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Published in: Journal of Neurology 10/2018

01-10-2018 | Original Communication

Efficacy of STA–MCA bypass surgery in moyamoya angiopathy: long-term follow-up of the Caucasian Krupp Hospital cohort with 81 procedures

Authors: Markus Kraemer, Rusen Karakaya, Toshinori Matsushige, Jonas Graf, Philipp Albrecht, Hans-Peter Hartung, Peter Berlit, Rudolf Laumer, Frank Diesner

Published in: Journal of Neurology | Issue 10/2018

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Abstract

Background

Despite the consensus on the efficacy of revascularizing surgery in moyamoya angiopathy (MA) in Asia, the indication in Caucasian moyamoya patients is controversially discussed.

Objective

The efficacy of revascularizing surgery in adult European patients with MA should be clarified.

Methods

This study retrospectively analyzed the rate of further strokes and hemorrhages as well as MRI and Duplex ultrasound features during long-term follow up after STA–MCA bypass.

Results

Eighty-one STA–MCA bypass procedures in 54 patients with MA operated in one single German institution were analyzed. All 54 patients (100%) were Caucasians. After two diffusion restricted spots in MRI perioperatively (2.5%) and short-lasting symptoms directly after surgery, no patient experienced further new symptoms related to stroke or hemorrhages nor no new gliotic scars or microbleeds on MRI for 38.2 months. Duplex ultrasound 3 months after surgery documented bypass patency in 100% and sonographic sign for good relevance of the bypass in 96.2%. In addition, the diameter of the donor vessel had increased in 89.9% as an indicator for the relevance of the bypass. Semi-quantitative analysis of perfusion changes in the operated hemispheres demonstrated an increase in perfusion in the MCA territory in 56 of 74 (75.7%) hemispheres 36.7 months after surgery. In MRA images, a reduction of typical moyamoya collaterals was found in 65 of 79 hemispheres (82.3%) after a mean of 37.2 months.

