Recent Progress in the Management of Cerebrovascular Diseases: Treatment strategies, techniques and complication avoidance 981163386X, 9789811633867

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Recent Progress in the Management of Cerebrovascular Diseases Treatment Strategies, Techniques and Complication Avoidance Yoko Kato Xiaohua Zhang Jiong Dai Ahmed Ansari Editors

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Recent Progress in the Management of Cerebrovascular Diseases

Yoko Kato  •  Xiaohua Zhang Jiong Dai  •  Ahmed Ansari Editors

Recent Progress in the Management of Cerebrovascular Diseases Treatment Strategies, Techniques and Complication Avoidance

Editors Yoko Kato Department of Neurosurgery Fujita Health University Bantane Hospital Nagoya Japan

Xiaohua Zhang Department of Neurosurgery Renji Hospital, Shanghai Jiaotong University School of Medicine Shanghai China

Jiong Dai Department of Neurosurgery Renji Hospital, Shanghai Jiaotong University School of Medicine Shanghai China

Ahmed Ansari Department of Neurosurgery UP University of Medical Sciences Saifai UP India Department of Neurosurgery Fujita Health University Bantane Hospital Nagoya Japan

ISBN 978-981-16-3386-7    ISBN 978-981-16-3387-4 (eBook) https://doi.org/10.1007/978-981-16-3387-4 Jointly published with Shanghai Jiao Tong University Press The print edition is not for sale in China (Mainland). Customers from China (Mainland) please order the print book from: Shanghai Jiao Tong University Press. © Shanghai Jiao Tong University Press 2021 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publishers, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publishers nor the authors or the editors give a warranty, express or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publishers remain neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore

Preface

The successful practice of neurosurgery embraces the concept of lifelong learning. Indeed, every field of neurosurgical specializations now boasts of comprehensive textbooks that run in thousands of pages. To the newly arrived practicing neurosurgeon, the scope of knowledge can seem overwhelming. This book is designed to assist surgeons endeavoring to learn the core concepts and common problems of cerebrovascular surgery. It invites readers to take part in a journey in the vast field of cerebrovascular surgery. We have included a vast array of topics from basics to surgical aspects in this huge field. The treatment strategies, management, and complication avoidance have been covered extensively in the chapters to guide the readers on when and what to expect the worst in surgeries. The concluding chapters embark on the neurosurgical aspect in the present scenario of COVID. The first edition has 19 chapters including basic anatomy and endovascular aspects of management of cerebrovascular diseases. We sincerely believe it will be a worthwhile addition in this ever growing field of cerebrovascular surgery. Nagoya, Japan Shanghai, China  Shanghai, China  Nagoya, Japan 

Yoko Kato Xiaohua Zhang Jiong Dai Ahmed Ansari

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Contents

1 Aneurysm Wall Property����������������������������������������������������������������   1 Paresh Korde 2 Pathogenesis of Thrombosed Giant Aneurysm ����������������������������   9 Gowtham Devareddy 3 Cerebral Vasospasm and Subarachnoid Hemorrhage ����������������  15 Qing Sun and Gang Chen 4 White Fibers of the Brain: A Novel Classification������������������������  21 Abhidha Shah, Sukhdeep Singh Jhawar, and Atul Goel 5 Computational Fluid Dynamics in Cerebral Aneurysms ������������  37 Ahmed Ansari, Ishu Bishnoi, and Gowtham Devareddy 6 Carotid Endarterectomy: Surgical Nuances ��������������������������������  45 Raja K. Kutty, Saurabh Sharma, and Jijo J. Joseph 7 Blister Aneurysm of Middle Cerebral Artery Bifurcation (Case Report and Review)��������������������������������������������������������������  53 Yan Zhao and Zhilin Guo 8 Flexible Endoscopic Aspiration of Intraventricular Hemorrhage��������������������������������������������������������������������������������������  59 Alberto Feletti and Riccardo Stanzani 9 Endoscopic Evacuation of Cerebral Haematoma ������������������������  63 Daisuke Suyama and Brajesh Kumar 10 Management (Surgical and Endovascular) of Acute Ischemic Stroke ����������������������������������������������������������������  81 Tianwei Wang, Hui Wu, Fulin Xu, Jun Li, Ximin Zhao, and Jiong Dai 11 Contralateral Aneurysm Clipping��������������������������������������������������  89 Ishu Bishnoi 12 Multimodality Management of Brain AVMs ��������������������������������  93 Abhidha Shah and Atul Goel

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13 Superficial Temporal Artery-­Middle Cerebral Artery Bypass Combined with Encephalo-Duro-­Myo-Synangiosis in Treating Moyamoya Disease ������������������������������������������������������ 103 Bin Xu, Yujun Liao, Hong Xu, and Chuanghong Liu 14 Stereotactic Radiosurgery for Brain AVM������������������������������������ 109 Enmin Wang 15 Endovascular Recanalization for Chronic Occlusion of Carotid Artery������������������������������������������������������������������������������ 127 Binghong Chen, Renhao Yang, Chaobo Liu, Li Ren, Zhiqiang Li, and Jiong Dai 16 Multimodality Technique of Microvascular Decompression Syndrome �������������������������������������������������������������� 137 Ishu Bishnoi and Sai Kalyan 17 Posterior Circulation Aneurysms Management���������������������������� 143 Tao Lv, Bin Zhao, Duo Chen, Yongming Qiu, and Xiaohua Zhang 18 Onyx Embolization of Intracranial Dural Arteriovenous Fistula (Trans-­Arterial Approach, Transvenous Approach, and Combined Approach) �������������������������������������������������������������� 151 Bin Xu, Yujun Liao, Chuanghong Liu, and Hong Xu 19 Experience in Neurosurgery During the Prevalence of COVID-19������������������������������������������������������������������������������������ 155 Jun Li, Ailong Lin, Yinchun Chen, Huanhuan Li, Bizhou Bie, Liuqing Sheng, and Xiaolong Yao

Contents

Contributors

Ahmed  Ansari Department of Neurosurgery, UP University of Medical Sciences, Saifai, UP, India Department of Neurosurgery, Fujita Health University Bantane Hospital, Nagoya, Japan Bizhou  Bie  Department of Neurosurgery, The Third People’s Hospital of Hubei Province, Wuhan, Hubei, China Ishu Bishnoi  Maharaja Agrasen Medical College, Agroha, Haryana, India Binghong  Chen Department of Neurosurgery, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China Duo Chen  Department of Neurosurgery, The Affiliated Shengjing Hospital of China Medical University, Shenyang, Liaoning, China Yinchun Chen  Department of Neurosurgery, The Third People’s Hospital of Hubei Province, Wuhan, Hubei, China Gang  Chen  Department of Neurosurgery, The First Affiliated Hospital of Soochow University, Suzhou, China Jiong Dai  Department of Neurosurgery, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China Gowtham Devareddy  Dr Rela Institute and Medical Centre, Chennai, Tamil Nadu, India Alberto Feletti  Department of Neurosciences, Biomedicine and Movement Sciences, Institute of Neurosurgery, University of Verona—AOUI Verona, Verona, Italy Atul  Goel Department of Neurosurgery, Seth G.S.  Medical College and K.E.M Hospital, Mumbai, India Zhilin  Guo Neurosurgical Department of the Ninth People’s Hospital of Shanghai, Shanghai Jiaotong University, Shanghai, China Sukhdeep Singh Jhawar  Department of Neurosurgery, Seth G.S. Medical College and K.E.M Hospital, Mumbai, India Jijo J. Joseph  Department of Neurosurgery, Government Medical College, Thiruvananthapuram, Kerala, India ix

x

Sai Kalyan  Department of Neurosurgery, KIMS Hospital, Hyderabad, India Paresh Korde  Fujita Health University, Nagoya, Japan Department of Neurosurgery, DMIMS, Wardha, Maharashtra, India Brajesh  Kumar  Department of Neurosurgery, IGIMS, Sheikhpura, Patna, India Raja K. Kutty  Department of Neurosurgery, Government Medical College, Thiruvananthapuram, Kerala, India Jun  Li Department of Neurosurgery, Shanghai No. 5 People’s Hospital, Shanghai, China Jun Li  Department of Neurosurgery, The Third People’s Hospital of Hubei Province, Wuhan, Hubei, China Zhiqiang  Li Department of Neurosurgery, Shanghai Fengxian District Central Hospital, Shanghai, China Huanhuan Li  Department of Neurosurgery, The Third People’s Hospital of Hubei Province, Wuhan, Hubei, China Yujun  Liao Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai, P. R. China Ailong  Lin Department of Neurosurgery, The Third People’s Hospital of Hubei Province, Wuhan, Hubei, China Chuanghong  Liu Department of Neurosurgery, Changshu First People Hospital, Suzhou University, Suzhou, P. R. China Chaobo  Liu Department of Neurosurgery, Pudong Hospital, Shanghai, China Tao  Lv Department of Neurosurgery, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China Yongming  Qiu Department of Neurosurgery, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China Li Ren  Department of Neurosurgery, Pudong Hospital, Shanghai, China Abhidha Shah  Department of Neurosurgery, Seth G.S. Medical College and K.E.M Hospital, Mumbai, India Saurabh Sharma  SGT Medical College, Gurgaon, Haryana, India Liuqing Sheng  Department of Neurosurgery, The Third People’s Hospital of Hubei Province, Wuhan, Hubei, China Riccardo Stanzani  Neurosurgery Unit, Azienda Ospedaliero-Universitaria di Modena, Modena, Italy Qing  Sun Department of Neurosurgery, The First Affiliated Hospital of Soochow University, Suzhou, China

Contributors

Contributors

xi

Daisuke  Suyama  Department of Neurosurgery, Fuchu Keijinkai Hospital, Tokyo, Japan Tianwei  Wang Department of Neurosurgery, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China Enmin  Wang Cyberknife and Gamma Knife Center, Department of Neurosurgery, Huashan Hospital, Fudan University, Neurosurgical Institute of Fudan University, Shanghai, China Shanghai Key Laboratory of Brain Function and Restoration and Neural Regeneration, Shanghai, China Hui  Wu Department of Neurosurgery, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China Fulin Xu  Department of Neurosurgery, Shanghai Minhang District Central Hospital, Shanghai, China Bin Xu  Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai, P. R. China Hong  Xu Department of Neurosurgery, Changshu First People Hospital, Suzhou University, Suzhou, P. R. China Renhao  Yang Department of Neurosurgery, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China Xiaolong Yao  Department of Neurosurgery, The Third People’s Hospital of Hubei Province, Wuhan, Hubei, China Xiaohua  Zhang Department of Neurosurgery, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China Ximin  Zhao Department of Neurosurgery, Shanghai Baoshan District Central Hospital, Shanghai, China Bin Zhao  Department of Neurosurgery, Renji Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, China Yan  Zhao Neurosurgical Department of the Ninth People’s Hospital of Shanghai, Shanghai Jiaotong University, Shanghai, China

1

Aneurysm Wall Property Paresh Korde

1.1

Introduction

Aneurysm is pathological outpouching of the normal vessel wall. Intracranial aneurysm can be saccular or fusiform. Underlying etiology contributing to the formation of intracranial aneurysm also can be varied, namely, spontaneous, infection, trauma, and tumor. Over a period of time, attempts have been made to understand the biomechanics and histology of formation and rupture of aneurysm and to predict as to which aneurysm can rupture so as to prepare for the prevention and screening of aneurysm for its effective management. Saccular aneurysm arise from the imbalance between local hemodynamic stress and vessel wall strength. There are multiple inciting factors like age, gender, family history atherosclerosis, and changes in the matrix of vessel wall depicting heterogeneous pathogenesis, but studies shows that arterial wall proteolysis by MMPs, apoptosis, and chronic inflammation are convincing contributors for the progression of the disease. However, which event is primary and which is secondary in the formation and rupture of aneurysm is still an enigma.

P. Korde (*) Fujita Health University, Nagoya, Japan Department of Neurosurgery, DMIMS, Wardha, Maharashtra, India

1.2

Understanding the Cerebral Aneurysms

The normal intracranial arterial wall is composed of three layers—intima, media, and adventitia. Intima and media are separated by internal elastic lamina. There is no external elastic lamina separating media and adventitia. Most of the connective tissue of the vessel wall is composed of an extracellular matrix which is formed by collagen (type 1 and type 3), elastin, fibronectin, laminin, nidogen, perlecans, and syndecans. Collagen gives tensile strength, elastin gives resilience, fibronectin is involved in intracellular repair mechanism, and laminin functions in adhesion migration and cell signaling of blood vessel [1–3]. In contrast to normal vascular architecture, an aneurysm wall shows less distinct layers and a disorganized wall. Some characteristic and usual changes are the loss or rupture of the internal elastic lamina, intimal thickening and intimal surface irregularity, muscle fiber disarray, and cellular component depletion [4–6]. Phenotypic changes in medial smooth muscle lead to the remodeling of the vessel wall, for example, no expression of desmin and increased expression of SMemb (smooth muscle myosin heavy chain isoform) contrary to normal arteries. Even difference in histological characteristic of ruptured and unruptured aneurysm has also been seen like a denser expression of fibronectin and pronounced endothelial damage and decreased wall density.

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 Y. Kato et al. (eds.), Recent Progress in the Management of Cerebrovascular Diseases, https://doi.org/10.1007/978-981-16-3387-4_1

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Frosen et al. proposed four histological types of aneurysm wall: 1. Organized wall with linearly organized smooth muscle cell—42% rupture rate 2. Thickened wall with disorganized smooth muscle cells—55% rupture rate 3. Hypocellular wall with myointimal ­hyperplasia—64% rupture rate 4. Thin, hyalinized and hypocellular wall— 100% rupture rate [7]. Injury or hemodynamic stress induces endothelial injury which causes smooth muscle of media to switch in phenotype (from contraction oriented phenotype to proinflammatory and matrix remodeling phenotype) [8]. It is still unclear that this change in phenotype is a compensatory mechanism or whether it contributes to the weakening of the vessel wall. But matrix degeneration and decellularization is an obvious cause of aneurysm rupture. Studies suggest that proteolysis, programmed cell death, inflammation, and hemodynamic stress have definite association with aneurysm formation and rupture. (a) Proteolysis: It is the degradation of structural proteins in the vessel wall at the site of aneurysm formation. It is seen that there is increased expression of matrix metalloproteinases (MMP-2 and MMP-9) in the aneurysm wall and more so in ruptured than unruptured aneurysm wall [9]. These MMPs are gelatinase which degrade elastin and denature collage in ECM of the vessel wall, thus contributing to the formation and rupture of aneurysm. Also, cathepsin-D, which is an endopeptidase, is seen in aneurysm wall where collagen layers are degraded. Correspondingly increased level of serum MMP-2 and MMP-9 has been observed [10, 11]. (b) Programmed cell death: Apoptosis. In contrast to the normal arterial wall, many apoptotic cells were found in the aneurysm wall. Hara et  al. in their study found more apoptotic cells near the neck and dome of aneurysm, especially near the rupture point [12]. On the contrary, no such cells were

P. Korde

e­vident in the control group. Though the chronology of the event is unclear, a proposition that cytokines produced as a result of local inflammation mainly. TNF-alpha and its downstream proapoptotic target—Fas—are increased in ruptured aneurysm [13, 14]. Also, various authors have observed that JNK pathway leading to apoptosis was seen as more active in ruptured than unruptured aneurysm [15]. (c) Inflammation: Innate and adaptive immune reactions seem to play a vital role in aneurysm formation and rupture evident by the presence of macrophages, T cells, B cells, Ig antibodies, and activated complements [6,  13, 16–18]. MCP-1, a proinflammatory chemokine, was observed to have increased expression in the aneurysm wall as opposed to their absence in the normal arterial wall. Shimada et  al. in their study on the mouse model came to the conclusion that peroxisome proliferator–activated receptor-gamma (PPAR gamma) is a nuclear hormone receptor whose activation can cause aneurysm to rupture by catalyzing inflammation in the aneurysm wall [19]. Pioglitazone, its antagonist, had shown a protective effect on aneurysm rupture rate in the mouse model. Koseki et al. have also studied the role of transendothelial migration of macrophages and also proposed potential therapeutic targets for the medicinal treatment of aneurysm [20]. (d) Hemodynamic factors: Data suggests that hemodynamic stress is contributory to the formation of aneurysm. Changes imparted in the arterial wall due to local hemodynamic stress  like internal elastic lamina fragmentation, adventitial tissue degeneration, de-­ endothelialization, macrophage infiltration, and apoptosis ultimately lead to the formation of intracranial aneurysm and eventually its rupture. Studies done by Boussel et al., Yamaguchi et al., and Jou et al. proposed that local hemodynamic stress and low wall shear stress are causative factors of aneurysm and that the aneurysms with higher aspect ratio are associated with low wall shear stress [21–23]. Tomohiro Aoki et al. found that turbulent blood flow and low wall shear stress collectively lead

1  Aneurysm Wall Property

to sustained expression of MCP-1 in endothelial cells, which cause increased macrophage infiltration and exacerbation of local inflammation ultimately causing enlargement or rupture of aneurysm [24]. Jing et al. after studying nine morphological factors (size, neck width, surface area, volume, diameter of parent arteries, aspect ratio, size ratio, lateral/bifurcation type, regular/irregular type) and six hemodynamic factors (wall shear stress (WSS) mean and WSS min, oscillatory shear index (OSI), low wall shear area (LSA), flow complexity, and flow stability) came to the conclusion that low WSS mean and large aspect ratio are independent risk factors for aneurysm rupture [25]. (e) Atherosclerosis and aneurysm: There are studies supporting the hypothesis that atherosclerosis and the formation of aneurysm are interrelated. Also, risk factors like smoking and hypertension are common between atherosclerosis and aneurysm. Immune and adaptive immune responses are also fairly common between them. Kosierkiewicz et al. found that aneurysm size and atherosclerotic plaque progression are related [16]. Bolger et  al. discovered that lipoprotein a (Lp [a]), which is an independent risk factor for atherosclerosis, was also found with doubled serum level in aneurysm patient than in normal control [26]. Tateshima et  al. showed a correlation between atherosclerotic area and low wall shear stress [27]. A hospital-based case control study by Nozaki et al. concluded that there is an inverse correlation between

3

consumption of statins and cerebral aneurysm rupture [28]. But studies countering the findings of the above data have also been made available in literature denying the correlation of atherosclerosis and aneurysm [29]. (f) Biomechanical properties: Though conventionally biomechanical properties of the aneurysm wall are not included in rupture risk evaluation of aneurysm, there have been studies supporting its importance. Costalat et al. worked on the excised aneurysm wall obtained from patients who underwent clipping of aneurysm. They preserved these tissue according to their collection protocol where they used ringer lactate and 10% DMSO and kept the samples in the freezer (−80  °C) to preserve their biomechanical properties till they were tested. These samples underwent mechanical uniaxial stress tests. Authors proposed that aneurysm wall can be categorized into three types as soft, rigid, and intermediate tissue walled and the unruptured aneurysms presented with more rigid tissue than ruptured ones [30]. Signorelli et  al. did an indentation test on fresh aneurysm wall sample barring the freezing bias caused due to collection and conserving the sample in freezing condition. They found that rupture occurs in the restricted area of increased elasticity, while the unruptured area of aneurysm has increased stiffness. Also, two-photon microscopy confirmed the disruption of the collagen fiber network in the ruptured zone of aneurysm [31]. y-displacement table

Displacement sensor Spherical indenter

y

Sample carrier

z

Schematic presentation of the indentation test used by Signorelli and coworkers

x

P. Korde

4

With all this knowledge and supporting data in hand, challenge still remains the same. How can one confidently predict the rupture risk or screen and prevent the aneurysm formation and treat them so as to dictate the outcome?

1.3

Radiological Advancement and Clinical Correlation

Currently, radiological investigations have offered some reliability in predicting the rupture risk of intracranial aneurysm. (a) Circumferential aneurysm wall enhancement (CAWE) on MRI: Edjlali et  al. graded the aneurysms in four grades to discriminate between stable and unstable unruptured intracranial aneurysms according to the enhancement patterns [32]. Grade 0: No enhancement Grade 1: Focal thick enhancement Grade 2: Thin circumferential enhancement Grade 3: Thick circumferential enhancement Grade 3 determines the highest specificity for detecting instability of aneurysm and the likelihood of its rupture. On similar lines, Nan et al. [33] studied 333 aneurysms and came to the conclusion that: –– False-positive results were rare. –– Approximately 90% negative predictive value of any type of enhancement, com-

Pressure Inst mmHg

bined with other risk factors of rupture or evolution, may indicate that UIAs without enhancement should be managed conservatively. –– Grey areas of using CAWE: No histological validation for enhancement of aneurysmal wall and CAWE may be the mere consequence of slow flow artifact near the wall. –– The advancement of VW-MRI offers a potential noninvasive means to detect in  vivo inflammation in IAs at a pathological level. –– Confounding issues in AWE are leaked or stagnant contrast agent and alteration of the radiological characteristics after IA rupture. –– With an increasing score, the proportion of aneurysm with AWE increased progressively. –– Approximately 42.7% of the AWE group was irregular in shape compared to the non-AWE group. –– Aneurysm size and location were independently associated with the presence of AWE in patients with UIAs. –– The median aneurysm size in the AWE group was significantly larger than in the non-AWE group. (b) Computational fluid dynamics (CFD): Decreased shear wall stress at high-pressure areas of the aneurysm wall can predict the rupture risk of aneurysm.

WSS Mag Inst Pa

100.140

20.495

99.575

13.665

99.610

6.835

99.345

0.005

1  Aneurysm Wall Property

5

A CFD of unruptured MCA sbifurcation aneurysm patient showing maximum pressure area in red color at the dome of aneurysm with another image depicting lowest wall shear stress at the same site of aneurysm painted in blue color indicating the probable site of anticipated rupture.

1.4

Future of Aneurysm Management

A concept of preemptive medicine in the management of cerebral aneurysm is proposed by Tomohiro Aoki and Kazuhiko Nozaki where

treatment includes both the prevention and cure of aneurysm [34]. Preemptive medicine targets every stage of the formation of aneurysm, right from genetic factors, vascular fragility, formation, progression, and its rupture. On the same lines of preemptive medicine, Shimizu et al. in the quest of therapeutic targets for the aneurysm management enlisted all potential targets through the data in the literature. These biomarkers and their drugs experimented on the rodent model showed varied effects on the formation, enlargement, and rupture of aneurysm. Validity for humans of these drugs is under trial [35].

Potential therapeutic targets for the treatment of intracranial aneurysms on the rat model

Therapeutic targets HMG-CoA reductase NF-kB Cyclooxygenase (COX) COX-2 PGE receptor subtype 2 Sphingosine −1 phosphate receptor type1 TNF alpha MMPs Inducible nitic oxide (iNOS) Endothelin receptors Cathepsins Reactive oxygen species Phosphodiesterase 4 Rho-kinase PPAR- gamma Dipeptidyl peptidase (DPP-4) ACE Angiotensin II receptor type 1 (AT1) AT2 Mineralocorticoid Receptor Estrogen receptor Mast cell Macrophage

Drugs Simvastatin/pitavastatin Nifedipine Aspirin Celecoxib PF-04418948 ASP4058 Etanercept Minocycline/doxycycline Aminoguanidine K-8794 NC-2300 Edaravone Ibudilast Fasudil hydrochloride Pioglitazone Anagliptin Captopril Losartan Angiotensin [1–7] Eplerenone 17 Beta-estradiol diarylpropionitrile Emedastine difumarate/ tranilast Clodronate liposome

Decreases aneurysm formation

+

Decreases aneurysm enlargement + + + + + + +

Decreases aneurysm rupture

+

+ + + + + + + + + + + + +

+ + +

+

P. Korde

6

1.5

Conclusion

Understanding aneurysm developmental pathophysiology can help explore new possibilities of management. Qualitative and noninvasive methods of assessment of the aneurysmal wall like CFD and CAWE are a current trend. But it requires histological validation. Therapeutic targets are still in infancy but can be developed as a great armor against cerebral aneurysm. Preemptive medicine can be established with specific biomarkers and imaging modalities to prevent or delay the onset of symptoms of cerebral aneurysms.

References 1. Hynes RO, Yamada KM.  Fibronectins: multifunctional modular glycoproteins. J Cell Biol. 1982;95(2):369–77. Available from: https://rupress.org/jcb/article/95/2/369/19796/ Fibronectins-­multifunctional-­modular-­glycoproteins 2. Hedin U, Bottger BA, Forsberg E, Johansson S, Thyberg J. Diverse effects of fibronectin and laminin on phenotypic properties of cultured arterial smooth muscle cells. J Cell Biol. 1988;107(1):307–19. Available from: https://rupress.org/jcb/article/107/1/307/13817/ Diverse-­effects-­of-­fibronectin-­and-­laminin-­on 3. Patarroyo M, Tryggvason K, Virtanen I. Laminin isoforms in tumor invasion, angiogenesis and metastasis. Semin Cancer Biol. 2002;12(3):197–207. Available from: https://linkinghub.elsevier.com/retrieve/pii/ S1044579X02000238 4. Drăghia F, Drăghia AC, Onicescu D. Electron microscopic study of the arterial wall in the cerebral aneurysms. Rom J Morphol Embryol. 2008;49(1):101−3. 5. Nakayama Y, Tanaka A, Kumate S, Tomonaga M, Takebayashi S.  Giant fusiform aneurysm of the basilar artery—consideration of its pathogenesis. Surg Neurol. 1999;51(2):140–5. Available from: https://linkinghub.elsevier.com/retrieve/pii/ S0090301998000500 6. Kataoka K, Taneda M, Asai T, Kinoshita A, Ito M, Kuroda R.  Structural fragility and inflammatory response of ruptured cerebral aneurysms: a comparative study between ruptured and unruptured cerebral aneurysms. Stroke. 1999;30(7):1396–401. Available from: https://www.ahajournals.org/doi/10.1161/01. STR.30.7.1396 7. Nakajima N, Nagahiro S, Sano T, Satomi J, Satoh K. Phenotypic modulation of smooth muscle cells in human cerebral aneurysmal walls. Acta Neuropathol. 2000;100(5):475–80. Available from: https://pubmed. ncbi.nlm.nih.gov/11045669/ 8. Starke RM, Chalouhi N, Ding D, Raper DMS, Mckisic MS, Owens GK, et al. Vascular smooth muscle cells

in cerebral aneurysm pathogenesis. Transl Stroke Res. 2014;5(3):338–46. Available from: https://pubmed. ncbi.nlm.nih.gov/24323713/ 9. Bruno G, Todor R, Lewis I, Chyatte D. Vascular extracellular matrix remodeling in cerebral aneurysms. J Neurosurg. 1998;89(3):431–40. Available from: https://pubmed.ncbi.nlm.nih.gov/9724118/ 10. Connolly ES, Fiore AJ, Winfree CJ, Prestigiacomo CJ, Goldman JE, Solomon RA. Elastin degradation in the superficial temporal arteries of patients with intracranial aneurysms reflects changes in plasma elastase. Neurosurgery. 1997;40(5):903–9. Available from: https://pubmed.ncbi.nlm.nih.gov/9149247/ 11. Baker CJ, Fiore A, Connolly ES, Baker KZ, Solomon RA. Serum elastase and alpha-1-antitrypsin levels in patients with ruptured and unruptured cerebral aneurysms. Neurosurgery. 1995;37(1):56–62. Available from: https://pubmed.ncbi.nlm.nih.gov/8587691/ 12. Hara A, Yoshimi N, Mori H.  Evidence for apoptosis in human intracranial aneurysms. Neurol Res. 1998;20(2):127–30. Available from: https://pubmed. ncbi.nlm.nih.gov/9522347/ 13. Frösen J, Piippo A, Paetau A, Kangasniemi M, Niemelä M, Hernesniemi J, et  al. Remodeling of saccular cerebral artery aneurysm wall is associated with rupture: Histological analysis of 24 unruptured and 42 ruptured cases. Stroke. 2004;35(10):2287– 93. Available from: https://www.ahajournals.org/ doi/10.1161/01.STR.0000140636.30204.da 14. Pentimalli L, Modesti A, Vignati A, Marchese E, Albanese A, Di Rocco F, et  al. Role of apoptosis in intracranial aneurysm rupture. J Neurosurg. 2004;101(6):1018–25. Available from: https:// pubmed.ncbi.nlm.nih.gov/15597763/ 15. Takagi Y, Ishikawa M, Nozaki K, Yoshimura S, Hashimoto N.  Increased expression of phosphorylated c-Jun amino-terminal kinase and phosphorylated c-Jun in human cerebral aneurysms: role of the c-Jun amino-terminal kinase/c-Jun pathway in apoptosis of vascular walls. Neurosurgery. 2002;51(4):997– 1004. Available from: https://academic.oup.com/ neurosurgery/article/51/4/997/2732478 16. Kosierkiewicz TA, Factor SM, Dickson DW.  Immunocytochemical studies of atherosclerotic lesions of cerebral berry aneurysms. J Neuropathol Exp Neurol. 1994;53(4):399–406. Available from: https://academic.oup.com/jnen/article-­l ookup/ doi/10.1097/00005072-­199407000-­00012 17. Chyatte D, Bruno G, Desai S, Todor DR. Inflammation and intracranial aneurysms. Neurosurgery. 1999;45(5):1137–47. Available from: https://pubmed. ncbi.nlm.nih.gov/10549930/ 18. Tulamo R, Frösen J, Hernesniemi J, Niemelä M.  Inflammatory changes in the aneurysm wall: a review. Vol. 2, Journal of NeuroInterventional Surgery. J Neurointerv Surg. 2010:120–30. Available from: https://pubmed.ncbi.nlm.nih.gov/21990591/ 19. Shimada K, Furukawa H, Wada K, Korai M, Wei Y, Tada Y, et al. Protective role of peroxisome proliferator–activated receptor-γ in the development of intracra-

1  Aneurysm Wall Property nial aneurysm rupture. Stroke. 2015;46(6):1664–72. Available from: https://www.ahajournals.org/ doi/10.1161/STROKEAHA.114.007722 20. Koseki H, Miyata H, Shimo S, Ohno N, Mifune K, Shimano K, et al. Two diverse hemodynamic forces, a mechanical stretch and a high wall shear stress, determine intracranial aneurysm formation. Transl Stroke Res. 2020;11(1):80–92. Available from: https://link. springer.com/article/10.1007/s12975-­019-­0690-­y 21. Boussel L, Rayz V, McCulloch C, Martin A, Acevedo-­ Bolton G, Lawton M, et al. Aneurysm growth occurs at region of low wall shear stress: Patient-specific correlation of hemodynamics and growth in a longitudinal study. Stroke. 2008;39(11):2997–3002. Available from: https://pubmed.ncbi.nlm.nih.gov/18688012/ 22. Yamaguchi R, Ujiie H, Haida S, Nakazawa N, Hori T.  Velocity profile and wall shear stress of saccular aneurysms at the anterior communicating artery. Heart Vessel. 2008;23(1):60–6. Available from: https://pubmed.ncbi.nlm.nih.gov/18273548/ 23. Der JL, Lee DH, Morsi H, Mawad ME.  Wall shear stress on ruptured and unruptured intracranial aneurysms at the internal carotid artery. Am J Neuroradiol. 2008;29(9):1761–7. Available from: www.ajnr.org 24. Aoki T, Yamamoto K, Fukuda M, Shimogonya Y, Fukuda S, Narumiya S.  Sustained expression of MCP-1 by low wall shear stress loading concomitant with turbulent flow on endothelial cells of intracranial aneurysm. Acta Neuropathol Commun. 2016;4:48. 25. Jing L, Fan J, Wang Y, Li H, Wang S, Yang X, et al. Morphologic and hemodynamic analysis in the patients with multiple intracranial aneurysms: ruptured versus unruptured. PLoS One. 2015;10:e0132494. 26. Bolger C, Phillips J, Gilligan S, Zourob T, Farrell M, Croake D, et al. Elevated levels of lipoprotein (a) in association with cerebrovascular saccular aneurysmal disease. Neurosurgery. 1995;37(2):241–5. Available from: https://pubmed.ncbi.nlm.nih.gov/7477775/ 27. Tateshima S, Tanishita K, Omura H, Sayre J, Villablanca JP, Martin N, et  al. Intra-aneurysmal hemodynamics in a large middle cerebral artery

7 aneurysm with wall atherosclerosis. Surg Neurol. 2008;70(5):454–62. Available from: https://pubmed. ncbi.nlm.nih.gov/18514767/ 28. Yoshimura Y, Murakami Y, Saitoh M, Yokoi T, Aoki T, Miura K, et al. Statin use and risk of cerebral aneurysm rupture: a hospital-based case-control study in Japan. J Stroke Cerebrovasc Dis. 2014;23(2):343–8. 29. Cao Y, Zhao J, Wang S, Zhong H, Wu B. Monocyte chemoattractant protein-1 mRNA in human intracranial aneurysm walls. Zhonghua Yu Fang Yi Xue Za Zhi. 2002;36(7):519−21. 30. Signorelli F, Pailler-Mattei C, Gory B, Larquet P, Robinson P, Vargiolu R, et al. Biomechanical Characterization of Intracranial Aneurysm Wall: A Multiscale Study. World Neurosurg. 2018;119:e882−e889. 31. Signorelli F, Pailler-Mattei C, Gory B, Larquet P, Robinson P, Vargiolu R, et al. Biomechanical characterization of intracranial aneurysm wall: a multiscale study. World Neurosurg. 2018;119:e882–9. 32. Edjlali M, Gentric JC, Régent-Rodriguez C, Trystram D, Hassen WB, Lion S, et  al. Does aneurysmal wall enhancement on vessel wall MRI help to distinguish stable from unstable intracranial aneurysms? Stroke. 2014;45(12):3704–6. Available from: https://www.ahajournals.org/doi/10.1161/ STROKEAHA.114.006626 33. Lv N, Karmonik C, Chen S, Wang X, Fang Y, Huang Q, Liu J. Relationship Between Aneurysm Wall Enhancement in Vessel Wall Magnetic Resonance Imaging and Rupture Risk of Unruptured Intracranial Aneurysms. Neurosurgery. 2019;84(6):E385−E391. 34. Aoki T, Nozaki K.  Preemptive medicine for cerebral aneurysms. Neurol Med Chir (Tokyo). 2016;56(9):552–68. Available from: /pmc/articles/ PMC5027238/?report=abstract. 35. Shimizu K, Kushamae M, Mizutani T, Aoki T.  Intracranial aneurysm as a macrophage-mediated inflammatory disease. Neurol Med Chir (Tokyo). 2019;59(4):126–132. Available from: ­ /pmc/articles/ PMC6465529/?report=abstract.

