AUTHOR(S): Matsushima, T., M.D.; Inoue, T., M.D.; Suzuki, S. O., M.D.; Fujii, K., M.D.; Fukui, M., M.D.; Hasuo, K., M.D. Department of Neurosurgery, Neurological Institute (TM, TI, SOS, KF, MF), and Department of Radiology (KH), Faculty of Medicine, Kyushu University, Fukuoka, Japan Neurosurgery 31; 401-405, 1992 ABSTRACT: EITHER ENCEPHALODUROARTERIOSYNANGIOSIS (EDAS) or superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis combined with encephalomyosynangiosis (EMS) has been performed on most of the children with moyamoya disease in our department. EDAS alone was done in the parietal region of 13 sides in 10 patients, and STAMCA anastomosis with EMS in the parietal region was done on 7 sides in 6 patients. The surgical results of these two different procedures were then compared. Postoperative collateral formation was observed on external carotid angiograms, and the improvement of clinical symptoms was monitored for 1 year after the bypass procedure. STA-MCA anastomosis with EMS was found to be superior to EDAS in both the development of collateral circulation (P < 0.05) and postoperative clinical improvement (P < 0.01). EDAS can be done easily and safely on small children with moyamoya disease, but STA-MCA anastomosis with EMS is considered to be more appropriate, whenever possible. KEY WORDS: Indirect nonanastomotic or direct anastomotic extracranial-to-intracranial bypass procedure; Moyamoya disease; Pediatric case; Surgical treatment Surgical treatment for pediatric patients with moyamoya disease has now become popular. It aims at establishing an efficient collateral circulation for the ischemic brain. Various techniques such as superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis (4,5,7,15), encephalomyosynangiosis (EMS) (3,4,6,9,18), and encephaloduroarteriosynangiosis (EDAS) (9-13,16) have been used. These modalities can basically be divided into direct and indirect revascularization procedures. A controversy has arisen, however, regarding the comparison of the effects of the two different surgical procedures. No detailed comparisons of direct and indirect revascularization procedures done at one institution have been done to date. We have operated on pediatric patients with moyamoya disease, first using EDAS and later STA-
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MCA anastomosis in recent cases. The results of these two different surgical procedures are presented and compared. MATERIALS AND METHODS Forty Japanese children were diagnosed and surgically treated at the Department of Neurosurgery, Kyushu University Hospital. Four different types of single or combined surgical procedures were used. We basically used EDAS in the parietal region during the period from 1983 to 1986, whereas STA-MCA anastomosis with EMS was mainly performed during the past 4 years, since 1987 (Fig. 1). In some recent cases, encephalomyoarteriosynangiosis was added to obtain a collateral formation in the anterior cerebral artery distribution. EDAS was performed above the ear, as described by Matsushima et al. (11-13) (Fig. 1, A and B). We first separated the posterior branch of the superficial temporal artery (STA) and the surrounding connective tissue without dividing the trunk and then sutured it to the edges of the exposed and incised dura mater. In STA-MCA anastomosis with EMS, we performed a wide craniotomy in the parietotemporal region and performed STA-MCA anastomosis (Fig. 1, A and C). The exposed frontoparietotemporal cortices and the anastomosed arteries were then covered with the temporal muscle instead of the dura mater. We used 11-0 monofilament nylon sutures for the anastomosis because arteries in children with moyamoya disease are very small, thin, and fragile, like veins. In the study presented here, the children who underwent only one of the two following procedures-EDAS alone and STA-MCA anastomosis with EMS in the parietal region-- were selected as representatives of indirect and direct procedures, respectively. The patients who received encephalomyoarteriosynangiosis in the frontal region were excluded because it was often found to influence the effects of EDAS and STA-MCA anastomosis in the parietal region. Ten patients (13 sides) received EDAS in the parietal region alone, whereas 6 patients (7 sides) received only STA-MCA anastomosis with EMS (Table 1). Table 2 shows the age at onset, clinical types, preoperative duration, and preoperative angiographic staging of the patients in each group. The angiographic staging described by Suzuki and Takaku (17) was used to estimate the preoperative angiographic findings. Their distribution was measured by the χ2 test, and the differences between the mean values of the parameters investigated were measured by Student's t test. The two groups were not significantly different regarding four preoperative factors. Their postoperative collateral formation and development of the clinical symptoms were studied by postoperative external carotid angiography and a postoperative clinical chart. Postoperative angiography and a follow-up examination were done during the period from 6 months to 1 year after bypass surgery. RESULTS Angiographic results Postoperative collateral formation was studied by
Redistribution of this article permitted only in accordance with the publisher’s copyright provisions.
