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Acta Neurochirurgica Supplement 132

Giuseppe Esposito · Luca Regli · Marco Cenzato


Yasuhiko Kaku · Michihiro Tanaka
Tetsuya Tsukahara Editors

Trends in
Cerebrovascular
Surgery and
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Interventions

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Acta Neurochirurgica Supplement 132

Series Editor
Hans-Jakob Steiger
Department of Neurosurgery
Heinrich Heine University
Düsseldorf, Germany
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
ACTA NEUROCHIRURGICA’s Supplement Volumes provide a unique opportunity to publish
the content of special meetings in the form of a Proceedings Volume. Proceedings of
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Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Giuseppe Esposito • Luca Regli
Marco Cenzato • Yasuhiko Kaku
Michihiro Tanaka • Tetsuya Tsukahara
Editors

Trends in Cerebrovascular
Surgery and Interventions
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Editors
Giuseppe Esposito Luca Regli
Department of Neurosurgery, Clinical Department of Neurosurgery
Neuroscience Center Clinical Neuroscience Center
University Hospital Zurich, University of Zurich University Hospital Zurich, University of Zurich
Zürich, Switzerland Zürich, Switzerland

Marco Cenzato Yasuhiko Kaku


Department of Neurosurgery Department of Neurosurgery
Ospedale Niguarda Ca' Granda Asahi University Hospital
Milan, Italy Gifu, Japan

Michihiro Tanaka Tetsuya Tsukahara


Department of Neuroendovascular Surgery Department of Neurosurgery
Kameda Medical Center Kyoto Medical Center
Chiba, Japan Kyoto, Japan

This book is an open access publication.

ISSN 0065-1419     ISSN 2197-8395 (electronic)


Acta Neurochirurgica Supplement 132
ISBN 978-3-030-63452-0    ISBN 978-3-030-63453-7 (eBook)
https://doi.org/10.1007/978-3-030-63453-7
Copyright © 2021. Springer International Publishing AG. All rights reserved.

© The Editor(s) (if applicable) and The Author(s) 2021


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Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Contents


History of the European-Japanese Cerebrovascular Congress �������������������������������������   1
Tetsuya Tsukahara

Part I Intracranial Aneurysms


When Is Diagnostic Subtraction Angiography Indicated Before Clipping
of Unruptured and Ruptured Intracranial Aneurysms? An International
Survey of Current Practice �����������������������������������������������������������������������������������������������   9
Martina Sebök, Jean-Philippe Dufour, Marco Cenzato, Yasuhiko Kaku,
Michihiro Tanaka, Tetsuya Tsukahara, Luca Regli, and Giuseppe Esposito

Current Strategies in the Treatment of Intracranial Large
and Giant Aneurysms��������������������������������������������������������������������������������������������������������� 19
Matthias Gmeiner and Andreas Gruber

Computational Fluid Dynamics for Cerebral Aneurysms in Clinical Settings������������� 27
Fujimaro Ishida, Masanori Tsuji, Satoru Tanioka, Katsuhiro Tanaka,
Shinichi Yoshimura, and Hidenori Suzuki

Microneurosurgical Management of Posterior Inferior
Cerebellar Artery Aneurysms: Results of a Consecutive Series������������������������������������� 33
Mattia Del Maestro, Sabino Luzzi, and Renato Galzio

Posterior Circulation Aneurysms: A Critical Appraisal of a Surgical
Series in Endovascular Era ����������������������������������������������������������������������������������������������� 39
Sabino Luzzi, Mattia Del Maestro, and Renato Galzio

Microneurosurgery for Paraclinoid Aneurysms in the Context of Flow
Diverters������������������������������������������������������������������������������������������������������������������������������� 47
Sabino Luzzi, Mattia Del Maestro, and Renato Galzio
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Part II Cerebral Revascularization


Characteristic Pattern of the Cerebral Hemodynamic Changes
in the Acute Stage After Combined Revascularization Surgery for
Adult Moyamoya Disease: N-isopropyl-p-[123I] iodoamphetamine
Single-Photon Emission Computed Tomography Study������������������������������������������������� 57
Miki Fujimura and Teiji Tominaga

Outcomes of Balloon Angioplasty and Stenting for Symptomatic
Intracranial Atherosclerotic Stenosis at a High Volume Center������������������������������������� 63
Toshihiro Ueda, Tatsuro Takada, Noriko Usuki, Satoshi Takaishi,
Yoshiaki Tokuyama, Kentaro Tatsuno, Yuki Hamada, and Tomohide Yoshie

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
vi Contents

Part III Arteriovenous Malformations and Dural Arteriovenous Fistulas


Living with a Brain AVM: A Quality of Life Assessment����������������������������������������������� 71
Péter Orosz, Ágnes Vadász, Dániel Sándor Veres, Zsolt Berentei,
István Gubucz, Sándor Nardai, Balázs Kis, and István Szikora
Complications in AVM Surgery����������������������������������������������������������������������������������������� 77
Marco Cenzato, Davide Boeris, Maurizio Piparo, Alessia Fratianni,
Maria Angela Piano, Flavia Dones, Francesco M. Crisà, and Giuseppe D’Aliberti

