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Early and noninvasive evaluation using superficial temporal artery duplex ultrasonography after indirect bypass for adult ischemic moyamoya disease

  • Original Article - Vascular
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Abstract

Background

The validity of indirect bypass for adult patients with moyamoya disease is still debatable. Some patients are poor responders to indirect bypass, and additive intervention is occasionally required in these cases. Therefore, it is necessary to evaluate the development of collateral circulation as early as possible postoperatively.

Methods

Fifteen adult patients (>17 years old) with moyamoya disease (22 affected sides) who underwent encephalo-duro-arterio-synangiosis (EDAS) at Fukuoka University Hospital from April 2008 to August 2014 were included. All patients had ischemic symptoms of at least one hemisphere. Superficial temporal artery duplex ultrasonography (STDU) was performed before and 3, 6, and 12 months postoperatively. Digital subtraction angiography was performed 1 year after the operation to evaluate the development of collateral circulation. Hemispheres exhibiting collateral formation of more than one-third of the MCA distribution were defined as good responders, and those with less than one-third were defined as poor responders.

Results

EDAS induced the formation of well-developed collaterals in 17 of 22 affected sides (77.3%) of adult patients with ischemic moyamoya disease. Regardless of the degree of collateral formation, the ischemic event subsided eventually with time in all patients. In good responders, the pulsatility index obtained by STDU showed a drastic decrease 3 months after the operation, while it did not change significantly in poor responders. Absence of this decrease in the pulsatility index along with no change in the flow velocity reliably indicated poor responders.

Conclusions

Neovascularization after EDAS can be evaluated noninvasively in early phase using STDU.

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References

  1. Abla AA, Gandhoke G, Clark JC, Oppenlander ME, Velat GJ, Zabramski JM, Albuquerque FC, Nakaji P, Spetzler RF, Wanebo JE (2013) Surgical outcomes for moyamoya angiopathy at barrow neurological institute with comparison of adult indirect encephaloduroarteriosynangiosis bypass, adult direct superficial temporal artery-to-middle cerebral artery bypass, and pediatric bypass: 154 revascularization surgeries in 140 affected hemispheres. Neurosurgery 73:430–439

    Article  PubMed  Google Scholar 

  2. Agarwalla PK, Stapleton CJ, Phillips MT, Walcott BP, Venteicher AS, Ogilvy CS (2014) Surgical outcomes following encephaloduroarteriosynangiosis in North American adults with moyamoya. J Neurosurg 121:1394–1400

    Article  PubMed  Google Scholar 

  3. Arikan F, Vilalta J, Torne R, Noguer M, Lorenzo-Bosquet C, Sahuquillo J (2015) Rapid resolution of brain ischemic hypoxia after cerebral revascularization in moyamoya disease. Neurosurgery 76:302–312, discussion 312

    Article  PubMed  Google Scholar 

  4. Bang JS, Kwon OK, Kim JE, Kang HS, Park H, Cho SY, Oh CW (2012) Quantitative angiographic comparison with the OSIRIS program between the direct and indirect revascularization modalities in adult moyamoya disease. Neurosurgery 70:625–632, discussion 632-623

    Article  PubMed  Google Scholar 

  5. Choi IJ, Cho SJ, Chang JC, Park SQ, Park HK (2012) Angiographic results of indirect and combined bypass surgery for adult moyamoya disease. J Cerebrovasc Endovasc Neurosurg 14:216–222

    Article  PubMed  PubMed Central  Google Scholar 

  6. Dusick JR, Gonzalez NR, Martin NA (2011) Clinical and angiographic outcomes from indirect revascularization surgery for moyamoya disease in adults and children: a review of 63 procedures. Neurosurgery 68:34–43, discussion 43

    Article  PubMed  Google Scholar 

  7. Fujimoto S, Toyoda K, Inoue T, Jinnouchi J, Kitazono T, Okada Y (2013) Changes in superficial temporal artery blood flow and cerebral hemodynamics after extracranial-intracranial bypass surgery in moyamoya disease and atherothrombotic carotid occlusion. J Neurol Sci 325:10–14

    Article  PubMed  Google Scholar 

  8. Fujimura M, Kaneta T, Mugikura S, Shimizu H, Tominaga T (2007) Temporary neurologic deterioration due to cerebral hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in patients with adult-onset moyamoya disease. Surg Neurol 67:273–282

    Article  PubMed  Google Scholar 

  9. Fujimura M, Shimizu H, Inoue T, Mugikura S, Saito A, Tominaga T (2011) 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 68:957–964, discussion 964-955

    Article  PubMed  Google Scholar 

  10. Gonzalez NR, Dusick JR, Connolly M, Bounni F, Martin NA, Van de Wiele B, Liebeskind DS, Saver JL (2015) Encephaloduroarteriosynangiosis for adult intracranial arterial steno-occlusive disease: long-term single-center experience with 107 operations. J Neurosurg 123:654–661

