Rare Presentation of Moyamoya Disease with an Acute Subdural Hemorrhage from a Rare Location of Aneurysm-Related Moyamoya Disease

Abstract

Spontaneous acute subdural hematoma is uncommon and usually caused by coagulopathy or other bleeding disorders, malignancy, intracranial hypotension, and abnormal intracranial vessels. We present unique cases of acute spontaneous subdural hematoma from moyamoya disease. There are a few cases reported, and we review previous literature and describe bleeding sources from aneurysms related to moyamoya disease in highly unusual locations.

Keywords

aneurysm-related moyamoya disease - anterior ethmoidal artery - moyamoya disease - subdural hematoma - transdural anastomosis

Introduction

Moyamoya disease (MMD), an uncommon chronic arterial steno-occlusive disorder, affects the anterior circulation near the circle of Willis. Although initially documented in Japan, the occurrence has been recognized in other ethnicities beyond Asia. The clinical manifestation typically comprises either a parenchymal hemorrhagic or ischemic stroke, contingent upon the age of the patient at the moment of presentation. Presenting symptoms consisting solely of subdural hemorrhage are exceedingly uncommon. A literature review and case study are presented regarding subdural hematoma in MMD with identifying bleeding sources from unusual locations.

Case Presentation

A 52-year-old woman experienced a sudden headache while showering, leading to a loss of consciousness. She was sent to a local hospital where she regained consciousness but observed weakness in both legs, making her unable to stand. She refuted any past incidents of head injury or other episodes of similar symptoms. No history of serious medical conditions and currently not on any medicines. Computed tomography (CT) brain scan report indicated a left subdural hematoma overlying the left fronto-temporo-parietal hemisphere. No more investigation was conducted. Upon admission, she had supportive therapy and rehabilitation, resulting in a progressive improvement in her headache and leg weakness. She sought a second opinion at our hospital 6 weeks later, during which time her headache had completely subsided. During the physical assessment, she exhibited bilateral leg weakness graded at 4+ but was able to walk independently. The remainder of the neurological assessment is normal. An acute subdural hematoma was found over the left fronto-temporo-parietal convexity on the reviewed CT brain scan as well as a thin acute subdural hematoma along the left parafalcine, moreover, a hypodense lesion in the right caudate head and right frontal periventricular white matter were also found ([Fig. 1A–E]). Regarding no traumatic history, an acute spontaneous subdural hemorrhage is being considered as the initial diagnosis. Laboratory tests, such as complete blood count and coagulogram, including basic metabolic panel, are within normal limits. In the absence of recent head trauma or use of antithrombotic medication and with normal laboratory results, abnormal intracranial vessels were considered as one of the potential causes. Brain imaging through magnetic resonance imaging (MRI) and magnetic resonance angiography (MRA) was performed. It showed subacute subdural hematoma overlying the left fronto-temporo-parietal hemisphere and old infarction at the right frontal periventricular white matter as seen in the CT brain and subacute hemorrhage also demonstrated with hyposignal intensity in the left gyrus rectus around round shape outpouching lesion, which is suspected as aneurysm ([Fig. 2]). Additionally, the magnetic resonance angiography (MRA) reveals bilateral occlusion of the supraclinoid internal carotid arteries, accompanied by dilated bilateral lenticulostriate arteries that serve as collateral flow. Furthermore, an unruptured aneurysm at the parieto-occipital branch of the left posterior cerebral artery is also observed. When reviewed twice at her initial CT brain, hemorrhage at the left gyrus rectus was already demonstrated but overlooked ([Fig. 1F]). Therefore, the diagnosis of MMD with intracranial aneurysms was made. Cerebral angiography was performed and confirmed findings consistent with those observed on the MRA. It provided additional insights into collateral vessels originating from the bilateral ophthalmic arteries, posterior choroidal arteries, splenial arteries, and cortical vessels of the posterior cerebral arteries. Furthermore, it demonstrated the development of external carotid col lateralization, which is consistent with Suzuki classification grade 4. Notably, the investigation highlighted a culprit intracranial aneurysm in the dilated left anterior ethmoidal artery, responsible for the subdural hematoma. Additionally, an aneurysm at the parieto-occipital branch of the posterior cerebral artery was confirmed, initially suspected by the MRA. ([Fig. 3]). Because of the patient's health insurance coverage, a neurosurgical consultation for revascularization and aneurysm care was performed in a different hospital. After undergoing a sequential superior temporal artery-middle cerebral artery bypass on both sides, the patient has not experienced any problems or aneurysmal rupture.

