Critical review of the evidence for each question
8. Management of complications How to manage systemic complications
Neurologists and neurosurgeons are regularly confronted by non-neurological complications in patients with aneurysmal SAH. Life-threatening complications occurred in 40% of 451 consecutive patients enrolled in a drug trial [126], and in another study a similar proportion of medical complications contributed to fatal outcomes [127]. Hyponatraemia is the most common of these but several other systemic disorders may cause secondary deterioration. Clinical detection of these metabolic derangements requires a high index of suspicion.
Hyponatraemia
Hyponatraemia, with or without intravascular volume change, is the most common electrolyte disturbance follow-ing aneurysmal rupture. The frequency depends on the cut off point that is chosen; if defined as a sodium level of 134 mmol or less on at least two consecutive days, it occurs Chapter 14: Aneurysmal subarachnoid haemorrhage 135
in about one-third of patients [91]. It develops most com-monly between the 2nd and 10th day [128].
Clinical manifestations of hyponatraemia usually do not occur until the plasma sodium is less than 125 mmol/L, but irritability, restlessness and confusion can result from a rapid decline of sodium, particularly if the downward trend con-tinues over a few days. Sodium levels below 100 mmol/L almost always give rise to seizures and, rarely, ventricular tachycardia or fibrillation [129]. But in patients with SAH the most dreaded complication of hyponatraemia is the pre-cipitation of delayed ischaemia, through associated hypo-volaemia and poor outcome in general [130].
In general, the causes of hyponatraemia vary according to the patient’s volume status. In most, but not all cases, the total body sodium has remained constant but the water con-tent of the extracellular volume is at fault; therefore hypona-traemia can be best classified according to the extracellular volume status. After the syndrome of inappropriate secretion of antidiuretic hormone (SIADH) had been initially described in the 1950s [131], hyponatraemia in SAH has often been incorrectly attributed to this condition, in which dilutional hyponatraemia ensues. In contrast, hyponatraemia after SAH results from excessive natriuresis, or cerebral salt wast-ing [128,132]. Predisposwast-ing factors for the development of hyponatraemia are hydrocephalus, particularly enlargement of the third ventricle [133], and ruptured aneurysms of the anterior communicating artery [134]. Mechanical pressure on the hypothalamus can perhaps disturb sodium and water homeostasis.
Correction of hyponatraemia in SAH is actually a problem of correcting volume depletion. Acute symptomatic hypona-traemia is rare and requires urgent treatment with hypertonic saline (1.8% or even 3%). On the other hand, over-rapid infusion of sodium may precipitate myelinolysis in the pons and in the white matter of the hemispheres [135]. If possible, correction should not be faster than 8 mmol/L/day [136,137].
A mild degree of hyponatraemia (125–134 mmol/L) is usually well tolerated, self-limiting and need not be treated in itself.
Hyponatraemia in patients with evidence of a negative fluid balance or excessive natriuresis is corrected with saline (0.9%;
sodium concentration 150 mmol/L).
Disorders of heart rhythm
Aneurysmal rupture is commonly associated with cardiac arrhythmias and electrocardiographic (ECG) abnormalities.
This is one of the reasons why patients with SAH are some-times initially misdiagnosed as acute myocardial infarction and admitted to coronary care units. Left ventricular dys-function may occur [138], even cardiogenic shock, usually in combination with pulmonary oedema.
Generally, severe ventricular arrhythmias are of short dur-ation. Beta-blockade has been proposed as preventive treat-ment aimed at lowering the sympathetic tone. In patients with SAH, routine administration of beta-blockers is not
warranted until there is evidence of improved overall out-come; the net benefits may be disappointing because beta-blockers also lower blood pressure.
Neurogenic pulmonary oedema
Pulmonary oedema occurs to some degree in approximately one-third of patients with SAH [139,140], but the fulminant variety is much more rare (2% in the largest series to date) [141]. The onset is usually rapid, within hours. What trig-gers pulmonary oedema is unclear.
The typical clinical picture consists of unexpected dyspnoea, cyanosis and production of pink and frothy sputum. Many patients are pale, sweat excessively and are hypertensive.
A chest X-ray usually demonstrates impressive pulmonary oedema which may disappear in a matter of hours following positive end-expiratory pressure ventilation. A problem is that liberal administration of fluids is beneficial for brain perfusion but may delay recovery of pulmonary oedema and hence impair brain oxygenation, and that positive end-expiratory pressure ventilation increases intracranial pressure.
