Skip to main content

Advertisement

SpringerLink
Log in

Indocyanine green videoangiography for assessment of postoperative hyperperfusion in moyamoya disease

  • Clinical Article - Vascular
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

Postoperative cerebral hyperperfusion (HP) is a notable complication that occurs more frequently in moyamoya disease (MMD) than in atherosclerosis. This study aimed to clarify the characteristics of intraoperative indocyanine green (ICG) videoangiography in MMD and atherosclerotic disease in terms of postoperative HP.

Methods

This prospective study included 47 patients with 60 sides that underwent superior temporal artery (STA)-middle cerebral artery (MCA) single bypass. ICG videoangiography was performed after revascularization. The ICG time intensity curve was recorded in the STA, proximal MCA, distal MCA, and superficial Sylvian vein, and the angiographic differences among adult MMD, pediatric MMD, and atherosclerosis were analyzed.

Results

Twenty-two patients (27 sides) had adult MMD, 14 patients (22 sides) had pediatric MMD, and 11 patients (11 sides) had atherosclerosis. Postoperative HP was significantly higher in adult MMD (40.7 %) than in pediatric MMD (18.2 %) and atherosclerosis (0 %). Adult MMD with HP was associated with a longer ICG peak time (P < 0.001). There was no correlation between the ICG peak time and preoperative cerebral blood flow or vascular reserve. The ratio of the vessel caliber was also higher in adult MMD with HP (P < 0.001).

Conclusions

ICG videoangiography provides different characteristics of bypass flow among adult MMD, pediatric MMD, and atherosclerosis. Poor run-off and stagnation of blood flow from the STA might contribute to postoperative HP in MMD. The occurrence of postoperative HP in MMD could depend on two factors: donor STA size and poor run-off and integrity of the blood brain barrier in the recipient MCA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. 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 73:668–674

    Article  PubMed  Google Scholar 

  2. Carlson AP, Yonas H, Chang YF, Nemoto EM (2011) Failure of cerebral hemodynamic selection in general or of specific positron emission tomography methodology?: Carotid Occlusion Surgery Study (COSS). Stroke 42:3637–3639

    Article  PubMed Central  PubMed  Google Scholar 

  3. Czabanka M, Pena-Tapia P, Schubert GA, Woitzik J, Horn P, Schmiedek P, Vajkoczy P (2009) Clinical implications of cortical microvasculature in adult Moyamoya disease. J Cereb Blood Flow Metab 29:1383–1387

    Article  PubMed  Google Scholar 

  4. Czabanka M, Pena-Tapia P, Schubert GA, Woitzik J, Vajkoczy P, Schmiedek P (2008) Characterization of cortical microvascularization in adult moyamoya disease. Stroke 39:1703–1709

    Article  PubMed  Google Scholar 

  5. Fujimura M, Inoue T, Shimizu H, Saito A, Mugikura S, Tominaga T (2012) Efficacy of prophylactic blood pressure lowering according to a standardized postoperative management protocol to prevent symptomatic cerebral hyperperfusion after direct revascularization surgery for moyamoya disease. Cerebrovasc Dis 33:436–445

    Article  PubMed  Google Scholar 

  6. 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 

  7. 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 71:442–447

    Article  PubMed  Google Scholar 

  8. 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

    PubMed  Google Scholar 

  9. Fujimura M, Watanabe M, Narisawa A, Shimizu H, Tominaga T (2009) Increased expression of serum Matrix Metalloproteinase-9 in patients with moyamoya disease. Surg Neurol 72:476–480, discussion 480

    Article  PubMed  Google Scholar 

  10. Fukui M (1997) Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis ('moyamoya' disease). Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya Disease) of the Ministry of Health and Welfare. Jpn Clin Neurol Neurosurg 99(2):S238–S240

