Combination of double and indirect two-sided revascularization of the brain in the treatment of moyamoya disease

Shul’gina A.A.; Lukshin V.A.; Korshunov A.E.; Usachev D.Iu.; Pronin I.N.

doi:https://doi.org/10.17116/neiro20208402193

Moyamoya disease is a rare hereditary chronic cerebrovascular disease characterized by slow progressive narrowing of the arteries of circle of Willis up to their complete occlusion [1, 2]. This disease is more common in Asian countries (prevalence 6–10 per 100 000) [3]. There are no national data on the incidence of moyamoya disease, all information is limited by small series, and case reports [4—6].

The disease is characterized by a deficiency of leptomeningeal vasculature following progressive steno-occlusive lesion of major cerebral arteries and insufficiency of natural extra-intracranial collaterals. Associated severe cerebrovascular insufficiency can lead to the development of ischemic stroke. Hemorrhagic course of moyamoya disease is caused by hemodynamic microaneurysms of intracranial collaterals. These aneurysms are presented as a puff of smoke on the angiograms (“moyamoya” from Japanese). This is a typical feature of this disease [7]. Surgery is preferred for both types of disease. The purpose of surgical interventions is formation of additional leptomeningeal network through extra-intracranial bypass (direct revascularization) and stimulation of leptomeningeal network through sinangiosis with vascularized tissues (indirect revascularization). Both methods are used individually and in combined fashion. Brain revascularization strategy, assessment of its effectiveness depending on the surgical procedure, age of patients and preoperative survey data are still discussable.

A rare variant of combination of bilateral double-barrel anastomoses with the most common methods of indirect brain revascularization is reported in the article. This approach ensured early postoperative compensation of cerebral blood flow in adult patient with moyamoya disease despite the progression of the disease.

Case report

A 27-year-old patient K. admitted to the Burdenko Neurosurgery Center in November 6, 2018. Complaints were persistent headaches, progressive fatigue and syncope. Сomputed tomography (CT) of the brain did not reveal significant changes. However, CT angiography found signs of bilateral stenoses of ICA bifurcations, bilateral stenoses of A1- and M1-segments of MCA and ACA, weak contrast enhancement of cortical vessels associated with enlarged basal collaterals of the brain (Fig. 1).

Fig. 1. Preoperative CT-angiography (13.08.2018). Axial (a) and coronal (b) planes: bifurcation stenosis of both ICA, bilateral stenoses of A1, M1 segments of MCA and ACA, abnormal basal vascular network ("moyamoya") (arrows).

These angiographic signs are characteristic for moyamoya disease Suzuki stage 3 [1].

CT perfusion was performed to assess severity of cerebrovascular insufficiency (Fig. 2).

Fig. 2. Preoperative CT perfusion (19.09.2018). Signs of cerebral blood flow decompensation in the pools of both MCA and ACA: increased MTT up to 10—12 sec in frontoparietal and temporal areas, more significant on the right (a), reduced regional blood flow in frontotoparietal and temporal areas up to 25—27 ml/100 g/min (pooled cerebral blood flow in the cortex and white matter) (b). The color scale reflects cerebral blood flow: red — high cerebral blood flow, > 60 ml/100 g/min, blue — low cerebral blood flow, <20 ml/100 g/min.

Significant bilateral circulatory deficiency in frontoparietal regions was observed. These disorders were more obvious on the right. There were reduced local blood flow within frontotoparietal cortex up to 25—27 ml/100 g/min (Fig. 2b), prolonged mean transit time (MTT) up to 10 seconds in the frontal lobes, up to 11 seconds in the left parietal lobe, up to 12 seconds in the right parietal lobe and up to 8—10 seconds in the posterior parietal areas. At the same time, MTT (3 sec) in the occipital lobes was normal (Fig. 2a).

Staged surgical treatment was proposed in order to prevent both ischemic (reduced cerebral blood flow) and hemorrhagic (increased blood flow through the enlarged basal collaterals) stroke.

Considering predominant perfusion deficiency in the right MCA pool, the first surgical procedure was carried out on November 7, 2018 (combined revascularization of the right MCA pool through bilateral extra-intracranial bypass anastomoses and encephaloduroarteriosynangiosis). Surgical intervention was carried out under endotracheal anesthesia in a patient’s lying position. The head was turned and fixed by a Mayfield stabilization system. Passage of both branches of superficial temporal artery was manually determined prior to marking of surgical approach (Fig. 3a).