In case of associated left ventricular failure, clinically mani-fested by sudden hypotension following initially elevated blood pressures, transient lactic acidosis and mild elevation of the creatine kinase MB fraction [142,143], inotropic agents are indicated (dobutamine, 5–15g/kg/min) [144].
Conclusion
We think we have distinguished in this chapter, explicitly or at least implicitly, between (a) solid evidence, from several well-performed clinical trials; (b) less reliable evidence, from single trials, case series or observational studies; and (c) pathophysiological reasoning, with all its fallacies. In every-day practice a multitude of management decisions must still be taken without good evidence. There are several reasons for this: there is no trial at all; trial results may be equivocal;
patients may be different from those enrolled in trials; new procedures require practice, or a trial may not be feasible.
‘Logical reasoning’ may be maligned and reviled in the present era but paradoxically it is still indispensable – not only to fill the gaps in empirical knowledge but also to inter-pret existing evidence and to plan new trials. In fact, the generation of new knowledge is a continuous, cyclical process in which newly gained insights in pathophysiology give rise to new therapeutic experiments, the results of which generate fresh hypotheses, and so on. Compassion, curiosity and doubt are the essential forces that keep the cycle moving [145].
References
1 Rinkel GJE, Djibuti M, Algra A, van Gijn J. Prevalence and risk of rupture of intracranial aneurysms – a systematic review. Stroke 1998; 29: 251–6.
136 Part 3: Neurological diseases
2 Linn FHH, Rinkel GJE, Algra A, van Gijn J. Incidence of sub-arachnoid hemorrhage – role of region, year, and rate of com-puted tomography: a meta-analysis. Stroke 1996; 27: 625–9.
3 Ruigrok YM, Buskens E, Rinkel GJE. Attributable risk of com-mon and rare determinants of subarachnoid hemorrhage. Stroke 2001; 32: 1173–5.
4 Pleizier CM, Ruigrok YM, Rinkel GJE. Relation between age and number of aneurysms in patients with subarachnoid haemor-rhage. Cerebrovasc. Dis. 2002; 14: 51–3.
5 Hop JW, Rinkel GJE, Algra A, van Gijn J. Case-fatality rates and functional outcome after subarachnoid hemorrhage – a system-atic review. Stroke 1997; 28: 660–4.
6 Huang J, Van Gelder JM. The probability of sudden death from rupture of intracranial aneurysms: a meta-analysis. Neurosurgery 2002; 51: 1101–5.
7. Hackett ML, Anderson CS, for the ACROSS Group. Health out-comes 1 year after subarachnoid hemorrhage – an international population-based study. Neurology 2000; 55: 658–62.
8 Roos YBWEM, de Haan RJ, Beenen LFM, Groen RJM, Albrecht KW, Vermeulen M. Complications and outcome in patients with aneurysmal subarachnoid haemorrhage: a prospective hospital based cohort study in the Netherlands. J. Neurol. Neurosurg.
Psychiatr. 2000; 68: 337–41.
9 Bardach NS, Zhao SJ, Gress DR, Lawton MT, Johnston SC.
Association between subarachnoid hemorrhage outcomes and number of cases treated at California hospitals. Stroke 2002; 33:
1851–6.
10 van Gijn J, van Dongen KJ. The time course of aneurysmal haemorrhage on computed tomograms. Neuroradiology 1982; 23:
153–6.
11 Hauerberg J, Eskesen V, Rosenorn J. The prognostic significance of intracerebral haematoma as shown on CT scanning after aneurysmal subarachnoid haemorrhage. Br. J. Neurosurg. 1994;
8: 333–9.
12 Heiskanen O, Poranen A, Kuurne T, Valtonen S, Kaste M. Acute surgery for intracerebral haematomas caused by rupture of an intracranial arterial aneurysm. A prospective randomized study.
Acta Neurochir. (Wien) 1988; 90: 81–3.
13 Niemann DB, Wills AD, Maartens NF, Kerr RS, Byrne JV, Molyneux AJ. Treatment of intracerebral hematomas caused by aneurysm rupture: coil placement followed by clot evacuation.
J. Neurosurg. 2003; 99: 843–7.
14 Smith ER, Carter BS, Ogilvy CS. Proposed use of prophylactic decompressive craniectomy in poor-grade aneurysmal sub-arachnoid hemorrhage patients presenting with associated large sylvian hematomas. Neurosurgery 2002; 51: 117–24.
