Neurosurgical Review

, Volume 36, Issue 3, pp 411–419 | Cite as

Hemodynamics and changes after STA–MCA anastomosis in moyamoya disease and atherosclerotic cerebrovascular disease measured by micro-Doppler ultrasonography

  • Hanako Morisawa
  • Takakazu Kawamata
  • Akitsugu Kawashima
  • Masataka Hayashi
  • Kohji Yamaguchi
  • Taku Yoneyama
  • Yoshikazu Okada
Original Article

Abstract

Moyamoya disease (MMD) and atherosclerotic cerebrovascular disease (ACVD) differ in angiographic appearance and probably hemodynamics. Pediatric MMD (PMMD) usually presents with cerebral ischemia, while intracranial hemorrhage is more common in adult MMD (AMMD), suggesting differences in cerebral hemodynamics. We analyzed the cortical flow velocity and direction of recipient arteries using micro-Doppler ultrasonography to evaluate the cortical circulation before and after anastomosis in MMD and ACVD. Twenty-eight patients with adult MMD (AMMD), 7 with pediatric MMD (PMMD), 16 with ACVD, and 12 control patients were studied. A micro-Doppler probe was applied on the cortical recipient artery (A4 or M4) before and after anastomosis. Systolic maximum flow velocity (V max) and blood flow direction were investigated at proximal and distal parts of anastomosed sites in recipient arteries. Pre- and postoperative regional cerebral blood flow was measured by cold xenon-computed tomography (Xe-CT). Before anastomosis, retrograde cortical flow was significantly more common in PMMD patients, and V max in cortical artery was significantly lower in AMMD patients. Bypass surgery changed the direction of blood flow from the anastomosis site to proximal and distal sites of the recipient artery in most patients, but pre-anastomosis flow direction was preserved more frequently in PMMD patients. The rate of V max increase after anastomosis was significantly higher in AMMD than in PMMD (11.6 ± 9.8 vs. 3.9 ± 1.8; P = 0.01). Micro-Doppler ultrasonography identified differences in cortical circulation among AMMD, PMMD, and ACVD. In AMMD, significantly low velocity in the cortical artery was observed before anastomosis, and bypass surgery reversed the flow and significantly increased flow velocity. The data of PMMD showed unique hemodynamics of the cortical artery before anastomosis, characterized by a higher frequency of retrograde flow and preserved velocity. The V max increase rate was significantly higher in patients with postoperative cerebral hyperperfusion on Xe-CT, and further study is warranted to validate the clinical use of intraoperative micro-Doppler monitoring to predict postoperative hyperperfusion.

Keywords

Atherosclerotic EC–IC bypass Hyperperfusion Micro-Doppler ultrasonography Moyamoya disease 

Notes

Acknowledgments

We thank the radiological technicians at the Departments of Neurosurgery and Radiology, Tokyo Women’s Medical University, Tokyo, Japan, for measurements of rCBF and CVR on cold Xe-CT. This study was supported by research funds of the Department of Neurosurgery, Tokyo Women’s Medical University.

Conflict of interest

All authors have no conflict of interest to declare.