2

Pathogenesis of Thrombosed Giant Aneurysm Gowtham Devareddy

2.1

Introduction

Large and giant aneurysms account for up to 5% of all intracranial aneurysms approximately. They often present during the fifth to seventh decades and have a female predominance. Unlike small aneurysms which often present with subarachnoid hemorrhage (SAH), giant aneurysms often present with symptoms of mass effect, ischemia [1]. Ischemia is mostly due to the development of thromboembolism. Approximately 17–33% of giant aneurysms were thrombotic. Though many cases follow mild and calm progression for long periods, some have rapid progression to large sizes [1, 2]. The risk of rupture of these giant aneurysms is approximately 50% in 5  years according to the International Study of Unruptured Intracranial Aneurysms (ISUIA) trial. In cerebral aneurysms, thrombosis is the healing mechanism by which the aneurysm gets occluded and the parent artery remodeled. Spontaneous thrombosis is more frequent in giant aneurysms than in small aneurysms [1–3]. The development of thrombus and its progression in the aneurysm has to be well understood for appropriate management of these aneurysms. Development of thrombosis is due to (1) abnormal vessel walls, (2) abnormal blood flow, and (3) abnormal blood constituents. These three form the G. Devareddy (*) Dr Rela Institute and Medical Centre, Chennai, Tamil Nadu, India

most popular Virchow’s triad [4]. How these factors are interdependent will provide a clear view of the pathogenesis of thrombosed giant aneurysms.

2.2

Illustrative Case 1

A 72-year-old lady presented with multiple episodes of TIA and was diagnosed to have a large basilar aneurysm of size 19 mm × 22 mm. Within 2  months, she presented with multiple acute infarcts (Fig. 2.1). She underwent cerebral digital subtraction angiography (3D-DSA) which revealed that there is the development of recirculatory flow (Fig.  2.2) in different directions causing stagnation of blood in between these flows, which is predicted by incomplete washout of contrast medium (Fig. 2.2). This is one of the risk factors for the development of intra-aneurysmal thrombosis.

2.3

Illustrative Case 2

A 50-year-old male presented with c/o headache and dizziness. MRI brain showed a partially thrombosed left vertebral artery aneurysm. He was kept under observation and managed conservatively in view of thrombosis of the aneurysm. He developed progressive diplopia, facial weakness, and dysarthria over the next 2 years. Repeat MRI done after 2  years showed increase in the size of aneurysm with thrombosis. He underwent

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 Y. Kato et al. (eds.), Recent Progress in the Management of Cerebrovascular Diseases, https://doi.org/10.1007/978-981-16-3387-4_2

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G. Devareddy

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Fig. 2.1  Large basilar artery aneurysm with 3D reconstruction

a

c

b

d

e

f

Fig. 2.2  Computational fluid dynamic (CFD) simulations (a, b) and DSA (c–f) of the Basilar artery aneurysm. CFD simulation showing the development of two recircu-

lation flows (white arrowhead). Flow stagnation (white arrow) demonstrated in DSA images

surgical treatment with clipping and excision of the aneurysm sac. Histopathological examination of the wall of aneurysm showed thickening of aneurysm sac wall with areas of hyaline degeneration, thickening of intima with degeneration of inner elastic membrane, and degeneration of smooth muscle (Fig. 2.3). This abnormal aneurysmal sac wall shows a predilection for thrombosis.

2.4

Discussion

Suzuki et al. have done an extensive histopathological study of 10 cases of giant aneurysms with thrombosis and found that there is distinctive thickening of the intimae and thinness of media along with degeneration and fragmentation of inner elastic membrane in the aneurysmal wall.

2  Pathogenesis of Thrombosed Giant Aneurysm

a

d

b

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c

e

f

Fig. 2.3  A case of large left vertebral artery aneurysm. (a) First MRI scan showing large thrombosed aneurysm. (b) MRI done after 2 years showing increase in the size of aneurysm. (c) Intraoperative image showing dilated vasa

vasorum supplying the wall of the aneurysm. (d) H&E staining 100×, (e) H&E staining 400×, (f) Azan staining showing the development of microvessels with inflammatory cells around it

The intimae continued to the thrombi of the aneurysm in almost all cases. In the majority of cases, they found partial hyalinization with associated microbleeds. There is infiltration of the media and intima by inflammatory cells around the microvessels, thus causing vascular degeneration and development of microbleeds [5]. Whittle et al. described 22 cases of giant aneurysms with thrombosis in their series of 302 patients and found that the incidence of thrombus formation within giant aneurysms is majorly to a critical ratio between aneurysm volume and aneurysm neck size [3]. Fogelson et  al. have done a detailed review on the complex interactions between blood components and the vascular wall involved in thrombus formation. They have highlighted several major points like (1) the role of red blood cells (RBCs) in the platelets margination from vessels center to the vessel wall surface; (2) the function of the GPIb-vWF bonds in the platelet adhesion at high shear stress; (3) the effect of the hydrodynamic forces on the extension of vWF and the modulation of its biological activity; (4) the complex network of proteins interactions and

the polymerization of the fibrin monomers; (5) the way blood molecules are transported by the flow; (6) the threshold density of tissue factor (TF) to trigger coagulation; (7) the fact that when the shear stress decreases, the amount of TF needed to generate the same quantity of fibrin decreases; and (8) the role of platelets to limit the clot growth by impeding access to TF and to immobilize coagulation enzymes complexes [6]. The process of initiation of thrombus formation and its growth is the result of appropriate molecules at the right place and right time and transported by fluid flow. In vitro studies were done by Malspinus et al. to study the response of the endothelial cells to low wall shear stress flow conditions and found that its effect on the production of tissue factor (TF) and its antagonist, thrombomodulin, and thus, these areas exhibit procoagulant nature [1, 5, 6]. Development and progression of thrombosis are both intraluminal, i.e., inside the sac of aneurysm and intrinsic to the wall of a giant aneurysm. As the aneurysmal wall loses its own elasticity, it begins to rupture given its inability to tolerate

G. Devareddy

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increased blood pressures. Fibrinogen and antithrombin are naturally present in blood, whereas thrombin and fibrin are created under specific conditions. Thrombin is released by the endothelium of blood vessels under stress or with damage to the endothelium. When thrombin meets fibrinogen, it produces fibrin. When there is altered blood flow with stagnation or recirculation flow in giant aneurysms, these fibrin molecules tend to attach to adjacent fibrin molecules or to the blood vessel wall, and thus, the blood clot can grow from the aneurysmal wall and progress towards the center of the cavity (Figs. 2.4 and 2.5).

After the development of aneurysm, there is a natural mechanism of healing and repair of the wall of the aneurysm of the sac (Fig. 2.4) [7, 8]. Distinctive thickening of the intimae, thinness of the media, degeneration of smooth muscle, and disappearance and fragmentation of the inner elastic membranes were recognized in the aneurysmal walls. Continuous hyperdynamic changes at the areas of impact of blood flow associated with poorly organized cells in the intima lead to the dissection of the intima, thus forming an organized clot. Blood flow between the thrombus and the vessel wall contributes to the progression

Macrophage MICROVESSELS IEL disintegration TNF a, IL-1b APOPTOSIS

Microbleed

VEGF

INTRINSIC THROMBUS

LUMINAL THROMBUS

Fig. 2.4  Representative picture showing the development of intramural thrombus formation and extramural development of thrombus

Fig. 2.5  Representative picture showing progression of thrombosis in the aneurysm

2  Pathogenesis of Thrombosed Giant Aneurysm

of the thrombus (Fig. 2.5). Such repeated events induce the enlargement of the aneurysm. With hypoxia and degeneration of the aneurysmal wall, there is the expression of vascular endothelial growth factor (VEGF) and development of microvascularization and microbleeds leading to progression of the thrombus [7–9]. Inflammation and neovascularization in the thrombus play an important role in the progression of thrombus in giant aneurysms. Histopathological examination of the giant aneurysm wall with thrombosis showed inflam-

13

matory cells (CD68+ cells, neutrophils, and lymphocytes) in the thrombi. These inflammatory cells infiltrated the intimae and media and were distributed primarily around the microvessels [10, 11]. Hyperplastic proliferation due to ­microbleeds and inflammation from microvessels occur in a vicious circle [1, 12, 13]. This inflammation causes degeneration of the neovessels leading to microbleeds inside the thrombus and aneurysm wall (Fig. 2.4) and thus increase in the size of the aneurysm wall to large sizes and intrinsic progression of the thrombus.

Development of velocity gradients

Aneurysm formation

Damaged endothelium

Thmbomodulin, Tissue factor expression

Release of VEGF

Migration of macrophag

TNF, IL Altered blood flow

Apoptosis

Microvessel proliferation

Activation of coagulation cascade Degeneration of media, Internal elastic lamina

Microbleeds

Extramural Thrombus development

Dissection in intima with intramural thrombus

Progression of intramural thrmobus

G. Devareddy

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2.5

Conclusion

Development of thrombosis in aneurysms starts with damage of endothelium and then progresses intrinsically in the wall and also intraluminally in the aneurysmal sac. Increase in the size of thrombosis intrinsically in the wall is mostly attributed to the proliferation of microvessels into the wall and development of microbleeds (flow chart). Intraluminally, the exposed thrombus due to wall degeneration progresses in size along the slow flow direction.

References 1. Malaspinas O, Turjman A. Ribeiro de Sousa D, et al. a spatio-temporal model for spontaneous thrombus formation in cerebral aneurysms. J Theor Biol. 2016;394:68– 76. https://doi.org/10.1016/j.jtbi.2015.12.022. 2. Cohen JE, Yitshayek E, Gomori JM, et al. Spontaneous thrombosis of cerebral aneurysms presenting with ischemic stroke. J Neurol Sci. 2007;254(1–2):95–8. https://doi.org/10.1016/j.jns.2006.12.008. 3. Whittle IR, Dorsch NW, Besser M.  Spontaneous thrombosis in giant intracranial aneurysms. J Neurol Neurosurg Psychiatry. 1982;45(11):1040–7. https:// doi.org/10.1136/jnnp.45.11.1040. 4. Chung I, Lip GYH. Virchow’ s triad revisited: blood constituents; 2004, pp. 449–454. 5. Suzuki H, Mikami T, Tamada T, et al. Inflammation promotes progression of thrombi in intracranial thrombotic aneurysms. Neurosurg Rev. 2019; https:// doi.org/10.1007/s10143-­019-­01184-­3.

6. Fogelson AL, Neeves KB.  Fluid mechanics of blood clot formation. Annu Rev Fluid Mech. 2015;47(1):377–403. https://doi.org/10.1146/ annurev-­fluid-­010814-­014513. 7. Hashimoto T, Meng H, Young WL. Intracranial aneurysms: links among inflammation, hemodynamics and vascular remodeling. Neurol Res. 2006;28(4):372–80. https://doi.org/10.1179/016164106X14973. 8. Mizutani T, Goldberg HI, Parr J, Harper C, Thompson CJ.  Cerebral dissecting aneurysm and intimal fibroelastic thickening of cerebral arteries. Case report. J Neurosurg. 1982;56(4):571–6. https://doi. org/10.3171/jns.1982.56.4.0571. 9. Kataoka K, Taneda M, Asai T, Kinoshita A, Ito M, Kuroda R.  Structural fragility and inflammatory response of ruptured cerebral aneurysms: a comparative study between ruptured and unruptured cerebral aneurysms. Stroke. 1999; https://doi.org/10.1161/01. STR.30.7.1396. 10. Tulamo R, Frösen J, Hernesniemi J, Niemelä M.  Inflammatory changes in the aneurysm wall: a review. J Neurointerv Surg. 2010;2(2):120–30. https://doi.org/10.1136/jnis.2009.002055. 11. Signorelli F, Sela S, Gesualdo L, et al. Hemodynamic stress, inflammation, and intracranial aneurysm development and rupture: a systematic review. World Neurosurg. 2018;115 https://doi.org/10.1016/j. wneu.2018.04.143. 12. Krings T, Piske RL, Lasjaunias PL. Intracranial arterial aneurysm vasculopathies: targeting the outer vessel wall. Neuroradiology. 2005;47(12):931–7. https:// doi.org/10.1007/s00234-­005-­1438-­9. 13. Krings T, Lasjaunias PL, Geibprasert S, Pereira V, Hans FJ. The aneurysmal wall. The key to a subclassification of intracranial arterial aneurysm vasculopathies? Interv Neuroradiol. 2008;14(SUPPL. 1):39–47. https://doi.org/10.1177/15910199080140S107.

3

Cerebral Vasospasm and Subarachnoid Hemorrhage Qing Sun and Gang Chen

3.1

Introduction

Cerebral vasospasm (CVS) is the leading cause of acute focal cerebral ischemia after subarachnoid hemorrhage (SAH). CVS occurs in about one-third of SAH patients. CVS usually starts 3–4  days after aneurysm rupture, peaks at 7–10  days, and recovers by 14–21  days [1]. About one-third of these patients die from CVS, and another one-third are left disabled [2]. The diagnosis of CVS is a clinical diagnosis and is defined as the development of new focal neurological deficits in SAH patients that are not caused by a seizure, hematoma, brain edema, hydrocephalus, and other structural or metabolic causes [2]. It’s widely agreed that severe SAH evident on computed tomography (CT) scan was the consistent risk factor for CVS after SAH [3]. Cigarette smoking, hypertension, and left ventricular hypertrophy (LVH) on electrocardiogram (ECG) were associated with CVS without any relationship to SAH severity. Effects of risk factors including age, clinical grade, rebleeding, intraventricular or intracerebral hemorrhage on CT scan, acute hydrocephalus, aneurysm site and size, leukocytosis, interleukin-6, and cardiac

Q. Sun · G. Chen (*) Department of Neurosurgery, The First Affiliated Hospital of Soochow University, Suzhou, China e-mail: [email protected]

abnormalities on CVS appeared to be associated with the severity of SAH [3].

3.2

Case Report

A 66-year-old woman presented with severe headache and progression into coma. Computed tomography without contrast demonstrated diffuse subarachnoid hemorrhage (Fig.  3.1). Emergency CT angiography showed right middle cerebral artery (MCA) bifurcation aneurysm and left posterior communicating artery (PcomA) aneurysm without vasospasm. The MCA aneurysm measured 1 cm in diameter and projecting laterally. The PcomA aneurysm measured 5 mm in diameter and projecting posteriorly (Fig. 3.2). The patient was delivered to the operating room for bilateral aneurysms clipping. A thick clot was obvious in Sylvain fissure and in the subarachnoid space of the frontal and temporal lobe (Fig. 3.3). Bilateral aneurysm was clipped, and the clot was evacuated as much as possible. The lamina terminalis was fenestrated during the surgery. Then, the basal cistern was wash repeatedly with papaverine solution before the end of the surgery. Postoperatively, the patient received volume expansion and nimodipine therapy for vasospasm. Six days after the clip surgery, the GCS score descended from E3V2M5 to E2V1M3. Serum electrolyte and glucose CT scan were detected to

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 Y. Kato et al. (eds.), Recent Progress in the Management of Cerebrovascular Diseases, https://doi.org/10.1007/978-981-16-3387-4_3

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Fig. 3.1  Axial CT images of the patient showed subarachnoid hemorrhage and hydrocephalus. Blood filling the subarachnoid cisterns and extending into bilateral Sylvian fissures and anterior longitudinal fissure (red arrows). Usually, the distribution of blood could give us clues about the location of the aneurysm. For example, the greater amount of blood in the left subarachnoid cisterns than in the right indicates a left aneurysm. However, the equal amount of blood in bilateral cisterns couldn’t help us decide where the ruptured aneurysm located. The enlarged temporal horns (white arrows) indicated hydrocephalus because in most patients, the temporal horns usually are not visible

exclude brain hematoma, edema, hydrocephalus, and other structural or metabolic causes. According to the diagnosis criteria, vasospasm was possible. Thus, transcranial Doppler sonography (TCD) arranged and the result indicated moderate cerebral vasospasm (Fig.  3.4a). CTA showed the left ICA C7 segment was very narrow which supported the diagnosis of CVS (Fig. 3.4b). Triple H treatment and lumbar cistern cerebrospinal fluid drainage were carried out to alleviate the CVS. The CSF was dark red, fulfilled with broken red blood cells and other spasmogens. Two weeks later, the CSF color turned from dark red to xanthochromic and then to light yellow even near water white. Repeated TCD indicated not worsen, the patient recovered well, E4V5M6, left limb muscle strength grade V, and right limb muscle strength grade IV.

Fig. 3.2  Emergency CT angiography showed right middle cerebral artery (MCA) bifurcation aneurysm (red arrow indicated) and left posterior communicating artery (PcomA) aneurysm (white arrow indicated) without vasospasm (from anterior to posterior view). The MCA bifurcation aneurysm measured 1 cm in diameter and projecting laterally. The PcomA aneurysm measured 5 mm in diameter and projecting posteriorly. The shape of the MCA bifurcation aneurysm is irregular with bubbles on its wall. Thus, the MCA aneurysm is possibly ruptured

3.3

Discussion

3.3.1 Surgical Technique/ Management How to deal with multiple aneurysms is controversial. Single-stage treatment of multiple aneurysms can be achieved with a good outcome. Even though radiation exposure is high while treating multiple aneurysms as compared to single aneurysm cases [4], double-stage is reasonable for less invasive. We think the most important is to identify the ruptured aneurysm. How to identify the ruptured aneurysm in patients with multiple cerebral aneurysms? CT images will give us some clues about the distribution of blood which indicated the location of the aneurysm. The greater amount of blood in the right basal cisterns than in the left points to a likely location of the aneurysm on the right

3  Cerebral Vasospasm and Subarachnoid Hemorrhage

side of the cerebral circulation [1]. Unfortunately, CT scan of this case showed bilateral equal distribution of blood. The irregular sharp of aneu-

17

rysm and the largest aneurysm [5] are likely to rupture among coexisting aneurysms in a patient with multiple cerebral aneurysms. Thus, the MCA aneurysm in this case was supposed to be the ruptured aneurysm which needs to be dealt with first. During the open surgery, the lamina terminalis was fenestrated which was reported to alleviate the symptomatic vasospasm [6] and hydrocephalus [7]. Besides, lamina terminalis fenestration accelerates cisternal blood evacuation in high-­ grade aneurysmal SAH [8]. Papaverine is a strong vasodilator widely used for the treatment of vasospasm from intra-artery [9]. In our practice, the basal cistern was washed repeatedly with papaverine solution before the end of the surgery. Arteries soaked in papaverine solution will be dilated obviously.

3.3.2 Outcome Fig. 3.3  Surgical picture of using pterion approach after open the dura. Blood fulfilling the subarachnoid space on the surface of the brain could be observed. Further, the brain press was a little bit high

a

Clipping all the possible aneurysms in a single-­ stage surgical process could stop the possibility

b

Fig. 3.4  Diagnosis of CVS in the case. A: upper panel: transcranial Doppler sonography (TCD) examination of left MCA showed the mean flow velocity was 129 cm/s which supports the diagnosis of CVS in this patient. Lower panel: TCD examination of the left extracranial

segment of ICA showed the mean flow velocity was 25 cm/s. The ratio of the mean flow velocity of MCA and ICA extracranial segment is more than 3, which also supports the diagnosis of CVS. B: CTA showed a narrow segment (arrow indicated) in the ICA C7 segment

Q. Sun and G. Chen

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of aneurysms re-rupture which would lead to death. As the vasospasm alleviated because of suitable treatment, the patient recovered well, E4V5M6, left limb muscle strength grade V, right limb muscle strength grade IV.

3.3.3 Advantages and Limitations According to the guidelines from Japan, Europe, America, the diagnosis and monitoring of the vasospasm include repeated neurological examinations, TCD, CTA + CTP, and DSA [10]. It is reported DSA test identified CVS in 79 out of 90 SAH patients, while the TCD test (mean flow velocity >120 cm/s) identified CVS in 75 out of 90 SAH patients. No significant difference was found between the two methods [11]. Although the DSA test is the golden standard for the diagnosis of CVS, the DSA test is an invasive examination and could not be performed repeatedly on patients. Thus, the noninvasive ultrasound imaging technology, TCD, is widely used to monitor the intracranial blood flow to help the diagnosis of CVS [11]. Nimodipine therapy and triple “H” (hypertension, hemodilution, hypervolemia) therapy are recommended in several guidelines [10]. Other treatments such as cisternal irrigation and lumbar CSF drainage are also useful. Endovascular therapy (including intra-arterial vasodilator therapy and transluminal balloon angioplasty) is suitable for patients not responding to medical therapy could alleviate the vasospasm. Pilot studies indicate these treatments are effective. However, some meta-analyses showed controversy conclusion [12, 13]; thus, higher-­ level evidence is required for conformation.

3.3.4 Complication Avoidance Avoiding dehydration: Hypovolemia and decreased CBF in SAH patients will increase the risk of symptomatic vasospasm. Hypovolemia is usually caused by the treatment of dehydration. Thus, careful fluid resuscitation to avoid hypovo-

lemia is suggested after surgery. Prophylactic hypervolemia is not suggested before the diagnosis of CVS [14]. Calcium channel antagonists: The British aneurysm nimodipine after the SAH trial indicated nimodipine help reduce the incidence of cerebral infarction [15]. Nimodipine now is used routinely in SAH patients to help decrease the risk of CVS. Routine TCD test: TCD, as an invasive test, should be a routine examination after SAH treatment. Even, computed tomography perfusion should be carried out to confirm infract lesion. Evacuation or drainage of the subarachnoid clot and spasmogen: Further, cistern clot evacuation to reduce the subarachnoid blood load during the clip surgery is suggested. For high-­ grade aneurysms, early lumbar cistern cerebrospinal fluid drainage might be helpful.

3.4

Conclusion

Advances in diagnostic neuroimaging and the development of monitoring devices have improved to an extent the ability to predict those patients who are at risk for vasospasm. Although vasospasm remains one of the dreaded complications following aneurysmal SAH, further advances in endovascular techniques and understanding of the disease would help improve outcomes.

References 1. Lawton MT, Vates GE. Subarachnoid hemorrhage[J]. N Engl J Med. 2017;377(3):257–66. 2. Janardhan V, Biondi A, Riina HA, Sanelli PC, Stieg PE, Gobin YP.  Vasospasm in aneurysmal subarachnoid hemorrhage: diagnosis, prevention, and management. Neuroimaging Clin N Am. 2006;16(3):483–96. 3. Inagawa T. Risk factors for cerebral vasospasm following aneurysmal subarachnoid hemorrhage: a review of the literature. World Neurosurg. 2016;85:56–76. 4. Tejus MN, Singh D, Jagetia A, Singh H, Tandon M, Chawla R, Ganjoo P. Endovascular nuances in management of multiple intracranial aneurysms. Neurol India. 2019;67(4):1062–5. 5. Shojima M, Morita A, Nakatomi H, Tominari S. Size is the most important predictor of aneurysm rup-

3  Cerebral Vasospasm and Subarachnoid Hemorrhage ture among multiple cerebral aneurysms: post hoc ­subgroup analysis of unruptured cerebral aneurysm study Japan. Neurosurgery. 2018;82(6):864–9. 6. Cengiz SL, Ilik MK, Erdi F, Ustun ME.  The role of fenestration of the lamina terminalis on symptomatic vasospasm after aneurysmal subarachnoid hemorrhage: a clinical research. Turk Neurosurg. 2016;26(5):714–9. 7. Tao C, Fan C, Hu X, Ma J, Ma L, Li H, Liu Y, Sun H, He M, You C. The effect of fenestration of the lamina terminalis on the incidence of shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage (FISH): study protocol for a randomized controlled trial. Medicine (Baltimore). 2016;95(52):e5727. 8. Mura J, Rojas-Zalazar D, Ruiz A, Vintimilla LC, Marengo JJ.  Improved outcome in high-grade aneurysmal subarachnoid hemorrhage by enhancement of endogenous clearance of cisternal blood clots: a prospective study that demonstrates the role of lamina terminalis fenestration combined with modern microsurgical cisternal blood evacuation. Minim Invasive Neurosurg. 2007;50(6):355–62. 9. Liu JK, Couldwell WT. Intra-arterial papaverine infusions for the treatment of cerebral vasospasm induced by aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2005;2(2):124–32. 10. Li K, Barras CD, Chandra RV, Kok HK, Maingard JT, Carter NS, Russell JH, Lai L, Brooks M, Asadi H. A

19 review of the management of cerebral vasospasm after aneurysmal subarachnoid hemorrhage. World Neurosurg. 2019;126:513–27. 11. Li DD, Chang JY, Zhou CX, Cui JB. Clinical diagnosis of cerebral vasospasm after subarachnoid hemorrhage by using transcranial Doppler sonography. Eur Rev Med Pharmacol Sci. 2018;22(7):2029–35. 12. Venkatraman A, Khawaja AM, Gupta S, Hardas S, Deveikis JP, Harrigan MR, Kumar G.  Intra-arterial vasodilators for vasospasm following aneurysmal subarachnoid hemorrhage: a meta-analysis. J NeuroInterv Surg. 2018;10(4):380–7. 13. Yao Z, Hu X, You C. Endovascular therapy for vasospasm secondary to subarachnoid hemorrhage: a meta-analysis and systematic review. Clin Neurol Neurosurg. 2017;163:9–14. 14. Lennihan L, Mayer SA, Fink ME, Beckford A, Paik MC, Zhang H, Wu YC, Klebanoff LM, Raps EC, Solomon RA. Effect of hypervolemic therapy on cerebral blood flow after subarachnoid hemorrhage: a randomized controlled trial. Stroke. 2000;31(2):383–91. 15. Pickard JD, Murray GD, Illingworth R, Shaw MD, Teasdale GM, Foy PM, Humphrey PR, Lang DA, Nelson R, Richards P, Et A. Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial. BMJ. 1989;298(6674):636–42.

