Influence of an improvement in frontal lobe hemodynamics on neurocognitive function in adult patients with moyamoya disease.
Humans
Moyamoya Disease
/ surgery
Female
Male
Adult
Frontal Lobe
/ surgery
Middle Aged
Cerebral Revascularization
/ methods
Hemodynamics
/ physiology
Neuropsychological Tests
Retrospective Studies
Treatment Outcome
Anterior Cerebral Artery
/ surgery
Young Adult
Cerebrovascular Circulation
/ physiology
Anterior cerebral artery
Bypass
Frontal lobe
Hemodynamic insufficiency
Moyamoya disease
Neurocognitive function
Revascularization
Journal
Neurosurgical review
ISSN: 1437-2320
Titre abrégé: Neurosurg Rev
Pays: Germany
ID NLM: 7908181
Informations de publication
Date de publication:
02 Aug 2024
02 Aug 2024
Historique:
received:
01
04
2024
accepted:
29
07
2024
revised:
31
05
2024
medline:
2
8
2024
pubmed:
2
8
2024
entrez:
2
8
2024
Statut:
epublish
Résumé
In adults, moyamoya disease (MMD) often presents with slight neurocognitive impairment, which may result from frontal lobe hemodynamic insufficiency. In this study, we performed revascularization surgery by superficial temporal artery-anterior cerebral artery (ACA) direct bypass in 20 adults with MMD with poor anterograde ACA flow (Group M). The pre- and postoperative neurocognitive test results of these patients were retrospectively analyzed. The comparative group (Group C) included 23 patients with unruptured aneurysms or brain tumors who underwent craniotomy, as well as the same neurocognitive tests as Group M. We calculated the compositive frontal lobe function index (CFFI) based on the results of seven neurocognitive tests for each patient, and the difference between the pre- and postoperative CFFI values (CFFI Post - Pre) was compared between the two groups. Frontal perfusion improved postoperatively in all patients in Group M. The CFFI Post - Pre was significantly higher in Group M than in Group C (0.23 ± 0.44 vs. - 0.20 ± 0.32; p < 0.001). After adjusting for postoperative age, sex, preoperative non-verbal intelligence quotient, and preoperative period of stress, Group M had a significantly higher CFFI Post - Pre than Group C in the multiple regression analysis (t value = 4.01; p < 0.001). Improving frontal lobe hemodynamics might be the key for improving neurocognitive dysfunction in adults with MMD. The surgical indication and method should be considered from the perspective of both stroke prevention and neurocognitive improvement or protection.
Sections du résumé
BACKGROUND
BACKGROUND
In adults, moyamoya disease (MMD) often presents with slight neurocognitive impairment, which may result from frontal lobe hemodynamic insufficiency.
METHODS
METHODS
In this study, we performed revascularization surgery by superficial temporal artery-anterior cerebral artery (ACA) direct bypass in 20 adults with MMD with poor anterograde ACA flow (Group M). The pre- and postoperative neurocognitive test results of these patients were retrospectively analyzed. The comparative group (Group C) included 23 patients with unruptured aneurysms or brain tumors who underwent craniotomy, as well as the same neurocognitive tests as Group M. We calculated the compositive frontal lobe function index (CFFI) based on the results of seven neurocognitive tests for each patient, and the difference between the pre- and postoperative CFFI values (CFFI Post - Pre) was compared between the two groups.
RESULTS
RESULTS
Frontal perfusion improved postoperatively in all patients in Group M. The CFFI Post - Pre was significantly higher in Group M than in Group C (0.23 ± 0.44 vs. - 0.20 ± 0.32; p < 0.001). After adjusting for postoperative age, sex, preoperative non-verbal intelligence quotient, and preoperative period of stress, Group M had a significantly higher CFFI Post - Pre than Group C in the multiple regression analysis (t value = 4.01; p < 0.001).
CONCLUSION
CONCLUSIONS
Improving frontal lobe hemodynamics might be the key for improving neurocognitive dysfunction in adults with MMD. The surgical indication and method should be considered from the perspective of both stroke prevention and neurocognitive improvement or protection.