Surgical Simulation with Three-­Dimensional Fusion Images
in Patients with Arteriovenous Malformation����������������������������������������������������������������� 83
Takayuki Hara and Masanori Yoshino

Surgical Treatment of Unruptured Brain AVMs: Short- and
Long-Term Results������������������������������������������������������������������������������������������������������������� 87
Shalva Eliava, Vadim Gorozhanin, Oleg Shekhtman, Yuri Pilipenko,
and Olga Kuchina

Maximum Nidus Depth as a Risk Factor of Surgical Morbidity
in Eloquent Brain Arteriovenous Malformations ����������������������������������������������������������� 91
Bikei Ryu, Koji Yamaguchi, Tatsuya Ishikawa, Fukui Atsushi,
Go Matsuoka, Seiichiro Eguchi, Akitsugu Kawashima, Yoshikazu Okada,
and Takakazu Kawamata

Brain Arteriovenous Malformations Classifications: A Surgical Point of View����������� 101
Giovanni Marco Sicuri, Nicola Galante, and Roberto Stefini

The Preoperative Functional Downgrading of Brain AVMs������������������������������������������� 107
Sabino Luzzi, Mattia Del Maestro, and Renato Galzio

Intracranial Dural Arteriovenous Fistulas: The Sinus and Non-Sinus Concept���������� 113
Giuseppe D’Aliberti, Giuseppe Talamonti, Davide Boeris, Francesco M. Crisà,
Alessia Fratianni, Roberto Stefini, Edoardo Boccardi, and Marco Cenzato

Complications of Endovascular Treatment of Intracranial Dural
Arteriovenous Fistulas������������������������������������������������������������������������������������������������������� 123
Naoya Kuwayama and Naoki Akioka

Spinal Dural AVFs: Classifications and Advanced Imaging������������������������������������������� 129
Michihiro Tanaka

Part IV Miscellaneous
Copyright © 2021. Springer International Publishing AG. All rights reserved.


Intraoperative BOLD-fMRI Cerebrovascular Reactivity Assessment ������������������������� 139
Giovanni Muscas, Christiaan Hendrik Bas van Niftrik, Martina Sebök,
Giuseppe Esposito, Luca Regli, and Jorn Fierstra

The Hybrid Neurosurgeon: The Japanese Experience��������������������������������������������������� 145
Yasuhiko Kaku, Takumi Yamada, Shouji Yasuda, Kiyomitsu Kanou,
Naoki Oka, and Jouji Kokuzawa

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
History of the European-Japanese
Cerebrovascular Congress

Tetsuya Tsukahara

The European-Japanese Cerebrovascular Congress origi- Publication of the proceedings books of the conference as
nally started as a Swiss-Japanese joint conference on cere- supplements of ACTA Neurochirurgica is one of the main
bral aneurysm. The Congress was held in Zürich, Switzerland, reasons we have been able to continue this conference for
from 5–7 May 2001 with Prof. Y. Yonekawa of Zürich and almost 20 years. We sincerely thank Prof. Steiger for his con-
Prof. Y. Sakurai of Sendai as the presidents. tinuous and generous cooperation as the series Editor of
At that time, Japanese National Hospitals received Health ACTA Neurochirurgica.
Sciences Research Grants for Medical Frontier Strategy The third meeting at Zürich in 2006 was the key congress
Research from the Japanese Ministry of Health, Labour and for future development. The conference was expanded to the
Welfare regarding multi-center studies on the treatment of European-Japanese Joint Conference for Stroke Surgery
unruptured cerebral aneurysms. Since an international coop- (Fig. 3).
erative study was organized between Prof. Yonekawa of the As the year of 2006 was the 70th Anniversary of the
Department of Neurosurgery of Zürich University and Department of Neurosurgery, University Hospital Zürich,
Japanese National Hospitals, the congress was planned as a Prof. Krayenbühl, Prof. Yasargil, and Prof. Yonekawa intro-
research meeting for the theme. duced the impressive history of the Department of
The first day offered a unique opportunity to gather Neurosurgery at the conference. We were all impressed by
European and Japanese neurosurgeons to discuss the treat- the contribution of Zürich University to the development of
ment of unruptured cerebral aneurysms. Presentation of neurosurgery in Europe, Japan, and throughout the world.
these new clinical experiences facilitated intensive discus- Symposiums on the treatment of moya moya disease,
sions in order to clarify updated and appropriate ways to aneurysms, AVM, and AVF were held at the same time.
focus the treatment. The second day provided updated infor- The AVM randomized trial (ARUBA) was introduced by
mation on neurocritical care as well as endovascular and sur- Prof. J. P. Mohr of New York. Professor A. Valavanis of
gical treatment modalities carried out in daily practice in Zürich gave a lecture on the endovascular treatment of
Zürich and Japan. Roundtable discussions encouraged inter- AVM, and Prof. E. Motti of Milano gave a lecture on AVM
active communication between the participants and faculties treatment using Gamma knife. An epidemiological survey
(Fig. 1). of dural AV fistula in Japan was described by Prof.
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Three years later, in July of 2004, the second meeting was N. Kuwayama of Toyama.
also held at Zürich, with wide-ranging conference topics on The natural history and annual rupture rate of unruptured
cerebral stroke surgery. intracranial aneurysms were discussed by Prof. M. Yonekura
The first day was to discuss the treatment of cerebral of Nagasaki.
aneurysms and subarachnoid hemorrhage. At the fourth European-Japanese Joint Conference on
The discussion on the second day focused on the treat- Stroke Surgery we moved from Zürich to the beautiful
ment of intracranial arteriovenous malformations, and dis- Nordic city of Helsinki, with Prof. Juha Hernesniemi as the
cussion on the third day was on cerebral revascularization conference president. The participants presented papers and
(Fig. 2). discussed surgery for cerebral aneurysms and the manage-
ment of subarachnoid hemorrhage and stroke, arterial dissec-
tion, intracranial arteriovenous malformations, and fistulas.
T. Tsukahara (*) Microsurgical extra-intracranial bypass surgery and revascu-
Department of Neurosurgery, National Hospital Organization, larization techniques were also discussed. On the same
Kyoto Medical Center, Kyoto, Japan