Neurosurgery 1992-98 September 1992, Volume 31, Number 3 401 Surgical Treatment of Moyamoya Disease in Pediatric Patients--Comparison between the Results of Indirect and Direct Revascularization Procedures Clinical Study
Clinical results Postoperative clinical improvements were classified into three grades such as A, B, and C (Table 4). In Grade A, the symptoms completely disappeared. In Grade B, the symptoms improved but remained to some extent, and in Grade C, the symptoms were unchanged. When the surgical effects were evaluated regarding the 20 operated sides relevant to the symptoms, A was obtained in 3 (23%) of the 13 sides with EDAS and in all 7 sides (100%) with STA-MCA anastomosis with EMS (Table 4). The postoperative clinical improvement after STAMCA anastomosis with EMS and thus significantly better than that after EDAS (P < 0.01). Complications Three of the 13 EDAS procedures and 1 of the 7 STA-MCA anastomoses with EMS were associated with postoperative complications. Two of the three complications after the EDAS were increased transient ischemic attacks (TIA) for a few weeks after surgery, and the remaining one was postoperative epilepsy. The one complication after the STA-MCA anastomosis with EMS was an increase in the frequency of TIA. In both groups, the complications were minor and transient. DISCUSSION Direct vascular reconstructive surgery for moyamoya disease has become popular since Krayenbühl's proposal of STA-MCA anastomosis in 1975. The bypass procedures used were proven to be effective for the ischemic type of this disease (2,4,9,10, 13,14,16) . However, the question remains as to which technique is the most effective and safe. There have been various arguments about the effects of different surgical procedures (8,10,14,15). These days, either one or any combination of direct and/or indirect revascularization procedure, such as STA-MCA
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anastomosis, EMS, or EDAS, may be commonly chosen for surgical treatment. We used only EDAS in the parietal region during the period from 1983 to 1986 and mainly STA-MCA anastomosis with EMS during the past 4 years, since 1987. Earlier, we used only indirect revascularization procedures to perform surgical treatment with a minimal risk, and we reported that postoperative collateral circulation could be obtained through them (9,10) . However, postoperative external carotid angiograms revealed either poor or no collateral formation through EDAS in about 20 to 30% of the operated sides (9,10). Furthermore, after EDAS, when the angiographic outcome is strictly graded (as in this study), a satisfactory collateral formation is seen in fewer patients. In addition, in a few patients, a second operation was required because of persistent clinical symptoms (8). Moyamoya cases refractory to indirect bypass procedures have also been recently reported (1,14) . Therefore, our department has selected STAMCA anastomosis with EMS instead of EDAS as the treatment of choice since 1987. A follow-up study was then completed on only 7 sides with STA-MCA anastomosis with EMS in 6 patients. The number of cases is still small, but sufficient results have been obtained so far in all of them. Causes of poor development of the collateral circulation after EDAS may include a technical problem and a local condition of cerebral blood circulation in the area where the EDAS was performed (8-10). We made an effort to make the flap of the STA as long as possible and to minimize the coagulation of the edges of the STA flap and the incised dura mater. In our previous positron emission tomography study (10), the regional cerebral blood flow and metabolism gave information concerning the demand of postoperative collateral formation in the brain area located under the anastomosis. The collateral circulation through the EDAS tended to be well established at the site of surgery with the preoperatively increased rOEF; however, in EDAS, the brain area exposed for anastomosis is narrow. Besides, the site cannot be chosen appropriately because the separated posterior branch of the STA cannot be widely moved without division of its distal portion. We fortunately did not have any major complications in either EDAS or STA-MCA anastomosis with EMS. However, we have seen a few children who had major postoperative complications after one of the two procedures performed in other hospitals. STA-MCA anastomosis in children with moyamoya disease requires meticulous techniques. Careful postoperative management is also needed to prevent ischemic insult. It is our opinion that the first choice of treatment should be STA-MCA anastomosis combined with EMS whenever possible. However, an indirect revascularization procedure such as EDAS remains the second choice for small children with moyamoya disease, especially in those who have TIA, reversible ischemic neurological deficit, and/or a minor stroke at the time of admission. In addition, any promoting factors for the development of collateral circulation,
Redistribution of this article permitted only in accordance with the publisher’s copyright provisions.