Fig. 3. Stages of combined revascularization. a — marking of skin incisions in the right frontoparietal and occipital regions. b — wide craniotomy with exposure of dura mater over the Sylvian fissure, right frontal, parietal and temporal lobes. c – dissection of dura mater with preservation of the trunk and large branches of the middle meningeal artery. d — double extra-intracranial microvascular anastomosis. e – inverted flaps of dura mater under the edges of the bone defect – encephalodurosynanangiosis (arrows). f – dura mater defect is closed by temporal muscle — encephalomyosynanangiosis.

Arcuate incision in the right frontoparietal and temporal areas was followed by wide osteoplastic craniotomy 8 x 10 cm. Dura mater was exposed over the right frontal, parietal and temporal lobes (Fig. 3b). Frontal and parietal branches with a diameter of 1.2 mm were sequentially dissected for 6 and 8 cm, respectively. Wide bases of dura mater flaps were oriented towards a bone defect. These flaps were later used for dural synangiosis. We did not intersect the trunk of the middle meningeal artery and its major branches in order to preserve natural extra-intracranial dural-cortical anastomoses (Fig. 3c). Two extra-intracranial anastomoses were formed between the frontal and temporal cortical arteries in order to increase revascularization volume (Fig. 3d). Time of cross-clamping of cortical arteries was 23 and 25 minutes, respectively. Donor arteries were additionally sutured to pia mater in order to create encephaloarteriosynangiosis. The flaps of dura mater were inverted under the edges of craniotomy to form encephalodurosynangiosis (Fig. 3e). Dissected temporal muscle (myosynangiosis) was placed on the frontotemporal and parietal cortex and fixed to the edge of craniotomy for closure of dura mater defect (Fig. 3f). Sutures were sealed with a tachocomb. Basal resection of the bone flap within 1 cm was applied to avoid muscle compression. Finally, bone flap was fixed by interrupted sutures.

The patient safely underwent intervention. Clinical condition remained stable in postoperative period. The patient noted improvement including increased activity, reduce incidence and severity of headache and regression of syncope.

Control MRI in 3 months after surgery confirmed bilateral progression of M1-segment stenoses up to their complete occlusion (Fig. 4a).

Fig. 4. Control MR angiography in 3 months after the first surgery. a — progression of bifurcation stenosis of both ICAs, occlusion of both MCAs, bilateral stenosis of ACA (red arrows); b — patent MCA-STA anastomosis (major trunk and both branches) (yellow arrow), network of collateral vessels de novo — indirect component (green arrow); c — ASL perfusion: improved perfusion of the right hemisphere (red arrow), significant perfusion deficit of the left hemisphere (yellow arrow).

Both anastomoses were visualized with signs of hypertrophy of the trunk and branches of superficial temporal artery. Moreover, leptomeningeal collaterals de novo within indirect myosynangiosis were also revealed (Fig. 4a, b). These structures ensured improvement of cerebral blood flow despite progression of bilateral bifurcation stenosis of ICA and occlusion of M1-segment of the right MCA. It was confirmed by ASL perfusion. There were signs of restored cerebral blood flow in the pool of the right MCA up to 40—45 ml/100 g/min with persistent low CBF values on the left (25—30 ml/100 g/min ) (Fig. 4c).

Considering perfusion deficit within the left MCA pool, the second surgical stage was made on March 28, 2019 (combined revascularization of the left MCA through two extra-intracranial bypass anastomoses and encephaloduroarteriomyosynangiosis on the left).

Surgical technique was the same. The patient safely underwent intervention. Cerebrovascular accidents were not observed in postoperative period.

Control CT angiography on the 7th postoperative day revealed bilateral patent double anastomoses (Fig. 5a—e).

Fig. 5. Control CT angiography in 7 days after the second operation. Frontal (a) and axial (b) planes, c—e — 3D reconstruction. Patent bilateral double extra-intracranial anastomoses, enlarged STA trunks (red arrows), a network of leptomeningeal collaterals de novo in the area of indirect synangiosis (yellow arrow) are visualized.

Improvement of perfusion parameters including bilateral restoration of MTT up to 3—4 sec (Fig. 6a)

Fig. 6. Control CT perfusion in 7 days after the second operation. Improved perfusion of the left hemisphere with reduced MTT in both hemispheres up to normal values (3 sec) (a), bilateral decrease of cerebral blood flow up to 1.2 ml/100 g in frontoparietal regions (b), increased CBF in frontoparietal areas up to 40—45 ml/100 g/min (c).

and significant augmentation of CBF compared with preoperative data was observed (Fig. 6b, c). ASL perfusion confirmed no hemispheric asymmetry of cerebral blood flow due to bilateral increase of CBF up to 40—45 ml/100g/min. Further clinical improvement with regression of syncope was noted.