Conclusion

Direct STA–MCA bypass is an effective therapy in Caucasian patients with hemodynamically compromised MA.
Literature
1.
go back to reference Kraemer M, Trakolis L, Platzen J et al (2016) Movement symptoms in European moyamoya angiopathy—first systematic questionnaire study. Clin Neurol Neurosurg 152:52–56CrossRef Kraemer M, Trakolis L, Platzen J et al (2016) Movement symptoms in European moyamoya angiopathy—first systematic questionnaire study. Clin Neurol Neurosurg 152:52–56CrossRef
2.
go back to reference Kraemer M, Lee SI, Ayzenberg I et al (2016) Headache in Caucasian patients with moyamoya angiopathy—a systematic cohort study. Cephalalgia 160:137–141 Kraemer M, Lee SI, Ayzenberg I et al (2016) Headache in Caucasian patients with moyamoya angiopathy—a systematic cohort study. Cephalalgia 160:137–141
3.
go back to reference Liu P, Liu AH, Han C et al (2016) Difference in angiographic characteristics between hemorrhagic and nonhemorrhagic hemispheres associated with hemorrhage risk of moyamoya disease in adults: a self-controlled study. World Neurosurg 95:348–356CrossRef Liu P, Liu AH, Han C et al (2016) Difference in angiographic characteristics between hemorrhagic and nonhemorrhagic hemispheres associated with hemorrhage risk of moyamoya disease in adults: a self-controlled study. World Neurosurg 95:348–356CrossRef
4.
go back to reference Kraemer M, Berlit P, Diesner F, Khan N (2012) What is the expert’s option on antiplatelet therapy in moyamoya disease? Results of a worldwide Survey. Eur J Neurol 19:163–167CrossRef Kraemer M, Berlit P, Diesner F, Khan N (2012) What is the expert’s option on antiplatelet therapy in moyamoya disease? Results of a worldwide Survey. Eur J Neurol 19:163–167CrossRef
5.
go back to reference Schubert GA, Biermann P, Weiss C et al (2014) Risk profile in extracranial/intracranial bypass surgery—the role of antiplatelet agents, disease pathology, and surgical technique in 168 direct revascularization procedures. World Neurosurg 82(5):672–677CrossRef Schubert GA, Biermann P, Weiss C et al (2014) Risk profile in extracranial/intracranial bypass surgery—the role of antiplatelet agents, disease pathology, and surgical technique in 168 direct revascularization procedures. World Neurosurg 82(5):672–677CrossRef
6.
go back to reference Ganesan V (2010) Moyamoya: to cut or not to cut is not the only question. A paediatric neurologist’s perspective. Dev Med Child Neurol 52(1):10–13CrossRef Ganesan V (2010) Moyamoya: to cut or not to cut is not the only question. A paediatric neurologist’s perspective. Dev Med Child Neurol 52(1):10–13CrossRef
7.
go back to reference Health Labour Sciences Research Grant for Research on Measures for Infractable D. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis) (2012) Treatment of spontaneous occlusion of the circle of W. Neurol Med Chir (Tokyo) 52(5):245–266CrossRef Health Labour Sciences Research Grant for Research on Measures for Infractable D. Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis) (2012) Treatment of spontaneous occlusion of the circle of W. Neurol Med Chir (Tokyo) 52(5):245–266CrossRef
8.
go back to reference Derdeyn CP (2014) Direct bypass reduces the risk of recurrent hemorrhage in moyamoya syndrome, but effect on functional outcome is less certain. Stroke 45(5):1245–1246CrossRef Derdeyn CP (2014) Direct bypass reduces the risk of recurrent hemorrhage in moyamoya syndrome, but effect on functional outcome is less certain. Stroke 45(5):1245–1246CrossRef
9.
go back to reference Kawaguchi S, Okuno S, Sakaki T (2000) Effect of direct arterial bypass on the prevention of future stroke in patients with the hemorrhagic variety of moyamoya disease. J Neurosurg 93(3):397–401CrossRef Kawaguchi S, Okuno S, Sakaki T (2000) Effect of direct arterial bypass on the prevention of future stroke in patients with the hemorrhagic variety of moyamoya disease. J Neurosurg 93(3):397–401CrossRef
10.
go back to reference Kuroda S (2017) Strategy and tactics of bypass surgery for moyamoya disease. Acta Neurochir (Wien) 159(8):1495–1496CrossRef Kuroda S (2017) Strategy and tactics of bypass surgery for moyamoya disease. Acta Neurochir (Wien) 159(8):1495–1496CrossRef
11.
