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Home Explore Handbook of Practical Medicine Stroke

Handbook of Practical Medicine Stroke

Published by andiny.clock, 2014-07-25 10:34:00

Description: We don’t care much for abbreviations. They are not literate (Oliver Twist was not abbreviated to OT each time
Dickens mentioned his name!), they don’t look good on
the printed page, and they make things more difficult to
read and understand, particularly for non-experts. But
they do save space and so we have to use them a bit.
However, we will avoid them as far as we can in tables,
figures and the practice points. We will try to define any
abbreviations the first time they are used in each chapter, or even in each section if they are not very familiar.
But, if we fail to be comprehensible, then here is a rather
long list to refer to.


Read the Text Version

9781405127660_4_008.qxd 10/13/07 11:01 AM Page 443 8.10 Subdural haematoma 443 not in patients with ischaemic cerebrovascular disease Table 8.5 Causes of spontaneous subdural haematomas (section 6.8.5). 382,383 Arterial dissection and contrast without associated intracerebral or subarachnoid haemorrhage. hypersensitivity are among the greatest dangers. Nonetheless, in patients with ICH, catheter angiography Acute, of arterial origin • Rupture of a small pial artery, spontaneous, 395,397 or in is still often indicated to detect underlying vascular association with cocaine (section 8.5.4) 401 lesions that are amenable to specific treatment, par- • Saccular aneurysm of major intracerebral artery (section ticularly arteriovenous malformations and saccular 402,403 9.1.1) aneurysms. This applies essentially to all patients under • Arteriovenous malformation (section 8.2.4) 404 50 years of age with ICH, provided they are fit for opera- • Intracavernous aneurysm of the carotid artery 405 tion or neuroradiological intervention (the probability • Aneurysm of middle meningeal artery 406 of finding a treatable lesion is in the order of 50–80% in • Moyamoya syndrome (sections 8.2.12 and 7.5) 407 normotensive patients under 45 with lobar haemor- Chronic, by rupture of a (bridging) vein rhage. 384,385 Angiography may be especially indicated if • Anticoagulant treatment (section 8.4.1) 394 the pattern of haemorrhage is compatible with a saccular • Thrombolytic treatment (section 8.4.3) 408 aneurysm but it should preferably be preceded by CT • Coagulation defects, genetically determined or acquired (section 8.4.4) 409 angiography, which may avoid the need for a catheter • Low cerebrospinal fluid pressure, secondary to angiogram (section 9.4.4). 386 Catheter angiography is spontaneous leak from a spinal root sleeve, 410 lumbar definitely indicated if MR scanning shows ‘flow voids’ 411 392,412 puncture, or with unknown cause consistent with an arteriovenous malformation. • Tension pneumocephalus 413 Unless an aneurysm is anticipated with its high early • Rupture of an arachnoid cyst 414 risk of rebleeding, it is wise to defer angiography until • Dural arteriovenous fistula (section 8.2.8) 415 the space-occupying effect of the haematoma has • Dural metastasis 416 resolved, because in the acute stage the vascular lesion • Autosomal dominant polycystic kidney disease 417,418 may be too compressed to be seen. 387,388 In any patient with intracerebral haemorrhage who is haemorrhage (Table 8.5). Subdural haematomas without fit for surgery, one should at least consider catheter attendant haemorrhage in the subarachnoid space or in angiography, with a view to detecting surgically or the brain parenchyma mostly arise from rupture of a radiologically treatable lesions, particularly saccular bridging vein and are traditionally associated with head aneurysms and arteriovenous malformations. The trauma in the elderly, but they can also occur ‘spont- indication is strongest if the patient is under the age of aneously’ (or, one might speculate, after trauma that about 50 years, if the haemorrhage is lobar rather than was too trivial to be remembered). Anticoagulants are in the deep regions of the brain, and if the patient is the most common precipitant (Fig. 8.34) in urbanized not hypertensive. areas of Western Europe, accounting for approximately 20% of all chronic forms of subdural haematomas. 389 Given the increasing sensitivity of CT and MR angio- In young patients, other coagulation disorders may pre- graphy, catheter angiography is rarely indicated in cipitate bleeding in the subdural space. 390 In such cases patients over 65 years old, and in hypertensive patients rapid correction of the coagulation status is mandatory with haemorrhage in the basal ganglia or the posterior (section 12.4.7), often followed by craniotomy. With fossa. How often this invasive procedure provides extra most subdural haematomas of venous origin the evolu- information that influences management to the benefit tion of symptoms is gradual and by the time they present of patients in this age group is not precisely known, but they may have evolved into fluid collections that appear probably any such gains are offset by the risks. hypodense on CT scans (‘hygromas’). Low cerebrospinal fluid pressure is increasingly recog- nized as a cause of chronic subdural haematomas, thanks to the characteristic appearances on MRI scanning: dif- fuse enhancement of the dura and sometimes descent of 8.10 Subdural haematoma the brain mimicking a Chiari malformation. 391,392 The leak may be iatrogenic (by lumbar puncture or opera- tion) but also spontaneous, most often from a dural root Although subdural haematomas are outside the brain, they sleeve. 393 are still included in this chapter because most of their Arterial sources of bleeding are less common causes many possible causes overlap with those of intracerebral of spontaneous bleeding in the subdural space than .. ..

9781405127660_4_008.qxd 10/13/07 11:01 AM Page 444 444 Chapter 8 What caused this intracerebral haemorrhage? 2 Hart RG, Boop BS, Anderson DC. Oral anticoagulants and intracranial hemorrhage: Facts and hypotheses. Stroke 1995; 26:1471–7. 3 Labovitz DL, Halim A, Boden-Albala B, Hauser WA, Sacco RL. The incidence of deep and lobar intracerebral hemorrhage in whites, blacks, and Hispanics. Neurology 2005; 65:518–22. 4 Jamrozik K, Broadhurst RJ, Anderson CS, Stewart Wynne EG. The role of lifestyle factors in the etiology of stroke. A population-based case-control study in Perth, Western Australia. Stroke 1994; 25:51–9. 5 Rodgers A, MacMahon S, Yee T et al. Blood pressure, cholesterol, and stroke in eastern Asia. Lancet 1998; 352:1801–7. 6 Woo D, Sauerbeck LR, Kissela BM et al. Genetic and environmental risk factors for intracerebral hemorrhage: preliminary results of a population-based study. Stroke 2002; 33:1190–5. 7 Zhang XF, Attia J, D’Este C, Yu XH. Prevalence and magnitude of classical risk factors for stroke in a cohort of 5092 Chinese steelworkers over 13.5 years of follow-up. Stroke 2004; 35:1052–6. 8 Jackson CA, Sudlow CL. Is hypertension a more frequent risk factor for deep than for lobar supratentorial intracerebral haemorrhage? J Neurol Neurosurg Psychiatry 2006; 77(11):1244–52. 9 Charcot JM, Bouchard C. Nouvelles recherches sur la pathogénie de l’hémorrhagie cérébrale. Arch Physiol norm pathol 1868; 1:110–27, 643–65, 725–34. Fig. 8.34 CT brain scan of an acute subdural haematoma in a 10 Ellis AG. The pathogenesis of spontaneous intracerebral 54-year-old man treated with oral anticoagulants (arrows). hemorrhage. Proc Pathol Soc Philadelphia 1909; 12:197–235. coagulopathies. 394 They include rupture of a small pial 11 Adams RD, vander Eecken HM. Vascular diseases of the artery, 395 most often in the region of the sylvian fissure; 396 brain. Ann Rev Med 1953; 4:213–52. angiography may show a small peripheral aneurysm or 12 Cole FM, Yates PO. Pseudo-aneurysms in relation to massive cerebral haemorrhage. J Neurol Neurosurg Psychiatry extravasation from a small artery at the surface of the 1967; 30:61–6. brain into the subdural space. 397 Subdural haematomas 13 Ross Russell RW. Observations on intracerebral aneurysms. may also be caused by aneurysm rupture; as a rule there Brain 1963; 86:425–42. is a tell-tale extravasation of blood in the subarachnoid 14 Cole FM, Yates PO. The occurrence and significance of space as well but occasionally the subdural haematoma intracerebral micro-aneurysms. J Pathol Bacteriol 1967; is the only manifestation (section 9.4.1). 93:393–411. Most spontaneous subdural haematomas occur over 15 Challa VL, Moody DM, Bell MA. The Charcot-Bouchard the convexity of the cerebral hemisphere, but they may aneurysm controversy: impact of a new histologic also be found in the posterior interhemispheric fissure, technique. J Neuropathol Exp Neurol 1992; 51:264–71. as a rule from a ruptured aneurysm, 398 and in the post- 16 Wakai S, Nagai M. Histological verification of erior fossa. 399 microaneurysms as a cause of cerebral haemorrhage in surgical specimens. J Neurol Neurosurg Psychiatry 1989; 52:595–9. 17 Horn EM, Zabramski JM, Feiz-Erfan I, Lanzino G, McDougall CG. Distal lenticulostriate artery aneurysm rupture presenting as intraparenchymal hemorrhage: References case report. Neurosurgery 2004; 55:E708–E712. 18 Fisher CM. Pathological observations in hypertensive cerebral hemorrhage. J Neuropathol Exp Neurol 1971; 1 Ariesen MJ, Claus SP, Rinkel GJE, Algra A. Risk factors for 30:536–50. intracerebral hemorrhage in the general population: a 19 Ooneda G, Yoshida Y, Suzuki K, Sekiguchi T. systematic review. Stroke 2003; 34:2060–5. Morphogenesis of plasmatic arterionecrosis as the cause .. ..