4

White Fibers of the Brain: A Novel Classification Abhidha Shah, Sukhdeep Singh Jhawar, and Atul Goel

4.1

Introduction

There has been resurgence in studying the anatomy of white matter tracts and understanding white matter tract disruptions giving rise to disconnection syndromes given the recent advances in glioma surgery. While damage to a cortical functional area can sometimes be compensated for by another region by plasticity, damage to the bundles of fibers is irreparable. White fibers of the brain are classified into three types: (1) association fibers that interconnect different cortical areas in the same hemisphere, (2) commissural fibers that connect similar regions of the two hemispheres across the midline, and (3) projection fibers that connect the cortex with subcortical regions, the brainstem, and spinal cord. The association fibers are the short association fibers or the U fibers, the superior longitudinal fasciculus (SLF), the arcuate fasciculus (AF), the inferior longitudinal fasciculus (ILF), the uncinate fasciculus (UF), the inferior occipitofrontal fasciculus (IFOF), and the cingulum. The commissural fibers consist of the corpus callosum, anterior commissure (AC), the posterior commissure, the hippocampal commissure, and the habenular commissure. The internal capsule and the thalamic radiations constitute the

A. Shah (*) · S. S. Jhawar · A. Goel Department of Neurosurgery, Seth G.S. Medical College and K.E.M Hospital, Mumbai, India

projection fiber system of the brain. The steps of dissection have been discussed by us in our publication and are alluded to here briefly [1–3].

4.2

Specimen Preparation and Steps of Dissection

The preparation of the specimens and dissection techniques used were based on the method described by Klingler et al. [2] Initially, normal human cerebral hemispheres were fixed in 10% formalin for 30  days. The formalin-fixed hemispheres were then frozen −10 degrees for 3–4  weeks [1–3]. Freezing allows formalin ice crystals to form between the nerve fibers, thus separating them and aiding subsequent dissection. After freezing, the specimens are allowed to thaw for 24 h in normal temperature water. The first step in the dissection involves the removal of the leptomeninges and the vascular structures. The dissection is then begun with the aid of the operating microscope under 6×–40× magnification. In between dissections, the hemispheres were stored in 4% formalin solution. The primary dissection tools were handmade wooden spatulas with tips of different sizes and shapes. The white fibers were studied by dissecting the brain from three avenues, lateral, inferior, and medial. Initially, all the major named gyri and sulci were identified (Fig. 4.1). The ­dissection was then commenced from each named gyrus.

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 Y. Kato et al. (eds.), Recent Progress in the Management of Cerebrovascular Diseases, https://doi.org/10.1007/978-981-16-3387-4_4

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Table 4.1  The classification of the white fibers of the brain based on direction and depth Classification of fiber bundles Horizontal layer 1. Superficial Group 1. Middle Group 1. Deep Group 1. Central Group Fig. 4.1  The superior surface of the cerebral hemisphere. On one side, the gray matter has been kept intact. On the other side, the superficial cortical gray matter in the depths of the sulci has been removed to show the short arcuate fibers. (a) Superior frontal gyrus, (b) middle frontal gyrus, (c) inferior frontal gyrus, (d) corpus callosum, (e) superficial gray matter, (f) short arcuate fibers

4.3

Novel Classification of the Brain White Fiber System

In our recent article on the subject, we presented a novel classification of the structural design of the white fibers of the brain based on the direction and depth of the fiber bundles [1] (Table 4.1). We believe that this will help both the novice and the trained neurosurgeon in understanding the intangible anatomy of the white fibers of the brain and in preventing neurological deficits (Table 4.2). We classified the white fibers of the brain into four horizontal and one vertical layer [1] (Fig. 4.2; Table 4.1). These are the superficial, middle, deep, central and vertical groups [1]. The superficial, middle and deep layers or groups consist of the association fibers, the central group of fibers is the commissural fibers, and the vertical group constitutes the projection fibers which run rostral to caudal. The first horizontal layer or the superficial group is that of the short association fibers, the U fibers, or the intergyral fibers. This is the first layer, which is present throughout the hemisphere. The second horizontal layer or the middle group is that of

Vertical layer  Projection fibers

Fibers included Short association fibers or the arcuate fibers SLF, AF, ILF, middle longitudinal fasciculus, UF, IFOF, sagittal stratum Fornix, stria terminalis, striae medullaris thalami, medial and lateral longitudinal striae Corpus callosum, anterior commissure, posterior commissure, habenular commissure, hippocampal commissure Internal capsule and thalamic radiations

the long association fibers that connect various regions in the same cerebral hemispheres. These are the superior longitudinal fasciculus (SLF), the arcuate fasciculus (AF), the middle longitudinal fasciculus, the inferior longitudinal fasciculus (ILF), and the cingulum. Further, deep are the UF, the IFOF, and the sagittal stratum. The central group of fibers consists of the corpus callosum, the anterior and posterior commissure, the habenular commissure, and the hippocampal commissure. These fibers run from one hemisphere horizontally across to the other and connect similar regions in the two hemispheres to each other. The vertical group of fibers is that of the projection fibers. These are comprised of the internal capsule and the thalamic radiations. This vertical bundle of fibers bisects the second (middle) layer of horizontal fibers into two medial and lateral compartments [1]. The most medial portion of the SLF and the cingulum lie medial to the projection fibers. The other association fibers lie lateral to this vertical layer of projection fibers. The central group or the commissural fibers lie medial to the vertical layer except for the anterior commissure that crosses this vertical projection fiber system on its inferior aspect.

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Table 4.2  The effects of damage to the major fiber bundles Fiber bundle Superior longitudinal fasciculus

Arcuate fasciculus Cingulum Inferior fronto-occipital fasciculus Uncinate fasciculus Optic radiations Middle longitudinal fasciculus Inferior longitudinal fasciculus Corpus callosum

Anterior commissure Hippocampal commissure Internal capsule Corona radiata Fornix

Deficit due to damage Nondominant hemisphere: Neglect syndromes, visuospatial inattention, difficulty in initiation of motor activity Dominant hemisphere: Articulatory disorders Conduction aphasia, transcortical motor aphasia Behavioral and emotional disturbances Semantic paraphasias

Behavioral and emotional disturbances Visual field deficits No known deficit

Unilateral damage causes no deficit, bilateral damage causes prosopagnosia Anterior disconnection—Left unilateral motor apraxia, crossed optic ataxia, agraphia of the left hand, right unilateral constructional apraxia, or alien hand syndrome Posterior disconnection—left visual anomia, left hemialexia, left auditory anomia, left tactile anomia, and right olfactory anomia Behavioral and emotional disturbances Memory disturbances Contralateral motor and sensory deficits Varying degrees of contralateral motor and sensory deficits Memory disturbances

The third horizontal layer or the deep group of fibers is that of the deep association fibers. These fibers lie within the ventricular system in close relation to the walls of the ventricular cavity. These are the fornix, the stria terminalis, striae medullaris thalami, and the medial and longitudinal striae. There are two other fiber bundles that lie within the gray matter of the thalamus and the upper midbrain, which are included here. These are the mammillothalamic and the mammilloteg-

Fig. 4.2  Dissected specimen of the medial aspect of cerebral hemisphere showing the classification of the various fiber bundles. The circles denote the various levels or groups. The first horizontal layer (yellow circle) or the superficial group is that of the short association fibers, the U fibers, or the intergyral fibers. The second horizontal layer (orange circle) or the middle group is that of the long association fibers. On the medial surface, these consist of the superior longitudinal fasciculus and the cingulum. The central group (purple circle) is that of the commissural fibers that run from one hemisphere horizontally to the other. On the medial surface, the corpus callosum constitutes the central group   The vertical group (blue circle) of fibers is that of the projection fibers. These is comprised of the internal capsule and the thalamic radiations. On the medial surface of the hemisphere, this is represented by the corona radiata   The third horizontal layer (green circle) or the deep group of fibers is that of the deep association fibers. These fibers lie within the ventricular system in close relation to the walls of the ventricular cavity. These are the fornix, the stria terminalis, the striae medullaris thalami, and the medial and longitudinal striae

mental tracts. The deep gray matter of the brain lies straddled on both sides of the vertical group of projection fibers [1].

4.4

 he First Layer/Superficial T Group

4.4.1 Short Association or U Fibers The short association or the U fibers connect adjoining gyri to each other. These fibers are seen after removing the superficial gray matter and the gray matter that runs in the depths of the sulci (Fig. 4.3). These fibers can be damaged when a transcortical incision is placed over the hemisphere [1].

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Fig. 4.3  Dissected specimen of the lateral aspect of the cerebral hemisphere. The cortical gray matter has been completely removed to show the short association fibers of the entire hemisphere

4.5

 he Second Layer/the Middle T Group

4.5.1 Superior Longitudinal Fasciculus (SLF) 4.5.1.1 Course and Connections The SLF is the most superficial of the long association fibers and runs between the frontal and parietal lobes and is the first fiber bundle that is encountered after removing the short association fibers (Fig. 4.4). Traditionally, the superior longitudinal fasciculus and the arcuate fasciculus were considered as part of a single fiber system and described as a single structure with a horizontal frontoparietal segment, a vertical temporoparietal segment, and a horizontal frontotemporal segment or the arcuate fasciculus [4, 5]. A few other studies have described the superior longitudinal fasciculus as having three parts: SLF I, SLF II, and SLF III from medial to lateral [6]. Our dissections have revealed the superior longitudinal fasciculus to be a broad sheet of fibers running from the frontal to the parietal regions of the brain. This broad layer is divided by the projection fibers into medial and lateral parts. [1, 7] The medial part of the SLF (also known as the SLF I) connects the superior frontal gyrus to the precuneus of the parietal lobe. The cingulum lies inferior to it and its lateral relations are the upcurving fibers of the corpus callosum and the corona radiata. The lateral part of the

superior longitudinal fasciculus (SLF II and SLF III) lies lateral to the projection group of fibers. The SLF II connects the middle frontal gyrus to the angular gyrus (SLF II), and the SLF III connects the inferior frontal gyrus to the supramarginal gyrus. Though categorized as two different parts, it is not very easy to separate these two portions of the SLF as they run as a thick confluent bundle between the frontal and parietal lobes. The AF courses inferior to this portion of the SLF. The mean length of the (frontoparietal segment of) superior longitudinal fasciculus is 13.5 cm (12.2–14.7 cm). It connects widely various regions of the frontal, parietal and temporal lobes. The fasciculus lies at a depth of 2.5–2.7 cm from the surface [1].

4.5.1.2 Function The SLF I by virtue of its connections between the superior frontal gyrus and the parietal lobe is involved in regulating motor behavior. [8–10] The SLF II connects the dorsal prefrontal cortex to the caudal inferior parietal cortex and provides the prefrontal cortex with information regarding perception of visual space [1]. The SLF III connects the ventral premotor and prefrontal cortex to the supramarginal gyrus. In the dominant hemisphere, this pathway is important for speech articulation, and in the nondominant hemisphere, it subserves visuospatial attention, prosody, and music processing [1].

4.5.2 Arcuate Fasciculus (AF) 4.5.2.1 Course and Connections In our dissections, the AF was visualized as a reverse C-shaped fiber bundle (Fig. 4.4) running inferior to the lateral portion of the SLF beneath the frontal and temporal opercula and then curving downwards in the region of the supramarginal and angular gyrus and then running forwards towards the temporal pole beneath the superior and middle temporal gyri (Fig.  4.4). The mean length of the AF was 12.5 cm. The AF runs below the middle and inferior frontal gyri, the suprasylvian portions of the precentral and postcentral gyri, the angular and supramarginal gyri, the

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Fig. 4.4  Stepwise dissection from the lateral perspective of the cerebral hemisphere. (a) Lateral view of the hemisphere. The superior, middle, inferior frontal gyri, the precentral and postcentral gyri, the superior and inferior parietal lobules, the superior temporal gyrus, and the occipital gyri have been removed to reveal the following fiber bundles. (a) Vertical fibers of the corona radiata, (b) the lateral portion of the superior longitudinal fasciculus (SLF II and III), (c) arcuate fasciculus, (d) extreme capsule and claustrum. (b) Lateral view of the hemisphere

after removal of the gray matter of the entire hemisphere. (a) Corona radiata, (b) lateral portion of superior longitudinal fasciculus (SLF II and SLF III), (c) arcuate fasciculus, (d) short arcuate fiber connecting the inferior frontal gyrus to the arcuate fasciculus, (e) ventral occipital fasciculus. (c) Tractography image showing the various fiber bundles. IFOF Inferior fronto-occipital fasciculus, ILF Inferior longitudinal fasciculus, AF Arcuate fasciculus, SS Sagittal stratum, IC Internal capsule

inferior portion of the superior temporal gyrus, and the superior portion of the middle temporal gyrus [1, 11].

The classical model of language consists of the Broca’s area, Wernicke’s area, and the arcuate fasciculus connecting these two regions. Recently, Hickok et  al. proposed a dual-stream model for language, the dorsal stream and the ventral stream [13]. The dorsal stream is involved with phonological processing and is mediated by the SLF II and III and the AF. The ventral stream of language is involved with semantic processing

4.5.2.2 Function The role of the AF in language use is best represented by conduction aphasia, caused by damage to the AF [12]. This type of aphasia prevents the patient from repeating unfamiliar sounds.

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and consists of the IFOF, the ILF, and the middle longitudinal fasciculus.

4.5.3 Ventral Occipital Fasciculus

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inferior temporal gyrus and the fusiform gyrus. The exact termination point of the inferior longitudinal fasciculus was not identified in our dissection specimens.

4.5.3.1 Course and Connections This fasciculus runs just posterior to the turn of the arcuate fasciculus. It connects the inferior occipital lobe to the superior occipital lobe and the angular gyrus (Fig. 4.4).

4.5.5.2 Function The inferior longitudinal fasciculus forms one of the components of the ventral stream of language processing. [1] Damage to the ILF leads to difficulties in reading, face recognition, visual perception, and visual memory.

4.5.3.2 Function This tract is said to have an important role in reading and facial recognition.

4.5.6 Inferior Fronto-Occipital Fasciculus (IFOF)

4.5.4 Middle Longitudinal Fasciculus 4.5.4.1 Course and Connections The existence of the middle longitudinal fasciculus in humans was much debated. However, recent fiber dissection studies have clearly demonstrated its presence in the human brain [14]. The middle longitudinal fasciculus can be visualized after the removal of the fibers of the AF. It is seen to course beneath the AF connecting the superior temporal gyrus to the parietal lobe. The fibers are seen to run posteriorly and slightly superiorly towards the parietal and occipital lobes and have a vague termination. They form the uppermost portion of the sagittal stratum. 4.5.4.2 Function The middle longitudinal fasciculus is thought to play a role in language processing; however, damage to even a significant portion of the fasciculus has not been observed to lead to any language impairment [14].

4.5.5 Inferior Longitudinal Fasciculus (ILF) 4.5.5.1 Course and Connections The ILF connects the inferior portions of the temporal and occipital lobes. The fibers can be visualized after removing the gray matter of the

4.5.6.1 Course and Connections Fibers from the lateral orbital gyri join fibers from the middle and inferior frontal gyri and pass lateral to the corona radiata fibers and inferior to the SLF and AF towards the temporal lobe to form the IFOF. The IFOF forms a component of the temporal stem (Fig. 4.5). In the region of the insula, IFOF and the UF form the ventral portion of the external capsule with the IFOF lying superiorly and the UF lying inferiorly. In the temporal lobe, the majority of the fibers of the IFOF pass through the superior and middle temporal gyri to reach the parietal and occipital gyri. The fibers of the IFOF running posteriorly form a component of the sagittal stratum and lie lateral to the optic radiations [1]. 4.5.6.2 Function The IFOF forms the main portion of the ventral semantic pathway of language. Intraoperative stimulation of the IFOF gives rise to semantic paraphasias (error in the meaning of the target word) [16, 17].

4.5.7 Uncinate Fasciculus (UF) 4.5.7.1 Course and Connections The UF is a horseshoe-shaped tract running in the anterior and inferior portion of the temporal stem connecting the orbitofrontal and temporal regions. In the temporal stem, the UF runs anteroinferior to the IFOF and ends in the superior and

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Fig. 4.5  Stepwise dissection of the insular region. (a) The frontal and temporal opercula have been removed to show the hidden insular lobe. (a) Short gyri of the insula, (b) long gyri of the insula. (b) The insular gyri have been removed to show the extreme capsule, the claustrocortical system, and the claustrum. (a) Extreme capsule, (b) claustrum, (c) fibers of the extreme capsule as they join the

corona radiata, (d) beginning of the inferior fronto-­ occipital fasciculus. (e) Fibers of the corona radiata. (c) Various fiber bundles in the region of the insula. (a) Arcuate fasciculus, (b) inferior fronto-occipital fasciculus, (c) uncinate fasciculus, (d) optic radiations, (e) fibers of the internal capsule seen after removing the putamen, (f) corona radiata, (g) lateral portion of the SLF

middle temporal gyri (Fig. 4.5). The dorsolateral portion of the UF connects the temporal pole to the lateral orbitofrontal gyri, and its ventromedial portion connects the temporal pole to the medial orbitofrontal cortex and the septal area. The ventromedial portion of the UF runs anterior to the anterior perforated substance deep to the posterior orbital gyrus. It covers the inferomedial portion of the nucleus accumbens and ultimately terminates in the region below the genu of the corpus callosum.

social–emotional functions [18]. UF involvement is seen in five disorders, namely, anxiety, schizophrenia, psychopathy, epilepsy, and frontotemporal dementia [19].

4.5.7.2 Function The UF is considered to be part of the ventral limbic pathway. The literature refers to three functions of the UF: associative and episodic memory functions, linguistic functions, and

4.5.8 S  agittal Stratum and the Optic Radiations 4.5.8.1 Course and Connections The sagittal stratum as the name suggests consists of a layer of fibers stacked one on top of each other. It mainly consists of the fibers of the IFOF, the fibers of the anterior commissure, and the optic radiations (Fig.  4.5). Some authors also include the fibers of the middle longitudinal fasciculus, the inferior longitudinal fasciculus, and

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the tapetum as part of the sagittal stratum. But in our dissections, we found that the bulk of the fibers consisted of the IFOF, the AC, and the optic radiations. These three fiber systems are difficult to distinguish after they merge with the optic radiations. However, our dissections have shown that the fibers of the anterior commissure and the IFOF lie laterally, and the optic radiations lie medially [1, 20]. The point where the three fiber systems converge was clearly identified in our fiber dissection previously. The optic radiations also known as the geniculocalcarine tract begin at the lateral geniculate body and end in the calcarine cortex (primary visual cortex) of the occipital lobe [21]. The optic radiations are composed of three bundles, anterior, central, and posterior running towards the occipital lobe (Fig.4.5). It is not usually possible to clearly delineate the three bundles by dissection. The anterior bundle forms the sublenticular portion, and the central and posterior bundles form the retrolenticular portion of the internal capsule. The anterior bundle (Meyer’s loop) courses first anteriorly from the lateral geniculate body to the roof of the temporal horn and then turns posteriorly to occupy the lateral wall of the temporal horn. It continues posteriorly to terminate at the inferior bank of the calcarine sulcus within the lingual gyrus. The central bundle runs over the roof of the temporal horn and then courses posteriorly in the lateral wall of the trigone and occipital horn and terminates at the occipital pole. The posterior bundle travels directly posteriorly over the trigone as part of the lateral wall and roof to end in the superior bank of the calcarine sulcus within the cuneus [21].

4.5.8.2 Function The optic radiations carry visual information from the lateral geniculate body onwards to the visual cortex. Damage to the anterior bundle will cause contralateral superior quadrantonopia, “a pie on the sky” type of visual field defect as the anterior bundle subserves the visual fibers from the superior quadrant of the contralateral visual field. Similarly, damage to the posterior bundle causes a contralateral inferior quadrantanopia or a “pie in the floor” type of visual field deficit as this bundle is composed of fibers from the infe-

rior quadrant of the contralateral visual field. The central bundle carries visual inputs from the macula.

4.5.9 Cingulum 4.5.9.1 Course and Connections The cingulum is a C-shaped association bundle which, runs just above and parallel to the corpus callosum, and is a major constituent of the limbic system [3]. It begins in the region of the subcallosal gyrus below the rostrum of the corpus callosum and then runs superiorly bends posteriorly above the genu of the corpus callosum and then continues posteriorly to terminate in the temporal lobe (Fig. 4.6). In the region superior to the splenium, the cingulum narrows to form the isthmus of the splenium. The cingulum then continues beneath the corpus callosum on the medial surface of the hemisphere as the radiation of the cingulum ends in the parahippocampal region adjacent to the hippocampus. The length of the whole cingulum from its origin in the subcallosal area to its termination in the parahippocampal region was found to be 19 cm [1]. The cingulum lies at a depth of 3.5 cm from the surface of the brain [1]. The cingulum communicates with the superior frontal gyrus and the precuneus by means of connections from its superior surface. Two of these connections are very clearly depicted in Fig. 4.7c.

Fig. 4.6  Medial surface of the hemisphere after the removal of the cortical gray matter. (a) Corona radiata, (b) superior longitudinal fasciculus, (c) cingulum, (d) corpus callosum, (e) caudate head

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Fig. 4.7  Images of the corpus callosum. (a) Image showing the entire anteroposterior extent of the corpus callosum. (a) Transverse running fibers of the corpus callosum. (b) Fibers of the corpus callosum as they curve upwards

on the medial aspect of the cerebral hemisphere. (b) Tractographic image showing the corpus callosum with its dorsal and ventral callosal radiations, running between the vertical layers of projection fibers bilaterally

4.5.9.2 Function The cingulum is a major component of the dorsal limbic pathway. Damage to this structure leads to behavioral and emotional disturbances. It is also involved in the appraisal of pain and reinforcement of behavior that reduces pain [15].

and the paraterminal gyrus on the medial surface of the cerebral hemisphere. The subcallosal area and the paraterminal gyrus constitute the septal area, beneath which are the septal nuclei [3, 22]. The medial septal nucleus connects to the amygdala via the diagonal band of Broca and the ventral amygdalo-fugal pathway.

4.5.10 Medial and Lateral Olfactory Striae

4.5.10.2 Function The medial and lateral olfactory striae form a component of the limbic system. Functionally, the septal nuclei are responsible for connecting limbic structures with the hypothalamus and the brainstem, principally via the hippocampal formation.

4.5.10.1 Course and Connections The olfactory tract terminates as the medial and lateral olfactory striae on the orbital surface of the frontal lobe. The lateral olfactory stria runs on the posterior margin of the posterior orbital gyrus and forms the anterior boundary of the anterior perforated substance. It courses laterally to terminate in the piriform cortex and the corticomedial part of the amygdaloid nuclear complex [3, 22]. The medial olfactory stria runs on the posterior margin of the medial orbital gyrus and gyrus rectus to becomes continuous with the subcallosal

4.6

The Central Group

4.6.1 Corpus Callosum 4.6.1.1 Course and Connections The corpus callosum forms the most prominent fiber bundle on the medial surface of the brain

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and is the largest commissural fiber system of the brain (Fig. 4.7a, b). It is divided into four parts: the rostrum, the genu, the body, and the splenium. The mean length of the corpus callosum as measured from the anterior end of the rostrum to the inward curve of the splenium was 12.4  cm (10.7–13.4  cm), and the average breadth was 12 mm (11.5–13 mm) [1]. The depth of the corpus callosum from the surface of the brain was 4 cm. The superior surface of the corpus callosum is covered by the indusium griseum, a thin sheet of gray matter. The dentate gyrus continues as the subsplenial gyrus on the posterior aspect of the corpus callosum and then curves superiorly over the surface of the corpus callosum as the indusium griseum. The medial and lateral longitudinal striae of Lancisi run within the indusium griseum. These fibers are considered to be aberrant fibers of the fornix, which leave the fimbria course over the superior surface of the corpus callosum along with the subsplenial gyrus and then join the fornix again anteriorly. On removing this layer, the transverse running fibers of the corpus callosum are visualized. When viewed from above, the fibers of the corpus callosum curving superiorly resemble upturned bicycle handles running from one corona radiata to the other corona radiata connecting both the hemispheres. Thus, the corpus callosum lies between the vertical layer of fibers in each hemisphere. This whole constellation of fibers of the horizontal spread of the corpus callosum and the two vertical fiber layers of the projection system on each side resembles a hanging rope bridge [1]. Unlike a rope bridge, however, the transfer of information occurs from side to side rather than from anterior to posterior. The transverse running fibers of the corpus callosum after crossing the cingulum turn anteriorly, superiorly, posteriorly, and inferiorly to form the anterior, dorsal, posterior, and ventral callosal radiations, respectively. The fibers arising from the genu of the corpus callosum curve anteriorly to form the forceps minor. They form the medial wall of the frontal horn of the lateral ventricle and connect the prefrontal and the orbitofrontal areas of the hemispheres to each other. The dorsal callosal radiations consist of the hori-

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zontal fibers of the corpus callosum coursing laterally and curving superiorly to connect the frontal and parietal lobes. They merge laterally with the fibers of the corona radiata. The posterior callosal radiations consist of fibers arising from the splenium of the corpus callosum or the forceps major. The ventral fibers emerging from the genu of the corpus callosum form the anteromedial portion of the medial wall of the frontal horn. These fibers connect the bilateral caudate nuclei to each other [1]. The callosal fibers emanating from the rostrum also form part of the ventral callosal radiations. They form the floor of the frontal horn of the lateral ventricle and connect the temporal lobes to each other by means of the temporal stem. The ventral callosal radiations arising from the body of the corpus callosum form the roof of the superior part of the frontal horn and the body of the lateral ventricle. The ventral and inferiorly curving fibers that arise the splenium run laterally and then downwards to form the superior and lateral wall of the atrium and temporal horn. These fibers are known as the tapetum. They separate the temporal and the atrial lateral walls from the optic radiations. Thus, the corpus callosum connects similar regions of the hemispheres to each other. It also encompasses the entire ventricular system within its callosal radiations.

4.6.1.2 Function The main function of the corpus callosum is to integrate and transfer information from both cerebral hemispheres to process sensory, motor, and high-level cognitive signals [1]. The corpus callosum seems to be topographically organized, involved in the transfer of visual, auditory, and somatosensory information in posterior regions and higher cognition in anterior regions. The anterior callosal fibers transfer motor information between the frontal lobes, and the posterior fibers are involved in the processing of somatosensory cues (posterior midbody), as well as auditory and visual cues (splenium) by connecting the parietal, temporal, and occipital lobes [1]. The corpus callosum is known to play a vital role in refining motor movements and cognitive functions. Anterior callosal disconnection can cause left

4  White Fibers of the Brain: A Novel Classification

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unilateral motor apraxia, crossed optic ataxia, agraphia of the left hand, right unilateral constructional apraxia, or alien hand syndrome. Posterior callosal disconnection can cause left visual anomia, left hemialexia, left auditory anomia, left tactile anomia, and right olfactory anomia [7].

4.6.2 Anterior Commissure 4.6.2.1 Course and Connections The anterior commissure resembles a horizontally placed bow and runs anterior to the columns of the fornix [1, 3, 21, 22] (Fig.  4.8). The anterior commissure courses deep and parallel to the fibers of the UF and IFOF in a canal of gray matter known as the canal of Gratiolet. It lies deep to the anterior perforated substance and the substantia innominata. The fibers of the anterior commissure divide into a small anterior or frontal and a large posterior or temporal component. The anterior fibers course on the basal surface of the frontal lobe and connect the anterior olfactory nucleus of one side to the contralateral side. The posterior portion of the anterior commissure courses laterally towards the temporal lobe. It runs deep to the lentiform nucleus and ultimately forms a component of the sagittal stratum just medial to the fibers of the IFOF. The globus pallidus lies posterior to the temporal component of the anterior commissure. The average total length of the anterior commissure before its amalgamation with the sagittal stratum was 78 mm (74–80 mm) [1]. The distance of the anterior commissure from the temporal pole was a mean of 18 mm (16–20 mm) [1]. As discussed earlier, the anterior commissure is the only fiber bundle that crosses the vertical layer of the projection system. 4.6.2.2 Function The role of the anterior commissure is not very well defined. It is a major component of the limbic system and is said to play a role in the interhemispheric transfer of visual, auditory, and olfactory information between temporal lobes. It is said to have a key role in pain sensation, sense of smell, and chemoreception [21]. Thus, the

Fig. 4.8  Dissection of the basal surface of the brain showing the entire extent of the anterior commissure. The anterior fibers of the anterior commissure connect the anterior olfactory nucleus of one side to the contralateral side. The posterior portion of the anterior commissure runs posterolaterally to form a component of the sagittal stratum. (a) Anterior commissure, (b) Columns of fornix, (c) Fibers of the internal capsule

anterior commissure seems to be involved in memory, emotion, speech and hearing, olfaction, instinct, and sexual behavior [1].

4.6.3 Hippocampal Commissure/ Psalterium 4.6.3.1 Course and Connections The hippocampal commissure or the psalterium (named after an ancient stringed instrument) has been known by various names such as the hippocampal fissure, the commissure of the fornix, forniceal commissure, or the interammonic commissure [1]. The commissure consists of transverse fibers connecting the crura of the two fornices to each other [23]. The psalterium occupies a triangular space between the two crura of the fornices and lies just beneath the splenium of the corpus callosum. Although it is in intimate contact with the splenium, it can be separated and distinguished from it by blunt dissection. Beneath the hippocampal commissure lies the velum interpositum and the roof of the third ventricle.

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4.6.3.2 Function The hippocampal commissure is involved in the transmission of information between the two hippocampi and damage to it results in memory disturbances.

4.7

The Vertical Group

4.7.1 Internal Capsule 4.7.1.1 Course and Connections The internal capsule is the projection fiber system of the brain and consists of the corticobulbar fibers, the corticospinal fibers, and the thalamic radiations [1]. It is made up of five parts, the anterior limb, the genu, the posterior limb, the retrolenticular portion, and the sublenticular portion (Fig. 4.9). The corticobulbar and corticospinal tracts lie laterally and the thalamic radiations lie medially [1]. The anterior limb of the internal capsule lies between the head of the caudate nucleus and the lentiform nucleus and consists of the anterior and superior thalamic radiations and the frontopontine fibers. The genu of the internal capsule is the junction of its anterior and posterior limbs in the same coronal plane as the foramen of Monroe [7]. It consists of the superior thalamic radiations, the corticobulbar fibers, and the anterior portion of the corticospinal tract [1]. The posterior limb of the internal capsule lies between the globus pallidus and the thalamus. It consists of the posterior part of the corticospinal tract, the parietal thalamic radiations, and the parietopontine fibers. The retrolenticular portion of the internal capsule includes the parietopontine fibers and some portion of the occipital thalamic radiations. [1] The sublenticular portion of the internal capsule consists of the occipitopontine, the temporopontine, and the major bulk of the occipital thalamic radiation. [1] The anterior bundle of the optic radiations lies in the sublenticular portion of the internal capsule, and the central and posterior bundles lie in the retrolenticular portion of the internal capsule.

