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Mechanism of intracranial rebleeding in Moyamoya disease
Clinical Neurology and Neurosurgery 99 Suppl. 2 (1997) S187 – S190
Mechanism of intracranial rebleeding in Moyamoya disease Toru Iwama *, Masafumi Morimoto, Nobuo Hashimoto, Yasunobu Goto, Tatemi Todaka, Motoshi Sawada Department of Neurosurgery, National Cardio6ascular Center, 5 – 7 – 1 Fujishirodai, Suita, Osaka 565, Japan
Abstract Intracranial hemorrhage is the major catastrophic event in the natural course of Moyamoya disease, and outcome of the patients with rebleeding is very poor. However, the mechanism underlying intracranial rebleeding is not well elucidated. We retrospectively analyzed 15 patients who bled two times or more among 46 bled patients with Moyamoya disease. The results indicated that there were two different types in the manner of rebleeding. One group consisted of seven cases, which bled two times or more at the same site than the original bleeding site. In four of these seven cases, a ruptured aneurysm was identified at the distal part of collateral vessel or on the major vessel. In the other three cases, no source of bleeding was identified. In all of these cases, rebleeding occurred within 2 months after the initial insult except for one case. Another group consisted of eight cases, which bled repeatedly but at different sites from the initial bleeding site. In any of these cases, neither aneurysms nor other vascular abnormalities were identified. In all of these cases, rebleeding occurred more than 2 months after the initial bleeding. The present result indicated that intracranial bleeding might occur as a result of rupture of a tiny aneurysm at the periphery of collateral vessels. These aneurysms may be blown out after the initial bleeding. When they persist after the event, they may rupture again in a fairly short interval. In other cases, bleeding occur at different sites from the initial site. They are considered to be a result of ruptured weak Moyamoya vessels which are forced to act as collateral pathways and are under unusually increased hemodynamic stress. © 1997 Elsevier Science B.V. Keywords: Aneurysm; Extracranial/intracranial bypass surgery; Hemodynamic stress; Moyamoya disease; Rebleeding
1. Introduction Patients with Moyamoya disease generally presented with cerebral ischemia in childhood and intracranial bleeding in adulthood. Increased hemodynamic stress is thought to result in a rupture of tiny small vessels which act as collateral channels in place of the stenotic internal carotid arteries [1,2]. Because the outcome of the patients with rebleeding is very poor, extracranial/ intracranial (EC/IC) bypass surgery has been performed in patients with hemorrhage as well as those with ischemia in an attempt to decrease the hemodynamic stress on the collateral channels [3,4]. However, the efficacy of bypass surgery in the prevention of intracranial bleeding remains unclear [3,4]. To discuss * Corresponding author. Tel.: +81 6 8335012; fax: + 81 6 8727486. 0303-8467/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PII S 0 3 0 3 - 8 4 6 7 ( 9 7 ) 0 0 0 8 0 - 2
the efficacy of surgery, it is considered that the mechanism of rebleeding should be resolved. To elucidate the mechanism of rebleeding in Moyamoya disease, we retrospectively analyzed 15 patients who bled twice or more among 46 patients with an episode of intracranial bleeding.
2. Clinical materials and methods Of 196 patients with Moyamoya disease who were treated at our institute over the last 17 years, 46 (23.5%) had episodes of intracranial bleeding. Their mean age at the time bleeding occurred was 37.4 years (range 7–61 years). Of these 46 patients, 21 episodes of repeat hemorrhage occurred in 15 patients; 11 patients bled twice, three bled three times and the remaining one patient bled five times. Twelve episodes occurred before
S188
T. Iwama et al. / Clinical Neurology and Neurosurgery 99 Suppl. 2 (1997) S187–S190
Fig. 1. This 35-year-old female had intraventricular hemorrhage twice with an interval of one day. A computed tomography obtained after ventricular drainage (a) demonstrating intraventricular clot and a high density spot next to the corpus of right lateral ventricle (arrow). The lateral view of right carotid angiogram (b) showing an aneurysm at the distal part of a collateral vessel (arrow). The high density spot on CT corresponds to the aneurysm.
surgical treatment and nine occurred after bypass surgery. The sites of bleeding, intervals to rebleeding, neuroradiological findings, treatments and outcomes were analyzed. All of the patients were followed up at our outpatient clinic; the mean follow-up period was 44.8 months (range: 6 – 163 months).
