Transient neurological events in childhood moyamoya disease

Kentaro ChibaDepartment of Neurosurgery, Tokyo Women’s Medical University, Tokyo;

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Yasuo AiharaDepartment of Neurosurgery, Tokyo Women’s Medical University, Tokyo;

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Atsushi FukuiDepartment of Neurosurgery, Tokyo Women’s Medical University, Tokyo;

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Koji YamaguchiDepartment of Neurosurgery, Tokyo Women’s Medical University, Tokyo;

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Akitsugu KawashimaDepartment of Neurosurgery, Tokyo Women’s Medical University, Yachiyo Medical Center, Chiba; and

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Yoshikazu OkadaDepartment of Neurosurgery, St. Luke’s International Hospital, Tokyo, Japan

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Takakazu KawamataDepartment of Neurosurgery, Tokyo Women’s Medical University, Tokyo;

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OBJECTIVE

Patients sometimes experience transient neurological events (TNEs) during the early postoperative period after revascularization surgery for childhood moyamoya disease. The clinical background and pathophysiology of TNEs remain unclear. This study aimed to evaluate the incidence rate of TNEs and discuss the factors associated with pediatric moyamoya disease.

METHODS

The authors retrospectively reviewed 110 cerebral hemispheres of 61 pediatric patients younger than 15 years who were treated from 2011 to 2020. All children underwent either simple double-direct or combined revascularization surgery. Of these 61 patients, 52 underwent bilateral surgery and 9 underwent unilateral surgery. The authors calculated the incidence of TNEs in accordance with a previously reported TNE definition. Cerebral blood flow (CBF) was evaluated in all eligible cases with xenon CT immediately after revascularization surgery.

RESULTS

The incidence rate of TNEs in patients with childhood moyamoya disease was 26.4%. TNEs occurred after an average (range) of 6.26 (2–12) days postoperatively without triggers, and all identified TNEs spontaneously resolved within 2 weeks. The most common symptoms were dysarthria, facial palsy, and numbness around the mouth, followed by sensory disturbance of the upper extremities. The presence of focal hyperperfusion on xenon CT performed immediately after revascularization surgery was strongly correlated with the incidence of TNEs (p = 0.0001). Focal hyperperfusion was observed in 43 of 110 operative sides (39.1%). Notably, only 25.6% of patients with focal hyperperfusion showed numerical global hyperperfusion. In addition, a decrease in CBF compared with the thalamic region in the contralateral side was observed in TNE-affected cases (p = 0.0443).

CONCLUSIONS

TNEs occurred more frequently in childhood moyamoya disease patients than expected. The clinical background, including symptoms, timing, and duration, was almost identical to TNEs in adults. Focal hyperperfusion, rather than numerical global hyperperfusion, was strongly correlated with the incidence of TNEs. Furthermore, the authors advocate the notion that a clinical course where symptoms occur without triggers may be a unique characteristic of TNEs, especially in childhood moyamoya disease.

ABBREVIATIONS

AVM = arteriovenous malformation; CBF = cerebral blood flow; CHB = cortical hyperintensity belt; ICA = internal carotid artery; MCA = middle cerebral artery; STA = superficial temporal artery; TIA = transient ischemic attack; TNE = transient neurological event.
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Figure from Candela-Cantó et al. (pp 61–70).

  • 1

    Fujimura M, Shimizu H, Inoue T, Mugikura S, Saito A, Tominaga T. Significance of focal cerebral hyperperfusion as a cause of transient neurologic deterioration after extracranial-intracranial bypass for moyamoya disease: comparative study with non-moyamoya patients using N-isopropyl-p-[(123)I]iodoamphetamine single-photon emission computed tomography. Neurosurgery. 2011;68(4):957965.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Hamano E, Kataoka H, Morita N, et al. Clinical implications of the cortical hyperintensity belt sign in fluid-attenuated inversion recovery images after bypass surgery for moyamoya disease. J Neurosurg. 2017;126(1):17.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Lu J, Zhao Y, Ma L, et al. Predictors and clinical features of transient neurological events after combined bypass revascularization for moyamoya disease. Clin Neurol Neurosurg. 2019;186:105505.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    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. 2012;43(10):26102616.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Egashira Y, Yamauchi K, Enomoto Y, Nakayama N, Yoshimura S, Iwama T. Disruption of cortical arterial network is associated with the severity of transient neurologic events after direct bypass surgery in adult moyamoya disease. World Neurosurg. 2017;100:311315.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Fujimura M, Kaneta T, Mugikura S, Shimizu H, Tominaga T. Temporary neurologic deterioration due to cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with adult-onset moyamoya disease. Surg Neurol. 2007;67(3):273282.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Hayashi K, Horie N, Suyama K, Nagata I. Incidence and clinical features of symptomatic cerebral hyperperfusion syndrome after vascular reconstruction. World Neurosurg. 2012;78(5):447454.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Shiba M, Toma N, Tanioka S, Yasuda R, Sakaida H, Suzuki H. Significance of novel subcortical low intensity score on transient neurological events after revascularization surgery for moyamoya disease. Clin Neurol Neurosurg. 2018;167:7075.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Hayashi T, Shirane R, Fujimura M, Tominaga T. Postoperative neurological deterioration in pediatric moyamoya disease: watershed shift and hyperperfusion. J Neurosurg Pediatr. 2010;6(1):7381.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Sasamori T, Kuroda S, Nakayama N, Iwasaki Y. Incidence and pathogenesis of transient cheiro-oral syndrome after surgical revascularization for moyamoya disease. Neurosurgery. 2010;67(4):10541060.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Kuroda S, Houkin K. Bypass surgery for moyamoya disease: concept and essence of surgical techniques. Neurol Med Chir (Tokyo). 2012;52(5):287294.