Fig. 4.9  Dissected specimen showing the entire extent of the internal capsule and the vertical layer of projection fibers. (a) Anterior limb of the internal capsule, (b) genu of the internal capsule, c. Posterior limb of the internal capsule, (d) retrolenticular portion of the internal capsule, (e) sublenticular portion of the internal capsule (Meyer’s loop)

4.7.1.2 Function The internal capsule is involved in transmitting motor, sensory and behavioral information from the higher cortical centers to the brainstem and the spinal cord. Damage to the anterior limb of the internal capsule causes behavioral disturbances and damage to the genu and the posterior limb causes contralateral motor and sensory deficits [7].

4.7.2 External Capsule 4.7.2.1 Course and Connections The external capsule is a vertical claustro-cortical projection fiber system that connects the insula to the frontal and parietal cortices (Fig. 4.5). It lies between the claustrum laterally and the putamen medially. It consists of two parts the ventral external capsule and the dorsal external capsule. The ventral portion consists of fibers of the IFOF and UF.  The dorsal portion consists of fibers which traverse superiorly to join the corona radiata. 4.7.2.2 Function The external capsule and the dorsal claustrocortical system are involved in the integration of visual, somatosensory, and motor information. Bilateral damage to the external capsule causes severe encephalopathy. [7]

4  White Fibers of the Brain: A Novel Classification

4.7.3 Corona Radiata 4.7.3.1 Course and Connections The external and internal capsule fibers join together at the upper edge of the putamen to form the corona radiata (Figs. 4.4 and 4.5). The corona radiate and the projection fibers divide the middle group of association fibers into medial and lateral halves [1]. At its medial margin, the callosal fibers join the corona radiata to form the centrum semiovale. 4.7.3.2 Function Damage to the corona radiata causes varying degrees of contralateral motor and sensory deficits.

4.8

The Third Layer/Deep Group

4.8.1 Fornix 4.8.1.1 Course and Connections The fornix forms the most important component of the Papez circuit and the limbic system. Axons from the subiculum and the pyramidal cells of the hippocampus form the alveus and the fimbria, which run on the surface of the hippocampus. The fimbria then turns superolaterally over the pulvinar of the thalamus to form the crus of the fornix (Latin meaning “vault or arch”) (Fig.  4.10). Further anteriorly, the two crura meet in the midline to form the body of the fornix. At the anterior end of the thalamus, the fibers of the fornix of the two sides again separate and arch downwards in front of the intraventricular foramen as the columns of the fornix [3]. We found from our dissections that the columns of fornix had an average length of 21.3  mm (20–23  mm) and an average breadth of 2.3  mm (2–2.6  mm) [3]. The fornix constitutes the main efferent pathway from the hippocampus, though it also carries a few afferent fibers [3]. Close to the anterior commissure, the columns of the fornix divide into a pre-­commissural and a post-commissural portion. The majority of the fibers constitute the post-­commissural portion [23, 24]. The post-­commissural fornix is made up

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of fibers from the subiculum and terminate into the medial mamillary nucleus of the mammillary body. En route to the mammillary body, the postcommissural fibers send some fibers directly to the lateral and anterior nucleus of the thalamus and to the lateral septal nuclei. Thus, the anterior nucleus of the thalamus receives fibers from the mamillothalamic tract and also receives direct fibers from the post-commissural fornix. A few fibers pass ventral to the anterior commissure as the pre-­ commissural fornix [3]. These fibers originate mainly from the pyramidal cells of the hippocampus. Their input is principal to the septal nuclei, the lateral pre-optica rea, the anterior part of the hypothalamus, and the nucleus of the diagonal band [1]. The pre-commissural fibers form a small compact bundle that cannot be detected grossly.

4.8.1.2 Function The fornix is the major fiber bundle involved in memory processing. Damage to this structure leads to amnesia [1].

Fig. 4.10  Dissection of the medial aspect of the hemisphere showing the various components of the limbic system. The Papez circuit begins at the hippocampus, continues as the fimbria and fornix, and terminates into the mammillary body. From the mammillary body, the mammillothalamic tract then reaches the cingulum, which turns around the splenium of the corpus callosum to end as the radiation of the cingulum into the hippocampus, thus completing the loop. (a) Hippocampus, (b) fimbria of the fornix, (c) fornix, (d) mammillary body, (e) mammillothalamic tract, (f) anterior nucleus of the thalamus, (g) thalamic radiations, (h) cingulum, (i) radiation of the cingulum

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4.8.2 Mammillothalamic and Mammillotegmental Tracts Fibers arising from the medial mammillary nucleus ascend upwards to the anterior nucleus of the thalamus to form the mammillothalamic tract of Vicq d’Azyr. Near its origin, the mammillothalamic tract gives rise to another smaller bundle known as the mammillotegmental tract, which runs posteriorly and inferiorly towards the brainstem and then terminates into the tegmental nucleus of Gudden [3] (Fig. 4.10). From the anterior nucleus of the thalamus, fibers of the anterior thalamic radiation diverge upward and mingle with the fibers of the anterior limb of the internal capsule to reach the cingulum (Latin meaning “girdle”) and the cingulate gyrus (Fig. 4.10).

4.8.3 Stria Terminalis The stria terminalis is an association fiber that connects the amygdala and the medial forebrain structures. The amygdala gives rise to two major pathways, the dorsal amygdalofugal pathway and the ventral amygdalofugal pathway [3, 20]. The stria terminalis forms the dorsal amygdalofugal pathway. It originates from the ventromedial portion of the amygdala and runs between the caudate nucleus and the thalamus around the lateral ventricle forming a C. These fibers terminate in the bed nuclei of the stria terminalis, which lies lateral to the columns of the fornix and superior to the anterior commissure. Some fibers also terminate in the hypothalamus and some join the medial forebrain bundle [3]. The bed nucleus of the stria terminalis has widespread connections to the rest of the limbic system and therefore provides an important route by which the amygdala can affect structures beyond the connections of the stria terminalis itself.

4.8.4 Stria Medullaris Thalami This fiber tract runs along the dorsomedial surface of the thalamus in the floor of the lateral ven-

tricle. It runs lateral to the lower lateral edge of the foramen of Monroe near the anterior commissure [3]. It connects the septal area with the habenula.

4.9

Surgical Implications of the Classification

We speculate that the origin of gliomas is from the white matter of the short arcuate fibers, the commissural fibers, and long association fibers in decreasing order of frequency. Despite the fact that gliomas are grouped under the term “malignant” tumors, they have a defined pattern of origin and extension. The extension is disciplined and is along a named white fiber tract, and its haphazard extension is restricted or limited by the adjoining traversing tracts. High-grade gliomas follow a similar pattern of tract involvement and confinement related to adjoining traversing tracts. The fibers around the tumor are edematous, and the edema is seen to extend along the course of the involved fiber.

4.9.1 Classification of Gliomas Based on Anatomical Understanding Based on our understanding, all gliomas (both low and high grade) could be morphologically classified into two broad categories: localized and diffuse. Localized gliomas arose from the short arcuate fibers of the involved gyrus and were named according to the gyrus they were associated with. The diffuse gliomas arose from the long association fiber bundles or the commissural fibers. As a general rule, localized gliomas remained confined to the particular gyrus that contained the involved short arcuate fibers. Some gliomas tend to involve the adjacent gyrus through the short arcuate connections between the two neighboring gyri. Gliomas that arose from the long association fibers on either side of the vertical group were confined to the respective side by the vertically coursing projection tracts (vertical group).

4  White Fibers of the Brain: A Novel Classification

Gliomas that arose medial to the vertical group remained medial to the vertical group and similarly gliomas that arose lateral to the vertical group remained lateral to it. Gliomas that arose from the commissural fibers had a predilection for a bilateral extension. Tumors that arose in the region of the genu and the forceps minor extended bilaterally anteriorly into the medial frontal brain. Tumors of the body of the corpus callosum extended bilaterally into the frontoparietal brain depending on the part of the corpus callosum that was involved. Tumors of the splenium and forceps major extended bilaterally into the medial parietooccipital lobes. Another peculiarity of the corpus callosal gliomas is that they never crossed the vertical group of fibers and remained confined medial to this group of fibers. Each of these types of glioma has been further discussed in detail.

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we advocate a safe radical piece meal excision as a total en masse resection may not be anatomically possible.

4.10 Conclusions

The precise origins, terminations, extent, and function of white matter tracts have yet to be fully characterized and understood. We present a novel method to classify these bundles based on the direction and depth of these bundles: Superficial, middle, deep, and central horizontal layers and the vertical layer. The superficial, middle, and deep layers comprise short and long association fibers, the central layer represents the commissural fibers, and the vertical layer represents the projection fibers. The anatomical classification of white fibers proposed by us was found to have implication in understanding the 4.9.2 Surgical Strategy origin and extension of both low- and high-grade gliomas. Understanding the trajectory of the Based on this anatomical knowledge and our sur- fibers makes it possible to evaluate the direction gical experience, we discuss novel surgical strat- of growth of the tumors and also provides us with egies for glioma resection. We advocate an en defined limits which the tumor will not breach. masse surgical resection for both low- and high-­ This understanding greatly aids in safe radical grade localized gliomas arising from the short excision of the glial tumors. arcuate fibers. A clear plan of dissection was available for most of these gliomas during surgery. This strategy of resection is actually a References supramarginal resection as the glioma is only localized to that region. This kind of resection is 1. Shah A, Goel A, Jhawar S, Patil A, Rangnekar R, Goel A.  The neural circuitry: architecture and funcpossible without using any kind of fluorescence tion, a fiber dissection study. Biosphere Neurosurg. as the complete lesion is removed en masse. This 2019;125:e620–38. holds true for all localized gliomas except for 2. Klingler J.  Erleichterung der makroskopischen Praeparation des Gehirnsdurchden Gefrier prozess those in the insula where an en masse resection is Schweiz. Arch Neurol Psychiatry. 1935;36:247–56. difficult due to the presence of the branches of 3. Shah A, Jhawar SS, Goel A.  Analysis of the anatthe middle cerebral arteries. omy of the Papez circuit and adjoining limbic system by fiber dissection techniques. J Clin Neurosci. Even tumors that arise from short arcuate 2012;19(2):289–98. fibers in eloquent cortical locations were local 4. Fernández-Miranda JC, Rhoton AL Jr, Alvarez-­ ized and could be excised by identification of a Linera J, Kakizawa Y, Choi C, de Oliveira EP. Three-­ well-defined plain of resection. The eloquent cordimensional microsurgical and tractographic anatomy of the white matter of the human brain. Neurosurgery. tex was seen to be displaced by the growth of the 2008;62(6 Suppl 3):989–1026; discussion 1026–8. tumor in low-grade tumors and in majority of 5. Fernandez-Miranda JC, Pathak S, Engh J, Jarbo K, high-grade tumors. A tailored resection was used Verstynen T, Yeh FC, et al. High-definition fiber tracfor tumors when the eloquent cortex was intraoptography of the human brain: neuroanatomical validation and neurosurgical applications. Neurosurgery. eratively mapped to be in close vicinity to the 2012;71(2):430–53. tumor. For diffuse tumors from the long tracts,

36 6. Yagmurlu K, Vlasak AL, Rhoton AL Jr. Three-­ dimensional topographic fiber tract anatomy of the cerebrum. Neurosurgery. 2015;11(Suppl 2):274–305; discussion 305. 7. Shah A, Goel A, Patil A, Goel A. Letter to the Editor. Superior longitudinal fasciculus. J Neurosurg. 2019;132:1309–11. 8. Makris N, Kennedy DN, McInerney S, Sorensen AG, Wang R, Caviness VS Jr, et al. Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in  vivo, DT-MRI study. Cereb Cortex. 2005;15(6):854–69. 9. Kamali A, Flanders AE, Brody J, Hunter JV, Hasan KM.  Tracing superior longitudinal fasciculus connectivity in the human brain using high resolution diffusion tensor tractography. Brain Struct Funct. 2014;219(1):269–81. 10. Makris N, Papadimitriou GM, Sorg S, Kennedy DN, Caviness VS, Pandya DN. The occipitofrontal fascicle in humans: a quantitative, in vivo, DT-MRI study. Neuroimage. 2007;37(4):1100–11. 11. Güngör A, Baydin S, Middlebrooks EH, Tanriover N, Isler C, Rhoton AL Jr. The white matter tracts of the cerebrum in ventricular surgery and hydrocephalus. J Neurosurg. 2017;126(3):945–71. 12. Jones DK, Catani M, Pierpaoli C, Reeves SJ, Shergill SS, O’Sullivan M, et al. A diffusion tensor magnetic resonance imaging study of frontal cortex connections in very-late-onset schizophrenia-like psychosis. Am J Geriatr Psychiatry. 2005;13(12):1092–9. 13. Hickok G, Poeppel D.  Towards a functional neu roanatomy of speech perception. Trends Cogn Sci. 2000;4:131–8. 14. Maldonado IL, de Champfleur NM, Velut S, Destrieux C, Zemmoura I, Duffau H. Evidence of a middle longitudinal fasciculus in the human brain from fiber dissection. J Anat. 2013;223(1):38–45. 15. Bruni J E, Montemurro D.  Human neuroanatomy: a text, brain atlas and laboratory dissection guide, Oxford University Press; 2009.

A. Shah et al. 16. Schmahmann JD, Pandya DN.  The complex history of the fronto-occipital fasciculus. J Hist Neurosci. 2007;16(4):362–77. 17. Almairac F, Herbet G, Moritz-Gasser S, de Champfleur NM, Duffau H. The left inferior fronto-­ occipital fasciculus subserves language semantics: a multilevel lesion study. Brain Struct Funct. 2015;220(4):1983–95. 18. Kier LE, Staib LH, Davis LM, Bronen RA. mr imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer’s loop of the optic radiation. Am J Neuroradiol. 2004;25(5):677–91. 19. Peltier J, Verclytte S, Delmaire C, Pruvo JP, Godefroy O, Le Gars D. Microsurgical anatomy of the temporal stem: clinical relevance and correlations with diffusion tensor imaging fiber tracking. J Neurosurg. 2010;112(5):1033–8. 20. Shah A, Jhawar SS, Goel A. Letter to the editor: optic radiations and anterior commissure. J Neurosurg. 2015;123(3):824–6. 21. Wilde EA, Bigler ED, Haider JM, Chu Z, Levin HS, Li X, et al. Vulnerability of the anterior commissure in moderate to severe pediatric traumatic brain injury. J Child Neurol. 2006;21(9):769–76. 22. Goel A, Shah A, Ramdasi R, Patni N.  Orbital cortical approach to lesions around the frontal horn of the lateral ventricle: indication and surgical parameters. Acta Neurochir (Wien). 2014;156(4):825–30. 23. Ribas GC.  The cerebral sulci and gyri. Neurosurg Focus. 2010;28(2):E2. 24. Wen HT, Rhoton AL Jr, de Oliveira E, Cardoso AC, Tedeschi H, Baccanelli M, et al. Microsurgical anatomy of the temporal lobe: part 1: mesial temporal lobe anatomy and its vascular relationships as applied to amygdalohippocampectomy. Neurosurgery. 1999;45:549–92.

5

Computational Fluid Dynamics in Cerebral Aneurysms Ahmed Ansari, Ishu Bishnoi, and Gowtham Devareddy

5.1

Introduction

Gonzalez et  al. published the first article which applied CFD to the field of aneurysm research, in 1992. Despite its conclusion that “computer modeling can further our understanding of factors that determine the origin and progression of intracranial aneurysms”, it was after a decade before CFD took off as a tool for studying cerebral aneurysms [1]. Over the last decade, a huge number of publications have come over, as the understanding of image-based CFD studies has grown. Virtual simulations have changed from idealized geometries to patient-specific geometries, and from steady-state flow to pulsatile flow [2]. Computation-based models provide an attractive method of investigating intra-luminal flow dynamics by providing the ability to theoretically model and study any possible geometry.

A. Ansari (*) Department of Neurosurgery, UP University of Medical Sciences, Saifai, UP, India Department of Neurosurgery, Fujita Health University Bantane Hospital, Nagoya, Japan I. Bishnoi Maharaja Agrasen Medical College, Agroha, Haryana, India G. Devareddy Dr Rela Institute and Medical Centre, Chennai, Tamil Nadu, India

5.2

CFD Methodology

It is done by the application of software “Hemoscope”. There are basic steps [3]: Image processing: The first step is to download a 3D CT angiography image of cerebral arteries. Geometry processing: The parent artery with aneurysm and its branches originating near the aneurysm are isolated after carefully removing the rest vessels or artifacts. Meshing: The clear image of the parent artery, aneurysm, and main branches is then used for the application of “Hemoscope”. Cross-sectional areas are marked at the entrance and the exit of blood and respective markings are marked. Flow solution and visualization: Application of software then generates colourful images of flow and generates fluid dynamic parameters. There are four parameters, which we study to find aneurysm wall thickness, impending area of rupture, and pressure. These are the following: 1 . Wall shear stress magnitude—WSSm 2. Wall shear stress vector—WSSv 3. Streamline flow and velocity 4. Pressure (circumferential) Wall shear stress: Blood flow inside a vessel is fastest at the centre and slowest close to the wall, assuming a parabola, referred as “laminar flow” profile.

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 Y. Kato et al. (eds.), Recent Progress in the Management of Cerebrovascular Diseases, https://doi.org/10.1007/978-981-16-3387-4_5

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This pattern of flow is the result of friction between blood flow and the vessel wall. This friction creates a tangential force exerted by the flowing fluid and is referred to as the wall shear stress. Wall shear stress importance • Magnitude—High WSSm means the flow is fast near endothelium. Low WSSm means slow flow near endothelium [4]. • Clinical importance—Low WSSm proximal to the stenosis leads to the formation of atherosclerotic lesions. It affects mostly intima [4]. • A high grade of shear stress increases wall thickness and expands the vessel’s diameter so that shear stress values return to their normal values. So, there are stable media and smooth muscle hyperplasia [4]. WSS vector: It indicates the direction of shear stress at the wall. Usually, parallel vectors are in the straight vessel, while convergent and divergent vectors are found at: • Turn or branching. • Stenotic (thick) or dilated areas (thin). Change in the direction of the vector in the straight vessel could be due to external factors like compression/traction of the vessel. Pressure: It is the force of blood column on the arterial wall circumferentially leading to stretching/stress on all wall layers. In shear stress, mostly intima is affected. Clinical importance—High pressure leads to remodelling of the vessel wall, athero- or arteriosclerosis. Streamline flow: Streamline flow is the measurement of the pattern of blood flow and velocity. Flow can be streamlined at low-velocity, straight vessel. Flow can be turbulent because of fast velocity, turn, closed end, and stenosis. It leads to high WSSm and change in WSSv.

5.3

Illustrative Cases

5.4

Results and Discussion

5.4.1 B  lood Flow Modelling with Theoretical Physics All vessels can become aneurismal; therefore, deformation is part of the minimalization of wall stress. Laplace’s law dictates that wall stress in spherical coordinates is half of the stress in cylindrical systems, and as a result, all vessels under stress will naturally seek a new spherical set point. Blood is mathematically modelled as a continuous incompressible fluid. The governing equations are the unsteady 3D Navier-Stokes equation, which is written as.



  ut  u u   p     F  u  0

where u is the velocity fluid, ρ is the density, p is the pressure, τ the deviatoric stress tensor, and F represents any externally applied body forces, such as gravity. Viscosity in cylindrical tubes (approximately three vessel diameters in length added to each outlet boundary) is adjusted to achieve the desired resistance value. Using Poiseuille’s formula, the pressure drop in the tube is represented as

p  Q  R

where ∆p is the pressure drop, Q is the flow rate, and R the resistance, given by

R  8  L a 4

where μ is the viscosity, L is the length of the tube, and a is the radius. With each reduction in tension and the formation of an aneurysm, there is also a subsequent reduction in the wall thickness. As the wall tension further increases, and moreover within the vessel

5  Computational Fluid Dynamics in Cerebral Aneurysms

a

39 hemoscope 2015

Pressure Var mmHg 10.461

WSS Vec inst

10.444

10.426

10.408

WSS Mag Inst Pa 7.964

5.312

2.660

0.008

Velocity m/s 0.185

0.123

0.062

0.000

b

Fig. 5.1 (a) CFD analysis of an IC aneurysm with a circular neck with streamline flow covering the whole aneurismal dome and increased pressure, (b) per operative photograph showing a thinned wall aneurysm

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40 Syncronized image

a

Pressure Inst mmHg 84.482

hemoscope 2015

WSS Vec inst

84.408

84.333

84.259

WSS Mag Inst Pa 21.990

Velocity m/s 0.296

14.666

0.197

7.343

0.099

0.019

0.000

b

Fig. 5.2 (a) CFD analysis of MCA aneurysm with a circular neck showing flow throughout the dome and increased pressure with low WSS, (b) intraoperative pho-

tograph showing a thinned wall aneurysm (inset showing endoscopic visualization of thinned wall aneurysm with perforators)

and inside the aneurysm, there is a further modification in the shape of an aneurysm. This sequence of events will keep on occurring, and the wall thickness reduces with each such change. Further, with approximately the third such event, the reduc-

tion in wall thickness and the increase in tension inside the aneurysm increase to an extent that the aneurysm ruptures. It can be explained by an analogy that to hang a mass on a cable with less sag, one needs to put more tension in the cable.

5  Computational Fluid Dynamics in Cerebral Aneurysms

Fig. 5.3  CFD of MCA aneurysm with an elliptical neck showing streamline flow not covering the entire dome of the aneurysm with low pressure pointing towards a thicker wall, and inset: confirming the presence of thick wall of the aneurysm

41

5.4.2 Aneurysmal Neck as the Deciding Factor

Fig. 5.4  CFD of anterior communicating artery aneurysm with an elliptical neck and low pressure with low WSS, and inset showing the presence of varied thickness of the wall. At times, the CFD software is unable to take into account very thin vessels of the anterior cerebral artery

We took elliptical and circular neck for aneurysms in terms of their simplicity and all practical purposes. For elliptical necks, the main flow from the parent artery strikes at the downstream side and enters inside the aneurysm and eventually creates a vortex in only a small portion. In the elliptical necks, the pressure is usually low. For the circular neck, the flow from the parent artery occupies nearly the whole dome of the aneurysm, with pressure inside the aneurysmal dome found

high on CFD studies. WSSm was usually low in circular neck aneurysms; however, with elliptical necks, WSS was found either high or low. Although again, the diameter of the aneurysm neck has a huge say on the turbulency and overall pressure inside the aneurismal dome. As the diameter of the neck increases, so does the reduction in thickness of the aneurismal wall and an overall increased chance of aneurysm rupture.

42

A. Ansari et al.

Fig. 5.5  CFD of two IC aneurysms with circular necks having flow covering the entire dome with high pressure, and inset showing a thinned wall aneurysm

5.4.3 Pattern in Ruptured Aneurysms Ruptured aneurysms tend to have complex and/or unstable flow patterns, concentrated inflow jets, and small impingement regions. Conversely, unruptured aneurysms were more likely to have simple stable flow patterns, broad or diffuse inflow jets, and large impaction zones.

Fig. 5.6  CFD analysis of MCA aneurysm with circular aneurysm neck showing flow in a small portion of the aneurysm with high pressure inside and low WSS and inset showing a thin-walled fundus

aneurysm has formed, further course is decided based upon whether WSS is high or low. If the WSS is high, it causes degeneration of cellular matrix and cell apoptosis, and they may rupture even if the aneurysm is small in size. Qian et al. [6] reported CFD analysis of prerupture imaging in which rupture occurred dur5.4.4 Wall Shear Stress as Deciding ing follow-up of observed unruptured aneurysms. Factor They found high energy loss was a risk factor for rupture. Takao et al. [7] analyzed the largest numMeng et  al. [5] indicated that high WSS and a ber of ruptured and unruptured aneurysms using positive WSS gradient can trigger mural cell-­ the images taken before rupture for ruptured mediated destructive remodelling, and low WSS cases. They performed CFD analysis for 100 and a high OSI can trigger inflammatory cell-­ aneurysms, including 87 unruptured and 13 rupmediated destructive remodelling. Initially, high tured aneurysms of the internal carotid artery WSS at the blood flow jet impingement zone is (ICA) and MCA.  For the ruptured aneurysms, related to the initiation of aneurysm. Once the they were able to perform CFD analysis using the

5  Computational Fluid Dynamics in Cerebral Aneurysms

images that were taken before their rupture because the aneurysms ruptured during observation. They hypothesized that a region with high pressure loss coefficient (PLc) undergoes aneurysmal growth to change its shape in order to avoid interfering with and adapting to the blood flow. This is the “remodelling process” that eventually will reach a stable hemodynamic condition and thereafter will transition from a low to a high risk of rupture. Kadasi et  al. [8] evaluated the surgical findings of aneurysmal wall condition and the role of WSS. They found that a thin wall was associated with low WSS. Suzuki et al. [9] reported surgical findings of wall condition and CFD parameters in 50 MCA aneurysms. They found that the maximum PD corresponded to aneurysmal thin-walled regions in 82.0% of the 50 MCA aneurysms, identified during craniotomy. We have found a huge correlation of the pressure changes with regard to the aneurysm wall thickness: thinned wall, which was mainly identified per operatively with the presence of swirling of blood inside the aneurysm, and thick wall, which didn’t show any swirl pattern of blood and along with yellowish wall (probably atherosclerotic bear no direct relation with the WSS magnitude). There was an increased pressure change inside the aneurysm in comparison with the proximal parent artery favoured towards a thin-walled aneurysm. There was another category which showed mixed pattern distribution of pressure changes inside the aneurysm. These were the ones which showed thinned and atherosclerotic walls on intraoperative finding, with the presence of bleb most commonly at the site of the thinned wall, or portion showing increased pressure changes. We found the role of high WSS in the initiation of aneurysm. Once the aneurysm has been formed, the further course is decided based on the pressure changes inside the aneurysm. Change in pressure bears a direct relation to the flow rate and resistance; hence, even a cyclical change in flow rate, as in hypertensive individuals, bears a huge effect on the pressure change, leading to the formation of bleb or rupture. Also, resistance bears a direct relation to the aneurismal neck radius. The more the size of the neck

43

radius, more is the resistance towards the flow and increased change in pressure, leading to the formation of bleb or rupture.

5.5

Limitations of CFD Studies

In almost all CFD studies involving a large number of aneurysms, no biological information is utilized. Only morphological data, without the input of actual blood pressure, blood viscosity, and the dynamic change in those biological factors, were considered. Blood is assumed to be a Newtonian fluid in most simulations for cerebral arteries. Hippelheuser et al. [10] investigated the effect of assuming a constant viscosity for cases with a bleb and found that the non-Newtonian viscosity model highlighted the hemodynamic differences induced by the presence of a bleb and improved the discriminant statistics in rupture prediction. Suzuki et  al. [11] first compared the CFD simulation results of the Newtonian viscosity model with those of actual viscosity data obtained from blood sample data of healthy volunteers. They concluded that CFD using either the common Newtonian or non-Newtonian viscosity assumption could lead to values different from those of the patient-specific viscosity model for hemodynamic parameters such as WSS.

References 1. Gonzalez CF, Cho YI, Ortega HV, Moret J. Intracranial aneurysms: flow analysis of their origin and progression. Am J Neuroradiol. 1992;13:181–8. 2. Robertson AM, Watton PN.  Computational fluid dynamics in aneurysm research: critical reflections, future directions. Am J Neuroradiol. 2012;33(6):992– 5. https://doi.org/10.3174/ajnr.A3192. 3. Cebral J, Mut F, Sforza D, Löhner R, Scrivano E, Lylyk P, Putman C.  Clinical application of image-­ based CFD for cerebral aneurysms. Int J Numer Method Biomed Eng. 2011;27(7):977–92. https://doi. org/10.1002/cnm.1373. 4. Thim T, et al. Wall shear stress and local plaque development in stenosed carotid arteries of hypercholesterolemic minipigs. J Cardiovasc Dis Res. 2012;5:76–83. 5. Meng H, Tutino VM, Xiang J, et  al. High WSS or low WSS? Complex interactions of hemodynamics

44 with intracranial aneurysm initiation, growth, and rupture: toward a unifying hypothesis. AJNR Am J Neuroradiol. 2014;35:1254–62. 6. Qian Y, Takao H, Umezu M, et  al. Risk analysis of unruptured aneurysms using computational fluid dynamics technology: preliminary results. AJNR Am J Neuroradiol. 2011;32:1948–55. 7. Takao H, Murayama Y, Otsuka S, et al. Hemodynamic differences between unruptured and ruptured intracranial aneurysms during observation. Stroke. 2012;43:1436–9. 8. Kadasi LM, Dent WC, Malek AM.  Colocalization of thin-walled dome regions with low hemodynamic wall shear stress in unruptured cerebral aneurysms. J Neurosurg. 2013;119:172–9.

A. Ansari et al. 9. Suzuki T, Takao H, Suzuki T, et al. Determining the presence of thin-walled regions at high-pressure areas in unruptured cerebral aneurysms by using computational fluid dynamics. Neurosurgery. 2016;79:589–95. 10. Hippelheuser JE, Lauric A, Cohen AD, et al. Realistic non-Newtonian viscosity modelling highlights hemodynamic differences between intracranial aneurysms with and without surface blebs. J Biomech. 2014;47:3695–703. 11. Suzuki T, Takao H, Suzuki T, et  al. Variability of hemodynamic parameters using the common viscosity assumption in a computational fluid dynamics analysis of intracranial aneurysms. Technol Health Care. 2017;25:37–47.

6

Carotid Endarterectomy: Surgical Nuances Raja K. Kutty, Saurabh Sharma, and Jijo J. Joseph

6.1

Introduction

Atherosclerotic disease of the cervical part of ICA is responsible for 20–40% of ischemic strokes [1]. The prevalence of significant asymptomatic carotid stenosis in the general population varies from 0% to 3.1%. [2] Most patients are generally asymptomatic and have a risk of stroke of 1.5% per year and 7.5% per 5  years [3]. Symptomatic carotid artery stenosis usually presents with neurological dysfunctions in the form of transient ischemic attacks, amaurosis fugax, and various forms of stroke. These patients have an increased risk of recurrent cerebrovascular events.

6.2

History

Any attempt at intervention on the carotid arteries was performed in Buenos Aires in 1951 by Carré, Mollins, and Murphy. In 1953, Strully et  al. performed ligation and resection of the internal carotid artery [4]. DeBakey performed the first eversion carotid endarterectomy (CEA), in 1953 [5].

