Synergistic Interactions Between Direct and Indirect Bypasses in Combined Procedures: The Significance of Indirect Bypasses in Moyamoya Disease

Neurosurgery ◽  
2017 ◽  
Vol 80 (2) ◽  
pp. 201-209 ◽  
Author(s):  
Haruto Uchino ◽  
Jae-Hoon Kim ◽  
Noriyuki Fujima ◽  
Ken Kazumata ◽  
Masaki Ito ◽  
...  

Abstract BACKGROUND: Whether additional indirect bypasses effectively contribute to revascularization in combined procedures remains unclear in patients with moyamoya disease. OBJECTIVE: To evaluate the longitudinal changes associated with combined procedures while following up pediatric and adult patients long term and to assess whether any other clinical factors or hemodynamic parameters affected these changes to determine an optimal surgical strategy. METHODS: We studied 58 hemispheres in 43 adults and 39 hemispheres in 26 children who underwent combined revascularization for moyamoya disease. To evaluate bypass development, we assessed the sizes of the superficial temporal artery and middle meningeal artery using magnetic resonance angiography. Multivariate analysis determined the effects of multiple variables on bypass development. RESULTS: Indirect bypass (middle meningeal artery) development occurred in 95% and 78% of the pediatric and adult hemispheres, respectively. Of these, dual development of direct and indirect bypasses occurred in 54% of the pediatric hemispheres and in 47% of the adult hemispheres. Reciprocal superficial temporal artery regression occurred in 28% of the hemispheres during the transition from the postoperative acute phase to the chronic phase during indirect bypass development. Good indirect bypass development was associated with adult hemispheres at Suzuki stage 4 or greater (odds ratio, 7.4; 95% confidence interval, 1.4-39.4; P = .02). Disease onset type and preoperative hemodynamic parameters were not considered predictors for the development of surgical revascularization. CONCLUSION: Simultaneous direct and indirect bypass development was most frequently observed, regardless of patient age and hemodynamic status. Applying indirect bypass as an adjunct to direct bypass could maximize revascularization in adults and children.

Stroke ◽  
2017 ◽  
Vol 48 (suppl_1) ◽  
Author(s):  
Kikutaro Tokairin ◽  
Haruto Uchino ◽  
Ken Kazumata ◽  
Masaki Ito ◽  
Naoki Nakayama ◽  
...  

Background & Purpose: The additional effects of indirect bypass on combined revascularization surgery in moyamoya disease (MMD) remain unclear. Our purpose in this study is to evaluate how direct and indirect bypass in combined revascularization change through long term follow up and to analyze the clinical factors or hemodynamic parameters involved in these changes. Methods: A retrospective survey was conducted with a sample size of 97 hemispheres from 69 consecutive patients (43 adults and 26 children) with MMD treated by combined revascularization. We used magnetic resonance angiography (MRA) to evaluate bypass development with the diameters of superior temporal artery (STA) for the direct bypass and middle meningeal artery (MMA) and deep temporal artery (DTA) for the indirect bypass. A multivariate logistic regression analysis was used to study the related multiple variables on bypass development. Results: Good indirect bypass indicated by MMA development was seen 78% of the adult hemispheres and 95% of the pediatric ones. Dual development of direct and indirect bypasses was most frequently observed (47% and 56% of the adult and pediatric hemispheres, respectively). When indirect bypasses developed, 28% of the STAs reduced in diameter reciprocally from the acute to the chronic phases after surgery. The development of indirect bypass was significantly better in the adult hemispheres at Suzuki stage 4 or greater ( P =0.02; odds ratio 7.4, 95% confidence interval, 1.4-39.4). The disease onset type and the hemodynamic parameters were not associated with the development of surgical revascularization. Conclusions: Indirect bypass developed effectively in both adult and pediatric patients, even in the presence of direct bypass. The universal application of indirect bypass is considered an optimal surgical strategy to maximize revascularization in MMD.


Stroke ◽  
2020 ◽  
Vol 51 (Suppl_1) ◽  
Author(s):  
Haruto Uchino ◽  
Shusuke Yamamoto ◽  
Daina Kashiwazaki ◽  
Naoki Akioka ◽  
Naoya Kuwayama ◽  
...  

