Headache as a warning symptom of impending aneurysmal subarachnoid haemorrhage
John R Østergaard
Cephalalgia Østergaard JR. Headache as a warning symptom of impending aneurysmal subarachnoid haemorrhage. Cephalalgia 1991;11:53-5. Oslo. ISSN 0333-1024 About half of the aneurysm patients admitted to neurosurgical departments experience warning symptoms in the form of minor bleeding episodes days or even several months before a major haemorrhage occurs. Headache is the most common symptom of this warning leak, occurring in 9 out of 10 patients. The onset of headache is sudden and is unusual in severity and location, being unlike any headache the patient has otherwise experienced. It is frequently accompanied by transient nausea, vomiting, visual disturbances or meningism. Medical advice may be sought by the patient but all too often the diagnostic importance of a warning headache is missed. It is misinterpreted as attacks of migraine, tension headache, the 'flu, sinuitis, or a "sprained neck", A more vigilant attention to the presence of a warning headache probably offers the greatest opportunity for altering the otherwise serious natural history of aneurysmal sub-arachnoid haemorrhage. If a warning headache is suspected, lumbar puncture is the examination of choice, once CT scanning has ruled out an intracranial mass lesion. • Migraine, saccular aneurysm, subarachnoid haemorrhage, tension headache, warning headache John R Østergaard, Department of Paediatrics A, Århus Kommunehospital, University Hospital of Århus, DK-8000 Århus C, Denmark; Accepted 8 January 1991 The well-known presentation of aneurysmal sub-arachnoid haemorrhage is that of a very severe headache associated with stiff neck, photophobia, nausea and vomiting, often with loss of consciousness. With such a presentation the diagnosis of subarachnoid haemorrhage is usually obvious. Neurosurgeons, who have the benefit of hindsight, are aware that about half of the patients they see with aneurysms have experienced minor bleeding episodes days to several months before their major haemorrhage-a "warning leak" (1-6). The most common symptom of such a warning leak is headache. The recognition of these warning headaches probably offers the best opportunity for altering the otherwise serious prognosis of aneurysmal subarachnoid haemorrhage (7), but they are often misinterpreted (4-6). In the present paper, the pathophysiology and characteristics of the warning headache will be discussed. Headache mechanisms
Localized headache or pain in the patient with a warning leak is most probably referred pain, according to the concept of Ray and Wolff (8). They produced headache and head pain by stimulation of arteries in the circle of Willis, which derive their innervation from the fifth, ninth and tenth cranial nerves and C-1 to C-3 spinal nerves. Histological study of aneurysms from patients who had had warning signs often shows minor haemorrhages in the aneurysmal wall and adherence of the aneurysm to the contiguous brain via reactive changes (9, 10). These small haemorrhages, by stimulating sensory nerve endings both mechanically and chemically, may cause the pain. This mechanism thus induces a localized headache of vascular origin. The majority of patients with warning leaks have generalized headache (2-4). This is most probably a manifestation of meningeal irritation due to a minor leakage of blood into the subarachnoid space. Other explanations which have been proposed for the forewarning of major subarachnoid haemorrhage include a sudden expansion of the aneurysm and ischaemia due to cerebral vasospasm (2, 11). Incidence of warning headache
The five largest series of patients with warning signs and intracranial aneurysms comprise a total of 629 patients, and the data show that about 50% (range 28-60%) of patients with a bleeding saccular aneurysm admitted to a neurosurgical department will have had a premonitory warning leak (2-6). In epidemiologic series, including not only hospitalizations but also cases who die before receiving medical attention, it has been reported that 15-20% of the aneurysm patients never reach the neuro-surgical department (12, 13). Thus, as many as 60% of all patients with aneurysms who eventually have a major haemorrhage will have one or more warning