    Article  PubMed  Google Scholar 

  11. Imai H, Miyawaki S, Ono H, Nakatomi H, Yoshimoto Y, Saito N (2015) The importance of encephalo-myo-synangiosis in surgical revascularization strategies for moyamoya disease in children and adults. World Neurosurg 83:691–699

    Article  PubMed  Google Scholar 

  12. Kim DS, Huh PW, Kim HS, Kim IS, Choi S, Mok JH, Huh CW (2012) Surgical treatment of moyamoya disease in adults: combined direct and indirect vs. indirect bypass surgery. Neurol Med Chir (Tokyo) 52:333–338

    Article  Google Scholar 

  13. 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 114:930–934

    Article  CAS  PubMed  Google Scholar 

  14. Lin N, Aronson JP, Manjila S, Smith ER, Scott RM (2014) Treatment of moyamoya disease in the adult population with pial synangiosis. J Neurosurg 120:612–617

    Article  PubMed  Google Scholar 

  15. Matsushima T, Inoue T, Suzuki SO, Fujii K, Fukui M, Hasuo K (1992) Surgical treatment of moyamoya disease in pediatric patients—comparison between the results of indirect and direct revascularization procedures. Neurosurgery 31:401–405

    Article  CAS  PubMed  Google Scholar 

  16. Pandey P, Steinberg GK (2011) Outcome of repeat revascularization surgery for moyamoya disease after an unsuccessful indirect revascularization. clinical article. J Neurosurg 115:328–336

    Article  PubMed  Google Scholar 

  17. Perren F, Horn P, Vajkoczy P, Schmiedek P, Meairs S (2005) Power Doppler imaging in detection of surgically induced indirect neoangiogenesis in adult moyamoya disease. J Neurosurg 103:869–872

    Article  PubMed  Google Scholar 

  18. Sahoo SS, Suri A, Bansal S, Devarajan SL, Sharma BS (2015) Outcome of revascularization in moyamoya disease: evaluation of a new angiographic scoring system. Asian J Neurosurg 10:252–259

    Article  PubMed  PubMed Central  Google Scholar 

  19. Starke RM, Komotar RJ, Connolly ES (2009) Optimal surgical treatment for moyamoya disease in adults: direct versus indirect bypass. Neurosurg Focus 26:E8

    Article  PubMed  Google Scholar 

  20. Uchino H, Kuroda S, Hirata K, Shiga T, Houkin K, Tamaki N (2012) Predictors and clinical features of postoperative hyperperfusion after surgical revascularization for moyamoya disease: a serial single photon emission CT/positron emission tomography study. Stroke 43:2610–2616

    Article  PubMed  Google Scholar 

  21. Wang Y, Chen L, Wang Y, Pan H, Wang Y, Xu B, Liao Y (2014) Hemodynamic study with duplex ultrasonography on combined (direct/indirect) revascularization in adult moyamoya disease. J Stroke Cerebrovasc Dis 23:2573–2579

    Article  PubMed  Google Scholar 

  22. Wu M, Huang Z, Zhang D, Wang L, Sun J, Wang S, Zhao Y, Zhao J (2011) Color doppler hemodynamic study of the superficial temporal arteries in superficial temporal artery-middle cerebral artery (STA-MCA) bypass surgery for moyamoya disease. World Neurosurg 75:258–263

    Article  PubMed  Google Scholar 

  23. Yoo M, Jin SC, Jin SJ, Choi BS (2015) Salvage STA-MCA bypass surgery in an adult moyamoya patient after failed indirect revascularization surgery. Br J Neurosurg 29:868–870

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank Mr. Hirofumi Shimada for his great help with the ultrasound examination.

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Authors and Affiliations

  1. Department of Neurosurgery, Faculty of Medicine, Fukuoka University, Fukuoka, Japan

    Sayaka Ogawa, Hiroshi Abe, Toshiro Katsuta, Kenji Fukuda, Koichi Miki & Tooru Inoue

  2. Department of Neurology, Faculty of Medicine, Fukuoka University, Fukuoka, Japan

    Toshiyasu Ogata

Authors
  1. Sayaka Ogawa
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  2. Hiroshi Abe
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  3. Toshiro Katsuta
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  4. Kenji Fukuda
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  5. Toshiyasu Ogata
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  6. Koichi Miki
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  7. Tooru Inoue
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Corresponding author

Correspondence to Hiroshi Abe.

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No funding was received for this research.

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All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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Ogawa, S., Abe, H., Katsuta, T. et al. Early and noninvasive evaluation using superficial temporal artery duplex ultrasonography after indirect bypass for adult ischemic moyamoya disease. Acta Neurochir 159, 577–582 (2017). https://doi.org/10.1007/s00701-016-3073-0

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  • DOI: https://doi.org/10.1007/s00701-016-3073-0

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