Acta Neurochirurgica

, Volume 159, Issue 3, pp 567–575 | Cite as

Indocyanine green visualization of middle meningeal artery before craniotomy during surgical revascularization for moyamoya disease

  • Nozomu Tanabe
  • Shusuke Yamamoto
  • Daina Kashiwazaki
  • Naoki Akioka
  • Naoya Kuwayama
  • Kyo Noguchi
  • Satoshi Kuroda
Original Article - Vascular



The middle meningeal artery (MMA) is well known to function as an important collateral channel to the territory of the anterior cerebral artery in moyamoya disease. This study was aimed to evaluate whether indocyanine green (ICG) videoangiography could visualize the anterior branch of the MMA before craniotomy during surgical revascularization for moyamoya disease.


This study included 19 patients who developed TIA, ischemic stroke or hemorrhagic stroke due to moyamoya disease. Plain CT scan and three-dimensional time-of-flight MR angiography were performed in all patients before surgery. All of them underwent superficial temporal artery to middle temporal artery anastomosis and indirect bypass on 27 sides in total.


ICG videoangiography could clearly visualize the anterior branch of the MMA in 10 (37%) of 27 sides. The patients with a “visible” MMA are significantly younger than those without. Radiological analysis revealed that ICG videoangiography could visualize it through the cranium when the diameter of the MMA is >1.3 mm and the sphenoid bone thickness over the MMA is <3.0 mm. The MMA could be preserved during craniotomy in all “visible” MMAs, but not in 4 (23.5%) of 17 “invisible” MMAs. The results strongly suggest that ICG videoangiography can visualize the anterior branch of the MMA before craniotomy in about one-third of patients with a large-diameter MMA (>1.3 mm) and thin sphenoid bone (<3.0 mm).


ICG videoangiography is a safe and valuable technique to preserve the anterior branch of the MMA during craniotomy for moyamoya disease.


Moyamoya disease Bypass surgery Middle meningeal artery Indocyanine green Collateral circulation 


  1. 1.
    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 43CrossRefPubMedGoogle Scholar
  2. 2.
    Hori S, Kashiwazaki D, Akioka N, Hayashi T, Hori E, Umemura K, Horie Y, Kuroda S (2015) Surgical anatomy and preservation of the middle meningeal artery during bypass surgery for moyamoya disease. Acta Neurochir (Wien) 157:29–36CrossRefGoogle Scholar
  3. 3.
    Karasawa J, Touho H, Ohnishi H, Miyamoto S, Kikuchi H (1992) Long-term follow-up study after extracranial-intracranial bypass surgery for anterior circulation ischemia in childhood moyamoya disease. J Neurosurg 77:84–89CrossRefPubMedGoogle Scholar
  4. 4.
    Kuroda S, Houkin K (2008) Moyamoya disease: current concepts and future perspectives. Lancet Neurol 7:1056–1066CrossRefPubMedGoogle Scholar
  5. 5.
    Kuroda S, Houkin K (2012) Bypass surgery for moyamoya disease—concept and essence of surgical technique-Neurol. Med Chir (Tokyo) 52:287–294CrossRefGoogle Scholar
  6. 6.
    Kuroda S, Houkin K, Abe H, Hoshi Y, Tamura M (1996) Near-infrared monitoring of cerebral oxygenation state during carotid endarterectomy. Surg Neurol 45:450–458CrossRefPubMedGoogle Scholar
  7. 7.
    Kuroda S, Houkin K, Hoshi Y, Tamura M, Kazumata K, Abe H (1996) Cerebral hypoxia after hyperventilation causes “re-build-up” phenomenon and TIA in childhood moyamoya disease. A near-infrared spectroscopy study. Childs Nerv Syst 12:448–452, discussion 453CrossRefPubMedGoogle Scholar
  8. 8.
    Kuroda S, Houkin K, Ishikawa T, Nakayama N, Iwasaki Y (2010) Novel bypass surgery for moyamoya disease using pericranial flap: its impacts on cerebral hemodynamics and long-term outcome. Neurosurgery 66:1093–1101, discussion 1101CrossRefPubMedGoogle Scholar
  9. 9.
    Ma S, Baillie LJ, Stringer MD (2012) Reappraising the surface anatomy of the pterion and its relationship to the middle meningeal artery. Clin Anat 25:330–339CrossRefPubMedGoogle Scholar
  10. 10.
    Matsushima T, Inoue K, Kawashima M, Inoue T (2012) History of the development of surgical treatments for moyamoya disease. Neurol Med Chir (Tokyo) 52:278–286CrossRefGoogle Scholar
  11. 11.
    McCormick PW, Stewart M, Lewis G, Dujovny M, Ausman JI (1992) Intracerebral penetration of infrared light. Technical note. J Neurosurg 76:315–318CrossRefPubMedGoogle Scholar
  12. 12.
    Miwa M (2010) The principle of ICG fluorescence method. Open Surg Oncol J 2:26–28CrossRefGoogle Scholar
  13. 13.
    Miyamoto S, Akiyama Y, Nagata I, Karasawa J, Nozaki K, Hashimoto N, Kikuchi H (1998) Long-term outcome after STA-MCA anastomosis for moyamoya disease. Neurosurg Focus 5:e5CrossRefPubMedGoogle Scholar
  14. 14.
    Obana A, Miki T, Hayashi K, Takeda M, Kawamura A, Mutoh T, Harino S, Fukushima I, Komatsu H, Takaku Y et al (1994) Survey of complications of indocyanine green angiography in Japan. Am J Ophthalmol 118:749–753CrossRefPubMedGoogle Scholar
  15. 15.
    Plummer SC (1896) III. Research on the surgical anatomy of the middle meningeal artery. Ann Surg 23:540–572CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Research Committee on the Pathology and Treatment of Spontaneous Occlusion of the Circle of Willis (2012) Guidelines for diagnosis and treatment of moyamoya disease (spontaneous occlusion of the circle of Willis). Neurol Med Chir (Tokyo) 52:245–266CrossRefGoogle Scholar
  17. 17.
    Shimizu S, Hagiwara H, Utsuki S, Oka H, Nakayama K, Fujii K (2008) Bony tunnel formation in the middle meningeal groove: an anatomic study for safer pterional craniotomy. Minim Invasive Neurosurg 51:329–332CrossRefPubMedGoogle Scholar
  18. 18.
    Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299CrossRefPubMedGoogle Scholar
  19. 19.
    Uchino H, Nakamura T, Kuroda S, Houkin K, Murata J, Saito H (2012) Intraoperative dual monitoring during carotid endarterectomy using motor evoked potentials and near-infrared spectroscopy. World Neurosurg 78:651–657CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2017

Authors and Affiliations

  • Nozomu Tanabe
    • 1
  • Shusuke Yamamoto
    • 1
  • Daina Kashiwazaki
    • 1
  • Naoki Akioka
    • 1
  • Naoya Kuwayama
    • 1
  • Kyo Noguchi
    • 2
  • Satoshi Kuroda
    • 1
  1. 1.Department of Neurosurgery, Graduate School of Medicine and Pharmaceutical ScienceUniversity of ToyamaToyamaJapan
  2. 2.Department of Radiology, Graduate School of Medicine and Pharmaceutical ScienceUniversity of ToyamaToyamaJapan

Personalised recommendations