Aneurysmatic Subdural Haemorrhage: Brief Review
Acute subdural hemorrhage caused by a ruptured intracranial aneurysm is a well-known association but usually linked to dismal outcome. We briefly reviewed the clinical and imaging features, surgical management and outcome of 45 patients with subdural bleeding related to intracranial aneurysm. Forty-two reports were encountered in the literature between 1981-2015 and three additional patients were identified in the author personal archives. A total of three patients had bilateral acute subdural hemorrhage, and the epidural hematoma was not present in any of the 45 reports. Coma was identified in 32/45 (71%) patients at admission. Only seven of 45 cases reported were managed by endovascular approach. A good clinical outcome was observed in 23/45 (51%) and early mortality occurred in 10/45 (22%) of the patients analysed. Neurosurgical management has evolved tremendously in recent years leading to more comprehensive understanding about this association. Factors leading to natural history, mechanisms, imaging aspects and improvement of clinical results of aneurysmatic subdural bleeding merit further studies.
Aneurysmatic subdural hemorrhage is a not uncommon event (1.8%), but it has been associated with a dismal prognosis.[1, 2, 3, 4, 5, 6, 7] Aneurysm-related subdural hemorrhage was first reported by German physician and professor of special pathology Sir Karl Ewald Hasse in 1855 in his publication Krankheiten des Nervensystems (Diseases of the Nervous System). Advancing age, an episode of sentinel headache before an index subarachnoid hemorrhage (SAH), an aneurysm originating from the posterior communicating artery and further intracranial hemorrhages on the initial CT scan are often associated with aneurysmal subdural hemorrhage. [1, 2] although the natural history and mechanisms leading with aneurysm bleed has been not completely elucidated.
Aneurysmatic subdural hemorrhage may be found in different intracranial locations, such as convexity, inter-hemispherical, tentorial, and intradural space, or even in the spinal subdural space, depending on the location of the aneurysm rupture.[9, 10, 11, 12, 13, 14] However, in a few cases, the hematoma was reported to have occurred far from the point of aneurysmatic rupture.[12, 15]
Five electronic databases: EMBASE, MEDLINE via PubMed, Web of Science, AMED Allied Medicine, and Europe PMC were searched. The following set of specific words were used to devise the search strategy: "subdural hemorrhage", " acute subdural hemorrhage", "subdural hematoma", "subdural haematoma", "subarachnoid hemorrhage", "intracranial aneurysms", "aneurysmal subdural hematoma". Single and combined words were matched. Thesaurus MeSH and systematization of bibliographic searches were used to improve the search.
At Table 1 were arranged the patients’ demographic data, clinical features (symptoms/signs), location and laterality of the aneurysm, characteristics of the aneurysmal subdural hemorrhage on CT scan, treatment and outcome were analyzed from each article separately and further results encountered.
There were four hundred eight articles founded. Due to relative rarity of the pathology and consequently lack of meta-analyses or randomized controlled trials, authors considered reported cases and cases series written in French, English, Portuguese, German, Danish, Japanese and Korean (total of 42 reported) and three cases from their personal experience of the author.
The mean age of patients reported was ± 46 years (range, 18-68 years) and 32/45 (71 %) were women. Coma was found in 71% (32/45) of cases. Eleven out of 45 patients had a headache at admission, 4/45 (8%) had mental confusion, (one case) oculomotor paresis, (one case) epileptic status were also reported. Other accompanying symptoms were dizziness, nausea, and vomiting.
The patients harbored intracranial aneurysms in several locations. There was only one patient with multiple aneurysms (one of our cases). The aneurysms were predominantly located at the internal carotid artery and posterior communicating artery junction (IC-PC) in 21/45 patients (46.6%), followed by 9/45 (20%) in MCA, 8/45 (17.7%) in anterior cerebral artery(ACA) one in distal ACA and two cases located in the pericallosal artery, 2/45 (4.4%) in carotid siphon (1/45 in the dorsal wall of the carotid artery and the other in the cavernous segment). We reported the first case located in the ophthalmic segment of the carotid siphon (Figure 1a, Figure 1b, Figure 1c, Figure 1d). In none of the reported cases has an aneurysm been located in the posterior circulation. Three cases of bilateral aneurysmal subdural hemorrhage were reported. None of the 45 patients showed epidural hematomas. Most of the cases of aneurysmatic subdural hemorrhage were located in the brain convexity, and in four cases there was an extension to the tentorial site or to the interhemispheric fissure.
