Secondary Intracerebral Hematoma

INVITED REVIEW online © ML Comm J Neurocrit Care 2010;3 Suppl 1:S15-S18 ISSN 2005-0348

Eui Kyo Seo, MD Department of Neurosurgery, Ewha Womans University School of Medicine, Seoul, Korea

Introduction: Intracerebral hemorrhage (ICH) accounts for 10 to 15% of all strokes. Although chronic hypertension accounts for the majority of ICH, other common causes include aneurysm rupture, AVM, moyamoya disease. Summary: This article review the diseases which cause secondary ICH. Additional etiologies that predispose to ICH include vascular malformations, moyamoya disease, brain aneurismal rupture, tumor bleeding. It is well known that: 1) middle cerebral artery and posterior communicating artery aneurysms will predominantly cause intratemporal clots, with possible extension into the adjacent lobes; 2) anterior communicating artery aneurysms will most likely produce frontobasal hematomas; and 3) anterior cerebral artery aneurysms will mainly cause interhemisph- eric clots. Secondary ICH caused by bleeding of aneurysm directly into the brain parenchyma from the sac adhered to the pia mater was fundamentally a subcortical hemorrhage. Moyamoya disease (MMD) is a chronic, occlusive cerebrovascular disease involving bilateral stenosis or occlusion of the terminal portion of the ICAs and/or the proximal portions of the ACAs and MCAs. Certebral arteriovenous malformation (AVM) is defined the direct communication of arteries to abnormally tortuous and dilated veins without interposing capillaries. Dilated and tortuous draining vein which has high intravascular pressure is always the rupture site and cause secondary ICH. The risk of initial hemorrhage is approximately 2-3% per year. For the treatment of intracranial arteriovenous malformations (AVMs), one of three established methods or combinations of them-microsurgery, embolization, and stereotactic radiosurgery. Conclusion: Aneurysm rupture, moyamoya disease, AVM rupture are the common cause of secondary ICH. The morbidity and mortality associated with secondary ICH remain high despite recent advances in our understanding of the clinical course and pathophysiology of these diseases which cause secondary ICH. Novel preventive and acute treatment therapies are needed and may be on the horizon. J Neurocrit Care 2010;3 Suppl 1:S15-S18

KEY WORDS: Secondary ICH·Aneurysm·Moyamoya disease·AVM.

Introduction nial bleeding: the rupture of dilated and fragile moyamoya vessels or rupture of saccular aneurysms in the circle of Willis, Intracerebral hemorrhage (ICH) occurs from the rupture of or on dilated perforators. small vessels into the brain parenchyma and accounts for approximately 10% of all strokes in the United States, and car- AVM ries with it a significantly high morbidity and mortality.1-4 The most common chronic vascular diseases that lead to ICH are BRAIN AVMs, first described as “erectile tumors” >200 chronic hypertension and cerebral amyloid angiopathy which years ago, are defined as the direct communication of arteries is regarded as primary ICH traditionally.5,6 Additional etiolo- to abnormally tortuous and dilated veins without interposing gies that predispose to ICH include vascular malformations, capillaries.10 moyamoya disease, brain aneurismal rupture, tumor bleed- Many authors have suggested that they are not static con- ing.7-9 Management in secondary ICH is first focused on re- genital lesions, but are dynamic with the ability to grow, regress, moval of etiology and IICP control. Etiology caused secondary and even reappear as de novo brain AVMs after complete re- ICH, pathophysiology and clinical presentation is completely section or radiosurgery.1,5,11,12 This behavior has historically understood for proper management. We review ruptured an- led AVMs to be classified as “proliferative capillaropathies,” eurysm, arteriovenous malformation, moyamoya disease which “erectile tumors,” “metamorphotic dysplastic vessels,” or le- commonly cause ICH. There are two main causes of intracra- sions with “autonomic growth.”5,10 These lesions rarely ap- Address for correspondence: Eui Kyo Seo, MD pear in childhood but instead typically manifest symptoms in Department of Neurosurgery, Ewha Womans University School of 12 adult life, usually by the 3rd decade. Approximately 50% of Medicine, 911 1 Mok dong, Yangcheon gu, Seoul 158 710, Korea - - - - 13 Tel: +82-2-2650-2650, Fax: +82-2-2650-2652 patients present with symptoms of hemornhage. The risk of 14 E-mail: [email protected] initial hemonrhage is approximately 2-3% per year. Subse-

