely predictable pattern (as ing arteries. These component arteries have different struc- depicted in many textbooks) and that there are patterns tural and functional characteristics, which means that of infarction which are ‘typical’ of a particular patho- infarction within their territory of distribution is likely genesis (e.g. embolism from the heart) should certainly to be caused predominantly by different causes (Table 4.2): not be accepted without closer scrutiny. Many classifications refer to ‘standard’ maps of the Table 4.2 Functional characteristics of the intracranial arteries. areas of distribution of individual arteries, especially those that have been produced as cross-sectional tem- Main parent arteries (e.g. middle cerebral artery) 3 plates to correspond with CT/MR sections (e.g. Damasio ). Anastomotic potential via circle of Willis, extracranial The theory goes that if one plots the site and size of the connections and pial collaterals lesion on the scan onto these maps, then the occluded Thus, marked variability in the area of ischaemia as a result artery can be identified. Additionally, certain sites are of occlusion identified as arterial boundary zones between the areas Embolism or in situ thrombosis is the most likely cause of of supply of individual arteries, and further assumptions occlusion are then often made about the underlying pathophysio- Cortical branch arteries logical process – e.g. low-flow haemodynamic ischaemic Anastomotic potential via pial collaterals stroke rather than thromboembolism (sections 4.2.4 and Thus, moderate variability in the area of ischaemia as a 6.7.5). However, it is clear that the cerebral circulation is result of occlusion a dynamic system with large inter-individual and intra- Embolism is the most likely cause of occlusion individual variability (i.e. between hemispheres and Deep perforating arteries even varying with time) and that atheroma or other Limited anastomotic potential arterial disease in one part of the system may have com- Thus, very restricted areas of ischaemia as a result of occlusion Intrinsic small vessel disease is the most likely cause of plex and relatively unpredictable effects on the patterns occlusion of vascular supply. 4–6 More recent publications dealing .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 134 134 Chapter 4 Which arterial territory is involved? (a) (b) (c) Fig. 4.1 Sequential T2-weighted MR brain scans of a patient There is slight compression of the adjacent left lateral ventricle with a pure motor stroke affecting the right arm and leg, showing (black arrow) and of the sylvian fissure (thick white arrow), which the decreasing size of the small, left deep infarct over time (thin decreases with time, so that at 19 months, there is an ex-vacuo white arrows): (a) day 1, (b) 2 months, (c) 19 months post-stroke. effect – the left lateral ventricle is now larger (black arrow) and Note that there is some swelling of the lesion in the acute phase. the sylvian fissure more visible (thick white arrow). (a) (b) (c) Fig. 4.2 (a) Internal carotid artery just above the common of comparable size. The media is virtually devoid of elastic · · carotid bifurcation (elastic van Gieson (EVG) × 120). The intima tissue. There is no definite external elastic lamina. (c) A pair of · · at the top of the photograph is barely visible, lying inside an basal ganglionic perforating vessels (EVG × 250). Each of these ill-defined internal elastic lamina. The relatively thick media is vessels has an indistinct internal elastic lamina, and a media rich in elastic tissue. The adventitia is thin and poorly defined. composed of two to three layers of smooth muscle cells; · · (b) Cross-section of the middle cerebral artery (EVG × 50). The arterioles are devoid of an internal elastic lamina. intima is barely visible, and lies internal to the folded internal (Photographs courtesy of Dr Alistair Lammie, Department elastic lamina, which shows mild focal reduplication. Both of Neuropathology, University of Wales College of media and adventitia are thinner than in extracranial arteries Medicine.) .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 135 4.2 Cerebral arterial supply 135 • The extracranial vessels (e.g. the common carotid artery) have a trilaminar structure (intima, media and adventitia) and act as capacitance vessels (Fig. 4.2a). There are a limited number of anastomotic channels between these arteries. • The larger intracranial arteries (e.g. the middle cerebral artery) have potentially important anastomotic con- nections over the pial surface of the brain and at the skull base via the circle of Willis and choroidal circula- tion (see below). 13 The adventitia of these large intracranial arteries is thinner than that of the extracranial vessels, with little elastic tissue (Fig. 4.2b). The media is also thinner, although the internal elastic lamina is thicker (such changes occurring gradually as the arterial diameter decreases). Thus, these vessels are more rigid than extracranial vessels of similar size. • The small, deep perforating (e.g. the lenticulostriate arteries) and superficial perforating arteries from the pial surface are predominantly end-arteries, with very limited anastomotic potential, and are primarily resis- tance vessels (Fig. 4.2c). The overall resistance in any part of the arterial tree is inversely proportional to the vascular density, which, on average, is approximately four times greater in grey matter (cortical and subcortical) than in white matter. 