Identifiants
pubmed: 39093494
doi: 10.1007/s10143-024-02639-y
pii: 10.1007/s10143-024-02639-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
395Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Suzuki J, Takaku A (1969) Cerebrovascular “Moyamoya” Disease: Disease Showing Abnormal Net-Like Vessels in Base of Brain. Arch Neurol 20:288–299. https://doi.org/10.1001/archneur.1969.00480090076012
doi: 10.1001/archneur.1969.00480090076012
pubmed: 5775283
Fujimura M, Tominaga T, Kuroda S, Takahashi JC, Endo H, Ogasawara K, Miyamoto S, Research Committee on Moyamoya Disease (Spontaneous Occlusion of Circle of Willis) of the Ministry of Health J Labor Welfare, Society the GC 2021 of the JS (2022) 2021 Japanese Guidelines for the Management of Moyamoya Disease: Guidelines from the Research Committee on Moyamoya Disease and Japan Stroke Society. Neurologia medico-chirurgica advpub:2021–0382. https://doi.org/10.2176/jns-nmc.2021-0382
Kuroda S, Yamamoto S, Funaki T, Fujimura M, Kataoka H, Hishikawa T, Takahashi J, Endo H, Nariai T, Osato T, Saito N, Sato N, Hori E, Ito YM, Miyamoto S, Inaji M, Morita K, Maruyama D, Nakagawara J, Hashimura N, Hamano E, Iihara K, Hashimoto N, Honjo K, Nakamura H, Kashiwazaki D, Imai H, Miyawaki S, Hongo H, Yoshida K, Kikuchi T, Mineharu Y, Isozaki M, Kikuta K, Araki Y, Kanamori F, Date I, Ono J, Machida T, Mase M, Katano H, Yamaguchi K, Kawamata T, Tominaga T, Uchino H, Tokairin K, Ito M, Houkin K, Chida K, Ogasawara K, Nagata I, Horie N, Oka H, Kumabe T, Itoh Y, Abe T, Oki K, Takahashi S, Suzuki N (2023) Five-Year Stroke Risk and Its Predictors in Asymptomatic Moyamoya Disease: Asymptomatic Moyamoya Registry (AMORE). Stroke 54:1494–1504. https://doi.org/10.1161/STROKEAHA.122.041932
doi: 10.1161/STROKEAHA.122.041932
pubmed: 37216455
Tsunoda S, Inoue T, Ohwaki K, Takeuchi N, Shinkai T, Fukuda A, Segawa M, Kawashima M, Akabane A, Miyawaki S, Saito N (2023) Association Between Frontal Lobe Hemodynamics and Neurocognitive Dysfunction in Adults With Moyamoya Disease: Retrospective Cohort Analysis. Neurosurgery 92:547. https://doi.org/10.1227/neu.0000000000002246
doi: 10.1227/neu.0000000000002246
pubmed: 36700728
Kuroda S, Fujimura M, Takahashi J, Kataoka H, Ogasawara K, Iwama T, Tominaga T, Miyamoto S, The Research Committee on Moyamoya Disease (Spontaneous Occlusion of Circle of Willis) of the Ministry of Health Labor, Welfare J 2022 Diagnostic Criteria for Moyamoya Disease - 2021 Revised Version Neurol Med Chir 62 307 312 https://doi.org/10.2176/jns-nmc.2022-0072
Brain Function Test Committee Trail Making Test Japanese version (TMT-J) . Shinko-igaku. http://shinkoh-igaku.jp/cgi-bin/order_inspection/tmt-j/ordermail.cgi . Accessed 21 Dec 2021
Ito E, Hatta T, Ito Y, Kogure T, Watanabe H (2004) Performance of verbal fluency tasks in Japanese healthy adults: Effect of gender, age and education on the performance. Japanese journal of neuropsychology 20:254–263
Kahima H (1995) Chuui shougai to zentouyou sonshou (in Japanese). Japanese Journal of Rehabilitation Medicine 32:294–297. https://doi.org/10.2490/jjrm1963.32.294