R. K. Kutty (*) · J. J. Joseph Department of Neurosurgery, Government Medical College, Thiruvananthapuram, Kerala, India S. Sharma SGT Medical College, Gurgaon, Haryana, India

6.3

Preoperative Evaluation

Duplex ultrasound is the most appropriate first test in patients suspected of having symptomatic carotid artery stenosis. Computed tomography angiography (CTA) or magnetic resonance angiography (MRA) is done when duplex findings are inconclusive, despite clinical suspicion, using one of the modalities. After clinical examination and imaging, the extent of stenosis is graded as normal/70% and attenuates stress response, but there is a lack stenosis. The ACAS [14] and ACST [15] studies of direct neurological monitoring during the prohave recommended CEA in asymptomatic cedure. The use of regional anesthesia allows patients with >60% stenosis. direct real-time neurological monitoring, avoids Contraindications the risks of airway intervention, reduces shunt A complete ipsilateral disabling stroke. rate, and reduces hospital stay. Disadvantages Relative contraindications include the chance of conversion to GA during Atypical anatomy such as: surgery, risks associated with sitting blocks (deep cervical plexus blockade), restricted access to the High bifurcation. airway during surgery, patient stress/pain causing Hemodynamically relevant tandem lesions. increased risk of myocardial ischemia, and need Radiation-induced stenosis and recurrent disease. for patient cooperation. Measures for cerebral Poor renal, cardiac, and pulmonary function. protection and monitoring are routine. Most studies also show significantly worse outThe patient is typically placed supine, with comes in patients >75 years of age. some mid-shoulder elevation with 10–15 degrees

6  Carotid Endarterectomy: Surgical Nuances

head rotation to the contralateral side with gentle extension at the craniocervical joint. Gentle overextension opens up the anterior triangle of the neck. Avoid too much rotation as it will cause IJV to come anterior to CA during dissection. Venous return can be optimized by some reverse Trendelenburg position. Antiseptic solution is applied carefully as this can provoke manual dislodgment of emboli. The incision is marked at the anterior border of the sternocleidomastoid muscle and curved posteriorly toward the mastoid process to avoid the marginal mandibular branch of the facial nerve. The length of incision depends upon the length of the plaque segment. The incision begins about 1 cm below the tip of the mastoid, curves 1 cm below the angle of the mandible, and ends 1  cm above the sternoclavicular joint. After dividing the superficial fat, the platysma muscle is identified and divided longitudinally (Fig. 6.2). Often, external jugular vein lies just beneath the platysma and may require suture ligation. Deep to the platysma lies a fat layer containing tributaries of the IJV and glandular tissue superiorly, which overlies the sternocleidomastoid muscle. The anterior border of this layer is the critical landmark for early dissection. Care should be taken to stay below the submandibular gland and adjacent lymph nodes. The dissection proceeds along the medial belly of SCM.  The jugular vein is identified between the soft tissue planes of SCM and midline swallowing muscles. Mobilize jugular vein laterally and divide any tributary if required. After making it free, displace the jugular vein to find the carotid sheath. The inferior extent of exposure is marked by omohyoid, and the superior extent of exposure is the posterior belly of the digastric muscle. The hypoglossal nerve (XII) is at risk during the dissection and should be protected. It always lies superficial to the ECA and ICA, just below the digastric muscle. Dissect soft-tissue planes between the carotid artery and jugular vein. Isolate carotid sheath using a tonsil clamp. The carotid sheath is opened

47

Fig. 6.2  Operative picture after the division of platysma muscle

at this stage of the procedure, and harsh manipulation may cause the dislodgement of plaque in surgery; therefore, intravenous heparinization (5000  U) is recommended at this stage. The carotid sheath is opened with a vertical incision. The ansa cervicalis is usually found superiorly over the carotid artery and vagus nerve along the deep and lateral surface of the carotid artery (between the carotid artery and jugular vein). Dissection deep to the carotid bifurcation should be trauma-less and in planes to avoid injury to the superior laryngeal branch of the vagus nerve. Injury to the superior laryngeal branch may result in significant dysphagia in the postoperative period. The carotid artery is dissected circumferentially free of its sheath. Omohyoid muscle can be divided as per the level of bifurcation. Before manipulation of the carotid artery in the region of the bifurcation, lidocaine (1% Xylocaine) without epinephrine is instilled into the carotid sinus and along the course of the nerve of Hering to minimize bradycardia and hypotension resulting from stimulation of these structures (Fig. 6.3). Prepare an adequate segment of the CCA; then, prepare the ECA and ICA with vessel loops for cross-clamping. The blood pressure is ­maintained at or slightly above awake baseline, and the electroencephalography results are examined. The shunt tubing is filled with heparinized

R. K. Kutty et al.

48

Fig. 6.3  The carotid sheath with the carotid bifurcation

saline and clamped to ensure that there are no intraluminal bubbles, and it is compared with the internal carotid artery to ensure proper sizing. The internal carotid artery is clamped first to prevent any embolic episode. The artery is clamped distal to plaque. The common carotid artery and the external carotid artery are clamped in this order. The clamp test: If LA or intraoperative EEG is used for selective shunting, then a clamp test distal to ICA has to be applied for at least 3 min to check for changes in the neurological examination and EEG pattern. If such changes occur, then the artery should be unclamped to allow reperfusion before re-clamping and an opening carotid artery to place a shunt as shunt placement takes 2–3 min and cannot be done on an already ischemic brain.

6.6

Exposure for a High Bifurcation or Plaque

High carotid bifurcation means plaque extends above the level of C3. Here, we can extend the incision cephalad to the mastoid tip, curving along the earlobe by going forward and inferior in the postauricular sulcus, ending superiorly in the pre-tragal skin crease.

6.7

Arteriotomy and Endarterectomy

An arteriotomy is started about 1 cm proximal to the bifurcation in the midline of the common carotid artery using a #11 blade. The electroen-

cephalogram is again examined to determine whether shunt placement is necessary. If no changes have occurred, dissection is carried distally along with the plaque with an angled Pott’s scissors. Dissection must be carried to at least 1 cm distal to the end of the plaque to allow for posterior wall extension and placement of a shunt, if necessary. The incision is carried through the arterial wall until plaque is encountered, and a smooth plane is developed between plaque and artery wall. If any changes occur in EEG, a shunt is inserted into the distal internal carotid artery, taking care not to cause dissection of the intima or embolization of debris distally. The proximal end of the shunt is placed in the common carotid artery to reestablish distal blood flow.

6.8

Closure

The arteriotomy is closed primarily or with a patch using a continuous suture. Although the patch closure of the arteriotomy is a risk for increasing the carotid clamp time, it reduces the risks for perioperative arterial occlusion and ipsilateral stroke. Different patch materials, such as bovine pericardium and vein, polyethylene terephthalate, and polytetrafluoroethylene, are used for the patch closure. Alternatively, external jugular and facial veins may be used, saving the saphenous vein for use in other vascular procedures. If a shunt has been placed, the distal end of the shunt is removed first. Just before final suturing at the proximal end of the arteriotomy, the internal carotid artery clamp is briefly released. The resulting backflow of blood ensures that the artery is patent and flushes any residual debris from the lumen. The superior thyroid artery clamp is removed as the final suture is placed to have continuous backflow of blood. The clamps are then removed in the following order: external carotid artery–common carotid artery–internal carotid artery. This sequence ensures that any potential embolic material is flushed into the external artery circulation. Thrombin-soaked cellulose foam is applied to the vessel to seal any residual needle puncture sites, and gentle pres-

6  Carotid Endarterectomy: Surgical Nuances

49

Fig. 6.4  Various steps of CEA

sure is applied to the wound with a sponge for about 1  min. Hemostasis should be achieved before closure (Fig. 6.4). Intraoperative Doppler or USG may be used to assess the repair and the blood flow velocity in the sutured vessel. Recently, the use of intraoperative in vivo optical spectroscopy (INOS) [16] to measure cerebral oximetry (CO) has become popular. For this, initially, a baseline recording of CO is recorded. After this, a temporary clamp is placed over the ipsilateral ICA for about 30 s and is monitored for any significant reduction in the CO recording. The presence of a significant fall in CO warrants a shunt placement before arteriotomy. The use of shunt helps to preserve blood circulation to the brain and thus significantly reduce the perioperative morbidity and mortality. CO has been found to be more accurate than TCD in predicting the need for carotid shunting [17]. INOS uses infrared light in the range of 650– 1100  nm [18, 19] and detects the hemoglobin

oxygen saturation of blood in the brain noninvasively. The use of dual-image video angiography helps in visualizing the extent of the plaque so that the arteriotomy can be made accordingly.

6.9

Comparison of Conventional and Eversion Carotid Endarterectomy

EVEREST (EVERsion carotid Endarterectomy versus Standard Trial study)—There were no statistically significant differences in outcomes between the two techniques. However, a slightly higher incidence of perioperative complications was noted with eversion CEA and a slightly higher incidence of restenosis with standard CEA. EVEREST trial demonstrated that patients who underwent eversion CEA had a lower inci-

R. K. Kutty et al.

50

dence of restenosis than standard CEA (patch and primary closure), but standard CEA with patch angioplasty had the lowest incidence of neurological complications and the lowest rate of restenosis—1.5%—versus 2.8% for eversion CEA and 7.9% for standard CEA with primary closure.

6.10 Complications of CEA Major Complications: Myocardial infarction, hyperperfusion syndrome, cranial nerve injury, perioperative stroke, restenosis, death Minor Complications: TIA, infection, dysphagia. Bleeding

6.11 Management of Complications All patients should be observed in an intensive care unit for 24–48  h after the procedure. A sequential neurological examination should be carried out. Blood pressure should be rigidly controlled in the approximate preoperative range with continuous monitoring by arterial catheter. Intravenous fluids, inotropic agents, and antihypertensive agents are routinely administered if required. Postoperative electrocardiography and chest radiography should be performed for all patients. Urine output and serum electrolytes are monitored during the period of intensive care. The cervical wound is repeatedly examined for enlargement or superficial bleeding. Aspirin therapy is initiated immediately after surgery, and stable patients are usually discharged to home within 3–5 days. Cerebral Hyperperfusion Syndrome: This is a relatively rare but potentially preventable condition, seen after carotid endarterectomy (CEA) or carotid artery stenting (CAS), and is described as focal cerebral damage following a revascularization procedure, usually as a result of hyperperfusion. Bouri et  al. suggest the following four criteria [20]:

1 . Occurrence within 30 days post-CEA. 2. Clinic features such as new-onset headache, seizure, hemiparesis, and Glasgow coma scale (GCS) 100% of perioperative values) on imaging studies (e.g., transcranial doppler, single-photon emission computerized tomography (SPECT) or magnetic resonance perfusion (MRP)) or systolic blood pressure >180 mmHg. 4. No evidence of new cerebral ischemia, postoperative carotid occlusion, and metabolic or pharmacologic cause (Table 6.1). Table 6.1  Management of complications 1.  Mean arterial BP >15 mmHg: Start β-blockers/ vasodilators 2.  New post-op neurological deficit: NCCT head No hemorrhagic bleed on NCCT head: Cerebral angiography to evaluate  •  Endarterectomy site.  •  Collateral circulation.  •  Intracranial emboli. If endarterectomy patent with distal emboli: Heparin anticoagulation If acute occlusion of ICA: Shift to OT Hemorrhagic bleed: If insignificant, manage conservatively    If significant, shift to OT 3. Postoperative neck hematoma: Exploration in OT

Trials comparing CAS and CEA Trials CAVATAS [2002]

Results Both symptomatic and asymptomatic patients included. CAS CEA 6.40% 5.90% Periprocedural disabling stroke/ deaths Death 10% 10% Cranial Neuropathy 0% 8.70% Groin/Neck 1.20% 6.70% Hematoma Re-stenosis at Similar Similar 1 year Re-stenosis at 30.70% 10.50% 3 year

6  Carotid Endarterectomy: Surgical Nuances Trials SAPPHIRE [2004]

EVA 3S [2006]

SPACE [2006]

ICSS [2010]

CREST [2010]

ACT-1 [2016]

Results Death/stroke/MI Similar Similar within 30 days Similar Similar Death/ipsilateral stroke between 31 days and 1 year Similar Similar Rate of restenosis requiring intervention at 3 year Symptomatic patients included, and the trial stopped prematurely due to high incidence of periprocedural stroke/death with CAS Symptomatic patients included Periprocedural 6.84% 6.34% complication rate. Recurrent More Less restenosis 8.50% 5.20% Periprocedural stroke, death or MI 8.5% 5.2% Risks of any stroke More Less and all-cause death Long term Similar Similar restenosis rates Periprocedural 4.10% 2.30% strokes Periprocedural MI/ Less More CN neuropathy Stroke/death/MI Similar Similar rates at 10 years Restenosis rates Similar Similar Asymptomatic patients were included 3.80% 3.40% Periprocedural stroke/deaths/MI within 1 year Postprocedurestroke Similar Similar /death rate at 5 years 5 years stroke-free Similar Similar survival

Most of these trials show similar complication rates and survival rates on comparing these two techniques.

6.12 Conclusion CEA provides better protection from stroke than medical therapy in patients with asymptomatic and symptomatic patients with carotid artery disease. Its success requires a careful patient and technique selection along with good knowledge

51

of the surgical anatomy of the area. It is a technique that is undergoing a lot of advancements and modifications, but the conventional CEA has proven its efficacy time and again.

References 1. In Eskandari MK, Pearce WH, Yao JST.  Modern trends in vascular surgery: Carotid Artery Disease. 1st ed. Shelton, CT: People Medical Publishing House USA; 2010. Chapter 21: Contemporary carotid endarterectomy results in the United States; p.199. 2. Clinical advisory: carotid endarterectomy for patients with asymptomatic internal carotid artery stenosis. Stroke. 1994;25(12):2523–4. 3. Wiebers DO, Whisnant JP, Sandok BA, O’Fallon WM. Prospective comparison of a cohort with asymptomatic carotid bruit and a population-based cohort without carotid bruit. Stroke. 1990;21(7):984–8. 4. Strully KJ, Hurwitt ES, Blankenberg HW. Thrombo-­ endarterectomy for thrombosis of the internal carotid artery in the neck. J Neurosurg. 1953;10(5):474–82. 5. De Bakey ME, Crawford ES, Cooley DA, Morris GC.  Surgical considerations of occlusive disease of innominate, carotid, subclavian, and vertebral arteries. Jr Ann Surg. 1959;149(5):690–710. 6. Grant EG, Benson CB, Moneta GL, et  al. Carotid artery stenosis: gray-scale and Doppler US diagnosis-­ Society of Radiologists in ultrasound consensus conference. Radiology. 2003;229(2):340–6. 7. Hathout GM, Fink JR, El-saden SM, et al. Sonographic NASCET index: a new doppler parameter for assessment of internal carotid artery stenosis. AJNR Am J Neuroradiol. 2005;26(1):68–75. 8. Lal BK, Hobson RW 2nd, Goldstein J, et al. In-stent recurrent stenosis after carotid artery stenting: life table analysis and clinical relevance. J Vasc Surg. 2003;38(6):1162–9. 9. Lal BK, Hobson RW 2nd, Goldstein J, et al. Carotid artery stenting: is there a need to revise ultrasound velocity criteria? J Vasc Surg. 2004;39(1):58–66. 10. Stanziale SF, Wholey MH, Boules TN, Selzer F, Makaroun MS.  Determining in-stent stenosis of carotid arteries by duplex ultrasound criteria. J Endovasc Ther. 2005;12(3):346–53. 11. Nederkoorn PJ, Brown MM. Optimal cut-off criteria for duplex ultrasound for the diagnosis of restenosis in stented carotid arteries: review and protocol for a diagnostic study. BMC Neurol. 2009;9:36. 12. North American symptomatic carotid endarterectomy trial methods, patient characteristics, and progress. Stroke. 1991;22:711–20. 13. Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of the MRC European carotid surgery trial (ECST). Lancet. 1998;351:1379–87.

52 1 4. Endarterectomy for asymptomatic carotid artery stenosis. Executive Committee for the Asymptomatic Carotid Atherosclerosis Study. JAMA. 1995;273:1421–8. 15. Halliday A, Mansfield A, Marro J, MRC Asymptomatic Carotid Surgery Trial (ACST) Collaborative Group, et al. Prevention of disabling and fatal strokes by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial. Lancet. 2004;363:1491–502. 16. INVOS Monitor serial number; 2013. Available from: http://www.covidien.com. 17. Ali AM, Green D, Zayed H, Halawa M, El-Sakka K, Rashid HI, et  al. Cerebral monitoring in patients undergoing carotid endarterectomy using a triple

R. K. Kutty et al. assessment technique. Interact Cardiovasc Thorac Surg. 2011;12:454–7. 18. McCormick PW, Stewart M, Lewis G, Dujovny M, Ausman JI. Intracerebral penetration of infrared light. Technical note. J Neurosurg. 1992;76:315–8. 19. de Letter JA, Sie TH, Moll FL, Algra A, Eikelboom BC, Ackerstaff GA, et  al. Transcranial cerebral oximetry during carotid endarterectomy: agreement between frontal and lateral probe measurements as compared with an electroencephalogram. Cardiovasc Surg. 1998;6:373–7. 20. Bouri S, Thapar A, Shalhoub J, Jayasooriya G, Fernando A, Franklin IJ, Davies AH. Hypertension and the postcarotid endarterectomy cerebral hyperperfusion syndrome. Eur J Vasc Endovasc Surg. 2011;41(2):229–37.

7

Blister Aneurysm of Middle Cerebral Artery Bifurcation (Case Report and Review) Yan Zhao and Zhilin Guo

7.1

Introduction

The term “blood blister aneurysm” (BBA) was proposed in the early 1970s, and the term “blister” was first professionally used in 1988 by Takashi, as a focal small arterial wall defect and subsequent vessel wall bulge covered with thin fibrous tissue at the nonbranching site [1, 2]. They differ from the typical saccular aneurysm in terms of histology, morphology, and location. Among the locations, supraclinoid internal carotid artery (ICA) is the most commonly described location, particularly involving the dorsomedial wall. Other locations such as anterior communicating artery (AComA) and basilar artery have been described [3–8]. However, bifurcation of the middle cerebral artery (MCA) is one of the rare sites reported. We report a case of MCA bifurcation blister aneurysm treated with clip but reoccurrence at 7 days after surgery and died.

7.2

Illustrative Case

A 54-year-old female patient was referred to our hospital with history of sudden-onset severe headache and vomiting. On neurological examiY. Zhao · Z. Guo (*) Neurosurgical Department of the Ninth People’s Hospital of Shanghai, Shanghai Jiaotong University, Shanghai, China

nation, except for neck rigidity, another neurological deficit was not found. She received a CT scan, which showed that subarachnoid hemorrhage (Fisher grade 1) CTA showed aneurysm in the bifurcation of the right MCA.  Then she underwent digital subtraction angiography which confirmed the aneurysm in MCA bifurcation (Fig. 7.1a, b). Owing to its shape, size, and location, the aneurysm was misdiagnosed as saccular aneurysm. Discussed with family members, the patient underwent clipping surgery. With pterional approach, the aneurysm was exposed at the bifurcation of M1, (Fig.  7.2a) however, when exposing the aneurysm, which ruptured. The bleeding was stopped with a small piece of cotton and suction compressing. During operation, the aneurysm wall and both M2 were founded very thin. At final, the aneurysm was satisfactorily clipped. (Fig. 7.2b, c). After operation, the patient recovered completely, and CTA on the first day after operation showed the aneurysm had been completely occluded. However, on the seventh day after operation, the patient suddenly lost consciousness and breath. The patient was supported with a machine and received a CT scan, which showed hemorrhage at the operative location; CTA showed local aneurysm reoccurrence. Family members did not agree to receive further therapy. The patient died on the ninth day after operation (Fig. 7.3).

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 Y. Kato et al. (eds.), Recent Progress in the Management of Cerebrovascular Diseases, https://doi.org/10.1007/978-981-16-3387-4_7

53

Y. Zhao and Z. Guo

54 Fig. 7.1 Oblique project of preoperative DSA (a and b) show the aneurysm of bifurcation of right cerebral aneurysm (red arrow)

a

b

7.3

Discussion

Intracranial blood blister aneurysm is a rare lesion and seen in 0.3–1% of all intracranial aneurysms. Its pathology differs from the real intracranial aneurysm, and it has a very thin wall which includes fibrin and lacking a collagenous tissue layer. This results in their rapid regrowth and high tendency to rupture if not treated [1]. Most intracranial blister-like aneurysm locates in the intracarotid artery; involvement of AComA and basilar artery have been reported [7–9]. However, only five cases in MCA were reported in the literature. The diagnosis of blister-like aneurysm depends on neuroimages. CTA has been shown to have a high sensitivity and specificity for identifying ruptured aneurysms, but its utility in the setting of BBA has rarely been assessed due to the small volume of this aneurysm. Gaughen

et  al. reported on a series of six patients with BBA of the internal carotid artery who underwent CTA; the false-negative rate was 33%. They suggested that these false results could come from the small size and shallow profiles of BBA, the lack of spatial resolution of CTA in comparison to that of DSA imaging, and the numerous potential pitfalls of CTA that can contribute to obscuring small hemispheric blebs [10]. Therefore, to date, DSA remains the main method to diagnose the blister aneurysm. In addition to a standard view, oblique views should be taken for every patient and magnified images obtained if necessary. Rotational 3D angiography is recommended when a BBA is suspected. Any suspicion should induce the clinician to review all sequences and question the significance of any vascular wall irregularities. When the initial angiography is not convincing and initially interpreted as negative, a close follow-up is indicated, because rapid  changes from small suspicious bulges to

7  Blister Aneurysm of Middle Cerebral Artery Bifurcation (Case Report and Review)

55

a

b

c

Fig. 7.2  During operation, the aneurysm ruptured, and bleeding was stopped with a small piece of cotton and suction compression. The aneurysm wall and two M2

were very thin. (a) After the aneurysm was completely clipped, both M2 were spared, which is confirmed with fluorescein angiography (b and c)

s­accular-­type lesions have been described. Our case presented normal vessels during the first operation after clipping with fluorescein angiography, but CTA showed a reoccurrence of large aneurysm on the seventh day after operation. Surgical technique and outcome: Irregular broad base, thin and fragile walls, and small sizes of blister-like aneurysm are characteristics that impose difficulty for any therapeutic method. Conservative treatment, however, is associated with high mortality rates, and inter-

vention is mandatory for these lesions. Surgical therapy includes open surgery and endovascular intervention [7, 8, 11]. The microsurgical techniques for BBA treatment consist of clipping, wrapping, trapping with or without revascularization, and primary suture repair. However, until now, there is no best method to treat this kind of aneurysm. Peschillo et  al. reported three cases of MCA blister aneurysms, one of these received clipping, and the other two cases underwent endovascular treatment [4]. After

Y. Zhao and Z. Guo

56 Fig. 7.3  On the seventh day after operation, the patient suddenly lost consciousness and breath; CTA showed that the reoccurrence of aneurysm and subarachnoid hemorrhage (a, b)

a

b

operation, one case was well, and two cases died. Londhe et  al. treated one case of MCA blister aneurysm with endovascular treatment, and the patients recovered well [3]. Wang et al. suture the defect of the middle cerebral artery; the results are very well without the stenosis of the parent artery [5]. Meling et  al. reported that intraoperative and early postoperative reruptures of BBA in intracarotid artery occurred in 47% of patients managed with direct clipping

and in 20% of patients treated with clipping or with wrapping material. The surgical morbidity is estimated to be 21%, with a mortality rate of 17% [10, 12]. ISAT study reported that the surgical morbidity and mortality rates were 36.4% and 8.3%, respectively [7]. For endovascular management of BBA, the estimated morbidity is 3.4% and the mortality 11.5%. ISAT study reported that the endovascular morbidity and mortality to be 25.4% and 7.5%, respectively.

7  Blister Aneurysm of Middle Cerebral Artery Bifurcation (Case Report and Review)

7.4

Advantage and Limitation

Our case was clipped but reoccurred on the seventh day after operation. According to the pathology of blister-like aneurysm, we think that the blister-like aneurysm of MCA should be treated by suturing the defect of the vascular wall if possible. Blister-like aneurysm has no medial and middle layers, just covered with fiber membrane. When clipped, only outer fiber membrane is clipped, the defect is not involved, and the aneurysm is easy to recur. However, this need be confirmed with more patients.

7.5

Complication Avoidance

In addition to the lack of consensus regarding the best treatment modality, there is controversy on the optimal timing for treatment. Although some authors have recommended treating BBA in the chronic stage because the clot covering the lesion will have had time to organize itself, however, most authors suggest that these lesions should be treated in the early stage so as to reduce the acute risk of rebleeding and regrowth [2, 7, 8]. Modern endovascular devices such as flow diverter and overlapping stents have shown promising results. A flow diverter is the emerging treatment option for ICA blister aneurysms [7]. However, it is difficult for blister-like aneurysm in the bifurcation of the middle cerebral artery to be treated with a flow diverter; most authors suggest that open surgery should be the first choice.

7.6

Conclusion

The blister aneurysm of bifurcation of the middle cerebral artery may be larger than 5 mm. Its treatment method is still controversy.

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References 1. Ishikawa T, Nakamura N, Houkin K, Nomura M. Pathological consideration of a “blister-like” aneurysm at the superior wall of the internal carotid artery: case report. Neurosurgery. 1997;40(2):403–5, discussion 405–406. 2. Jha AN, Gupta V.  Blister aneurysms. Neurol India. 2009;57(1):2–3. 3. Londhe S, Gupta V, Parthasarthy R, Ganie HA, Jain N.  Blister aneurysm of middle cerebral artery division: stent-assisted coiling using shelfing technique. J Clin interv radiol ISVIR. 2019;3:126–9. 4. Peschillo S, Missori P, Piano M, Cannizzaro D, Guidetti G, Santoro A, Cenzato M. Blister-like aneurysms of middle cerebral artery: a multicenter retrospective review of diagnosis and treatment in three patients. Neurosurg Rev. 2015;38:197–203. 5. Wang L, Cai L, Qian H, Wang L, Cai L, Qian H, Shi XE. Microsurgical suture technique for blood blister like aneurysm of middle cerebral artery:2-D video. World Neurosurg. 2018;118:148–9. 6. Cıkla U, Sadighi A, Bauer A, Başkaya MK.  Fatal ruptured blood blister-like aneurysm of middle cerebral artery associated with Ehlers-Danlos syndrome type VIII (periodontitis type). J Neurol Surg Rep. 2014;75(2):e210–3. 7. Papasilekas TI, Themistoklis KM, Andreou AA.  Current trends in the surgical management of blister aneurysm. An illustrative case series. Clin Neurol Neurosurg. 2018;168:54–95. 8. Owen CM, Montemurro N, Lawton MT.  Blister aneurysm of the internal carotid artery: microsurgical results and management strategy. Neurosurgery. 2017;80(2):235–47. 9. Kim YS, Joo SP, Kim TS. Microsurgical management of ruptured blood blister aneurysms of the internal carotid artery without bypass: a retrospective single center study of 36 patients over 20 years. World Neurosurg. 2019;128:e956–65. 10. Meling TR.  What are the treatment options for blister-­like aneurysms? Neurosurg Rev. 2017;40(4): 587–93. 11. Kalani MYS, Zabramski JM, Kim LJ, et  al. Long-­ term follow-up of blister aneurysms of the internal carotid artery. Neurosurgery. 2013;73(6):1026–33, discussion 1033. 12. Meling TR, Patet G.  The role of EC-IC bypass in ICA blood blister aneurysms-a systematic review. Neurosurg Rev. 2021;44:905–14.

8

Flexible Endoscopic Aspiration of Intraventricular Hemorrhage Alberto Feletti and Riccardo Stanzani

8.1

Introduction

Intraventricular hemorrhage (IVH) can be due to the ventricular extension of a thalamic hemorrhage or to the rupture of a cerebral aneurysm or AVM. Some patients with IVH require an EVD because of intracerebral hypertension or obstructive hydrocephalus. In such cases, endoscopic aspiration of IVH is indicated, before placing the EVD. During the endoscopic aspiration of IVH, the vision of anatomical landmarks is severely impaired. Detailed knowledge of intraventricular anatomy is therefore mandatory before facing this type of surgery. In the lateral ventricle, it is important to recognize the choroid plexus, the vena terminalis (or thalamo-striate vein), and the septum pellucidum. They are oriented in a sagittal direction, helping the surgeon to find the way to the foramen of Monro. In the third ventricle, the mammillary bodies and the tuber cinereum are the first visible structures. More ventrally, the infundibulum, the optic chiasm, and the lamina terminalis can be seen. Directing the scope towards the posterior third ventricle, A. Feletti (*) Department of Neurosciences, Biomedicine and Movement Sciences, Institute of Neurosurgery, University of Verona—AOUI Verona, Verona, Italy

the adhaesio interthalamica, the choroid plexus of the roof of the ventricle, the habenular and posterior commissures, and the adytum of the cerebral aqueduct can be seen. After passing the superior constriction, the ampulla, and the inferior constriction of the cerebral aqueduct, the fourth ventricle is inspected. It is mandatory to recognize at least the choroid plexus on the roof of the ventricle, the brainstem, the lateral recesses with the Luschka foramina, the Magendie foramen, and the PICAs (1–4).

8.2

Case Report

Figure 8.1 shows the case of a 79-year-old man who presented to our emergency room in a severely impaired neurological state. CT scan revealed the presence of a left thalamic hemorrhage that broke the ependymal layer of the third ventricle and determined a tetraventricular hemorrhage. The IVH produced intracranial hypertension, obstructive hydrocephalus, and compression on the brainstem due to the significant clot in the fourth ventricle. The patient was therefore immediately operated on for the endoscopic aspiration of IVH.  Figure  8.1 shows the immediate postoperative results, with ICP control, decompression of the third and the fourth ventricles, and EVD in the right lateral ventricle.