Fig. 1 Noncontrast computed tomography (CT) brain in axial view demonstrated acute subdural hematoma at the left frontoparietotemporal convexity (A–D) and left parafalcine region (arrow in C–E), which caused mild subfalcine herniation. Acute hematoma at the left gyrus rectus is observed (F). Old infarctions at the right caudate head and right periventricular white matter are detected (arrowhead in B and C). The axial fluid-attenuated inversion recovery (FLAIR) magnetic resonance imaging (MRI) (G, H) and coronal FLAIR MRI (I) showed old infarctions at the right periventricular white matter.

Fig. 2 Coronal maximal intensity projection (MIP) of the contrast-enhanced magnetic resonance angiography (MRA) (A) and coronal fluid-attenuated inversion recovery (FLAIR) fat saturation (FS) (B) over the next 2 months demonstrated a round shape outpouching lesion at the previous hemorrhagic area at the left gyrus rectus, which is suspected as aneurysm.

Fig. 3 Lateral view of the left internal carotid artery (ICA) angiogram in early arterial phase (A) and late arterial phases (B), three-dimensional (3D) left ICA angiogram (C) with axial (D) and coronal (E) maximal intensity projection (MIP) images in the next 2 weeks demonstrated left supraclinoid ICA occlusion with collateral vessels from the left ophthalmic artery, left posterior choroidal artery, left splenial artery, and left posterior cerebral artery (PCA) cortical vessels with intracranial aneurysm of the dilated left anterior ethmoidal artery (arrow). The aneurysm of the left parieto-occipital artery is also detected (arrowhead in A–C). The right supraclinoid ICA occlusion with multiple collateral supplied by the dilated lenticulostriate arteries and parieto-occipital branches of the right PCAs are demonstrated on the right ICA angiogram in anteroposterior (AP) (F) and lateral views (G).

Discussion

The patient experienced a temporary loss of consciousness and weakness in the legs. A subdural hematoma was identified on a CT scan of the brain. The sudden rise in intracranial pressure likely caused these symptoms, while the location of the hematoma close to the parasagittal area could explain the leg weakness. Acute subdural hematoma is often the result of the tearing of bridging veins due to head trauma. In contrast, spontaneous subdural hemorrhage can have various causes such as cortical artery bleeding, arteriovenous malformations, coagulopathy, neoplasms (e.g., meningioma or metastasis), spontaneous intracranial hypotension, cocaine use, and arachnoid cysts.

Our patient does not have any substantial history of head trauma, medical conditions, or surgeries including normal laboratory tests. Her CT brain revealed an acute subdural hematoma, which occurred spontaneously, indicating the need to investigate cerebral vascular pathology unless proven differently. MRA brain and definite cerebral angiogram revealed MMD affecting both internal carotid arteries with grade V according to the Suzuki grading system with the formation of collaterals from the external carotid branches on both sides. In addition, these radiological workups reveal bleeding source of subdural hematoma from ruptured left anterior ethmoidal aneurysm.

The presence of an asymptomatic cerebral infarct in the right periventricular white matter, as observed in both the CT brain and MRI brain, does not indicate infarction from MMD. Infarctions caused by MMD typically exhibit abnormal patterns such as gyral, atypical territorial, or honeycomb patterns.[1] Borderline or lacunar infarct is infrequently observed in MMD. However, if an unusual pattern of infarction is initially detected, it may aid in the consideration of MMD.

MMD is commonly seen in Asia and has a bimodal presentation at around the age of 10 years and the fourth decade of life with more prevalence in women than men and women could have a clinical presentation later than men, our case was a woman in her 50s, compatible with these demographic findings. In adults, MMD usually presents as parenchymal bleeding, while in pediatric patients it presents as transient cerebral ischemia or infarction. Other manifestations such as headache, seizure, or involuntary movement disorders like hemichorea and cognitive deterioration have also been documented. Notably, in the United States,[1] there has been a recent rise in both the occurrence and frequency of MMD.

Hemorrhage in MMD typically occurs in the brain parenchyma most commonly located at the putamen and is followed by lobar hemorrhage that is caused by rupture of fragile moyamoya vessel or basal collateral, which may extend into intraventricular, and the hemorrhage could also be from aneurysmal rupture for which the prognosis maybe worse. Additionally, microbleeds of the brain surrounding the ventricles may contribute to intraventricular hemorrhage. Furthermore, corpus callosum and subarachnoid hemorrhage were reported but with less frequency.

As far as we know, there have been only 11 reported cases[2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12] of MMD with bleeding acutely occurring exclusively in the subdural area ([Table 1]), largely presumed to have originated from transdural anastomosis rupture. But only Matsumura and Nojiri[2] were able to identify a bleeding site during the operation and Umemura[3] identified the middle meningeal artery as the culprit bleeding location with three-dimensional rotational cerebral angiogram. Our case is unique in that subdural hemorrhage originated from aneurysmal-related MMD rupture at the uncommon location from the anterior ethmoidal artery.