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9781405127660_4_009.qxd 10/13/07 11:03 AM Page 457 9 What caused this subarachnoid haemorrhage? 9.1 Causes of spontaneous subarachnoid haemorrhage 457 9.2 Clues from the history 471 9.3 Clues from the examination 473 9.4 Investigations 476 clinical spectrum 9.1 Causes of spontaneous subarachnoid sudden coma obvious few only haemorrhage death deficits symptoms headache Spontaneous (i.e. non-traumatic) subarachnoid haemor- subarachnoid haemorrhage in the population rhage (SAH) is a serious disorder that occurs in relatively young patients and has a poor prognosis. If the 15% of A patients who die before reaching hospital are taken into primary care physician % ? account, the case fatality of aneurysmal SAH is around 50%, while another 20% remain dependent in activ- C B 1 ities of daily living. SAH accounts for around 5% of all emergency department 15 % % ? strokes. In most populations the incidence is around 9 per 100 000 per year, but in Finland and Japan the E D 2 incidence is twice as high. The incidence increases with neurovascular intervention centre % ? % ? age, but half the patients are younger than 55 years at the 2 time of the SAH. Because of the young age at which SAH Fig. 9.1 Clinical spectrum of aneurysmal subarachnoid occurs and the poor prognosis, the loss of productive life haemorrhage and reasons for failing to reach a neurovascular years from SAH in the population is as large as that from intervention centre where specialized treatment can be applied. 3 ischaemic stroke. Although advances have been made A: some patients with only headache do not consult their in the treatment of patients with SAH (Chapter 14), the primary care physician. B: in some patients the primary care 1,4 case fatality has only slightly decreased . The main physician does not recognize the cause of the headache or other symptoms. C: 15% of patients die suddenly or before reaching reason for this slow progress is that only a proportion of hospital. D: in some patients the emergency physician does patients reach centres which specialize in treating SAH not recognize the cause of the headache or other symptoms. (Fig. 9.1). E: some patients die before reaching the specialist centre. Rupture of a saccular aneurysm at the base of the brain is not the cause in every patient with an SAH, but it is of even rarer conditions (section 9.1.4). But, whatever in approximately 85%. About 10% of patients have a the cause, in the vast majority of patients there is so-called perimesencephalic haemorrhage, the cause of haemorrhage in the basal cisterns (Fig. 9.2). which is unknown (section 9.1.2). The rest are due to intracranial arterial dissections (section 9.1.3) or a variety Subarachnoid haemorrhage is not synonymous with a ruptured aneurysm. About 85% of all spontaneous subarachnoid haemorrhages are caused by rupture Stroke: practical management, 3rd edition. C. Warlow, J. van Gijn, of an intracranial saccular aneurysm, 10% by non- M. Dennis, J. Wardlaw, J. Bamford, G. Hankey, P. Sandercock, aneurysmal perimesencephalic haemorrhage, and G. Rinkel, P. Langhorne, C. Sudlow and P. Rothwell. Published 5% by rarities. 2008 Blackwell Publishing. ISBN 978-1-4051-2766-0. 457 ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 458 458 Chapter 9 What caused this subarachnoid haemorrhage? ambient Sylvian cistern fissure (lateral part) fourth quadrigeminal ventricle cistern suprasellar third cistern ventricle sylvian frontal horn fissure of lateral (basal part) ventricle anterior interhemispheric Fig. 9.2 CT brain showing the basal fissure cisterns. The presenting features of patients with all these aneurysms in adults to some degree depend on whether different causes are usually indistinguishable: a severe fatal cases of SAH have been included, on the definition headache of sudden onset, a depressed level of con- of the minimal size for a lesion to be called an aneurysm, sciousness, or both; sometimes there are focal deficits and finally on the diligence with which the search for or cranial nerve palsies (section 9.3.6). The exception is unruptured aneurysms has been performed. In our sys- perimesencephalic non-aneurysmal haemorrhage, where tematic review of studies reporting the prevalence of all explosive headache is usually the only symptom at intracranial aneurysms in patients studied for reasons onset. In the following sections on the pathological and other than SAH, the best estimate of the frequency for an pathophysiological background of all these causes, we average adult without specific risk factors was 2.3% (95% will occasionally run ahead of the story by mentioning confidence interval, 1.7–3.1%); this proportion tended the findings on CT scanning, because this technique, as to increase with age. 5 an early adjunct to the history and examination, pro- vides an in vivo picture of the pathology. Intracranial aneurysms are not congenital but generally develop during life. 9.1.1 Intracranial saccular aneurysms Saccular aneurysms arise at sites of arterial branching, Aneurysms of the cerebral vessels are not congenital usually at the base of the brain, either on the circle of but develop during the course of life, usually after the Willis itself or at a nearby branching point (Fig. 9.3). The 5 second decade. In the exceptional case of childhood exact reason why aneurysms develop is unknown. In aneurysms, there is often an underlying cause such the search for answers attention has been paid to (ultra) as trauma, infection or connective tissue disorder structural abnormalities, familial intracranial aneurysms, (Table 9.1). 6–10 The absolute frequencies of intracranial conditions predisposing to intracranial aneurysms such .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 459 9.1 Causes of spontaneous subarachnoid haemorrhage 459 Table 9.1 Hereditary and congenital conditions associated of attributable risk, the modifiable risk factors – alcohol, with saccular aneurysms. smoking and hypertension – account for about half of first SAH episodes, genetic factors for only about one- Disorders of connective tissue tenth. 11 In patients with multiple aneurysms a pre- • Ehlers-Danlos syndrome type IV 30,347 dominance of genetic factors is suggested by the fact that • Autosomal dominant polycystic kidney disease* 5,11,27,28 • (Infantile) fibromuscular dysplasia 348,349 these patients are younger at the time of rupture than patients with SAH and a single aneurysm. 12 Other factors Disorders of angiogenesis • Hereditary haemorrhagic telangiectasia (section 8.2.7) 350 that have been linked with multiple aneurysms are • Progressive hemifacial atrophy (Parry-Romberg female gender, smoking and hypertension. 13–15 syndrome) 351 Associated hypertension • Congenital heart disease 352 Structural abnormalities in the vessel wall • Coarctation of the aorta 353 It is unknown why only some adults develop aneur- • Aortitis syndrome 354 ysms at arterial bifurcations while most do not, except Local haemodynamic stress in specific, mostly genetically determined, conditions • Anomalies of the circle of Willis; 355 these occur more (Table 9.1). The once popular notion of a congenital gap often in women 356 in the muscle layer of the wall (tunica media), through • Arteriovenous malformations (section 9.1.4) • Moyamoya syndrome 357 (section 7.5) which the inner layers of the arterial wall could bulge, has been largely dispelled. Defects in the muscle layer of *In polycystic kidney disease, hypertension may contribute intracranial arteries are equally common in patients with to the formation of intracranial aneurysms, but aneurysms and without aneurysms, and are usually strengthened by do occur in patients who have no hypertension. densely packed collagen fibrils. 16–18 Note: In the following conditions a relationship with Studies at the ultrastructural level have however shown cerebral aneurysms has been assumed in the past but definite abnormalities. 19 The proteins of the extracellu- subsequently questioned: neurofibromatosis type 1, 358 lar matrix that are decreased in the intracranial arterial Marfan’s syndrome, 359,360 and pseudoxanthoma elasticum. 361 wall of many ruptured aneurysms, in skin biopsies, and in intracranial and extracranial arteries of patients with aneurysms are collagen type III, collagen type IV and pericallosal artery elastin fibres. Therefore, because the disruption of the extracellular matrix proteins has been found not only in middle cerebral artery aneurysms but also in skin and unaffected intracranial and extracranial arteries, intracranial aneurysms might anterior not represent a localized disease but rather a more gen- communicating artery eral disorder of the extracellular matrix. This decrease branches of in extracellular matrix proteins might be explained by carotid artery disrupted synthesis. On the other hand, there is con- stant degradation and synthesis of the constituents of top of basilar the extracellular matrix regulated by a range of proteases artery (matrix metalloproteinases, neutrophil or leucocyte branches of elastase) and their inhibitors (tissue inhibitor of matrix vertebral artery metalloproteinases and α1 antitrypsin), growth factors and cytokines. Accelerated protein degradation may, therefore, also be caused by an imbalance between these proteases and protease inhibitors. 19 Fig. 9.3 MR angiogram of the circle of Willis, showing the sites Familial occurrence of aneurysms were aneurysms are usually found. Around 10% of patients with SAH have one or more as autosomal dominant polycystic kidney disease and affected parents, siblings or children, i.e. first-degree Ehlers-Danlos type IV, genetic abnormalities at the relatives. 20,21 In familial SAH, aneurysms are more chromosomal or molecular level, the development of often large and multiple than in patients with sporadic new aneurysms after a first episode of SAH, and finally SAH. 22 But, because familial SAH constitutes only 10% to the important issue of acquired risk factors. In terms of all cases of SAH, in practice more large and multiple .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 460 460 Chapter 9 What caused this subarachnoid haemorrhage? aneurysms are associated with sporadic rather than showed reduced production of collagen type III, and with familial SAH. Patients with familial SAH are in there was no defect in the collagen type III gene. 31 general younger than those with sporadic SAH, and in families with two generations affected the age at onset Genetic studies in the younger generation is earlier than in the older generation. 22,23 candidate genes Some degree of familial clustering also occurs in So far, in intracranial aneurysms, there have only been so-called sporadic SAH. The risk of SAH in first-degree association studies of functional and positional candi- relatives of index patients with SAH is approximately date genes, those involved in maintaining the integrity five times higher than in the general population. 20,24,25 of the extracellular matrix being proposed as the most Undoubtedly this familial clustering can to some extent likely candidates. 32 So far positive associations have been be explained by shared classical (acquired) vascular risk found for the genes of collagen type III-A1 (a single small factors, which are associated with ruptured aneurysms study), collagen type I-A2, α1 antitrypsin and – more (see below). Nevertheless, classical risk factors such recently – for member 3 of clade A of serine proteinase as hypertension explain only part of the familial inhibitors (SERPINA3, known previously as alpha-1- aggregation. 24 antichymotrypsin), 33 whereas results have been negative or conflicting for lysyl oxidase, fibrillin 2, different metalloproteinases, inhibitors of metalloproteinases, Autosomal dominant polycystic kidney disease endoglin, angiotensin converting enzyme, NADPH In patients with autosomal dominant polycystic kidney oxidase, P22PHOX and phospholipase C. disease (ADPKD) intracranial aneurysms are found in approximately 10%. 5 But, although SAH frequently linkage studies occurs in patients with ADPKD, 27 the relative rarity of Linkage studies can establish whether there is co- ADPKD is the reason why the proportion of patients segregation of a disease phenotype with DNA markers with ADPKD in series of patients with SAH is less than of known location, dispersed throughout the genome, 1%. 11,27 Hypertension is not a necessary factor for the in families with the disease. This type of study mainly development of aneurysms in patients with ADPKD. 27 detects genetic factors with large effects. Fine mapping is In 85% of the patients the gene responsible for the dis- not possible and, therefore, the genetic factors must lie ease is on chromosome 16p (PKD1) and in the remaining in large regions of several hundreds of genes. Also, the 15% it is in most cases on chromosome 4q (PKD2). Most mode of inheritance needs to be defined, except with aneurysms are found in PKD1 patients and the position affected sibling-pair analysis, but given the high case of the mutation predicts the development of intracranial fatality in SAH that type of analysis is rarely possible. So aneurysms. 