3. Results
3.1. Types of rebleeding Comparison between computed tomography (CT) findings at the time of initial bleeding and those of at the time of rebleeding indicated that there were two different types in the manner of rebleeding. One was rebleeding at the same site and in the same mode to those of the initial bleeding. Such rebleeding was thought to be from the same source as the initial bleeding. The other was rebleeding at a different site. Cases with repeat primary intraventricular hemorrhage (IVH) in which distribution of clot was obviously different from the initial one was included in the group of rebleeding at a different site. Rebleeding at the same site was seen eight times in seven patients. Rebleeding at a different site was seen 13 times in eight patients. In each of the four patients who bled three times or more, the type of rebleeding was the same through their courses.
3.2. Rebleeding at the same site The mean age of the seven patients with rebleeding at the same site was 42.4 years (range 27 – 61 years). All
were female. The mode of bleeding was primary IVH in four patients, subarachnoid hemorrhage (SAH) in two patients and intracerebral hemorrhage (ICH) in one patient. Rebleeding of this type was counted eight times. All but one of such rebleeding occurred within 2 months after the first bleeding episode and all episodes happened before surgical treatment. A ruptured aneurysm was recognized in four patients who subsequently underwent simultaneous direct surgery to the ruptured aneurysm and EC/IC bypass surgery. The location of the aneurysm was at the distal part of the collateral vessel or Moyamoya vessel in three patients (Fig. 1) and at the A1 –A2 junction in one patient. In two patients without an aneurysm, EC/IC bypass surgery was performed. The remaining one patient died of massive rebleeding before surgical treatment. None of the six surviving patients experienced bleeding during the postoperative follow-up period. The outcomes at the final follow-up scored well in three patients, moderately disabled in two and persistent vegetative state in one patient.
3.3. Rebleeding at a different site The mean age of the eight patients with rebleeding at a different site was 36.6 years (range 10–58 years). They were two males and six females. The mode of initial bleeding was ICH in five patients and IVH in two patients. No ruptured aneurysms were recognized in these eight patients, although one patient had an unruptured aneurysm on the basilar artery at the junction of the superior cerebellar artery. Rebleeding of this type occurred 13 times between 3 and 122 months after the previous bleeding episode. These rebleeding were
T. Iwama et al. / Clinical Neurology and Neurosurgery 99 Suppl. 2 (1997) S187–S190
S189
Fig. 2. This 46-year-old female presented with a sudden headache and a computed tomography (a) revealed to have intracerebral hemorrhage at the left caudate nucleus. Seven years after the first bleeding, she bled again at the right thalamus (b).
ten ICH and three IVH (Fig. 2). They were seen before surgical treatment in three patients and after bypass surgery in seven patients. In these seven patients with postoperative rebleeding, bypass surgery was done bilaterally in one and unilaterally in six patients. Postoperative rebleeding occurred ipsilaterally to the surgery in three patients and contralaterally in four patients. In all of these seven patients Moyamoya vessels were not decreased on the follow-up angiograms despite the patency of the bypass. Two patients died of intracranial rebleeding. The outcomes of the six surviving patients scored well in two, moderately disabled in two and severely disabled in two patients.
4. Discussion Prevention of rebleeding is one of the major goals in the treatment of Moyamoya disease. Although patients who experience rebleeding tend to have worse outcomes [2,4], there have been few studies on rebleeding in Moyamoya disease. To prevent rebleeding, the mechanism of rebleeding should be solved. By reviewing 15 patients who bled twice or more, we found that there were two types of rebleeding in Moyamoya disease. Rebleeding at the same site as the original bleeding was seen in seven of our patients. A ruptured aneurysm was identified at the periphery of the Moyamoya vessels in three patients and at the major artery in one patient. Although no aneurysm was detected in the other three patients, it is probable that a small aneurysm ruptured and was blown away. SAH and primary IVH were predominant in these patients and these rebleeding
episodes occurred within 2 months of the initial bleeding in all but one patient. It is suggested that this bleeding occurs and repeats as a result of a rupture of a tiny aneurysm [6]. In patients whose rebleeding stems from SAH or primary IVH, a careful search for an associated aneurysm is advisable. If an aneurysm is detected and considered to be ruptured, early direct surgery to the aneurysm should be performed to prevent further bleeding [5]. Rebleeding at a different site was seen in eight of our patients. In contrast to the cases with rebleeding at the same site, neither aneurysms nor other vascular abnormalities which was suggested to be a source of bleeding were identified in any of these cases. Such rebleeding at a different site occurred more than 2 months after the previous bleeding episode. These features were different from those observed in patients with rebleeding at the same site, indicating different mechanism of rebleeding in these cases. Such bleeding can occur as a result of rupture of another collateral vessel which has been exposed to unusual hemodynamic stress [1,2]. Of 15 patients with repeat bleeding, we performed EC/IC bypass surgery in 14 patients in an attempt to reduce the hemodynamic stress on Moyamoya vessels and to prevent further bleeding. However, seven patients bled at a different site after bypass surgery. In all of these seven patients, angiograms revealed that filling of the MCA branches via the bypass was minimal and the Moyamoya vessels were not decreased despite patency of the bypasses. Of 31 patients with single episode of bleeding, we performed EC/IC bypass surgery in 30 patients and follow-up angiography was done in 22 patients. Of 28 patients who did not bleed after surgery
T. Iwama et al. / Clinical Neurology and Neurosurgery 99 Suppl. 2 (1997) S187–S190
S190
and who underwent follow-up angiography, 20 evidenced regression of the Moyamoya vessels and a satisfactory flow through the bypass. This suggests that patients with developed collateral circulation following EC/IC bypass surgery are at lower risk for postoperative rebleeding than are patients with a poorly developed collateral circulation. Thus, bypass surgery may be effective in the prevention of rebleeding when the bypass establishes sufficient collateral channels. While there is a subgroup of patients in whom the collateral circulation is not well developed despite patency of the bypass. In such cases, bypass surgery is not considered to be effective to reduce the risk of rebleeding. This difference should be more clearly elucidated.
