Top

Acta Neurochirurgica

Published in:

01-09-2014 | Clinical Article - Vascular

Intraoperative assessment of cortical perfusion by indocyanine green videoangiography in surgical revascularization for moyamoya disease

Authors: Haruto Uchino, Ken Kazumata, Masaki Ito, Naoki Nakayama, Satoshi Kuroda, Kiyohiro Houkin

Published in: Acta Neurochirurgica | Issue 9/2014

Abstract

Background

Postoperative hyperperfusion is a potential complication of the direct bypass procedure for moyamoya disease (MMD). However, no reliable modality is available yet for the prediction of postoperative hyperperfusion during surgery for MMD. This study aimed to investigate whether semiquantitative analysis of indocyanine green (ICG) videoangiography could contribute to the prediction of postoperative hyperperfusion in MMD.

Methods

This study included 12 hemispheres from 10 patients who underwent surgical revascularization for MMD. Intraoperative ICG videoangiography was performed before and after a direct bypass procedure. The ICG intensity-time curves were semiquantitatively analyzed to evaluate cortical perfusion by calculating the blood flow index (BFI). Using single-photon emission computed tomography (SPECT), postoperative cerebral blood flow measurements were performed thrice: immediately, and 2 and 7 days after surgery.

Results

BFI significantly increased from 21.3 ± 10.5 to 38.4 ± 20.0 after bypass procedures in all the hemispheres (p < 0.01). The ratio of BFI before and after the bypass procedure was 2.4 ± 2.0, ranging from 0.5 to 8.0. Postoperative hyperperfusion was observed in nine of the 12 operated hemispheres within 7 days after surgery. Of these, three hemispheres developed hyperperfusion immediately after surgery. In the adult cases, the increase in the ratio of BFI after bypass was significantly greater in those who developed hyperperfusion immediately after surgery than in those who did not (6.5 ± 0.5 vs. 1.8 ± 2.1, p < 0.01). In contrast, no significant increase in BFI was observed in the pediatric MMD patients who experienced immediate hyperperfusion. No correlation between the changes in BFI and the occurrence of delayed hyperperfusion was observed.

Conclusions

Our results suggest that semiquantitative analysis of BFI by intraoperative ICG videoangiography is useful in evaluating changes in cortical perfusion after bypass procedures for MMD and can predict the occurrence of early-onset hyperperfusion in MMD patients after direct bypass.

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

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

Guzman R, Lee M, Achrol A, Bell-Stephens T, Kelly M, Do HM, Marks MP, Steinberg GK (2009) Clinical outcome after 450 revascularization procedures for moyamoya disease. Clinical article. J Neurosurg 111:927–935PubMedCrossRef

Houkin K, Kamiyama H, Takahashi A, Kuroda S, Abe H (1997) Combined revascularization surgery for childhood moyamoya disease: STA-MCA and encephalo-duro-arterio-myo-synangiosis. Childs Nerv Syst 13:24–29PubMedCrossRef

Ishikawa T, Houkin K, Kamiyama H, Abe H (1997) Effects of surgical revascularization on outcome of patients with pediatric moyamoya disease. Stroke 28:1170–1173PubMedCrossRef

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 77:84–89PubMedCrossRef

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 1101PubMedCrossRef

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:e5PubMedCrossRef

Kuroda S, Houkin K (2012) Bypass surgery for moyamoya disease: concept and essence of sugical techniques. Neurol Med Chir (Tokyo) 52:287–294

10.

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 67:273–282PubMedCrossRef

11.

Ogasawara K, Komoribayashi N, Kobayashi M, Fukuda T, Inoue T, Yamadate K, Ogawa A (2005) Neural damage caused by cerebral hyperperfusion after arterial bypass surgery in a patient with moyamoya disease: case report. Neurosurgery 56:E1380, discussion E1380PubMedCrossRef

12.