15 Gelabert-Gonzalez M, Iglesias-Pais M, Fernandez-Villa J. Acute subdural haematoma due to ruptured intracranial aneurysms.
Neurosurg. Rev. 2004; 27: 259–62.
16 Inamasu J, Saito R, Nakamura Y, et al. Acute subdural hematoma caused by ruptured cerebral aneurysms: diagnostic and therapeutic pitfalls. Resuscitation 2002; 52: 71–6.
17 O’Sullivan MG, Whyman M, Steers JW, Whittle IR, Miller JD.
Acute subdural haematoma secondary to ruptured intracranial
aneurysm: diagnosis and management. Br. J. Neurosurg. 1994; 8:
439–45.
18 Sasaki T, Sato M, Oinuma M, et al. Management of poor-grade patients with aneurysmal subarachnoid hemorrhage in the acute stage: importance of close monitoring for neurological grade changes. Surg. Neurol. 2004; 62: 531–5.
19 van Gijn J, Hijdra A, Wijdicks EFM, Vermeulen M, van Crevel H.
Acute hydrocephalus after aneurysmal subarachnoid hemor-rhage. J. Neurosurg. 1985; 63: 355–62.
20 Rinkel GJE, Wijdicks EFM, Ramos LMP, van Gijn J. Progression of acute hydrocephalus in subarachnoid haemorrhage: a case report documented by serial CT scanning. J. Neurol. Neurosurg.
Psychiatr. 1990; 53: 354–5.
21 Hasan D, Lindsay KW, Vermeulen M. Treatment of acute hydro-cephalus after subarachnoid hemorrhage with serial lumbar puncture. Stroke 1991; 22: 190–4.
22 Suzuki M, Otawara Y, Doi M, Ogasawara K, Ogawa A.
Neurological grades of patients with poor-grade subarachnoid hemorrhage improve after short-term pretreatment. Neurosurgery 2000; 47: 1098–104.
23 Roos YBWEM, Hasan D, Vermeulen M. Outcome in patients with large intraventricular haemorrhages: a volumetric study. J.
Neurol. Neurosurg. Psychiatr. 1995; 58: 622–4.
24 Nieuwkamp DJ, de Gans K, Rinkel GJE, Algra A. Treatment and outcome of severe intraventricular extension in patients with subarachnoid or intracerebral hemorrhage: a systematic review of the literature. J. Neurol. 2000; 247: 117–21.
25 Naff NJ, Carhuapoma JR, Williams MA, et al. Treatment of intraventricular hemorrhage with urokinase – effects on 30-day survival. Stroke 2000; 31: 841–7.
26 Shimoda M, Oda S, Shibata M, Tominaga J, Kittaka M, Tsugane R.
Results of early surgical evacuation of packed intraventricular hemorrhage from aneurysm rupture in patients with poor-grade subarachnoid hemorrhage. J. Neurosurg. 1999; 91: 408–14.
27 Lagares A, Putman CM, Ogilvy CS. Posterior fossa decompression and clot evacuation for fourth ventricle hemorrhage after aneurysmal rupture: case report. Neurosurgery 2001; 49: 208–11.
28 Wijdicks EFM, Vermeulen M, Murray GD, Hijdra A, van Gijn J.
The effects of treating hypertension following aneurysmal sub-arachnoid hemorrhage. Clin. Neurol. Neurosurg. 1990; 92: 111–17.
29 Hasan D, Vermeulen M, Wijdicks EFM, Hijdra A, van Gijn J.
Effect of fluid intake and antihypertensive treatment on cerebral ischemia after subarachnoid hemorrhage. Stroke 1989; 20:
1511–15.
30 Wijdicks EFM, Vermeulen M, Hijdra A, van Gijn J. Hyponatremia and cerebral infarction in patients with ruptured intracranial aneurysms: is fluid restriction harmful? Ann. Neurol. 1985; 17:
137–40.
31 Rosenwasser RH, Delgado TE, Buchheit WA, Freed MH. Control of hypertension and prophylaxis against vasospasm in cases of subarachnoid hemorrhage: a preliminary report. Neurosurgery 1983; 12: 658–61.
