Patients with Moyamoya syndrome (MMS) show distal internal carotid artery (ICA) occlusion, similar to patients with Moyamoya disease (MMD); however, MMS is associated with well-recognized underlying diseases, which distinguishes it from MMD.12) Various causes of MMS are recognized, including neurofibromatosis type 1, Down's syndrome, thyroid disease, and cranial irradiation.9) MMS with tuberculous meningitis (TBM) is rare.5)14) Intracranial aneurysms associated with MMD occasionally occur (3–14% of MMD patients),1) and aneurysm rupture has been frequently reported.2)4) However, the middle meningeal artery (MMA) is a rare location for aneurysms in MMD, and few cases of MMA aneurysmal rupture and hemorrhage have been reported.8) Moreover, MMA aneurysm rupture in patients with MMS is more rare than in MMD and has not been reported, especially related to TBM. Here, we present a delayed manifestation of MMS after TBM, presenting with an intracerebral hemorrhage as a result of MMA aneurysmal rupture.

A 38-year-old unconscious female with left hemiplegia was admitted to out hospital. The neurologic evaluation on admission revealed that her consciousness level was drowsy (Glasgow coma scale 14, eye opening 3, verbal response 5, motor response 6), and motor grade was I on the left side. The patient had a history of TBM at the age of one, and she suffered from mental retardation as a consequence of the TBM. Except for mental retardation, no neurologic deficits were noted prior to the hemorrhage, and cerebral angiography had never been performed. Brain computed tomography (CT) scan disclosed a 35 mL hematoma in the right temporo-parietal lobe and an intraventricular hemorrhage (IVH) from the right lateral ventricle to the 4th ventricle (Fig. 1A). CT angiography revealed a saccular aneurysm, presumed to be the origin of the hemorrhage, at the right temporal area and hypotrophy of the branches of the right middle cerebral artery with M1 occlusion. For further evaluation, digital subtraction angiography was performed. The right distal ICA was occluded proximal to the ophthalmic artery with basal collaterals on the right common carotid artery (Fig. 1B, C). A small aneurysm was seen at the petrous branch of the right MMA. Angiography of the left common carotid artery revealed the left distal ICA and middle cerebral artery vessels to be patent, and the right middle cerebral artery and the anterior cerebral artery received blood supply through the anterior communicating artery channel (Fig. 1D).

MMS has a variety of risk factors, including infectious meningitis and especially TBM.14) TBM is caused by Mycobacterium tuberculosis and frequently affects children under 4 years of age.13) In vessel studies of TBM patients, ICA stenosis is characteristically observed, which is assumed to be the result of chronic and repetitive inflammation of the brain parenchyme and great arteries. Subsequent to the ICA stenosis, demand for perfusion flow induces development of collateral vessels in ischemic areas, which might be the cause of hemorrhage with significant neurologic deficit.5)7)10) Pinardi et al.10) reviewed several cases of post-infectious Moyamoya disease, including cases of MMD caused by Mycobacterium tuberculosis infection. Nakayama et al.7) reported a case of intracerebral hemorrhage with Moyamoya phenomenon caused by tuberculous arteritis.

MMA aneurysms associated with MMD have been reported in previous studies. Borota et al.1) reported a case with a saccular aneurysm at the MMA posterior branch with subarachnoid hemorrhage and subdural hemorrhage, and the patient died 4 days after surgery. Park et al.8) presented experiences of repeated MMA aneurysm rupture in an MMD patient treated with craniotomy and aneurysmal neck clipping.

However, MMA aneurysms are less common in patients with MMS than in patients with MMD, and only one case of pure intracerebral hemorrhage following a ruptured MMA aneurysm in an MMS patient has been reported.3) In the study of Koebbe and Horowitz,3) an MMS patient with Down's syndrome had an aneurysm located in a collateral branch between the MMA and occipital arteries, and the patient was treated with an endovascular approach by occlusion of the parent branch.

Peripheral artery aneurysms in MMD have been sporadically reported, and most are confirmed on pathologic examination as false aneurysms, also known as pseudoaneurysms. The arterial walls are completely disrupted and are often contained only by a cavitated clot. Since the walls contain collagen and fibrin without elastic fibers, the aneurysms have a tendency to rapidly grow in the early stage.1)11) Because peripheral pseudoaneurysms have fragile walls and tend to repeatedly bleed and rapidly grow, immediate treatment is essential. The MMA and its dural branches play important roles in collateral blood supply in both MMD and MMS,6) and both neurosurgeons and neuro-interventionists should consider the increased MMA flow during treatment to prevent ischemic complications. Both surgical excision and endovascular embolization could be excellent treatment options for a ruptured aneurysm, and treatment options should be carefully selected under multidisciplinary considerations regarding the patient's neurologic status, coexisting brain lesions such as ICH and IVH, and collateral vessel involvement. In this study, we chose surgical treatment for aneurysmal occlusion because removing the ICH and draining the hydrocephalus were helpful in the patient's recovery. The patient's life was saved, but the motor weakness on her left side remained.

We reported our experience with a very rare case of ruptured MMA pseudoaneurysm associated with MMS in a patient with TBM. It is helpful to evaluate the cerebral vessels with an imaging modality for lowering the mortality and morbidity of patients with TBM. Early detection of vascular changes, including aneurysm formation, may prevent more significant neurologic complications.