29 far six linkage regions have been identified: 19 7q11 (in more than one study; it includes the candidate gene for collagen type I-A2), 14q22, 19q13.3, 5q22–q31 (which Ehlers-Danlos disease type IV region includes the candidate genes for lysyl oxidase and Ehlers-Danlos disease is frequently mentioned as an fibrillin 2), 2p13 and 1p34.3–p36.13 (possible candidate important association with intracranial aneurysms, but genes in this region include polycystic kidney disease- given its rarity it too is a very infrequent cause of SAH. like 1, fibronectin type III domain-containing gene, and In our own database, which now includes over 2000 collagen type XVI-A2). consecutive patients with SAH, we have only one patient on record who later proved to have Ehlers-Danlos dis- gene expression studies ease. Ehlers-Danlos type IV is especially associated with To date, the expression of a selection of genes has been arterial dissection and aneurysms of large and medium- analysed in samples of 24 ruptured and unruptured sized arteries, including intracranial arteries. Intracranial intracranial aneurysms, superficial temporal arteries of 43 aneurysms can be either saccular or fusiform. In a survey intracranial aneurysm patients, and 19 control patients of 131 patients who had died from Ehlers-Danlos type without intracranial aneurysms. 34 Concentrations of IV, 7% did so from an SAH. 30 Patients with Ehlers-Danlos prostacyclin-stimulating factor and the protein RAI, type IV have a defect in collagen type III. This association both implicated in the process of tissue repair, were between a defect in collagen type III and aneurysms has lower in those with ruptured intracranial aneurysms prompted interest in the association between patients than in superficial temporal arteries of patients with with aneurysms and collagen type III in general; how- intracranial aneurysms. Furthermore, there was a ever, in a consecutive series of patients only a minority decrease of collagen-type-III expression. .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 461 9.1 Causes of spontaneous subarachnoid haemorrhage 461 haemangioblastoma, 42 but in these cases the aneurysm New aneurysms after SAH is seldom in one of the common locations at or near the Because aneurysms develop during life, patients who circle of Willis, but rather on an artery closely related to have survived an SAH and in whom all aneurysms have the AVM or angioma. been treated may still be at risk of developing new Iatrogenic causes include: aneurysms and new episodes of SAH. Indeed, in the first • radiation therapy 43–46 (section 7.12); 10 years after SAH the chance of finding a new aneurysm • acrylate applied externally to an intracranial artery for on screening is 16%. 35 Moreover, in the first 10 years microvascular decompression; 47 after an SAH with successful clipping of the detected • superficial temporal artery–middle cerebral artery aneurysms, the risk of a recurrent SAH is 2–3%, about bypass surgery, with the aneurysm forming at the site 20 times higher than expected in a population of com- of the anastomosis. 48,49 parable age and sex. 36,37 Besides this relatively high risk of recurrent SAH, patients who have survived an SAH may Triggers for aneurysm rupture also be at increased risk of vascular diseases in general. In a Finnish study, those who had made a good recovery SAH from an aneurysm is the end result of the develop- from an SAH had a twofold risk of dying from cere- ment and finally rupture of an aneurysm but little is brovascular or cardiovascular disorders compared with known about what actually precipitates the rupture. A the general population. 37 plausible factor is a sudden increase in arterial pressure. If this does play an important role, factors that increase it may be associated with the onset of SAH. Acquired risk factors A few studies have collected data on the activities A recent systematic review included much new informa- immediately preceding the onset of SAH: tion that has become available over the last few years. 37 • physical exertion preceding the haemorrhage was The analysis included only studies in the English lan- found in 2–20% of patients; 50–52 guage that gave crude data (actual numbers of those • sexual intercourse in 0–11%; 48,50–52 exposed or non-exposed), and studies in which the • activities with a Valsalva manoeuvre in 4–20%; 50,53,54 diagnosis of SAH had been confirmed by CT angio- • stress in 1–2%. 50,53 graphy or postmortem in at least 70% of patients. Given Because none of these studies accounted for the usual these constraints, it contained 14 longitudinal and 23 frequency of these factors in everyday life, it is uncertain case–control studies. Statistically significant risk factors whether they actually increase the risk of aneurysm were: rupture or not. • current smoking (risk ratio [RR] 2.2 [95% CI 1.3– In a case–control study, the risk of SAH was increased 3.6]); by smoking in the 3 h before the onset of SAH with never • hypertension (RR 2.5 [2.0–3.1]); and smokers as the reference group (OR 7.0; 95% CI 3.7–13.1) • excessive alcohol intake (RR 2.1 [1.5–2.8]). and by drinking more than 5 units of alcohol in the Non-white ethnicity was a less robust risk factor (RR 24 h before the onset with teetotallers as reference (OR 1.8 [0.8–4.2]). Oral contraceptives did not definitely 4.3; 95% CI 1.5–12.3). 55 In a study where vigorous act- affect the risk (RR 5.4 [0.7–43.5]). Lower risks were found ivity preceding the SAH occurred in 3% of patients, it for hormone replacement therapy (RR 0.6 [0.2–1.5]), increased the risk of SAH, in comparison with episodes hypercholesterolaemia (RR 0.8 [0.6–1.2]) and – surpris- without vigorous activity in the same patient (RR ingly – diabetes (RR 0.3 [0–2.2]). Data were inconsistent 15.0; 95% CI 4.3–52.2). 51 In another study with a case- for lean body mass index (RR 0.3 [0.2–0.4]) and rigorous crossover design, moderate to extreme exertion in the exercise (RR 0.5 [0.3–1.0]). 2 h before SAH, which occurred in 19% of patients, Seasonal variation in the occurrence of SAH is found in also increased the risk, but to a lesser extent (RR 2.7; 95% some studies but not in most. There is clear variation, CI 1.6–4.6). 52 with lower rates of rupture during the night than during waking hours. 40,41 This variation suggests that activity is 9.1.2 Non-aneurysmal perimesencephalic a risk factor for aneurysmal rupture, but does not prove it haemorrhage because only time of onset was recorded, not the activ- ities preceding onset. In this radiologically distinct and strikingly harmless Some vascular malformations may predispose to variety of SAH, the extravasated blood is confined to the the formation of aneurysms, especially arteriovenous cisterns around the midbrain. 56–58 This disease entity is malformations (AVMs) (section 9.1.4) and cerebellar entirely defined by the characteristic distribution of the .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 462 462 Chapter 9 What caused this subarachnoid haemorrhage? Fig. 9.4 (a) Typical example on CT scan of a perimesencephalic haemorrhage with blood adjacent to the brainstem in the suprasellar cistern (arrow). (b) Another example of a perimesencephalic haemorrhage on CT scan with blood in front of the pons (arrowhead) and in the (a) (b) left ambient cistern (arrow). extravasated blood on brain CT, in combination with There is a distinct and benign variety of subarachnoid a normal angiographic study. The densest collection of haemorrhage, in which the distribution of extravasated blood is mostly immediately anterior to the extravasated blood on the brain CT scan is different midbrain, in the interpeduncular cistern (Fig. 9.4). In from aneurysmal haemorrhage, in the cisterns around some patients, most or even the only evidence of blood the midbrain or ventral to the pons. The cause of is found in the quadrigeminal cistern, 59–61 or anterior to the bleeding is unknown but it is not a ruptured the pons. 62,63 There is no extension of the haemorrhage aneurysm. The long-term outcome is invariably to the lateral sylvian fissures or to the anterior part of the excellent. This condition accounts for 10% of all interhemispheric fissure. Some sedimentation of blood subarachnoid haemorrhages and two-thirds of in the posterior horns of the lateral ventricles may occur, subarachnoid haemorrhages with a normal but frank intraventricular haemorrhage or extension of angiogram. the haemorrhage into the brain parenchyma rules out this particular condition. 56–58 However, the pattern of Clinically, there is little to distinguish this idiopathic bleeding is not entirely specific: one in 20–40 patients perimesencephalic haemorrhage from aneurysmal hae- with a perimesencephalic pattern of haemorrhage morrhage. The headache onset is more often gradual has a ruptured aneurysm of the basilar or vertebral (minutes rather than seconds) than with aneurysmal artery. 57,64,65 Conversely, about 10–20% of all ruptured haemorrhage, but this has poor predictive value (section posterior fossa aneurysms have a perimesencephalic 9.2.1). 72 Loss of consciousness and focal symptoms are pattern of subarachnoid bleeding on CT. 66–68 To exclude exceptional, and then only transient; a seizure at onset an aneurysm, imaging of the cerebral vasculature is virtually rules out the diagnosis. 73 A memory gap of a few therefore indispensable, but repeated studies after a tech- hours after the haemorrhage occurs in about one-third, nically satisfactory initial study that is negative are not and is associated with enlargement of the temporal needed (section 9.4.1). horns on the initial CT scan. 74 On admission, all patients Perimesencephalic haemorrhage accounts for approx- are in perfect clinical condition, apart from their head- imately 10% of all episodes of SAH and two-thirds of ache. 56,75 Typically, the subsequent course is uneventful, those with a normal angiogram. 64,69–71 It can occur at rebleeding and delayed cerebral ischaemia simply do not any age, including childhood, 10,72 but most patients occur. About 20% of patients have acute hydrocephalus are in their sixth decade, as with aneurysmal haemor- on their admission brain CT scan (Fig. 9.5), associated rhage. In one-third of the patients, strenuous activ- with extravasation of blood in all the perimesencephalic ities immediately precede the onset of symptoms, a cisterns, which probably causes obstruction of the cere- proportion similar to that found in aneurysmal brospinal fluid circulation at the tentorial hiatus. 76 Only haemorrhage. 56 a small proportion have symptoms from this ventricular .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 463 9.1 Causes of spontaneous subarachnoid haemorrhage 463 Fig. 9.5 CT scans of a patient with perimesencephalic haemorrhage with blood in all perimesencephalic cisterns and hydrocephalus with dilatation of the temporal (arrowheads) and frontal horns (arrow). (a) (b) dilatation, and even then an excellent outcome can be or small bulges of the basilar artery. 87 However, it is anticipated. 77,78 The period of convalescence is short, rather unlikely that any of these rare lesions cause all and almost invariably patients are able to resume their instances of idiopathic perimesencephalic haemorrhage. previous work and other activities. 78,79 Rebleeding after the hospital period has not been convincingly docu- 9.1.3 Intracranial arterial dissection mented so far and life expectancy is not reduced com- pared to the general population. 80 Vertebral artery dissection For the time being, the definition of this mild and idiopathic variant of SAH remains a purely descriptive Dissection in general tends to be recognized more often one, based on a combination of radiological and clinical in the carotid than in the vertebral artery (section 7.2.1), criteria. The cause of the bleeding is unknown, largely but SAH from arterial dissection most often occurs from because postmortem studies have not been done, the the vertebral artery (Fig. 9.6), preferentially starting in the very reason being that the outcome is so good. The mild extracranial segment (section 7.2.2). 88,89 Blunt rotational clinical features, the limited extension of the extravasated or hyperextension trauma, even if slight, is a common blood on brain CT and the normal angiograms are all cause of vertebral artery dissection, 90 in adults and also against bleeding from an aneurysm, or in fact from any in children. 91 Iatrogenic causes include not only osteo- other arterial source. Instead, rupture of a vein or a venous pathic manipulation but also surgery for glioma. 92 In malformation in the prepontine or interpeduncular middle-aged patients, dissection may occur more or less cistern seems a reasonable hypothesis. Indeed variants of spontaneously. Sometimes there is an interval of days or venous drainage of the brainstem have been demon- even months between ischaemic symptoms and SAH from strated in a proportion of these patients. 81,82 The hypo- vertebral dissection. 93 What proportion of all SAHs arises thesis of a venous source of the haemorrhage is further from a dissected vertebral artery is not exactly known supported by a single patient with a perimesencephalic but all miscellaneous causes together (including dissec- pattern of haemorrhage caused by a spinal dural arterio- tion) account for only about 5%. In a postmortem study venous fistula. 83 In this patient the fistula was located at of fatal SAH, dissection was found in 5 of 110 patients. 94 the C1 level and drained into a perimedullary vein con- Neurological deficits may accompany SAH from ver- nected to the venous system of the posterior cranial fossa. tebral artery dissection (section 4.2.3): ninth and tenth We have already emphasized that a perimesencephalic cranial nerve palsies, by subadventitial dissection, or pattern of haemorrhage may occasionally (in 2.5–5%) Wallenberg syndrome, partial or complete, indicating be caused by a ruptured posterior fossa aneurysm. By subintimal dissection with impairment of blood flow in the same token, even rarer vascular abnormalities may the territory of the posterior inferior cerebellar artery, also cause haemorrhage in the cisterns ventral to the resulting in ischaemia of the dorsolateral medulla. lower brainstem: a (possible) capillary telangiectasia in Rebleeding is common, between 30% and 70% in differ- the pons, 84 lacunar infarction in the vicinity of the ent series; the interval may be as short as a few hours or haemorrhage, with the conjecture that a small perforat- as long as a few weeks 95–98 and it may occur even after ing artery had occluded and subsequently ruptured, 85,86 proximal clipping of the artery. 