32 Egge A, Waterloo K, Sjoholm H, Solberg T, Ingebrigtsen T, Romner B. Prophylactic hyperdynamic postoperative fluid ther-apy after aneurysmal subarachnoid hemorrhage: a clinical, Chapter 14: Aneurysmal subarachnoid haemorrhage 137
prospective, randomized, controlled study. Neurosurgery 2001;
49: 593–605.
33 Takagi K, Tsuchiya Y, Okinaga K, Hirata M, Nakagomi T, Tamura A. Natural hypothermia immediately after transient global cere-bral ischemia induced by spontaneous subarachnoid hemor-rhage. J. Neurosurg. 2003; 98: 50–6.
34 Rousseaux P, Scherpereel R, Bernard MH, Graftieaux JP, Guyot JF.
Fever and cerebral vasospasm in intracranial aneurysms. Surg.
Neurol. 1980; 14: 459–65.
35 Oliveira-Filho J, Ezzeddine MA, Segal AZ, et al. Fever in sub-arachnoid hemorrhage: relationship to vasospasm and outcome.
Neurology 2001; 56: 1299–304.
36 Vermeulen M, Lindsay KW, Murray GD, et al. Antifibrinolytic treatment in subarachnoid hemorrhage. N. Engl. J. Med. 1984;
311: 432–7.
37 Siironen J, Juvela S, Varis J, et al. No effect of enoxaparin on outcome of aneurysmal subarachnoid hemorrhage: a random-ized, double-blind, placebo-controlled clinical trial. J. Neurosurg.
2003; 99: 953–9.
38 Amaragiri SV, Lees TA. Elastic compression stockings for preven-tion of deep vein thrombosis. Cochrane Database Sys. Rev. 2000:
CD001484.
39 Guglielmi G, Vinuela F, Duckwiler G, et al. Endovascular treat-ment of posterior circulation aneurysms by electrothrombosis using electrically detachable coils. J. Neurosurg. 1992; 77: 515–24.
40 Brilstra EH, Rinkel GJE, van der Graaf Y, van Rooij WJJ, Algra A.
Treatment of intracranial aneurysms by embolization with coils – a systematic review. Stroke 1999; 30: 470–6.
41 van der Schaaf I, Algra A, Wermer M, et al. Endovascular coiling versus neurosurgical clipping for patients with aneurysmal sub-arachnoid haemorrhage. Cochrane Database Sys. Rev. 2005; 4:
CD003085.
42 Lozier AP, Connolly Jr ES, Lavine SD, Solomon RA. Guglielmi detachable coil embolization of posterior circulation aneurysms – a systematic review of the literature. Stroke 2002; 33: 2509–18.
43 Molyneux A, Kerr R, Stratton I, et al. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endo-vascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 2002; 360: 1267–74.
44 Wiebers DO, Whisnant JP, Huston III J, et al. Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 2003; 362:
103–10.
45 Molyneux AJ, Kerr RS, Yu LM, et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovas-cular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet 2005; 366: 809–17.
46 Tsutsumi K, Ueki K, Usui M, Kwak S, Kirino T. Risk of recurrent subarachnoid hemorrhage after complete obliteration of cere-bral aneurysms. Stroke 1998; 29: 2511–13.
47 Wermer MJ, Greebe P, Algra A, Rinkel GJ. Incidence of recur-rent subarachnoid hemorrhage after clipping for ruptured intracranial aneurysms. Stroke 2005; 36: 2394–9.
48 Majoie CB, Sprengers ME, Van Rooij WJ, et al. MR angiography at 3T versus digital subtraction angiography in the follow-up of intracranial aneurysms treated with detachable coils. AJNR Am.
J. Neuroradiol. 2005; 26: 1349–56.
49 Slob MJ, Sluzewski M, Van Rooij WJ, Roks G, Rinkel GJE.
Additional coiling of previously coiled cerebral aneurysms:
clinical and angiographic results. AJNR Am. J. Neuroradiol. 2004;
25: 1373–6.
50 Zhang YJ, Barrow DL, Cawley CM, Dion JE. Neurosurgical man-agement of intracranial aneurysms previously treated with endovascular therapy. Neurosurgery 2003; 52: 283–93.
51 McKissock W, Richardson A, Walsh L. ‘Posterior-communicating aneurysms’. A controlled trial of conservative and surgical treat-ment of ruptured aneurysms of the internal carotid artery at or near the point of origin of the posterior communicating artery.