Object: The calibers of donor arteries can change dynamically after bypass surgery in moyamoya disease (MMD). The present study aimed to evaluate the cut-offs of caliber changes in donor arteries associated with good surgical revascularization and to assess the impact of clinical factors potentially related to bypass development. Methods: We studied 71 hemispheres of 30 adults and 16 children with MMD, who underwent combined revascularization. We quantitatively measured the calibers of the superficial temporal artery (STA), deep temporal artery (DTA), and middle meningeal artery (MMA) with magnetic resonance angiography (MRA) source images and calculated the postoperative caliber change ratios (CCRs), to assess direct and indirect bypass development. They were compared with the findings of digital subtraction angiography, in which revascularization areas were categorized into 3 groups (poor, good, and excellent). Results: In both adult and pediatric hemispheres, median STA and DTA CCRs were higher in better revascularization groups (p < 0.05), while MMA CCRs were not significantly different among the groups. Receiver operation characteristic analysis revealed that the cut-off of >1.1 and >1.3 STA CCRs were associated with good direct revascularization in adult and pediatric hemispheres, respectively. The cut-off of >1.6 and >1.2 DTA CCRs were associated with good indirect revascularization in adult and pediatric hemispheres, respectively. Considering these cut-off values, STA and DTA CCRs showed high median values, irrespective of age, severity of cerebrovascular reserve, disease stage, and disease onset type. Conclusions: Caliber changes in STA and DTA can be easily measured by MRA, which could be indicators of direct and indirect bypass development. The combined bypass procedure could maximize revascularization in both adults and children with MMD.


2013 ◽  
Vol 118 (1) ◽  
pp. 104-108 ◽  
Author(s):  
Nancy McLaughlin ◽  
Neil A. Martin

Numerous surgical techniques have been developed and refined for the treatment of moyamoya disease. Among the indirect techniques of revascularization, encephaloduroarteriosynangiosis has been recognized as effective in promoting revascularization and reversing symptomatology. Neovascularization occurs between the donor artery, either the superficial temporal artery or the occipital artery, and the underlying ischemic cortex. Additionally, the middle meningeal artery and its dural branches have also been shown to contribute to collateral blood supply. In this report the authors describe an integrated management of the meninges for optimal revascularization. They emphasize the importance of recognizing the 3 major layers of the dura and describe a technique of dural splitting at the locus minoris resistentiae between the dura mater's vascular (middle) layer and internal median layer. Applying the dura's vascular layer to the surface of the brain after opening of the arachnoid is designed to optimize dural-pial synangiosis related to middle meningeal artery branches.


2017 ◽  
Vol 15 (1) ◽  
pp. 89-96 ◽  
Author(s):  
Hamid Reza Niknejad ◽  
Albert van der Zwan ◽  
Sam Heye ◽  
Frank Van Calenbergh ◽  
Johannes Van Loon

Abstract BACKGROUND Over the past decade, there has been a revival and a renewed interest for cerebrovascular bypass procedures. The superficial temporal artery (STA) has its value as a reliable donor vessel; however, a possible role for the middle meningeal artery (MMA) as a donor artery is still unclear. OBJECTIVE To assess the feasibility of using the MMA as a donor vessel in cerebrovascular surgery. METHODS We performed cadaveric dissections on 12 fresh specimens (23 sides) after bilateral silicone injection into the internal and external carotid arteries. We compared the size, diameter, and possibility to perform a bypass to the middle cerebral artery for both the MMA and the STA. Measurements were done using an electrical caliper. Additional measurements of the MMA and STA were performed on 20 random angiograms. RESULTS There was no statistically significant difference in diameter of the MMA at its ostium being 2.4 mm, compared to 2.7 mm for the STA ostium (t-test; P = .21). The MMA could be mobilized over 4.1 cm, whereas the STA over 8.3 cm. Finally, the mean diameter of the donor vessel at the site of the anastomosis was 1.6 mm versus 1.9 mm for MMA and STA, respectively (P = .0026). We were able to perform an MMA and middle cerebral artery anastomosis on 17 sides. CONCLUSION These results suggest that the MMA is a potentially valuable donor vessel to be used in selected cases. The availability of a suitable MMA branch should be assessed preoperatively on the angiogram.


2019 ◽  
pp. 1-9 ◽  
Author(s):  
Haruto Uchino ◽  
Shusuke Yamamoto ◽  
Daina Kashiwazaki ◽  
Naoki Akioka ◽  
Naoya Kuwayama ◽  
...  