doi: 10.2490/jjrm1963.32.294
Kazuhiro Fujita, Maekawa H, Dairoku H, Yamanaka K Wechsler Adult Intelligence Scale-Third Edition, Nihon Bunka Kagakusya. https://www.nichibun.co.jp/kensa/detail/wais3.html . Accessed 23 Dec 2021
Terada T, Obi T, Sugiura A (2009) Effect of aging on the Frontal Assessment Battery (FAB). Jpn J Neuropsychol 25:51–56
Naito K, Motomuro N. Gengosei oyobi higengosei no kadai wo motiita ryuuchousei no ktnou (in Japanses). Journal of Kyushu University of Health and Welfare 12:133–140. https://doi.org/10.15069/00000775
Kim JE, Oh CW, Kwon O-K, 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. CED 25:580–586. https://doi.org/10.1159/000132205
doi: 10.1159/000132205
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: Clinical article. J Neurosurg 111:1158–1164. https://doi.org/10.3171/2009.4.JNS08585
doi: 10.3171/2009.4.JNS08585
pubmed: 19425891
Tsunoda S, Inoue T, Segawa M, Kawashima M, Akabane A, Saito N (2022) Superficial temporal artery lengthening technique to prevent postoperative wound complications in direct revascularization to the anterior cerebral artery for Moyamoya disease. Acta Neurochir 164:1845–1854. https://doi.org/10.1007/s00701-022-05180-3
doi: 10.1007/s00701-022-05180-3
pubmed: 35304649
Jeon JP, Kim JE, Cho W-S, Bang JS, Son Y-J, Oh CW (2017) Meta-analysis of the surgical outcomes of symptomatic moyamoya disease in adults. J Neurosurg 128:793–799. https://doi.org/10.3171/2016.11.JNS161688
doi: 10.3171/2016.11.JNS161688
pubmed: 28474994
Kim T, Oh CW, Kwon O-K, Hwang G, Kim JE, Kang H-S, Cho W-S, Bang JS (2016) Stroke prevention by direct revascularization for patients with adult-onset moyamoya disease presenting with ischemia. J Neurosurg 124:1788–1793. https://doi.org/10.3171/2015.6.JNS151105
doi: 10.3171/2015.6.JNS151105
pubmed: 26636391
Kuroda S (2021) Moyamoya Disease: Current Knowledge and Future Perspectives. Springer Nature
doi: 10.1007/978-981-33-6404-2
Araki Y, Takagi Y, Ueda K, Ubukata S, Ishida J, Funaki T, Kikuchi T, Takahashi JC, Murai T, Miyamoto S (2014) Cognitive Function of Patients with Adult Moyamoya Disease. J Stroke Cerebrovasc Dis 23:1789–1794. https://doi.org/10.1016/j.jstrokecerebrovasdis.2014.04.032
doi: 10.1016/j.jstrokecerebrovasdis.2014.04.032
pubmed: 24957308
Calviere L, Catalaa I, Marlats F, Januel A-C, Lagarrigue J, Larrue V (2011) Improvement in cognitive function and cerebral perfusion after bur hole surgery in an adult with moyamoya disease: Case report. J Neurosurg 115:347–349. https://doi.org/10.3171/2011.3.JNS101117
doi: 10.3171/2011.3.JNS101117
pubmed: 21529135
Calviere L, Catalaa I, Marlats F, Viguier A, Bonneville F, Cognard C, Larrue V (2010) Correlation between cognitive impairment and cerebral hemodynamic disturbances on perfusion magnetic resonance imaging in European adults with moyamoya disease: Clinical article. J Neurosurg 113:753–759. https://doi.org/10.3171/2010.4.JNS091808
doi: 10.3171/2010.4.JNS091808
pubmed: 20469988
Karzmark P, Zeifert PD, Bell-Stephens TE, Steinberg GK, Dorfman LJ (2012) Neurocognitive Impairment in Adults With Moyamoya Disease Without Stroke. Neurosurgery 70:634–638. https://doi.org/10.1227/NEU.0b013e3182320d1a