episodes before the major haemorrhage. The incidence may be slightly higher in women than in men (2, 3). Headache as a warning symptom occurs in nearly all the patients (range 86-97%) (2-4, 6). In about two-thirds, the headache has associated signs and symptoms: nausea and vomiting (about 20%), meningism or neck pain (about 30%), visual disturbances including blurred or decreased vision and visual defects (about 15%), and even motor or sensory disturbances (15-20%) (2-4, 6). Photophobia rarely occurs (6). Loss of consciousness, often very transitory, without antecedent headache has also been described (4). On awakening, however, all of these patients complained of a severe headache. Nausea, vomiting, or both, seem to be characteristic of patients with anterior cerebral artery aneurysms and patients with aneurysms originating in the posterior circulation. Motor weakness and speech disturbances often reflect an aneurysm of the middle cerebral artery (3). Another characteristic warning feature in patients with an aneurysm of the internal carotid artery is impairment of the extraocular muscles due to third nerve palsy. Waga et al. in a retrospective study found this symptom in one patient in four with a warning leak and an aneurysm of the internal carotid artery (3). The pattern of the headache
The headache is usually characterized as unusual in severity and location, being unlike any headache the patient has otherwise experienced. The onset is sudden and usually subsides during one or two days (4), but in some cases it is unremitting for as long as two weeks or until a subsequent major haemorrhage occurs (6). Overall, the site of the headache seems to be a poor localizing symptom for the aneurysm-with the exception of internal carotid-posterior communicating artery aneurysms, in which the headache is often ipsilateral and retro-orbital (3,4, 6). Aneurysms originating from the anterior communicating artery complex are usually associated with a bifrontal headache radiating bi-occipitally, as is headache due to minor leakage from the middle cerebral artery aneurysms (3, 6). Aneurysms in the posterior circulation cause a severe generalized headache associated with nausea and vomiting (3). How often do patients with a sudden, severe and unusual type of headache have a subarachnoid haemorrhage originating from a saccular aneurysm? Information on this question is sparse. In the study of Duffy (5), 71 patients were admitted to the regional neurosurgical department during a period of two years. All patients had symptoms of sudden onset suggestive of subarachnoid haemorrhage and all had meningism. They all underwent CT and angiography. If subarachnoid bleeding was not demonstrated on CT, lumbar puncture was performed. Forty-six of the 63 patients with a proven subarachnoid haemorrhage harboured an aneurysm (73%). In 8 patients no subarachnoid haemorrhage was demonstrated either on CT or on lumbar puncture, despite the fact that all the patients complained of sudden onset of headache or neck pain radiating into the head, and meningism. Angiography was performed in view of the suggestive history. No aneurysms or other vascular malformations were found. They were followed for a minimum of six months; none had recurrence of their symptoms. The warning headache is often so unusual that patients seek medical advice. In Leblanc's study this was true of 4 out of every 10 patients, but in no case was the correct diagnosis made (6). The attacks of headache were misinterpreted as attacks of migraine, tension headache, the 'flu, sinuitis, or a "sprained neck". Similarly, in Duffy's series 8 out of 13 patients with a warning symptom had consulted their general practitioners at the time of the warning headache; 2 were seen in the Casualty Department of the hospital, and 3 had been admitted to hospital and discharged home without undergoing appropriate investigations for a possible intracranial haemorrhage (5). The tentative diagnoses made at the time of consultation were tension headache (3 patients); neck pain (3 patients); gastroenteritis (2 patients); hypertension, migraine, viral illness, temporal arteritis, and eye strain (1 patient, respectively). The clinical importance of a (missed) warning headache