© The Author(s) 2021 1


G. Esposito et al. (eds.), Trends in Cerebrovascular Surgery and Interventions, Acta Neurochirurgica Supplement 132,
https://doi.org/10.1007/978-3-030-63453-7_1

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
2 T. Tsukahara

Fig. 1 Conference program (a) and the proceedings book of the first Supplement 82. Springer-Verlag/Wien; 2002. (b). Prof. Y. Yonekawa of
meeting: Yonekawa Y, Sakurai E, Keller E, Tsukahara T, eds. New Zürich and Prof. Y. Sakurai of Sendai in the Saal of Zurich University at
Trends in Cerebral Aneurysm Management. ACTA Neurochirurgica the first meeting (c)

Fig. 2 Conference program


(a) and the proceedings book
of the second conference:
Yonekawa Y, Sakurai E,
Keller E, Tsukahara T, eds.
New Trends for Stroke and its
Perioperative Management.
Acta Neurochirurgica
Supplement 94. Springer-­
Verlag/Wien; 2005. (b)
Copyright © 2021. Springer International Publishing AG. All rights reserved.

o­ccasion, we visited Prof. Hernesniemi’s world-famous bral vascular reconstruction. In order to strengthen the focus
operating room in Helsinki (Fig. 4). on new trends, an open invitation for submission was made.
The fifth joint conference was held at Düsseldolf am Rein A number of emerging concepts were presented and dis-
with Prof. Hans-Jakob Steiger as the conference president. cussed in the resulting meeting (Fig. 5).
Management of cerebral and ventricular hemorrhage, sub- The sixth conference, named “The European-
arachnoid hemorrhage, extra-intracranial bypass surgery, Japanese Stroke Surgery Conference” (EJSSC), was
surgical and endovascular treatment of arterial occlusive dis- held in Utrecht, The Netherlands. Professor Luca Regli
ease, and embolization and microsurgery of AVM and dural and Prof. Gabriel Rinkel were the conference presi-
AV-fistula were the main themes. Special topics of the con- dents. The main topics of the conference comprised
ference were cerebral and ventricular hemorrhage and cere- surgical and endovascular management of intracranial

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
History of the European-Japanese Cerebrovascular Congress 3

Fig. 3 Conference program


(a) and the proceedings book
of the third conference:
Yonekawa Y, Tsukahara T,
Valavanis A, Khan N, eds.
Changing Aspects in Stroke
Surgery: Aneurysms,
Dissections, Moyamoya
Angiopathy and EC-IC
Bybass. ACTA
Neurochirurgica Supplement
103. Springer-Verlag/Wien;
2008. (b)

Fig. 4 Conference program


(a) and the proceedings book
of the fourth conference:
Laakso A, Hernesniemi J,
Yonekawa Y, Tsukahara T,
eds. Surgical Management of
Cerebrovascular Disease.
Acta Neurochirurgica
Supplement 107. Springer-­
Verlag/Wien; 2010. (b)
Copyright © 2021. Springer International Publishing AG. All rights reserved.