6 4.2.2 Anterior (carotid) system Common carotid artery The left common carotid artery (CCA) usually arises directly from the left side of the aortic arch, whereas the right CCA arises from the innominate (brachiocephalic) Fig. 4.3 (a) An anteroposterior projection of a contrast- artery (Figs 4.3 and 6.2). The CCA ascends through enhanced MR angiogram, showing the origins of the major the anterior triangle of the neck, and at the level of the vessels from the aorta, the cervical course of the carotid and thyroid cartilage divides into the internal carotid artery vertebral arteries, and the intracranial connections of anterior (ICA) and the external carotid artery (ECA). Throughout, and posterior arterial systems. R right; L left; 1 aortic arch; 2 innominate artery; 3 right common carotid artery; 4 right the CCA is intimately associated with the ascending subclavian artery; 5 left common carotid artery; 6 left sympathetic nerve fibres. Thus, lesions of the CCA subclavian artery; 7 right vertebral artery; 8 left vertebral artery; (trauma, dissection or sometimes thrombotic occlusion) 9 right internal carotid artery; 10 left internal carotid artery; may cause an ipsilateral oculosympathetic palsy (Horner’s 11 basilar artery; 12 right external carotid artery; 13 left syndrome) with involvement of sudomotor fibres to the external carotid artery. (See also Fig. 6.2.) face. Damage to the CCA, or thrombus within it, may also result in carotidynia, a syndrome characterized by Carotid bifurcation tenderness over the artery and pain referred to the ipsilateral frontotemporal region. It may also be the site The carotid bifurcation is usually at the level of the of radiotherapy-induced damage (section 7.12). thyroid cartilage, but the exact site may vary by several centimetres (Fig. 4.4). It contains the carotid body (see Lesions of the common carotid artery (trauma, below). The ICA is usually posterior to the ECA. The dissection or sometimes thrombotic occlusion) may carotid body and carotid sinus nerve receive their blood cause an ipsilateral oculosympathetic palsy (Horner’s supply from the ECA. The bifurcation is one of the most syndrome) with involvement of sudomotor fibres to common sites for atheroma to develop in whites, and it the face because they are intimately associated with is over this area that bruits can be heard (section 6.7.7). the ascending sympathetic nerve fibres. However, there is no way of telling on auscultation .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 136 136 Chapter 4 Which arterial territory is involved? intracranial circulation by ECA–ICA collaterals (see below). It has been suggested that transient monocular blindness can occur due to intermittent failure of per- fusion through ECA–ICA collaterals because of stenosis of the ECA origin, particularly when there is ipsilateral ICA occlusion or severe stenosis. Palpable pulsation of the superficial temporal artery may be reduced or absent with ipsilateral CCA or ECA occlusion and, con- versely, may be increased when there is ipsilateral ICA occlusion. Extracranial internal carotid artery The extracranial internal carotid artery (ICA) arises from the carotid bifurcation, ascends through the neck to the carotid canal of the petrous temporal bone, before passing through the foramen lacerum in the skull base. Along the petrosal section, it gives off small branches to the tympanic cavity and the artery of the pterygoid Fig. 4.4 Lateral view of catheter carotid angiogram. ECA external canal, which may anastomose with the internal max- carotid artery and its branches (curved arrows); ICA internal illary artery, a branch of the ECA. When neurological carotid artery (straight arrows); CCA common carotid artery symptoms occur from disease of the ICA, they may be (arrow with tail). due to artery-to-artery embolism, low distal flow, or whether a bruit arises from the ICA, ECA or both. One occlusion due to local arterial thrombosis. The clinical practical point relates to carotid duplex scanning; in picture may range from a transient disturbance of ipsi- most people this images the bifurcation and ICA/ECA lateral cortical or ocular function to the ‘full house’ for a few centimetres distal, so in patients with a high of hemiplegia, hemianaesthesia, hemianopia and pro- bifurcation only the CCA may be imaged. found disturbance of higher cortical function. The vari- The carotid body responds to increases in the arterial ability in clinical presentation does not seem to depend partial pressure of oxygen (PaO ), blood flow and arterial on the presence of collateral flow, but the risk of stroke 2 pH, and to decreases in PaCO and blood temperature. and TIA is increased when there is severely impaired 2 It has a modulatory role on pulse rate, blood pressure cerebrovascular reactivity. 