Lancet 1960; i: 1203–6.
52 McKissock W, Richardson A, Walsh L. Anterior communicating aneurysms. A trial of conservative and surgical treatment. Lancet 1965; i: 873–6.
53 Brilstra EH, Algra A, Rinkel GJE, Tulleken CAF, van Gijn J.
Effectiveness of neurosurgical clip application in patients with aneurysmal subarachnoid hemorrhage. J. Neurosurg. 2002; 97:
1036–41.
54 Laidlaw JD, Siu KH. Ultra-early surgery for aneurysmal sub-arachnoid hemorrhage: outcomes for a consecutive series of 391 patients not selected by grade or age. J. Neurosurg. 2002; 97: 250–8.
55 Öhman J, Heiskanen O. Timing of operation for ruptured supra-tentorial aneurysms: a prospective randomized study.
J. Neurosurg. 1989; 70: 55–60.
56 Whitfield PC, Kirkpatrick PJ. Timing of surgery for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst. Rev. 2001;
CD001697.
57 de Gans K, Nieuwkamp DJ, Rinkel GJE, Algra A. Timing of aneurysm surgery in subarachnoid hemorrhage: a systematic review of the literature. Neurosurgery 2002; 50: 336–40.
58 Ross N, Hutchinson PJ, Seeley H, Kirkpatrick PJ. Timing of sur-gery for supratentorial aneurysmal subarachnoid haemorrhage:
report of a prospective study. J. Neurol. Neurosurg. Psychiatr. 2002;
72: 480–4.
59 Nieuwkamp DJ, de GK, Algra A, et al. Timing of aneurysm sur-gery in subarachnoid haemorrhage – an observational study in The Netherlands. Acta Neurochir. (Wien) 2005; 147: 815–21.
60 Wermer MJ, Buskens E, van der Schaaf I, Bossuyt PM, Rinkel GJE. Yield of screening for new aneurysms after treatment for subarachnoid hemorrhage. Neurology 2004; 62: 369–75.
61 Fodstad H, Pilbrant A, Schannong M, Stromberg S.
Determination of tranexamic acid (AMCA) and fibrin/fibrino-gen degradation products in cerebrospinal fluid after aneurys-mal subarachnoid haemorrhage. Acta Neurochir. (Wien) 1981; 58:
1–13.
62 Roos YBWEM, for the STAR Study Group. Antifibrinolytic treat-ment in subarachnoid hemorrhage – a randomized placebo-con-trolled trial. Neurology 2000; 54: 77–82.
63 Hillman J, Fridriksson S, Nilsson O, Yu Z, Saveland H, Jakobsson KE. Immediate administration of tranexamic acid 138 Part 3: Neurological diseases
and reduced incidence of early rebleeding after aneurysmal sub-arachnoid hemorrhage: a prospective randomized study.
J. Neurosurg. 2002; 97: 771–8.
64 Pickard JD, Kirkpatrick PJ, Melsen T, et al. Potential role of NovoSeven(R) in the prevention of rebleeding following aneurysmal subarachnoid haemorrhage. Blood Coagul. Fibrinol.
2000; 11: S117–20.
65 Rinkel GJE, Feigin VL, Algra A, Van den Bergh WM, Vermeulen M, van GJ. Calcium antagonists for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst. Rev. 2005; CD000277.
66 Pickard JD, Murray GD, Illingworth R, et al. Effect of oral nimodipine on cerebral infarction and outcome after subarach-noid haemorrhage: British aneurysm nimodipine trial. BMJ 1989; 298: 636–42.
67 Philippon J, Grob R, Dagreou F, Guggiari M, Rivierez M, Viars P.
Prevention of vasospasm in subarachnoid haemorrhage. A con-trolled study with nimodipine. Acta Neurochir. (Wien) 1986; 82:
110–4.
68 Petruk KC, West M, Mohr G, et al. Nimodipine treatment in poor-grade aneurysm patients. Results of a multicenter double-blind placebo-controlled trial. J. Neurosurg. 1988; 68: 505–17.
69 Ahmed N, Nasman P, Wahlgren NG. Effect of intravenous nimodipine on blood pressure and outcome after acute stroke.
Stroke 2000; 31: 1250–5.
70 Van den Bergh WM, Algra A, Van der Sprenkel JWB, Tulleken CAF, Rinkel GJE. Hypomagnesemia after aneurysmal subarach-noid hemorrhage. Neurosurgery 2003; 52: 276–81.
