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Moyamoya disease presenting with subarachnoid hemorrhage localized over the frontal cortex: case report
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Surgical Neurology 69 (2008) 197 – 200 www.surgicalneurology-online.com
Vascular
Moyamoya disease presenting with subarachnoid hemorrhage localized over the frontal cortex: case report Toshiya Osanai, MD, Satoshi Kuroda, MD, PhD4, Naoki Nakayama, MD, PhD, Tomohiro Yamauchi, MD, Kiyohiro Houkin, MD, PhD, Yoshinobu Iwasaki, MD, PhD Department of Neurosurgery, Hokkaido University Graduate School of Medicine, Sapporo 060-8638, Japan Received 12 December 2006; accepted 18 January 2007
Abstract
Background: In moyamoya disease, intracranial bleeding is known to occur because of the rupture of saccular aneurysms in the circle of Willis or because of the rupture of dilated, fragile moyamoya vessels. The former causes subarachnoid hemorrhage (SAH), and the latter causes intracerebral or intraventricular hemorrhage. Case Description: In this report, we describe the case of a 34-year-old woman with moyamoya disease who suddenly developed headache and jacksonian seizure. Plain computed tomographic scans on admission revealed SAH localized over the left frontal cortex. The patient was diagnosed with moyamoya disease on cerebral angiography. However, no aneurysm was found on cerebral angiography. Positron emission tomography showed the reduction of CBF and its reactivity to acetazolamide and the elevation of CBV in the left hemisphere. She underwent STA to MCA anastomosis and indirect synangiosis. Intraoperative observations revealed that the pial arterioles were markedly dilated on the brain surface. The CBF in the left hemisphere significantly improved after surgery. The patient has experienced no further episode of cerebral ischemia or intracranial bleeding. Conclusions: Subarachnoid hemorrhage of unknown cause is quite rare in moyamoya disease. Based on the findings in the present case, the dilated collateral arteries on the brain surface may rupture and cause SAH over the cerebral cortex, which is the third cause of intracranial bleeding in patients with persistent cerebral ischemia due to moyamoya disease. D 2008 Elsevier Inc. All rights reserved.
Keywords:
Moyamoya disease; Subarachnoid hemorrhage; Cerebral blood flow; Pial anastomosis; Bypass surgery
1. Introduction Adult patients with moyamoya disease typically present with TIA, cerebral infarction, and intracranial bleeding. Intracerebral or intraventricular hemorrhage usually occurs because of the rupture of the dilated, fragile moyamoya vessels. Alternatively, SAH results from the rupture of saccular aneurysms in the circle of Willis [3,5,6,8,9]. In this report, we describe the rare case of a patient with moyamoya disease who experienced SAH localized only Abbreviations: CBF, cerebral blood flow; CBV, cerebral blood volume; CVR, cerebrovascular reactivity; MCA, middle cerebral artery; PET, positron emission tomography; SAH, subarachnoid hemorrhage; SPECT, single-photon emission computed tomography; STA, superficial temporal artery; TIA, transient ischemic attack. 4 Corresponding author. Tel.: +81 11 706 1161; fax: +81 11 708 7737. E-mail address: [email protected] (S. Kuroda). 0090-3019/$ – see front matter D 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.surneu.2007.01.070
over the frontal cortex. The third cause of intracranial bleeding is discussed, based on radiologic and intraoperative findings in the present case. 2. Case report A 34-year-old healthy woman suddenly complained of headache and developed jacksonian seizure arising from the right side of the face. Plain computed tomographic scans on admission showed that SAH was localized over the left frontal cortex (Fig. 1). She fully recovered after administration of anticonvulsants. Internal carotid angiograms revealed severe stenosis of the bilateral carotid forks and markedly developed moyamoya vessels in the basal ganglia. External carotid angiograms showed vault moyamoya vessels over the left temporal lobe. However, there were no vault moyamoya vessels over the frontal cortex
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Fig. 1. A: Plain computed tomographic scans on admission showed SAH over the left frontal cortex (white arrows). Note that SAH clots were not distributed in the basal cisterns. B: T2*-weighted MRI showed hemosiderin deposits in the sulcus of the left frontal lobe (white arrows).
(Fig. 2). Based on the findings, she was diagnosed as having moyamoya vessels. Positron emission tomographic scans performed 4 weeks later revealed that CBF was reduced and that CBV was elevated in the left hemisphere.