doi: 10.1227/NEU.0b013e3182320d1a
pubmed: 21849919
Karzmark P, Zeifert PD, Tan S, Dorfman LJ, Bell-Stephens TE, Steinberg GK (2008) EFFECT OF MOYAMOYA DISEASE ON NEUROPSYCHOLOGICAL FUNCTIONING IN ADULTS. Neurosurgery 62:1048–1052. https://doi.org/10.1227/01.NEU.0000312712.55567.E6
doi: 10.1227/01.NEU.0000312712.55567.E6
pubmed: 18580802
Nakamizo A, Amano T, Michiwaki Y, Kawano Y, Kuwashiro T, Yasaka M, Okada Y (2018) Long-Term Neurocognitive Outcomes in Patients with Adult Moyamoya Disease. World Neurosurgery 119:e441–e448. https://doi.org/10.1016/j.wneu.2018.07.179
doi: 10.1016/j.wneu.2018.07.179
pubmed: 30071332
Takagi Y, Miyamoto S, Group C-JS (2015) Cognitive Dysfunction Survey of the Japanese Patients with Moyamoya Disease (COSMO-JAPAN Study): Study Protocol. Neurologia medico-chirurgica advpub. https://doi.org/10.2176/nmc.ra.2014-0326
doi: 10.2176/nmc.ra.2014-0326
Zeifert PD, Peter K, Bell-Stephens TE, Steinberg GK, Dorfman LJ (2017) Neurocognitive Performance After Cerebral Revascularization in Adult Moyamoya Disease. Stroke 48:1514–1517. https://doi.org/10.1161/STROKEAHA.116.016028
doi: 10.1161/STROKEAHA.116.016028
pubmed: 28487332
Uchida S, Kubo Y, Oomori D, Yabuki M, Kitakami K, Fujiwara S, Yoshida K, Kobayashi M, Terasaki K, Ogasawara K (2021) Long-Term Cognitive Changes after Revascularization Surgery in Adult Patients with Ischemic Moyamoya Disease. CEE 11:145–154. https://doi.org/10.1159/000521028
doi: 10.1159/000521028
Lei Y, Li Y-J, Guo Q-H, Liu X-D, Liu Z, Ni W, Su J-B, Yang H, Jiang H-Q, Xu B, Gu Y-X, Mao Y (2017) Postoperative executive function in adult moyamoya disease: a preliminary study of its functional anatomy and behavioral correlates. J Neurosurg 126:527–536. https://doi.org/10.3171/2015.12.JNS151499
doi: 10.3171/2015.12.JNS151499
pubmed: 27058195
Kuwabara Y, Ichiya Y, Sasaki M, Yoshida T, Masuda K, Ikezaki K, Matsushima T, Fukui M (1997) Cerebral hemodynamics and metabolism in Moyamoya disease—a positron emission tomography study. Clin Neurol Neurosurg 99:S74–S78. https://doi.org/10.1016/S0303-8467(97)00061-9
doi: 10.1016/S0303-8467(97)00061-9
pubmed: 9409411
Karasawa J, Kikuchi H, Furuse S, Kawamura J, Sakaki T (1978) Treatment of moyamoya disease with STA-MCA anastomosis. J Neurosurg 49:679–688. https://doi.org/10.3171/jns.1978.49.5.0679
doi: 10.3171/jns.1978.49.5.0679
pubmed: 712390
Iwama T, Hashimoto N, Miyake H, Yonekawa Y (1998) Direct Revascularization to the Anterior Cerebral Artery Territory in Patients with Moyamoya Disease: Report of Five Cases. Neurosurgery 42:1157–1161. https://doi.org/10.1097/00006123-199805000-00124
doi: 10.1097/00006123-199805000-00124
pubmed: 9588563
Hori S, Acker G, Vajkoczy P (2016) Radial Artery Grafts as Rescue Strategy for Patients with Moyamoya Disease for Whom Conventional Revascularization Failed. World Neurosurgery 85:77–84. https://doi.org/10.1016/j.wneu.2015.08.037
doi: 10.1016/j.wneu.2015.08.037
pubmed: 26341437