71 Van den Bergh WM, Zuur JK, Kamerling NA, et al. Role of mag-nesium in the reduction of ischemic depolarization and lesion volume after experimental subarachnoid hemorrhage.
J. Neurosurg. 2002; 97: 416–22.
72 Veyna RS, Seyfried D, Burke DG, et al. Magnesium sulfate ther-apy after aneurysmal subarachnoid hemorrhage. J. Neurosurg.
2002; 96: 510–4.
73 Van den Bergh WM, on behalf of the MASH study group.
Magnesium sulfate in aneurysmal subarachnoid hemorrhage. A randomized controlled trial. Stroke 2005; 36: 1011–15.
74 Juvela S, Kaste M, Hillbom M. Platelet thromboxane release after subarachnoid hemorrhage and surgery. Stroke 1990; 21: 566–71.
75 Ohkuma H, Suzuki S, Kimura M, Sobata E. Role of platelet function in symptomatic cerebral vasospasm following aneurys-mal subarachnoid hemorrhage. Stroke 1991; 22: 854–9.
76 Dorhout Mees SM, Rinkel GJE, Hop JW, Algra A, van Gijn J.
Antiplatelet therapy in aneurysmal subarachnoid hemorrhage: a systematic review. Stroke 2003; 34: 2285–9.
77 Robinson JG, Smith B, Maheshwari N, Schrott H. Pleiotropic effects of statins: benefit beyond cholesterol reduction? A meta-regression analysis. J. Am. Coll. Cardiol. 2005; 46: 1855–62.
78 Lynch JR, Wang H, McGirt MJ, et al. Simvastatin reduces vasospasm after aneurysmal subarachnoid hemorrhage: results of a pilot randomized clinical trial. Stroke 2005; 36: 2024–6.
79 Tseng MY, Czosnyka M, Richards H, Pickard JD, Kirkpatrick PJ.
Effects of acute treatment with pravastatin on cerebral vasospasm, autoregulation, and delayed ischemic deficits after
aneurysmal subarachnoid hemorrhage: a phase II randomized placebo-controlled trial. Stroke 2005; 36: 1627–32.
80 Singhal AB, Topcuoglu MA, Dorer DJ, Ogilvy CS, Carter BS, Koroshetz WJ. SSRI and statin use increases the risk for vasospasm after subarachnoid hemorrhage. Neurology 2005; 64:
1008–13.
81 Kassell NF, Haley Jr EC, Apperson-Hansen C, et al. Randomized, double-blind, vehicle-controlled trial of tirilazad mesylate in patients with aneurysmal subarachnoid hemorrhage: a coopera-tive study in Europe, Australia, and New Zealand. J. Neurosurg.
1996; 84: 221–8.
82 Haley Jr EC, Kassell NF, Apperson-Hansen C, Maile MH, Alves WM. A randomized, double-blind, vehicle-controlled trial of tiri-lazad mesylate in patients with aneurysmal subarachnoid hem-orrhage: a cooperative study in North America. J. Neurosurg.
1997; 86: 467–74.
83 Lanzino G, Kassell NF, Dorsch NWC, et al. Double-blind, ran-domized, vehicle-controlled study of high-dose tirilazad mesy-late in women with aneurysmal subarachnoid hemorrhage. Part I. A cooperative study in Europe, Australia, New Zealand, and South Africa. J. Neurosurg. 1999; 90: 1011–17.
84 Lanzino G, Kassell NF. Double-blind, randomized, vehicle-controlled study of high-dose tirilazad mesylate in women with aneurysmal subarachnoid hemorrhage. Part II. A cooperative study in North America. J. Neurosurg. 1999; 90: 1018–24.
85 Asano T, Takakura K, Sano K, et al. Effects of a hydroxyl radical scavenger on delayed ischemic neurological deficits following aneurysmal subarachnoid hemorrhage: results of a multicenter, placebo-controlled double-blind trial. J. Neurosurg. 1996; 84:
792–803.
86 Saito I, Asano T, Sano K, et al. Neuroprotective effect of an antioxi-dant, ebselen, in patients with delayed neurological deficits after aneurysmal subarachnoid hemorrhage. Neurosurgery 1998; 42:
269–77.