16,17 It is possible that the dis- and hypoxic ventilatory drive. 14 Increased discharges in tal extent of any ICA thrombosis may be limited where the carotid sinus nerve can be caused by stretching of its there is retrograde filling of the ophthalmic artery. 18 wall, and will increase the depth and rate of respiration Occlusion of the ICA is not always symptomatic; in a and increase peripheral vascular resistance. Carotid sinus series of 994 consecutive autopsies, only 42 of 54 (78%) hypersensitivity is probably an under-recognized cause cases with an ICA occlusion had evidence of ipsilateral of collapse in the elderly, but is not necessarily associated infarction, and in about 20% the occlusion had not with structural disease of the bifurcation. 15 caused any symptoms, at least as far as could be estab- lished from retrospective case note review. 19,20 The proximal extracranial ICA just beyond the bifurca- External carotid artery tion is commonly affected by atheroma and when The branches of the external carotid artery (ECA) symptoms occur they are most often due to instability (ascending pharyngeal, superior thyroid, lingual, occipi- and rupture of an atherosclerotic plaque causing artery- tal, facial, posterior auricular, internal maxillary and to-artery embolism, or much less often low flow distal to superficial temporal) are mainly of interest because of an occlusion 21 (section 6.3.2). Other conditions involv- their potential for anastomoses with branches of the ing the extracranial ICA include arterial dissection (tradi- intracranial ICA (either spontaneously or by surgery) and tionally associated with trauma but also recognized as their involvement in giant-cell arteritis (section 7.3.1). occurring spontaneously, section 7.2.1) pseudo-aneurysms The presence of extracranial branches distinguishes the (caused by dissection) which may be a source of emboli ECA from the ICA on arterial studies (Fig. 4.4). In the (section 7.1.1); fibromuscular dysplasia (section 7.4.1) and presence of an extracranial ICA occlusion or severe a local arteritis secondary to paratonsillar infections stenosis, blood flow may be maintained to the ipsilateral (section 7.11). .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 137 4.2 Cerebral arterial supply 137 The sympathetic nerve fibres lie on the surface of the ICA and can be affected by any of the above processes. The resulting oculosympathetic palsy should spare the sudomotor (sweating) fibres to the face because they are associated with the branches of the ECA. Around the origin of the ICA are the superior laryngeal and hypoglossal nerves, which may be affected by operative procedures and cause hoarseness and tongue weakness respectively (section 16.11.4 and Fig. 16.36). Carotid siphon and cavernous sinus After passing through the skull base, the next part of the ICA is the S-shaped carotid siphon which lies within the venous plexus of the cavernous sinus adjacent to cranial nerves III, IV, V , V and VI, which run in the lateral wall 1 2 of the sinus. There are several small branches (the most important of which is the meningo-hypophyseal trunk), which may anastomose with branches of the ECA. One congenital variant worth noting is the persistence of the trigeminal artery, which may arise from the ICA as it enters the cavernous sinus and links with the basilar artery, usually between the superior cerebellar artery and the anterior inferior cerebellar artery. Fig. 4.5 A T1-weighted, gadolinium-enhanced, coronal MR Atheroma may affect the ICA in the siphon but scan, showing thrombosis within the left cavernous sinus. The although this may be a source of embolism, flow restric- thrombus (long arrow) is seen separate from the flow void in the tion and, in a few cases, complete occlusion, the result- left internal carotid artery (short arrow). Enhancement is seen in ing symptoms are similar to those originating from the sphenoid sinus (broad arrow), which is due to infection. The more proximal ICA disease. The degree of atheroma is patient had a fever, chemosis and a partial third nerve palsy. not necessarily related to that at the carotid bifurcation and when occlusion occurs in the siphon it is more likely (lacrimal, supraorbital, ethmoidal, palpebral), the to be due to impaction of an embolus from a proximal ophthalmic artery is probably the most important ana- site than in situ thrombosis. 21 stomotic link with the ECA (Fig. 4.6). Cavernous sinus thrombosis classically presents with Transient monocular blindness (amaurosis fugax) may varying degrees of ophthalmoplegia, eye swelling be due to emboli passing from the ICA to the ophthalmic (chemosis) and proptosis (sometimes bilateral, because artery 23 (section 3.3.6). However, a large proportion of the venous plexus communicates across the midline) such patients have no evidence of ICA disease, nor for in a patient with facial or sinus infection (Fig. 4.5). 