    Article  Google Scholar 

  11. Hayashi K, Horie N, Suyama K, Nagata I (2012) Incidence and clinical features of symptomatic cerebral hyperperfusion syndrome after vascular reconstruction. World Neurosurg 78:447–454

    Article  PubMed  Google Scholar 

  12. Horie N, Morikawa M, Nozaki A, Hayashi K, Suyama K, Nagata I (2011) "Brush Sign" on susceptibility-weighted MR imaging indicates the severity of moyamoya disease. AJNR Am J Neuroradiol 32:1697–1702

    Article  CAS  PubMed  Google Scholar 

  13. Horie N, So G, Debata A, Hayashi K, Morikawa M, Suyama K, Nagata I (2012) Intra-arterial indocyanine green angiography in the management of spinal arteriovenous fistulae: technical case reports. Spine 37:E264–E267

    Article  PubMed  Google Scholar 

  14. Kaku Y, Iihara K, Nakajima N, Kataoka H, Fukuda K, Masuoka J, Fukushima K, Iida H, Hashimoto N (2012) Cerebral blood flow and metabolism of hyperperfusion after cerebral revascularization in patients with moyamoya disease. J Cereb Blood Flow Metab 32:2066–2075

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Kamp MA, Slotty P, Turowski B, Etminan N, Steiger HJ, Hanggi D, Stummer W (2012) Microscope-integrated quantitative analysis of intraoperative indocyanine green fluorescence angiography for blood flow assessment: first experience in 30 patients. Neurosurgery 70:65–73, discussion 73–64

    Article  PubMed  Google Scholar 

  16. Kang HS, Kim JH, Phi JH, Kim YY, Kim JE, Wang KC, Cho BK, Kim SK (2010) Plasma matrix metalloproteinases, cytokines and angiogenic factors in moyamoya disease. J Neurol Neurosurg Psychiatry 81:673–678

    Article  PubMed  Google Scholar 

  17. 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 34:355–362, discussion 362

    Article  PubMed  Google Scholar 

  18. Kim JE, Oh CW, Kwon OK, Park SQ, Kim SE, Kim YK (2008) Transient hyperperfusion after superficial temporal artery/middle cerebral artery bypass surgery as a possible cause of postoperative transient neurological deterioration. Cerebrovasc Dis 25:580–586

    Article  PubMed  Google Scholar 

  19. Kuroda S, Houkin K (2008) Moyamoya disease: current concepts and future perspectives. Lancet Neurol 7:1056–1066

    Article  PubMed  Google Scholar 

  20. 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 31:262–274

    Article  PubMed Central  PubMed  Google Scholar 

  21. 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:E5

    Article  PubMed Central  PubMed  Google Scholar 

  22. Mizumura S, Nakagawara J, Takahashi M, Kumita S, Cho K, Nakajo H, Toba M, Kumazaki T (2004) Three-dimensional display in staging hemodynamic brain ischemia for JET study: objective evaluation using SEE analysis and 3D-SSP display. Ann Nucl Med 18:13–21

    Article  PubMed  Google Scholar 

  23. Nakagawa A, Fujimura M, Arafune T, Sakuma I, Tominaga T (2009) Clinical implications of intraoperative infrared brain surface monitoring during superficial temporal artery-middle cerebral artery anastomosis in patients with moyamoya disease. J Neurosurg 111:1158–1164

    Article  PubMed  Google Scholar 

  24. Powers WJ (2012) Letter by Powers Regarding Article, "Failure of cerebral hemodynamic selection in general or of specific positron emission tomography methodology? Carotid occlusion surgery study (COSS)". Stroke 43:e43, author reply e44

    Article  PubMed  Google Scholar 

  25. Powers WJ, Clarke WR, Grubb RL Jr, Videen TO, Adams HP Jr, Derdeyn CP, Investigators C (2011) Extracranial-intracranial bypass surgery for stroke prevention in hemodynamic cerebral ischemia: the Carotid Occlusion Surgery Study randomized trial. JAMA 306:1983–1992