aneurysms and arteriovenous malformations; current were surgical and endovascular management of intracranial
concepts in cerebrovascular reconstruction; and new aneurysms and arteriovenous malformations and cerebro-
developments in cerebrovascular imaging. A number vascular reconstruction. We also enjoyed beautiful paint-
of emerging concepts were also presented and dis- ings by Veronese and opera at the ancient Arena de Verona
cussed at this meeting (Fig. 6). (Fig. 7).
The seventh European-Japanese Stroke Surgery The eighth European-Japanese Cerebrovascular
Conference (EJSSC) was held in the beautiful city of Congress (EJCVC) came back to Zürich in the year
Verona, Italy with Presidents Prof. Alberto Pasqualin and 2016 with Prof. Luca Regli as the president. The main
Prof. Giampietro Pinna. The main topics of the conference topics of the conference consisted of management of

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
4 T. Tsukahara

Fig. 5 Conference program (a) and the proceedings book of the fifth conference: Tsukahara T. Regli L, Hänggi D, Turowski B, Steiger H-J, eds.
Trends in Neurovascular Surgery. Acta Neurochirurgica Supplement 112. Springer-Verlag/Wien; 2011. S (b)

Fig. 6 Conference program


(a) and the proceedings book
of the sixth conference:
Tsukahara T, Esposito G,
Steiger H-J, Rinkel GJE,
Regli L, eds. Trends in
Neurovascular Interventions.
Acta Neurochirurgica
Supplement 119. Springer-­
Verlag/Wien; 2014. (b)
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
History of the European-Japanese Cerebrovascular Congress 5

intracranial aneurysms, arteriovenous malformations, neuroanatomy, and new concepts in cerebrovascular


cavernoma and dural arteriovenous fistulas, and hem- imaging.
orrhagic and ischemic stroke, current trends in cere- At the same time, the Cerebral Blood Flow Meeting and
brovascular reconstruction and cerebrovascular Microsurgery Course Zürich were organized (Fig. 8).

Fig. 7 Conference program (a) and the proceedings book of the seventh conference: Tsukahara T, Pasqualin A, Esposito G, Regli L, Pinna G, eds.
Trends in Cerebrovascular Surgery. Acta Neurochirurgica Supplement 123. Springer International Publishing Switzerland; 2016. (b)

Fig. 8 Conference program


(a) and the proceedings book
of the eighth conference:
Esposito G, Regli L, Kaku Y,
Tsukahara T, eds. Trends in
the Management of
Cerebrovascular Diseases.
Acta Neurochirurgica
Supplement 129. Springer
International Publising; 2018.
(b)
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
6 T. Tsukahara

The ninth European-Japanese Cerebrovascular


Congress (EJCVC) was held in the historical room of
Grande Ospedale Metropolitano Niguarda Milan, Italy, on
7–9 June 2018, with Prof. Marco Cenzato as the president.
The main theme of the congress was preventive cerebro-
vascular surgery. A number of emerging concepts were
presented and discussed by European and Japanese partici-
pants. Very fruitful presentations and discussions will be
published as the proceedings book of ACTA
Neurochirurgica Supplement, the same as with previous
meetings (Fig. 9).
The tenth European-Japanese Cerebrovascular Congress
(EJCVC) will be held in Kyoto, Japan with Prof. Tetsuya
Tsukahara and Prof. Yasuhiko Kaku as the presidents. Due to
the pandemic crisis of Covid-19, the 10th EJCVC in Kyoto
has been postponed to November 2021.
It will be the first meeting in Japan of the European-­
Japanese Cerebrovascular Congress (EJCVC). A number of
European and Japanese participants will be expected to join
the congress and have fruitful discussions on New Trends of
Cerebrovascular treatment.

Conflict of Interest The author declares that I have no conflict of


interest.

Fig. 9 Program of ninth conference


Copyright © 2021. Springer International Publishing AG. All rights reserved.

Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.
org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropri-
ate credit to the original author(s) and the source, provide a link to the Creative Commons license and indicate if changes were made.
The images or other third party material in this chapter are included in the chapter's Creative Commons license, unless indicated otherwise in
a credit line to the material. If material is not included in the chapter's Creative Commons license and your intended use is not permitted by statu-
tory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Part I
Intracranial Aneurysms
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
When Is Diagnostic Subtraction
Angiography Indicated Before Clipping
of Unruptured and Ruptured
Intracranial Aneurysms?
An International Survey of Current
Practice

Martina Sebök, Jean-Philippe Dufour, Marco Cenzato,


Yasuhiko Kaku, Michihiro Tanaka, Tetsuya Tsukahara,
Luca Regli, and Giuseppe Esposito