Conventional surgical treatment in almost all cases of the aneurysm was performed by hematoma evacuation and clipping with good results (1981-2005). Mortality occurred in three cases with no mention of the treatment used. Endovascular coiling started to be performed alone if the aneurysmal subdural hemorrhage was clinically well tolerated or without significant midline shift after surgical evacuation of the aneurysmal subdural hemorrhage and has been described as the treatment of choice since 2002. Seven of 45 cases received endovascular treatment for their ruptured intracranial aneurysm. Data regarding outcome were available in 43/45 (95%) patients. Half the patients (23/45) had a good clinical outcome, ten patients remained disabled and nine patients died.
The frequency of aneurysm-related subdural hematoma is estimated to be 0.5-8% of cases of intracranial bleeding based on case reports, small clinical series, and autopsy series.[1, 2, 18, 19, 20, 21] The majority of case reports describe aneurysmal rupture resulting from the posterior communicating artery or IC-PC aneurysms.[1, 2, 20]
However, Clarke & Walton who divided intracranial vascular anomaly with a complicating subdural hemorrhage into three groups (Group I, II and III), depending upon the amount of clot present and clinical course as illustrated in Table 2. As group I - All posterior circulation aneurysms were included, in other words, large and resulting in death within 1-72 hours of onset. Vertebrobasilar or posterior circulation is less cited probably because subdural collection in the posterior fossa is overwhelming and rapidly fatal as frequently demonstrated by autopsy cases.[22, 23]
One of the likely causes of subdural hemorrhage encountered in association with ruptured intracranial aneurysm is thought to be due to head trauma, which may cause disruption of superficial cerebral or cortical bridging veins. Arteriovenous malformations, cocaine abuse, dural metastasis, coagulopathy, falx meningioma and rupture of a cortical artery located near the Sylvian region are other likely causes.[24, 25] Several risk factors have been described, such as sex, age, smoking, hypertension, history of SAH, sentinel headache, a location of the rupture aneurysm, intracerebral hemorrhage and IC-PC aneurysm. Finally, among these associated factors age, the location of the aneurysm, sentinel headache and presence of intraventricular hemorrhage seems to be determinant and have been well described as high risk of an aneurysmatic subdural hematoma by Biesbroek. [1, 2]. The same author also suggested that aneurysm anatomy, perianeurysmal environment and extension of subdural hemorrhage probably are probably also important factors that might well need further studies.[1, 2]
Two main circumstances among other mechanisms underlying aneurysm-related hemorrhage are hypothesized (i) on bleeding directly into the subdural space, in which case an aneurysm might be projected from the surface of the brain through the leptomeninges and rupture in the subdural space; or (ii) bleeding into the subdural space via the subarachnoid space.
Other possibilities are less cited: (iii) sentinel hemorrhages might cause the adhesion of an aneurysm to the adjacent arachnoid membrane, and the final rupture occurs into the subdural spaces; (iv) the stream of blood may rupture through the arachnoid membrane at some distant weak point; (v) secondary to decompression of an intracerebral hematoma into the subdural space following disruption of the arachnoid covering the cerebral cortex; (vi) when an aneurysm may penetrate the arachnoid mater transfixing and entering the subdural space, before its rupture and where the vessel passes through the subdural space (small cortical artery located at the Sylvian fissure) on its way to the circle of Willis it may cause direct blood flow into the subdural space. At Figure 2 and Figure 3, we demonstrated two giant MCA aneurysms (our experience) which adhered to the dura mater of an anterior clinoid process and the proximal side of plica petroclinoid anterior.