go back to reference Fujimura M, Mugikura S, Kaneta T, Shimizu H, Tominaga T (2009) Incidence and risk factors for symptomatic cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease. Surg Neurol 71(4):442–447CrossRef Fujimura M, Mugikura S, Kaneta T, Shimizu H, Tominaga T (2009) Incidence and risk factors for symptomatic cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease. Surg Neurol 71(4):442–447CrossRef
12.
go back to reference Fujimura M, Tominaga T (2012) Lessons learned from moyamoya disease: outcome of direct/indirect revascularization surgery for 150 affected hemispheres. Neurol Med Chir (Tokyo) 52(5):327–332CrossRef Fujimura M, Tominaga T (2012) Lessons learned from moyamoya disease: outcome of direct/indirect revascularization surgery for 150 affected hemispheres. Neurol Med Chir (Tokyo) 52(5):327–332CrossRef
13.
go back to reference Kazumata K, Ito M, Tokairin K et al (2014) The frequency of postoperative stroke in moyamoya disease following combined revascularization: a single-university series and systematic review. J Neurosurg 121(2):432–440CrossRef Kazumata K, Ito M, Tokairin K et al (2014) The frequency of postoperative stroke in moyamoya disease following combined revascularization: a single-university series and systematic review. J Neurosurg 121(2):432–440CrossRef
14.
go back to reference Yu J, Shi L, Guo Y, Xu B, Xu K (2016) Progress on complications of direct bypass for moyamoya disease. Int J Med Sci 13(8):578–587CrossRef Yu J, Shi L, Guo Y, Xu B, Xu K (2016) Progress on complications of direct bypass for moyamoya disease. Int J Med Sci 13(8):578–587CrossRef
15.
go back to reference Ge P, Zhang Q, Ye X et al (2017) Long-term outcome after conservative treatment and direct bypass surgery of moyamoya disease at late suzuki stage. World Neurosurg 103:283–290CrossRef Ge P, Zhang Q, Ye X et al (2017) Long-term outcome after conservative treatment and direct bypass surgery of moyamoya disease at late suzuki stage. World Neurosurg 103:283–290CrossRef
16.
go back to reference Kim H, Jang DK, Han YM et al (2016) Direct bypass versus indirect bypass in adult moyamoya angiopathy with symptoms or hemodynamic instability: a meta-analysis of comparative studies. World Neurosurg 94:273–284CrossRef Kim H, Jang DK, Han YM et al (2016) Direct bypass versus indirect bypass in adult moyamoya angiopathy with symptoms or hemodynamic instability: a meta-analysis of comparative studies. World Neurosurg 94:273–284CrossRef
17.
go back to reference Liu L, Su SW, Sun HY (2017) Safety of extracranial–intracranial arterial bypass in the treatment of moyamoya disease. J Craniofac Surg 28(6):e522–e527CrossRef Liu L, Su SW, Sun HY (2017) Safety of extracranial–intracranial arterial bypass in the treatment of moyamoya disease. J Craniofac Surg 28(6):e522–e527CrossRef
18.
go back to reference EC/IC Bypass Study Group (1985) Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. The EC/IC Bypass Study Group. N Engl J Med 313(19):1191–1200CrossRef EC/IC Bypass Study Group (1985) Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke. Results of an international randomized trial. The EC/IC Bypass Study Group. N Engl J Med 313(19):1191–1200CrossRef
19.
go back to reference Powers WJ, Clarke WR, Grubb RL Jr et al (2011) Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the Carotid Occlusion Surgery Study randomized trial. JAMA 306(18):1983–1992CrossRef Powers WJ, Clarke WR, Grubb RL Jr et al (2011) Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the Carotid Occlusion Surgery Study randomized trial. JAMA 306(18):1983–1992CrossRef
20.
go back to reference Powers WJ, Grubb RL Jr, Raichle ME (1989) Clinical results of extracranial-intracranial bypass surgery in patients with hemodynamic cerebrovascular disease. J Neurosurg 70(1):61–67CrossRef Powers WJ, Grubb RL Jr, Raichle ME (1989) Clinical results of extracranial-intracranial bypass surgery in patients with hemodynamic cerebrovascular disease. J Neurosurg 70(1):61–67CrossRef
21.
go back to reference Ogawa S, Abe H, Katsuta T et al (2017) Early and noninvasive evaluation using superficial temporal artery duplex ultrasonography after indirect bypass for adult ischemic moyamoya disease. Acta Neurochir (Wien) 159(3):577–582CrossRef Ogawa S, Abe H, Katsuta T et al (2017) Early and noninvasive evaluation using superficial temporal artery duplex ultrasonography after indirect bypass for adult ischemic moyamoya disease. Acta Neurochir (Wien) 159(3):577–582CrossRef
22.