99 Recurrent bleeding .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 464 464 Chapter 9 What caused this subarachnoid haemorrhage? Fig. 9.6 CT scan (a) and CT angiogram (b) from a patient with subarachnoid haemorrhage from vertebral arterial dissection. The dissection shows as a narrowing (small arrows) followed by a dilatation (a) (b) (large arrow). from a dissected vertebral artery is fatal in approximately has become clear that haemorrhages from AVMs almost half the patients. invariably involve the brain parenchyma (section 8.2.4). SAH may result if the haemorrhage reaches the surface of the brain, but of all haemorrhages secondary to a Dissection of arteries in the anterior circulation ruptured AVM only 4% are purely subarachnoid, with- The intracranial portion of the internal carotid artery, out any parenchymal component. 114 Given that the or one of its branches, as the site of dissection is far less annual incidence of haemorrhage from an AVM (per common than with the internal carotid artery in the 100 000 in the general population) is of the order of neck, a condition encountered several times a year 0.5, 115,116 against at least six for haemorrhage from in most major neurology centres (section 7.2.1). It ruptured aneurysms, 117 four of which are purely in the should especially be suspected if cerebral angiography subarachnoid space, 118,119 at most only one in every 200 is negative despite a pattern of haemorrhage on CT purely SAHs are caused by an AVM. It is therefore some- that suggests aneurysmal rupture in the anterior thing of a mystery how in a small population-based circulation. 100,101 Reported cases have affected the term- study in Norway 9% (7/76) of SAH episodes were inal portion of the internal carotid artery, 102–104 the attributed to an AVM. 120 middle cerebral artery 105–108 and the anterior cerebral Saccular aneurysms form on the feeding arteries of artery 109–112 (Fig. 9.7). 10–20% of AVMs, presumably because of the greatly Subarachnoid haemorrhage is not an invariable con- increased flow and the attendant strain on the arterial sequence of dissection in the anterior circulation; as wall. If bleeding occurs in these cases, it is more often with patients with vertebral artery dissection, the neuro- from the aneurysm than from the malformation itself, logical symptoms may also result from ischaemia. 101,113 but the site of these aneurysms is different from the In patients with haemorrhage from a dissection, rebleed- classical sites of saccular aneurysms on the circle of ing has been reported in up to half the patients within Willis, and again the haemorrhage is more often into the the first 2 weeks after the initial haemorrhage, resulting brain itself than into the subarachnoid space. 121–124 in a poor outcome in most patients. 108 Very few arteriovenous malformations rupture only into the subarachnoid space. The vast majority form 9.1.4 Rare conditions causing subarachnoid an intracerebral haematoma, with or without extension haemorrhage into the subarachnoid space. If there is an associated These are listed in Table 9.2 and some deserve comment. aneurysm this is generally the source of bleeding. Cerebral arteriovenous malformations Cerebral fusiform aneurysms Cerebral AVMs were formerly believed to cause a sub- A fusiform ‘aneurysm’ of an intracerebral artery is in fact stantial proportion of SAHs, but since the advent of CT it an abnormal dilatation of a segment of the vessel. .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 465 9.1 Causes of spontaneous subarachnoid haemorrhage 465 Table 9.2 Causes of subarachnoid haemorrhage, other than intracranial saccular aneurysms. Idiopathic perimesencephalic haemorrhage (section 9.1.2) Non-inflammatory lesions of intracerebral vessels arterial dissection (sections 7.2.2 and 9.1.3) cerebral arteriovenous malformations (section 9.1.4) fusiform aneurysms (section 9.1.4) cerebral dural arteriovenous fistulae (section 9.1.4) intracerebral cavernous malformation 362 (section 8.2.5) intracranial venous thrombosis (section 9.1.4) cerebral amyloid angiopathy 363,364 (section 8.2.2) blister-like bulges of the internal carotid artery 365,366 rupture of circumferential artery in pontine cistern 367 moyamoya syndrome 368 (section 7.5) Vascular lesions in the spinal cord saccular aneurysm of spinal artery (section 9.1.4) spinal arteriovenous fistula or malformation (section 9.1.4) cavernous malformation at spinal level 340,369 Inflammatory lesions of cerebral arteries (section 7.3) mycotic aneurysms (sections 6.5.9 and 9.1.4) borreliosis 370 (section 7.11) Behçet’s disease 371 (section 7.3.11) primary angiitis of the central nervous system (section 7.3.17) polyarteritis nodosa 135,372,373 (section 7.3.6) Churg-Strauss syndrome 374 (section 7.3.6) Wegener’s granulomatosis 375 (section 7.3.6) Sickle cell disease (section 7.9.8 and 9.1.4) Tumours pituitary apoplexy (section 9.1.4) cerebral metastases of cardiac myxoma (sections 6.5.13 and 9.1.4) malignant glioma 376 acoustic neuroma 377 Fig. 9.7 Subarachnoid haemorrhage from dissection of an cervical meningioma 378 intracranial artery. Top row: CT brain scan within hours of the angiolipoma 379 haemorrhage, showing diffuse extravasation of blood in the schwannoma of accessory nerve or spinal root 380–383 basal cisterns, predominantly on the right side. Middle row, spinal meningeal carcinomatosis 384 left: right catheter carotid angiogram (antero-posterior view) melanoma of the cauda equina 385 after 1 day showing a narrowed segment in the proximal part cervical spinal cord haemangioblastoma 386 of the anterior cerebral artery (arrow). Middle row, right: second Drugs angiogram (oblique view) after 11 days showing even more cocaine use (sections 7.15.1 and 9.1.4) marked narrowing at the same site (arrow). Lower row, left: third anticoagulants (section 9.1.4) angiogram (oblique view), 3 months after the haemorrhage; Head trauma (section 9.1.4) the affected segment has almost returned to a normal calibre Superficial siderosis of the central nervous system (arrow). Bottom row, right: spiral CT scan after intravenous (section 9.1.4) contrast, with maximal intensity projection, 9 months after the haemorrhage; the segment of the proximal right anterior cerebral artery is now completely normal (arrow). The abnormality most often occurs in the vertebro- basilar system, where dilatation is often accompanied Haemorrhages into the vessel wall are probably an import- by elongation and tortuosity, so-called dolichoectasia ant factor in their development (Fig. 9.8). 125 The present- (section 6.3.6). The haemorrhage in patients with verte- ing symptoms mostly result from ischaemia or local brobasilar dolichoectasia may be the initial event, 127 but compression, but rupture may also occur (Fig. 9.9) when most often it follows other symptoms. 126,128,129 The risk intraparenchymal extension of the haemorrhage is more of rupture is relatively high, according to analyses from common than purely subarachnoid haemorrhage (SAH). 126 a few patient series, if there is evidence of aneurysm .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 466 466 Chapter 9 What caused this subarachnoid haemorrhage? Fig. 9.8 MR scans from a woman aged 63 with vertebrobasilar transient ischaemic attacks and a history of smoking and hypertension. (a) T2-weighted MR showing an enlarged basilar artery. The arrow points to the flow void of the basilar artery. (b) Two years later no new clinical symptoms had occurred, but the wall of the aneurysm has enlarged from intramural thrombus. The arrow points to the flow void of the basilar artery; the straight line shows the intraluminal (a) (b) thrombus. (a) (b) (c) Fig. 9.9 Subarachnoid haemorrhage from a ruptured fusiform subarachnoid blood as well as blood in the third (arrowhead) aneurysm of the basilar artery. (a) CT brain scan showing and fourth (arrow) ventricle. (c) CT angiogram showing the thrombus in the wall of the basilar artery (arrow) and blood in enlarged lumen of the basilar artery (arrow). the basal cisterns (arrowheads). (b) CT brain scan showing enlargement, if the aneurysm configuration is transitional posterior inferior cerebellar artery. 136 If intracranial fusi- between a fusiform and a dolichoectatic abnormality, 129 form aneurysms are multiple, a cardiac myxoma should with extensive lateral displacement of the basilar artery, be suspected (section 6.5.13 and see below). 137 in the presence of hypertension, if the patient is taking antiplatelet drugs or anticoagulants, or if the patient is Cerebral dural arteriovenous fistulae female. 126 SAH may also occur from large fusiform aneurysms of Dural arteriovenous fistulae of the tentorium or the the middle cerebral artery (Fig. 9.10); the dilatation may basal parts of the dura can give rise to a basal haemor- be secondary to dissection or to atherosclerosis. 130,131 rhage that is indistinguishable on CT from aneurysmal Other locations are even rarer, such as the anterior cere- haemorrhage 138 (section 8.2.8); other patients present bral artery, 132 the posterior cerebral artery, 133 the sup- with intracerebral or subdural haemorrhage. 139 The erior cerebellar artery, 134 the anterior inferior cerebellar anomaly is rare and can be found from adolescence to artery (secondary to polyarteritis nodosa) 135 and the old age. Rebleeding may occur. 139,140 .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 467 9.1 Causes of spontaneous subarachnoid haemorrhage 467 Fig. 9.10 Subarachnoid haemorrhage from a fusiform aneurysm of the left middle cerebral artery. (a) CT brain scan and (b) CT angiography showing the aneurysm (arrows). (a) (b) symptom. Potential precipitating factors are starting Intracranial venous thrombosis anticoagulation, general surgery, vaginal delivery, and (See section 7.21) discontinuation of dopamine agonists for prolact- Rarely, intracranial venous thrombosis presents with inoma. 150 The initial features are a sudden and severe both the clinical and radiological features that initially headache, with or without nausea, vomiting, neck stiff- suggest SAH from a ruptured aneurysm. In such cases, ness and depressed consciousness. 151–153 Circulatory the diagnosis is largely based on neuroimaging. Recogni- shock is not uncommon. 154 Characteristics to distin- tion of intracranial venous thrombosis-induced SAH is guish pituitary apoplexy from other causes of SAH are important because in both conditions treatment should an accompanying decrease in visual acuity or a dis- be initiated without delay, while the nature of the inter- turbance of eye movements through compression of ventions is completely different: venous thrombosis- the oculomotor, trochlear and abducens nerves in the induced SAH should be treated with anticoagulants, 141 adjacent cavernous sinus. 155 Brain CT or MR scanning whereas these are obviously contraindicated in aneurys- reveals the pituitary fossa as the source of the haemor- mal SAH until the the aneurysm has been occluded. rhage, and in most instances the adenoma itself is visible; The clinical features of intracranial venous thrombosis associated radiological features may be extension of the may closely mimic SAH since the headache may be sudden haemorrhage into the frontal lobe, 156 or thickening of in onset. 142 Also any extravasation of blood may be at the mucosa of the sphenoid sinus. 157 the base of the brain if the venous congestion affects the basal parts of the temporal lobe as with thrombosis of Cerebral mycotic aneurysms the transverse, sigmoid or straight sinus. 143,144 The dia- gnosis is much easier if subarachnoid blood is located Mycotic aneurysms underlying SAH are most frequently at the convexity, as may occur with thrombosis of the caused by infective endocarditis (section 6.5.9) or superior sagittal sinus or cortical veins, 145,146 which prac- aspergillosis (section 7.11). Of course, in the context of tically excludes a ruptured aneurysm. infective endocarditis most strokes are (haemorrhagic) infarcts or intracerebral haemorrhages from pyogenic arteritis (section 8.2.11). Aneurysms associated with Pituitary apoplexy infective endocarditis are most often located on distal Pituitary apoplexy is a somewhat archaic term for branches of the middle cerebral artery, because the septic arterial haemorrhage within a pituitary tumour, prob- emboli tend to lodge at the periphery of the arterial ably caused by tissue necrosis involving the wall of one tree Fig. 6.9. Only about 10% of the aneurysms develop or more hypophyseal arteries. There can also be diffuse at more proximal sites. 158 Consequently, haemorrhages haemorrhage in the basal cisterns, mimicking a ruptured from mycotic aneurysms occur mostly in the cortex and aneurysm. 147–149 The pituitary tumour may have already in the underlying white matter, and only occasionally in been known about, or the haemorrhage may be the first the subarachnoid space, at the convexity of the brain .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 468 468 Chapter 9 What caused this subarachnoid haemorrhage? or even at its base. 159 However, in SAH associated with cause of (intracranial) subarachnoid haemorrhage. In infective endocarditis an aneurysm is not always iden- our database of 2142 patients in the period 1985–2004, tified, 160 presumably because pyogenic arteritis can also we have only one patient, while a review of the literature lead to rupture of the arterial wall without aneurysm found 35 patients. 