observing the lateral views of the postoperative serial external angiograms. The new development of collateral circulation through the bypass was classified into three degrees according to the extent of the blood supply: A, in which the area supplied by the surgical bypass covered more than two thirds of the middle cerebral artery (MCA) distribution; B, in which between two thirds and one third of the MCA distribution was covered; and C, in which only one cortical branch of the MCA was covered through the bypass or no collateral circulation was observed (Fig. 2). Our results on the 20 operated sides are presented in Table 3. Of the 13 sides operated on by EDAS, 2 sides showed A, 6 sides showed B, and 5 sides showed C. Only two sides (15%) showed a collateral formation extending throughout more than two thirds of the MCA distribution (Table 3). On the other hand, the sides with STA-MCA anastomosis with EMS showed A on five sides and B on two sides. The collateral formation of A was observed in 71% (Table 3; Fig. 3). The postoperative collateral formation through STA-MCA anastomosis with EMS was significantly better than that through EDAS (P < 0.05).
ACKNOWLEDGMENTS We express our thanks to Prof. Emeritus K. Kitamura, Neurological Institute, Faculty of Medicine, Kyushu University for his valuable suggestions. We also thank B. Quinn for his critical comments on the manuscript. Received, December 3, 1991. Accepted, April 6, 1992. Reprint requests: Toshio Matsushima, M.D., Department of Neurosurgery, Neurological Institute, Faculty of Medicine, Kyushu University 60, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812, Japan.
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REFERENCES: (1-18) 1. 2. 3.
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Cahan LD: Failure of encephalo-duro-arteriosynangiosis procedure in moyamoya disease. Pediatr Neurosci 12:58-62, 1985-1986. Ishii R: Surgical treatments for moyamoya disease. Neurol Surg 14:1059-1068, 1986 (in Japanese). Karasawa J, Kikuchi H, Furuse S, Sakaki T, Yoshida Y, Ohnishi H, Taki W: A surgical treatment of "Moyamoya" disease-"encephalo- myo-synangiosis" Neurol Med Chir 17(part 1):29-37, 1977. Karasawa J: Studies on the surgical treatment of "Moyamoya" disease. J Nara Med Assoc 29:375-397, 1978 (in Japanese). Karasawa J, Kikuchi H, Furuse S, Kawamura J, Sakaki T: Treatment of moyamoya disease with STA-MCA anastomosis. J Neurosurg 49:679-688, 1978. Kobayashi K, Takeuchi S, Tsuchida T, Ito J: Encephalo-myo synangiosis (EMS) in moyamoya disease--with special reference to postoperative angiography. Neurol Med Chir 21:1229-1238, 1981 (in Japanese). Krayenbühl HA: The moyamoya syndrome and neurosurgeon. Surg Neurol 4:353-360, 1975. Matsushima T, Fujiwara S, Nagata S, Fujii K, Fukui M, Hasuo K: Reoperation for moyamoya disease refractory to encephaloduro- arterio-synangiosis. Acta Neurochir 107:129-132, 1990. Matsushima T, Fujiwara S, Nagata S, Fujii K, Fukui M, Kitamura K, Hasuo K: Surgical treatment for pediatric patients with moyamoya disease by indirect revascularization procedures (EDAS, EMS, EMAS) Acta Neurochir (Wien) 98:135-140, 1989. Matsushima T, Fukui M, Kitamura K, Hasuo K, Kuwabara Y, Kurokawa T: Encephalo-duroarterio-synangiosis in children with moyamoya disease. Acta Neurochir (Wien) 104:96-102, 1990. Matsushima Y, Fukai N, Tanaka K, Tsuruoka S, Aoyagi M, Inaba Y: A new operative
Downloaded from https://academic.oup.com/neurosurgery/article-abstract/31/3/401/2752037 by Technische Universitaet Muenchen user on 07 July 2018
15.