Introduction [12] reported a per-aneurysm pooled sensitivity and specific-


ity of MRA of 87% and 95% for the detection of IAs, respec-
Digital subtraction angiography (DSA) is considered the tively. Both CTA and MRA can in many cases provide the
gold standard for understanding the angioanatomy in rup- necessary information for the preoperative planning of intra-
tured and unruptured intracranial aneurysms (IAs) [1–5]. cranial aneurysms, comparable to DSA [10, 11, 13, 14]. In
More recently, computed tomography angiography (CTA) cases of mural calcifications, CTA has a sensitivity superior
has been introduced as an alternative imaging modality for to that of MRA [10, 15].
ruptured aneurysms [6]. Sensitivities ranging from 77–97% The goal of this survey is to investigate the daily practice
and specificities ranging from 87–100% for the identification regarding indications for DSA before clipping of ruptured
of ruptured aneurysms using CTA have been reported [3, 4, and unruptured IAs in an international panel of neurovascu-
7–9]. High-resolution magnetic resonance angiography lar specialists.
(MRA), on the other hand, is frequently used for unruptured
aneurysms as an alternative noninvasive modality [10]. In a
systematic review [11] of studies evaluating the value of Methods
MRA for the diagnosis of intracranial aneurysms, a pooled
sensitivity of 95% and pooled specificity of 89% have been Survey Development and Distribution
reported. By comparison, in 2000 the very first meta-analysis
We elaborated an anonymous survey containing 23 multiple-­
M. Sebök · J.-P. Dufour · L. Regli · G. Esposito (*) choice questions (see Appendix) to investigate when and
Department of Neurosurgery, Clinical Neuroscience Center, why cerebrovascular specialists consider a DSA to be indi-
University Hospital Zurich, University of Zurich, Zurich, cated before the clipping of ruptured and unruptured IAs.
Switzerland
e-mail: [email protected]; [email protected]; The survey was structured as follows. First, general ques-
Copyright © 2021. Springer International Publishing AG. All rights reserved.

[email protected] tions about the responder’s specialty and institution were


M. Cenzato asked: country, specialty of responder, number of treated
Department of Neurosurgery, Grande Ospedale Metropolitano aneurysms as main surgeon, and number of treated ruptured
Niguarda, Milan, Italy and unruptured aneurysms per year at responders’ institu-
e-mail: [email protected] tion. Second, questions regarding the choice of aneurysm
Y. Kaku treatment and the quality of imaging modalities at the
Department of Neurosurgery, Asahi University Murakami responders’ institutions were asked. Third, responders were
Memorial Hospital, Gifu, Japan
e-mail: [email protected] asked the situations (unruptured aneurysms/ruptured aneu-
rysms/ruptured aneurysms with life-threatening hematoma)
M. Tanaka
Department of Neurosurgery, Kameda Medical Center, and aneurysm locations (MCA or locations other than MCA)
Chiba, Japan in which microsurgical treatment is to be performed without
T. Tsukahara preoperative DSA. Finally, responders were asked to select
Department of Neurosurgery, National Hospital Organization, factors which in their view influence the need for p­ reoperative
Kyoto Medical Center, Kyoto, Japan

© The Author(s) 2021 9


G. Esposito et al. (eds.), Trends in Cerebrovascular Surgery and Interventions, Acta Neurochirurgica Supplement 132,
https://doi.org/10.1007/978-3-030-63453-7_2

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
10 M. Sebök et al.