Copyright © 2010 The Korean Neurocritical Care Society S15 J Neurocrit Care ▌2010 ;3 Suppl 1:S15-S18 quent bleeding is more frequent in the year following the intraventricular hemorrhage associated with an ICH, com- first episode of hemorrhage, occurring in 6-17% of the cases. pared with ICH only, IVH only, and SAH only group. It is This risk gradually returns to a rate of about 2-3% per year.14,15 generally accepted that cerebral ischemia caused by increased Intracranial bleeding represents the most devastating compli- ICP following ICH and SAH compromises the BBB, resulting cation of AVMs. It produces significant morbidity, often in the in early cytotoxic edema and later vasogenic edema. The rap- form of a permanent neurologic deficit. There is considerable id formation of mass effect is a prominent feature of cerebral risk of death, with a mortality rate of approximately 10% from contusion25,26 which is not seen in other pathologic conditions the first hemorrhage.12,13 Several therapies are available for the associated with brain edema. The cellular elements in the cen- treatment of patients with AVMs, including surgery, emboli- tral areas of contusion uniformly undergo disintegration and zation, and radiosurgery.2,16,17 All of these procedures involve a homogenization as the primary consequence of mechanical in- risk of serious complications. Because hemorrhage is the most jury, even early after injury. This can create a pathophysiolo- significant risk in the patient with an AVM, it is important to gical condition in which tissue osmolality increases rapidly in identify the subgroup of patients most likely to develop clini- the core of the contusion and attracts a large amount of water cal bleeding. These patients should be expected to derive grea- within the necrotic tissue27 Nowadays, burr hole aspiration of ter benefit from therapeutic intervention than those who may localized hematoma in hemorrhagic stroke is indicated for not bleed. For the treatment of intracranial arteriovenous mal- all patients with moderate, severe and fulminant types of he- formations(AVMs), one of three established methods or com- morrhage instead of open surgery but not in traumatic ICH binations of them-microsurgery, embolization, and stereotac- usually associated with multiple contusion. This may berre- tic radiosurgery-have been applied.6,18,19 The important prog- lated to the inherent difference between a spontaneous and a nostic factors that affect the outcomes in treating AVMs are traumatic ICH. Decompressive craniectomy may be effective the volume of the nidus and its location along with hemody- in selected patients with aneurysmal ICH, but its widespread namic characteristics of the AVM itself in relation to the sur- use as a standard management of such patients is not support- rounding vasculature.7,18 Friedman et al.20 reported a complete ed because the data is too small to have statistical impact and obliteration rate of 69% after radiosurgery for AVM nidi over give guidelines concerning indications for craniectomy. Vari- 10 cm. Pollock et al .21 reported a 77% complete obliteration ous factors such as surgical manipulation, retraction, and dis- rate in nidi 10 to 15 cm in size and a 25% complete oblitera- turbed venous drainage may be responsible for the develop- tion rate in nidi over 15 cm3 during a follow-up period of 40 ment of intraoperative cerebral swelling. months. Moyamoya Disease Aneurysm Rupture Moyamoya disease (MMD) is a chronic, occlusive cerebro- ICH constitutes a less frequent manifestation of aneurysm vascular disease involving bilateral stenosis or occlusion of rupture than SAH. Its incidence in patients with ruptured an- the terminal portion of the ICAs and/or the proximal portions eurysm varies from 4% to 35%.3,22,23 Certain patterns of collec- of the ACAs and MCAs.28 Moyamoya disease is also charac- tions of blood seem to be related to specific aneurysmal loca- terized by irregular perforating vascular networks, called tions. It is well known that: 1) middle cerebral artery and po- moyamoya vessels, near the occluded or stenotic regions cor- sterior communicating artery aneurysms will predominantly responding to the lenticulostriate and thalamoperforate arter- cause intratemporal clots, with possible extension into the ad- ies. It is this outgrowth of small vessels that produces the ra- jacent lobes; 2) anterior communicating artery aneurysms will diological image of a hazy “puff of smoke” giving the disease most likely produce frontobasal hematomas; and 3) anterior its name, “moyamoya” in Japanese.28 cerebral artery aneurysms will mainly cause interhemispher- The highest known prevalence of MMD is in Japan. This ic clots. Shimoda et al.8 found that favorable outcomes in pa- prevalence corresponds to a rate of newly diagnosed cases in tients with ICH and diffuse SAH was lower than for patients Japan of 0.54 per 100,000 people in 2003.29 The incidence of with ICH alone. They suggested that ICH caused by bleed- MMD in California was only 0.087 per 100,000 from 1987 to ing of aneurysm directly into the brain parenchyma from the 1998, even with a higher Asian population. The adjusted in- sac adhered to the pia mater was fundamentally a subcortical cidence rates by ethnicity were Caucasian 0.06, Asian Amer- hemorrhage. Patients with temporal or frontal hematoma with- ican 0.28, African American 0.13, and Hispanic 0.03.30 Moy- out diffuse SAH from ruptured aneurysm were much better amoya was more prevalent in women than men, with a female tolerated notwithstanding persisting ICP. Kang24 also report- to male ratio of 2:1.29 There was a family history of MMD in ed that it was related to a grave prognostic significance when 12.4% and 11.9% of cases for men and women, respectively.29