16.
17.
18.
method for "Moya-moya" disease: A presentation of a case who underwent encephalo-duro-arterio(STA) synangiosis. Nervous Syst Children 5:249-255, 1980 (in Japanese). Matsushima Y, Fukai N, Tanaka K, Tsuruoka S, Inaba Y, Aoyagi M, Ohno K: A new surgical treatment of moyamoya disease in children: A preliminary report. Surg Neurol 15:313-320, 1981. Matsushima Y, Inaba Y: Moyamoya disease in children and its surgical treatment. Introduction of a new surgical procedure and its follow-up angiograms. Child Brain 11:155170, 1984. Miyamoto S, Kikuchi H, Karasawa J, Nagata I, Yamazoe N, Akiyama Y: Pitfalls in the surgical treatment of moyamoya diseases. Operative techniques for refractory cases. J Neurosurg 68:537-543, 1988. Nakagawa Y, Gotoh S, Shimoyama M, Ohtsuka K, Mabuchi S, Sawamura Y, Abe H, Tsuru M: Reconstructive operation for moyamoya disease--surgical indication for the hemorrhagic type and preferable operative methods. Neurol Med Chir 23:464-470, 1983 (in Japanese). Olds MV, Griebel RW, Hoffman HJ, Craven M, Chuang S, Schutz H: The surgical treatment of childhood moyamoya disease. J Neurosurg 66:675-680, 1987. Suzuki J, Takaku A: Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288-299, 1969. Takeuchi S, Tsuchida T, Kobayashi K, Fukuda M, Ishii R, Tanaka R, Ito J: Treatment of moyamoya disease by temporal muscle graft "Encephalo-myo synangiosis. " Child Brain 10:1-15, 1983.
COMMENTS The authors present a comparison of the results of treatment of Japanese children with moyamoya disease by the use of two different forms of surgical treatment. The direct procedure, superficial temporal artery to middle cerebral artery bypass (STA-MCA) with encephalomyosynangiosis, was significantly more effective than was the indirect procedure, encephaloduroarteriosynangiosis, for both the angiographic development of collateral circulation as well as clinical improvement. The authors describe the various techniques they use to treat this frustrating condition. This report gives convincing data to suggest that when attempting revascularization in moyamoya disease, the STA-MCA bypass with encephalomyosynangiosis procedure is the most successful and should be used whenever possible. Harold L. Rekate
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if present, should be clarified for the use of indirect revascularization procedures (10).
This report demonstrates a convincing superiority of STA-MCA anastomosis combined with encephalomyosynangiosis over encephaloduroarteriosynangiosis in treatment of symptomatic moyamoya disease in children, both in the degree of revascularization achieved and improvement in symptomatology. This information will be helpful to those of us who see occasional cases of moyamoya disease and are perplexed as to the best treatment option. Presumably, these results would be applicable to adults as well? Unfortunately, it seems most inappropriately, in the United States, Medicare reimbursement for STAMCA anastomosis in the treatment of moyamoya disease has been withdrawn even though this entity was not specifically studied in the International Randomized Trial on Extracranial-to-Intracranial Bypass. To my knowledge, patients with moyamoya disease are not being studied in the New Japanese Cooperative Study of Extracranial-to-Intracranial Bypass. Hopefully, as more data of this type accumulate, especially from our Japanese colleagues, third-party payers, especially the Health Care Financing Administration, will reconsider this particular aspect of its opinion. David G. Piepgras Rochester, Minnesota
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Phoenix, Arizona
Figure 2. Classification of the development of collateral formation demonstrated on the postoperative external carotid angiograms in patients with EDAS. A, more than two- thirds of the MCA distribution; B, between two-thirds and one-third of the MCA; and C, slight or none.