Cerebrovascular reactivity to acetazolamide was also impaired in the left hemisphere (Fig. 3). Hemosiderin deposits were detected only in the cerebral sulcus of the left frontal cortex on T2*-weighted magnetic resonance imag-
Fig. 2. Right (A) and left (B) internal carotid angiograms showed severe stenosis of the carotid forks and development of basal and ethmoidal moyamoya vessels. C: Left external carotid angiograms demonstrated transdural anastomosis over the temporal lobe but not over the frontal lobe.
T. Osanai et al. / Surgical Neurology 69 (2008) 197 – 200
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Fig. 3. A: Preoperative PET scans showed the reduction of CBF and its reactivity to acetazolamide (ACZ) and the elevation of CBV in the left cerebral hemisphere. B: Postoperative SPECT measured 9 months after surgery demonstrated a significant improvement in CBF in the left cerebral hemisphere.
ing (MRI) (Fig. 1). Subsequently, she often experienced transient motor aphasia and underwent left STA to MCA anastomosis and indirect synangiosis [2]. Pial arterioles were markedly dilated on the brain surface, although the operative field did not include the site of SAH (Fig. 4). The frontal and parietal branches were anastomosed to the cortical branches of the MCA, and the brain surface was covered with the temporal muscle and pericranial flaps. Postoperative course was uneventful. Significant improvement of CBF in the left hemisphere was confirmed on SPECT scans taken 6 months after surgery (Fig. 3). She has experienced no further episodes of ischemic or hemorrhagic stroke.
Fig. 4. Intraoperative observations revealed a marked dilatation of the pial arterioles on the brain surface. Arrows indicate the site of STA-MCA anastomosis.
3. Discussion In adult moyamoya disease, saccular aneurysms predominantly occur in the posterior circulation, which plays an essential role as collaterals [5,6,8]. The aneurysms are at high risk for rupture because of increased hemodynamic stress, which are the main causes of SAH in adult moyamoya disease. In such cases, SAH clots are mainly distributed in the basal cisterns. Therefore, the present case is quite rare because SAH was not due to the rupture of an aneurysm, and SAH clots were localized over the frontal cortex. Recent studies have clarified that T2*-weighted MRI can detect microbleeds with high sensitivity in adult patients with moyamoya disease [4,7]. However, the modality could detect old SAH clots over the frontal cortex but not in the basal cisterns in the present case. Importantly, PET scans revealed that both CBF and CVR to acetazolamide were reduced, and CBV was elevated in the left hemisphere. Intraoperative observations showed that the pial arterioles on the brain surface were markedly dilated. After surgery, CBF significantly improved, and the patient has experienced no further episode of ischemic or hemorrhagic stroke. These findings strongly suggest that autoregulatory cerebral vasodilation occurred in response to the reduction of cerebral perfusion pressure in the left hemisphere, but could not keep CBF normal because the cerebral perfusion pressure reduction was too severe [10,11]. Based on these considerations, it is most likely that the markedly dilated, fragile arterioles on the brain surface ruptured because of increased hemodynamic stress, causing SAH over the frontal cortex. To the best of our knowledge, only 2 similar cases have been reported in the literature. Dietrichs et al [1] reported the case of a 21-year-old woman who developed headache and generalized tonic-clonic seizure after delivery. Computed tomographic scans revealed SAH over the left frontal and
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parietal cortex and in the left sylvian fissure. No aneurysms were found on cerebral angiography. Single-photon emission computed tomographic scans revealed that both CBF and CVR to acetazolamide were reduced in the left hemisphere. Her radiologic findings were very similar to those in the present case. Recently, Marushima et al [12] also reported the case of a 38-year-old woman who suddenly developed headache and nausea. Computed tomographic scans detected SAH over the left frontal cortex. No aneurysms were detected on cerebral angiography, but well-developed collateral circulation was found through leptomeningeal anastomosis and transdural anastomosis. Cerebral blood flow was normal in the left hemisphere on SPECT. They hypothesized that SAH occurred because of the rupture of transdural anastomosis vessels. In conclusion, it should be recognized that the dilated collateral arteries on the brain surface may rarely rupture and cause SAH over the cerebral cortex, which is the third cause of intracranial bleeding in patients with persistent cerebral ischemia due to moyamoya disease. Acknowledgments This study was supported by a grant from the Research Committee on Moyamoya Disease sponsored by the Ministry of Health, Labor, and Welfare of Japan (Tokyo). References [1] Dietrichs E, Dahl A, Nyberg-Hansen R, et al. Cerebral blood flow findings in moyamoya disease in adults. Acta Neurol Scand 1992;85: 318 - 322.