Control MRI in 6 months after the second operation confirmed progression of the underlying disease with occlusion of both ICA, MCA and ACA (Fig. 7a).

Fig. 7. Comprehensive MRI in 6 months after the second operation. a — 3D TOF MRI: progression of the underlying disease – bilateral occlusion of ICA, MCA, ACA (red arrows), patent bilateral double MCA-STA anastomoses, enlarged STA trunk (yellow arrows); b — ASL perfusion: normalization of CBF in both hemispheres — 55—65 ml/100g/min (arrows).

However, patent double-barrel bilateral extra-intracranial anastomoses and leptomeningeal collaterals de novo ensured complete circulatory compensation up to 55—65 ml/100 g/min without interhemispheric asymmetry (Fig. 7b).

Discussion

Moyamoya disease is rarely diagnosed in the Russian Federation. Therefore, the algorithm of examination and surgical treatment is still unclear.

In this report, the most common course of disease with widespread stenoses of the arteries of circle of Willis followed by severe cerebral ischemia is presented. Thus, increased MTT (over 11 seconds) in both MCA pools combined with reduced regional blood flow by more than 30% corresponded to threshold values of decompensated cerebral blood flow with increased risk of ischemic stroke [8]. Moreover, dominant compensation of cerebral blood flow through the enlarged basal collaterals was associated with increased risk of hemorrhagic stroke [9]. Thus, neuroimaging data combined with characteristic clinical symptoms and progressive course of disease determined the indications for surgical treatment (brain revascularization through collateral blood flow pathways de novo) [10].

Surgical treatment of moyamoya disease was developed in the 70s of the XX century when direct and indirect brain revascularization has been applied. In 1972, MCA-STA bypass surgery was first performed in a patient with moyamoya disease [11—12]. An alternative approach implies translocation of well-vascularized soft tissues directly on the brain surface. These measures facilitate neoangiogenesis followed by development of spontaneous extra-intracranial anastomoses from external carotid artery [13—15]. Each of these methods of surgical treatment of moyamoya disease is characterized by certain advantages and disadvantages [10, 16, 17]. Nevertheless, overall correlation between the outcomes of brain revascularization and degree of compensation of cerebral blood flow through anastomoses de novo was confirmed [18]. One of the approaches ensuring increased number of these collaterals and revascularization volume is a combination of direct anastomoses and indirect synangioses [16]. These techniques have been described since the 90s [19] and reflect the current trend in surgical treatment of moyamoya disease. At the same time, combined brain revascularization has not been considered in detail in national literature.

In this report, combined revascularization of both hemispheres with maximum application of all available donor vessels of external carotid artery was preferred considering preoperative symptoms of severe moyamoya disease followed by cerebrovascular insufficiency. Both branches of superficial temporal artery were used for direct anastomoses, branches of middle meningeal artery – for dural synangiosis, branches of deep temporal artery – for myosynangiosis [16]. Two-stage surgical approach was applied. In case of bilateral lesion, the hemisphere for primary intervention is usually determined by predominant symptoms [16]. Dominant hemisphere or hemisphere with prevailed perfusion deficiency is preferred if lateralization of focal neurological symptoms is absent [16].

Considering the signs of separated blood supply of the frontal and temporal lobes due to severe stenotic lesion of M1-segment of MCA and no compensatory flows through the distal branches of MCA, two MCA-STA anastomoses were imposed using both branches of STA. In this case, cortical arteries of the M4-segment of MCA on both sides from Sylvian fissure were chosen as acceptor arteries. Additional revascularization factors were suturing of both donor arteries of MCA-STA anastomoses to the pia mater to create encephaloarteriosynangiosis and the widest possible area of dural and myosynangioses due to advanced craniotomy.

It is noteworthy that the first stage of revascularization was followed by bilateral occlusion of MCA. The last one maybe associated with progression of the underlying disease and hemodynamic restructuring of cerebral blood flow through leptomeningeal and pial arteries [20]. These process, in turn, can lead to regression of enlarged basal vessels of the brain [21].