87 Saito I, Asano T, Ochiai C, Takakura K, Tamura A, Sano K. A double-blind clinical evaluation of the effect of Nizofenone (Y-9179) on delayed ischemic neurological deficits following aneurysmal rupture. Neurol. Res. 1983; 5: 29–47.
88 Shaw MDM, Vermeulen M, Murray GD, Pickard JD, Bell BA, Teasdale GM. Efficacy and safety of the endothelin A/B receptor antagonist TAK-044 in treating subarachnoid hemorrhage: a report by the Steering Committee on behalf of the UK/
Netherlands/Eire TAK-044 Subarachnoid Haemorrhage Study Group. J. Neurosurg. 2000; 93: 992–7.
89 Rinkel GJE, Feigin VL, Algra A, van Gijn J. Circulatory volume expansion therapy for aneurysmal subarachnoid haemorrhage.
Cochrane Database Syst. Rev. 2004; CD000483.
90 Wijdicks EFM, Vermeulen M, van Brummelen P, van Gijn J. The effect of fludrocortisone acetate on plasma volume and natriure-sis in patients with aneurysmal subarachnoid hemorrhage. Clin.
Neurol. Neurosurg. 1988; 90: 209–14.
91 Hasan D, Lindsay KW, Wijdicks EFM, et al. Effect of fludrocorti-sone acetate in patients with subarachnoid hemorrhage. Stroke 1989; 20: 1156–61.
Chapter 14: Aneurysmal subarachnoid haemorrhage 139
92 Mori T, Katayama Y, Kawamata T, Hirayama T. Improved effi-ciency of hypervolemic therapy with inhibition of natriuresis by fludrocortisone in patients with aneurysmal subarachnoid hemorrhage. J. Neurosurg. 1999; 91: 947–52.
93 Moro N, Katayama Y, Kojima J, Mori T, Kawamata T.
Prophylactic management of excessive natriuresis with hydro-cortisone for efficient hypervolemic therapy after subarach-noid hemorrhage. Stroke 2003; 34: 2807–11.
94 Klimo Jr P, Kestle JR, MacDonald JD, Schmidt RH. Marked reduction of cerebral vasospasm with lumbar drainage of cere-brospinal fluid after subarachnoid hemorrhage. J. Neurosurg.
2004; 100: 215–24.
95 Amin-Hanjani S, Ogilvy CS, Barker FG. Does intracisternal thrombolysis prevent vasospasm after aneurysmal subarach-noid hemorrhage? A meta-analysis. Neurosurgery 2004; 54:
326–34.
96 Hamada J, Kai Y, Morioka M, et al. Effect on cerebral vasospasm of coil embolization followed by microcatheter intrathecal urokinase infusion into the cisterna magna: a prospective ran-domized study. Stroke 2003; 34: 2549–54.
97 Hijdra A, Vermeulen M, van Gijn J, van Crevel H. Rerupture of intracranial aneurysms: a clinicoanatomic study. J. Neurosurg.
1987; 67: 29–33.
98 Hijdra A, Braakman R, van Gijn J, Vermeulen M, van Crevel H.
Aneurysmal subarachnoid hemorrhage. Complications and outcome in a hospital population. Stroke 1987; 18: 1061–7.
99 Inagawa T, Kamiya K, Ogasawara H, Yano T. Rebleeding of ruptured intracranial aneurysms in the acute stage. Surg.
Neurol. 1987; 28: 93–9.
100 Kassell NF, Peerless SJ, Durward QJ, Beck DW, Drake CG, Adams Jr HP Treatment of ischemic deficits from vasospasm with intravascular volume expansion and induced arterial hypertension. Neurosurgery 1982; 11: 337–43.
101 Qureshi AI, Suarez JI, Bhardwaj A, Yahia AM, Tamargo RJ, Ulatowski JA. Early predictors of outcome in patients receiving hypervolemic and hypertensive therapy for symptomatic vasospasm after subarachnoid hemorrhage. Crit. Care. Med.
2000; 28: 824–9.
102 Sen J, Belli A, Albon H, Morgan L, Petzold A, Kitchen N.
Triple-H therapy in the management of aneurysmal subarach-noid haemorrhage. Lancet Neurol. 2003; 2: 614–21.
103 Amin-Hanjani S, Schwartz RB, Sathi S, Stieg PE. Hypertensive encephalopathy as a complication of hyperdynamic therapy for vasospasm: report of two cases. Neurosurgery 1999; 44: 1113–16.