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Figure 1. Illustrations showing operative procedures and techniques. A, skin incision and craniotomy; a shows EDAS, and b shows STA-MCA anastomosis with EMS. B, procedures of EDAS. C, procedures of STA-MCA anastomosis with EMS. An arrow shows the side-to-end anastomosis between the STA and one cortical branch of the MCA. (B, burr hole; BF, bone flap; D, dura mater; G, galea; MF, temporal muscle flap; S, STA.)
Table 1. Surgical Procedures in Pediatric Cases of Moyamoya Disease
Table 2. Clinical Features of Investigated Casesa
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Figure 3. Postoperative external carotid angiograms in patients with STA-MCA anastomosis associated with EMS, best (A) and worst development (B).
Table 4. Postoperative Outcome of Clinical Symptomsa
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Table 3. Postoperative Collateral Formation on External Angiogramsa
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MCA anastomosis in recent cases. The results of these two different surgical procedures are presented and compared. MATERIALS AND METHODS Forty Japanese children were diagnosed and surgically treated at the Department of Neurosurgery, Kyushu University Hospital. Four different types of single or combined surgical procedures were used. We basically used EDAS in the parietal region during the period from 1983 to 1986, whereas STA-MCA anastomosis with EMS was mainly performed during the past 4 years, since 1987 (Fig. 1). In some recent cases, encephalomyoarteriosynangiosis was added to obtain a collateral formation in the anterior cerebral artery distribution. EDAS was performed above the ear, as described by Matsushima et al. (11-13) (Fig. 1, A and B). We first separated the posterior branch of the superficial temporal artery (STA) and the surrounding connective tissue without dividing the trunk and then sutured it to the edges of the exposed and incised dura mater. In STA-MCA anastomosis with EMS, we performed a wide craniotomy in the parietotemporal region and performed STA-MCA anastomosis (Fig. 1, A and C). The exposed frontoparietotemporal cortices and the anastomosed arteries were then covered with the temporal muscle instead of the dura mater. We used 11-0 monofilament nylon sutures for the anastomosis because arteries in children with moyamoya disease are very small, thin, and fragile, like veins. In the study presented here, the children who underwent only one of the two following procedures-EDAS alone and STA-MCA anastomosis with EMS in the parietal region-- were selected as representatives of indirect and direct procedures, respectively. The patients who received encephalomyoarteriosynangiosis in the frontal region were excluded because it was often found to influence the effects of EDAS and STA-MCA anastomosis in the parietal region. Ten patients (13 sides) received EDAS in the parietal region alone, whereas 6 patients (7 sides) received only STA-MCA anastomosis with EMS (Table 1). Table 2 shows the age at onset, clinical types, preoperative duration, and preoperative angiographic staging of the patients in each group. The angiographic staging described by Suzuki and Takaku (17) was used to estimate the preoperative angiographic findings. Their distribution was measured by the χ2 test, and the differences between the mean values of the parameters investigated were measured by Student's t test. The two groups were not significantly different regarding four preoperative factors. Their postoperative collateral formation and development of the clinical symptoms were studied by postoperative external carotid angiography and a postoperative clinical chart. Postoperative angiography and a follow-up examination were done during the period from 6 months to 1 year after bypass surgery. RESULTS Angiographic results Postoperative collateral formation was studied by
Redistribution of this article permitted only in accordance with the publisher’s copyright provisions.