Combined revascularization showed high efficiency. Control CT angiography after 3 months revealed extensive network of extra-intracranial collaterals ensuring compensation of perfusion deficiency. Thus, surgical approach was valuable to prevent a probable ischemic stroke associated with progression of stenosis and occlusion of M1-segment of MCA and also to improve clinical condition of the patient. Visualization of direct anastomoses and indirect synangioses should be emphasized. These data confirm high efficiency of combined revascularization in children and adults for improvement of their prognosis [18, 22].

Undoubtedly, the role of direct and indirect components of revascularization in overall improvement of cerebral blood supply, the likelihood of long-term postoperative adverse effects and comparison of combined and isolated methods of revascularization are of interest. Data of researches devoted to these issues will be presented in subsequent manuscripts.

Conclusion

High efficiency of combined brain revascularization in the treatment of a patient with moyamoya disease is reported. This procedure made it possible to compensate cerebral blood supply and prevent possible cerebrovascular disturbances despite the progression of stenotic and occlusive lesion. A large role belongs to double-barrel MCA-STA anastomoses ensuring compensation of severe perfusion deficiency in early postoperative period. Neoangiogenesis and development of leptomeningeal vessels after indirect synangioses indicate advisability of these procedures for combined brain revascularization.

The authors declare no conflicts of interest.

Commentary

Successful treatment of adult patient with moyamoya disease is reported. This is a rare stenotic-occlusive vascular disease in the Russian Federation. There is more than 50-year world experience of brain revascularization in the treatment of this disease. However, national researches devoted to surgical treatment of moyamoya disease are few that emphasizes an importance of this report.

The authors used an interesting combination of various techniques for revascularization. This approach ensured early postoperative compensation of severe cerebrovascular insufficiency and prevention of possible adverse consequences. At the same time, an importance of various components of revascularization (direct MCA-STA anastomosis and indirect synanangiosis) is emphasized. CT-confirmed network of leptomeningeal collaterals de novo within indirect synangiosis emphasizes the effectiveness of indirect components even in adult patients. This is of great practical importance, since it justifies advisability of combined interventions in children and adults.

Clinical data, indications for surgery, data of pre- and postoperative survey are justified and do not cause objection. The manuscript is well illustrated and may be used as a guide for combined brain revascularization. It is also interesting to analyze the long-term outcomes of this procedure and compare these results with direct and indirect revascularization. Publication of these data in further issues would be desirable.

V.A. Lazarev (Moscow, Russia)

References:

Suzuki J, Takaku A. Cerebrovascular «moyamoya» disease. Disease showing abnormal net-like vessels in base of brain. Archives of Neurology. 1969;20:288-299. https://doi.org/10.1001/archneur.1969.00480090076012
Akagawa H, Mukawa M, Nariai T, Nomura S, Aihara Y, Onda H, Yoneyama T, Kudo T, Sumita K, Maehara T, Kawamata T, Kasuya H. Novel and recurrent RNF213 variants in Japanese pediatric patients with moyamoya disease. Human Genome Variation. 2018;25(5):17060. https://doi.org/10.1038/hgv.2017.60
Weidner W, Hanafee W, Markham CH. Intracranial collateral circulation via leptomeningeal and rete mirabile anastomoses. Neurology. 1965;15:39-48. https://doi.org/10.1212/wnl.15.1.39
Буркова К.И., Ажермачева М.Н., Алифирова В.М. Болезнь моя-моя (клиническое наблюдение). Неврологический журнал. 2014;5:38-42.
Коршунов А.Е., Головтеев А.Л., Аронов М.С. Успешное лечение болезни мойямойя у ребенка методом энцефало-дуро-артериосинангиоза. Вопросы нейрохирургии им. Н.Н. Бурденко. 2010;1:54-58.
Злотник Э.И., Кузнецов В.Ф., Кастрицкая З.М., Беззубик С.Д. Болезнь мойямойя. Вопросы нейрохирургии. 1978;2:41-46.
Takeuchi K, Shimizu K. Hypoplasia of the bilateral internal carotid arteries. No To Shinkei. 1957;9:37-43.
Wintermark M, Flanders AE, Velthuis B, Meuli R, van Leeuwen M, Goldsher D, Pineda C, Serena J, van der Schaaf I, Waaijer A, Anderson J, Nesbit G, Gabriely I, Medina V, Quiles A, Pohlman S, Quist M, Schnyder P, Bogousslavsky J, Dillon WP, Pedraza S. Perfusion-CT assessment of infarct core and penumbra: receiver operating characteristic curve analysis in 130 patients suspected of acute hemispheric stroke. Stroke. 2006;37:979-985. https://doi.org/10.1161/01.STR.0000209238.61459.39
Funaki T, Takahashi JC, Houkin K, Kuroda S, Takeuchi S, Fujimura M, Tomata Y, Miyamoto S. Angiographic features of hemorrhagic moyamoya disease with high recurrence risk: a supplementary analysis of the Japan Adult Moyamoya Trial. Journal of Neurosurgery. 2018;128(3):777-784. https://doi.org/10.3171/2016.11.JNS161650
Guzman R, Lee M, Achrol A, Bell-Stephens T, Kelly M, Do HM, Marks MP, Steinberg GK. Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article. Journal of Neurosurgery. 2009;111(5):927-935. https://doi.org/10.3171/2009.4.JNS081649
Yasargil MG, Yonekawa Y. Results of microsurgical extra-intracranial arterial bypass in the treatment of cerebral ischemia. Neurosurgery. 1977;1(1):22-24. https://doi.org/10.1227/00006123-197707000-00005
Karasawa J, Kikuchi H, Furuse S, Kawamura J, Sakaki T. Treatment of moyamoya disease with STA-MCA anastomosis. Journal of Neurosurgery. 1978;49:679-688. https://doi.org/10.3171/jns.1978.49.5.0679
Spetzler RF, Roski RA, Kopaniky DR. Alternative superficial temporal artery to middle cerebral artery revascularization procedure. Neurosurgery. 1980;7:484-485. https://doi.org/10.1227/00006123-198011000-00012
Matsushima T, Inoue TK, Suzuki SO, Inoue T, Ikezaki K, Fukui M, Hasuo K. Surgical treatment for pediatric patients with moyamoya disease by indirect revascularization procedures (EDAS, EMS, EMAS). Acta Neurochirurgica. 1989;98:135-140. https://doi.org/10.1016/s0303-8467(97)00076-0
Matsushima T, Fukui M, Kitamura K, Hasuo K, Kuwabara Y, Kurokawa T. Encephalo-duro-arterio-synangiosis in children with moyamoya disease. Acta Neurochirurgica. 1990;104:961-902. https://doi.org/10.1007/bf01842826
Xu B, Song DL, Mao Y, Gu YX, Xu H, Liao YJ, Liu CH, Zhou LF Superficial temporal artery-middle cerebral artery bypass combined with encephalo-duro-myo-synangiosis in treating moyamoya disease: surgical techniques, indications and midterm follow-up results. Chinese Medical Journal. 2012;125(24):4398-405.
Amin-Hanjani S, Singh A, Rifai H, Thulborn KR, Alaraj A, Aletich V, Charbel FT. Combined direct and indirect bypass for moyamoya: quantitative assessment of direct bypass flow over time. Neurosurgery. 2013;73(6):962-967. https://doi.org/10.1227/NEU.0000000000000139
Zhao J, Liu H, Zou Y, Zhang W, He S. Clinical and angiographic outcomes after combined direct and indirect bypass in adult patients with moyamoya disease: A retrospective study of 76 procedures. Experimental and Therapeutic Medicine. 2018;15(4):3570-3576. https://doi.org/10.3892/etm.2018.5850
Houkin K, Kamiyama H, Takahashi A, Kuroda S, Abe H. Combined revascularization surgery for childhood moyamoya disease: STA-MCA and encephalo-duro-arterio-myo-synangiosis. Child’s Nervous System. 1997;13(1):24-29. https://doi.org/10.1007/s003810050034
Филатов Ю.М., Шахнович А.Р. Влияние экстра-интракраниальных анастомозов на эволюцию стенозов в системе внутренней сонной артерии. Вопросы нейрохирургии. 1985;4:8-14.
Sahoo SS, Suri A, Bansal S, Devarajan SLJ, Sharma B S. Outcome of revascularization in moyamoya disease: Evaluation of a new angiographic scoring system. Asian Journal of Neurosurgery. 2015;10(4):252-259. https://doi.org/10.4103/1793-5482.162681
Chen Z, Zhang L, Qu J, Wu Y, Mao G, Zhu X, Zhu J Clinical analysis of combined revascularization in treating ischemic Moyamoya disease in adults. Neurochirurgie. 2018;64(1):49-52. https://doi.org/10.1016/j.neuchi.2017.08.005