R. Stanzani Neurosurgery Unit, Azienda Ospedaliero-Universitaria di Modena, Modena, Italy © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 Y. Kato et al. (eds.), Recent Progress in the Management of Cerebrovascular Diseases, https://doi.org/10.1007/978-981-16-3387-4_8

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a

b

c

d

e

f

Fig. 8.1 (a, b, c) Preop CT scan showing a left thalamic hemorrhage with intraventricular extension. (d, e, f) Immediate postop CT scan after endoscopic IVH aspiration

8.3

Discussion

8.3.1 Surgical Technique After a precoronal, paramedian, curved skin incision at the side of the lateral ventricle with the largest amount of blood, a burr hole is placed at about 1.5 cm from the midline. It is important for the burr hole not to be too lateral; otherwise, entering the cerebral aqueduct would be troublesome. A semirigid 14-French peel-away introducer catheter is used to cannulate the lateral ventricle and create a passage for the flexible scope. It is advisable to use endoscopes with an external diameter not larger than 4  mm for this kind of procedure, as a larger size may not fit the diameter of the cerebral aqueduct. After entering the

ventricular system, the screen appears completely red or dark because the tip of the scope is dipped in blood. Although the severely impaired vision might be worrisome and frustrating, intermittent aspirations and irrigation using an external 20 mL syringe connected to the outer end of the scope allow the breaking of the clots and their initial removal. The second operator balances the suction force depending on the resistance he can perceive. In any case, when the whitish color of the ependymal layer appears on the screen, the aspiration must be immediately stopped. Ringer lactate irrigations can clear the field and improve the vision. Therefore, the operative channel of the scope is used as a sucker and an irrigator. The choroid plexus is usually the first anatomical landmark to be revealed. The choroid plexus must be followed forwards in order to identify

8  Flexible Endoscopic Aspiration of Intraventricular Hemorrhage

the foramen of Monro, which is the second key landmark. After crossing the Monro foramen, further aspirations and irrigations unveil the mammillary bodies and the tuber cinereum. The tip of the scope is then bent towards the posterior part of the third ventricle, where the posterior and habenular commissures along with the adytum of the cerebral aqueduct can be seen. The scope can then be advanced into the cerebral aqueduct to remove the clots from the fourth ventricle until the patency of the foramina of Luschka and Magendie is restored. Only aspirating the blood from both the third and the fourth ventricles can reestablish the patency of the whole CSF pathway. The aspiration of blood from the lateral ventricles is more difficult and time-consuming compared to the third and the fourth ventricles. Moreover, as long as the way between the Monro foramen and the Magendie foramen is set free, extensive clot removal from both the lateral ventricles is not clinically relevant. Actually, the CSF pulsations through the restored pathway would clear the blood remnants in a few days after surgery. However, if deemed appropriate, a standard septostomy can be performed to remove blood clots from the contralateral ventricle, although a contralateral approach through a different burr hole is also possible. Prolonged direct irrigation is sufficient to stop eventual bleeding. Eventually, gentle compression with an inflated Fogarty balloon can speed up the bleeding control. At the end of the procedure, an EVD is left in place for both ICP monitoring and CSF drainage (5). CT scan is performed immediately after surgery. EVD should be kept open at about 15 cm from the tragus and possibly weaned off during the following 2–3 days.

8.3.2 Outcome A study showed a higher favorable outcome (GOS 3–5) in the endoscopy group compared to the group of patients who received urokinase treatment (62% vs 36%) (5). Another study pub-

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lished in 2012, comparing EVD alone with endoscopic aspiration of IVH, revealed that IVH aspiration did not significantly affect the outcome at 1 year according to the modified Rankin Scale. However, patients treated with EVD alone required temporary CSF diversion for a longer time and had a five times greater chance of requiring a permanent shunt. Neuroendoscopy showed a 34% reduction of shunting rates when compared with EVD alone (6). Further investigations indicated that neuroendoscopy  +  EVD could become an alternative to EVD  +  fibrinolytic agents (7). In any case, the amount of IVH assessed with Graeb score and the ventriculocranial ratio (VCR) have been described as two negative predictors of IVH outcome (8, 9), and especially persistence of blood in the fourth ventricle is related to poor outcome in IVH patients (10). Several series clearly reported significant reduction of both Graeb score and VCR after endoscopic removal of IVH (5). Although randomized controlled trials are still lacking, evidences are available that endoscopic treatment can provide ICP control in the acute phase, fast removal of EVD, reduction of shunt dependency, and intracranial infections (11).

8.3.3 Advantages and Limitations The advantages that can be obtained through flexible endoscopic aspiration of IVH are significant. It is possible to quickly restore CSF pathways, decrease intracranial hypertension, reduce EVD obstruction and replacement rates, and consequently minimize infections. Moreover, a potential decrease of shunt dependency has been shown (6, 11). In any case, being the amount of intraventricular blood a strong negative prognostic factor, its fast removal has been associated with better outcome (12, 13). Some limitations of the technique must be noted. First, the quality of vision is currently suboptimal because flexible endoscopes with external diameters less than 4 mm are based on optical fibers. Second, surgery should be performed within 48–72 h from the bleeding. Delayed inter-

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vention may be extremely demanding due to the organization of the clots that become hard and difficult to break and aspirate. Moreover, IVH aspiration of blood clots is not a single-surgeon procedure: a well-trained assistant surgeon is always required. It is necessary to master simpler procedures with flexible scope as septostomy or third ventriculostomy, before attempting endoscopic removal of IVH.

8.3.4 Complications Avoidance Before surgery, it is crucial to assess the blood coagulation and aggregation of the patient and correct them if needed. Burr hole must be placed precoronal, and not more lateral than 1.5  cm from the midline, in order to get a straight and comfortable direction to the cerebral aqueduct. Mean arterial pressure should be kept below 110 mmHg and perfusion pressure greater than 70  mmHg. Aspiration must be discontinued immediately when the whitish color of the ventricular ependyma appears on the screen, to avoid any damage. Aspiration and irrigation volumes must be carefully balanced, especially in the fourth ventricle: actually, as the diameter of the endoscope occludes the cerebral aqueduct completely, excessive irrigation can determine hypertension in the fourth ventricle and bradycardia. When withdrawing the endoscope from the fourth and the third ventricles, care must be taken to accurately retrace the same route used previously, in order to avoid damages to the ependymal walls, veins, and choroid plexus.

8.4

Conclusion

Flexible endoscopic aspiration of IVH is a safe and effective procedure, if performed within 48–72 h after hemorrhage. It can provide immediate ICP control and brainstem decompression, decrease of EVD obstruction rate and faster EVD removal, and reduction of shunt dependency.

References 1. Longatti P, Fiorindi A, Feletti A, D’Avella D, Martinuzzi A. Endoscopic anatomy of the fourth ventricle. J Neurosurg. 2008;109(3):530–5. 2. Rhoton AL.  Cerebellum and fourth ventricle. Neurosurgery. 2000;47(3 Suppl):S7–27. 3. Rhoton AL.  The lateral and third ventricles. Neurosurgery. 2002;51(4 Suppl):S207–71. 4. Alberto F, Alessandro F, Vincenzo L, Rafael B-B, Elisabetta M, Veronica M, Raffaele DC, Pierluigi L, Andrea P, Giacomo P. A light on the dark side: in vivo endoscopic anatomy of the posterior third ventricle and its variations in hydrocephalus. J Neurosurg. 2020; https://doi.org/10.3171/2020.4.JNS20493. 5. Longatti PL, Martinuzzi A, Fiorindi A, Maistrello L, Carteri A. Neuroendoscopic management of intraventricular hemorrhage. Stroke. 2004;35(2):e35–8. 6. Basaldella L, Marton E, Fiorindi A, Scarpa B, Badreddine H, Longatti P.  External ventricular drainage alone versus endoscopic surgery for severe intraventricular hemorrhage: a comparative retrospective analysis on outcome and shunt dependency. Neurosurg Focus. 2012;32(4):E4. 7. Li Y, Zhang H, Wang X, She L, Yan Z, Zhang N, et al. Neuroendoscopic surgery versus external ventricular drainage alone or with intraventricular fibrinolysis for intraventricular hemorrhage secondary to spontaneous supratentorial hemorrhage: a systematic review and meta-analysis. PLoS One. 2013;8(11):e80599. 8. Pia HW.  The surgical treatment of intracerebral and intraventricular haematomas. Acta Neurochir. 1972;27(3):149–64. 9. Kramer AH, Mikolaenko I, Deis N, Dumont AS, Kassell NF, Bleck TP, et  al. Intraventricular hemorrhage volume predicts poor outcomes but not delayed ischemic neurological deficits among patients with ruptured cerebral aneurysms. Neurosurgery. 2010;67(4):1044–52; discussion 1052–1053. 10. Lagares A, Putman CM, Ogilvy CS.  Posterior fossa decompression and clot evacuation for fourth ventricle hemorrhage after aneurysmal rupture: case report. Neurosurgery. 2001;49(1):208–11. 11. Toyooka T, Kageyama H, Tsuzuki N, Ishihara S, Oka K.  Flexible endoscopic aspiration for intraventricular casting hematoma. Acta Neurochir Suppl. 2016;123:17–23. 12. Nakagawa T, Suga S, Mayanagi K, Akaji K, Inamasu J, Kawase T, et  al. Predicting the overall management outcome in patients with a subarachnoid hemorrhage accompanied by a massive intracerebral or full-packed intraventricular hemorrhage: a 15-year retrospective study. Surg Neurol. 2005;63(4):329–34; discussion 334–335. 13. Song Z, Yang Q-D, Zi X-H, Fan X. Modified Graeb criteria for predicting the post-hemorrhagic hydrocephalus in intraventricular hemorrhage. Chin Med Sci J. 2004;19(2):138–41.

9

Endoscopic Evacuation of Cerebral Haematoma Daisuke Suyama and Brajesh Kumar

Although there are controversies about the optimal management of spontaneous intracerebral haemorrhage (ICH), there are definite benefits of endoscopic procedures in ICH as it causes less cerebral damage. The purpose of this chapter is to guide the young new endoscopic surgeons to produce repeatability and reproducibility in the procedure for good outcome.

9.1

A. Small Putaminal Haemorrhage

Key Points Discussed • Three-dimensional visualization of procedure before the surgery • Coagulation of even small vessels • Waiting for the softening of haematoma for easy evacuation The decision regarding position of the burr hole—Degree of entry to the haematoma is more important than the closeness to the surface.

D. Suyama Department of Neurosurgery, Fuchu Keijinkai Hospital, Tokyo, Japan B. Kumar (*) Department of Neurosurgery, IGIMS, Sheikhpura, Patna, India

9.1.1 Introduction Endoscopic evacuation of haematoma was started appearing in the major journals around 2000, gradually widened [1, 2]. In 2014, doctors started operating under medical insurance in Japan. The procedure is simple, but there is a learning curve. Beginners learn from the seniors, and everyone has some own methods, so there is no repeatability and reproducibility. The aim of this article is to highlight the basic points of the endoscopic evacuation of the putaminal haemorrhage to achieve repeatability and reproducibility among the different new endoscopic surgeons.

9.1.2 Pre-Procedure Preparations Instruments: Translucent sheath (5–10  mm), suction tube non-tapered (2–4 mm), rigid endoscope (2.7 mm), flexible endoscope (Fig. 9.1). Haematoma Evacuation: After making the burr hole, durotomy is done. A translucent sheath is inserted. An endoscope and suction tube are inserted through the port. Evacuation of haematoma is started from the margin. The tip of the suction tube should not be taken far from the sheath. Haemostasis: Coagulation of the bleeding vessel can be done by monopolar through the suction tube. The author prefers artificial CSF (ARTCERIB)R for the irrigation of the h­ aematoma

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 Y. Kato et al. (eds.), Recent Progress in the Management of Cerebrovascular Diseases, https://doi.org/10.1007/978-981-16-3387-4_9

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Suction Tube TRANSLUCENT SHEATH

SIZE- 2.5, 3.0, 4.0mm dia. Medikit: NEUROSHEATH OD: 14Fr, 17.5Fr, 22Fr

ENDOSCOPE

CLEAR SHEATH WITH GUIDE ID 6.0mm, OD 8.0mm

MACHIDA: RIGID2.7mm dia. FLEXIBLE4.8mm dia.

Fig. 9.1  Instruments used in the procedure (Neurosheath; Suction Tube; Clear sheath with guide)

cavity, but Ringer’s lactate (RL) (warm) can also be used. Four packs (2000 mL) of ARTCERIB/ RL should be kept reserved for the procedure.

9.1.3 Trephination and Puncture There are different ways adopted by the different doctors for making flaps, burr hole, and puncture. Any of the methods is acceptable. Some prefer stereotactic drainage of the haematoma, and some prefer evacuation by craniotomy. In many cases, micro AVMs are associated with the putaminal haemorrhage so there is need to change from endoscopic to the microscopic procedure. For an endoscopic surgeon, his endoscope is like a microscope, which uses a sheath as brain spatula and keyhole as craniotomy. Burr holes need to be close to the haematoma, and the direction of puncture should be vertical to the skull as it is easy to manipulate the sheath in this trajectory. The position of the burr hole should be posterolateral to the burr hole for the frontal horn. We

can mark the burr-hole point through the coronal image. It is very important to always keep the image of the brain shift after the decompression (Fig. 9.2).

9.1.4 Evacuation of Haematoma At the time of the presentation of this procedure, there was a report using an endoscope as a method of stereotactic haematoma drainage, puncturing from the forehead part in conformity with the long axis of the CT axial view of OM line, suction in front of the haematoma [3]. Today, we use translucent sheath, through which we can check margin and evacuate the haematoma and instruments can be moved like brain spatula as in microscopic surgery. In putaminal haemorrhage, we remove haematoma from the proximal part to the deeper part. Once the sheath is inserted in the centre of the haematoma, we move the sheath toward the margin of haematoma toward the proximal part, and we make some working space

9  Endoscopic Evacuation of Cerebral Haematoma A° Target ahead of the hematoma with a CT axial view before surgery and decide the site to be buried with reference to the position where it can pierce perpendicularly to the skull. With the hematoma apiration, as the brain shifts backwards,. C° Hematomas have been almost completely removed by CT axial view after surgery. The hematoma cavities are shrinking with hematoma aspiration.

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a

c

b

B° A pre-operative CT coronal view aims at the upper part of the hematoma and decides the site to be buired with reference to the postion where it can pierce perpendiccularly to the skull. With the hematoma aspiration, the brain shifts downwards, so aspiration also proceeds downwards

d D Check the position of burr hole -by postoperative X-ray A-P view to see if it was the same as the image and make sure to use it for subsequent cases.:

Fig. 9.2  Position of burr holes over CT scan

after evacuating some haematoma. After this the marginal part is evacuated, it is followed by a deeper part behind the centre, and finally, the deeper marginal part is evacuated (Fig. 9.3). After the decompression of haematoma, there is a brain shift in the haematoma cavity, and the cavity slowly disappears and so the working space. If we lose orientation at this point, we should get back to the margin and check around the haematoma. Sometimes, we can also remove contused brain tissue to get working space. If we encounter bleeding, it is either from the surface or tract, and it needs to get coagulated.

not have the working space, we should first make working space using the large bore suction cannula and then should search for the bleeding. We can put a suction tube over the bleeding point and do the electrocoagulation by monopolar placed over the suction cannula in wet condition over many times (four to five times) with low voltage. If the suction has a big vessel, it must be released as it is difficult to haemostasis one vessel get torn. If there is minor oozing, irrigation with artificial CSF/ RL is sufficient. Even after this oozing continues, then we can do pressure control with cotton (Fig. 9.4).

9.1.5 Haemostasis

9.1.6 Irrigation of Haematoma Cavity

We should do haemostasis all the time. Fresh bleeding is red in colour, and haematoma is dark red, so we can easily differentiate them during the surgery and should be coagulated as soon as we find them. If we find arterial bleeding but do

When there is no bleeding, we irrigate the haematoma cavity with the artificial CSF/ RL.  We can put a 5F angiographic catheter or a flexible endoscope for the irrigation of the haematoma

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a

b

A When inserting the sheath into the hematoma, sheath tip is placed at the boundaty between the brain parenchyma and the hematoma,

c

B Aspirate the hematoma at the front boundary, Extend the working space.

C: If you go straight to get the hematoma in the back, the surroundings of the sheath become hematoma, the orientation is lost and the surgical field becomes dark

Fig. 9.3  Placement of sheath in haematoma cavity during evacuation

cavity. Widening of the haematoma cavity with irrigation is important as it stops oozing (Fig. 9.5).

9.2

B. Large Putaminal Haemorrhage

In large putaminal haemorrhage, puncture point is not the big problem. We should better use superior temporal line and coronal suture meeting point and imagine the wideness of haematoma from CT axial, sagittal, and coronal image (Fig. 9.6). Burr-hole point is put the nearest point of haemorrhage, vertically from the skull. A bigger size sheath and a suction tube should be used as many times we encounter big perforators with atherosclerotic changes. For large putaminal haemorrhage, it is important to decompress as fast as possible. In the acute phase, it is difficult to remove haematoma as it is hard. A bigger sheath should be used so

that a larger suction tube can be negotiated through it. The sheath side is usually taken 6 mm or more internal diameter, endoscope 2.7  mm, and suction 4 and 6 mm. During the evacuation of the haematoma, we first evacuate the central haematoma with a larger suction tube; then, we come proximally (toward the puncture site). The margin is evacuated with suction of the lower size and the deepest part in the last (Fig. 9.7). If we find the fresh bleeding, it is mostly from the tract or the puncture site. Any bleeding should be coagulated immediately. Principle of haemostasis after the completion of the procedure should not be followed as working space is lost after the decompression. If the patient is young and there is no brain atrophy, haematoma is usually pushed by the brain to the centre, and there is no need to move the sheath. How to evacuate haematoma depends on the hardness and the duration of the bleeding. In some cases, we do not decompress haematoma too much due to larger perforators.

9  Endoscopic Evacuation of Cerebral Haematoma

a

A The surrounding area is white brain parenchyma, hematoma can be confirmed only at the distal end of the sheath. By moving the sheath finely, we will aspirate the hematoma entering the sheath

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b

c

B Even with artctial bleeding, there is no problem as long as it captures the surgical filed at the tip of the sheath. Check the surroundings little by little at the position and coagulare hemostasis from around the bleeding sites.

C. The surrounding of the sheath are red. I do not know wheather the point is behind or just in front. While aspirating, search the bleeding point while returing the sheath to the front

Fig. 9.4  Haemostasis technique during the evacuation

Tips: Sequence of evacuation in large putaminal haemorrhage is centre, proximal, margin, and deeper part in the last. In case of large putaminal haemorrhage, bleeding should be coagulated immediately each time we find the bleeding. The difference from the microscopic approach is that the bleeding point can be found directly. We use monopolar in endoscopic approach whereas bipolar in microscopic approach. Lateral sides and proximal sides are blind in endoscopy, and haemostasis can be achieved with pressure and irrigation as we cannot see the bleeding point. The author recommends using the flexible endoscope for observing the haematoma cavity. In putaminal haemorrhage, there is no special point in closure. It is the same as usual craniotomy. ICP monitoring can be used, if there is incomplete haematoma evacuation. The author does not put the drainage tube in endoscopic operation unless there is associated hydrocephalus. Peridural haematoma is absorbed spontane-

ously. Endoscopic evacuation can be tried again in case of incomplete evacuation.

9.2.1 Conclusion It is important with the endoscopic approach to learn how to cope with hard haematoma. We should observe and wait for the softening of the haematoma. We should not chase too far for complete clearance of the haematoma. Getting disoriented is another problem in endoscopic surgery. In this situation, we should again go back to the margin or proximally come deeper again. Brain shift should always be kept in mind. If we feel bleeding is troublesome, it is not wise to lose valuable time to control bleeding, and there should be no hesitation in switching over to a microscopic procedure. Before one gets enough experience, we should operate with an experienced surgeon. If it is not possible to have an expert, beginner should start with small craniotomy rather than burr hole.

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a

A The hematoma cavities can be confirmed at the tip of the sheath Confimation of haemostasis is inadequate.

b

c

B While checking residual hematoma, the sheath is advanced inside the hematoma space, but the space is collapsed from the surroundings and the whole picture can not be confirmed

C The sheath is returned to the front boundary portion to perfuse the hematoma cavity contiuously. At first it is muddy to see nothing but wait for a while to see the whole picture. It is perfuse until clear.

Fig. 9.5  Irrigation of haematoma cavity

Puncture point in Putaminal Bleed Axial CT

Coronal CT

CT

• Axial CT- Calculate the distance from the midline, aim at the upper side of the hematoma • Coronal CT- Measurement of the temporal line, the distance to be drilled and the distance to the hematoma Fig. 9.6  Burr-hole placement in large putaminal haemorrhage

9  Endoscopic Evacuation of Cerebral Haematoma

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Evacuation and haemostais of Putaminal Haemorrhage Coronal CT Post op CT

Compression hemostasis

Pefusion haemostasis

Side wall

Bottom

• Hematoma aspiration in the order of upper front → center → front → surrounding → back • Confitm in the front, coagulate in the back, check the haemostasis with irrigation throughout Fig. 9.7  Evacuation and haemostasis in large putaminal haemorrhage

9.3

Subcortical (Lobar) Haemorrhage

Key Points Discussed • Waiting for the softening of haematoma for easy evacuation. • Decision regarding the position of the burr hole—Degree of entry to the haematoma is more important than the closeness to the surface.

9.3.1 Introduction According to the guidelines of the treatment of stroke 2015 [4] indication for the treatment of subcortical haemorrhage, we should take into consideration the following factors: 1 . Disturbance of consciousness. 2. Volume of blood more than 30 mL or more. 3. Activities of daily living (ADL) is affected. 4. General condition of the elderly patients.

5. Expectation of the family member of the patient. 6. Chances of clinical improvement after the surgery. 7. Timing of operation—It should be done earliest to prevent secondary injury. However, in some cases, waiting is good for the patients. This time, in this paper, the author has explained the points to successfully remove the endoscopic cerebral haematoma to elderly people, focusing on the technique of subcortical bleeding. As for the basic procedure of the endoscopic intracerebral haematoma removal surgery, he has mentioned it in detail in his other paper [5].

9.3.2 Before the Procedure 1. Timing of the Operation: In elderly patients, there are many comorbid conditions which need to be evacuated in a shorter time and under local anaesthesia (LA). It is better to wait for 72 h to 1 week to allow for the soften-

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ing of the haematoma. But the timing of operation should be guided by the general condition and the symptoms of the patients. In such cases, we should expect hard haematoma and bleeding if operated on before 72 h. 2. Pre-operative Evaluation: We should always check for the vessel abnormality with MRA and CTA as we have to operate with one suction tube and bleeding can be troublesome. Especially in subcortical cases, we should check for AVMs and AVFs. If there is a possibility of bleeding, we should not go for an endoscopic procedure. 3 . Preparation of instruments: We require the general instruments for burr hole or small craniotomy or enlargement of the translucent sheath, a suction tube, a rigid endoscope, ViewSite™ Brain Access System (Vycor

Medical) (Fig. 9.8), and an operating bipolar. A flexible endoscope is required especially for the subcortical bleed. Training is required to keep the endoscope in position and introducing suction through the port. If the port is not available, we may need a spatula and microscope system. 4 . Anaesthesia: The author prefers local anaesthesia (LA) with some sedation (propofol/ dexmedetomidine) in patients who have altered consciousness and those who cannot obey commands. In other patients, the writer prefers general anaesthesia (GA). 5. Making Burr Hole, Puncture of Dura, and Position: For endoscopic evacuation, we should not go by the closest point of haematoma by CT. Normally, we think that it will be easy to remove haematoma from the closest point, but

• ViewSite Brain Acess System (PORT)

Suction tube Biplolar Endoscope

Working channel: 12~22mm. Length: 3~7cm (tapered)

• Neurosheath (Transparent sheath) Endoscope Suction tube

Transparent sheath is used to secure the working space and port to secure the tract. It is not moved like transparent sheath and fixed from the tract to the hematoma space. It can be used with endoscope or microsacope. Use of suction tuvbe and biploar has added advantage, not in transparent sheath.

Working channel: 5~8mm Length: ~10cm (peel off)

Fig. 9.8  Instruments used in evacuation (Sheath, Working channel, Bipolar, Suction Tube and Endoscope)

9  Endoscopic Evacuation of Cerebral Haematoma

A

B

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C

D

Pre-op

CT at Cut Lines

Example when Burr site was only determined by the CT Axial view B Was sliced at the height of the slice, but the puncture direction often faces downward from he OM line (bule arrow.)

A B C D

It is diffecult to

A

B

C

Post op

D

A punture the direction B of the OM C line after clothing the D sugical filed and adjust the postion so that the burr hole part comes up. Hematoma will not be evacuated in upper side. Slightly upper, hematoma and often piercing from a disatcnce away (red arrow.)

Fig. 9.9  Placement of burr hole

this is a pitfall as we cannot see the part of the haematoma close to the endoscope and we may lose the orientation. The philosophy of the closest point entry works better in the deeper lesions. There, we can move the endoscope in a rotating manner and can see the margins of haematoma. CT axial image (Fig. 9.9), OM line only shows the wideness of haematoma, not the depth of haematoma. When entering vertical to the haematoma (90 degrees), we can view a wider area, and the burr hole should be put on the upper side of the haematoma (Fig. 9.10). All the view (axial, coronal, and sagittal) should be taken into consideration for marking the burr-hole point, and a marker should be placed on the skull (Fig. 9.11). The puncture point should be directed vertically directed toward the centre of haematoma. We should always reconsider the scan and match the marker and puncture point before making a burr hole. If we make a big skin incision, there is a mismatch between the marker and the puncture point, and we may lose

the orientation even if the difference is less than 1  cm as subcortical haemorrhage may come close to the surface. The patient should be in a comfortable position with padding of all pressure points. Puncture point should be the highest. Brain shift should always be kept in mind (Fig. 9.12).

9.3.3 Evacuation of the Haematoma In the putaminal haemorrhage case, we start the haematoma evacuation from the margin of the haematoma, but in the subcortical haemorrhage, we can’t observe the whole border of the haematoma, so we should approach from the centre of the haematoma. After some decompression, the brain gradually shifts down. We should come out as haematoma close to the surface is then evacuated. Then again, the deeper part of the haematoma is evacuated. We should

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a

C: Difficult to coagulate if not approached vertically

c A- Puncture point close to the hematoma

b

Bleeder

d B: Puncture point at a distance- we can check all over the hematoma

D- here we can easily coagualte if approached vertically

Fig. 9.10  Burr placement vertical to haematoma to visualize the bleeding point

always keep in mind the limitation of movement of the endoscope and should not go laterally below the angle of the sheath (Fig. 9.13). If the centre of haematoma cannot be evacuated, this implies it is hard. Then, we need to move the position of the sheath and need bigger suction but decreases the field of vision. We need a 2.7 mm neural sheath, a rigid endoscope, and a 4  mm suction tube. If we cannot remove with the 4 mm suction, then we can try to remove the sheath together with the suction and clots comes along with that. If we fail again, we need tumour holding forceps to hold or crush the haematoma which can remove with suction. We should always keep in mind the brain shifts during the procedure.

9.3.4 Haemostasis Bleeding is mostly on the lateral side and closer to the brain surface. These points are difficult to check by rigid endoscopes, so flexible endoscopes

are required. Irrigation is important for controlling the small bleedings. Blind coagulation should not be done. We should always see the bleeding point by adequate irrigation before going for the coagulation as there may be some bigger vessels which may cause clinical deterioration. After the removal of haematoma, we remove the translucent sheath and irrigate it from the burr-hole point. We also put the tip of the flexible endoscope to the burr hole and irrigate the haematoma cavity till clear fluid comes out. If water is not clear, we keep on irrigating and wait for 10–15 min till clear water comes out. If it is not clear in spite of this, we decrease blood pressure 30%) and at 1  day (>40%), which predict a long-term independent favorable outcome [22–24]. For acute supratentorial malignant ischemic infarction, some randomized controlled trials concluded that those factors (undergoing DC within 48  h after stroke onset was performed, age2) was reported in 35% [29]. Kim and co-workers found 33% of patients have a significant benefit from DC [30]. In Pfefferkorn’s report [31], 60% of patients had poor outcomes, and 76% of patients had additional brainstem infarction, and the mortality was 40% and 58%, respectively. This study found the age above 60 years and the timing of DC did not influence the outcome, and the quality of life was impaired moderately.

10.6 Advantages and Limitations Approximately 62% of the patients with acute ischemic stroke were able to regain self-care ability within 90 days after the treatment of intravascular thrombolysis combined with mechanical thrombectomy. Ma et  al. reported that the total bleeding rate and the incidence of asymptomatic cerebral hemorrhage in acute cerebral artery occlusion treated with intravenous thrombolysis combined with mechanical thrombectomy were lower than those treated with arteriovenous thrombolysis. However, the Chinese prehospital triage system is more complicated than many western countries, with patients often being sent to hospital by personal transport, and stroke center teams are usually mobilized only on admission rather than before the patients’ arrival. In addition, informed consent must be required before the administration of alteplase due to the tensions between doctors and patients in China; therefore, counseling commonly involves many family members before treatment and is time-­ consuming, which leads to workflow times being relatively long. Without neurosurgical intervention, the mortality of malignant MCA infarction is approximately 80%, and neurological deterioration often occurs within 5  days, with the highest

10  Management (Surgical and Endovascular) of Acute Ischemic Stroke

rate of death due to transtentorial herniation [28]. Arterial occlusion is found in cerebellar ischemic stroke with severe edema, brainstem compression, upward and downward herniation, and occlusive hydrocephalus. Therefore, early diagnosis and surgical treatment of this life-­threatening disease are important, and quality of life after DC for supratentorial malignant stroke was acceptable for most of patients, and the patients with impairment and depression do not regret receiving DC [32–34]. However, quality of life was impaired to some extent, there was mean overall reduction of about 50% and almost 60% of patients had major depression, and chronic physical disability, outcomes, psychosocial impairment, and depression need to be solved in the future [34]. It is well accepted that suboccipital DC is efficient for alleviating brainstem compression and reducing mortality, while data is limited on optimal timing and benefit of a patient, which should be analyzed by prospective studies [28].