22 that matter cardiac or aortic sources of embolism, and Aneurysms of the ICA at the level of the cavernous sinus therefore local atheroma within the ophthalmic artery is are relatively common and may present with oculomo- presumed to be the cause in many cases. Fixed deficits tor nerve dysfunction. If there is rupture of the artery come from retinal artery occlusion (usually considered that is confined by the sinus, then a caroticocavernous to be embolic) and ischaemic optic neuropathy (sec- fistula may develop. The typical picture is of pulsatile tion 3.5.2), although the latter is surprisingly infrequent proptosis, with ophthalmoplegia and reduced visual with ICA occlusion, presumably because of adequate acuity (section 8.2.14). collateral flow. The combination of ocular and cerebral hemisphere ischaemic attacks on the same side is a strong pointer Supraclinoid internal carotid artery towards severe ICA stenosis or occlusion, although the The short supraclinoid part of the ICA lies in the sub- symptoms rarely occur simultaneously. When ICA arachnoid space close to the oculomotor (III) cranial occlusion occurs, the distal extent of the thrombus usu- nerve. The most important branch from this part of the ally ends at the level of the ophthalmic artery. 18 The ICA is the ophthalmic artery, which enters the orbit supraclinoid ICA may also be involved by inflammat- through the optic foramen. Along with its branches ory/infective processes, such as tuberculous meningitis, .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 138 138 Chapter 4 Which arterial territory is involved? in the basal subarachnoid space. Severe stenosis or occlu- sion of the distal supraclinoid ICA is always present in the moyamoya syndrome (section 7.5). The combination of ocular and cerebral hemisphere ischaemic attacks on the same side is a strong pointer towards severe internal carotid artery stenosis or occlusion. There are also a number of small perforating branches that supply the pituitary gland, hypothalamus and optic chiasm. Other branches may pass through the anterior perforated substance to supply the genu and part of the posterior limb of the internal capsule, and the globus pallidus. Posterior communicating artery (a) The next branch of the ICA is usually the posterior com- municating artery (PCoA). Arising from the dorsal aspect of the ICA, it runs back above the oculomotor (III) nerve to join the posterior cerebral artery (PCA) (Fig. 4.7). The PCoA may give off small branches which contribute to the blood supply of the basal ganglia. Aneurysms at the origin of the PCoA may present with a painful oculomotor (III) nerve palsy usually but not always with a fixed, dilated pupil, or with subarachnoid haemorrhage (section 9.3.6). In a few patients, both PCoAs are absent which may result in much more (b) Fig. 4.6 (a) A selective intra-arterial catheter angiogram, lateral view, showing occlusion of the left internal carotid artery (ICA, short arrow) and filling of the external carotid artery (ECA, long Fig. 4.7 Demonstration of the components of the circle of arrow). (b) Intracranial views (lateral projection), showing Willis by intra-arterial catheter angiography (anteroposterior retrograde filling of the ophthalmic artery (long arrow) from projection). The whole of the circle is filled from a selective left the ECA, which provides a collateral supply to the distal ICA vertebral artery injection in a patient who had bilateral internal (short arrow, showing the carotid siphon). carotid artery occlusions. The components are: 1 anterior communicating artery; 2 anterior cerebral artery; 3 middle cerebral artery; 4 posterior communicating artery; 5 posterior cerebral artery. .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 139 4.2 Cerebral arterial supply 139 marked neurological deficits from lesions of the post- optic tract and sends branches to the lateral geniculate erior circulation than in patients with a functionally nucleus (LGN) and the anterior part of the optic radia- intact circle of Willis (see below). tion. It may anastomose with the posterior choroidal artery (a branch of the posterior cerebral artery). The cause of occlusion of the AChA is very variable Anterior choroidal artery although when infarction is restricted to the internal Just before its terminal bifurcation into the anterior capsule it is probably more often due to intrinsic disease cerebral artery and middle cerebral artery (MCA), the of the artery complicated by in situ thrombosis than 25 ICA usually gives rise to the anterior choroidal artery embolism from more proximal sources . Also, the AChA (AChA) (Fig. 4.8), although occasionally the AChA arises may be particularly susceptible to the effects of intrac- from either the proximal stem of the MCA or the post- arotid chemotherapy. 26 AChA territory infarcts typically erior communicating artery. It is a relatively small artery produce a contralateral hemiparesis and hemisensory which gains its name because it supplies the choroid deficit, the latter often sparing proprioception. Langu- plexus. It may also supply the globus pallidus, anterior age and visuospatial function may be affected, and are hippocampus, uncus, lower part of the posterior limb of attributed to extension of the ischaemia to the lateral the internal capsule and anterior part of the midbrain, thalamus. Large AChA territory infarcts have an addi- including the cerebral peduncle. 