In patients with saccular aneurysms morbidity and mortality figures have not changed in recent decades, primarily because the diagnosis is still usually established only after rupture (14, 15). One of the more important factors determining the ultimate outcome in a patient with a ruptured aneurysm is his or her clinical condition on admission to hospital (16). Leblanc's prospective study of 87 patients consecutively admitted with subarachnoid hemorrhage from an aneurysm showed that 25 had had a minor leak followed by a major rupture, and of these only 10 (40%) were in good clinical condition on admission (Hunt and Hess stages I-II (17)), in contrast with 89% of those patients who had had only one bleeding episode (6). Not surprisingly, the mortality in the former group of patients was three times higher than in those who had had only one bleed. This obvious clinical benefit of recognizing and treating the patient with an aneurysm before a major rupture occurs has been well documented by others (2, 5). Indeed, the adverse prognostic effect of a
missed warning leak is as severe as the effect of a clear-cut sequence of rebleeding episodes, either when the rebleed complicates the hospital course (18-20) or when it occurs several years later (21, 22). Summary and conclusion
A minor leak preceding the major rupture of a cerebral aneurysm is a common occurrence. It is associated with a high mortality rate if it is unrecognized. On the other hand, if an aneurysm is suspected and treated following a minor bleeding episode, the prognosis is excellent (4-6). Headache is the most common symptom of a premonitory leak, occurring in 9 out of 10 patients. A minor leak of a saccular aneurysm should be suspected in those patients without a history of severe headache who present with severe, unremitting, unusual pain in the head or face, particularly if it is hemicranial or hemifacial. Vomiting and meningism certainly strengthen the case; patients with these symptoms require urgent referral and need further investigation. In the future, magnetic resonance studies might be the first-line imaging strategy in cases of suspected subarachnoid haemorrhage because the potential for visualizing aneurysms is much greater with MR imaging than with CT (23). Furthermore, as a result of the para-magnetic effects of deoxyhaemoglobin in intact red blood cells, MRI may reveal a subarachnoid haemorrhage for an extended period of time (24). For the present, however, CT remains the quicker, more accessible, and probably cheaper procedure. More importantly, the interpretation of some MR appearances is still at an early stage, and it is not always possible to draw firm conclusions or to formulate a definite therapeutic plan. Dully has shown that CT may be unreliable in showing the sub-arachnoid blood produced by a minor leak, and for the time being lumbar puncture is the examination of choice once CT has ruled out an intracranial mass lesion or intracranial hypertension (5). If xantho-chromic staining of the cerebrospinal fluid is seen or if the cerebrospinal fluid is bloody after an atraumatic puncture, then angiography should be performed. If, on the other hand, the CT scan and cerebrospinal fluid findings are normal, the headache can be regarded as a benign symptom, and cerebral angiography is not indicated (25). References
1.
Gillingham FJ. The management of ruptured intracranial aneurysms. Scot Med J 1967;12:377-83
2.
Okawara S-H. Warning signs prior to rupture of an intra-cranial aneurysm. J Neurosurg 1973;38:575-80
3.
Waga S, Ohtsubo K, Handa H. Warning signs in intracranial aneurysms. Surg Neurol 1973;3:15-20
4.
King RB, Saba MI. Forewarnings of major subarachnoid hemorrhage. Due to congenital berry aneurysms. NY State J Med 1974;74:638-9
5.
Duffy GP. The warning leak in spontaneous subarachnoid hemorrhage. Med J Aust 1983;1:514-16
6.
Leblanc R. The minor leak preceding subarachnoid hemorrhage. J Neurosurg 1987;66:35-9
7.
Østergaard JR. Risk factors in intracranial saccular aneurysms. Aspects on the formation and rupture of aneurysms, and development of cerebral vasospasm (Thesis). Acta Neurol Scand 1989;80:81-98
8.
Ray BS, Wolff HG. Experimental studies on headache: pain-sensitive structures of the head and their significances in headache. Arch Surg 1940;41:81356
9.
Gillingham FJ. The management of ruptured intracranial aneurysm. Ann R Coil Surg Engl 1958;23:89-117
10.
Ball MJ. Pathogenesis of the "sentinel headache" preceding berry aneurysm rupture. Can Med Assoc J 1975;112:78-9
11.
Day JW, Raskin NH. Thunderclap headache: symptoms of unruptured cerebral aneurysm. Lancet 1986;ii:12474
12.
Bonita R, Thomsom S. Subarachnoid hemorrhage: epidemiology, diagnosis, management, and outcome. Stroke 1985;16:591-4
13.
Ljunggren B, Saveland H, Brandt L, Zygmunt S. Early operation and overall outcome in aneurysmal subarachnoid hemorrhage. J Neurosurg 1985;62:547-51
14.
Phillips LH, Whisnant JP, O'Fallon WM, Sundt TM. The unchanging pattern of subarachnoid hemorrhage in a community. Neurology 1980;30:1034-40
15.