170 The arteriovenous shunt was formation. 161 located at the craniocervical junction in 14 patients, at the cervical level in 11 and at the thoracolumbar level Most mycotic aneurysms associated with infective in the remaining 11 patients. Intracranial SAH from endocarditis are located superficially in the cerebral a spinal arteriovenous shunt occurred at any age (4–72 hemisphere, in the cortex or underlying white matter; years). Most patients (n = 26, 72%) had no disabling they rupture mostly into brain tissue, but sometimes deficits at discharge or follow-up but rebleeding may into the subarachnoid space. occur, even repeatedly. 171 Aspergillosis is a dreaded complication in immuno- Aneurysms of spinal arteries suppressed patients. Mycotic aneurysms from aspergillo- sis are usually located on the proximal part of the basilar SAH from aneurysms of spinal arteries is also extremely or carotid artery and rupture causes massive and some- rare, with only about 20 patients on record. 172,173 These times fatal SAH in the basal cisterns, indistinguishable aneurysms are fusiform rather than saccular and develop from that of a saccular aneurysm. 162–164 Aspergillosis is along the course of an artery rather than at branching difficult to diagnose but should particularly be suspected sites. A spinal aneurysm may form in the nidus of a in patients undergoing long-term treatment with anti- spinal AVM, 174 or on a feeding artery of a spinal AVF. 175 biotics or immunosuppressive agents. Most patients with As with AVMs of the spinal cord, the clinical features of haematogenous dissemination have pulmonary lesions, spinal SAH may be accompanied by those of a transverse but the chest X-ray may be normal early in the course. 165 lesion of the cord, partial or complete. Tests to detect metabolites produced by the fungus, or aspergillus-specific antibodies in serum, are now avail- Sickle cell disease able, but their diagnostic properties have not yet been established. 166 Sickle cell disease is commonly complicated by ischaemic Other sources of microorganisms leading to the stroke (section 7.9.8), but seldom by SAH. 176,177 Thirty formation of mycotic aneurysms include the teeth per cent of patients with sickle cell disease and SAH (Pseudomonas aeruginosa). 167 are children; their CT scans show blood mostly in the superficial cortical sulci and angiograms reveal no aneurysms but often multiple distal branch occlusions Cerebral metastases from cardiac myxoma 178,179 and a leptomeningeal collateral circulation. The Cardiac myxoma is an extremely rare cause of aneurysm outcome is poor. Young adults in whom sickle cell dis- formation; the tumour can, after metastasizing to an ease underlies SAH usually have one or more aneurysms intracranial artery, infiltrate the wall and thus cause an at the base of the brain. aneurysm to develop, sometimes more than 1 year after operation for the primary tumour 168 (section 6.5.13). Cocaine use These aneurysms have also been reported in children. 169 The aneurysms are often fusiform and may be multiple Cocaine use is associated with haemorrhagic as well as (Fig. 6.13). 137 On MR imaging, T1 sequences may show with ischaemic stroke (sections 7.15.1 and 8.5.4). In unusual foci of signal dropout surrounded by hyper- patients with SAH, about half have a vascular anomaly, intense rims around the aneurysms, similar in appearance an aneurysm or arteriovenous malformation, 180 but to the artifacts produced by metallic aneurysm clips; the patients are younger and the aneurysms smaller these are probably caused by dense accumulation of iron than usual. 181 Rebleeding does occur, even in patients and haemosiderin produced by recurrent intramural with a normal angiogram, and the outcome is often haemorrhages. poor. 182,183 The source of the haemorrhage in patients without a vascular anomaly is unknown. Although biopsy-proven vasculitis has been found, 184 angiography Spinal arteriovenous malformations and dural seldom shows the changes suggestive of vasculitis arteriovenous fistulas 180,185 but this is a very insensitive test. Ingestion of Spinal arteriovenous malformations (AVMs) and dural ephedrine or ‘ecstasy’ may also precipitate aneurysmal arteriovenous fistulas (DAVFs) are an extremely rare SAH. 186,187 .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 469 9.1 Causes of spontaneous subarachnoid haemorrhage 469 therefore be rewarding, especially in patients with dis- Anticoagulation-related subarachnoid haemorrhage proportionate headache or neck stiffness. If aneurysmal rupture occurs in patients on anti- coagulants the outcome is almost invariably poor. 188 Spontaneous subarachnoid haemorrhage may lead to Anticoagulants, however, are a rare cause for SAH in head trauma, while head injury may cause superficial itself. In a series of 116 patients with intracranial, but contusion of the brain, with accumulation of blood in extracerebral, haemorrhage while on anticoagulants, the subarachnoid space. If there is any doubt, it is vital seven had only SAH, and in just three of these patients to disentangle the course of events as accurately as was there no cause for the haemorrhage other than anti- possible. coagulation. 189 Severe coagulopathy, other than anti- coagulant-induced, for example congenital deficiency If trauma is the cause of SAH, CT scanning usually of factor VII, is also a rare cause of haemorrhage confined shows most of the blood in the superficial sulci at the to the subarachnoid space. 190 convexity of the brain, adjacent to a fracture or to an intracerebral contusion. Head trauma Superficial siderosis of the central nervous system Trauma and spontaneous SAH are sometimes difficult to disentangle. Patients may be found alone after having This condition is characterized by iron overload of the been beaten up in a brawl or hit by a drunken driver who pial membranes, through chronic oozing of blood from drove off. There may be no external wounds to indicate any source in the subarachnoid space. It has been an accident, a decreased level of consciousness making included in this section on SAH only for the sake of it impossible to obtain a history, and neck stiffness completeness. The CSF contains blood or haemosiderin, causing the patient to be worked up for SAH (Fig. 9.11). but the clinical picture is completely different and does Conversely, patients who rupture an aneurysm while not include sudden headache. 195,196 The syndrome riding a bicycle or driving a car may hit a tree or another almost invariably includes subacute sensorineural deaf- vehicle, and the initial diagnosis will be ‘traffic accid- ness (95% of patients), cerebellar ataxia (88%) and pyra- ent’. 191 The diagnostic conundrum becomes really midal signs (76%). Less frequent features are cognitive difficult when patients after aneurysmal rupture fall, impairment, 197 bladder disturbance and anosmia. Men hit their head and sustain a skull fracture, 192 or when are more often affected than women (3 : 1). A source of head trauma causes an aneurysm to burst. 193,194 Meticul- bleeding has been identified in a little more than half ous reconstruction of traffic or sports accidents may of the cases reported up to 1995. 196 (b) (a) Fig. 9.11 CT brain scan of a 66-year-old woman with (a) a repeated episodes of falling before; on admission after this ‘contre coup’ subarachnoid haemorrhage and (b) a skull base traumatic subarachnoid haemorrhage, sick sinus syndrome was fracture (indicated) after a fall on the floor. She had had diagnosed. .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 470 470 Chapter 9 What caused this subarachnoid haemorrhage? Causes of chronic bleeding include: of the head and spinal canal. Although non-aneurysmal • spinal pseudomeningoceles, spontaneous 198 or second- types of SAH were distinguished more than 20 years ago, 56 ary to traumatic root avulsion; 199,200 a steady stream of publications in which SAH patients • vascular abnormalities of the dura surrounding the with a normal angiogram are still treated as a single spinal cord or cervical roots; 201 group has continued to clutter up the scientific literat- • a vascular tumour such as an ependymoma of the ure. That they contribute so little knowledge is to some cauda equina; not really the first place to look if the extent the result of the invariably retrospective design, problem is deafness; 202 but the most serious flaw is that they contain a mixed • as a late complication of neurosurgical interven- bag of patients. The three most common subgroups are: tions; 203,204 • patients whose ‘SAH’ is not real but in whom a mis- • or any other vascular abnormality, including rarities diagnosis results from a traumatic lumbar puncture such as familial transthyretin-related amyloidosis of (section 3.7.3); meningeal vessels. 205,206 • patients with non-aneurysmal types of haemorrhage Probably the remaining cases are also due to chronic (section 9.1.2); haemorrhage, but it is not clear from where. The high • patients with a pattern of haemorrhage that is entirely iron content of the pial membranes cause a characteristic consistent with a ruptured aneurysm but who never- signal on MR scanning (Fig. 9.12). 199,207 theless have a normal angiogram. It is this last category of patient that we shall consider here. This group is getting smaller as the neuroradiological investigations Idiopathic subarachnoid haemorrhage become more sophisticated, but it is probably still In some patients no cause for a SAH is ever found, even heterogeneous, encompassing unidentified lesions of after extensive and repeated radiological examinations arteries, arterioles, capillaries and veins. (b) (a) Fig. 9.12 Superficial siderosis of the nervous system. A T2- due to a paramagnetic effect, over the entire pial surface weighted magnetic resonance image of the brain in a 50-year- (arrows), and in the acoustic nerves (arrowheads). (With old man who presented with bilateral sensorineural hearing permission from Padberg & Hoogenraad 2000.) loss. The accumulation of ferric ions causes signal loss (black), .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 471 9.2 Clues from the history 471 There are three studies of patients with an aneurysmal Table 9.3 Causes of primary intraventricular haemorrhage. pattern of bleeding on CT who were separately distin- guished among a larger group with SAH and one or more Uncommon aneurysms 387,388 negative angiograms. After a single negative angiogram, Posterior inferior cerebellar artery, or its choroidal branch 389 saccular aneurysms still may become symptomatic in Anterior inferior cerebellar artery 390 a minority of patients, by rebleeding, delayed cerebral Arteriovenous malformations ischaemia or compression of a cranial nerve. 69,208 After 218–220 In the ependymal lining three negative angiograms, no episodes of aneurysmal Of the choroid plexus 391 rebleeding were documented, at least in a small series Dural fistula of a cerebral venous sinus 392,393 of 15 patients followed up for an average period of Occlusive arterial disease 5.5 years, but some patients had an ischaemic stroke or Moyamoya syndrome: idiopathic, 394 atherosclerotic 395 or an intracerebral haemorrhage in the meantime. 209 The with associated aneurysm 396 (section 7.5) occurrence of all these complications is in stark contrast Lacunar infarction 397 to patients with a non-aneurysmal perimesencephalic Clotting disorders 398 pattern of haemorrhage, in whom the subsequent course Haemophilia Tumours is almost invariably uneventful. Pituitary adenoma 399 or metastasis 400 The substantial risk of rebleeding in patients with an Ependymoma 401 aneurysmal pattern of haemorrhage and a single neg- 402 Meningioma ative angiogram means that at least in some patients an Schwannoma 382 aneurysm escapes radiological detection. Other than Infectious diseases technical reasons, such as insufficient use of oblique Brain abscess 403 projections or misreading the films, 210 this may be Parasitic granuloma 404 because of: Drugs • Narrowing of blood vessels by ‘vasospasm’ which has Cocaine 180 been suggested in some cases. 211,212 Amphetamine 405,406 • Thrombosis of the neck of the aneurysm, or of the Wernicke’s encephalopathy 407 entire sac, is another possible reason. 212 • Obliteration of the aneurysm by pressure of an in exceptional cases have these actually been demon- adjacent haematoma may also prevent visualization, strated. 218–220 Specific other causes range from tumours, particularly with aneurysms of the anterior commun- which are immediately obvious on CT scanning, to small icating artery. 213 aneurysms at uncommon sites which only assiduous investigation can uncover (Table 9.3). 9.1.5 Spontaneous intraventricular haemorrhage Intraventricular haemorrhage is usually caused by either a ruptured aneurysm (most often on the anterior communicating artery complex) 214 or by extension of 9.2 Clues from the history an intracerebral haemorrhage. In both situations, the outcome is worse with intraventricular rupture than without, and an intraventricular clot of more than 20 mL The a priori probability of an aneurysm as the cause of is invariably fatal without surgical intervention. 