.
.
References [1] Oka K, Yamashita M, Sadoshima S, Tanaka K. Cerebral haemorrhage in Moyamoya disease at autopsy. Virchows Arch [Pathol Anat] 1981;392:247 – 61. [2] Yamashita M, Oka K, Tanaka K. Histopathology of the brain vascular network in Moyamoya disease. Stroke 1983;14:50–8. [3] Karasawa J, Kikuchi H, Furuse S, Kawamura J, Sakaki T. Treatment of Moyamoya disease with STA-MCA anastomosis. J Neurosurg 1978;49:679 – 88. [4] Yonekawa Y, Okuno T, Handa H. ‘Moyamoya’ disease: clinical review and surgical treatment. In: Fein JM, Flamm ES, editors. Cerebrovascular Surgery II. New York: Springer-Verlag, 1985:557 – 580. [5] Hamada J, Hashimoto N, Tsukahara T. Moyamoya disease with repeated intraventricular hemorrhages due to rupture of aneurysm: report of two cases. J Neurosurg 1994;80:328 – 31. [6] Konishi Y, Kadowaki C, Hara M, Takeuchi K. Aneurysms associated with Moyamoya disease. Neurosurgery 1985;16:484–90.
Mechanism of intracranial rebleeding in Moyamoya disease Toru Iwama *, Masafumi Morimoto, Nobuo Hashimoto, Yasunobu Goto, Tatemi Todaka, Motoshi Sawada Department of Neurosurgery, National Cardio6ascular Center, 5 – 7 – 1 Fujishirodai, Suita, Osaka 565, Japan
Abstract Intracranial hemorrhage is the major catastrophic event in the natural course of Moyamoya disease, and outcome of the patients with rebleeding is very poor. However, the mechanism underlying intracranial rebleeding is not well elucidated. We retrospectively analyzed 15 patients who bled two times or more among 46 bled patients with Moyamoya disease. The results indicated that there were two different types in the manner of rebleeding. One group consisted of seven cases, which bled two times or more at the same site than the original bleeding site. In four of these seven cases, a ruptured aneurysm was identified at the distal part of collateral vessel or on the major vessel. In the other three cases, no source of bleeding was identified. In all of these cases, rebleeding occurred within 2 months after the initial insult except for one case. Another group consisted of eight cases, which bled repeatedly but at different sites from the initial bleeding site. In any of these cases, neither aneurysms nor other vascular abnormalities were identified. In all of these cases, rebleeding occurred more than 2 months after the initial bleeding. The present result indicated that intracranial bleeding might occur as a result of rupture of a tiny aneurysm at the periphery of collateral vessels. These aneurysms may be blown out after the initial bleeding. When they persist after the event, they may rupture again in a fairly short interval. In other cases, bleeding occur at different sites from the initial site. They are considered to be a result of ruptured weak Moyamoya vessels which are forced to act as collateral pathways and are under unusually increased hemodynamic stress. © 1997 Elsevier Science B.V. Keywords: Aneurysm; Extracranial/intracranial bypass surgery; Hemodynamic stress; Moyamoya disease; Rebleeding
1. Introduction Patients with Moyamoya disease generally presented with cerebral ischemia in childhood and intracranial bleeding in adulthood. Increased hemodynamic stress is thought to result in a rupture of tiny small vessels which act as collateral channels in place of the stenotic internal carotid arteries [1,2]. Because the outcome of the patients with rebleeding is very poor, extracranial/ intracranial (EC/IC) bypass surgery has been performed in patients with hemorrhage as well as those with ischemia in an attempt to decrease the hemodynamic stress on the collateral channels [3,4]. However, the efficacy of bypass surgery in the prevention of intracranial bleeding remains unclear [3,4]. To discuss * Corresponding author. Tel.: +81 6 8335012; fax: + 81 6 8727486. 0303-8467/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PII S 0 3 0 3 - 8 4 6 7 ( 9 7 ) 0 0 0 8 0 - 2
the efficacy of surgery, it is considered that the mechanism of rebleeding should be resolved. To elucidate the mechanism of rebleeding in Moyamoya disease, we retrospectively analyzed 15 patients who bled twice or more among 46 patients with an episode of intracranial bleeding.