DSA, from a list of aneurysm-, patient-, and treatment-­ Table 1 Baseline characteristics of 67 respondents to the survey
related factors (Table 5). Number of respondents (%)
A paper version of this survey was distributed to the Continent
attendees of the ninth European–Japanese Cerebrovascular Europe 50 (75)
Congress (EJCVC—www.ejcvc2018.com), which took Japan 16 (24)
place in Milan, Italy at 7–9 June 2018 and was thereafter col- Other 1 (1)
Specialty
lected. The EJCVC is a biennial cerebrovascular meeting
Neurosurgeon 57 (85)
initiated in Zurich in 2001 and represents a unique opportu- Neurointerventionalist 5 (7.5)
nity to gather the latest updates on neurovascular surgery and Hybrid surgeon 5 (7.5)
interventions for cerebrovascular diseases. Number of aneurysms treated as a main surgeon
None 13 (20)
1–20 8 (12)
Data Analysis 20–100 15 (23)
100–200 7 (10)
Data were manually imported into a digital database 200–500 12 (18)
>500 11 (17)
(Statistical Package for the Social Science) (SPSS) version
Number of treated UNRUPTURED aneurysms at institution per
24 for Windows (IBM, Armonk, New York, USA). The vari- year
ous results were reported as value or proportion (%). <20 14 (21)
Descriptive statistics were used to analyze the collected data. 20–50 32 (48)
Categorical data were analyzed using the χ2 test. Statistical 50–100 19 (28)
significance was defined at p < 0.05. >100 2 (3)
Number of treated RUPTURED aneurysms at institution per year
<20 11 (16)
Results 20–50 36 (54)
50–100 18 (27)
>100 2 (3)
Baseline Characteristics of Survey Responders Final decision for the type of treatment
Interdisciplinary 53 (80)
The total number of participants at the EJCVC was 152. The Neurosurgeon 10 (15)
survey was offered to all participants at the entrance to the Neurointerventionalist 1 (2)
conference auditorium. A total of 93 surveys were distrib- Hybrid surgeon 2 (3)
uted and 67 (72%) completed surveys were returned during
the three days of the conference. The responders worked in
13 different countries. The baseline characteristics are shown Concerning the final decision for the type of treatment,
in Table 1. 80% of responders assume an interdisciplinary approach (on
Eighty-five percent of all responders were neurosurgeons, neurovascular boards or by directly discussing the cases
7.5% neurointerventionalists, and 7.5% hybrid neurosur- among neurosurgeons, neuroradiologists, and neurologist).
geons. A hybrid surgeon is a cerebrovascular specialist able Ninety-one percent of all responders worked at institu-
to treat aneurysms both by microsurgical and by endovascu- tions offering good quality CTA and 97% at an institution
lar methods. with a good quality MRA (at least 1.5 T). Good quality neu-
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Seventeen percent of responders had treated more than roimaging is defined as imaging capable of displaying every
500 aneurysms as main surgeon, 18% between 200 and 500 vessel of the circle of Willis in high definition. In cases where
aneurysms, 10% between 100 and 200 aneurysms, 23% had a preoperative DSA is considered indicated, 82% of respond-
treated between 20 and 100 aneurysms, and 12% between 1 ers also request tridimensional rotational sequences.
and 20 aneurysms. Twenty percent of responders had never No statistical differences were seen in the baseline char-
treated an aneurysm as a main surgeon. acteristics between survey responders from Europe and
Twenty-eight percent of all responders worked at institu- Japan.
tions that treated 50–100 unruptured aneurysms per year,
while 48% of all responders worked at institutions that
treated 20–50 unruptured aneurysms per year. I mpact of Aneurysm Location and Rupture
Twenty-seven percent of all responders worked in institu- Status
tions where the number of ruptured aneurysms treated per
year is 50–100, while 54% of responders worked at an insti- For MCA aneurysms, 64% of survey responders would treat
tution treating 20–50 ruptured aneurysms per year. unruptured aneurysms without preoperative DSA, and 60%

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
When Is Diagnostic Subtraction Angiography Indicated Before Clipping of Unruptured and Ruptured Intracranial Aneurysms… 11

Table 2 Crosstab of surgical aneurysm treatment without preoperative Table 3 Crosstab of surgical aneurysm treatment without preoperative
DSA based on aneurysm location—all survey responders DSA based on aneurysm location—excluding survey responders who
Number of respondents (%) never treated an aneurysm as main surgeon
Unruptured Ruptured In case of life Number of respondents (%)
Aneurysm aneurysm aneurysm threatening Unruptured Ruptured In case of life-­
location hematoma Aneurysm aneurysm aneurysm threatening
MCA 43 (64) 40 (60) 65 (97) location hematoma
Other 45 (68) 49 (73) 64 (96) MCA 37 (70) 36 (68) 51 (96)
location Other 39 (74) 39 (74) 51 (96)
location

of responders would treat ruptured MCA aneurysms with- Table 4 Impact of surgeon’s experience to treat aneurysm without pre-
out preoperative DSA. Ninety-seven percent of responders operative DSA
would treat ruptured MCA aneurysms with life-threatening Experienced surgeon (n (%))
hematoma without preoperative DSA (Table 2). Aneurysm location YES (n = 30) NO (n = 37) p-value
Regarding aneurysms in locations other than the MCA, MCA
68% of survey responders would treat unruptured aneu- Unruptured 23 (71) 22 (49) 0.08
rysms without preoperative DSA, and 73% of responders Ruptured 24 (80) 25 (68) 0.20
would treat ruptured aneurysms without preoperative Other location
DSA. Ninety-­six percent of all responders would treat rup- Unruptured 24 (80) 16 (43) 0.002
tured aneurysms in other locations than the MCA with Ruptured 22 (73) 19 (51) 0.18
life-threatening hematoma without preoperative DSA
(Tables 2 and 3). There were no statistically significant dif- preoperative DSA more often than less experienced col-
ferences in decision-making regarding preoperative DSA leagues (experienced vs. less-experienced: 71% vs. 49%,
for aneurysm treatments between European and Japanese p = 0.08).
neurosurgeons. For ruptured MCA aneurysms and ruptured aneurysms in
Because 20% of all responders never treated an aneurysm other locations, the data again show differences in absolute
as a main surgeon, in Table 3 we adapted a crosstab of surgi- numbers, whereby preoperative DSAs are less frequently
cal aneurysm treatment without preoperative DSA based on requested by experienced neurosurgeons (but without reach-
aneurysm location and performed a calculation excluding ing significant differences between the experienced and less-­
survey responders who never treated an aneurysm as main experienced group).
surgeon. Results do not show significant changes if one does
not consider the surgeons who never clipped an aneurysm
(Tables 2 and 3).  actors Influencing the Decision to Perform
F
a Preoperative DSA