Several locations have been mentioned as potential sites where aneurysmal subdural hemorrhage associated without SAH, may be found. All such cases exhibited blood over the convexity and in other locations: seven cases showed blood tracking along the tentorium, blood was seen within the interhemispheric fissure in five cases, one case had aneurysmatic subdural hemorrhage along the dorsal aspect of the clivus, as well as the tentorium and convexity, and along the diaphragma sellae, migrating down into the spinal canal. Bilateral locations of subdural aneurysmatic hemorrhage are more rare.[26, 27]
Simple assessments based on neuroradiological findings may differentiate aneurysmatic subdural hemorrhage associated with intracranial aneurysm from those in which it is secondary to head trauma. For example, continuity between a convexity subdural hematoma and an interhemispheric hemorrhage could be related to a ruptured aneurysm of AcomA, and continuity between a tentorial hematoma and interhemispheric acute subdural hematoma may indicate a ruptured aneurysm of the internal carotid and IC-PC.[27, 28] All patients who present acute subdural hematoma at admission could also be evaluated by neuroimaging examination such as CT angiography (CTA), Magnetic resonance angiography (MRA) or conventional angiography to exclude not only aneurysm, but other conditions such as arteriovenous malformations (MAV) or arteriovenous (AV) fistulas.
Additional tools such as 3-D CTA and VasoCT® might provide a high resolution assessment of the relative composition of the aneurysm and vessels (presence of thrombus or vessel dissection) and delineation of some anatomical aspects, perianeurysmal environment and extent of the hemorrhage.[6, 7]
Based on our reviewed data (Table 1), surgical management in almost all cases was hematoma evacuation and clipping, with good results (1981-2005), and only three cases with death or no treatment. Endovascular management with or without hematoma evacuation through craniotomy has been done in seven patients. In the particular patients, coiling treatment, as well as hematoma evacuation, had produced favorable outcome.
The initial management depends on the clinical presentation of the acute subdural hematoma, on the volume of hematoma and on the mass effect that it may cause. Besides, the timing of surgical evacuation of hematoma is still a controversial issue. If a rapid clinical deterioration occurs, an emergency evacuation of hematoma should be performed before further investigations. Also, in the clinical worsening scenario, only subdural hematoma evacuation without an aneurysm-directed treatment (surgical clipping and / or endovascular coil embolization) will cause rapid decrease in intracranial pressure and intramural pressure in the aneurysm wall, and thus can increase risk of aneurysmal subarachnoid hemorrhage and further severe cerebral vasospasm. This situation ultimately complicates surgical clipping and reduces the success of surgical treatment. Within the indication, it seems more likely that early surgical clipping in the same session will increase the success of the treatment in these cases, concurrently with the early subdural hematoma evacuation as much as possible. Based on the review cases, endovascular coiling of ruptured intracranial aneurysm was preferred if subdural hemorrhage was clinically well tolerated or after surgical evacuation of acute subdural hematoma and has been described as the treatment of choice for ruptured aneurysm with subdural hemorrhage since 2005 according to reviewed cases.
New tips on the treatment strategy for aneurysmal subdural hematoma in the endovascular era are methodologically difficult to analyze, since open surgical management involves irrigation and removal of blood products has their unique indications depending on the clinical presentation and the strategy of the treatment aneurysm. New endovascular treatment strategies that aim to interrupt this cycle and tip this balance back in favor of resorption of hemorrhage as endovascular therapies aim to devascularize these membranes are already possible and need to be further investigated.  As well as other medical therapies, including the reduction of the micro-hemorrhage rate of the dural membranes, changes in the osmotic environment or changes in angiogenesis, also need to be further studied.
The treatment strategy for ruptured intracranial aneurysms has been decided by the character, shape, size and location of an aneurysm like any other kind of ruptured aneurysm depending by each department protocol.
In conclusion, this study suggests that aneurysmatic subdural hemorrhage due to ruptured aneurysms is quite uncommon and are more frequently seen related to anterior circulation aneurysms. A high degree of clinical suspicion is still important in the initial management of acute hematoma associated with intracranial aneurysm, which may permit an early diagnosis and appropriate treatment. Half of the cases had a good clinical outcome. Futures studies might target underlying mechanisms related with aneurysm-related hemorrhage and factors which influence the clinical and surgical outcome.
Conflicts of Interest/Disclosures
The authors declare no relevant financial or other conflict of interest or disclosures in relation to this paper.
This paper and the research behind it would not have been possible without the exceptional support of my family that always understands my enthusiasm, knowledge and time spending in attention to each detail to keep my work on track to the final draft of this paper. I am also very grateful for the insightful comments offered by Assoc. Professor Dr. Feyzi Birol Sarica and our peer reviewers. The generosity and expertise of all have improved this article in innumerable ways.