215,216 subarachnoid haemorrhage (SAH) is so high (85%) that In contrast, the outcome of ‘primary’ intraventricular other conditions are very unlikely unless there are very haemorrhage, i.e. without detectable cause, is much strong clues in the history (head trauma, infective endo- better than if it is associated with subarachnoid or carditis, sickle cell disease, pituitary adenoma) or in any intracerebral haemorrhage; patients may survive even antecedent events (violent head movements, cocaine with intraventricular haemorrhages far exceeding 20 ingestion), or if the first pain was felt in the neck rather mL. 216,217 The advent of CT scanning proved that intra- than in the head (arterial dissection, or spinal SAH). ventricular haemorrhage is not the invariably lethal con- dition it was once thought to be when the diagnosis 9.2.1 Nature of the headache at onset was made only in those who died. ‘Primary’ – or idiopathic – intraventricular hae- The key feature in diagnosing SAH is the sudden onset of morrhage is often speculatively attributed to occult an unusually severe headache. Classically it comes on in vascular malformations in the ependymal wall. But only seconds (‘a flash’, ‘just like that’, ‘a bolt from a blue sky’, .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 472 472 Chapter 9 What caused this subarachnoid haemorrhage? ‘as if I was hit on the head’), or in a few minutes at most. with de novo epilepsy over the age of 25 will have under- However, the speed of onset of headache is of little help lying conditions other than SAH, but the diagnosis in distinguishing aneurysmal from perimesencephalic should at least be suspected if any postictal headache is haemorrhage. Although headache develops more often unusually severe or prolonged. Seizures have not been in minutes rather than in a split second in patients documented in patients with perimesencephalic SAH with a perimesencephalic haemorrhage (35%) than in but they may well complicate haemorrhages from arter- patients with aneurysmal haemorrhage (20%), 73 rup- ial sources other than aneurysms, such as dissection of tured aneurysms are nine times as common as non- the vertebral artery, or a vascular malformation. aneurysmal perimesencephalic haemorrhages. 89 Thus, only three of every 21 patients presenting with a more 9.2.4 Antecedent events gradual onset of headache from SAH have a perimesen- cephalic haemorrhage, another example of the risk or A previous episode of sudden headache hardly increases prevention paradox (section 3.7.1). And nor does vomit- the likelihood of aneurysmal SAH despite a still wide- ing accompanying the headache discriminate between spread belief in the existence of so-called ‘sentinel aneurysmal and perimesencephalic haemorrhage. In headaches’, thought to be ‘warning leaks’ from the patients with perimesencephalic haemorrhage vomiting aneurysm that is eventually diagnosed. Indeed, on occurs in four out of every five patients, 73 which is no specific questioning, about one-third of patients recall less than after aneurysmal rupture; it can even be the a previous episode of headache that was unusually sole manifestation of the haemorrhage. 221 severe and lasted several hours. 225 Many neurosurgeons Pain at onset in the lower part of the neck (upper neck and neurologists are therefore convinced that import- pain is common with ruptured intracranial aneurysms), ant advances in the overall management of ruptured or a sudden and stabbing pain between the shoulder aneurysms can be expected from early recognition of blades (coup de poignard or dagger thrust), with or minute episodes of subarachnoid haemorrhage, fol- without radiation to the arms, suggests a spinal arteri- lowed by emergency clipping or coiling of the aneurysm. ovenous malformation or fistula as the source of SAH A major difficulty with the notion of these ‘warning (section 9.1.4). leaks’ is that almost all the studies have been hospital- based, most have been retrospective, and that even Sudden pain in the lower neck or between the prospectively conducted studies are probably biased by shoulder blades is a pointer to spinal subarachnoid hindsight (recall bias). haemorrhage, particularly if the pain radiates to the In a prospective study of 148 patients with sudden, shoulders or arms. Dissection of the thoracic aorta is severe headache identified in general practice, no neuro- another possibility. logical cause of headache was found in 93 and after 5 years of following them up there were no episodes of SAH. Only two of the 37 patients with SAH had had 9.2.2 Loss of consciousness previous episodes of sudden headache on systematic Loss of consciousness at onset occurs in over half questioning by the general practitioner at the time of the patients with aneurysmal SAH (section 3.7.1). presentation with the headache. 226 Also, in the 37 pat- Some patients complain of headache before they lose ients with SAH in this series, the amount and distribu- consciousness, and all patients have severe headache if tion of extravasated blood on brain CT, as well as the they regain consciousness. Non-aneurysmal perimesen- overall outcome, was similar to that in a previous hospital- cephalic SAH is typically associated with normal cognit- based series of patients with SAH. In other words, first- ive function; loss of consciousness or altered behaviour ever episodes of SAH detected (or missed) in general practically rules out this diagnosis, but amnesia may practice are not ‘small leaks’, but the real thing and occur, mostly in association with an enlarged ventricular represent the same spectrum of severity as those seen in system. 74 Head trauma should always be considered in hospital. patients who are found unconscious (section 9.1.4). A second approach to understanding the notion of ‘warning leaks’ is to study the clinical and radiological features in a prospective series of patients admitted to 9.2.3 Epileptic seizures hospital with aneurysmal SAH and then to compare Epileptic seizures at the onset of aneurysmal SAH occur those with and without a history of preceding episodes in about 10% of patients, 222–224 those with a large of sudden severe headache. There is no difference between amount of cisternal blood on brain CT being relatively these two groups, whereas patients with documented more often affected. 222 Almost every patient presenting rebleeding in hospital have more severe clinical deficits .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 473 9.3 Clues from the examination 473 and more abnormalities on the CT scan. 227 In brief, the temporal fields, but often these symptoms lead to the notion of frequent ‘warning leaks’ is not supported by diagnosis only in retrospect. On CT scanning the hae- epidemiological, clinical and radiological evidence. This morrhage is usually confined within the tumour capsule, does not mean that an episode of SAH cannot be missed rarely extending throughout the basal cisterns as with by primary care physicians – or hospital doctors. ruptured aneurysms. A history of even quite minor neck trauma or of sudden, unusual head movements before the onset of 9.2.6 Family history headache may provide a clue to the diagnosis of verte- bral artery dissection as a cause of SAH. And head trauma A family history of SAH can be a useful clue in patients and primary SAH may be confused as we have previously with sudden headache, although of course that same fact discussed (section 9.1.4). Trauma should always be may give rise to false alarms. There are some families in suspected in patients found unconscious in the street, which numerous relatives suffer from ruptured aneurysms even if there is marked neck stiffness and no superficial (section 9.1.1), but even in cases of so-called sporadic wound. Conversely, a traffic accident may sometimes be SAH, the risk in first-degree relatives is increased. 20,24,25 the result rather than the cause of SAH, and invaluable Families in which aneurysmal rupture has occurred in information may be obtained from the police or ambu- two or more first-degree relatives may have an under- lance workers. For example, in a patient known to have lying or associated disorder (Table 9.1), but these repres- swerved from one side of the road to the other before ent only a minority of familial aneurysms. crashing into someone else, the a priori probabilities are rather different (i.e. illness, falling asleep) from those in someone hit by a car that ignored a red traffic light. 9.3 Clues from the examination 9.2.5 Medical history In patients with a distant history of head injury, and particularly if there was a skull fracture, a dural arterio- 9.3.1 Level of consciousness venous fistula should be suspected, since healing of the fracture may be accompanied by the development of If the level of consciousness is depressed at the time such a lesion. 228 of the initial examination, it is important to ascertain Mycotic aneurysms may give rise to SAH even in pat- whether this was the situation from the onset, in which ients not known to have a disorder of the heart valves, case it should probably be attributed to global perfusion but this presentation of infective endocarditis is excep- failure caused by the high intracranial pressure at the tional. 229 For practical purposes the possibility can be time of rupture, or sometimes to an intracerebral or safely dismissed in a previously healthy patient in whom subdural haematoma. On the other hand, if the level of the haemorrhage is located at the base of the brain. A consciousness deteriorated later, other, often treatable diagnosis of a ruptured mycotic aneurysm may well be causes should be suspected, such as acute hydrocephalus entertained, however, if there is a history of malaise and (section 14.2.4) or oedema formation around an intra- a haemorrhage located at the convexity of the brain. cerebral haemorrhage. If the level of consciousness was Usually it will not be hard for the physician to discover depressed from the outset, the bleeding is very likely sickle cell disease, a history of cardiac myxoma, or the to have been from an arterial source; patients with influence of coagulation disorders. The use of anti- perimesencephalic haemorrhage have a normal level of coagulants in itself should not be regarded as a sufficient consciousness at onset. 75 However, a depressed level of explanation for SAH (section 9.1.4); the search for an consciousness on arrival at the emergency department underlying lesion ought to be just as vigorous as in other does not entirely rule out a perimesencephalic haemor- patients. rhage, because acute hydrocephalus leading to coma can Pituitary apoplexy may be difficult to diagnose if an occur within the first hours after the haemorrhage. 76 adenoma is not already known about, particularly if A few patients with SAH (2–16%) enter a confused a decrease in the level of consciousness precludes a and agitated state (delirium). 230,231 Of course, in patients proper assessment of any visual and oculomotor deficits. presenting with an acute confusional state to an emer- Usually, the underlying adenoma has insidiously man- gency department, causes other than SAH are much ifested itself before the dramatic occurrence of the hae- more likely – SAH is the cause in only around 1% in this morrhage, such as by a dull retro-orbital pain, fatigue, a scenario. 232 However, more than once, such behaviour gradual decrease of visual acuity, or constriction of the has been misinterpreted as psychological in origin. But .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 474 474 Chapter 9 What caused this subarachnoid haemorrhage? on careful assessment most patients with SAH who do found if the it does not exceed 38.5°C and the pulse rate present with a confusional state have had an episode of has not increased. Patients with further or later increases loss of consciousness, severe headache or subtle signs in temperature should be carefully investigated for infec- on neurological examination which reveal the purely tion (section 14.3.3). neurological cause of the behavioural disorder. 230 9.3.5 Blood pressure 9.3.2 Neck stiffness In most patients with SAH, regardless of its cause, blood Neck stiffness is a common sign in SAH of any cause but pressure is increased early after the onset of the haemor- it takes hours to develop and therefore cannot be used to rhage. A low blood pressure in a patient with sudden exclude the diagnosis if a patient is seen soon after the headache should bring pituitary apoplexy to mind sudden-onset headache. Neck stiffness is also absent in (section 9.1.4), or myocardial damage secondary to deep coma. If present, the sign does not distinguish intracranial aneurysm rupture (section 14.9.3). between the different causes of SAH, nor between SAH and meningitis (section 3.7.1). 9.3.6 Focal neurological deficits Classically, in the acute phase of aneurysmal SAH, there 9.3.3 Subhyaloid haemorrhages are no neurological signs other than those of meningeal Subhyaloid haemorrhages occur if a sudden increase in irritation, but exceptions to this rule can provide use- cerebrospinal fluid (CSF) pressure is transmitted to the ful information about the site or the extent of the CSF spaces surrounding the optic nerves and blocks the haemorrhage (Table 9.4). Later, in the second or third venous outflow from the retina, which in turn leads to week after rupture, focal deficits are not uncommon, rupture of retinal veins (section 3.7.1). Thus, subhyaloid most often as a consequence of secondary ischaemia haemorrhages point to an arterial source of the haemor- (section 14.7.1). rhage. Such intraocular haemorrhages occur in approx- In some patients, there may have been focal deficits imately 17% of patients with aneurysmal haemorrhage or other symptoms before rupture, especially if the who survive the acute phase; 233,234 in half of them aneurysm is large. For example: the blood remains confined to the space between the • cranial nerve palsies, especially of the olfactory, optic retina and the vitreous body, in the other half it ruptures and oculomotor nerves; 238,239 into the vitreous body (Terson syndrome) (section • deficits as a result of local compression of brain 14.10.1). 