Sasamori T, Kuroda S, Nakayama N, Iwasaki Y (2010) Incidence and pathogenesis of transient cheiro-oral syndrome after surgical revascularization for moyamoya disease. Neurosurgery 67:1054–1059, discussion 1060PubMedCrossRef

13.

Uno M, Nakajima N, Nishi K, Shinno K, Nagahiro S (1998) Hyperperfusion syndrome after extracranial-intracranial bypass in a patient with moyamoya disease–case report. Neurol Med Chir (Tokyo) 38:420–424CrossRef

14.

Furuya K, Kawahara N, Morita A, Momose T, Aoki S, Kirino T (2004) Focal hyperperfusion after superficial temporal artery-middle cerebral artery anastomosis in a patient with moyamoya disease. Case report. J Neurosurg 100:128–132PubMedCrossRef

15.

Ohue S, Kumon Y, Kohno K, Watanabe H, Iwata S, Ohnishi T (2008) Postoperative temporary neurological deficits in adults with moyamoya disease. Surg Neurol 69:281–286, discussion 286–287PubMedCrossRef

16.

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 71:442–447PubMedCrossRef

17.

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 43:2610–2616PubMedCrossRef

18.

Killory BD, Nakaji P, Gonzales LF, Ponce FA, Wait SD, Spetzler RF (2009) Prospective evaluation of surgical microscope-integrated intraoperative near-infrared indocyanine green angiography during cerebral arteriovenous malformation surgery. Neurosurgery 65:456–462, discussion 462PubMedCrossRef

19.

Kuroiwa T, Kajimoto Y, Ohta T (2001) Development and clinical application of near-infrared surgical microscope: preliminary report. Minim Invasive Neurosurg 44:240–242PubMedCrossRef

20.

Pena-Tapia PG, Kemmling A, Czabanka M, Vajkoczy P, Schmiedek P (2008) Identification of the optimal cortical target point for extracranial-intracranial bypass surgery in patients with hemodynamic cerebrovascular insufficiency. J Neurosurg 108:655–661PubMedCrossRef

21.

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 139PubMed

22.

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 103:982–989PubMedCrossRef

23.

Woitzik J, Horn P, Vajkoczy P, Schmiedek P (2005) Intraoperative control of extracranial-intracranial bypass patency by near-infrared indocyanine green videoangiography. J Neurosurg 102:692–698PubMedCrossRef

24.

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 (Wien) 155:599–605CrossRef

25.

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) 52:245–266CrossRef

26.

Hokari M, Kuroda S, Shiga T, Nakayama N, Tamaki N, Iwasaki Y (2008) Combination of a mean transit time measurement with an acetazolamide test increases predictive power to identify elevated oxygen extraction fraction in occlusive carotid artery diseases. J Nucl Med 49:1922–1927PubMedCrossRef

27.

Hokari M, Kuroda S, Shiga T, Nakayama N, Tamaki N, Iwasaki Y (2009) Impact of oxygen extraction fraction on long-term prognosis in patients with reduced blood flow and vasoreactivity because of occlusive carotid artery disease. Surg Neurol 71:532–538, discussion 538, 538–539PubMedCrossRef

28.

Kuroda S, Shiga T, Houkin K, Ishikawa T, Katoh C, Tamaki N, Iwasaki Y (2006) Cerebral oxygen metabolism and neuronal integrity in patients with impaired vasoreactivity attributable to occlusive carotid artery disease. Stroke 37:393–398PubMedCrossRef

29.

Kuroda S, Shiga T, Ishikawa T, Houkin K, Narita T, Katoh C, Tamaki N, Iwasaki Y (2004) Reduced blood flow and preserved vasoreactivity characterize oxygen hypometabolism due to incomplete infarction in occlusive carotid artery diseases. J Nucl Med 45:943–949PubMed

30.

Kuroda S, Houkin K, Kamiyama H, Mitsumori K, Iwasaki Y, Abe H (2001) Long-term prognosis of medically treated patients with internal carotid or middle cerebral artery occlusion: can acetazolamide test predict it? Stroke 32:2110–2116PubMedCrossRef

31.