M-male, F-female, ACA- anterior cerebral artery, MCA- medial cerebral artery, IC-PC- internal carotid-posterior communication junction, HE- haematoma evacuation, SAH- subarachnoid haemorrhage
- Biesbroek JM, Rinkel GJ, Algra A, van der Sprenkel JW. Risk factors for acute subdural hematoma from intracranial aneurysm rupture. Neurosurgery. 2012;71(2):264-8; discussion 8-9.
- Biesbroek JM, van der Sprenkel JW, Algra A, Rinkel GJ. Prognosis of acute subdural haematoma from intracranial aneurysm rupture. J Neurol Neurosurg Psychiatry. 2013;84(3):254-7.
- Kulwin C, Bohnstedt BN, Payner TD, Leipzig TJ, Scott JA, DeNardo AJ, et al. Aneurysmal acute subdural hemorrhage: Prognostic factors associated with treatment. Journal of Clinical Neuroscience. 2014;21(8):1333-6.
- Marbacher S, Fandino J, Lukes A. Acute subdural hematoma from ruptured cerebral aneurysm. Acta Neurochir (Wien). 2010;152(3):501-7.
- O'Leary PM, Sweeny PJ. Ruptured intracerebral aneurysm resulting in a subdural hematoma. Ann Emerg Med. 1986;15(8):944-6.
- Rengachary SS, Szymanski DC. Subdural hematomas of arterial origin. Neurosurgery. 1981;8(2):166-72.
- Watanabe K, Wakai S, Okuhata S, Nagai M. Ruptured distal anterior cerebral artery aneurysms presenting as acute subdural hematoma--report of three cases. Neurol Med Chir (Tokyo). 1991;31(8):514-7.
- Hasse KE. The diseases of nervous system. Therapeutics HoSPa, Editor: Erlanger F Enke; 1855.
- Bassett RC, Lemmen LJ. Subdural hematoma associated with bleeding intracranial aneurysm. J Neurosurg. 1952;9(5):443-50.
- Boop WC, Chou SN, French LA. Ruptured intracranial aneurysm complicated by subdural hematoma. J Neurosurg. 1961;18:834-6.
- Ishibashi A, Yokokura Y, Sakamoto M. Acute subdural hematoma without subarachnoid hemorrhage due to ruptured intracranial aneurysm-case report. Neurol Med Chir (Tokyo). 1997;37(7):533-7.
- Bartoli A, Kotowski M, Pereira VM, Schaller K. Acute spinal epidural hematoma and cranial intradural hematoma due to a rupture of a posterior communicating artery aneurysm: case report. Neurosurgery. 2011;69(4):E1000-4; discussion E4.
- Gilad R, Fatterpekar GM, Johnson DM, Patel AB. Migrating subdural hematoma without subarachnoid hemorrhage in the case of a patient with a ruptured aneurysm in the intrasellar anterior communicating artery. Am J Neuroradiol. 2007;28(10):2014-6.
- Onda J kY, Emoto K, Yuki K. A case report of “pure” acute subdural hematoma secondary to ruptured intracranial aneurysm. Kyukyu Igaku 1989;13:631-4.
- Hornyak M, Hillard V, Nwagwu C, Zablow BC, Murali R. Ruptured intrasellar superior hypophyseal artery aneurysm presenting with pure subdural haematoma. Case report. Interv Neuroradiol. 2004;10(1):55-8.
- Pradat P, Doyon D, Navarro-Artiles G, Raymond JP. [Subdural arteriovenous aneurysm of the olfactory groove]. Neurochirurgie. 1968;14(8):923-30.
- Sørensen P, Jørgensen J. [Subdural haematoma from aneurysm without concurrent subarachnoid haemorrhage]. Ugeskr Laeger. 2009;171(1-2):59.
- Kondziolka D, Bernstein M, ter Brugge K, Schutz H. Acute subdural hematoma from ruptured posterior communicating artery aneurysm. Neurosurgery. 1988;22(1 Pt 1):151-4.
- Pasqualin A, Bazzan A, Cavazzani P, Scienza R, Licata C, Da Pian R. Intracranial hematomas following aneurysmal rupture: experience with 309 cases. Surg Neurol. 1986;25(1):6-17.