10.7 Complication Avoidance The complications of MT include extracranial complications, intracranial complications, and anaphylaxis. Access site complications include access site hematoma, retroperitoneal hematoma, distal emboli leading to limb ischemia, dissection, pseudoaneurysms, and arteriovenous fistula, which are well-recognized. The rate for puncture site hematoma in non-RCTs ranges from 1% to 2% [19, 35, 36] as opposed to 2% to 10.7% in RCTs [37–39]. The overall rate of groin complication ranged from 0.4% to 0.8%. Most groin hematomas are usually managed conservatively by manual compression. Ultrasoundguided compression or direct thrombin injection can treat pseudoaneurysms effectively [40]. Arteriovenous fistulas should be repaired by surgery, and other treatment options include coil embolization, covered stent placement, and glue embolization. The frequency of arterial dissections ranged between 0.6% and 3.9% [41, 42]. Depending on the severity of flow limitation and the hemodynamic significance, treatment ranges

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from conservative management with anticoagulation or dual-antiplatelet therapy in asymptomatic non-flow-limiting dissections to balloon angioplasty or stenting that may be required to line up the intimal flap with the vessel wall and therefore restore the flow [43–45]. The rate of vasospasm in RCTs was 3.9–23% [36, 46, 47]. For most patients, vasospasm is self-limited, and they improve spontaneously within minutes by minimizing irritation of the vessel wall and retracting the catheter. Selective injection of a calcium channel blocker such as nimodipine can be considered for persisting vasospasm; monitoring the systemic hypotension is important during this process [45, 48]. Inadvertent stent retriever detachment during thrombectomy is extremely rare and mostly found in first-generation devices, and at present, there is no standardized way to deal with this complication [49]. It is reported the incidence of vascular perforation is 1.6% [19, 36, 42, 47]. The potential mechanisms include microwire penetration or direct endoluminal trauma and shear forces [50, 51]. Vessel perforation manifested by contrast extravasation is another rare drastic complication, and it is associated with mortality rates exceeding 50% and an overall poor outcome rate of 75% [51]. If vascular perforation occurs, the perforating device should not be pulled back immediately for it may be sealing the site of injury [52]. For vessel injuries proximal to the clot, the anesthesia team is important to reduce blood pressure and to watch for and deal with the Cushing response. In patients who received heparin, the use of protamine sulfate is an effective way to reverse the systemic effect of heparinization [50, 51]. If bleeding persists with repeated rounds of balloon inflation, sacrifice of the injured segment with detachable coils or embolic agents can be considered for it is a life-saving option. The frequency of migration of emboli to a new vascular territory ranges from 1% to 8.6% [19, 35, 36, 46]. Management depends on the location of emboli and the risks versus benefits for patients. If the affected vessel is too small or distal and the risks outweigh the benefits, conservative treatment is recommended. Intra-arterial injection of t-PA can be considered in distal migration of the clot.

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The migrated clot can be retracted by aspiration alone or stent retrieval combined with aspiration for proximal emboli [53]. Anaphylaxis to contrast media is not rare, while it is rarely life-­ threatening. However, severe anaphylaxis caused by cardiovascular and/or respiratory symptoms should be addressed immediately [54]. Initial management includes supplemental oxygen, intravenous epinephrine, intubation, and volume resuscitation with fluids [55]. Surgical complications of DC are commonly classified into early and late complications, and they can occur at any time. The main complications are hemorrhage, infection, cerebrospinal fluid disturbance, and seizures [56]. Malignant stroke patients have a high risk of hemorrhage, owing to most of the patients received antiplatelet medication and intravenous thrombolytic therapy [57]. Approximately 10% of patients will have epidural hemorrhage after DC, while only a few patients require reoperation [56]. Antiplatelet therapy rather than intravenous thrombolysis appears to be a risk factor for hemorrhage, and thrombectomy and intra-arterial thrombolysis prior to DC do not appear to increase the risk of hemorrhage [58]. The rate of infection of the surgical site or central nervous system is less than 10% after DC, including wound infections, empyema, and cerebral abscess [42, 47], especially the patients with an external ventricular drain, and the use of antibiotic-impregnated ventricular catheters can minimize this risk to less than 5% [42, 47]. CSF disturbances frequently occur after DC: 20 to 80% of patients develop hygroma and internal communicating hydrocephalus occurred in 30–40% of patients [59– 61]. A small number of CSF disturbances resolve either spontaneously or after cranioplasty, and a shunt surgery might be required for others patients. Approximately 6–12% of the patients had the risk of single or recurrent seizures within 5 years, especially anterior circulation stroke and severe stroke [62, 63]. For patients who received DC after malignant cerebral infarction, 45% will develop epilepsy, and 50% suffer a seizure [64].

10.8 Conclusion The mechanical thrombectomy with stent retrievers offers an effective and safe treatment option in ischemic stroke due to LVOs with reperfusion rates and a safety profile. Decompressive craniectomy is an effective way to improve the outcome for patients with malignant ischemic stroke.

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10  Management (Surgical and Endovascular) of Acute Ischemic Stroke 12. Saver JL, Goyal M, Bonafe A, et  al. Stent-retriever thrombectomy after intravenous t-PA vs. t-PA alone in stroke. N Engl J Med. 2015;372(24):2285–95. 13. Powers WJ, Rabinstein AA, Ackerson T, et  al. 2018 guidelines for the early management of patients with acute ischemic stroke: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2018;49(3):e46–e110. 14. Zerna C, Thomalla G, Campbell B, et  al. Current practice and future directions in the diagnosis and acute treatment of ischaemic stroke. Lancet. 2018;392(10154):1247–56. 15. Campbell BC, Mitchell PJ, Kleinig TJ, et al. Endovascular therapy for ischemic stroke with perfusion-imaging selection. N Engl J Med. 2015;372(11):1009–18. 16. Goyal M, Menon BK, van Zwam WH, et  al. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet. 2016;387(10029):1723–31. 17. Ciccone A, Valvassori L, Nichelatti M, et  al. Endovascular treatment for acute ischemic stroke. N Engl J Med. 2013;368(10):904–13. 18. Pigretti SG, Alet MJ, Mamani CE, et  al. Consensus on acute ischemic stroke. Medicina (B Aires). 2019;79(Suppl 2):1–46. 19. Goyal M, Menon BK, van Zwam WH, et  al. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet. 2016;387(10029):1723–31. 20. Sheen JJ, Kim YW.  Paradigm shift in intra-arterial mechanical thrombectomy for acute ischemic stroke : a review of randomized controlled trials after 2015. J Korean Neurosurg Soc. 2020; 21. Will L, Maus V, Maurer C, et al. Mechanical thrombectomy in acute ischemic stroke using a manually expandable stent retriever (tigertriever): preliminary single center experience. Clin Neuroradiol. 2020; https://doi.org/10.1007/s00062-­020-­00919-­w. 22. Rudilosso S, Laredo C, Amaro S, et  al. Clinical improvement within 24 hours from mechanical thrombectomy as a predictor of long-term functional outcome in a multicenter population-based cohort of patients with ischemic stroke. J Neurointerv Surg. 2021;13:119–23. 23. Cao Y, Wang S, Sun W, et al. Prediction of favorable outcome by percent improvement in patients with acute ischemic stroke treated with endovascular stent thrombectomy. J Clin Neurosci. 2017;38:100–5. 24. Agarwal S, Cutting S, Grory BM, et  al. Redefining early neurological improvement after reperfusion therapy in stroke. J Stroke Cerebrovasc Dis. 2020;29(2):104526. 25. Juttler E, Schwab S, Schmiedek P, et al. Decompressive surgery for the treatment of malignant infarction of the middle cerebral artery (DESTINY): a randomized, controlled trial. Stroke. 2007;38(9):2518–25.

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26. Vahedi K, Hofmeijer J, Juettler E, et al. Early decompressive surgery in malignant infarction of the middle cerebral artery: a pooled analysis of three randomised controlled trials. Lancet Neurol. 2007;6(3):215–22. 27. Beez T, Munoz-Bendix C, Steiger HJ, et  al. Decompressive craniectomy for acute ischemic stroke. Crit Care. 2019;23(1):209. 28. Heros RC. Surgical treatment of cerebellar infarction. Stroke. 1992;23(7):937–8. 29. Jauss M, Krieger D, Hornig C, et al. Surgical and medical management of patients with massive cerebellar infarctions: results of the German-Austrian cerebellar infarction study. J Neurol. 1999;246(4):257–64. 30. Creutzfeldt CJ, Tirschwell DL, Kim LJ, et  al. Seizures after decompressive hemicraniectomy for ischaemic stroke. J Neurol Neurosurg Psychiatry. 2014;85(7):721–5. 31. Pfefferkorn T, Eppinger U, Linn J, et  al. Long-term outcome after suboccipital decompressive craniectomy for malignant cerebellar infarction. Stroke. 2009;40(9):3045–50. 32. Arnaout OM, Aoun SG, Batjer HH, et  al. Decompressive hemicraniectomy after malignant middle cerebral artery infarction: rationale and controversies. Neurosurg Focus. 2011;30(6):E18. 33. Rahme R, Zuccarello M, Kleindorfer D, et  al. Decompressive hemicraniectomy for malignant middle cerebral artery territory infarction: is life worth living? J Neurosurg. 2012;117(4):749–54. 34. Vahedi K, Benoist L, Kurtz A, et  al. Quality of life after decompressive craniectomy for malignant middle cerebral artery infarction. J Neurol Neurosurg Psychiatry. 2005;76(8):1181–2. 35. Campbell BC, Mitchell PJ, Kleinig TJ, et  al. Endovascular therapy for ischemic stroke with perfusion-imaging selection. N Engl J Med. 2015;372(11):1009–18. 36. Jovin TG, Chamorro A, Cobo E, et al. Thrombectomy within 8 hours after symptom onset in ischemic stroke. N Engl J Med. 2015;372(24):2296–306. 37. Weber R, Nordmeyer H, Hadisurya J, et  al. Comparison of outcome and interventional complication rate in patients with acute stroke treated with mechanical thrombectomy with and without bridging thrombolysis. J Neurointerv Surg. 2017;9(3):229–33. 38. Serles W, Gattringer T, Mutzenbach S, et  al. Endovascular stroke therapy in Austria: a nationwide 1-year experience. Eur J Neurol. 2016;23(5):906–11. 39. Nikoubashman O, Jungbluth M, Schurmann K, et al. Neurothrombectomy in acute ischaemic stroke: a prospective single-Centre study and comparison with randomized controlled trials. Eur J Neurol. 2016;23(4):807–16. 40. Mishra A, Rao A, Pimpalwar Y.  Ultrasound guided percutaneous injection of thrombin: effective technique for treatment of iatrogenic femoral pseudoaneurysms. J Clin Diagn Res. 2017;11(4):C4–6. 41. Balami JS, White PM, McMeekin PJ, et  al. Complications of endovascular treatment for acute

88 ischemic stroke: prevention and management. Int J Stroke. 2018;13(4):348–61. 42. Berkhemer OA, Fransen PS, Beumer D, et al. A randomized trial of intraarterial treatment for acute ischemic stroke. N Engl J Med. 2015;372(1):11–20. 43. Davis MC, Deveikis JP, Harrigan MR.  Clinical presentation, imaging, and management of complications due to neurointerventional procedures. Semin Intervent Radiol. 2015;32(2):98–107. 44. Papanagiotou P, White CJ. Endovascular reperfusion strategies for acute stroke. JACC Cardiovasc Interv. 2016;9(4):307–17. 45. Akpinar SH, Yilmaz G.  Periprocedural complica tions in endovascular stroke treatment. Br J Radiol. 2016;89(1057):20150267. 46. Bracard S, Ducrocq X, Mas JL, et  al. Mechanical thrombectomy after intravenous alteplase versus alteplase alone after stroke (THRACE): a randomised controlled trial. Lancet Neurol. 2016;15(11):1138–47. 47. Saver JL, Goyal M, Bonafe A, et  al. Stent-retriever thrombectomy after intravenous t-PA vs. t-PA alone in stroke. N Engl J Med. 2015;372(24):2285–95. 48. Bauer AM, Rasmussen PA.  Treatment of intracranial vasospasm following subarachnoid hemorrhage. Front Neurol. 2014;5:72. 49. Masoud H, Nguyen TN, Martin CO, et al. Inadvertent stent retriever detachment: a multicenter case series and review of device experience FDA reports. Interv Neurol. 2016;4(3–4):75–82. 50. Mokin M, Fargen KM, Primiani CT, et  al. Vessel perforation during stent retriever thrombectomy for acute ischemic stroke: technical details and clinical outcomes. J Neurointerv Surg. 2017;9(10):922–8. 51. Leishangthem L, Satti SR. Vessel perforation during withdrawal of Trevo ProVue stent retriever during mechanical thrombectomy for acute ischemic stroke. J Neurosurg. 2014;121(4):995–8. 52. Doerfler A, Wanke I, Egelhof T, et  al. Aneurysmal rupture during embolization with Guglielmi detachable coils: causes, management, and outcome. AJNR Am J Neuroradiol. 2001;22(10):1825–32. 53. Darkhabani Z, Nguyen T, Lazzaro MA, et  al. Complications of endovascular therapy for acute

T. Wang et al. ischemic stroke and proposed management approach. Neurology. 2012;79(13 Suppl 1):S192–8. 54. Yilmaz R, Yuksekbas O, Erkol Z, et  al. Postmortem findings after anaphylactic reactions to drugs in Turkey. Am J Forensic Med Pathol. 2009;30(4):346–9. 55. Brown SG.  Cardiovascular aspects of anaphylaxis: implications for treatment and diagnosis. Curr Opin Allergy Clin Immunol. 2005;5(4):359–64. 56. Kurland DB, Khaladj-Ghom A, Stokum JA, et  al. Complications associated with decompressive craniectomy: a systematic review. Neurocrit Care. 2015;23(2):292–304. 57. Bruder M, Schuss P, Konczalla J, et  al. Ventriculostomy-related hemorrhage after treatment of acutely ruptured aneurysms: the influence of anticoagulation and antiplatelet treatment. World Neurosurg. 2015;84(6):1653–9. 58. Fischer U, Taussky P, Gralla J, et al. Decompressive craniectomy after intra-arterial thrombolysis: safety and outcome. J Neurol Neurosurg Psychiatry. 2011;82(8):885–7. 59. Lee MH, Yang JT, Weng HH, et  al. Hydrocephalus following decompressive craniectomy for malignant middle cerebral artery infarction. Clin Neurol Neurosurg. 2012;114(6):555–9. 60. Waziri A, Fusco D, Mayer SA, et  al. Postoperative hydrocephalus in patients undergoing decompressive hemicraniectomy for ischemic or hemorrhagic stroke. Neurosurgery. 2007;61(3):489–93, 493–494. 61. Ropper AE, Nalbach SV, Lin N, et  al. Resolution of extra-axial collections after decompressive craniectomy for ischemic stroke. J Clin Neurosci. 2012;19(2):231–4. 62. Burn J, Dennis M, Bamford J, et al. Epileptic seizures after a first stroke: the Oxfordshire Community Stroke Project. BMJ. 1997;315(7122):1582–7. 63. So EL, Annegers JF, Hauser WA, et  al. Population-­ based study of seizure disorders after cerebral infarction[J]. Neurology. 1996;46(2):350–5. 64. Creutzfeldt CJ, Tirschwell DL, Kim LJ, et  al. Seizures after decompressive hemicraniectomy for ischaemic stroke. J Neurol Neurosurg Psychiatry. 2014;85(7):721–5.

Contralateral Aneurysm Clipping

11

Ishu Bishnoi

11.1 Introduction Aneurysm clipping is progressively evolving. The neurosurgeons are continuously putting efforts to make it maximum useful. One such effort is “contralateral aneurysm clipping”. Contralateral aneurysm clipping is a method of clipping aneurysm present on the opposite side of craniotomy, e.g., clipping of right MCA aneurysm through left pterional craniotomy. For multiple aneurysms, coiling is preferred as endovascular wires can be advanced into any artery in a single setting, while clipping can be restricted by different locations of aneurysms. Contralateral clipping was one step in achieving the goal—multiple aneurysms clipping in a single setting. The idea of contralateral clipping is not very old. The first case report was published by Nakao et al. in 1981 [1]. They reported successful clipping of carotid-ophthalmic aneurysm in two cases. Few case reports were published in the next 10 years. Oshiro EM et al. first described it properly in 1997 [2]. They did a cadaveric study to define guidelines for contralateral clipping. The idea behind its introduction was “to avoid second craniotomy and coiling”. Anterior communicating artery, A1 and A2 aneurysms were

I. Bishnoi (*) Maharaja Agrasen Medical College, Agroha, Haryana, India

excluded as they can be safely approached from either side. Caplan et  al. have beautifully described this technique in a video uploaded in Neurosurgery Focus journal [3]. This video can help in real-­ time visualization and learning of it. Hernández AR et  al. have described it in 11 patients with bilateral MCA aneurysms [4]. They recommended contralateral aneurysm clipping in short M1, unruptured aneurysm, directed anteriorly or inferiorly and have a simple neck. To simplify contralateral aneurysm clipping, it has been explained in steps—indications, contraindications, method and side effects.

11.2 Indications and Criteria Indication • A patient with multiple anterior circulation aneurysms on both sides. Criteria • Elderly patients as they have cerebral atrophy and thus wide Sylvian fissure. • Small-size aneurysms especially contralateral aneurysm and contralateral aneurysm should be unruptured, directed either anterior or inferiorly. • In case of contralateral MCA aneurysm, a short M1 segment should be present.

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 Y. Kato et al. (eds.), Recent Progress in the Management of Cerebrovascular Diseases, https://doi.org/10.1007/978-981-16-3387-4_11

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90

11.3 H  ow to Plan and Proceed! (Figs 11.1, 11.2, 11.3, 11.4, 11.5, 11.6, and 11.7)

I. Bishnoi

After carefully selecting the case, the anatomy of aneurysms must be studied thoroughly. The pro-

cess of clip application should be planned before surgery. A long clip applicator must be kept to clip on the contralateral side. We have included operative figures of clipping of ipsilateral ICA-­Pcom junction aneurysm and contralateral MCA (M1) aneurysm for explaining the surgical steps.

Fig. 11.1  Ipsilateral optic nerve after opening Sylvian fissure and retracting frontal lobe

Fig. 11.3  Very nice V shaped optic chiasma (blue star), both optic nerves and contralateral ICA (blue dot)

Fig. 11.2  Ipsilateral ICA, Pcom artery origin after wide arachnoid dissection

Fig. 11.4  Contralateral MCA aneurysm (arrow), visualized after tracing M1. Optic chiasma and contralateral ICA (blue dot) can be identified

11  Contralateral Aneurysm Clipping

Fig. 11.5 Clipping of contralateral MCA aneurysm (arrow), ICA (dot)

Fig. 11.6  Ipsilateral ICA-Pcom aneurysm

After doing the usual pterional craniotomy and opening dura, Sylvian fissure should be opened widely from distal to proximal.

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Fig. 11.7  Clipping of aneurysm

The arachnoid dissection must be meticulous and wide. On both sides, optic cisterns, carotid cisterns, Sylvian cisterns and lamina terminalis and interhemispheric cistern must be opened. It will provide a wide view of contralateral aneurysm. The cerebral retraction of the frontal lobe should be used to widen the opening. Special attention must be given to olfactory nerve compression. To expose widely, damage to nerves can occur during retraction. It must be avoided. The retractor must not cross beyond the ipsilateral nerve. After wide opening, the contralateral optic nerve should be dissected, and ICA should be traced along with it. If aneurysm is arising from the ICA-­ ophthalmic junction or ICA-PCom, the contralateral optic nerve should be mobilized by cutting the falciform dural ligament. Contralateral MCA aneurysm requires opening of Sylvian cistern and tracing of M1 from its origin. It is followed till aneurysm. The MCA aneurysm, which is directed either anterior or inferior, can be clipped with ease. If there is a need for a temporary clip, it should be applied on ICA or

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near M1 origin to avoid obstruction of aneurysm view. The aneurysm must be dissected, and the neck must be defined. A permanent clip should be applied after complete visualization of the neck and surroundings. It is preferred to clip contralateral aneurysm first and then ipsilateral aneurysm. Closure is done in the usual way. Advantages • It avoids another craniotomy. • It deals with all aneurysms in a single setting.

Complications • Contralateral optic nerve injury • Anosmia due to excessive pressure of olfactory nerves • Higher chances of rupture of contralateral aneurysm due to extreme location, lesser space for mobilization and control • Excessive cerebral retraction can cause cerebral oedema or ischemia.

11.4 Conclusion Contralateral aneurysm clipping is a good technique to deal with opposite side aneurysms in single sitting with one side craniotomy; however,

it needs meticulous microsurgical skills, wide exposure and correct patient selection.

References 1. Nakao S, Kikuchi H, Takahashi N.  Successful clipping of carotid-ophthalmic aneurysms through a contralateral pterional approach. Report of two cases. J Neurosurg. 1981;54:532–6. 2. Oshiro EM, Rini DA, Tamargo RJ.  Contralateral approaches to bilateral cerebral aneurysms: a microsurgical anatomical study. J Neurosurg. 1997;87:163–9. 3. Caplan JM, Sankey E, Gullotti D, et al. Contralateral approach for clipping of bilateral anterior circulation aneurysms. Neurosurg Focus. 2015;39:V9. Video Suppl 1. https://doi.org/10.3171/2015.7.Focus Vid.14599. 4. Hernández AR, Gabarrós A, Lawton MT. Contralateral clipping of middle cerebral artery aneurysms: rationale, indications, and surgical technique. Oper Neurosurg. 2012;71:116–24.

Multimodality Management of Brain AVMs

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Abhidha Shah and Atul Goel

12.1 Introduction

12.2 Issues in Surgery for AVMs

The treatment of arteriovenous malformations (AVMs) has undergone a wide swing in the last two decades with the emergence of endovascular neuroradiological treatment and the noninvasive method of treatment by radiosurgery [1–4]. Despite this, surgery is the only definitive and ‘curative’ solution to treat AVMs [1]. The location, size, and degree or rate of blood flow in the AVM determines the potential surgical difficulty. Decision regarding the possibility of successful surgical resection of AVM is crucial. The difficulty in the dissection of the nidus, potential of uncontrollable bleeding during the operation, possibility of normal vessel compromise leading to minor or major neurological deficits and death, and several such issues can overpower the psyche of a neurosurgeon. On the other hand, apart from surgery, there is no other proven or accepted treatment for AVM. The role of embolization and gamma knife in the treatment of AVMs is still under intense evaluation.

If surgery can be done safely and the nidus is resected completely, the outcome of treatment is in the best interest of the patient and is the best form of treatment. However, to achieve this outcome, the surgeon has to be confident and experienced in dealing with the issue. Surgery on AVMs requires precise dissection techniques, surgical skills, and experience. However, the increasing trend of subjecting the patients to nonsurgical ‘safer’ methods of treatment by endovascular treatment and by radiosurgery has depleted the total number of AVM cases currently treated by surgery. The important key for the success of surgery in a case with AVM is to select the correct patient.

12.3 Indications for Surgery The symptoms have to be compelling and the nature and architecture of the AVM should be within the realistic surgical domain. Apart from manifest or potential bleeding, severe headache, disabling giddiness, memory disturbance, altered behavior, and uncontrolled convulsions can form indications for surgery.

A. Shah (*) · A. Goel Department of Neurosurgery, Seth G.S. Medical College and K.E.M Hospital, Mumbai, India © The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 Y. Kato et al. (eds.), Recent Progress in the Management of Cerebrovascular Diseases, https://doi.org/10.1007/978-981-16-3387-4_12

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12.4 Surgical Planning Surgery on most AVMs is challenging, and the surgeon has to be well prepared mentally and physically. Surgery has to be based on the exact three-dimensional understanding of the anatomy of the AVM evaluated and studied on available angiographic images. The surgeon has to prepare a road map of surgery. The nidus of the AVM should be drawn, and the major arterial feeders and venous draining vessels should be identified on it. The indicators of difficulties in surgery are related to the location and size of the AVM and the nature and multiplicity of feeding blood vessels. The presence of large arterial feeders, large draining veins, intranidal aneurysmal dilatations of blood vessels, high flow observed during angiography, and presentation of the patient with bleed or with severe headache are suggestions that the AVM will be high flow, bleeding can be excessive, and the dissection can be difficult [1]. The surgical strategy planning has to be based on the anatomical features, location, and flow characters of AVM. The surgeon has to plan prior to surgery as to how he is going to approach the AVM. He has to plan details about which vessels he is going to address early in the operation and which vessels he will avoid. The strategy of saving the venous drainage whilst continuing with the dissection of AVM nidus has to be planned prior to surgery. The surgeon has to be clear that if he has planned to do the case, he cannot withdraw during the case. Voluntary piecemeal AVM resection is not an option. Partial resections are possible in tumors but not in AVMs. Staged resection is not possible and can lead to disasters. When it is decided that the resection can be done, the dissection has to be completed. Backing out during surgery after an incomplete surgery can be dangerous. When a surgeon decides to go in an AVM, he should know clearly as to how he plans to come out of the surgery.

12.5 Type of AVM Nidus The entire surgical procedure on AVMs is dependent on the nature of AVM and the degree of its blood flow. All AVMs have a discrete type of nidus with an individual variety of clinical pre-

sentation and surgery-related issues. Accordingly, it is impossible to classify each variety or type of AVM nidus. The nidus can be of the following types: 1. Small, medium, or large in size 2. Superficial/deep location 3. Located in critical brain areas (motor area/ speech area, visual cortex) 4. Fed by large blood vessels or by multiple small blood vessels 5. Having superficial or deep draining veins 6. Having small or large draining veins 7. Having single or multiple feeders or drainers 8. Having aneurysms in the feeding arterial vessel/s 9. Having intranidal aneurysm 10. Fed by one or more territories (like anterior cerebral artery circulation/middle cerebral artery circulation/posterior cerebral artery circulation/external carotid artery circulation) 11. Located in the ventricle/thalamus/brainstem/ basal ganglia/Sylvian fissure 12. Single or multiple nidus 13. Diffuse nidus

12.6 Case Illustration 12.6.1  Motor Strip AVM 12.6.1.1 Case Description A 46-year-old male patient presented to us with complaints of headache and multiple episodes of seizures for the last 3 years. The convulsions had been increasing in intensity and had become uncontrollable even with anticonvulsant drugs. On neurological examination, the patient had no neurological deficit. The surgery was initially deferred considering the location and ­morphology of the AVM. However, the patient continued to have multiple intractable seizures, and hence, a decision to perform surgery was made. 12.6.1.2 Indication for Surgery Intractable seizures formed a major indication for surgery in this case.

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12.6.1.3 Imaging Digital subtraction angiography forms the baseline investigation. This investigation cannot be avoided even if other investigations show the AVM clearly. CT angiography is of great help in identifying the size and location of the AVM. The entire AVM is visualized in one picture. The arteries, veins, and the nidus overlap and provide a surgical image of the AVM.  MRI assists in localizing the AVM in relationship to the brain parenchyma. We sometimes use 3D printed models for a three-dimensional understanding of the AVM [5]. The model assists in identifying the size, location, and number of the feeding vessels in a three-dimensional perspective. As the model is contoured as per the patient’s anatomy, the craniotomy can be planned with precision depending on the location of the AVM.  The model is placed in the exact surgical position as the patient during the actual operation and serves as a guide for the vascular anatomy during the surgery. Secondly, along with the abnormal vessels, the relevant normal vessels and their location with respect to the AVM are clearly visualized. In this patient, MRI revealed a compact arteriovenous malformation in the left medial posterior superior frontal gyrus (supplementary motor area) with its posterior margin just abutting the precentral gyrus. (Fig.  12.1a) CT angiography showed the compact nidus in the medial frontal brain with multiple venous aneurysms. (Fig. 12.1b–e) A fourvessel angiography showed the high flow AVM fed by branches of the anterior cerebral artery, middle cerebral artery, and choroidal arteries. (Fig. 12.2a–c) The AVM was also found to be filling from the right anterior cerebral artery through the anterior communicating artery. The venous drainage was through the vein of Galen into the straight sinus and the transverse sinus.

Grade 3: Very difficult and risky but possible Grade 4: Not safe or possible due to the type and site of AVM This can be called a ‘dynamic’ classification as grading of AVM will vary for each surgeon and the grading will change as the experience of the surgeon increases. The present case is Grade 3 AVM.

12.6.2  Surgical Planning

12.8 Assessment of a Case for Surgery

12.6.2.1 Goel’s Classification of AVMs We have classified AVMs according to the extent of possible difficulties that can be encountered during surgery [1]. Grade 1: Easy Grade 2: Difficult but possible

12.6.2.2 Spetzler-Martin Grading of Arteriovenous Malformation Spetzler and Martin in 1986 proposed a grading system for arteriovenous malformations to determine the feasibility of surgical resection. The AVMs were graded based on their size, eloquence, and pattern of venous drainage. Graded feature Size of AVM Small (6 cm) Eloquence of adjacent brain Non-eloquent Eloquent Pattern of venous drainage Superficial only Deep

Points assigned 1 2 3 0 1 0 1

The AVMs were graded from 1 to 5 based on the score obtained on summing the points in each category.

12.7 Preoperative Embolization The authors do not prefer preoperative embolization in the management of AVMs. Such a procedure can have its own potential complications and does not significantly alter the course of surgery or reduce the extent and intensity of bleeding.

Apart from the patient and the angiographic issues, there can be no other consideration in decision-making regarding the indication for surgery. Any wrong decision can be dangerous for the patient and make the surgical procedure look

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a

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Fig. 12.1  Preoperative images (a) T2 weighted axial image of MRI showing the compact AVM nidus in the left posterior medial superior frontal gyrus abutting the precentral gyrus. (b) Sagittal image of CT angiography showing the arteriovenous malformation being fed by

branches of the anterior cerebral artery. (c) Coronal image showing the AVM in the medial frontal region. (d) Axial image showing the AVM nidus. (e) 3D reconstructed image of CT angiography showing the AVM with multiple venous aneurysms

regretful and the outcome unacceptable to the patient, family, and the surgeon himself.

in an AVM. In the presented case, there were several of these factors that indicated the high degree of blood flow:

12.9 Issues in Planning of Surgery

1 . The larger the AVM, the higher the flow. 2. The more the number of feeding arterial territories, the higher the flow. 3. Patients presenting with bleed, severe headache, and focal neurological deficits have higher flow. 4. The larger the draining veins, the higher the degree of flow. 5. AVMs having aneurysms in the feeding artery have higher flow. 6. AVMs with intranidal aneurysms have higher flow.

The anesthetist is informed about the extent of possible blood loss. Although some surgeons recommend the need for hypotensive anesthesia, the authors do not prefer any alteration of blood pressure during the surgical procedure.