104 Rosenwasser RH, Jallo JI, Getch CC, Liebman KE. Complica-tions of Swan-Ganz catheterization for hemodynamic monitor-ing in patients with subarachnoid hemorrhage. Neurosurgery 1995; 37: 872–5.
105 Harvey S, Harrison DA, Singer M, et al. Assessment of the clin-ical effectiveness of pulmonary artery catheters in manage-ment of patients in intensive care (PAC-Man): a randomised controlled trial. Lancet 2005; 366: 472–7.
106 Shah MR, Hasselblad V, Stevenson LW, et al. Impact of the pul-monary artery catheter in critically ill patients: meta-analysis of randomized clinical trials. JAMA 2005; 294: 1664–70.
107 Hoh BL, Ogilvy CS. Endovascular treatment of cerebral vasospasm: transluminal balloon angioplasty, intra-arterial papaverine, and intra-arterial nicardipine. Neurosurg. Clin. N.
Am. 2005; 16: 501–16.
108 Rabinstein AA, Friedman JA, Nichols DA, et al. Predictors of outcome after endovascular treatment of cerebral vasospasm.
AJNR Am. J. Neuroradiol. 2004; 25: 1778–82.
109 Polin RS, Coenen VA, Hansen CA, et al. Efficacy of translumi-nal angioplasty for the management of symptomatic cerebral vasospasm following aneurysmal subarachnoid hemorrhage. J.
Neurosurg. 2000; 92: 284–90.
110 Fandino J, Kaku Y, Schuknecht B, Valavanis A, Yonekawa Y.
Improvement of cerebral oxygenation patterns and metabolic validation of super-selective intraarterial infusion of papaver-ine for the treatment of cerebral vasospasm. J. Neurosurg. 1998;
89: 93–100.
111 Polin RS, Hansen CA, German P, Chadduck JB, Kassell NF.
Intra-arterially administered papaverine for the treatment of symptomatic cerebral vasospasm. Neurosurgery 1998; 42:
1256–64.
112 Smith WS, Dowd CF, Johnston SC, et al. Neurotoxicity of intra-arterial papaverine preserved with chlorobutanol used for the treatment of cerebral vasospasm after aneurysmal sub-arachnoid hemorrhage. Stroke 2004; 35: 2518–22.
113 Arakawa Y, Kikuta K, Hojo M, Goto Y, Ishii A, Yamagata S.
Milrinone for the treatment of cerebral vasospasm after sub-arachnoid hemorrhage: report of seven cases. Neurosurgery 2001; 48: 723–8.
114 Feng L, Fitzsimmons BF, Young WL, et al. Intraarterially administered verapamil as adjunct therapy for cerebral vasospasm: safety and 2-year experience. Am. J. Neuroradiol.
2002; 23: 1284–90.
115 Badjatia N, Topcuoglu MA, Pryor JC, et al. Preliminary experi-ence with intra-arterial nicardipine as a treatment for cerebral vasospasm. Am. J. Neuroradiol. 2004; 25: 819–26.
116 European CGRP in Subarachnoid Haemorrhage Study Group.
Effect of calcitonin-gene-related peptide in patients with delayed postoperative cerebral ischaemia after aneurysmal subarachnoid haemorrhage. Lancet 1992; 339: 831–4.
117 Hasan D, Vermeulen M, Wijdicks EFM, Hijdra A, van Gijn J.
Management problems in acute hydrocephalus after subarach-noid hemorrhage. Stroke 1989; 20: 747–53.
118 Kolluri VR, Sengupta RP. Symptomatic hydrocephalus follow-ing aneurysmal subarachnoid hemorrhage. Surg. Neurol. 1984;
21: 402–4.
119 Ruijs AC, Dirven CM, Algra A, Beijer I, Vandertop WP, Rinkel G.
The risk of rebleeding after external lumbar drainage in patients with untreated ruptured cerebral aneurysms. Acta Neurochir. (Wien) 2005; 147: 1157–62.
120 Fountas KN, Kapsalaki EZ, Machinis T, Karampelas I, Smisson HF, Robinson JS. Review of the literature regarding the relationship of rebleeding and external ventricular drainage in patients with subarachnoid hemorrhage of aneurysmal ori-gin. Neurosurg. Rev. 2005; 29: 14–18.
140 Part 3: Neurological diseases