Rosenørn J. Eskesen V, Schmidt K, et al. Clinical features and outcome in 1076 patients with ruptured intracranial saccular aneurysms: a prospective consecutive study. Br J Neurosurg 1987;1:33-46
16.
Disney L, Weir B, Grace M, and the Canadian Nimodipine Study Group. Factors influencing the outcome of aneurysm rupture in poor grade patients: A prospective series. Neuro-surgery 1988;23:1-9
17.
Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 1968;28:14-20
18.
Locksley HB. Report on the cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Section V, part I. Natural history of subarachnoid hemorrhage, intracranial aneurysms, and arteriovenous malformations. J Neurosurg 1966;25:219-39
19.
Drake CG. Management of cerebral aneurysms. Stroke 1981;12:273-83
20.
Torner JC, Kassell NF, Wallace RB, Adams HP. Preoperative prognostic factors for rebleeding and survival in aneurysm patients receiving antifibrinolytic therapy: report on the cooperative study. Neurosurgery 1981;9:506-13
21.
Winn HR, Almaani WS, Berga SL, Jana JA, Richardson AE. The long-term outcome in patients with multiple aneurysms. Incidence of late hemorrhage and implications for treatment of incidental aneurysms. J Neurosurg 1983;59:642-51
22.
Nishioka H, Torner JC, Graf CJ, Kassels NF, Sahs AL, Goettler LC. Cooperative study of intracranial aneurysms and sub-arachnoid hemorrhage: a long-term prognostic study. II. Ruptured intracranial aneurysms managed conservatively. Arch Neurol 1984;41:1142-6
23.
Jenkins A, Hadley DM, Teasdale GM, Condon B, Macpherson P, Patterson J. Magnetic resonance imaging of acute sub-arachnoid haemorrhage. J Neurosurg 1988;68:731-6
24.
Di Chiro G, Brooks RA, Girton ME, et al. Sequential MR studies of intracranial hematomas in monkeys. AJNR 1986;7:193-9
25.
Wijdick EFM, Kerkhoff H, van Gijn J. Long-term follow-up of 71 patients with thunderclap headache mimicking sub-arachnoid hemorrhage. Lancet 1988;ii:68-70
John R Østergaard
Cephalalgia Østergaard JR. Headache as a warning symptom of impending aneurysmal subarachnoid haemorrhage. Cephalalgia 1991;11:53-5. Oslo. ISSN 0333-1024 About half of the aneurysm patients admitted to neurosurgical departments experience warning symptoms in the form of minor bleeding episodes days or even several months before a major haemorrhage occurs. Headache is the most common symptom of this warning leak, occurring in 9 out of 10 patients. The onset of headache is sudden and is unusual in severity and location, being unlike any headache the patient has otherwise experienced. It is frequently accompanied by transient nausea, vomiting, visual disturbances or meningism. Medical advice may be sought by the patient but all too often the diagnostic importance of a warning headache is missed. It is misinterpreted as attacks of migraine, tension headache, the 'flu, sinuitis, or a "sprained neck", A more vigilant attention to the presence of a warning headache probably offers the greatest opportunity for altering the otherwise serious natural history of aneurysmal sub-arachnoid haemorrhage. If a warning headache is suspected, lumbar puncture is the examination of choice, once CT scanning has ruled out an intracranial mass lesion. • Migraine, saccular aneurysm, subarachnoid haemorrhage, tension headache, warning headache John R Østergaard, Department of Paediatrics A, Århus Kommunehospital, University Hospital of Århus, DK-8000 Århus C, Denmark; Accepted 8 January 1991 The well-known presentation of aneurysmal sub-arachnoid haemorrhage is that of a very severe headache associated with stiff neck, photophobia, nausea and vomiting, often with loss of consciousness. With such a presentation the diagnosis of subarachnoid haemorrhage is usually obvious. Neurosurgeons, who have the benefit of hindsight, are aware that about half of the patients they see with aneurysms have experienced minor bleeding episodes days to several months before their major haemorrhage-a "warning leak" (1-6). The most common symptom of such a warning leak is headache. The recognition of these warning headaches probably offers the best opportunity for altering the otherwise serious prognosis of aneurysmal subarachnoid haemorrhage (7), but they are often misinterpreted (4-6). In the present paper, the pathophysiology and characteristics of the warning headache will be discussed. Headache mechanisms