I mpact of Surgeon Experience on Decision Table 5 summarizes aneurysm-related factors, patient-


to Perform a Preoperative DSA related factors, and treatment-related factors that influence
the choice of survey responders to perform a preoperative
The benchmark for an experienced surgeon was set at 100 DSA.
Copyright © 2021. Springer International Publishing AG. All rights reserved.

treated aneurysms as main surgeon. Forty-five percent of survey The most important aneurysm-related factors indicating
responders classify as experienced aneurysm surgeons. Table 4 a preoperative DSA examination are: aneurysmal shape
represents a crosstab of the impact of a surgeons’ experience on (fusiform or dissecting aneurysms: >80% of responders
the decision to perform a preoperative DSA. Because in cases of ask for a preoperative DSA); infectious aneurysm etiology
life-threatening hematoma nearly all survey responders decide (72% of responders); maximum aneurysm diameter
to waive a preoperative DSA (Tables 2 and 3), the impact of >25 mm (85% of responders); paraclinoidal or posterior
experience in these cases was not calculated. circulations aneurysms (>70% of responders); possible
In cases of unruptured aneurysms in locations other than perforators and vessels arising from aneurysm sac (85% of
the MCA, experienced neurosurgeons treat aneurysms sig- responders for both); intra-aneurysmal thrombus (73% of
nificantly more often without a preoperative DSA, compared responders); and previous treatment (90% of survey
to less experienced colleagues (experienced vs. less-­ responders).
experienced: 80% vs. 43%, p = 0.002). There are no patient-related factors (age, clinical status)
In cases of unruptured MCA aneurysms, a similar trend is (Table 5) that influence the decision for a preoperative
seen: Experienced neurosurgeons perform surgeries without DSA.

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
12 M. Sebök et al.

Table 5 Aneurysm-, patient- and treatment-related factors influencing Table 5 (continued)


the choice to perform a preoperative DSA
Number of respondents
Number of respondents answering YES (%)
answering YES (%) – <40 20 (30)
Aneurysm-related factors – 40–60 18 (27)
Aneurysm location – >60 18 (27)
• Middle cerebral artery (MCA) proximal 29 (43) • Clinical situation:
(M1-M2 segments) – SAH 22 (33)
• Middle cerebral artery (MCA) distal 31 (46) – Cranial nerve deficit 23 (34)
(M3-M4 segments) – Clinical mass effect 26 (39)
• Carotid-posterior communicating artery 35 (52) – Radiological mass effect 23 (34)
(PCom)
– Previous SAH 29 (43)
• Carotid-anterior choroidal artery (ACho) 41 (61)
Treatment-related factors
• Carotid-T 34 (51)
• Bypass contemplated 52 (78)
• Carotid-hypophyseal 41 (61)
– Visualization of possible donor 51 (76)
• Carotid-paraclinoidal (ophthalmic) 48 (72) artery (e.g. STA)
• Anterior cerebral artery (ACA) proximal 31 (46) – Visualization of possible recipient 47 (70)
(A1-A2 segments) artery
• Anterior cerebral artery (ACA) proximal 29 (43) • Collateral circulation 57 (85)
(A3-A4 segments)
• Anterior communicating artery (ACom)
– Anterior projecting 31 (46)
– Posterior projecting 39 (58)
– Superior projecting 37 (55) Regarding treatment-related factors, 78% of responders
– Inferior projecting 33 (49) would ask for a DSA preoperatively in cases where a flow-­
• Posterior circulation: replacement bypass is contemplated as a treatment option.
– posterior inferior cerebellar artery 47 (70) Similarly, 85% of responders would ask for a preoperative
(PICA) DSA to assess the collateral circulation in cases where the
– others (anterior inferior cerebellar 51 (76) possibility of bypass is evaluated.
artery, superior cerebellar artery, basilar
artery, posterior cerebral artery)
Aneurysmal morphology
• Etiology: Discussion
– Saccular 25 (37)
– Fusiform 54 (81) The goal of the survey was to investigate, among an interna-
– Dissecting 58 (87) tional panel of neurovascular specialists participating at the
– Infectious (i.e., mycotic) 48 (72) ninth EJCVC, the workup and in particular the indication for
• Shape:
preoperative DSA for patients undergoing microsurgical
– Irregularity (bleb/lobulation/ 40 (60)
daughter aneurysm) treatment of ruptured or unruptured intracranial aneurysms.
– Broad neck 41 (61) The analysis of the survey showed that in more than 80%
• Maximum diameter (single): of responders, the final decision for the type of aneurysm
– <5 mm 22 (33) treatment at the responder’s institution is taken in an interdis-
– >10 mm 35 (52) ciplinary setting.
Copyright © 2021. Springer International Publishing AG. All rights reserved.

