Abstract
Brain arteriovenous malformations (AVMs) near/within eloquent areas are challenging to treat surgically. The insufficient lesion-to-eloquence distance (LED) is related to poor neurological outcomes. This paper reports the use of in situ embolization combined with surgical resection in a one-staged hybrid operation for eloquent area protection. Nine patients who underwent one-staged in situ embolization combined with surgical resection were selected from the database of a prospective clinical trial (NCT03774017). Nidus got partial in situ embolization in the parts located near/within the eloquence. The rest of nidus was removed via a microsurgical procedure in the same operation. The in situ embolization ensured a sufficient LED to prevent eloquent areas and tracts from being damaged in the subsequent resection. All of the patients achieved complete obliteration with no neurological deficits or complications. One-staged hybrid operation initiates closer cooperation between surgical and endovascular treatments and proposes an integrative therapeutic mode for AVMs. The in situ embolization combined with surgical resection is safe and effective for improving the functional outcome of AVMs with eloquence and tracts involved. The clinical trial is registered at ClinicalTrials.gov (NCT03774017, https://clinicaltrials.gov/ct2/show/NCT03774017).
References
Aboukais R, Vinchon M, Quidet M, Bourgeois P, Leclerc X, Lejeune JP (2017) Reappearance of arteriovenous malformations after complete resection of ruptured arteriovenous malformations: true recurrence or false-negative early postoperative imaging result? J Neurosurg 126:1088–1093. https://doi.org/10.3171/2016.3.JNS152846
Chiluwal A, Dehdashti AR (2017) Surgical treatment of a complex grade III Spetzler-Martin posterior temporal arteriovenous malformation. Neurosurg Focus 43:V9. https://doi.org/10.3171/2017.7.FocusVid.1786
Del Maestro M, Luzzi S, Gallieni M, Trovarelli D, Giordano AV, Gallucci M, Ricci A, Galzio R (2018) Surgical treatment of arteriovenous malformations: role of preoperative staged embolization. Acta Neurochir Suppl 129:109–113. https://doi.org/10.1007/978-3-319-73739-3_16
Fandino J, Taussky P, Marbacher S, Muroi C, Diepers M, Fathi AR, Remonda L (2013) The concept of a hybrid operating room: applications in cerebrovascular surgery. Acta Neurochir Suppl 115:113–117. https://doi.org/10.1007/978-3-7091-1192-5_24
Gruter BE, Mendelowitsch I, Diepers M, Remonda L, Fandino J, Marbacher S (2018) Combined endovascular and microsurgical treatment of arteriovenous malformations in the hybrid operating room. World Neurosurg 117:e204–e214. https://doi.org/10.1016/j.wneu.2018.05.241
Han SJ, Englot DJ, Kim H, Lawton MT (2015) Brainstem arteriovenous malformations: anatomical subtypes, assessment of “occlusion in situ” technique, and microsurgical results. J Neurosurg 122:107–117. https://doi.org/10.3171/2014.8.JNS1483
Hartmann A, Mast H, Mohr JP, Pile-Spellman J, Connolly ES, Sciacca RR, Khaw A, Stapf C (2005) Determinants of staged endovascular and surgical treatment outcome of brain arteriovenous malformations. Stroke 36:2431–2435. https://doi.org/10.1161/01.STR.0000185723.98111.75
Jiao Y, Lin F, Wu J, Li H, Wang L, Jin Z, Wang S, Cao Y (2018) A supplementary grading scale combining lesion-to-eloquence distance for predicting surgical outcomes of patients with brain arteriovenous malformations. J Neurosurg 128:530–540. https://doi.org/10.3171/2016.10.JNS161415
Kotowski M, Sarrafzadeh A, Schatlo B, Boex C, Narata AP, Pereira VM, Bijlenga P, Schaller K (2013) Intraoperative angiography reloaded: a new hybrid operating theater for combined endovascular and surgical treatment of cerebral arteriovenous malformations: a pilot study on 25 patients. Acta Neurochir 155:2071–2078. https://doi.org/10.1007/s00701-013-1873-z
Li K, Guo Y, Qu L, Xu B, Xu K, Yu J (2018) Hybrid surgery for an arteriovenous malformation fed by an accessory middle cerebral artery and drained by a developmental venous anomaly: a case report and literature review. Exp Ther Med 16:1994–2000. https://doi.org/10.3892/etm.2018.6372
Lin F, Zhao B, Wu J, Wang L, Jin Z, Cao Y, Wang S (2016) Risk factors for worsened muscle strength after the surgical treatment of arteriovenous malformations of the eloquent motor area. J Neurosurg 125:289–298. https://doi.org/10.3171/2015.6.JNS15969
Lin F, Jiao Y, Wu J, Zhao B, Tong X, Jin Z, Cao Y, Wang S (2017) Effect of functional MRI-guided navigation on surgical outcomes: a prospective controlled trial in patients with arteriovenous malformations. J Neurosurg 126:1863–1872. https://doi.org/10.3171/2016.4.JNS1616
