Skip to main content
Erschienen in: Acta Neurochirurgica 3/2017

17.01.2017 | Original Article - Vascular

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

verfasst von: Sayaka Ogawa, Hiroshi Abe, Toshiro Katsuta, Kenji Fukuda, Toshiyasu Ogata, Koichi Miki, Tooru Inoue

Erschienen in: Acta Neurochirurgica | Ausgabe 3/2017

Einloggen, um Zugang zu erhalten

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.
Literatur
1.
Zurück zum Zitat 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 73:430–439CrossRefPubMed 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 73:430–439CrossRefPubMed
2.
Zurück zum Zitat 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 121:1394–1400CrossRefPubMed 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 121:1394–1400CrossRefPubMed
3.
Zurück zum Zitat 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 312CrossRefPubMed 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 312CrossRefPubMed
4.
Zurück zum Zitat 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 632-623CrossRefPubMed 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 632-623CrossRefPubMed
5.
Zurück zum Zitat 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 14:216–222CrossRefPubMedPubMedCentral 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 14:216–222CrossRefPubMedPubMedCentral
6.
Zurück zum Zitat 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 43CrossRefPubMed 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 43CrossRefPubMed
7.
Zurück zum Zitat 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 325:10–14CrossRefPubMed 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 325:10–14CrossRefPubMed
8.
Zurück zum Zitat 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 67:273–282CrossRefPubMed 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 67:273–282CrossRefPubMed
9.
Zurück zum Zitat 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 964-955CrossRefPubMed 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 964-955CrossRefPubMed
10.
Zurück zum Zitat 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 123:654–661CrossRefPubMed 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 123:654–661CrossRefPubMed
11.
Zurück zum Zitat 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 83:691–699CrossRefPubMed 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 83:691–699CrossRefPubMed
12.
Zurück zum Zitat 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) 52:333–338CrossRef 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) 52:333–338CrossRef
13.
Zurück zum Zitat 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 114:930–934CrossRefPubMed 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 114:930–934CrossRefPubMed
14.
Zurück zum Zitat Lin N, Aronson JP, Manjila S, Smith ER, Scott RM (2014) Treatment of moyamoya disease in the adult population with pial synangiosis. J Neurosurg 120:612–617CrossRefPubMed Lin N, Aronson JP, Manjila S, Smith ER, Scott RM (2014) Treatment of moyamoya disease in the adult population with pial synangiosis. J Neurosurg 120:612–617CrossRefPubMed
15.
Zurück zum Zitat 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 31:401–405CrossRefPubMed 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 31:401–405CrossRefPubMed
16.
Zurück zum Zitat Pandey P, Steinberg GK (2011) Outcome of repeat revascularization surgery for moyamoya disease after an unsuccessful indirect revascularization. clinical article. J Neurosurg 115:328–336CrossRefPubMed Pandey P, Steinberg GK (2011) Outcome of repeat revascularization surgery for moyamoya disease after an unsuccessful indirect revascularization. clinical article. J Neurosurg 115:328–336CrossRefPubMed
17.
Zurück zum Zitat 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 103:869–872CrossRefPubMed 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 103:869–872CrossRefPubMed
18.
Zurück zum Zitat 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 10:252–259CrossRefPubMedPubMedCentral 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 10:252–259CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Starke RM, Komotar RJ, Connolly ES (2009) Optimal surgical treatment for moyamoya disease in adults: direct versus indirect bypass. Neurosurg Focus 26:E8CrossRefPubMed Starke RM, Komotar RJ, Connolly ES (2009) Optimal surgical treatment for moyamoya disease in adults: direct versus indirect bypass. Neurosurg Focus 26:E8CrossRefPubMed
20.
Zurück zum Zitat 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 43:2610–2616CrossRefPubMed 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 43:2610–2616CrossRefPubMed
21.
Zurück zum Zitat 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 23:2573–2579CrossRefPubMed 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 23:2573–2579CrossRefPubMed
22.
Zurück zum Zitat 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 75:258–263CrossRefPubMed 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 75:258–263CrossRefPubMed
23.
Zurück zum Zitat 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 29:868–870CrossRefPubMed 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 29:868–870CrossRefPubMed
Metadaten
Titel
Early and noninvasive evaluation using superficial temporal artery duplex ultrasonography after indirect bypass for adult ischemic moyamoya disease
verfasst von
Sayaka Ogawa
Hiroshi Abe
Toshiro Katsuta
Kenji Fukuda
Toshiyasu Ogata
Koichi Miki
Tooru Inoue
Publikationsdatum
17.01.2017
Verlag
Springer Vienna
Erschienen in
Acta Neurochirurgica / Ausgabe 3/2017
Print ISSN: 0001-6268
Elektronische ISSN: 0942-0940
DOI
https://doi.org/10.1007/s00701-016-3073-0

Weitere Artikel der Ausgabe 3/2017

Acta Neurochirurgica 3/2017 Zur Ausgabe

Review Article - Forthcoming Meeting

An update on idiopathic intracranial hypertension

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.