Localized headache or pain in the patient with a warning leak is most probably referred pain, according to the concept of Ray and Wolff (8). They produced headache and head pain by stimulation of arteries in the circle of Willis, which derive their innervation from the fifth, ninth and tenth cranial nerves and C-1 to C-3 spinal nerves. Histological study of aneurysms from patients who had had warning signs often shows minor haemorrhages in the aneurysmal wall and adherence of the aneurysm to the contiguous brain via reactive changes (9, 10). These small haemorrhages, by stimulating sensory nerve endings both mechanically and chemically, may cause the pain. This mechanism thus induces a localized headache of vascular origin. The majority of patients with warning leaks have generalized headache (2-4). This is most probably a manifestation of meningeal irritation due to a minor leakage of blood into the subarachnoid space. Other explanations which have been proposed for the forewarning of major subarachnoid haemorrhage include a sudden expansion of the aneurysm and ischaemia due to cerebral vasospasm (2, 11). Incidence of warning headache
The five largest series of patients with warning signs and intracranial aneurysms comprise a total of 629 patients, and the data show that about 50% (range 28-60%) of patients with a bleeding saccular aneurysm admitted to a neurosurgical department will have had a premonitory warning leak (2-6). In epidemiologic series, including not only hospitalizations but also cases who die before receiving medical attention, it has been reported that 15-20% of the aneurysm patients never reach the neuro-surgical department (12, 13). Thus, as many as 60% of all patients with aneurysms who eventually have a major haemorrhage will have one or more warning
episodes before the major haemorrhage. The incidence may be slightly higher in women than in men (2, 3). Headache as a warning symptom occurs in nearly all the patients (range 86-97%) (2-4, 6). In about two-thirds, the headache has associated signs and symptoms: nausea and vomiting (about 20%), meningism or neck pain (about 30%), visual disturbances including blurred or decreased vision and visual defects (about 15%), and even motor or sensory disturbances (15-20%) (2-4, 6). Photophobia rarely occurs (6). Loss of consciousness, often very transitory, without antecedent headache has also been described (4). On awakening, however, all of these patients complained of a severe headache. Nausea, vomiting, or both, seem to be characteristic of patients with anterior cerebral artery aneurysms and patients with aneurysms originating in the posterior circulation. Motor weakness and speech disturbances often reflect an aneurysm of the middle cerebral artery (3). Another characteristic warning feature in patients with an aneurysm of the internal carotid artery is impairment of the extraocular muscles due to third nerve palsy. Waga et al. in a retrospective study found this symptom in one patient in four with a warning leak and an aneurysm of the internal carotid artery (3). The pattern of the headache
The headache is usually characterized as unusual in severity and location, being unlike any headache the patient has otherwise experienced. The onset is sudden and usually subsides during one or two days (4), but in some cases it is unremitting for as long as two weeks or until a subsequent major haemorrhage occurs (6). Overall, the site of the headache seems to be a poor localizing symptom for the aneurysm-with the exception of internal carotid-posterior communicating artery aneurysms, in which the headache is often ipsilateral and retro-orbital (3,4, 6). Aneurysms originating from the anterior communicating artery complex are usually associated with a bifrontal headache radiating bi-occipitally, as is headache due to minor leakage from the middle cerebral artery aneurysms (3, 6). Aneurysms in the posterior circulation cause a severe generalized headache associated with nausea and vomiting (3). How often do patients with a sudden, severe and unusual type of headache have a subarachnoid haemorrhage originating from a saccular aneurysm? Information on this question is sparse. In the study of Duffy (5), 71 patients were admitted to the regional neurosurgical department during a period of two years. All patients had symptoms of sudden onset suggestive of subarachnoid haemorrhage and all had meningism. They all underwent CT and angiography. If subarachnoid bleeding was not demonstrated on CT, lumbar puncture was performed. Forty-six of the 63 patients with a proven subarachnoid haemorrhage harboured an aneurysm (73%). In 8 patients no subarachnoid haemorrhage was demonstrated either on CT or on lumbar puncture, despite the fact that all the patients complained of sudden onset of headache or neck pain radiating into the head, and meningism. Angiography was performed in view of the suggestive history. No aneurysms or