OBJECTIVEThe calibers of donor arteries can change dynamically after bypass surgery in patients with moyamoya disease (MMD). The present study aimed to evaluate the cutoffs of caliber changes in donor arteries associated with good surgical revascularization and to assess the impact of clinical factors potentially related to bypass development.METHODSThe authors studied 71 hemispheres of 30 adults and 16 children with MMD who underwent combined direct and indirect revascularization. They quantitatively measured the calibers of the superficial temporal artery (STA), deep temporal artery (DTA), and middle meningeal artery (MMA) with MR angiography (MRA) source images and calculated the postoperative caliber change ratios (CCRs) to assess direct and indirect bypass development. These values were compared with the findings of digital subtraction angiography, in which revascularization areas were categorized into 3 groups (poor, good, and excellent).RESULTSIn both adult and pediatric hemispheres, the median STA and DTA CCRs were higher in better-revascularization groups (p < 0.05), while MMA CCRs were not significantly different among the groups. Receiver operating characteristic analysis revealed that the cutoff STA CCRs of > 1.1 and > 1.3 were associated with good direct revascularization in adult and pediatric hemispheres, respectively. Cutoff DTA CCRs of > 1.6 and > 1.2 were associated with good indirect revascularization in adult and pediatric hemispheres, respectively. Considering these cutoff values, STA and DTA CCRs showed high median values, irrespective of age, severity of cerebrovascular reserve, disease stage, and disease-onset type.CONCLUSIONSCaliber changes in STAs and DTAs can be easily measured using MRA, and they could be indicators of direct and indirect bypass development. The dual development of a direct and indirect bypass was most frequently observed in the context of a combined bypass procedure in both adults and children with MMD.


Neurosurgery ◽  
2011 ◽  
Vol 68 (1) ◽  
pp. 34-43 ◽  
Author(s):  
Joshua R. Dusick ◽  
Nestor R. Gonzalez ◽  
Neil A. Martin

Abstract BACKGROUND: Several forms of indirect cerebral revascularization have been proposed to promote neovascularity to the ischemic brain. OBJECTIVE: To present clinical and angiographic outcomes of indirect revascularization by encephaloduroarteriosynangiosis and burr holes for the treatment of Moyamoya disease in adults and children. METHODS: Data from 63 hemispheres treated in 42 patients (average age, 30 years; 33 adults; 30 female patients; median follow-up, 14 months) were reviewed. In hemispheres with preoperative and postoperative (6- to 12-month) angiograms available, superficial temporal artery (STA) and middle meningeal artery (MMA) diameters were measured. Preoperative and postoperative corrected arterial sizes were compared. RESULTS: Seven patients (17%) had transient ischemic attacks that resolved within 1 month of surgery. No patients suffered moyamoya-related hemorrhage after treatment. Two patients developed additional symptoms many years after surgery. In 18 hemispheres with preoperative and postoperative angiograms, there was an average postoperative increase in STA and MMA diameters of 51% (P = .003) and 49% (P = .002), respectively. Both children and adults displayed revascularization. Two patients did not demonstrate increased vessel size. STA blush and new branches and MMA blush and new branches were identified in 12, 14, 14, and 16 hemispheres, respectively. Angiographic blush was identified in 59% of frontal and 19% of parietal burr holes (P = .03). Surgical complications included 2 subdural hemorrhages requiring evacuation and 2 new ischemic deficits (1 transient). CONCLUSION: Indirect revascularization by encephaloduroarteriosynangiosis and burr holes for moyamoya results in long-term resolution of ischemic and hemorrhagic manifestations in 95% of adults and children. The MMA appears to contribute significantly to the revascularization on follow-up angiograms with increased size and neovascularity comparable to that of the STA. Angiographically, parietal burr holes do not contribute as significantly as frontal burr holes.


2018 ◽  
Vol 128 (5) ◽  
pp. 1304-1310 ◽  
Author(s):  
Tao Yang ◽  
Yoshifumi Higashino ◽  
Hiroharu Kataoka ◽  
Eika Hamano ◽  
Daisuke Maruyama ◽  
...  