References

  1. 1.
    Akdemir H, Oktem S, Menkü A, Tucer B, Tuğcu B, Günaldi O (2007) Image-guided microneurosurgical management of small arteriovenous malformation: role of neuronavigation and intraoperative Doppler sonography. Minim Invasive Neurosurg 50:163–169CrossRefPubMedGoogle Scholar
  2. 2.
    Awano T, Sakatani K, Yokose N, Kondo Y, Igarashi T, Hoshino T, Nakamura S, Fujiwara N, Murata Y, Katayama Y, Shikayama T, Miwa M (2010) Intraoperative EC-IC bypass blood flow assessment with indocyanine green angiography in moyamoya and non-moyamoya ischemic stroke. World Neurosurg 73:668–674CrossRefPubMedGoogle Scholar
  3. 3.
    Bishop CCR, Powell S, Rutt D (1986) Transcranial Doppler measurement of middle cerebral artery blood flow velocity: a validation study. Stroke 17:913–915CrossRefPubMedGoogle Scholar
  4. 4.
    Czabanka M, Peña-Tapia P, Schubert GA, Heppner FL, Martus P, Horn P, Schmiedek P, Vajkoczy P (2011) Proposal for a new grading of moyamoya disease in adult patients. Cerebrovasc Dis 32:41–50CrossRefPubMedGoogle Scholar
  5. 5.
    Czabanka M, Peña-Tapia P, Schubert GA, Woitzik J, Vajkoczy P, Schmiedek P (2008) Characterization of cortical microvascularization in adult Moyamoya disease. Stroke 39:1703–1709CrossRefPubMedGoogle Scholar
  6. 6.
    Fujimura M, Mugikura S, Kaneta T, Shimizu H, Tominaga T (2009) Incidence and risk factors for symptomatic cerebral hyperperfusion after superficial temporal artery–middle cerebral artery anastomosis in patients with moyamoya disease. Surg Neurol 71:442–447CrossRefPubMedGoogle Scholar
  7. 7.
    Gesang DZ, Zhang D, Zhao JZ, Wang S, Zhao YL, Wang R, Sun JJ, Meng Z (2009) Laser Doppler flowmeter study on regional cerebral blood flow in early stage after standard superficial temporal artery–middle cerebral artery bypass surgery for moyamoya disease. Chin Med J 122:2412–2418PubMedGoogle Scholar
  8. 8.
    Houkin K, Yoshimoto T, Kuroda S, Ishikawa T, Takahashi A, Abe H (1996) Angiographic analysis of moyamoya disease—how does moyamoya disease progress? Neurol Med Chir (Tokyo) 36:783–788CrossRefGoogle Scholar
  9. 9.
    Kapsalaki EZ, Lee GP, Robinson JS 3rd, Grigorian AA, Fountas KN (2008) The role of intraoperative micro-Doppler ultrasound in verifying proper clip placement in intracranial aneurysm surgery. J Clin Neurosci 15:153–157CrossRefPubMedGoogle Scholar
  10. 10.
    Kawamata T, Kawashima A, Yamaguchi K, Hori T, Okada Y (2011) Usefulness of intraoperative laser Doppler flowmetry and thermography to predict a risk of postoperative hyperperfusion after superficial temporal artery–middle cerebral artery bypass for moyamoya disease. Neurosurg Rev 34:355–362CrossRefPubMedGoogle Scholar
  11. 11.
    Kawamata T, Okada Y, Kawashima A, Yoneyama T, Yamaguchi K, Ono Y, Hori T (2009) Postcarotid endarterectomy cerebral hyperperfusion can be prevented by minimizing intraoperative cerebral ischemia and strict postoperative blood pressure control under continuous sedation. Neurosurgery 64:447–454CrossRefPubMedGoogle Scholar
  12. 12.
    Kawashima A, Kawamata T, Yamaguchi K, Hori T, Okada Y (2010) Successful superficial temporal artery–anterior cerebral artery direct bypass using a long graft for moyamoya disease: technical note. Neurosurgery 67 (3 Suppl Operative):ons145–149Google Scholar
  13. 13.
    Kim SK, Seol HJ, Cho BK, Hwang YS, Lee DS, Wang KC (2004) Moyamoya disease among young patients: its aggressive clinical course and the role of active surgical treatment. Neurosurgery 54:840–846CrossRefPubMedGoogle Scholar
  14. 14.
    Lee M, Guzman R, Bell-Stephens T, Steinberg GK (2011) Intraoperative blood flow analysis of direct revascularization procedures in patients with moyamoya disease. J Cereb Blood Flow Metab 31:262–274CrossRefPubMedGoogle Scholar
  15. 15.