2. Clinical materials and methods Of 196 patients with Moyamoya disease who were treated at our institute over the last 17 years, 46 (23.5%) had episodes of intracranial bleeding. Their mean age at the time bleeding occurred was 37.4 years (range 7–61 years). Of these 46 patients, 21 episodes of repeat hemorrhage occurred in 15 patients; 11 patients bled twice, three bled three times and the remaining one patient bled five times. Twelve episodes occurred before
S188
T. Iwama et al. / Clinical Neurology and Neurosurgery 99 Suppl. 2 (1997) S187–S190
Fig. 1. This 35-year-old female had intraventricular hemorrhage twice with an interval of one day. A computed tomography obtained after ventricular drainage (a) demonstrating intraventricular clot and a high density spot next to the corpus of right lateral ventricle (arrow). The lateral view of right carotid angiogram (b) showing an aneurysm at the distal part of a collateral vessel (arrow). The high density spot on CT corresponds to the aneurysm.
surgical treatment and nine occurred after bypass surgery. The sites of bleeding, intervals to rebleeding, neuroradiological findings, treatments and outcomes were analyzed. All of the patients were followed up at our outpatient clinic; the mean follow-up period was 44.8 months (range: 6 – 163 months).
3. Results
3.1. Types of rebleeding Comparison between computed tomography (CT) findings at the time of initial bleeding and those of at the time of rebleeding indicated that there were two different types in the manner of rebleeding. One was rebleeding at the same site and in the same mode to those of the initial bleeding. Such rebleeding was thought to be from the same source as the initial bleeding. The other was rebleeding at a different site. Cases with repeat primary intraventricular hemorrhage (IVH) in which distribution of clot was obviously different from the initial one was included in the group of rebleeding at a different site. Rebleeding at the same site was seen eight times in seven patients. Rebleeding at a different site was seen 13 times in eight patients. In each of the four patients who bled three times or more, the type of rebleeding was the same through their courses.
3.2. Rebleeding at the same site The mean age of the seven patients with rebleeding at the same site was 42.4 years (range 27 – 61 years). All
were female. The mode of bleeding was primary IVH in four patients, subarachnoid hemorrhage (SAH) in two patients and intracerebral hemorrhage (ICH) in one patient. Rebleeding of this type was counted eight times. All but one of such rebleeding occurred within 2 months after the first bleeding episode and all episodes happened before surgical treatment. A ruptured aneurysm was recognized in four patients who subsequently underwent simultaneous direct surgery to the ruptured aneurysm and EC/IC bypass surgery. The location of the aneurysm was at the distal part of the collateral vessel or Moyamoya vessel in three patients (Fig. 1) and at the A1 –A2 junction in one patient. In two patients without an aneurysm, EC/IC bypass surgery was performed. The remaining one patient died of massive rebleeding before surgical treatment. None of the six surviving patients experienced bleeding during the postoperative follow-up period. The outcomes at the final follow-up scored well in three patients, moderately disabled in two and persistent vegetative state in one patient.
3.3. Rebleeding at a different site The mean age of the eight patients with rebleeding at a different site was 36.6 years (range 10–58 years). They were two males and six females. The mode of initial bleeding was ICH in five patients and IVH in two patients. No ruptured aneurysms were recognized in these eight patients, although one patient had an unruptured aneurysm on the basilar artery at the junction of the superior cerebellar artery. Rebleeding of this type occurred 13 times between 3 and 122 months after the previous bleeding episode. These rebleeding were
T. Iwama et al. / Clinical Neurology and Neurosurgery 99 Suppl. 2 (1997) S187–S190
S189
Fig. 2. This 46-year-old female presented with a sudden headache and a computed tomography (a) revealed to have intracerebral hemorrhage at the left caudate nucleus. Seven years after the first bleeding, she bled again at the right thalamus (b).
ten ICH and three IVH (Fig. 2). They were seen before surgical treatment in three patients and after bypass surgery in seven patients. In these seven patients with postoperative rebleeding, bypass surgery was done bilaterally in one and unilaterally in six patients. Postoperative rebleeding occurred ipsilaterally to the surgery in three patients and contralaterally in four patients. In all of these seven patients Moyamoya vessels were not decreased on the follow-up angiograms despite the patency of the bypass. Two patients died of intracranial rebleeding. The outcomes of the six surviving patients scored well in two, moderately disabled in two and severely disabled in two patients.