Table 1 Reviews of previously reported cases with demographic, clinical presentation, bleeding site and origin, and treatment including the outcome

Authors	Chronicity	Age, gender	Clinical symptoms	Affected side and bleeding origin	Treatment	Outcome
Matsumura and Nojiri[2]	Acute	57, F	Acute on top chronic subdural hematoma, sudden unconscious, and vomiting	-Left frontoparietal -Transdural anastomosis bleeding at middle meningeal artery	Craniotomy	Mild right hemiparesis and motor aphasia
Takeuchi et al[3]	Acute	17, M Juvenile rheumatoid arthritis	Mild head trauma then develops headache, nausea, and vomiting	-Right frontotemporal -Probably transdural anastomosis	Conservation treatment	Improved
Vijayasaradhi and Prasad[4]	Acute	35, M	Headache, vomiting after sneezing followed by brief episode of unconsciousness	-Bilateral frontoparietal subdural hematoma and diffuse subarachnoid hemorrhage -Probably transdural anastomosis	Plan STA-MCA bypass	NA
Umehara et al[5]	Acute	37, F	Impaired consciousness	-Left side subdural hematoma and left basal temporal lobe hematoma -Middle meningeal artery aneurysm	Decompressive craniotomy	MRS 3 at one year
Ghosh[6]	Acute	46, M	Headache, vomiting, decreased level of consciousness	Right	Decompressive craniotomy, evacuation	Good recovery
Oppenheim et al[7]	Acute	57, F	Congestive heart failure, headache, vomiting, altered consciousness	-Left -Rupture vault moyamoya vessel	Blur hole	Good recovery
Nakakita et al[8]	Acute	55, F	Coma	Transdural rupture from subarachnoid and then stretch transdural anastomosis	Evacuation	Not regain consciousness, apallic syndrome
Shen and Lee[9]	Acute	59, F	Headache and vomiting	Bilateral		Dead
Kim et al[10]	Acute	62, F	Sudden severe headache	Left subdural hematoma, subarachnoid hemorrhage and left frontal hematoma	Supportive	Improved
Kato et al[11]	Acute	NA, F	Sudden coma	Subcortical temporoparietal hemorrhage and subdural hematoma	Decompression and evacuation followed by indirect revascularization later	MRS 1 and 1 year
Otsu et al[12]	Acute	24, F	Decreased consciousness	-Right subdural hematoma with temporal lobe intracerebral hemorrhage -aneurysm at middle cranial fossa	Evacuation and decompressive craniotomy	MRS 5

Abbreviations: F, female; M, male; MRS, modified Rankin scale; NA, not applicable; STA-MCA, superior temporal artery-middle cerebral artery.

There are other few reports[13] [14] [15] of MMD presenting with subacute or chronic subdural hematoma for which the bleeding cause would be the same etiology, transdural anastomosis rupture. All MMD, either presenting with acute or subacute, chronic subdural hematomas are at the late-stage grading by Suzuki in which ethmoidal or vault moyamoya vessels are involved. One individual in the acute subdural hematoma group died, while some of the other individuals have not achieved good clinical outcomes. The learning point from our case is if a nontraumatic or spontaneous subdural hematoma is detected without any other known etiology, vascular imaging, either noninvasive or invasive, is required. Moreover, the natural progression of acute subdural hematoma cases form MMD tends to be more severe based on documented cases. Furthermore, treatment of subdural hematoma from MMD needs to be a concern to preserve transdural anastomosis during surgery.

As stenosis or occlusion of the distal internal carotid or middle cerebral arteries progresses in MMD, alterations in blood flow dynamics can result in the development of intracranial aneurysms, with an incidence ranging from 3.4 to 14.8%.[16] This condition also increases the risk of intracranial bleeding. An aneurysm related to MMD systematically described by many authors[16] [17] [18] [19] [20] [21] can develop in the major arteries of the anterior or posterior circulation, which is the most common location among intracranial aneurysms associated with MMD, peripheral arteries such as the anterior or posterior choroidal artery, moyamoya vessels like the lenticulostriate or thalamoperforating artery, meningeal arteries, or at the point of anastomosis. However, there are quite a few cases reporting aneurysm from anterior ethmoidal artery. Treating an aneurysm associated with MMD can be challenging due to the specific location of the aneurysm, which may require either surgical or endovascular intervention.

Conclusion

Adults between the ages of 30 and 50 who have spontaneous subdural hematomas without any other known cause should have vascular pathology evaluated; MMD is one of the possibilities when presenting as subdural hematoma referring to advancing stage of MMD for which extracranial artery involvement and risk of recurrence of cerebral infarct or even cerebral hemorrhage is high. Revascularization may halt or reduce the incidence of recurrence.