other vascular malformations were found. They were followed for a minimum of six months; none had recurrence of their symptoms. The warning headache is often so unusual that patients seek medical advice. In Leblanc's study this was true of 4 out of every 10 patients, but in no case was the correct diagnosis made (6). The attacks of headache were misinterpreted as attacks of migraine, tension headache, the 'flu, sinuitis, or a "sprained neck". Similarly, in Duffy's series 8 out of 13 patients with a warning symptom had consulted their general practitioners at the time of the warning headache; 2 were seen in the Casualty Department of the hospital, and 3 had been admitted to hospital and discharged home without undergoing appropriate investigations for a possible intracranial haemorrhage (5). The tentative diagnoses made at the time of consultation were tension headache (3 patients); neck pain (3 patients); gastroenteritis (2 patients); hypertension, migraine, viral illness, temporal arteritis, and eye strain (1 patient, respectively). The clinical importance of a (missed) warning headache
In patients with saccular aneurysms morbidity and mortality figures have not changed in recent decades, primarily because the diagnosis is still usually established only after rupture (14, 15). One of the more important factors determining the ultimate outcome in a patient with a ruptured aneurysm is his or her clinical condition on admission to hospital (16). Leblanc's prospective study of 87 patients consecutively admitted with subarachnoid hemorrhage from an aneurysm showed that 25 had had a minor leak followed by a major rupture, and of these only 10 (40%) were in good clinical condition on admission (Hunt and Hess stages I-II (17)), in contrast with 89% of those patients who had had only one bleeding episode (6). Not surprisingly, the mortality in the former group of patients was three times higher than in those who had had only one bleed. This obvious clinical benefit of recognizing and treating the patient with an aneurysm before a major rupture occurs has been well documented by others (2, 5). Indeed, the adverse prognostic effect of a
missed warning leak is as severe as the effect of a clear-cut sequence of rebleeding episodes, either when the rebleed complicates the hospital course (18-20) or when it occurs several years later (21, 22). Summary and conclusion
A minor leak preceding the major rupture of a cerebral aneurysm is a common occurrence. It is associated with a high mortality rate if it is unrecognized. On the other hand, if an aneurysm is suspected and treated following a minor bleeding episode, the prognosis is excellent (4-6). Headache is the most common symptom of a premonitory leak, occurring in 9 out of 10 patients. A minor leak of a saccular aneurysm should be suspected in those patients without a history of severe headache who present with severe, unremitting, unusual pain in the head or face, particularly if it is hemicranial or hemifacial. Vomiting and meningism certainly strengthen the case; patients with these symptoms require urgent referral and need further investigation. In the future, magnetic resonance studies might be the first-line imaging strategy in cases of suspected subarachnoid haemorrhage because the potential for visualizing aneurysms is much greater with MR imaging than with CT (23). Furthermore, as a result of the para-magnetic effects of deoxyhaemoglobin in intact red blood cells, MRI may reveal a subarachnoid haemorrhage for an extended period of time (24). For the present, however, CT remains the quicker, more accessible, and probably cheaper procedure. More importantly, the interpretation of some MR appearances is still at an early stage, and it is not always possible to draw firm conclusions or to formulate a definite therapeutic plan. Dully has shown that CT may be unreliable in showing the sub-arachnoid blood produced by a minor leak, and for the time being lumbar puncture is the examination of choice once CT has ruled out an intracranial mass lesion or intracranial hypertension (5). If xantho-chromic staining of the cerebrospinal fluid is seen or if the cerebrospinal fluid is bloody after an atraumatic puncture, then angiography should be performed. If, on the other hand, the CT scan and cerebrospinal fluid findings are normal, the headache can be regarded as a benign symptom, and cerebral angiography is not indicated (25). References
1.
Gillingham FJ. The management of ruptured intracranial aneurysms. Scot Med J 1967;12:377-83
2.
Okawara S-H. Warning signs prior to rupture of an intra-cranial aneurysm. J Neurosurg 1973;38:575-80
3.