Kuroda S, Kamiyama H, Abe H, Houkin K, Isobe M, Mitsumori K (1993) Acetazolamide test in detecting reduced cerebral perfusion reserve and predicting long-term prognosis in patients with internal carotid artery occlusion. Neurosurgery 32:912–918, discussion 918–919PubMedCrossRef

32.

Kazumata K, Ito M, Tokairin K, Ito Y, Houkin K, Nakayama N, Kuroda S, Ishikawa T, Kamiyama H (2014) The frequency of postoperative stroke in moyamoya disease following combined revascularization: a single-university series and systematic review. J Neurosurg

33.

Kuebler WM, Sckell A, Habler O, Kleen M, Kuhnle GE, Welte M, Messmer K, Goetz AE (1998) Noninvasive measurement of regional cerebral blood flow by near-infrared spectroscopy and indocyanine green. J Cereb Blood Flow Metab 18:445–456PubMedCrossRef

34.

Perbeck L, Lewis DH, Thulin L, Tyden G (1985) Correlation between fluorescein flowmetry, 133Xenon clearance and electromagnetic flow measurement: a study in the intestine of the pig. Clin Physiol 5:293–299PubMedCrossRef

35.

Woitzik J, Pena-Tapia PG, Schneider UC, Vajkoczy P, Thome C (2006) Cortical perfusion measurement by indocyanine-green videoangiography in patients undergoing hemicraniectomy for malignant stroke. Stroke 37:1549–1551PubMedCrossRef

36.

Hatazawa J, Fujita H, Kanno I, Satoh T, Iida H, Miura S, Murakami M, Okudera T, Inugami A, Ogawa T, Shimosegawa E, Noguchi K, Shohji Y, Uemura K (1995) Regional cerebral blood flow, blood volume, oxygen extraction fraction, and oxygen utilization rate in normal volunteers measured by the autoradiographic technique and the single breath inhalation method. Ann Nucl Med 9:15–21PubMedCrossRef

37.

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 33:436–445PubMedCrossRef

38.

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 362PubMedCrossRef

39.

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 64:447–453, discussion 453–444PubMedCrossRef

40.

van Mook WN, Rennenberg RJ, Schurink GW, van Oostenbrugge RJ, Mess WH, Hofman PA, de Leeuw PW (2005) Cerebral hyperperfusion syndrome. Lancet Neurol 4:877–888PubMedCrossRef

41.

Horie N, Fukuda Y, Izumo T, Hayashi K, Suyama K, Nagata I (2014) Indocyanine green videoangiography for assessment of postoperative hyperperfusion in moyamoya disease. Acta Neurochir (Wien) 156:919–926CrossRef

Title: Intraoperative assessment of cortical perfusion by indocyanine green videoangiography in surgical revascularization for moyamoya disease
Authors: Haruto Uchino
Ken Kazumata
Masaki Ito
Naoki Nakayama
Satoshi Kuroda
Kiyohiro Houkin
Publication date: 01-09-2014
Publisher: Springer Vienna
Published in: Acta Neurochirurgica / Issue 9/2014
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI: https://doi.org/10.1007/s00701-014-2161-2

At a glance: The STEP trials

Springer Medicine

Intraoperative assessment of cortical perfusion by indocyanine green videoangiography in surgical revascularization for moyamoya disease

Abstract

Background

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 9/2014

Pathophysiology of flow impairment during carotid artery stenting with an embolus protection filter

Michael T. Lawton: Seven AVMs: tenets and techniques for resection

Endovascular approaches for morphologically unfavorable intracranial aneurysms: adjunctive coiling techniques versus flow diversion

Carotid endarterectomy and carotid artery stenting: changing paradigm during 10 years in a high-volume centre

Response to letter, ‘Endovascular approaches for morphologically unfavorable intracranial aneurysms: adjunctive coiling techniques versus flow diversion’

Aneurysms of the anterior and posterior cerebral circulation: comparison of the morphometric features