[2] Houkin K, Kamiyama H, Takahashi A, et al. Combined revascularization surgery for childhood moyamoya disease: STA-MCA and encephalo-duro-arterio-myo-synangiosis. Childs Nerv Syst 1997;13: 24 - 9. [3] Irikura K, Miyasaka Y, Kurata A, et al. A source of haemorrhage in adult patients with moyamoya disease: the significance of tributaries from the choroidal artery. Acta Neurochir (Wien) 1996;138: 1282 - 6. [4] Ishikawa T, Kuroda S, Nakayama N, et al. Prevalence of asymptomatic microbleeds in patients with moyamoya disease. Neurol Med Chir (Tokyo) 2005;45:495 - 500. [5] Iwama T, Todaka T, Hashimoto N. Direct surgery for major artery aneurysm associated with moyamoya disease. Clin Neurol Neurosurg 1997;99(Suppl 2):S191- 3. [6] Kawaguchi S, Sakaki T, Morimoto T, et al. Characteristics of intracranial aneurysms associated with moyamoya disease. A review of 111 cases. Acta Neurochir (Wien) 1996;138:1287 - 94. [7] Kikuta K, Takagi Y, Nozaki K, et al. Asymptomatic microbleeds in moyamoya disease: T2*-weighted gradient-echo magnetic resonance imaging study. J Neurosurg 2005;102:470 - 5. [8] Kodama N, Suzuki J. Moyamoya disease associated with aneurysm. J Neurosurg 1978;48:565 - 9. [9] Kuroda S, Houkin K, Kamiyama H, et al. Effects of surgical revascularization on peripheral artery aneurysms in moyamoya disease: report of three cases. Neurosurgery 2001;49:463 - 8. [10] Kuroda S, Houkin K, Kamiyama H, et al. Long-term prognosis of medically treated patients with internal carotid or middle cerebral artery occlusion: can acetazolamide test predict it? Stroke 2001;32: 2110 - 6. [11] Kuroda S, Kamiyama H, Abe H, et al. Acetazolamide test in detecting reduced cerebral perfusion reserve and predicting long-term prognosis in patients with internal carotid artery occlusion. Neurosurgery 1993;32:912 - 9. [12] Marushima A, Yanaka K, Matsuki T, et al. Subarachnoid hemorrhage not due to ruptured aneurysm in moyamoya disease. J Clin Neurosci 2006;13:146 - 9.
Surgical Neurology 69 (2008) 197 – 200 www.surgicalneurology-online.com
Vascular
Moyamoya disease presenting with subarachnoid hemorrhage localized over the frontal cortex: case report Toshiya Osanai, MD, Satoshi Kuroda, MD, PhD4, Naoki Nakayama, MD, PhD, Tomohiro Yamauchi, MD, Kiyohiro Houkin, MD, PhD, Yoshinobu Iwasaki, MD, PhD Department of Neurosurgery, Hokkaido University Graduate School of Medicine, Sapporo 060-8638, Japan Received 12 December 2006; accepted 18 January 2007
Abstract
Background: In moyamoya disease, intracranial bleeding is known to occur because of the rupture of saccular aneurysms in the circle of Willis or because of the rupture of dilated, fragile moyamoya vessels. The former causes subarachnoid hemorrhage (SAH), and the latter causes intracerebral or intraventricular hemorrhage. Case Description: In this report, we describe the case of a 34-year-old woman with moyamoya disease who suddenly developed headache and jacksonian seizure. Plain computed tomographic scans on admission revealed SAH localized over the left frontal cortex. The patient was diagnosed with moyamoya disease on cerebral angiography. However, no aneurysm was found on cerebral angiography. Positron emission tomography showed the reduction of CBF and its reactivity to acetazolamide and the elevation of CBV in the left hemisphere. She underwent STA to MCA anastomosis and indirect synangiosis. Intraoperative observations revealed that the pial arterioles were markedly dilated on the brain surface. The CBF in the left hemisphere significantly improved after surgery. The patient has experienced no further episode of cerebral ischemia or intracranial bleeding. Conclusions: Subarachnoid hemorrhage of unknown cause is quite rare in moyamoya disease. Based on the findings in the present case, the dilated collateral arteries on the brain surface may rupture and cause SAH over the cerebral cortex, which is the third cause of intracranial bleeding in patients with persistent cerebral ischemia due to moyamoya disease. D 2008 Elsevier Inc. All rights reserved.