  • 12

    Kurihara H, Yamaguchi K, Ishikawa T, et al. Direct double bypass using the posterior auricular artery as initial surgery for moyamoya disease: technical note. J Neurosurg. 2020;133(4):11681171.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Takahashi S, Tanizaki Y, Kimura H, et al. Hemodynamic stress distribution reflects ischemic clinical symptoms of patients with moyamoya disease. Clin Neurol Neurosurg. 2015;138:104110.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Yonas H, Darby JM, Marks EC, Durham SR, Maxwell C. CBF measured by Xe-CT: approach to analysis and normal values. J Cereb Blood Flow Metab. 1991;11(5):716725.

  • 15

    Carlson AP, Brown AM, Zager E, et al. Xenon-enhanced cerebral blood flow at 28% xenon provides uniquely safe access to quantitative, clinically useful cerebral blood flow information: a multicenter study. AJNR Am J Neuroradiol. 2011;32(7):13151320.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Haku T, Hosoya T, Komatani A, Watanabe N, Yamaguchi K. Correlation of regional cerebral blood flow between Xe-CT and 133Xe-SPECT: validity of Xe-CT in evaluating rCBF. Article in Japanese. Nihon Igaku Hoshasen Gakkai Zasshi. 1996;56(12):828833.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Gur D, Wolfson SK Jr, Yonas H, et al. Progress in cerebrovascular disease: local cerebral blood flow by xenon enhanced CT. Stroke. 1982;13(6):750758.

  • 18

    Nambu K, Suzuki R, Hirakawa K. Cerebral blood flow: measurement with xenon-enhanced dynamic helical CT. Radiology. 1995;195(1):5357.

  • 19

    Touho H, Ogawa D, Ueki H, Isotani N. Lessening of effective dose in stable xenon-enhanced CT, especially in childhood moyamoya disease: about serial scan times. Surg Cereb Stroke. 2012;40(5):322327.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20

    Uchino H, Nakayama N, Kazumata K, Kuroda S, Houkin K. Edaravone reduces hyperperfusion-related neurological deficits in adult moyamoya disease: historical control study. Stroke. 2016;47(7):19301932.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Nakamoto H, Aihara Y, Yamaguchi K, Kawamata T, Okada Y. Efficacy, safety, and outcomes in 17 pediatric cases treated with the free radical scavenger edaravone. Childs Nerv Syst. 2015;31(9):15331540.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Aihara Y, Kashiwase S, Chiba K, et al. Aspirin use and platelet aggregation in ischemic onset-type pediatric moyamoya patients with intractable headaches (moya-ache). Childs Nerv Syst. 2021;37(5):16491657.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Okada Y, Kawamata T, Kawashima A, Yamaguchi K, Ono Y, Hori T. The efficacy of superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease complaining of severe headache. J Neurosurg. 2012;116(3):672679.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Matsuoka G, Aihara Y, Yamaguchi K, et al. Early surgical treatment benefits early staged pediatric moyamoya disease—single case report. Childs Nerv Syst. 2015;31(7):11951199.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Mendez NV, Chen C, Richardson AM, Morcos JJ, Deepika K. Hemoglobin concentration may influence the incidence of postoperative transient neurological events in patients with moyamoya after extracranial-intracranial arterial bypass: a retrospective single center experience. J Neurosurg Anesthesiol. 2022;34(2):238242.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Nomura S, Yamaguchi K, Ishikawa T, Kawashima A, Okada Y, Kawamata T. Factors of delayed hyperperfusion and the importance of repeated cerebral blood flow evaluation for hyperperfusion after direct bypass for moyamoya disease. World Neurosurg. 2018;118:e468e472.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Kuroda S, Kamiyama H, Abe H, Asaoka K, Mitsumori K. Temporary neurological deterioration caused by hyperperfusion after extracranial-intracranial bypass—case report and study of cerebral hemodynamics. Neurol Med Chir (Tokyo). 1994;34(1):1519.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Mukerji N, Cook DJ, Steinberg GK. Is local hypoperfusion the reason for transient neurological deficits after STA-MCA bypass for moyamoya disease? J Neurosurg. 2015;122(1):9094.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Fujimura M, Kaneta T, Shimizu H, Tominaga T. Symptomatic hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in a child with moyamoya disease. Childs Nerv Syst. 2007;23(10):11951198.

    • Crossref
    • Search Google Scholar
    • Export Citation

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