Strategy and effect of repeat bypass surgery for anterior/posterior circulation in refractory moyamoya disease

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  • 1 Department of Neurosurgery, Graduate School of Medicine and Pharmaceutical Science, University of Toyama, Toyama; and
  • 2 Department of Neurosurgery, Hokkaido University Graduate School of Medicine, Sapporo, Japan
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OBJECTIVE

In this study the authors aimed to describe clinical features, surgical techniques, and long-term outcomes of repeat bypass surgery required for a certain subset of patients with moyamoya disease.

METHODS

The authors retrospectively reviewed a total of 22 repeat bypass surgeries for 20 patients (age range 1–69 years) performed during the last 20 years at their institutions. The patients were classified into 2 groups. Group A included 10 patients who underwent repeat bypass surgery for anterior circulation due to insufficient revascularization on the ipsilateral side. Group B included 10 patients who underwent repeat bypass surgery for posterior circulation due to the involvement of the posterior cerebral artery (PCA) after successful initial surgery for anterior circulation.

RESULTS

Preoperative symptoms included headache in 3 patients, transient ischemic attack in 10, cerebral infarction in 3, and intracranial hemorrhage in 4 patients. Intervals between the initial bypass surgery and repeat bypass surgery were 0.3–30 years (median 3 years). In group A, superficial temporal artery to middle cerebral artery (MCA) anastomosis and indirect bypass were performed on 7 hemispheres. Only indirect bypass was performed on 3 hemispheres because of the lack of suitable donor or recipient arteries. In group B, occipital artery (OA) to PCA anastomosis and indirect bypass were conducted on 4 hemispheres, and OA-MCA anastomosis and indirect bypass on 1 hemisphere. Only indirect bypass was conducted on 7 hemispheres because of the lack of suitable recipient arteries. All 22 repeat bypass surgeries were successfully conducted. During follow-up periods (median 4 years), none of the patients suffered repeat stroke except 1 patient who died of recurrent intracerebral hemorrhage 3 years after repeat bypass surgery for anterior circulation.

CONCLUSIONS

Repeat bypass surgery was feasible and effective to reduce further incidence of headache attack, transient ischemic attack, and ischemic/hemorrhagic stroke in moyamoya disease patients. Through precise radiological analysis, surgical procedures should be planned to yield maximal therapeutic effects.

ABBREVIATIONS CBF = cerebral blood flow; EDAS = encephalo-duro-arterio-synangiosis; EDMAPS = encephalo-duro-myo-arterio-pericranio-synangiosis; EDPS = encephalo-duro-pericranio-synangiosis; EMAS = encephalo-myo-arterio-synangiosis; EMS = encephalo-myo-synangiosis; ICH = intracranial hemorrhage; MCA = middle cerebral artery; MMD = moyamoya disease; OA = occipital artery; PCA = posterior cerebral artery; STA = superficial temporal artery; TIA = transient ischemic attack.

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Contributor Notes

Correspondence Haruto Uchino: Graduate School of Medicine and Pharmaceutical Science, University of Toyama, Toyama, Japan. uchino-hok@umin.ac.jp.

INCLUDE WHEN CITING Published online May 31, 2019; DOI: 10.3171/2019.3.JNS181979.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

  • 1

    Arias EJ, Dunn GP, Washington CW, Derdeyn CP, Chicoine MR, Grubb RL Jr, : Surgical revascularization in North American adults with moyamoya phenomenon: long-term angiographic follow-up. J Stroke Cerebrovasc Dis 24:15971608, 2015

    • Search Google Scholar
    • Export Citation
  • 2

    Arikan F, Vilalta J, Torne R, Noguer M, Lorenzo-Bosquet C, Sahuquillo J: Rapid resolution of brain ischemic hypoxia after cerebral revascularization in moyamoya disease. Neurosurgery 76:302312, 2015

    • Search Google Scholar
    • Export Citation
  • 3

    Czabanka M, Vajkoczy P, Schmiedek P, Horn P: Age-dependent revascularization patterns in the treatment of moyamoya disease in a European patient population. Neurosurg Focus 26(4):E9, 2009

    • Search Google Scholar
    • Export Citation
  • 4

    Funaki T, Takahashi JC, Takagi Y, Yoshida K, Araki Y, Kikuchi T, : Impact of posterior cerebral artery involvement on long-term clinical and social outcome of pediatric moyamoya disease. J Neurosurg Pediatr 12:626632, 2013

    • Search Google Scholar
    • Export Citation
  • 5

    Fung LW, Thompson D, Ganesan V: Revascularisation surgery for paediatric moyamoya: a review of the literature. Childs Nerv Syst 21:358364, 2005