go back to reference Saito N, Nakagawara J, Nakamura H, Teramoto A (2004) Assessment of cerebral hemodynamics in childhood moyamoya disease using a quantitative and a semiquantitative IMP-SPECT study. Ann Nucl Med 18(4):323–331CrossRef Saito N, Nakagawara J, Nakamura H, Teramoto A (2004) Assessment of cerebral hemodynamics in childhood moyamoya disease using a quantitative and a semiquantitative IMP-SPECT study. Ann Nucl Med 18(4):323–331CrossRef
23.
go back to reference Kurokawa T, Tomita S, Ueda K et al (1985) Prognosis of occlusive disease of the circle of Willis (moyamoya disease) in children. Pediatr Neurol 1(5):274–277CrossRef Kurokawa T, Tomita S, Ueda K et al (1985) Prognosis of occlusive disease of the circle of Willis (moyamoya disease) in children. Pediatr Neurol 1(5):274–277CrossRef
24.
go back to reference Kim YO, Joo SP, Seo BR, Rho YI, Yoon W, Woo YJ (2013) Early clinical characteristics according to developmental stage in children with definite moyamoya disease. Brain Dev 35(6):569–574CrossRef Kim YO, Joo SP, Seo BR, Rho YI, Yoon W, Woo YJ (2013) Early clinical characteristics according to developmental stage in children with definite moyamoya disease. Brain Dev 35(6):569–574CrossRef
25.
go back to reference Hallemeier CL, Rich KM, Grubb RL Jr et al (2006) Clinical features and outcome in North American adults with moyamoya phenomenon. Stroke 37(6):1490–1496CrossRef Hallemeier CL, Rich KM, Grubb RL Jr et al (2006) Clinical features and outcome in North American adults with moyamoya phenomenon. Stroke 37(6):1490–1496CrossRef
26.
go back to reference Kraemer M, Heienbrok W, Berlit P (2008) Moyamoya disease in Europeans. Stroke 39(12):3193–3200CrossRef Kraemer M, Heienbrok W, Berlit P (2008) Moyamoya disease in Europeans. Stroke 39(12):3193–3200CrossRef
27.
go back to reference Lanterna LA, Brembilla C, Gritti P, Bernucci C (2016) Universal bypass for treatment of symptomatic moyamoya disease or moyamoya syndrome. Analysis of a personal case series on behalf of the Italian Moyamoya Association. Acta Neurochir Suppl 123:129–132CrossRef Lanterna LA, Brembilla C, Gritti P, Bernucci C (2016) Universal bypass for treatment of symptomatic moyamoya disease or moyamoya syndrome. Analysis of a personal case series on behalf of the Italian Moyamoya Association. Acta Neurochir Suppl 123:129–132CrossRef
28.
go back to reference Khan N, Schuknecht B, Boltshauser E et al (2003) Moyamoya disease and moyamoya syndrome: experience in Europe; choice of revascularisation procedures. Acta Neurochir (Wien) 145(12):1061–1071 (discussion 1071) CrossRef Khan N, Schuknecht B, Boltshauser E et al (2003) Moyamoya disease and moyamoya syndrome: experience in Europe; choice of revascularisation procedures. Acta Neurochir (Wien) 145(12):1061–1071 (discussion 1071) CrossRef
29.
go back to reference Czabanka M, Pena-Tapia P, Scharf J et al (2011) Characterization of direct and indirect cerebral revascularization for the treatment of European patients with moyamoya disease. Cerebrovasc Dis 32(4):361–369CrossRef Czabanka M, Pena-Tapia P, Scharf J et al (2011) Characterization of direct and indirect cerebral revascularization for the treatment of European patients with moyamoya disease. Cerebrovasc Dis 32(4):361–369CrossRef
30.
go back to reference Hanggi D, Mehrkens JH, Schmid-Elsaesser R, Steiger HJ (2008) Results of direct and indirect revascularisation for adult European patients with moyamoya angiopathy. Acta Neurochir Suppl 103:119–122CrossRef Hanggi D, Mehrkens JH, Schmid-Elsaesser R, Steiger HJ (2008) Results of direct and indirect revascularisation for adult European patients with moyamoya angiopathy. Acta Neurochir Suppl 103:119–122CrossRef
31.
go back to reference Herve D, Kossorotoff M, Bresson D et al (2018) French clinical practice guidelines for moyamoya angiopathy. Rev Neurol (Paris) 174(5):292–303CrossRef Herve D, Kossorotoff M, Bresson D et al (2018) French clinical practice guidelines for moyamoya angiopathy. Rev Neurol (Paris) 174(5):292–303CrossRef
32.
go back to reference Ha M, Choi CH, Lee JI, Cha SH, Lee SW, Ko JK (2016) The efficacy of single barrel superficial temporal artery-middle cerebral artery bypass in treatment of adult patients with ischemic-type moyamoya disease. J Cerebrovasc Endovasc Neurosurg 18(3):239–246CrossRef Ha M, Choi CH, Lee JI, Cha SH, Lee SW, Ko JK (2016) The efficacy of single barrel superficial temporal artery-middle cerebral artery bypass in treatment of adult patients with ischemic-type moyamoya disease. J Cerebrovasc Endovasc Neurosurg 18(3):239–246CrossRef