24 It accompanies the tional visual field defect. This can be a homonym- ous hemianopia (due to ischaemia of the optic tract) but the pathognomonic pattern is considered to be a homonymous horizontal sectoranopia due to involve- ment of the LGN. 27 Distal internal carotid artery At the bifurcation of the ICA, the main continuing branch is usually the middle cerebral artery, while the smaller anterior cerebral artery and the posterior commun- icating artery form the anterior portion of the circle of (a) Willis (Fig. 4.7). This is not a common site for atheroma, but can be the superior extent of a carotid dissection (section 7.2.1). It is also a site of aneurysm formation (section 9.1.1). Circle of Willis In the embryo, a large branch from the ICA provides most of the blood supply to the occipital lobes. From this branch, the future posterior communicating artery (PCoA) and post-communicating (P2) segment of the posterior cerebral artery (PCA) will develop and these usually will link with the pre-communicating (P1) seg- ment of the PCA, which develops from the basilar artery. The arterial components of the circle of Willis and the origins of its branches (i.e. the anterior cerebral arteries (ACAs), the PCAs, the anterior communicating artery (ACoA) and the PCoAs) are formed by 6–7 weeks of gesta- tion. 28 At this stage, the PCoA and the P1 segment of the PCA are usually of approximately similar diameter and contribute equally to the supply of the P2 segment of the PCA. This ‘transitional’ configuration is present in nearly (b) 80% of fetuses under 20 weeks gestation, but over the Fig. 4.8 Carotid catheter angiograms, showing the anterior next 20 weeks (and particularly between the 21st and choroidal artery (arrows): (a) lateral view, (b) anteroposterior view. 29th weeks of gestation, which coincides with the period .. ..

9781405127660_4_004.qxd 10/13/07 11:09 AM Page 140 140 Chapter 4 Which arterial territory is involved? of most rapid growth of the occipital lobes) there is a the pre-communicating (A1) segment of the ACA, there change. 29 In the majority, the P1 segment of the PCA was usually an ectopic origin of the distal branches. becomes larger than the PCoA, resulting in the ‘adult’ Taken alongside the haemodynamic consequences of configuration, where the occipital lobes are supplied the hypoplastic segments of the circle of Willis, these primarily by the posterior circulation. However, in a anatomical factors result in considerable variation in the minority, the PCoA becomes larger and the occipital area of supply of the major intracerebral arteries and lobes then obtain most of their blood supply from the the ability of the cerebral circulation to respond to carotid circulation, a situation which is referred to as changes in perfusion pressure when more proximal a ‘fetal’ configuration. The ‘transitional configuration’ arteries are diseased. 6,32 Not surprisingly, one cannot persists in less than 10% of adults although the exact identify any particular clinical syndrome related to any proportions of the different configurations are difficult specific anomalies of the circle of Willis. to estimate from the literature, because of the very variable selection criteria that have been used. 29,30 Anterior cerebral artery Anomalies of the circle of Willis are reported in between half and four-fifths of normal individuals, depending on The anterior cerebral artery (ACA) arises as the medial selection criteria; for example, anomalies certainly seem branch of the bifurcation of the ICA, at the level of to be more prevalent in patients with cerebrovascular the anterior clinoid process and is traditionally divided disease. 30,31 The distribution of the abnormalities found into sections. The proximal (A1) sections of the ACAs in a study of 994 autopsies is shown in Fig. 4.9. 30 In this pass medially and forward over the optic nerve or chiasm study, hypoplasia of part of the anterior part of the and corpus callosum to enter the inter-hemispheric circle of Willis was found in 13%, of the posterior part fissure, where they are linked by the anterior com- in 32%, and of both parts in 36%. When there was municating artery (ACoA) (Fig. 4.10). After the AChA maldevelopment of either the P1 segment of the PCA or the distal (A2) sections of the ACAs run together in the 3 4 ACoA 2 ACA 5 MCA ICA PCoA PCA 1 BA 6 10 7 9 8 (b) (a) Fig. 4.9 Anomalies of the circle of Willis. (a) In the centre is and no collateral supply in 7%. The most common anomaly of a complete circle of Willis (1). There are 21 possible variants. the PCoA is direct origin from the internal carotid artery (ICA) Those involving the anterior cerebral arteries (ACA) and (6 and 9), which occurs in 30% of people (BA basilar artery; anterior communicating artery (ACoA) are shown at the PCA posterior cerebral artery; MCA middle cerebral artery). top (2–5) and some of those involving the posterior (b) An MR angiogram of the circle of Willis demonstrating communicating arteries (PCoA) below (6–10). The anterior part absence of both posterior communicating arteries (1) and of the circle provides poor collateral supply in 24% of people hypoplasia of the left ACA (2). .. ..