- Saito A, Nishino A, Suzuki I, Suzuki H, Utsunomiya A, Suzuki S, et al. Subarachnoid Hemorrhage Caused by Rupture of a Distal Anterior Inferior Cerebellar Artery Aneurysm -Three Case Reports. Neurologia Medico-Chirurgica. 2008;48(11):506-11.
- Triantafyllopoulou A, Beaumont A, Ulatowski J, Tamargo RJ, Varelas PN. Acute subdural hematoma caused by an unruptured, thrombosed giant intracavernous aneurysm. Neurocrit Care. 2006;5(1):39-42.
- Clarke E, Walton JN. Subdural haematoma complicating intracranial aneurysm and angioma. Brain. 1953;76(3):378-404.
- Kim MS, Jung JR, Yoon SW, Lee CH. Subdural hematoma of the posterior fossa due to posterior communicating artery aneurysm rupture. Surg Neurol Int. 2012;3:39.
- Blake G, James M, Ramjit C, Char G, Hunter R, Crandon I. Acute subdural haematoma without subarachnoid haemorrhage caused by rupture of an intracranial aneurysm. West Indian Med J. 2003;52(1):80-1.
- Alves OL, Gomes O. Cocaine-related acute subdural hematoma: an emergent cause of cerebrovascular accident. Acta Neurochir (Wien). 2000;142(7):819-21.
- Boujemâa H, Góngora-Rivera F, Barragán-Campos H, Karachi K, Chiras J, Sourour N. Bilateral acute subdural hematoma from ruptured posterior communicating artery aneurysm. A case report. Interv Neuroradiol. 2006;12(1):37-40.
- Krishnaney AA, Rasmussen PA, Masaryk T. Bilateral tentorial subdural hematoma without subarachnoid hemorrhage secondary to anterior communicating artery aneurysm rupture: a case report and review of the literature. AJNR Am J Neuroradiol. 2004;25(6):1006-7.
- Williams JP, Joslyn JN, White JL, Dean DF. Subdural hematoma secondary to ruptured intracranial aneurysm: computed tomographic diagnosis. J Comput Tomogr. 1983;7(2):142-53.
- Heran NS, Song JK, Namba K, Smith W, Niimi Y, Berenstein A. The utility of DynaCT in neuroendovascular procedures. AJNR Am J Neuroradiol. 2006;27(2):330-2.
- Weir B, Myles T, Kahn M, Maroun F, Malloy D, Benoit B, et al. Management of acute subdural hematomas from aneurysmal rupture. Can J Neurol Sci. 1984;11(3):371-6.
- Shinmura F, Nakajima S, Maruyama T, Azuma S. [A case of ruptured middle cerebral artery aneurysm with acute subdural hematoma after clipping of the aneurysm nine years previously]. No Shinkei Geka. 1989;17(12):1175-9.
- Ragland RL, Gelber ND, Wilkinson HA, Knorr JR, Tran AA. Anterior communicating artery aneurysm rupture: an unusual cause of acute subdural hemorrhage. Surg Neurol. 1993;40(5):400-2.
- Eggers FM, Tomsick TA, Lukin RR, Chambers AA. Recognition of subdural hematoma secondary to ruptured aneurysm by computerized tomography. Comput Radiol. 1982;6(5):309-13.
- Hatayama T, Shima T, Okada Y, Nishida M, Yamane K, Okita S, et al. [Ruptured distal anterior cerebral artery aneurysms presenting with acute subdural hematoma: report of two cases]. No Shinkei Geka. 1994;22(6):577-82.
- Ishibashi A, Yokokura Y, Sakamoto M. Acute subdural hematoma without subarachnoid hemorrhage due to ruptured intracranial aneurysm--case report. Neurol Med Chir (Tokyo). 1997;37(7):533-7.
- Satoh K, Sasaki T, Osato T. Intracranial aneurysm presenting as acute subdural hematoma without subarachnoid hemorrhage: report of three cases. Hokkaido Brain Res Found 1999;8:27–31
- Nonaka Y, Kusumoto M, Mori K, Maeda M. Pure acute subdural haematoma without subarachnoid haemorrhage caused by rupture of internal carotid artery aneurysm. Acta Neurochir (Wien). 2000;142(8):941-4.