12.10 Indicators of High-Flow AVM Degree of flow in the AVM is the more critical factor that determines the course of the surgery. The following factors indicate the degree of flow

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Fig. 12.2 Preoperative four-vessel DSA images (a) Lateral view of left carotid injection showing the arteriovenous malformation being fed by the anterior cerebral artery. (b) Oblique view of angiogram showing the arteriovenous malformation being fed by both the anterior

cerebral and middle cerebral arteries. (c) Venous phase of angiogram showing the arteriovenous malformation with venous aneurysms draining via the straight sinus into the transverse sinus

12.11 Surgical Technique

craniotomy was performed, and the interhemispheric fissure was opened, and the abnormal vasculature of the AVM was visualized. The central sulcus was identified by using strip electrodes and phase reversal and appropriately marked. The AVM resection was then commenced. The major feeders from the anterior cerebral artery were identified and handled first. The AVM with its large aneurysmal venous dilatations were exposed dissected and separated

The exposure should be wide and elaborate and should extend significantly beyond the extent of the nidus. Small, micro, or mini exposure will not be appropriate in cases with AVMs. The patient was placed in a supine position with the head turned to the right for a left frontoparietal interhemispheric exposure with intraoperative neurophysiological monitoring. The

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from the surrounding brain parenchyma. The feeders from the middle cerebral artery and intraventricular choroidal feeders were identified and coagulated amidst furious bleeding. The AVM was then disconnected from its venous drainage and excised. The transcranial MEPs were checked intermittently during surgery and finally at the end of surgery. During the dissection, a decline in MEP was observed; however, in view of the ferocious bleeding, the AVM resection had to be continued and completed. The bottom line of successful surgery is to distinguish the feeding vessels from normal blood vessels. Whenever identification of the normal from feeding arterial blood vessels is difficult, a temporary clip may be applied to the artery prior to considering coagulation and cutting of the vessel. Whenever there is doubt, the surgeon should follow the vessel right up to the AVM nidus before coagulation. The operation is essentially conducted by dissection around the AVM in a circumferential manner. The dissection of the AVM is progressive and circumferential and ultimately aims to resect the nidus completely.

A. Shah and A. Goel

12.13 Complication Avoidance 12.13.1  C  ontrol of Bleeding During Surgery

The dissection of the AVM has to be conducted like a vascular tumor. The plain of the dissection has to be identified, and the dissection has to continue around the AVM nidus without actually entering within its confines. The entire operation involves control of bleeding from large vessels, medium-sized vessels, and small vessels. The large vessels feeding the AVM have to be identified, differentiated from normal blood vessels, coagulated, and then cut. Bleeding can sometimes be from more than one point. Bleeding can be quite furious in highflow AVMs. The surgeon has to maintain his composure and continue and progress in his dissection. Extensive coagulation of the region can be counter-effective. In high-­flow AVMs, it may sometimes appear as if the bleeding is getting out of control, and patience and persistence are necessary to control the situation. Larger feeding vessels should first be identified; they are coagulated for a significant length and then cut. Whenever necessary or when it is felt that 12.12 Postoperative Care the flow in the vessel is significant and the vessel can open up despite coagulation, liga or siland Outcome ver clips should be applied on both sides of the The patient was placed on conventional postop- cut vessel. The dissection has to proceed and erative drugs. No special drugs are given that will progress and has to be completed. Small blood increase or decrease his blood pressure. As in vessels are frequently encountered and can be most neurosurgical cases, the first 48 h after sur- the most difficult to control. The vessels are gery are crucial and will determine the outcome. thin-­ walled and are difficult to coagulate. If the patient is well for 48 h, he can be considered Frequently, it is these small vessels that can out of danger and ‘cured’. Postoperative angiog- cause significant blood loss. The understanding raphy is generally done after about 2  weeks of of these vessels forms the major basis of undersurgery. standing the surgery of AVM and executing its In the present case, the patient developed a complete resection. It is necessary that these typical SMA syndrome following surgery, right-­ ‘small’ bleeding vessels are identified and folsided limb weakness, and aphasia. The patient lowed towards the feeding ‘mother’ vessel that improved over a period of months but still has is coagulated. It may be waste of time to attempt some residual deficits at follow-up of 2 years. A to coagulate these small vessels as it is difficult postoperative angiogram showed complete exci- to coagulate them, and it is difficult to even stop sion of the AVM (Fig. 12.3a–c). their bleeding by pressure. Moreover, an oppor-

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Fig. 12.3  Postoperative images (a) Postoperative CT angiogram showing complete excision of the arteriovenous malformation. (b) Postoperative anteroposterior

view of CT angiogram. (c) Resected specimen of the arteriovenous malformation

tunity to identify a major feeding vessel can be lost. Understanding the fact that intraventricular feeding vessels can be a source of major supply to the AVM makes the surgeon alert during the terminal phase of operation.

general, the theory of normal pressure breakthrough bleeding appears to be flawed. Postoperative bleeding appears to be a consequence of incomplete resection of the AVM.

12.13.2  Postoperative Bleeding

12.14 R  ole of Awake Craniotomy and Brain Mapping

If the AVM has been completely resected, postoperative bleeding is a rare phenomenon. Although, several authors have discussed the issue of normal pressure breakthrough bleeding, meaning thereby that the extra load on the adjoining normal blood vessels after the resection of the AVM can lead to their rupture [6]. In

With advances in microsurgery and neuroanesthesia, awake craniotomy and neurophysiological monitoring have been recommended for AVMs in eloquent regions of the brain [7, 8]. The mapping allows for the identification of the eloquent motor or speech area permitting safe dissection of the AVM nidus and preventing

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unwanted neurological deficits. Suspicious or en passage vessels can be distinguished from vessels feeding the nidus by temporary clipping and watching for any neurological or neurophysiological change during surgery.

12.15 Preoperative Embolization Endovascular embolization has mainly an adjunctive role in the management of AVMs as the obliteration rate is only 13% with associated peri-procedural morbidity of −20% and a 1–3% risk of mortality [9, 10]. Embolization may be considered safe in AVMs that have a non-­eloquent location, a low number of feeding vessels, the lack of direct arteriovenous fistula, small size, arterial feeders that directly feed the nidus, feeders whose size and location are amenable to selective catheterization, a safe distance between the arterial feeders and the nidus, and multiple small but identifiable draining veins. Presently, embolization is used as a preoperative adjunct before surgery or prior to stereotactic radiosurgery. The results of this modality of treatment are varied, and no definite conclusion can be drawn. Embolization has been used to treat aneurysms and venous ectasias in high-flow AVMs that are not amenable to any other form of treatment. However, the benefits of this treatment have to be weighed against the risk of increased hemorrhage from a partially treated AVM. At our center, we do not use embolization in the management of AVMs. Many surgeons prefer preoperative embolization of the feeding vessels or of the nidus. The author’s personal experience suggests that embolization should be avoided; it can sometimes have its own set of complications and does not remarkably assist in controlling the blood loss during surgery. Moreover, complete obliteration of AVM is only rarely possible. And incomplete obliteration has little clinical value, both in the reduction of long-term bleeding rate and also in the resolution of symptoms. The authors who find preoperative embolization useful advocate its following usefulness:

1 . Some AVMs can be completely embolized. 2. The feeding AVM vessels that are relatively difficult to approach or are located in depth can be safely embolized. 3. ‘Weak’ points within the AVM nidus, like intranidal aneurysm or arteriovenous fistula, can be obliterated by embolization. 4. Aneurysm located on the feeding arterial vessel can be embolized. Although the concept and usefulness of embolization of aneurysms and dural fistulae have now been established beyond doubt, indications of embolization for AVM have not been entirely convincing and the subject has remained under intense discussion. As far as the authors are concerned, preoperative embolization does not seem to be of great surgical help. Although may not be correct, but it appears that such embolization can even have some negative issues in that the bleeding subsequently occurs from some otherwise smaller blood vessels that possibly take up the brunt of supplying blood to the AVM.

12.16 Stereotactic Radiosurgery Gamma knife radiosurgery has been used as an alternative to surgery in patients with small-size AVMs, for AVMs located in eloquent regions, and for deep-seated AVMs. The mechanism is by causing vascular thrombosis and occlusion, which usually occurs over a period of 2–3 years. In a recent multicenter cohort study, the overall obliteration rate was 65% with symptomatic and permanent radiation-induced changes of 9% and 3%, respectively [11, 12].

12.17 Conclusions Surgery for AVMs of the brain has a defined role in the management. Surgery is difficult and on occasion dangerous; however, if appropriately planned and meticulously executed, the outcome can be gratifying, and cure from the problem of AVM can be achieved.

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References 1. Goel A. Arteriovenous malformations: current status of surgery. Neurol India. 2005;53:11–35. 2. Kato Y, Dong VH, Chaddad F, et al. Expert consensus on the management of brain arteriovenous malformations. Asian J Neurosurg. 2019;14(4):1074–81. 3. Lawton MT, Abla AA. Management of brain arteriovenous malformations. Lancet. 2014;383(9929):1634–5. 4. Goel A. Bilateral parafalcine approach for arteriovenous malformations located in the interhemispheric fissure. In: Kobayashi S, Goel A, Hongo K, editors. Neurosurgery of complex tumours and vascular lesions. New  York: Churchill Livingstone; 1997. p. 143. 5. Shah A, Jankharia B, Goel A.  Three-dimensional model printing for surgery on arteriovenousmalformations. Neurol India. 2017;65(6):1350–4. 6. Spetzler RF, Hargraves RW, McCormick PW, et  al. Relationship of perfusion pressure and size to risk of hemorrhage from arteriovenous malformations. J Neurosurg. 1992;76:918–23. 7. Abdulrauf SI.  Awake craniotomies for aneurysms, arteriovenous malformations, skull base tumors, high

101 flow bypass and brainstem lesions. J Craniovertebr Junction Spine. 2015;6(1):8–9. 8. Gabarrós A, Young WL, McDermott MW, Lawton MT. Language and motor mapping during resection of brain arteriovenous malformations: indications, feasibility, and utility. Neurosurgery. 2011;68(3):744–52. 9. Perret G, Nishioka H. Report on the cooperative study of intracranial aneurysms and subarachnoid hemorrhage. Section VI. Arteriovenous malformations. An analysis of 545 cases of cranio-cerebral arteriovenous malformations and fistulae reported to the cooperative study. J Neurosurg. 1966;25:467–90. 10. Chang SD, Marcellus ML, Marks MP, et  al. Multimodality treatment of giant intracranial arteriovenous malformations. Neurosurgery. 2003;53:1–11, discussion 11–13. 11. Kano H, Lunsford LD, Flickinger JC, et  al. Stereotactic radiosurgery for arteriovenous malformations, part 1: management of Spetzler-Martin Grade I and II arteriovenous malformations. J Neurosurg. 2012;116:11–20. 12. Fokas E, Henzel M, Wittig A, et al. Stereotactic radiosurgery of cerebral arteriovenous malformations: long-term follow-up in 164 patients of a single institution. J Neurol. 2013;260:2156–62.

Superficial Temporal Artery-­ Middle Cerebral Artery Bypass Combined with Encephalo-Duro-­ Myo-Synangiosis in Treating Moyamoya Disease

13

Bin Xu, Yujun Liao, Hong Xu, and Chuanghong Liu

13.1 Skin Incision An enlarged pterional incision was used in a routine procedure. The skin incision was curved posteriorly to include both anterior and posterior branches of STA (a-STA and p-STA) in the flap and extended by 1.0–1.5 cm above the superior temporal line (Fig.  13.1). The length of p-STA would be sufficient for anastomosis with any of the cortical arteries in the bone window. In some cases, occipital artery or post-\auricular artery would be used as a substitute, and the skin flap would be adjusted to include donor artery, usually extended posteriorly by 2 cm. For tailored adjustment, skin incision would be moved forward or backward, either to avoid injury to the skin artery with preexisted spontaneous collaterals or to cover ischemic areas. For example, a horseshoe-shaped incision in the temporal-­parietal-occipital lobe would be used in cases with severe ischemia in the occipital lobe, and a coronal incision would be a better choice for bi-frontal ischemia.

13.2 Temporal Muscle and Bone Flap The temporal muscle was separated from the temporal bone as a whole, usually 0.5  cm less than the skin flap, to protect the entire deep temporal artery (DTA) network on the deep surface of the muscle. A bone flap 0.5  cm less than the temporal muscle flap was used as a routine. When cutting bone flap around the sphenoidal crest, the middle meningeal artery (MMA) should be protected well since it’s a potential source of indirect anastomosis. Usually, a sphenoidal crest residue would be a good way to achieve this (Fig. 13.2). In the case of well-formed anastomosis from MMA, double-window bone flaps would be a better choice. Bone flaps anterior and posterior to MMA would be formed respectively, with a bone bridge left to cover the course of MMA.  It’s proved to be an effective and quick method to preserve MMA. As mentioned before, bi-frontal bone flaps would be opened in patients with bi-­ frontal ischemia.

13.3 Dura B. Xu (*) · Y. Liao Department of Neurosurgery, Huashan Hospital, Fudan University, Shanghai, P. R. China H. Xu · C. Liu Department of Neurosurgery, Changshu First People Hospital, Suzhou University, Suzhou, P. R. China

The MMA trunk and its main branches were preserved intact and incised on both sides. Dura mater strips with a width of 0.5–1.0 cm could be formed. The remaining part of the dura mater

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would be cut using radial incisions. After hemostasis, the dura mater would be flipped over and spread over the bone window with its outer surface (with vessel network) in close contact with the cortical surface (Fig. 13.3). The flip-over of the dura mater should be skipped in the existence of preoperative spontaneous anastomoses between dura and cortex in the convexity of a hemisphere, more commonly

Fig. 13.1  Skin incision. An enlarged pterional incision was used to include both branches of STA in the flap and extended by 1.0–1.5 cm above the superior temporal line

Fig. 13.2  Temporal muscle and bone flap. Left: The temporal muscle was dissected from the cranium with an intact deep temporal artery (DTA) network. Right: Fronto-­

seen in late-stage patients. In some cases, the “Chinese spring roll” technique is helpful in the hemostasis of dura veins, by suturing the dura into the shape of a barrel (with the cortical surface facing outside) containing the MMA, the accompanying veins, and some gelatin sponge (Fig. 13.3).

13.4 Skin Artery Dissection Usually, the p-STA would be a better choice as a donor artery, because of fewer branches, relatively straight course, and a safe distance to facial nerves. The artery would be incised with low-­ power monopolar, leaving 0.5 cm strips on both sides to avoid injuries, and then, it would be cut and dissected in a proper length according to the site of the recipient artery. Normally, the harvest of the donor artery could be finished within 10 min, because it could be observed clearly from the inner surface of the skin flap. During closure, the artery bed in the skin flap should be repaired with autologous facial to prevent delayed necrosis or infection, because of potential ischemia after the removal of STA (Fig. 13.4). The occipital artery or postauricular artery would be harvested in the same way.

temporal bone flap was formed with sphenoidal crest residue (blue star) to preserve MMA

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13.5 Selection of the Cortical Arteries for Anastomosis

Fig. 13.3  Dura processing. The MMA trunk and its main branches were preserved intact. “Chinese spring roll” technique in the hemostasis of dura veins (blue star)

a

A cortical branch of the middle cerebral artery (MCA) in good match with STA, usually 1 mm in diameter (or at least 0.6 mm), would be selected as recipient artery. A better candidate should also have fewer branches and a relatively straight course as well. In some cases, both branches of the STA would be dissociated for double-barrel bypass. Usually, the cortical branches were extremely thin in MMD patients, with congestion of very small arteries. And arteries on the site of the infarcted brain shouldn’t be selected as recipient artery (Fig. 13.5). b

c

Fig. 13.4 Skin artery dissection and repair of skin wound. (a) The p-STA was incised with low-power mono-­ polar, leaving 0.5 cm strips on both sides. (b) The p-STA

was cut and dissected in a proper length according to the site of the recipient artery. (c) The artery bed in the skin flap was repaired to prevent delayed necrosis or infection

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Fig. 13.5  Selection of the cortical arteries for anastomosis. (a) Extremely thin cortical branches in MMD patients. (b and c) Infarcted gyrus in subacute phase (blue star in b) and old infarctions (blue circle in c)

13.6 Artery Anastomosis The outer facial would be cut, and the lumen would be rinsed with pressurized normal saline containing heparin. After that, the p-STA would be anastomosed with the cortical artery in an end-­ to-­side fashion using a single 10–0 nylon suture, with interrupted sutures. After the anastomosis, Doppler ultrasound and indocyanine green (ICG) fluorescence angiography were performed to verify the patency of the anastomotic stoma (Fig. 13.6).

13.7 T  emporal Muscle Processing and Bone Fixation The temporal muscle would be sutured with the dura mater and then fixed to the bone window. As the bone flap and the temporal muscle exchanged positions in the operation, the lower part of the bone flap would be cut to avoid compression of the temporal muscle and donor artery. In patients with hypertrophic muscle, the inferior edge of the bone flap should be elevated to some extent to reduce compression also (Fig. 13.7).

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Fig. 13.6  Artery anastomosis. (a–c) Stomas with interrupted sutures. (d) Indocyanine green (ICG) fluorescence angiography to confirm bypass patency

Fig. 13.7  Temporal muscle processing and bone fixation

13.8 Postoperative Management and Follow-Up The baseline blood pressure should be maintained throughout the entire treatment. No hemostatic

agent, antithrombotic or anticoagulant, would be administered postoperatively. Within 1 week after operation, CT angiography (CTA) would be performed to verify the patency of bypass, CT perfusion (CTP) to evaluate h­emodynamic changes.

B. Xu et al.

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Neurological examinations were carried out as a routine, including intelligence, linguistic ability, motor functions, and sensory functions. In a sixmonth follow-up, DSA was performed to examine bypass patency and development of indirect bypass, CTP to evaluate long-­term hemodynamic changes. Then, the patients were followed in the outpatient department by CTA, CTP, and neurological examinations.

a

Follow-up DSA demonstrated significant increase in diameter in all ECA branches, including STA, MMA, and DTA. The perfusion area of ECA would be developing continuously after surgery, covering almost all the MCA territory. Sometimes, the reconstructive blood flow may even perfuse the entire anterior circulation (Fig. 13.8).

b

c Fig. 13.8  Follow-up DSA. (a) Significant increase in diameter of all ECA branches, including STA, MMA, and DTA. (b) Blood flow redistribution between ICA (red)

and ECA (green). (c) Bilateral anterior circulation was totally perfused by blood flow from ECA

Stereotactic Radiosurgery for Brain AVM

14

Enmin Wang

14.1 Introduction Brain arteriovenous malformations (bAVMs) are rare congenital lesions in which blood flow is shunted from feeding arteries to draining veins through a pathological nidus, rather than through the normal capillary network of the brain. Brain AVM is often embedded within the parenchyma of the central nervous system. The etiology of bAVMs is incompletely understood, but the current thought is that they represent nests of abnormal regression in the fetal vasculature [1–3]. Brain AVMs vary in size, location, and angioarchitecture. They are frequently supplied by multiple arterial pedicles causing abnormally high flow and pressure within the nidus and draining veins (Fig.  14.1). The abnormal hemodynamic forces within the bAVM and surrounding vasculature can result in intracranial hemorrhage. From epidemiological studies, the incidence of AVMs ranges from 1.12 to 1.42 cases per 100,000 person-years. Annual rates of hemorrhage in untreated bAVMs have been estimated at E. Wang (*) Cyberknife and Gamma Knife Center, Department of Neurosurgery, Huashan Hospital, Fudan University, Neurosurgical Institute of Fudan University, Shanghai, China Shanghai Key Laboratory of Brain Function and Restoration and Neural Regeneration, Shanghai, China e-mail: [email protected]

2.10–4.12% with combined annual morbidity and mortality of approximately 1% [4, 5]. Although these lesions are approximately 10 times less common than intracranial aneurysms, they account for 2% of all strokes and 38% of intracerebral hemorrhages in patients between 15 and 45 years of age. Approximately two-thirds of brain AVMs occur before the age of 40 [4–6]. Many bAVMs are identified because of the sudden onset of intracranial hemorrhage, which can be fatal or merely lead to serious headaches with or without new neurological deficits. Patients may also have seizures or headaches. Seizures occur as the presenting symptom in 25–50% of patients with AVM. These may be focal or secondary generalized seizures. Headache occurs in 10–50% of patients with AVM.  The number of incidentally discovered brain AVMs keeps gradual rising as more patients undergo magnetic resonance imaging (MRI) of the head [7, 8].

14.2 AVM Management Treatment options for patients diagnosed with bAVMs are aimed at reducing the risk of intracranial hemorrhage. The management of options includes observation, surgical resection, endovascular embolization, and stereotactic radiosurgery (SRS) (Fig.14.2). Treatment decisions need to be based on an understanding of the natural history of the AVM, as well as the risks and

© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021 Y. Kato et al. (eds.), Recent Progress in the Management of Cerebrovascular Diseases, https://doi.org/10.1007/978-981-16-3387-4_14

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E. Wang

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Fig. 14.1  A 29-year old female patient had once seizure attack. MRI examination incidentally found a left-side frontal lobe AVM. Digital subtraction angiography dem-

onstrates the three main components of an AVM: arterial feeding artery (white arrow), nidus (red arrow), draining vein (yellow arrow) into the sagittal sinus

Craniotomy Resection Small AVM lobar location

Small AVM deep location

2nd resection Residual AVM

Embolization

Radiosurgery

Radiosurgery

Residual AVM

2nd radiosurgery

Radiosurgery

Residual AVM

2nd radiosurgery

Observation Resection Patients with Cerebral AVM (unruptured)

Large AVM lobar location

Embolization

Residual AVM Radiosurgery

Staged radiosugery

Observation Large AVM deep location

Staged radiosurgery+/ -embolization Resection

Patient’s choice

Radiosurgery

Fig. 14.2  Proposed management algorithm for patients with brain AVM

Residual AVM

2nd radiosurgery

14  Stereotactic Radiosurgery for Brain AVM

expectations of surgery, radiosurgery, and embolization. In addition, these treatment modalities can be combined. Kim and colleagues, using results from combined series of more than 2500 untreated bAVMs, reported a lower risk of rupture for unruptured bAVM with an annual first hemorrhage rate of 1.3% (95% CI, 1.0–1.7%) [9]. In the recent study (ARUBA, A Randomized Trial of Unruptured Brain Arteriovenous Malformation) on 223 patients with unruptured brain AVMs, the risk of death or stroke was significantly lower in the medical management group (patients were symptomatically treated) than in the interventional therapy group, after a mean follow-up of 33 months [10]. Despite the failure to randomize a large number of eligible patients, the lack of standardized treatments, and short follow-up, its results have been widely spread, and conservative management is considered by many as the best treatment option, especially for patients who have never bled and have large-volume, deep location AVM [11, 12]. Endovascular embolization of bAVMs as primary treatment has been utilized for more than 10 years [13, 14] but is more often performed in conjunction with either surgical resection or SRS.  Traditionally, surgical resection has been the only treatment for these lesions. However, with the development of minimally invasive techniques including embolization and SRS, AVM treatment plans have become more complex and frequently require a multimodality approach. Resection is often the first option recommended for patients with smaller AVMs in noncritical areas of the brain. Patients who present a large intracranial hemorrhage require surgical evacuation to remove the hematoma with mass effect. The benefit of surgical resection compared to radiosurgery is the immediate elimination of future hemorrhage risk. AVM location is an important factor to consider when weighing the relative risks of surgical versus nonsurgical treatment. The Spetzler-Martin(SM) grading system has been accepted as an accurate method to predict patient outcomes after resection at centers with extensive vascular expertise. This grading scale is based on AVM size, AVM

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location, and the pattern of venous drainage [15, 16]. Selected reports from such centers indicate that surgery for SM Grade I and II AVMs may be associated with no morbidity or mortality. Not all low-grade AVMs may have the same prognosis. For example, a Grade II AVM (small with superficial venous drainage) located within the motor cortex may be associated with at least temporary contralateral motor weakness after surgical removal [17–19]. Additionally, patients are medically unfit to tolerate the physiologic burden of r­ esection, or patients are unwilling to undergo an invasive neurosurgical procedure.

14.3 AVM Radiosurgery Techniques Brain AVMs are one of the earliest indications for stereotactic radiosurgery. In 1972, Steiner and colleagues from the Karolinska Institute first reported that single fraction, high-dose irradiation caused the progressive obliteration of AVMs and subsequent cure from the risk of later hemorrhage [20]. Since the initial use of Gamma Knife® (GK) (Elekta, Stockholm, Sweden) to treat an AVM, developments in adjunct technologies such as digital subtraction angiography and MRI imaging have greatly improved SRS targeting and dose planning. Additional radiosurgical devices followed Gamma Knife as treatment options for AVM, including the linear accelerator (LINAC), proton beam radiosurgery, and more recently CyberKnife radiosurgery (Accuray, Sunnyvale, CA, USA), a frameless system. Over the past 40 years, more than 100,000 patients have undergone Gamma Knife radiosurgery for brain AVM, and it is accepted as an important treatment modality for this group. In this part, we introduce two stereotactic techniques which are Leksell Gamma Knife® and CyberKnife® radiosurgery. Leksell Gamma Knife is the first technology with image-guided stereotactic radiosurgery, allowing for the treatment of virtually any target in the brain with ultrahigh precision. There are two types of Leksell Gamma Knife device in clinical practice, Leksell Gamma Knife Perfexion

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and Leksell Gamma Knife Icon (Fig. 14.3). The Icon introduces a number of new innovations, such as integrated imaging and software for the continuous control of dose delivery. It also makes it possible to treat patients with frameless immobilization while assuring the same highest level of precision. The high-definition motion management system monitors the patient in real time during treatment with an accuracy of 0.15 mm. If the patient moves outside the preset threshold, the system’s gating functionality instantly blocks the radiation. Although the definition of SRS has been modified to include treatment in 1–5 fractions, the majority of patients with intracranial AVMs treated with Leksell Gamma Knife are treated in a single fraction. Leksell Gamma Plan is a treat-

Fig. 14.3  Leksell Gamma Knife Icon Fig. 14.4 CyberKnife® (Accuray Inc., Sunnyvale, California)

E. Wang

ment planning system. A full treatment plan can take just a few minutes to complete, even for complex cases. Dose sculpting enables precise handling of complex targets, and with dynamic shaping, critical structures are protected. The goal of AVM planning is to create a conformal dose plan that precisely covers the shape of the nidus. Feeding arteries and draining veins are not included in the dose plan if possible. Dose prescription must take into account two conflicting considerations: the chance of obliteration versus the chance of radiation-related complications. Increasing radiation dose directly correlates with the chance of obliteration. But higher radiation dose increases the complications. Recent studies have shown that the probability of radiation complications after AVM SRS is related to a radiation dose of the surrounding normal tissues [21]. Patients who undergo Gamma Knife radiosurgery most often have AVMs with an average diameter less than 3  cm (Volume: 0.1–10  cm3). The optimal dose range for AVM Gamma Knife radiosurgery has been largely established based on the location and volume of the AVM. Doses at the margin of the AVM typically range from 16 to 25 Gy in a single fraction. The CyberKnife® (Accuray Inc., Sunnyvale, California) is a relatively recently developed neurosurgical device consisting of a frameless, robotic linear accelerator that can be used to deliver radiation to highly targeted regions of the brain parenchyma (Fig.14.4). CyberKnife System

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follows the target throughout the treatment, intelligently delivering treatments with submillimeter precision. CyberKnife System is versatile and can deliver beams from thousands of noncoplanar, isocentric, or non-isocentric angles. Treatments demonstrate excellent tumor coverage, steep dose gradients, and tight dose conformity, regardless of the target shape. Depending on the type of tumor being treated, the CyberKnife uses different targeting and tracking methods. Six-Dimension Skull Tracking System uses the bony anatomy of the skull to continuously track intracranial targets and automatically correct even for the slightest translational or rotational target shift during the treatment delivery. In our center, we usually deliver radiation doses in two to three fractions according to the AVM volume and location.

orrhage rate [22]. A multivariate analysis of 220 patients similarly identified small AVM volume as a predictor for successful SRS, defined as nidus obliteration without new neurologic deficit [28]. Thus, the ideal candidate for SRS treatment would be a patient with an AVM that is less than 3.0 cm in diameter, either symptomatic or previously ruptured, and located in deep regions. For individual patients, a comparison of the chance of AVM elimination without risk of new deficits by surgical resection versus that by radiosurgery should be undertaken. Standardized scales such as the Spetzler-Martin grade, radiosurgery-­ based AVM score (RBAS), and Virginia Radiosurgery AVM Scale (VRAS) can be used to estimate the efficacy of surgical resection and radiosurgery, respectively, for individual AVM patients.

14.4 Indications for the Use of SRS in AVMs

14.5 Grading Systems of Brain AVM

Surgical resection has traditionally been the first-­ line therapy for low-grade AVMs in superficial brain regions due to its highly effective and immediate AVM obliteration [22]. Patients with a recent intracranial hemorrhage and a surgically accessible AVM are best managed with surgical resection. However, resection can be challenging to accomplish in deep locations, where it carries a higher risk of morbidity and mortality. Proper patient selection is important for successful AVM radiosurgery. In particular, a number of factors must be taken into consideration when discussing radiosurgery for AVM patients, including their age, presentation, AVM size, and AVM location. However, patients with a surgically inaccessible small volume AVM are generally good candidates for radiosurgery. SRS is a widely used alternative recommended for small- to medium-­ sized AVMs less than 3 cm in diameter(volume 4 = 2 Non-eloquent = 0 Eloquent location =1

0.02 * (patient age, years) Unruptured = 0 point Ruptured =1 point

14.6 Outcomes of SRS for AVMs The goal of SRS is to provide nidus obliteration without new neurologic deficits from either postradiosurgery hemorrhage or adverse radiation effects(ARE). Unlike surgical resection, which provides protection from future intracranial hemorrhage immediately, SRS requires a latency period measured as years before the arteriovenous shunting is stopped and the risk of intracranial hemorrhage is eliminated. During the latency period of typically 1–3 years between SRS treatment and complete obliteration, the patent nidus remains at risk of hemorrhage. A study of 1204 patients treated with Gamma Knife found latency period hemorrhage to be reduced compared with hemorrhage rate from diagnosis to treatment. Overall preradiosurgical annual hemorrhage rate was 2.0% from birth or 6.6% from AVM diagnosis, and corresponding rates were higher in the subset of patients who initially presented with hemorrhage (3.7% from birth and 10.4% from diagnosis) [35]. Obliteration rates depend on a multitude of factors relating to AVM characteristics and treatment parameters, and they vary widely from 50% to 90% in reported studies. Flickinger et  al. analyzed the radiosurgery outcomes for 197 AVM patients with >3  years

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of angiographic follow-up to determine the ­relationship between dose and obliteration. The median target volume, radiosurgical margin dose, maximum dose, isodose line, and the number of isocenters were 4.1  cm3, 20  Gy, 36 Gy, 50%, and 2, respectively. A multivariate analysis for independent predictors of in-field obliteration identified only margin dose (p