    • Search Google Scholar
    • Export Citation
  • 6

    Guzman R, Lee M, Achrol A, Bell-Stephens T, Kelly M, Do HM, : Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article. J Neurosurg 111:927935, 2009

    • Search Google Scholar
    • Export Citation
  • 7

    Hayashi T, Shirane R, Tominaga T: Additional surgery for postoperative ischemic symptoms in patients with moyamoya disease: the effectiveness of occipital artery-posterior cerebral artery bypass with an indirect procedure: technical case report. Neurosurgery 64:E195E196, 2009

    • Search Google Scholar
    • Export Citation
  • 8

    Hishikawa T, Tokunaga K, Sugiu K, Date I: Assessment of the difference in posterior circulation involvement between pediatric and adult patients with moyamoya disease. J Neurosurg 119:961965, 2013

    • Search Google Scholar
    • Export Citation
  • 9

    Hori S, Acker G, Vajkoczy P: Radial artery grafts as rescue strategy for patients with moyamoya disease for whom conventional revascularization failed. World Neurosurg 85:7784, 2016

    • Search Google Scholar
    • Export Citation
  • 10

    Houkin K, Kuroda S, Nakayama N: Cerebral revascularization for moyamoya disease in children. Neurosurg Clin N Am 12:575584, ix, 2001

  • 11

    Huang AP, Tu YK: Progressive PCA steno-occlusive changes after revascularization for moyamoya disease: a neglected phenomenon. Neurosurgery 67:E1865E1866, 2010

    • Search Google Scholar
    • Export Citation
  • 12

    Karasawa J, Kikuchi H, Furuse S, Sakaki T, Yoshida Y: A surgical treatment of “moyamoya” disease “encephalo-myo synangiosis”. Neurol Med Chir (Tokyo) 17:2937, 1977

    • Search Google Scholar
    • Export Citation
  • 13

    Kawaguchi T, Fujita S, Hosoda K, Shose Y, Hamano S, Iwakura M, : Multiple burr-hole operation for adult moyamoya disease. J Neurosurg 84:468476, 1996

    • Search Google Scholar
    • Export Citation
  • 14

    Kazumata K, Ito M, Tokairin K, Ito Y, Houkin K, Nakayama N, : The frequency of postoperative stroke in moyamoya disease following combined revascularization: a single-university series and systematic review. J Neurosurg 121:432440, 2014

    • Search Google Scholar
    • Export Citation
  • 15

    Kazumata K, Kamiyama H, Saito H, Maruichi K, Ito M, Uchino H, : Direct anastomosis using occipital artery for additional revascularization in moyamoya disease after combined superficial temporal artery-middle cerebral artery and indirect bypass. Oper Neurosurg (Hagerstown) 13:213223, 2017

    • Search Google Scholar
    • Export Citation
  • 16

    Kim SK, Seol HJ, Cho BK, Hwang YS, Lee DS, Wang KC: Moyamoya disease among young patients: its aggressive clinical course and the role of active surgical treatment. Neurosurgery 54:840846, 2004

    • Search Google Scholar
    • Export Citation
  • 17

    Kuroda S, Houkin K, Ishikawa T, Nakayama N, Ikeda J, Ishii N, : Determinants of intellectual outcome after surgical revascularization in pediatric moyamoya disease: a multivariate analysis. Childs Nerv Syst 20:302308, 2004

    • Search Google Scholar
    • Export Citation
  • 18

    Kuroda S, Houkin K, Ishikawa T, Nakayama N, Iwasaki Y: Novel bypass surgery for moyamoya disease using pericranial flap: its impacts on cerebral hemodynamics and long-term outcome. Neurosurgery 66:10931101, 2010

    • Search Google Scholar
    • Export Citation
  • 19

    Kuroda S, Houkin K, Kamiyama H, Abe H, Mitsumori K: Regional cerebral hemodynamics in childhood moyamoya disease. Childs Nerv Syst 11:584590, 1995

    • Search Google Scholar
    • Export Citation
  • 20

    Lee JY, Choi YH, Cheon JE, Paeng JC, Ryu HW, Kim KJ, : Delayed posterior circulation insufficiency in pediatric moyamoya disease. J Neurol 261:23052313, 2014

    • Search Google Scholar
    • Export Citation
  • 21

    Matsushima T, Fujiwara S, Nagata S, Fujii K, Fukui M, Hasuo K: Reoperation for moyamoya disease refractory to encephalo-duro-arterio-synangiosis. Acta Neurochir (Wien) 107:129132, 1990

    • Search Google Scholar
    • Export Citation
  • 22

    Matsushima Y: Failure of encephalo-duro-arterio-synangiosis procedure in moyamoya disease. Pediatr Neurosci 12:326327, 1985–1986