235 Exceptionally, preretinal haemorrhages are tissue; 240 the only sign of SAH. 236,237 • ischaemic deficits through embolism (section 7.6); • or focal epilepsy. 241 But aneurysms smaller than 1 cm may occasionally 9.3.4 Pyrexia 242,243 cause such deficits without having ruptured. An In most patients the body temperature rises during the unruptured aneurysm may even cause intermittent first 2–3 days after SAH, usually with no infection being ptosis (‘pseudomyasthenia’). 244 Table 9.4 Focal neurological signs early after subarachnoid haemorrhage, and their explanation. Sign Most common explanation Hemiparesis Large subarachnoid haemorrhage in sylvian fissure (middle cerebral artery aneurysm) Paraparesis Aneurysm of anterior communicating artery; spinal arteriovenous malformation Cerebellar ataxia, Wallenberg Dissection of vertebral artery syndrome or both IIIrd cranial nerve palsy Aneurysm of internal carotid artery at the origin of posterior communicating artery; rarely aneurysm of basilar artery or superior cerebellar artery, or pituitary apoplexy VIth cranial nerve palsy Non-specific rise of intracranial pressure IXth–XIIth cranial nerve palsy Dissection of vertebral artery Sustained downward gaze, Acute hydrocephalus, with dilatation of the small proximal part of the sylvian aqueduct and unreactive pupils Note: intracerebral haemorrhages may give rise to other deficits, depending on their site. .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 475 9.3 Clues from the examination 475 pressure, at the time of rupture or later. Therefore sixth Visual field defects nerve palsy has no localizing value, though occasionally Ruptured anterior communicating artery aneurysms aneurysms of the posterior circulation cause direct may, in exceptional cases, compress the optic nerve or compression. 257 its blood supply and cause monocular blindness. 245,246 They may also penetrate one side of the optic chiasm, Lower cranial nerve palsies and with posterior lesions of the chiasm (optic tract) the visual field defect may be hemianopic. 247 However, Transmural dissection of the vertebral artery may lead involvement of the optic chiasm should always raise not only to SAH, but also to compression of the ninth or the possibility of haemorrhage into a pituitary tumour tenth nerve 258 and to ischaemia in the territory of the (section 9.1.4). posterior inferior cerebellar artery. 95 Third cranial nerve palsy Hemiparesis Complete or partial third nerve palsy is a well-recognized Hemiparesis at onset occurs in approximately 15% sign after rupture of aneurysms of the internal carotid of patients with a ruptured aneurysm, usually of the artery at the origin of the posterior communicating middle cerebral artery. 259 As with other motor sym- artery. 248 It may also occasionally occur with aneurysms ptoms that are descibed below, the deficit may only be of the basilar tip, or of the superior cerebellar artery, 249 short-lived (for a period of a few minutes) but because and has once been reported with non-aneurysmal peri- these deficits may provide a clue to the cause of SAH, mesencephalic haemorrhage. 250 The pupil is most often or the site of the aneurysm, they should not be dis- dilated and unreactive but in some patients the pupil regarded. Aneurysms vastly outnumber all other is spared. 251,252 Bilateral oculomotor palsies can result potential causes of SAH, so the presence or absence of from pituitary apoplexy (section 9.1.4) and there may a hemiparesis does not contribute much to the dia- be an interval of several days between the oculomotor gnosis of rarer causes, in which hemiparesis may be rel- palsy and then the haemorrhage, presumably by expan- atively common, for example with ruptured mycotic sion of the wall of the aneurysm first and later the aneurysms. rupture. Reactive CSF pleocytosis has been reported in aneurysmal third nerve palsies, which erroneously sug- Cerebellar signs gests a primary inflammatory process. 253 Deficits indicating lesions of the cerebellum or brainstem, such as dysmetria, scanning speech, rotatory nystagmus Parinaud syndrome or Horner syndrome, strongly suggest vertebral artery After subarachnoid haemorrhage (SAH), small, unreact- dissection (section 9.1.3). ive pupils with impairment of vertical eye movements usually signify hydrocephalus rather than a direct impact Paraparesis of the haemorrhage on the midbrain. In a prospective study of 34 patients with acute hydrocephalus after Early paraparesis may be a manifestation of a bifrontal SAH, 30 had an impaired level of consciousness, nine of haematoma complicating rupture of an anterior com- these 30 had small, non-reactive pupils, and four of these municating artery complex aneurysm. 260 Later, if it nine also showed persistent downward deviation of the develops after an interval of several days, it is more likely eyes, with otherwise intact brainstem reflexes. 254,255 to reflect delayed ischaemia in the territory of both The eye signs reflect dilatation of the proximal part of anterior cerebral arteries. 261 the aqueduct, which causes dysfunction of the pretectal area. 256 All nine patients with non-reactive pupils had a Monoparesis relative ventricular size of more than 1.2 and were in coma, i.e. they did not open their eyes, obey commands Weakness of one leg in the setting of SAH is most or utter words. often caused by a ruptured aneurysm of the anterior communicating artery, 262 but occasionally and quite unexpectedly the aneurysm is of the posterior inferior Sixth cranial nerve palsies cerebellar artery – explained by the close proximity of Sixth nerve palsies, often bilateral in the acute stage, the aneurysm to the corticospinal tract to the contra- usually result from the sustained rise of intracranial lateral leg. 263 .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 476 476 Chapter 9 What caused this subarachnoid haemorrhage? (a) (b) Fig. 9.13 A 47-year-old woman with a subarachnoid haemorrhage and two aneurysms. The pattern of haemorrhage points to the one that had ruptured. (a) CT scan showing diffuse haemorrhage in the basal cisterns. (b) CT scan showing more blood in the right than in the left sylvian fissure. (c) Catheter angiogram showing an aneurysm on the proximal part of the right middle cerebral artery (circled), it was this one which had ruptured. (d) Catheter angiogram showing a larger aneurysm on the proximal part of the left middle cerebral (c) (d) artery (circled). their site, and also the radiological characteristics of 9.4 Investigations non-aneurysmal sources of haemorrhage. The distribution of extravasated blood on brain CT is an important though not infallible guide in deter- The following sections are devoted to the investigations mining the presence and site of the ruptured aneurysm. aimed at detecting the underlying cause of SAH, with a Identifying the source of haemorrhage from the scan is view to treatment, but of course the other investigations especially helpful if more than one aneurysm is found needed to assess and monitor the patient’s general medi- (Fig. 9.13) because there is a vast difference between the cal condition remain essential: full blood count, glucose, management of a ruptured aneurysm (urgent) (section urea, electrolytes, chest X-ray and an electrocardiogram. 14.4) and an unruptured aneurysm (not urgent, if indi- cated at all) (section 15.2.4). This applies particularly to elderly patients, in whom surgical or endovascular repair 9.4.1 CT scanning of the brain of any additional unruptured aneurysms is not always CT brain scanning is still the first-line investigation if indicated. SAH is suspected because of the characteristic appear- ance of extravasated blood (section 3.7.3). On MR scan- Intracerebral extension of the haemorrhage ning, the abnormalities are much more subtle, at least in the acute stage. In this section, we will describe the Any intracerebral extension of the SAH is a good indica- patterns of bleeding in ruptured aneurysms, according to tor of the site of the ruptured aneurysm, whether the .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 477 9.4 Investigations 477 (c) (a) (b) Fig. 9.14 CT brain scans after rupture of an aneurysm of the large clot in the distended fourth ventricle (arrow). (b) A higher anterior communicating artery; the haemorrhage extends into slice showing extension of the haematoma into the frontal lobe the brain parenchyma and the ventricular system. (a) CT slice (black arrowhead), blood in the temporal horn of the lateral through the base of the brain shows a haematoma in the right ventricle (white arrowhead), and the third ventricle (arrow). gyrus rectus (black arrowheads), intraventricular blood in the (c) CT angiogram shows the aneurysm (arrow) adjacent to the temporal horn of the lateral ventricle (white arrowhead), and a haematoma (arrowheads). haematoma is truly intraparenchymal or only distends Middle cerebral artery aneurysms are almost exclus- the subarachnoid space. The prediction of the site of ively located close to the temporal bone, where the the ruptured aneurysm is correct in at least 90% of main stem of the artery divides and turns superiorly and haematomas. 264,265 posteriorly to enter the lateral part of the sylvian fissure. Haematomas from an aneurysm of the anterior com- Haematomas from aneurysms of this type usually extend municating artery (Fig. 9.14) touch the midline with from this point posteriorly and superiorly, to follow the their deepest part; the extension into the frontal lobe course of the lateral fissure. Less often, the haemorrhage may be paramedially, in the gyrus rectus on one or both is directed medially, in which case it can still be distin- sides, 266 or they may split the frontal lobe more laterally. guished from a ‘hypertensive’ haemorrhage in the basal A clot between the frontal horns, in the corpus callosum ganglia by its lateral extension to the inner table of the or the cavum septi pellucidi is a particularly reliable skull (Fig. 9.18). sign of a ruptured anterior communicating artery Aneurysms arising from the posterior circulation rarely aneurysm. 267 A haematoma confined to the pericallosal give rise to intracerebral extension of the haemorrhage. cistern indicates that the aneurysm lies more distally on However, it must be borne in mind that there will the anterior cerebral artery, usually at the origin of the always be exceptional situations where physicians are pericallosal artery (Fig. 9.15). wrong-footed by aneurysms at unusual locations. If Aneurysms arising from the internal carotid artery are doubt remains in a deteriorating patient, for whom most often at the origin of the posterior communicating rapid evacuation of the haematoma seems indicated, CT artery, and any so intracerebral haematomas from rup- angiography may show – or to some extent exclude – an ture at this site are usually in the medial part of the tem- aneurysm (section 9.4.4). poral lobe (Fig. 9.16). Very large haematomas from such aneurysms, or from aneurysms at the top of the carotid Blood in the subarachnoid cisterns artery, may also involve the frontal lobe (Fig. 9.17). Haematomas from an aneurysm at the origin of the oph- The pattern of haemorrhage if the extravasated blood is thalmic artery tend to involve the frontal lobe on one confined to the subarachnoid cisterns is less specific for side and do not reach the midline, which distinguishes the site of the aneurysm, especially if the haemorrhage is them from intracerebral bleeding from an aneurysm of diffuse rather than local. 268,269 Moreover, after an inter- the anterior communicating artery. val of 5 days, 50% of patients no longer show cisternal .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 478 478 Chapter 9 What caused this subarachnoid haemorrhage? (a) (b) (c) Fig. 9.15 CT scans after rupture of a pericallosal artery. (a) CT slice through the base of the brain with blood in the basal cisterns (arrowheads); (b) higher slice with blood in the vicinity of the pericallosal artery (arrowhead); (c) slice at the level of the body of the lateral ventricles with blood over the corpus callosum (arrowheads); (d) CT angiogram showing the aneurysm (arrow); (e) reconstruction of the CT angiogram delineating the aneurysm from the parent and branching vessels (Also reproduced (e) (d) in colour in the plate section.). Fig. 9.16 Rupture of a posterior communicating artery aneurysm. (a) Brain CT showing a haematoma in (b) the medial part of the right temporal lobe (arrow). (b) CT angiography showing a large aneurysm of the posterior communicating artery at its origin from (a) the internal carotid artery (arrow). .