Link TW, Winston G, Schwarz JT, Lin N, Patsalides A, Gobin P, Pannullo S, Stieg PE, Knopman J (2018) Treatment of unruptured brain arteriovenous malformations: a single-center experience of 86 patients and a critique of the a randomized trial of unruptured brain arteriovenous malformations (ARUBA) trial. World Neurosurg 120:e1156–e1162. https://doi.org/10.1016/j.wneu.2018.09.025
Morgan MK, Heller GZ (2018) The role of embolization before surgery for Spetzler-Ponce class B and C brain AVMs: a prospective cohort series. J Neurosurg Sci 62:429–436. https://doi.org/10.23736/S0390-5616.18.04371-0
Murayama Y, Arakawa H, Ishibashi T, Kawamura D, Ebara M, Irie K, Takao H, Ikeuchi S, Ogawa T, Kato M, Kajiwara I, Nishimura S, Abe T (2013) Combined surgical and endovascular treatment of complex cerebrovascular diseases in the hybrid operating room. J Neurointerv Surg 5:489–493. https://doi.org/10.1136/neurintsurg-2012-010382
Pasqualin A, Scienza R, Cioffi F, Barone G, Benati A, Beltramello A, Da Pian R (1991) Treatment of cerebral arteriovenous malformations with a combination of preoperative embolization and surgery. Neurosurgery 29:358–368
Pietila TA, Stendel R, Jansons J, Schilling A, Koch HC, Brock M (1998) The value of intraoperative angiography for surgical treatment of cerebral arteriovenous malformations in eloquent brain areas. Acta Neurochir 140:1161–1165
Rubio RR, Vigo V, Bonaventura RD, Abla AA (2018) Right retrosigmoid approach for in situ occlusion of brainstem arteriovenous malformation surrounding the trigeminal nerve: 3-dimensional operative video. Oper Neurosurg (Hagerstown) 16:E42. https://doi.org/10.1093/ons/opy171
Sano H, Kato Y, Iritani K, Akashi K, Kanno T (1998) Minimally invasive surgery for cerebral AVM in the eloquent cortex. J Clin Neurosci 5(Suppl):98–105
Sun L, Zhang H, Ren J (2017) Microsurgical resection of a high-grade occipital arteriovenous malformation after staged embolization. Neurosurg Focus 43:V11. https://doi.org/10.3171/2017.7.FocusVid.1769
Tian J, Lin Z, Zhang J, Yang Q, Huang J, Zhang H, Li M, Huang J, Zong X (2014) Combined surgical and endovascular treatments of complex cerebral arteriovenous malformation in hybrid operating room. Zhonghua Yi Xue Za Zhi 94:3763–3766
Wang MZ, Qiu HC, Wang S, Cao Y, Zhao M, Zhao JZ (2018) A new technique for transvenous embolization of brain arteriovenous malformations in hybrid operation. Chin Med J 131:2993–2996. https://doi.org/10.4103/0366-6999.247199
Wang M, Jiao Y, Cao Y, Wang S, Zhao J (2019) Surgical management of complex brain arteriovenous malformations with hybrid operating technique: study protocol of a prospective registry and a pragmatic clinical trial. BMC Neurol 19:75. https://doi.org/10.1186/s12883-019-1289-3
Wong J, Slomovic A, Ibrahim G, Radovanovic I, Tymianski M (2017) Microsurgery for ARUBA trial (a randomized trial of unruptured brain arteriovenous malformation)-eligible unruptured brain arteriovenous malformations. Stroke 48:136–144. https://doi.org/10.1161/STROKEAHA.116.014660
Yonekawa Y, Imhof HG, Bjeljac M, Curcic M, Khan N (2005) Three cases of AVM at eloquent areas finally treated with conventional microsurgical method. Acta Neurochir Suppl 94:105–110
Acknowledgments
H. Li and M. Zhao provided critical advice on our work. This report relied on the careful perioperative management of neurosurgeons and nurses at our institute.
Funding
This study was supported by Beijing Science and Planning Project (No. D161100003816005) and Key Technologies Research and Development Program (No. 2016YFC1301800).
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Conception and design: Zhao, S. Wang, and Y. Cao. Analysis and interpretation of the data: M. Wang. Drafted the article: M. Wang. Critically revised the article: Qiu and Y. Cao. Reviewed the submitted version of the manuscript: H. Qiu, Y. Cao, S. Wang, and J. Zhao. Approved the final version of the manuscript on behalf of all of the authors: M. Wang, H. Qiu, Y. Cao, S. Wang, and J. Zhao.
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The study was approved by the Institutional Review Board of Beijing Tiantan Hospital (approval number KY2016-034-02).
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Wang, M., Qiu, H., Cao, Y. et al. One-staged in situ embolization combined with surgical resection for eloquence protection of AVM: technical note. Neurosurg Rev 42, 783–790 (2019). https://doi.org/10.1007/s10143-019-01137-w
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DOI: https://doi.org/10.1007/s10143-019-01137-w