- Inamasu J, Saito R, Nakamura Y, Ichikizaki K, Suga S, Kawase T, et al. Acute subdural hematoma caused by ruptured cerebral aneurysms: diagnostic and therapeutic pitfalls. Resuscitation. 2002;52(1):71-6.
- Araki T, Sampei T, Murata H, Fujiwara H, Taki W. [A case of internal carotid-posterior communicating artery aneurysm presenting pure acute subdural hematoma]. No Shinkei Geka. 2002;30(8):861-6.
- Aghakhani N, David P, Parker F, Morar S, Tadie M. Acute pure spontaneous subdural haematoma from ruptured intracranial aneurysms. Interventional Neuroradiology. 2002;8(4):393-8.
- Katsuno M, Murai Y, Teramoto A. [Acute subdural hematoma without subarachnoid hemorrhage following rupture of a distal anterior cerebral artery aneurysm: a case report]. No To Shinkei. 2003;55(5):435-8.
- Koerbel A, Ernemann U, Freudenstein D. Acute subdural haematoma without subarachnoid haemorrhage caused by rupture of an internal carotid artery bifurcation aneurysm: case report and review of literature. Br J Radiol. 2005;78(931):646-50.
- Ishikawa E, Sugimoto K, Yanaka K, Ayuzawa S, Iguchi M, Moritake T, et al. Interhemispheric subdural hematoma caused by a ruptured internal carotid artery aneurysm: case report. Surg Neurol. 2000;54(1):82-6.
- De Blasi R, Salvati A, Renna M, Chiumarulo L. Pure subdural hematoma due to cerebral aneurysmal rupture: an often delayed diagnosis. Cardiovasc Intervent Radiol. 2010;33(4):870-3.
- Weil AG, McLaughlin N, Lessard-Bonaventure P, Bojanowski MW. A misleading distal anterior cerebral artery aneurysm. Surgical Neurology International. 2010;1:55-.
- Bozzetto-Ambrosi P. Aneurysms of carotid-ophthalmic segment: clinical and angiographic findings.[Master’s Dissertation]. Recife: Federal University of Pernambuco; 2010.
- Field TS, Heran MK. Teaching NeuroImages: middle cerebral artery aneurysm rupture presenting as pure acute subdural hematoma. Neurology. 2010;74(4):e13.
- Gong J, Sun H, Shi X-Y, Liu W-X, Shen Z. Pure subdural haematoma caused by rupture of middle cerebral artery aneurysm: Case report and literature review. Journal of International Medical Research. 2014;42(3):870-8.
- Gonzales-Portillo G, Heros RC. Contralateral subdural hematoma resulting from intraoperative aneurysm rupture. Case illustration. J Neurosurg. 2000;93(1):147.
- Ishibashi A, Yokokura Y, Sakamoto M. Acute subdural hematoma without subarachnoid hemorrhage due to ruptured intracranial aneurysm-case report. Neurol Med Chir (Tokyo). 1997;37(7):533-7.
- Mrfka M, Pistracher K, Augustin M, Kurschel-Lackner S, Mokry M. Acute subdural hematoma without subarachnoid hemorrhage or intraparenchymal hematoma caused by rupture of a posterior communicating artery aneurysm: case report and review of the literature. The Journal of emergency medicine. 2013;44(6):e369-73.
- Schuss P, Konczalla J, Platz J, Vatter H, Seifert V, Guresir E. Aneurysm-related subarachnoid hemorrhage and acute subdural hematoma: single-center series and systematic review Clinical article. Journal of Neurosurgery. 2013;118(5):984-90.
- Shigematsu H, Sorimachi T, Aoki R, Osada T, Srivatanakul K, Matsumae M. Acute subdural hematoma caused by a ruptured cavernous internal carotid artery giant aneurysm following abducens nerve palsy: case report and review of the literature. Acta Neurochirurgica. 2015;157(7):1113-6.
- Suhara S, Wong AS, Wong JO. Post-traumatic pericallosal artery aneurysm presenting with subdural haematoma without subarachnoid haemorrhage. Br J Neurosurg. 2008;22(2):295-7.
- Bozzetto-Ambrosi P, Andrade G, Azevedo H. Traumatic pseudoaneurysm of the middle meningeal artery and cerebral intraparenchymal hematoma: case report. Surgical Neurology 2006-S29- S31.
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