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Most autopsy specimens are obtained from adults who anastomosis). Extracranial-intracranial bypass was first per- died of intracranial hemorrhage. Intracerebral hemorrhage is formed in 1972 by Yaşargil. Indirect bypass can involve any often the major cause of death in patients with MMD.31 There of several procedures including encephaloduroarteriosynan- are two main causes of intracranial bleeding: the rupture of giosis, encephalomyosynangiosis, encephalomyoarteriosynan- dilated and fragile moyamoya vessels or rupture of saccular giosis, encephaloarteriosynangiosis, durapexy, multiple cranial aneurysms in the circle of Willis, or on dilated perforators.32 bur holes, and transplantation of omentum.39,40 Direct revascu- Yamashita et al.33 performed autopsies on 22 cadavers and larization has been shown to drastically improve CBF and thus described 2 types of these perforating arteries: the first a dilat- potentially prevent brain infarction.41 Bypass also offloads st- ed artery with a relatively thin wall, and the second a thick- ressed moyamoya vessels, thus potentially decreasing the risk walled artery showing luminal stenosis. The dilated type was of hemorrhage. Direct bypass is generally limited to adults or found to be more prominent in children compared with adults. older children due to the small caliber of the STA in younger The majority of dilated vessels are fibrotic, have attenuated me- children. dia, and often have segmentation of the elastic lamina.34,35 In the stenotic type, vessels show concentric thickening of the intima Conclusion with duplication of the elastic lamina and fibrosis of the tunica media.4,9,33,35 Fibrocellular intimal thickening is responsible for Aneurysm rupture, moyamoya disease, AVM rupture are luminal stenosis in both large and perforating arteries.34,36,37 the common cause of secondary ICH. The morbidity and mor- Histopathologically, the intima of the major arteries shows tality associated with secondary ICH remain high despite re- eccentrically laminated thickening. This thickness is 2 or 3 cent advances in our understanding of the clinical course and times that of normal corresponding vessels and has a wavy ap- pathophysiology of these diseases which cause secondary ICH. pearance representing the discontinuity of the elastica lami- Novel preventive and acute treatment therapies are needed na. These changes in the vessel may predispose to microaneu- and may be on the horizon. rysmal formation. The frequency of aneurysms in the vertebro- basilar system in MMD is much higher than that of the gene- REFERENCES 38 ral population. 1. Fuwa I, Wada H, Matsumoto T. Recurrence of AVM after disappearing The criteria for a diagnosis of MMD have been set forth by on postoperative angiography: report of two cases. No Shinkei Geka the Research Committee on Spontaneous Occlusions of the Cir- 1988;16:887-91. 2. Crawford PM, West CR, Chadwick DW, Shaw MDM. 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