33.
go back to reference Bao XY, Zhang Y, Wang QN et al (2018) Long-term outcomes after encephaloduroarteriosynangiosis in adult patients with moyamoya disease presenting with ischemia. World Neurosurg 115:e482–e489CrossRef Bao XY, Zhang Y, Wang QN et al (2018) Long-term outcomes after encephaloduroarteriosynangiosis in adult patients with moyamoya disease presenting with ischemia. World Neurosurg 115:e482–e489CrossRef
34.
go back to reference Hanggi D, Steiger HJ, Vajkoczy P (2014) The role of MCA-STA bypass surgery after COSS and JET: the European point of view. Acta Neurochir Suppl 119:77–78PubMed Hanggi D, Steiger HJ, Vajkoczy P (2014) The role of MCA-STA bypass surgery after COSS and JET: the European point of view. Acta Neurochir Suppl 119:77–78PubMed
35.
go back to reference Grubb RL Jr, Powers WJ, Clarke WR et al (2013) Surgical results of the Carotid Occlusion Surgery Study. J Neurosurg 118(1):25–33CrossRef Grubb RL Jr, Powers WJ, Clarke WR et al (2013) Surgical results of the Carotid Occlusion Surgery Study. J Neurosurg 118(1):25–33CrossRef
36.
go back to reference Krämer M (2015) Über den Stellenwert der Duplexsonografie und der transkraniellen Doppler-Emboliedetektion bei der Moyamoya-Angiopathie. Klin Neurophysiol 46(01):47–49CrossRef Krämer M (2015) Über den Stellenwert der Duplexsonografie und der transkraniellen Doppler-Emboliedetektion bei der Moyamoya-Angiopathie. Klin Neurophysiol 46(01):47–49CrossRef
37.
go back to reference Yeh SJ, Tang SC, Tsai LK et al (2017) Color Doppler ultrasonography as an alternative tool for postoperative evaluation of collaterals after indirect revascularization surgery in moyamoya disease. PLoS One 12(12):e0188948CrossRef Yeh SJ, Tang SC, Tsai LK et al (2017) Color Doppler ultrasonography as an alternative tool for postoperative evaluation of collaterals after indirect revascularization surgery in moyamoya disease. PLoS One 12(12):e0188948CrossRef
38.
go back to reference Kraemer M, Schuknecht B, Jetzer AK, Yonekawa Y, Khan N (2012) Postoperative changes in the superficial temporal artery and the external carotid artery duplex sonography after extra-intracranial bypass surgery in European moyamoya disease. Clin Neurol Neurosurg 114(7):930–934CrossRef Kraemer M, Schuknecht B, Jetzer AK, Yonekawa Y, Khan N (2012) Postoperative changes in the superficial temporal artery and the external carotid artery duplex sonography after extra-intracranial bypass surgery in European moyamoya disease. Clin Neurol Neurosurg 114(7):930–934CrossRef
39.
go back to reference Wang Y, Chen L, Wang Y et al (2014) Hemodynamic study with duplex ultrasonography on combined (direct/indirect) revascularization in adult moyamoya disease. J Stroke Cerebrovasc Dis 23(10):2573–2579CrossRef Wang Y, Chen L, Wang Y et al (2014) Hemodynamic study with duplex ultrasonography on combined (direct/indirect) revascularization in adult moyamoya disease. J Stroke Cerebrovasc Dis 23(10):2573–2579CrossRef
41.
go back to reference Jin Q, Noguchi T, Irie H et al (2011) Assessment of moyamoya disease with 3.0-T magnetic resonance angiography and magnetic resonance imaging versus conventional angiography. Neurol Med Chir (Tokyo) 51(3):195–200CrossRef Jin Q, Noguchi T, Irie H et al (2011) Assessment of moyamoya disease with 3.0-T magnetic resonance angiography and magnetic resonance imaging versus conventional angiography. Neurol Med Chir (Tokyo) 51(3):195–200CrossRef
42.
go back to reference Matsushige MK, Berlit P, Forsting M, Ladd ME, Sure U, Khan N, Schlamann M, Wrede KH (2018) Visualization and classification of deeply seated collateral networks in moyamoya angiopathy with 7T MRI. Am J Neuroradiol 2018:29880473 Matsushige MK, Berlit P, Forsting M, Ladd ME, Sure U, Khan N, Schlamann M, Wrede KH (2018) Visualization and classification of deeply seated collateral networks in moyamoya angiopathy with 7T MRI. Am J Neuroradiol 2018:29880473
Metadata
Title
Efficacy of STA–MCA bypass surgery in moyamoya angiopathy: long-term follow-up of the Caucasian Krupp Hospital cohort with 81 procedures
Authors
Markus Kraemer
Rusen Karakaya
Toshinori Matsushige
Jonas Graf
Philipp Albrecht
Hans-Peter Hartung
Peter Berlit
Rudolf Laumer
Frank Diesner
Publication date
01-10-2018
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 10/2018
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-018-9031-4

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