Neurosurgery 1992-98 September 1992, Volume 31, Number 3 401 Surgical Treatment of Moyamoya Disease in Pediatric Patients--Comparison between the Results of Indirect and Direct Revascularization Procedures Clinical Study
Clinical results Postoperative clinical improvements were classified into three grades such as A, B, and C (Table 4). In Grade A, the symptoms completely disappeared. In Grade B, the symptoms improved but remained to some extent, and in Grade C, the symptoms were unchanged. When the surgical effects were evaluated regarding the 20 operated sides relevant to the symptoms, A was obtained in 3 (23%) of the 13 sides with EDAS and in all 7 sides (100%) with STA-MCA anastomosis with EMS (Table 4). The postoperative clinical improvement after STAMCA anastomosis with EMS and thus significantly better than that after EDAS (P < 0.01). Complications Three of the 13 EDAS procedures and 1 of the 7 STA-MCA anastomoses with EMS were associated with postoperative complications. Two of the three complications after the EDAS were increased transient ischemic attacks (TIA) for a few weeks after surgery, and the remaining one was postoperative epilepsy. The one complication after the STA-MCA anastomosis with EMS was an increase in the frequency of TIA. In both groups, the complications were minor and transient. DISCUSSION Direct vascular reconstructive surgery for moyamoya disease has become popular since Krayenbühl's proposal of STA-MCA anastomosis in 1975. The bypass procedures used were proven to be effective for the ischemic type of this disease (2,4,9,10, 13,14,16) . However, the question remains as to which technique is the most effective and safe. There have been various arguments about the effects of different surgical procedures (8,10,14,15). These days, either one or any combination of direct and/or indirect revascularization procedure, such as STA-MCA
Downloaded from https://academic.oup.com/neurosurgery/article-abstract/31/3/401/2752037 by Technische Universitaet Muenchen user on 07 July 2018
anastomosis, EMS, or EDAS, may be commonly chosen for surgical treatment. We used only EDAS in the parietal region during the period from 1983 to 1986 and mainly STA-MCA anastomosis with EMS during the past 4 years, since 1987. Earlier, we used only indirect revascularization procedures to perform surgical treatment with a minimal risk, and we reported that postoperative collateral circulation could be obtained through them (9,10) . However, postoperative external carotid angiograms revealed either poor or no collateral formation through EDAS in about 20 to 30% of the operated sides (9,10). Furthermore, after EDAS, when the angiographic outcome is strictly graded (as in this study), a satisfactory collateral formation is seen in fewer patients. In addition, in a few patients, a second operation was required because of persistent clinical symptoms (8). Moyamoya cases refractory to indirect bypass procedures have also been recently reported (1,14) . Therefore, our department has selected STAMCA anastomosis with EMS instead of EDAS as the treatment of choice since 1987. A follow-up study was then completed on only 7 sides with STA-MCA anastomosis with EMS in 6 patients. The number of cases is still small, but sufficient results have been obtained so far in all of them. Causes of poor development of the collateral circulation after EDAS may include a technical problem and a local condition of cerebral blood circulation in the area where the EDAS was performed (8-10). We made an effort to make the flap of the STA as long as possible and to minimize the coagulation of the edges of the STA flap and the incised dura mater. In our previous positron emission tomography study (10), the regional cerebral blood flow and metabolism gave information concerning the demand of postoperative collateral formation in the brain area located under the anastomosis. The collateral circulation through the EDAS tended to be well established at the site of surgery with the preoperatively increased rOEF; however, in EDAS, the brain area exposed for anastomosis is narrow. Besides, the site cannot be chosen appropriately because the separated posterior branch of the STA cannot be widely moved without division of its distal portion. We fortunately did not have any major complications in either EDAS or STA-MCA anastomosis with EMS. However, we have seen a few children who had major postoperative complications after one of the two procedures performed in other hospitals. STA-MCA anastomosis in children with moyamoya disease requires meticulous techniques. Careful postoperative management is also needed to prevent ischemic insult. It is our opinion that the first choice of treatment should be STA-MCA anastomosis combined with EMS whenever possible. However, an indirect revascularization procedure such as EDAS remains the second choice for small children with moyamoya disease, especially in those who have TIA, reversible ischemic neurological deficit, and/or a minor stroke at the time of admission. In addition, any promoting factors for the development of collateral circulation,
Redistribution of this article permitted only in accordance with the publisher’s copyright provisions.