OBJECTIVEHyperperfusion syndrome (HPS) is a notable complication that causes various neurological symptoms after superficial temporal artery (STA)–middle cerebral artery (MCA) bypass surgery for moyamoya disease (MMD). The authors used intraoperative indocyanine green (ICG) videoangiography to measure the change in microvascular transit time (MVTT) after bypass surgery. An analysis was then conducted to identify the correlation between change in MVTT and presence of postoperative HPS.METHODSThis study included 105 hemispheres of 81 patients with MMD who underwent STA-MCA single bypass surgery between January 2010 and January 2015. Intraoperative ICG videoangiography was performed before and after bypass surgery. The MVTT was calculated from the ICG time intensity curve recorded in the pial arterioles and venules. Multivariate logistic regression analysis was conducted to test the effect of multiple variables, including the change in MVTT after bypass surgery, on postoperative HPS.RESULTSPostoperative HPS developed in 28 (26.7%) of the 105 hemispheres operated on. MVTT was reduced significantly after bypass surgery (prebypass 5.34 ± 2.00 sec vs postbypass 4.12 ± 1.60 sec; p < 0.001). The difference between prebypass and postbypass MVTT values, defined as ΔMVTT, was significantly greater in the HPS group than in the non-HPS group (2.55 ± 2.66 sec vs 0.75 ± 1.78 sec; p < 0.001). Receiver operating characteristic curve analysis revealed that the optimal cutoff point of ΔMVTT was 2.6 seconds (sensitivity 46.4% and specificity 85.7% as a predictor of postoperative HPS). A ΔMVTT > 2.6 seconds was an independent predictor of HPS in multivariate analysis (hazard ratio 4.88, 95% CI 1.76–13.57; p = 0.002).CONCLUSIONSMVTT in patients with MMD was reduced significantly after bypass surgery. Patients with a ΔMVTT > 2.6 seconds tended to develop postoperative HPS. Because ΔMVTT can be easily measured during surgery, it is a useful diagnostic tool for identifying patients at high risk for HPS after STA-MCA bypass surgery for MMD.


2020 ◽  
pp. 1-8
Author(s):  
Ryosuke Tashiro ◽  
Miki Fujimura ◽  
Masahito Katsuki ◽  
Taketo Nishizawa ◽  
Yasutake Tomata ◽  
...  

OBJECTIVESuperficial temporal artery–middle cerebral artery (STA-MCA) anastomosis is the standard surgical management for moyamoya disease (MMD), whereas cerebral hyperperfusion (CHP) is one of the potential complications of this procedure that can result in delayed intracerebral hemorrhage and/or neurological deterioration. Recent advances in perioperative management in the early postoperative period have significantly reduced the risk of CHP syndrome, but delayed intracerebral hemorrhage and prolonged/delayed CHP are still major clinical issues. The clinical implication of RNF213 gene polymorphism c.14576G>A (rs112735431), a susceptibility variant for MMD, includes early disease onset and a more severe form of MMD, but its significance in perioperative pathology is unknown. Thus, the authors investigated the role of RNF213 polymorphism in perioperative hemodynamics after STA-MCA anastomosis for MMD.METHODSAmong 96 consecutive adult patients with MMD comprising 105 hemispheres who underwent serial quantitative cerebral blood flow (CBF) analysis by N-isopropyl-p-[123I]iodoamphetamine SPECT after STA-MCA anastomosis, 66 patients consented to genetic analysis of RNF213. Patients were routinely maintained under strict blood pressure control during and after surgery. The local CBF values were quantified at the vascular territory supplied by the bypass on postoperative days (PODs) 1 and 7. The authors defined the radiological CHP phenomenon as a local CBF increase of more than 150% compared with the preoperative values, and then they investigated the correlation between RNF213 polymorphism and the development of CHP.RESULTSCHP at POD 1 was observed in 23 hemispheres (23/73 hemispheres [31.5%]), and its incidence was not statistically different between groups (15/41 [36.6%] in RNF213-mutant group vs 8/32 [25.0%] in RNF213–wild type (WT) group; p = 0.321). CHP on POD 7, which is a relatively late period of the CHP phenomenon in MMD, was evident in 9 patients (9/73 hemispheres [12.3%]) after STA-MCA anastomosis. This prolonged/delayed CHP was exclusively observed in the RNF213-mutant group (9/41 [22.0%] in the RNF213-mutant group vs 0/32 [0.0%] in the RNF213-WT group; p = 0.004). Multivariate analysis revealed that RNF213 polymorphism was significantly associated with CBF increase on POD 7 (OR 5.47, 95% CI 1.06–28.35; p = 0.043).CONCLUSIONSProlonged/delayed CHP after revascularization surgery was exclusively found in the RNF213-mutant group. Although the exact mechanism underlying the contribution of RNF213 polymorphism to the prolonged/delayed CBF increase in patients with MMD is unclear, the current study suggests that genetic analysis of RNF213 is useful for predicting the perioperative pathology of patients with MMD.


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