    Lee M, Zaharchuk G, Guzman R, Achrol A, Bell-Stephens T, Steinberg GK (2009) Quantitative hemodynamic studies in moyamoya disease: a review. Neurosurg Focus 26:E5CrossRefPubMedGoogle Scholar
  16. 16.
    Mücke T, Wolff KD, Wagenpfeil S, Hölzle F, Scholz M (2010) Reliability of near-infrared angiography and micro-Doppler sonography for evaluating microvascular anastomoses. Plast Reconstr Surg 126:1506–1514CrossRefPubMedGoogle Scholar
  17. 17.
    Nakagawa A, Fujimura M, Arafune T, Suzuki H, Sakuma I, Tominaga T (2008) Intraoperative infrared brain surface blood flow monitoring during superficial temporal artery–middle cerebral artery anastomosis in a patient with moyamoya disease: clinical implication of the gradation value in postoperative clinical course—a case report. Acta Neurochir Suppl 102:159–163CrossRefPubMedGoogle Scholar
  18. 18.
    Nishimoto A, Takeuchi S (1968) Abnormal cerebral vascular network related to the internal carotid arteries. J Neurosurg 29:255–260CrossRefPubMedGoogle Scholar
  19. 19.
    Obara K, Fukuuchi Y, Kobari M, Watanabe S, Dembo T (1997) Cerebral hemodynamics in patients with moyamoya disease and in patients with atherosclerotic occlusion of the major cerebral arterial trunks. Clin Neurol Neurosurg 99(Suppl 2):S86–S89CrossRefPubMedGoogle Scholar
  20. 20.
    Ogasawara K, Ogawa A (2006) JET study (Japanese EC-IC Bypass Trial). Nippon Rinsho 64(Suppl 7):524–527PubMedGoogle Scholar
  21. 21.
    Okada Y, Kawamata T, Kawashima A, Hori T (2007) Intraoperative application of thermography in extracranial-intracranial bypass surgery. Neurosurgery 60(4 Suppl 2):362–365PubMedGoogle Scholar
  22. 22.
    Okada Y, Kawamata T, Kawashima A, Yamaguchi K, Ono Y, Hori T (2012) The efficacy of superficial temporal artery–middle cerebral artery anastomosis in patients with moyamoya disease complaining of severe headache. J Neurosurg 116:672–679CrossRefPubMedGoogle Scholar
  23. 23.
    Okada Y, Shima T, Nishida M, Yamane K, Yamada T, Yamanaka C (1998) Effectiveness of superficial temporal artery–middle cerebral artery anastomosis in adult moyamoya disease: cerebral hemodynamics and clinical course in ischemic and hemorrhagic varieties. Stroke 29:625–630CrossRefPubMedGoogle Scholar
  24. 24.
    Okada Y, Shima T, Yamane K, Yamanaka C, Kagawa R (1999) Cylindrical or T-shaped silicone rubber stents for microanastomosis—technical note. Neurol Med Chir (Tokyo) 39:55–58CrossRefGoogle Scholar
  25. 25.
    Ruan LT, Duan YY, Cao TS, Zhuang L, Huang L (2006) Color and power Doppler sonography of extracranial and intracranial arteries in Moyamoya disease. J Clin Ultrasound 34:60–69CrossRefPubMedGoogle Scholar
  26. 26.
    Suzuki J, Kodama N (1983) Moyamoya disease: a review. Stroke 14:104–109CrossRefPubMedGoogle Scholar
  27. 27.
    Suzuki J, Takaku A (1969) Cerebrovascular “moyamoya” disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299CrossRefPubMedGoogle Scholar
  28. 28.
    Takanashi J (2011) Moyamoya disease in children. Brain Dev 33:229–234CrossRefPubMedGoogle Scholar
  29. 29.
    Takase K, Kashihara M, Hashimoto T (1997) Transcranial Doppler ultrasonography in patients with moyamoya disease. Clin Neurol Neurosurg 99(Suppl 2):S101–S105PubMedGoogle Scholar
  30. 30.
    Yamaguchi K, Kawamata T, Kawashima A, Hori T, Okada Y (2010) Incidence and predictive factors of cerebral hyperperfusion after extracranial–intracranial bypass for occlusive cerebrovascular diseases. Neurosurgery 67:1548–1554CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Hanako Morisawa
    • 1
  • Takakazu Kawamata
    • 1
  • Akitsugu Kawashima
    • 1
  • Masataka Hayashi
    • 1
  • Kohji Yamaguchi
    • 1
  • Taku Yoneyama
    • 1
  • Yoshikazu Okada
    • 1
  1. 1.Department of NeurosurgeryTokyo Women’s Medical UniversityTokyoJapan

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