4. Discussion Prevention of rebleeding is one of the major goals in the treatment of Moyamoya disease. Although patients who experience rebleeding tend to have worse outcomes [2,4], there have been few studies on rebleeding in Moyamoya disease. To prevent rebleeding, the mechanism of rebleeding should be solved. By reviewing 15 patients who bled twice or more, we found that there were two types of rebleeding in Moyamoya disease. Rebleeding at the same site as the original bleeding was seen in seven of our patients. A ruptured aneurysm was identified at the periphery of the Moyamoya vessels in three patients and at the major artery in one patient. Although no aneurysm was detected in the other three patients, it is probable that a small aneurysm ruptured and was blown away. SAH and primary IVH were predominant in these patients and these rebleeding
episodes occurred within 2 months of the initial bleeding in all but one patient. It is suggested that this bleeding occurs and repeats as a result of a rupture of a tiny aneurysm [6]. In patients whose rebleeding stems from SAH or primary IVH, a careful search for an associated aneurysm is advisable. If an aneurysm is detected and considered to be ruptured, early direct surgery to the aneurysm should be performed to prevent further bleeding [5]. Rebleeding at a different site was seen in eight of our patients. In contrast to the cases with rebleeding at the same site, neither aneurysms nor other vascular abnormalities which was suggested to be a source of bleeding were identified in any of these cases. Such rebleeding at a different site occurred more than 2 months after the previous bleeding episode. These features were different from those observed in patients with rebleeding at the same site, indicating different mechanism of rebleeding in these cases. Such bleeding can occur as a result of rupture of another collateral vessel which has been exposed to unusual hemodynamic stress [1,2]. Of 15 patients with repeat bleeding, we performed EC/IC bypass surgery in 14 patients in an attempt to reduce the hemodynamic stress on Moyamoya vessels and to prevent further bleeding. However, seven patients bled at a different site after bypass surgery. In all of these seven patients, angiograms revealed that filling of the MCA branches via the bypass was minimal and the Moyamoya vessels were not decreased despite patency of the bypasses. Of 31 patients with single episode of bleeding, we performed EC/IC bypass surgery in 30 patients and follow-up angiography was done in 22 patients. Of 28 patients who did not bleed after surgery
T. Iwama et al. / Clinical Neurology and Neurosurgery 99 Suppl. 2 (1997) S187–S190
S190
and who underwent follow-up angiography, 20 evidenced regression of the Moyamoya vessels and a satisfactory flow through the bypass. This suggests that patients with developed collateral circulation following EC/IC bypass surgery are at lower risk for postoperative rebleeding than are patients with a poorly developed collateral circulation. Thus, bypass surgery may be effective in the prevention of rebleeding when the bypass establishes sufficient collateral channels. While there is a subgroup of patients in whom the collateral circulation is not well developed despite patency of the bypass. In such cases, bypass surgery is not considered to be effective to reduce the risk of rebleeding. This difference should be more clearly elucidated.
.
.
References [1] Oka K, Yamashita M, Sadoshima S, Tanaka K. Cerebral haemorrhage in Moyamoya disease at autopsy. Virchows Arch [Pathol Anat] 1981;392:247 – 61. [2] Yamashita M, Oka K, Tanaka K. Histopathology of the brain vascular network in Moyamoya disease. Stroke 1983;14:50–8. [3] Karasawa J, Kikuchi H, Furuse S, Kawamura J, Sakaki T. Treatment of Moyamoya disease with STA-MCA anastomosis. J Neurosurg 1978;49:679 – 88. [4] Yonekawa Y, Okuno T, Handa H. ‘Moyamoya’ disease: clinical review and surgical treatment. In: Fein JM, Flamm ES, editors. Cerebrovascular Surgery II. New York: Springer-Verlag, 1985:557 – 580. [5] Hamada J, Hashimoto N, Tsukahara T. Moyamoya disease with repeated intraventricular hemorrhages due to rupture of aneurysm: report of two cases. J Neurosurg 1994;80:328 – 31. [6] Konishi Y, Kadowaki C, Hara M, Takeuchi K. Aneurysms associated with Moyamoya disease. Neurosurgery 1985;16:484–90.