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Raabe A, Beck J, Gerlach R, Zimmermann M, Seifert V (2003) Near-infrared indocyanine green video angiography: a new method for intraoperative assessment of vascular flow. Neurosurgery 52:132–139, discussion 139

    PubMed  Google Scholar 

  27. Raabe A, Nakaji P, Beck J, Kim LJ, Hsu FP, Kamerman JD, Seifert V, Spetzler RF (2005) Prospective evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green videoangiography during aneurysm surgery. J Neurosurg 103:982–989

    Article  PubMed  Google Scholar 

  28. Schubert GA, Seiz-Rosenhagen M, Ortler M, Czabanka M, Scheufler KM, Thome C (2012) Cortical indocyanine green videography for quantification of acute hypoperfusion after subarachnoid hemorrhage: a feasibility study. Neurosurgery 71:260–267, discussion ons267-268

    Article  Google Scholar 

  29. Suzuki J, Kodama N (1983) Moyamoya disease–a review. Stroke 14:104–109

    Article  CAS  PubMed  Google Scholar 

  30. Suzuki J, Takaku A (1969) Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299

    Article  CAS  PubMed  Google Scholar 

  31. Takagi Y, Sawamura K, Hashimoto N, Miyamoto S (2012) Evaluation of serial intraoperative surgical microscope-integrated intraoperative near-infrared indocyanine green videoangiography in patients with cerebral arteriovenous malformations. Neurosurgery 70:34–42, discussion 42–33

    Article  PubMed  Google Scholar 

  32. Terborg C, Groschel K, Petrovitch A, Ringer T, Schnaudigel S, Witte OW, Kastrup A (2009) Noninvasive assessment of cerebral perfusion and oxygenation in acute ischemic stroke by near-infrared spectroscopy. Eur Neurol 62:338–343

    Article  CAS  PubMed  Google Scholar 

  33. 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 

  34. Uchino H, Nakamura T, Houkin K, Murata J, Saito H, Kuroda S (2013) Semiquantitative analysis of indocyanine green videoangiography for cortical perfusion assessment in superficial temporal artery to middle cerebral artery anastomosis. Acta Neurochir 155:599–605

    Article  PubMed  Google Scholar 

  35. Washington CW, Zipfel GJ, Chicoine MR, Derdeyn CP, Rich KM, Moran CJ, Cross DT, Dacey RG Jr (2013) Comparing indocyanine green videoangiography to the gold standard of intraoperative digital subtraction angiography used in aneurysm surgery. J Neurosurg 118:420–427

    Article  PubMed  Google Scholar 

  36. Yoshimoto T, Houkin K, Kuroda S, Abe H, Kashiwaba T (1997) Low cerebral blood flow and perfusion reserve induce hyperperfusion after surgical revascularization: case reports and analysis of cerebral hemodynamics. Surg Neurol 48:132–138, discussion 138–139

    Article  CAS  PubMed  Google Scholar 

Download references

Conflicts of interest

This work was supported in part by a Grant-in-Aid for Scientific Research to N.H. (23791611) and I.N. (24592134). The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Nagasaki University School of Medicine, 1-7-1 Sakamoto, Nagasaki, 852-8501, Japan

    Nobutaka Horie, Yuhtaka Fukuda, Tsuyoshi Izumo, Kentaro Hayashi, Kazuhiko Suyama & Izumi Nagata

Authors
  1. Nobutaka Horie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuhtaka Fukuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tsuyoshi Izumo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kentaro Hayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kazuhiko Suyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Izumi Nagata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nobutaka Horie.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Horie, N., Fukuda, Y., Izumo, T. et al. Indocyanine green videoangiography for assessment of postoperative hyperperfusion in moyamoya disease. Acta Neurochir 156, 919–926 (2014). https://doi.org/10.1007/s00701-014-2054-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-014-2054-4

Keywords

Search

Navigation