Keywords:
Moyamoya disease; Subarachnoid hemorrhage; Cerebral blood flow; Pial anastomosis; Bypass surgery
1. Introduction Adult patients with moyamoya disease typically present with TIA, cerebral infarction, and intracranial bleeding. Intracerebral or intraventricular hemorrhage usually occurs because of the rupture of the dilated, fragile moyamoya vessels. Alternatively, SAH results from the rupture of saccular aneurysms in the circle of Willis [3,5,6,8,9]. In this report, we describe the rare case of a patient with moyamoya disease who experienced SAH localized only Abbreviations: CBF, cerebral blood flow; CBV, cerebral blood volume; CVR, cerebrovascular reactivity; MCA, middle cerebral artery; PET, positron emission tomography; SAH, subarachnoid hemorrhage; SPECT, single-photon emission computed tomography; STA, superficial temporal artery; TIA, transient ischemic attack. 4 Corresponding author. Tel.: +81 11 706 1161; fax: +81 11 708 7737. E-mail address: [email protected] (S. Kuroda). 0090-3019/$ – see front matter D 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.surneu.2007.01.070
over the frontal cortex. The third cause of intracranial bleeding is discussed, based on radiologic and intraoperative findings in the present case. 2. Case report A 34-year-old healthy woman suddenly complained of headache and developed jacksonian seizure arising from the right side of the face. Plain computed tomographic scans on admission showed that SAH was localized over the left frontal cortex (Fig. 1). She fully recovered after administration of anticonvulsants. Internal carotid angiograms revealed severe stenosis of the bilateral carotid forks and markedly developed moyamoya vessels in the basal ganglia. External carotid angiograms showed vault moyamoya vessels over the left temporal lobe. However, there were no vault moyamoya vessels over the frontal cortex
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T. Osanai et al. / Surgical Neurology 69 (2008) 197 – 200
Fig. 1. A: Plain computed tomographic scans on admission showed SAH over the left frontal cortex (white arrows). Note that SAH clots were not distributed in the basal cisterns. B: T2*-weighted MRI showed hemosiderin deposits in the sulcus of the left frontal lobe (white arrows).
(Fig. 2). Based on the findings, she was diagnosed as having moyamoya vessels. Positron emission tomographic scans performed 4 weeks later revealed that CBF was reduced and that CBV was elevated in the left hemisphere.
Cerebrovascular reactivity to acetazolamide was also impaired in the left hemisphere (Fig. 3). Hemosiderin deposits were detected only in the cerebral sulcus of the left frontal cortex on T2*-weighted magnetic resonance imag-
Fig. 2. Right (A) and left (B) internal carotid angiograms showed severe stenosis of the carotid forks and development of basal and ethmoidal moyamoya vessels. C: Left external carotid angiograms demonstrated transdural anastomosis over the temporal lobe but not over the frontal lobe.
T. Osanai et al. / Surgical Neurology 69 (2008) 197 – 200
199
Fig. 3. A: Preoperative PET scans showed the reduction of CBF and its reactivity to acetazolamide (ACZ) and the elevation of CBV in the left cerebral hemisphere. B: Postoperative SPECT measured 9 months after surgery demonstrated a significant improvement in CBF in the left cerebral hemisphere.
ing (MRI) (Fig. 1). Subsequently, she often experienced transient motor aphasia and underwent left STA to MCA anastomosis and indirect synangiosis [2]. Pial arterioles were markedly dilated on the brain surface, although the operative field did not include the site of SAH (Fig. 4). The frontal and parietal branches were anastomosed to the cortical branches of the MCA, and the brain surface was covered with the temporal muscle and pericranial flaps. Postoperative course was uneventful. Significant improvement of CBF in the left hemisphere was confirmed on SPECT scans taken 6 months after surgery (Fig. 3). She has experienced no further episodes of ischemic or hemorrhagic stroke.
Fig. 4. Intraoperative observations revealed a marked dilatation of the pial arterioles on the brain surface. Arrows indicate the site of STA-MCA anastomosis.