Conflict of Interest

None declared.

• References

• 1 Kim JS. Moyamoya disease: epidemiology, clinical features, and diagnosis. J Stroke 2016; 18 (01) 2-11
• 2 Matsumura M, Nojiri K. Resolved chronic subdural hematoma associated with acute subdural hematoma in moyamoya disease [in Japanese]. Neurol Med Chir (Tokyo) 1984; 24 (08) 622-627
• 3 Takeuchi S, Ichikawa A, Koike T, Tanaka R, Arai H. Acute subdural hematoma in young patient with moyamoya disease–case report. Neurol Med Chir (Tokyo) 1992; 32 (02) 80-83
• 4 Vijayasaradhi M, Prasad VB. Moyamoya disease presenting as bilateral acute subdural hematomas without deficits. Asian J Neurosurg 2017; 12 (02) 228-231
• 5 Umehara T, Goto Y, Kajikawa R, Wakayama A, Kishima H. Life-threatening hemorrhagic moyamoya disease: report of rare case of atraumatic acute subdural hematoma due to ruptured transdural anastomosis. World Neurosurg 2018; 118: 16-20
• 6 Ghosh AK. Moyamoya disease presenting with acute subdural hemorrhage. Neurol India 2014; 62 (02) 202-203
• 7 Oppenheim JS, Gennuso R, Sacher M, Hollis P. Acute atraumatic subdural hematoma associated with moyamoya disease in an African-American. Neurosurgery 1991; 28 (04) 616-618
• 8 Nakakita K, Tanaka S, Fukuda A, Fujii C, Kohama A, Miyasato H. Nontraumatic acute subdural hematoma caused by the rupture of transdural anastomotic vessels in moyamoya disease [in Japanese]. No Shinkei Geka 1994; 22 (06) 561-565
• 9 Shen WC, Lee WY. Moyamoya disease causes acute subdural hematomas and sudden death: a case report. Zhonghua Yi Xue Za Zhi (Taipei) 1998; 61 (10) 619-623
• 10 Kim MS, Hur JW, Lee JW, Lee HK. Non-traumatic subdural hematoma in an adult patient with probable moyamoya disease: case report. J Korean Neurosurg Soc 2003; 33 (04) 406-409
• 11 Kato N, Kakizaki S, Hirokawa Y. et al. Encephalo-arterio-synangiosis with cranioplasty after treatment of acute subdural hematoma associated with subcortical hemorrhage due to unilateral moyamoya disease. Case Rep Neurol Med 2023; 2023: 1787738
• 12 Otsu Y, Kikuchi J, Nakahara Y. et al. A ruptured aneurysm of the transdural anastomotic artery occurring at the temporal base in moyamoya disease: case report and literature review. NMC Case Rep J 2024; 11: 79-84
• 13 Kawakami K, Takahashi S, Sonobe M, Koshu K, Hirota S, Kusunose M. Subacute subdural hematoma associated with moyamoya phenomenon–a case report [in Japanese]. No Shinkei Geka 1988; 16 (02) 205-209
• 14 Takeuchi S, Nawashiro H, Uozumi Y. et al. Chronic subdural hematoma associated with moyamoya disease. Asian J Neurosurg 2014; 9 (03) 165-167
• 15 Sasannejad P, Rezaei F, Bidaki R, Zarepur E. Rare presentation of moyamoya disease with sub acute presentation in Iran. Iran J Child Neurol 2018; 12 (01) 89-93
• 16 Zhang L, Xu K, Zhang Y, Wang X, Yu J. Treatment strategies for aneurysms associated with moyamoya disease. Int J Med Sci 2015; 12 (03) 234-242
• 17 Hu Y, Wang X, Li C. et al. Classification and treatment strategy for moyamoya disease-related aneurysms. Chin Neurosurg J 2023; 9 (01) 37
• 18 Yeon JY, Kim JS, Hong SC. Incidental major artery aneurysms in patients with non-hemorrhagic moyamoya disease. Acta Neurochir (Wien) 2011; 153 (06) 1263-1270
• 19 Ni W, Jiang H, Xu B. et al. Treatment of aneurysms in patients with moyamoya disease: a 10-year single-center experience. J Neurosurg 2018; 128 (06) 1813-1822
• 20 Konishi Y, Kadowaki C, Hara M, Takeuchi K. Aneurysms associated with moyamoya disease. Neurosurgery 1985; 16 (04) 484-491
• 21 Otawara Y, Ogasawara K, Seki K, Kibe M, Kubo Y, Ogawa A. Intracerebral hemorrhage after prophylactic revascularization in a patient with adult moyamoya disease. Surg Neurol 2007; 68 (03) 335-337 , discussion 337

Publication History

Article published online:
17 January 2025