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Long-term follow-up of pediatric moyamoya disease treated by combined direct–indirect revascularization surgery: single institute experience with surgical and perioperative management

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Abstract

Moyamoya disease (MMD) is a rare occlusive cerebrovascular disease that mainly presents in children as cerebral ischemia. Prompt treatment with either a direct or indirect revascularization procedure is necessary for children with MMD in order to prevent repeated ischemic events. We herein present our experience with combined direct and indirect bypass surgery for the treatment of pediatric MMD as well as our uniquely designed perioperative protocol. Twenty-three patients with MMD, aged between 2 and 16 years old (mean 9.36), underwent 38 combined bypass procedures between 2008 and 2015. All patients underwent single superficial temporal artery-middle cerebral artery (STA-MCA) anastomosis combined with encephalo-duro-myo-synangiosis (EDMS). The perioperative management protocol was stratified into two unique eras: the first era with normotensive care and the second era with strict blood pressure control (systolic 100–130 mmHg) and routine aspirin administration. Patients were followed after surgery for a period ranging between 3 and 131 months (mean 77 months) in yearly clinical and radiological follow-ups. Three postoperative complications were observed: two cases of cerebral hyperperfusion (2/38, 5.3 %) and one case of perioperative minor stroke (1/38, 2.6 %), two of which were in the first era. No strokes, either ischemic or hemorrhagic, were observed in the follow-up period, and the activity of daily living as shown by the modified Rankin Scale improved in 20 patients, with no deterioration being observed in any of our patients. STA-MCA bypass with EDMS is safe and effective for the management of pediatric MMD and provides long-term favorable outcomes. Perioperative care with blood pressure control combined with the administration of aspirin may reduce the potential risk of surgical complications.

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Abbreviations

ECA:

External carotid artery

EDAS:

Encephalo-duro-arterio-synangiosis

EDMS:

Encephalo-duro-myo-synangiosis

ICA:

Internal carotid artery

MCA:

Middle cerebral artery

SPECT:

Single photon emission computed tomography

STA:

Superficial temporal artery

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Acknowledgment

This research is partially supported by a grant (J150001575) from the Japan Agency for Medical Research and Development (AMED).

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Authors and Affiliations

  1. Department of Neurosurgery, Tohoku University Graduate School of Medicine, 1-1 Seiryo-machi, Aoba-ku, Sendai, 980-8574, Japan

    Sherif Rashad, Miki Fujimura, Kuniyasu Niizuma, Hidenori Endo & Teiji Tominaga

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  1. Sherif Rashad
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  2. Miki Fujimura
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  3. Kuniyasu Niizuma
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  4. Hidenori Endo
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  5. Teiji Tominaga
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Corresponding author

Correspondence to Miki Fujimura.

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The authors declare that they have no conflict of interest regarding the present study.

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Comments

Motohiro Morioka, Fukuoka, Japan

Sherif Rashad et al. examined the long-term outcome of pediatric moyamoya disease (MMD) patients treated by combined direct–indirect revascularization surgery and obtained good surgical outcome. The authors emphasized the importance of combination surgical method of direct and indirect revascularization. As the authors described, the poor outcome of pediatric MMD patients is principally caused by cerebral infarction.

I agree with the authors’ representation that combination therapy of direct–indirect surgery is the best treatment for pediatric patients, as the cerebral blood flow would increase immediately after surgery, if direct bypass could be performed.

I consider there are some problems in the surgical strategy for pediatric (especially very young) patients with MMD: First, in some pediatric cases, direct bypass is difficult because of fragile and small vessels in very young children, as authors discussed. If the very young patient have only one branch of STA, the failure of direct bypass would result in loss of blood flow source (for example, source of EDAS).

Second, it is unclear how to manage the case with bilateral severe CBF decrease, or the case with bilateral rapid progression of arterial stenosis. The authors did not perform bilateral revascularization surgery simultaneously (within the same day). Although it is rare, there might be the possibility that the contralateral hemisphere might suffer stroke in the time waiting for second surgery. No ischemic complications were observed during the latency period between the first and second surgeries in this study, and the authors emphasized blood pressure control and oral aspirin. However, I experienced one severe case suffered complete stroke of contralateral hemisphere 1 month after the first surgery, while she took low-dose aspirin. I considered the simultaneous bilateral revascularization surgery could prevent the contralateral stroke for this case, although blood transfusion might be necessary.

It is necessary in future to establish more certain and safe bypass procedure for small arteries and to establish the method to detect severe and rapid progressive cases

Jeong Eun Kim, Seoul, South Korea

The article describes a series of cases of pediatric moyamoya disease (MMD) operated on at a single center using combined revascularization procedures. Because of technical easiness and good revascularization outcome, simple indirect revascularization surgery is usually done for the pediatric MMD. I agree with the authors’ emphasis on combined procedures for the pediatric MMD in three regards. First, some groups, especially younger ones among the pediatric MMD patients, are well known to have more aggressive progression. In those patients, hemodynamic compensation should be too urgent for the indirect revascularization to meet the need. Second, the direct procedures, including superficial temporal artery-to-middle cerebral artery bypass, are very challenging for the vessels with smaller caliber in the pediatric patients. However, the neurovascular surgeons who are skilled at the STA-MCA bypass for the adult MMD patients can sufficiently cope with that kind of technical challenge after experiencing the learning curve for the procedures. Moreover, indirect procedure can act as insurance in the case of failure of direct procedures. Third, the main critique for the direct procedures in the MMD patients is that the direct one shows more complication, such as hyperperfusion syndrome, than the indirect one. The authors well describe how to deal with and reduce the potential risk of surgical complications after combined revascularization.

The weaknesses are the small number of the enrolled patients with wide range of age (2 to 16 years), which confounds the effects of combined procedures. In spite of such flaws, this work is very thoughtful and presents a good option for the pediatric MMD patients along with traditional techniques.

Akitsugu Kawashima, Chiba, Japan

The authors demonstrate experience with combined direct and indirect bypass surgery for pediatric cases of moyamoya disease with their perioperative management. This manuscript demonstrates low surgical complication rate and long-term excellent outcome. I agree with authors’ argument that there are difference features of moyamoya disease between in childhood (before the age of 12) and in adolescent (between the ages of 12 and 16). Cases of moyamoya disease in childhood were more complicated than were the cases in adolescent in the points of present symptoms and postoperative complications. They also described that adolescent cases of moyamoya disease are similar to adults in terms of their pathophysiology. The authors’ view is almost the same as our 60 cases of pediatric cases of moyamoya disease. A further study of features of pediatric moyamoya disease in the point of view of ages should be conducted. I believe the manuscript is interesting and useful contribution for neurosurgeon engaged in treatment of moyamoya disease as detail of surgical and perioperative management.

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Rashad, S., Fujimura, M., Niizuma, K. et al. Long-term follow-up of pediatric moyamoya disease treated by combined direct–indirect revascularization surgery: single institute experience with surgical and perioperative management. Neurosurg Rev 39, 615–623 (2016). https://doi.org/10.1007/s10143-016-0734-7

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  • DOI: https://doi.org/10.1007/s10143-016-0734-7

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