3. Discussion In adult moyamoya disease, saccular aneurysms predominantly occur in the posterior circulation, which plays an essential role as collaterals [5,6,8]. The aneurysms are at high risk for rupture because of increased hemodynamic stress, which are the main causes of SAH in adult moyamoya disease. In such cases, SAH clots are mainly distributed in the basal cisterns. Therefore, the present case is quite rare because SAH was not due to the rupture of an aneurysm, and SAH clots were localized over the frontal cortex. Recent studies have clarified that T2*-weighted MRI can detect microbleeds with high sensitivity in adult patients with moyamoya disease [4,7]. However, the modality could detect old SAH clots over the frontal cortex but not in the basal cisterns in the present case. Importantly, PET scans revealed that both CBF and CVR to acetazolamide were reduced, and CBV was elevated in the left hemisphere. Intraoperative observations showed that the pial arterioles on the brain surface were markedly dilated. After surgery, CBF significantly improved, and the patient has experienced no further episode of ischemic or hemorrhagic stroke. These findings strongly suggest that autoregulatory cerebral vasodilation occurred in response to the reduction of cerebral perfusion pressure in the left hemisphere, but could not keep CBF normal because the cerebral perfusion pressure reduction was too severe [10,11]. Based on these considerations, it is most likely that the markedly dilated, fragile arterioles on the brain surface ruptured because of increased hemodynamic stress, causing SAH over the frontal cortex. To the best of our knowledge, only 2 similar cases have been reported in the literature. Dietrichs et al [1] reported the case of a 21-year-old woman who developed headache and generalized tonic-clonic seizure after delivery. Computed tomographic scans revealed SAH over the left frontal and
200
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parietal cortex and in the left sylvian fissure. No aneurysms were found on cerebral angiography. Single-photon emission computed tomographic scans revealed that both CBF and CVR to acetazolamide were reduced in the left hemisphere. Her radiologic findings were very similar to those in the present case. Recently, Marushima et al [12] also reported the case of a 38-year-old woman who suddenly developed headache and nausea. Computed tomographic scans detected SAH over the left frontal cortex. No aneurysms were detected on cerebral angiography, but well-developed collateral circulation was found through leptomeningeal anastomosis and transdural anastomosis. Cerebral blood flow was normal in the left hemisphere on SPECT. They hypothesized that SAH occurred because of the rupture of transdural anastomosis vessels. In conclusion, it should be recognized that the dilated collateral arteries on the brain surface may rarely rupture and cause SAH over the cerebral cortex, which is the third cause of intracranial bleeding in patients with persistent cerebral ischemia due to moyamoya disease. Acknowledgments This study was supported by a grant from the Research Committee on Moyamoya Disease sponsored by the Ministry of Health, Labor, and Welfare of Japan (Tokyo). References [1] Dietrichs E, Dahl A, Nyberg-Hansen R, et al. Cerebral blood flow findings in moyamoya disease in adults. Acta Neurol Scand 1992;85: 318 - 322.
[2] Houkin K, Kamiyama H, Takahashi A, et al. Combined revascularization surgery for childhood moyamoya disease: STA-MCA and encephalo-duro-arterio-myo-synangiosis. Childs Nerv Syst 1997;13: 24 - 9. [3] Irikura K, Miyasaka Y, Kurata A, et al. A source of haemorrhage in adult patients with moyamoya disease: the significance of tributaries from the choroidal artery. Acta Neurochir (Wien) 1996;138: 1282 - 6. [4] Ishikawa T, Kuroda S, Nakayama N, et al. Prevalence of asymptomatic microbleeds in patients with moyamoya disease. Neurol Med Chir (Tokyo) 2005;45:495 - 500. [5] Iwama T, Todaka T, Hashimoto N. Direct surgery for major artery aneurysm associated with moyamoya disease. Clin Neurol Neurosurg 1997;99(Suppl 2):S191- 3. [6] Kawaguchi S, Sakaki T, Morimoto T, et al. Characteristics of intracranial aneurysms associated with moyamoya disease. A review of 111 cases. Acta Neurochir (Wien) 1996;138:1287 - 94. [7] Kikuta K, Takagi Y, Nozaki K, et al. Asymptomatic microbleeds in moyamoya disease: T2*-weighted gradient-echo magnetic resonance imaging study. J Neurosurg 2005;102:470 - 5. [8] Kodama N, Suzuki J. Moyamoya disease associated with aneurysm. J Neurosurg 1978;48:565 - 9. [9] Kuroda S, Houkin K, Kamiyama H, et al. Effects of surgical revascularization on peripheral artery aneurysms in moyamoya disease: report of three cases. Neurosurgery 2001;49:463 - 8. [10] Kuroda S, Houkin K, Kamiyama H, et al. Long-term prognosis of medically treated patients with internal carotid or middle cerebral artery occlusion: can acetazolamide test predict it? Stroke 2001;32: 2110 - 6. [11] Kuroda S, Kamiyama H, Abe H, et al. Acetazolamide test in detecting reduced cerebral perfusion reserve and predicting long-term prognosis in patients with internal carotid artery occlusion. Neurosurgery 1993;32:912 - 9. [12] Marushima A, Yanaka K, Matsuki T, et al. Subarachnoid hemorrhage not due to ruptured aneurysm in moyamoya disease. J Clin Neurosci 2006;13:146 - 9.