Teo M, Johnson J, Steinberg GK (2017) Strategies for and Outcome of Repeat Revascularization Surgery for Moyamoya Disease: An American Institutional Series. Neurosurgery 81:852–859. https://doi.org/10.1093/neuros/nyx122
doi: 10.1093/neuros/nyx122
pubmed: 28605467
Kuroda S, Houkin K, Nunomura M, Abe H (2000) Frontal Lobe Infarction Due to Hemodynamic Change after Surgical Revascularization in Moyamoya Disease. Neurol Med Chir 40:315–320. https://doi.org/10.2176/nmc.40.315
doi: 10.2176/nmc.40.315
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 73:430–439. https://doi.org/10.1227/NEU.0000000000000017
doi: 10.1227/NEU.0000000000000017
pubmed: 23756739
Deng X, Gao F, Zhang D, Zhang Y, Wang R, Wang S, Cao Y, Zhao Y, Pan Y, Liu X, Zhang Q, Zhao J (2017) Direct versus indirect bypasses for adult ischemic-type moyamoya disease: a propensity score–matched analysis. J Neurosurg 128:1785–1791. https://doi.org/10.3171/2017.2.JNS162405
doi: 10.3171/2017.2.JNS162405
pubmed: 28799875
Deng X, Gao F, Zhang D, Zhang Y, Wang R, Wang S, Cao Y, Zhao Y, Pan Y, Ye X, Liu X, Zhang Q, Wang J, Yang Z, Zhao M, Zhao J (2017) Effects of different surgical modalities on the clinical outcome of patients with moyamoya disease: a prospective cohort study. J Neurosurg 128:1327–1337. https://doi.org/10.3171/2016.12.JNS162626
doi: 10.3171/2016.12.JNS162626
pubmed: 28686113
Kim H, Jang D-K, Han Y-M, Sung JH, Park IS, Lee K-S, Yang J-H, Huh PW, Park YS, Kim D-S, Han K-D (2016) Direct Bypass Versus Indirect Bypass in Adult Moyamoya Angiopathy with Symptoms or Hemodynamic Instability: A Meta-analysis of Comparative Studies. World Neurosurgery 94:273–284. https://doi.org/10.1016/j.wneu.2016.07.009
doi: 10.1016/j.wneu.2016.07.009
pubmed: 27423200
Mizoi K, Kayama T, Yoshimoto T, Nagamine Y (1996) Indirect revascularization for moyamoya disease: is there a beneficial effect for adult patients. Surg Neurol 45(541–8):discussion 548-9. https://doi.org/10.1016/0090-3019(95)00475-0
doi: 10.1016/0090-3019(95)00475-0
Uchino H, Ito M, Kazumata K, Hama Y, Hamauchi S, Terasaka S, Sasaki H, Houkin K (2018) Circulating miRNome profiling in Moyamoya disease-discordant monozygotic twins and endothelial microRNA expression analysis using iPS cell line. BMC Med Genomics 11:72. https://doi.org/10.1186/s12920-018-0385-3
doi: 10.1186/s12920-018-0385-3
pubmed: 30157848
pmcid: 6114494
Acker G, Fekonja L, Vajkoczy P (2018) Surgical Management of Moyamoya Disease. Stroke 49:476–482. https://doi.org/10.1161/STROKEAHA.117.018563
doi: 10.1161/STROKEAHA.117.018563
pubmed: 29343587
Tashiro R, Fujimura M, Katsuki M, Nishizawa T, Tomata Y, Niizuma K, Tominaga T (2020) Prolonged/delayed cerebral hyperperfusion in adult patients with moyamoya disease with RNF213 gene polymorphism c.14576G>A (rs112735431) after superficial temporal artery–middle cerebral artery anastomosis. J Neurosurg 135:417–424. https://doi.org/10.3171/2020.6.JNS201037
doi: 10.3171/2020.6.JNS201037
pubmed: 33096527
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. https://doi.org/10.1038/jcbfm.2012.110
doi: 10.1038/jcbfm.2012.110
pubmed: 22850406
pmcid: 3493997