  • 23

    Matsushima Y, Fukai N, Tanaka K, Tsuruoka S, Inaba Y, Aoyagi M, : A new surgical treatment of moyamoya disease in children: a preliminary report. Surg Neurol 15:313320, 1981

    • Search Google Scholar
    • Export Citation
  • 24

    Miyamoto S, Kikuchi H, Karasawa J, Nagata I, Yamazoe N, Akiyama Y: Pitfalls in the surgical treatment of moyamoya disease. Operative techniques for refractory cases. J Neurosurg 68:537543, 1988

    • Search Google Scholar
    • Export Citation
  • 25

    Miyamoto S, Yoshimoto T, Hashimoto N, Okada Y, Tsuji I, Tominaga T, : Effects of extracranial-intracranial bypass for patients with hemorrhagic moyamoya disease: results of the Japan Adult Moyamoya Trial. Stroke 45:14151421, 2014

    • Search Google Scholar
    • Export Citation
  • 26

    Mizoi K, Kayama T, Yoshimoto T, Nagamine Y: Indirect revascularization for moyamoya disease: is there a beneficial effect for adult patients? Surg Neurol 45:541549, 1996

    • Search Google Scholar
    • Export Citation
  • 27

    Morimoto M, Iwama T, Hashimoto N, Kojima A, Hayashida K: Efficacy of direct revascularization in adult moyamoya disease: haemodynamic evaluation by positron emission tomography. Acta Neurochir (Wien) 141:377384, 1999

    • Search Google Scholar
    • Export Citation
  • 28

    Mugikura S, Higano S, Shirane R, Fujimura M, Shimanuki Y, Takahashi S: Posterior circulation and high prevalence of ischemic stroke among young pediatric patients with moyamoya disease: evidence of angiography-based differences by age at diagnosis. AJNR Am J Neuroradiol 32:192198, 2011

    • Search Google Scholar
    • Export Citation
  • 29

    Pandey P, Steinberg GK: Outcome of repeat revascularization surgery for moyamoya disease after an unsuccessful indirect revascularization. Clinical article. J Neurosurg 115:328336, 2011

    • Search Google Scholar
    • Export Citation
  • 30

    Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis, Health Labour Sciences Research Grant for Research on Measures for Infractable Diseases: Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52:245266, 2012

    • Search Google Scholar
    • Export Citation
  • 31

    Suzuki J, Takaku A: Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288299, 1969

    • Search Google Scholar
    • Export Citation
  • 32

    Takahashi A, Kamiyama H, Houkin K, Abe H: Surgical treatment of childhood moyamoya disease—comparison of reconstructive surgery centered on the frontal region and the parietal region. Neurol Med Chir (Tokyo) 35:231237, 1995

    • Search Google Scholar
    • Export Citation
  • 33

    Takahashi T, Shirane R, Sato S, Yoshimoto T: Developmental changes of cerebral blood flow and oxygen metabolism in children. AJNR Am J Neuroradiol 20:917922, 1999

    • Search Google Scholar
    • Export Citation
  • 34

    Takeuchi K: Hypoplasia of the bilateral internal carotid arteries. Brain Nerve 9:3743, 1957

  • 35

    Teo M, Johnson J, Steinberg GK: Strategies for and outcome of repeat revascularization surgery for moyamoya disease: an American institutional series. Neurosurgery 81:852859, 2017

    • Search Google Scholar
    • Export Citation
  • 36

    Touho H, Karasawa J, Ohnishi H, Yamada K, Shibamoto K: Surgical reconstruction of failed indirect anastomosis in childhood moyamoya disease. Neurosurgery 32:935940, 1993

    • Search Google Scholar
    • Export Citation
  • 37

    Uchino H, Kim JH, Fujima N, Kazumata K, Ito M, Nakayama N, : Synergistic interactions between direct and indirect bypasses in combined procedures: the significance of indirect bypasses in moyamoya disease. Neurosurgery 80:201209, 2017

    • Search Google Scholar
    • Export Citation
  • 38

    Uchino H, Kuroda S, Hirata K, Shiga T, Houkin K, Tamaki N: Predictors and clinical features of postoperative hyperperfusion after surgical revascularization for moyamoya disease: a serial single photon emission CT/positron emission tomography study. Stroke 43:26102616, 2012

    • Search Google Scholar
    • Export Citation
  • 39

    Vuignier S, Ito M, Kurisu K, Kazumata K, Nakayama N, Shichinohe H, : Ivy sign, misery perfusion, and asymptomatic moyamoya disease: FLAIR imaging and 15O-gas positron emission tomography. Acta Neurochir (Wien) 155:20972104, 2013

    • Search Google Scholar
    • Export Citation

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