observing the lateral views of the postoperative serial external angiograms. The new development of collateral circulation through the bypass was classified into three degrees according to the extent of the blood supply: A, in which the area supplied by the surgical bypass covered more than two thirds of the middle cerebral artery (MCA) distribution; B, in which between two thirds and one third of the MCA distribution was covered; and C, in which only one cortical branch of the MCA was covered through the bypass or no collateral circulation was observed (Fig. 2). Our results on the 20 operated sides are presented in Table 3. Of the 13 sides operated on by EDAS, 2 sides showed A, 6 sides showed B, and 5 sides showed C. Only two sides (15%) showed a collateral formation extending throughout more than two thirds of the MCA distribution (Table 3). On the other hand, the sides with STA-MCA anastomosis with EMS showed A on five sides and B on two sides. The collateral formation of A was observed in 71% (Table 3; Fig. 3). The postoperative collateral formation through STA-MCA anastomosis with EMS was significantly better than that through EDAS (P < 0.05).
ACKNOWLEDGMENTS We express our thanks to Prof. Emeritus K. Kitamura, Neurological Institute, Faculty of Medicine, Kyushu University for his valuable suggestions. We also thank B. Quinn for his critical comments on the manuscript. Received, December 3, 1991. Accepted, April 6, 1992. Reprint requests: Toshio Matsushima, M.D., Department of Neurosurgery, Neurological Institute, Faculty of Medicine, Kyushu University 60, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812, Japan.
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REFERENCES: (1-18) 1. 2. 3.
4. 5.
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7. 8.
9.
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Cahan LD: Failure of encephalo-duro-arteriosynangiosis procedure in moyamoya disease. Pediatr Neurosci 12:58-62, 1985-1986. Ishii R: Surgical treatments for moyamoya disease. Neurol Surg 14:1059-1068, 1986 (in Japanese). Karasawa J, Kikuchi H, Furuse S, Sakaki T, Yoshida Y, Ohnishi H, Taki W: A surgical treatment of "Moyamoya" disease-"encephalo- myo-synangiosis" Neurol Med Chir 17(part 1):29-37, 1977. Karasawa J: Studies on the surgical treatment of "Moyamoya" disease. J Nara Med Assoc 29:375-397, 1978 (in Japanese). Karasawa J, Kikuchi H, Furuse S, Kawamura J, Sakaki T: Treatment of moyamoya disease with STA-MCA anastomosis. J Neurosurg 49:679-688, 1978. Kobayashi K, Takeuchi S, Tsuchida T, Ito J: Encephalo-myo synangiosis (EMS) in moyamoya disease--with special reference to postoperative angiography. Neurol Med Chir 21:1229-1238, 1981 (in Japanese). Krayenbühl HA: The moyamoya syndrome and neurosurgeon. Surg Neurol 4:353-360, 1975. Matsushima T, Fujiwara S, Nagata S, Fujii K, Fukui M, Hasuo K: Reoperation for moyamoya disease refractory to encephaloduro- arterio-synangiosis. Acta Neurochir 107:129-132, 1990. Matsushima T, Fujiwara S, Nagata S, Fujii K, Fukui M, Kitamura K, Hasuo K: Surgical treatment for pediatric patients with moyamoya disease by indirect revascularization procedures (EDAS, EMS, EMAS) Acta Neurochir (Wien) 98:135-140, 1989. Matsushima T, Fukui M, Kitamura K, Hasuo K, Kuwabara Y, Kurokawa T: Encephalo-duroarterio-synangiosis in children with moyamoya disease. Acta Neurochir (Wien) 104:96-102, 1990. Matsushima Y, Fukai N, Tanaka K, Tsuruoka S, Aoyagi M, Inaba Y: A new operative
Downloaded from https://academic.oup.com/neurosurgery/article-abstract/31/3/401/2752037 by Technische Universitaet Muenchen user on 07 July 2018
15.
16.
17.