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 479 9.4 Investigations 479 Fig. 9.17 Rupture of an aneurysm at the top of the carotid artery. (a) Brain CT showing a haematoma in the frontal lobe (arrowheads). The aneurysm is visible as a ‘filling defect’ (arrow) within the hyperdense clot of subarachnoid (b) blood. (b) CT angiogram shows the aneurysm (arrow) adjacent to the haematoma (arrowheads). (a) (c) (a) (b) Fig. 9.18 Haematoma from a ruptured aneurysm of the right from a ruptured perforating artery in the basal ganglia. The middle cerebral artery. (a) Brain CT showing the haematoma characteristic feature of aneurysmal bleeding is the extreme extending medially from the sylvian fissure. Note the lateral extension of the haematoma, up to the inner table absence of blood in the suprasellar cistern (arrowhead). (b) The of the skull (arrowhead). (c) CT angiography to show the haematoma extends into the subinsular cortex and putamen, aneurysm (arrow) at the trifurcation of middle cerebral thereby partly mimicking a primary intracerebral haemorrhage artery (arrowhead) that had caused the haemorrhage. blood on CT, 118 and in exceptional cases the abnorm- present but are not visible, due to the presence of a alities have all but disappeared within a single day small amount of blood that is isodense to the brain (Fig. 9.19). The source of SAH can be inferred if the parenchyma. haemorrhage remains confined to, or is most dense in a The most common site for aneurysms is the anterior single cistern, near an arterial branching point site where cerebral artery near the anterior communicating artery aneurysms are known to arise (Fig. 9.3). Sometimes the (Fig. 9.3) and these can be recognized from a region of hyperdensity is local but very subtle (Fig. 9.20), which hyperdensity in the deepest part of the frontal inter- may easily lead to a missed diagnosis of SAH in the hemispheric fissure (Fig. 9.21). Haemorrhage in the middle of the night. It is helpful to specifically look for interhemispheric fissure at higher levels, particularly the slight dilatation of the temporal horns of the lateral supracallosal cistern (Fig. 9.15), suggests an aneurysm at ventricles, and for fissures and sulci that should be the origin of the pericallosal artery, although occasionally .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 480 480 Chapter 9 What caused this subarachnoid haemorrhage? haemorrhages from an aneurysm of the anterior com- municating artery complex may extend this far. 267 An asymmetrical distribution of subarachnoid blood in the region of the suprasellar cisterns suggests an aneurysm of the internal carotid artery, usually at the origin of the posterior communicating artery; there may be some extension into the basal part of the sylvian fissure (Fig. 9.22). If the patient has an arachnoid cyst of the middle fossa, a posterior communicating artery aneurysm may bleed into the cyst. 270 An aneurysm of the middle cerebral artery can be inferred from extravasation of blood at the junction of the basal and lateral parts of the sylvian fissure (Fig. 9.20). The haemorrhage may further extend into the lateral fissure. Basilar artery aneurysms are almost invariably found at the terminal bifurcation of the artery; haemorrhages from this site are often directed forwards and fill the suprasellar, interhemispheric and (basal) sylvian cisterns (Fig. 9.23). The posterior inferior cerebellar artery is located near the base of the skull in the posterior fossa, a notoriously difficult region for CT; haemorrhages in this region can be detected only if the posterior fossa is adequately visualized 66 (Fig. 9.24). It is even more difficult if the aneurysm is on a loop of the posterior inferior cerebellar artery below the foramen magnum. 271 Fig. 9.19 Exceptionally rapid disappearance of subarachnoid blood. Upper row: CT brain scan 4 h after rupture of an Fusiform aneurysms of the posterior circulation often aneurysm of the right posterior communicating artery, at its bleed into the brain parenchyma as well as in the sub- origin from the carotid artery. Abundant extravasation of arachnoid space (Fig. 9.9). blood, throughout the basal cisterns (arrows). Lower row: CT scan 24 h after symptom onset; only a small amount of blood remains (arrows). (From van der Wee et al., 1995 408 ; courtesy of Intraventricular haemorrhage the authors and the Journal of Neurology, Neurosurgery and The cerebral ventricles can fill with blood as a result of Psychiatry.) almost any type of intracranial haemorrhage (section Fig. 9.20 Subtle sign of subarachnoid haemorrhage in a patient with a ruptured aneurysm of the right middle cerebral artery. (a) CT brain scan on the day of admission showing a small amount of blood in the right sylvian fissure (arrowhead). (b) Repeat CT scan 2 days after the initial scan showing (a) (b) disappearance of the blood (arrowhead). .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 481 9.4 Investigations 481 (c) (a) (b) Fig. 9.21 Ruptured aneurysm of the anterior communicating higher slice the blood is most prominent in the anterior artery. (a) CT brain scan slice through the base of the brain interhemispheric fissure (arrow). (c) CT angiogram showing shows diffuse blood in the anterior interhemispheric fissure the anterior communicating artery aneurysm (arrow); note the (arrow); blood is also present in the suprasellar cistern (black distortion of the anterior cerebral arteries (arrowhead) from the arrowheads) and sylvian fissures (white arrowheads). (b) On a extravasated blood in the fissure. Fig. 9.22 Ruptured aneurysm of the posterior communicating artery. (a) CT brain scan showing diffuse subarachnoid haemorrhage most dense in the left half of the suprasellar cistern extending into the basal part of the sylvian fissure (arrowhead). (b) CT angiogram shows the aneurysm of the posterior communicating artery, at its origin from the internal carotid artery (arrow). (a) (b) 9.1.5). Transmission of pressure through the floor of the artery may preferentially fill the fourth ventricle (and fourth ventricle can then cause acute failure of pontine sometimes also the third) from below (Fig. 9.24). and medullary functions, which accounts for 25–50% of early deaths after SAH. 272 Intraventricular haemorrhage Subdural haematomas occurs mostly with aneurysms of the anterior communi- cating artery, which bleed through the lamina terminalis Subdural haematomas develop in 2–3% of all cases of to fill the third and lateral ventricles (Fig. 9.14). 214 Filling aneurysmal rupture, 273–275 more often after rebleeding of the third, but not the lateral ventricles, suggests rup- than after a first episode. 227 They are most often asso- ture of a basilar artery aneurysm, especially if the poste- ciated with subarachnoid blood but can sometimes be rior part of the basal cisterns is filled as well. Similarly, the only manifestation of aneurysmal rupture. 276,277 The rupture of an aneurysm of the posterior inferior cerebellar subdural collection is usually found at the convexity of .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 482 482 Chapter 9 What caused this subarachnoid haemorrhage? (a) (b) Fig. 9.23 Ruptured aneurysm at the top of the basilar artery. (a) CT brain scan shows blood in front of and alongside the pons (arrowhead); (b) higher slice showing blood in the basal part of the suprasellar cistern and in the ambient cistern (white arrowheads), extending into the frontal part of the suprasellar cistern (black arrow), the anterior interhemispheric fissure (white arrow) and the sylvian fissure (black arrowhead); (c) blood in the ambient cistern (white arrowhead) and in both sylvian fissures (black arrowheads); (d) CT angiogram showing the aneurysm at the (c) (d) top of the basilar artery (arrowhead). the brain, seldom in the interhemispheric fissure. because with trauma the haematoma is more often Subdural collections near the skull base are not well visu- unilateral, hyperdense and crescentic in shape. 273 alized on axial CT images. The ruptured aneurysm can be at any of the common sites, sometimes far removed from Non-aneurysmal (perimesencephalic) patterns of the subdural collection. 278 The most plausible explana- haemorrhage tion for the rupture through the arachnoid membrane is that the dome of the aneurysmal sac has become adher- Fifteen per cent of patients with SAH do not have an ent to it, usually as a result of a previous rupture, recog- aneurysm on angiographic studies, and two-thirds of nized or unrecognized. 279 A more indirect pathogenesis these show basal haemorrhages of a distinct kind: mainly is also conceivable, through traction on veins traversing or only in the perimesencephalic cisterns, a pattern of the subdural space, but patients with subdural hae- haemorrhage that is seen only rarely in patients with matomas are no older than those without. 275 The dis- a demonstrable aneurysm (Fig. 9.25) (section 9.1.2). tinction from subdural haematomas of traumatic origin A problem is that about one out of 20 patients with a can often be made on the basis of the associated exten- perimesencephalic type of haemorrhage harbours an sive haemorrhage in the subarachnoid space, and also aneurysm after all, located on the posterior circulation .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 483 9.4 Investigations 483 (a) (b) Fig. 9.24 Ruptured aneurysm of the posterior inferior cerebellar artery. (a) Brain CT scan showing diffuse subarachnoid blood in the basal cisterns (black arrowheads) and blood in the fourth ventricle (white arrowhead); note also the enlarged lateral and third ventricles. (b) A higher slice showing subarachnoid blood in both ambient cisterns (black arrowheads) and lateral (white arrows) and third ventricle (white arrowhead). (c) CT angiogram showing the aneurysm (white arrow) at the origin of the posterior inferior cerebellar artery (black arrow) from the vertebral artery (black (d) arrowheads). (d) Reconstruction of the CT angiogram showing better the relationship between the aneurysm (arrow) and parent and branching vessel. (Also reproduced in colour in the plate section.) (c) (Fig. 9.26). 57,64,68,280 An estimate of the balance of risks experience with SAH patients and CT angiography. 284 leads to the conclusion that withholding surgical or In contrast, repeating a negative angiographic study is endovascular treatment in approximately 5% of patients mandatory with aneurysmal patterns of haemorrhage with a perimesencephalic pattern of bleeding but an on the CT scan (section 9.4.6). undetected basilar artery aneurysm is more unfavourable than the complications of ‘unnecessary’ angiographic CT angiography (rather than catheter angiography) imaging in the remaining 95%. However, there is no is still required in patients with a perimesencephalic need to repeat a normal CT angiogram in a patient with a perimesencephalic pattern of haemorrhage, 281 or subarachnoid pattern of subarachnoid haemorrhage, even though the chance of finding an aneurysm is to proceed to catheter angiography after a normal CT angiogram. 282 A decision analysis indicates that a CT extremely small. However, unlike with aneurysmal patterns of bleeding, there is no need to repeat the angiogram is sufficient to exclude a posterior fossa aneur- ysm, 283 provided the local radiological team has sufficient angiogram after a negative initial angiogram. .. ..

9781405127660_4_009.qxd 10/13/07 11:03 AM Page 489 References 489 (c) (b) (a) Fig. 9.29 A patient with a subarachnoid haemorrhage from a interhemispheric fissure (arrowhead); (b) MR angiogram gives very small aneurysm on the proximal part of the middle some suggestion of an aneurysm (circle); (c) Catheter three- cerebral artery. (a) CT brain scan showing diffuse blood in the dimensional angiogram confirms a very small aneurysm basal part of the right sylvian fissure (arrow) and in the anterior (arrow) which was clipped by the neurosurgeon. was 58 aneurysms in 386 patients, or 15%. 212,213,328–338 makes it difficult to make the correct diagnosis. 340 Not If it is taken into account that patients with perimesen- only negative angiography of the cerebral circulation, cephalic non-aneurysmal haemorrhage were often not but also clinical clues such as sudden backache, should excluded from these series, the yield of repeat angio- suggest the need for spinal angiography. However, this grams in patients with a diffuse or anteriorly located procedure is not always diagnostic. 341,342 Also, angiogra- pattern of haemorrhage on CT scanning must be even phy is impractical without localizing signs or symptoms higher. If a second angiogram again fails to demonstrate because so many intercostal arteries have to be catheter- the suspected aneurysm, an aneurysm may still be demon- ized, while the procedure itself carries a risk of some 5% strated by exploratory craniotomy – or rebleeding. 69,339 of a transient or even persisting neurological deficit. 343,344 If a first, as well as a second, angiogram is completely In practice, if a vascular abnormality of the spinal cord is negative (not only both internal carotid arteries but also suspected, MRI, particularly in the sagittal plane, is the both vertebral arteries having been injected) despite first-line investigation for detecting the characteristic an aneurysmal pattern of haemorrhage on the CT scan, serpiginous structures, usually on the dorsal aspect of the the search for a vascular lesion should still be doggedly cord, indicating a dural arteriovenous fistula (section pursued. In a unique, consecutive series of 14 patients 9.1.4), or at least for detecting an associated extradural subjected to a third angiogram, a single aneurysm was or subdural haematoma. 345,346 There are no systematic found. 331 A reasonable approach is to perform a third studies about the usefulness of spinal angiography after a investigation some 3 months after SAH onset, the choice negative MR scan of the spinal cord. (repeat catheter angiography, CT angiography, MRI/ MRA) depending on the patient’s clinical condition, age and personal wishes. CT angiography or MR angio- graphy with three-dimensional projection will in due References time probably replace catheter angiography in detecting ‘occult’ aneurysms. 1 Hop JW, Rinkel GJE, Algra A, van Gijn J. Case-fatality rates 9.4.7 Spinal imaging and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke 1997; 28(3):660–4. In the case of subarachnoid haemorrhage from a spinal 2 De Rooij NK, Linn FHH, van der Plas JAP, Algra A, arteriovenous malformation, brain CT may show blood Rinkel GJE. Incidence of Subarachnoid Haemorrhage: A throughout the basal cisterns and ventricles, which systematic review with emphasis on region, age, gender .. ..

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