Waga S, Ohtsubo K, Handa H. Warning signs in intracranial aneurysms. Surg Neurol 1973;3:15-20
4.
King RB, Saba MI. Forewarnings of major subarachnoid hemorrhage. Due to congenital berry aneurysms. NY State J Med 1974;74:638-9
5.
Duffy GP. The warning leak in spontaneous subarachnoid hemorrhage. Med J Aust 1983;1:514-16
6.
Leblanc R. The minor leak preceding subarachnoid hemorrhage. J Neurosurg 1987;66:35-9
7.
Østergaard JR. Risk factors in intracranial saccular aneurysms. Aspects on the formation and rupture of aneurysms, and development of cerebral vasospasm (Thesis). Acta Neurol Scand 1989;80:81-98
8.
Ray BS, Wolff HG. Experimental studies on headache: pain-sensitive structures of the head and their significances in headache. Arch Surg 1940;41:81356
9.
Gillingham FJ. The management of ruptured intracranial aneurysm. Ann R Coil Surg Engl 1958;23:89-117
10.
Ball MJ. Pathogenesis of the "sentinel headache" preceding berry aneurysm rupture. Can Med Assoc J 1975;112:78-9
11.
Day JW, Raskin NH. Thunderclap headache: symptoms of unruptured cerebral aneurysm. Lancet 1986;ii:12474
12.
Bonita R, Thomsom S. Subarachnoid hemorrhage: epidemiology, diagnosis, management, and outcome. Stroke 1985;16:591-4
13.
Ljunggren B, Saveland H, Brandt L, Zygmunt S. Early operation and overall outcome in aneurysmal subarachnoid hemorrhage. J Neurosurg 1985;62:547-51
14.
Phillips LH, Whisnant JP, O'Fallon WM, Sundt TM. The unchanging pattern of subarachnoid hemorrhage in a community. Neurology 1980;30:1034-40
15.
Rosenørn J. Eskesen V, Schmidt K, et al. Clinical features and outcome in 1076 patients with ruptured intracranial saccular aneurysms: a prospective consecutive study. Br J Neurosurg 1987;1:33-46
16.
Disney L, Weir B, Grace M, and the Canadian Nimodipine Study Group. Factors influencing the outcome of aneurysm rupture in poor grade patients: A prospective series. Neuro-surgery 1988;23:1-9
17.
Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 1968;28:14-20
18.
Locksley HB. Report on the cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Section V, part I. Natural history of subarachnoid hemorrhage, intracranial aneurysms, and arteriovenous malformations. J Neurosurg 1966;25:219-39
19.
Drake CG. Management of cerebral aneurysms. Stroke 1981;12:273-83
20.
Torner JC, Kassell NF, Wallace RB, Adams HP. Preoperative prognostic factors for rebleeding and survival in aneurysm patients receiving antifibrinolytic therapy: report on the cooperative study. Neurosurgery 1981;9:506-13
21.
Winn HR, Almaani WS, Berga SL, Jana JA, Richardson AE. The long-term outcome in patients with multiple aneurysms. Incidence of late hemorrhage and implications for treatment of incidental aneurysms. J Neurosurg 1983;59:642-51
22.
Nishioka H, Torner JC, Graf CJ, Kassels NF, Sahs AL, Goettler LC. Cooperative study of intracranial aneurysms and sub-arachnoid hemorrhage: a long-term prognostic study. II. Ruptured intracranial aneurysms managed conservatively. Arch Neurol 1984;41:1142-6
23.
Jenkins A, Hadley DM, Teasdale GM, Condon B, Macpherson P, Patterson J. Magnetic resonance imaging of acute sub-arachnoid haemorrhage. J Neurosurg 1988;68:731-6
24.
Di Chiro G, Brooks RA, Girton ME, et al. Sequential MR studies of intracranial hematomas in monkeys. AJNR 1986;7:193-9
25.
Wijdick EFM, Kerkhoff H, van Gijn J. Long-term follow-up of 71 patients with thunderclap headache mimicking sub-arachnoid hemorrhage. Lancet 1988;ii:68-70