18.
method for "Moya-moya" disease: A presentation of a case who underwent encephalo-duro-arterio(STA) synangiosis. Nervous Syst Children 5:249-255, 1980 (in Japanese). Matsushima Y, Fukai N, Tanaka K, Tsuruoka S, Inaba Y, Aoyagi M, Ohno K: A new surgical treatment of moyamoya disease in children: A preliminary report. Surg Neurol 15:313-320, 1981. Matsushima Y, Inaba Y: Moyamoya disease in children and its surgical treatment. Introduction of a new surgical procedure and its follow-up angiograms. Child Brain 11:155170, 1984. Miyamoto S, Kikuchi H, Karasawa J, Nagata I, Yamazoe N, Akiyama Y: Pitfalls in the surgical treatment of moyamoya diseases. Operative techniques for refractory cases. J Neurosurg 68:537-543, 1988. Nakagawa Y, Gotoh S, Shimoyama M, Ohtsuka K, Mabuchi S, Sawamura Y, Abe H, Tsuru M: Reconstructive operation for moyamoya disease--surgical indication for the hemorrhagic type and preferable operative methods. Neurol Med Chir 23:464-470, 1983 (in Japanese). Olds MV, Griebel RW, Hoffman HJ, Craven M, Chuang S, Schutz H: The surgical treatment of childhood moyamoya disease. J Neurosurg 66:675-680, 1987. Suzuki J, Takaku A: Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288-299, 1969. Takeuchi S, Tsuchida T, Kobayashi K, Fukuda M, Ishii R, Tanaka R, Ito J: Treatment of moyamoya disease by temporal muscle graft "Encephalo-myo synangiosis. " Child Brain 10:1-15, 1983.
COMMENTS The authors present a comparison of the results of treatment of Japanese children with moyamoya disease by the use of two different forms of surgical treatment. The direct procedure, superficial temporal artery to middle cerebral artery bypass (STA-MCA) with encephalomyosynangiosis, was significantly more effective than was the indirect procedure, encephaloduroarteriosynangiosis, for both the angiographic development of collateral circulation as well as clinical improvement. The authors describe the various techniques they use to treat this frustrating condition. This report gives convincing data to suggest that when attempting revascularization in moyamoya disease, the STA-MCA bypass with encephalomyosynangiosis procedure is the most successful and should be used whenever possible. Harold L. Rekate
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if present, should be clarified for the use of indirect revascularization procedures (10).
This report demonstrates a convincing superiority of STA-MCA anastomosis combined with encephalomyosynangiosis over encephaloduroarteriosynangiosis in treatment of symptomatic moyamoya disease in children, both in the degree of revascularization achieved and improvement in symptomatology. This information will be helpful to those of us who see occasional cases of moyamoya disease and are perplexed as to the best treatment option. Presumably, these results would be applicable to adults as well? Unfortunately, it seems most inappropriately, in the United States, Medicare reimbursement for STAMCA anastomosis in the treatment of moyamoya disease has been withdrawn even though this entity was not specifically studied in the International Randomized Trial on Extracranial-to-Intracranial Bypass. To my knowledge, patients with moyamoya disease are not being studied in the New Japanese Cooperative Study of Extracranial-to-Intracranial Bypass. Hopefully, as more data of this type accumulate, especially from our Japanese colleagues, third-party payers, especially the Health Care Financing Administration, will reconsider this particular aspect of its opinion. David G. Piepgras Rochester, Minnesota
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Phoenix, Arizona
Figure 2. Classification of the development of collateral formation demonstrated on the postoperative external carotid angiograms in patients with EDAS. A, more than two- thirds of the MCA distribution; B, between two-thirds and one-third of the MCA; and C, slight or none.
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Figure 1. Illustrations showing operative procedures and techniques. A, skin incision and craniotomy; a shows EDAS, and b shows STA-MCA anastomosis with EMS. B, procedures of EDAS. C, procedures of STA-MCA anastomosis with EMS. An arrow shows the side-to-end anastomosis between the STA and one cortical branch of the MCA. (B, burr hole; BF, bone flap; D, dura mater; G, galea; MF, temporal muscle flap; S, STA.)
Table 1. Surgical Procedures in Pediatric Cases of Moyamoya Disease
Table 2. Clinical Features of Investigated Casesa
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Figure 3. Postoperative external carotid angiograms in patients with STA-MCA anastomosis associated with EMS, best (A) and worst development (B).
Table 4. Postoperative Outcome of Clinical Symptomsa
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Table 3. Postoperative Collateral Formation on External Angiogramsa