– >25 mm 57 (85) Tables 2 and 3 show a crosstab of microsurgical aneurysm


• Possible perforators arising from the 57 (85) treatment without preoperative DSA based on aneurysm
aneurysm
location and rupture status. For MCA aneurysms, approxi-
• Efferent vessels arising from aneurysmal 57 (85)
sac mately 60% of responders perform microsurgery without
• Calcification/atherosclerotic plaque of the 26 (39) preoperative DSA, regardless of rupture status. For aneu-
aneurysm wall rysms in locations other than MCA, microsurgery is done
• Intra-aneurysmal thrombus 49 (73) without preoperative DSA in 68% of unruptured and 73% of
• Recurrence/previous treatment 60 (90) ruptured cases. In the case of ruptured MCA and non-MCA
• Computational fluid dynamic analysis 20 (30) aneurysms with life-threatening hematoma, the vast majority
based decision
of the responders (96% and 97%, respectively) perform sur-
Patient-related factors
• Patient age: gery without preoperative DSA.
This high percentage of responders who do not perform a
DSA in cases of life-threatening hematoma is to be expected.

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
When Is Diagnostic Subtraction Angiography Indicated Before Clipping of Unruptured and Ruptured Intracranial Aneurysms… 13

In these cases there is no time for a DSA examination: the including preoperative DSA. The aneurysmal complexity is
hematoma must be evacuated and the brain decompressed. namely related to at least one of the following features: (1)
For MCA aneurysms without life-threating hematoma, size ≥2.5 cm, (2) anatomic location (vertebral, basilar, para-
40% of responders ask for a DSA preoperatively. This is clinoid), (3) involvement of critical perforating or branch
quite a high percentage, especially if one considers the pos- vessels, (4) previous treatment (endovascular or surgical),
sible complications of a DSA: According to the literature, (5) dissecting, fusiform, saccular lesions with very broad
neurological complications after a DSA examination occur neck, (6) intraluminal thrombosis, and (7) atherosclerotic
in 2.63% of cases, where 0.14% of these are strokes with plaques and calcifications of the aneurysm wall and/or neck
permanent disability [16]. [17–24]. There are no patient-related factors (except clinical
Our survey results suggest that a surgeons’ experience status) that influence the decision for a preoperative
plays a role in deciding whether a preoperative DSA is indi- DSA. This is an expected finding because in cases of bad
cated. A clear difference between experienced (>100 treated clinical status, often caused by life-threatening hematoma,
aneurysms as main surgeon) and less experienced neurosur- there is no time for a preoperative DSA.
geons is seen especially in cases of unruptured aneurysms: One of the aims of the survey was to assess in which
experienced surgeons ask for a preoperative DSA signifi- direction the use of diagnostic DSA before microsurgical
cantly less frequently in these patients. management of ruptured and unruptured cerebral aneurysms
Regarding the difference in requests for a preoperative is moving among European and Japanese neurosurgeons.
DSA in MCA aneurysms, an almost-significant difference is Several advantages of both noninvasive CTA and invasive
seen in unruptured aneurysms (p = 0.08) and a trend toward DSA are known and should be considered, as well as the pos-
statistical significance is seen in ruptured aneurysms sible complications of DSA. Previous studies introduced
(p = 0.20) between experienced surgeons and less experi- CTA as an alternative imaging modality for ruptured IAs and
enced surgeons. reported sensitivities ranging from 77–97%, and specificities
To simplify our questionnaire and the statistical workup, ranging from 87–100% [3, 4, 7, 8]. The most recent meta-­
we separated the aneurysm location into MCA and locations analysis by Menke et al. [8] was published in 2011 and
other than the MCA. As a consequence, the non-MCA group encompassed 45 previous studies, for a total of 3643 patients
includes a heterogeneous group of aneurysms from the ante- with ruptured and unruptured aneurysm. This meta-analysis
rior and posterior circulation. reported an overall CTA sensitivity of 97.2% and a specific-
According to the consensus among neurovascular special- ity of 97.9%, as well as a per-aneurysm sensitivity of 95%
ists, a preoperative DSA is performed more often for aneu- and specificity of 96.2%.
rysms of the posterior circulation. Our survey confirms this In a comparative analysis between CTA and DSA for the
trend: ≥70% of survey responders perform a preoperative diagnosis of ruptured intracranial aneurysms, Philipp et al.
DSA in patients with posterior circulation aneurysms. [25] concluded that the accuracy of CTA for the diagnosis of
Therefore, the higher percentage of survey responders per- ruptured intracranial aneurysm may be lower than previously
forming surgeries without DSA in locations other than the reported: in fact they found a low sensitivity of CTA (57.6%)
MCA compared to MCA aneurysms regardless of rupture for aneurysms smaller than 5 mm in size, located adjacent to
status (unruptured locations other than MCA vs. unruptured bony structures, and for those arising from small caliber par-
MCA aneurysms: 68% vs. 64%; ruptured locations other ent vessels.
than MCA vs. ruptured MCA aneurysms: 73% vs. 60%) is a The “Guidelines for the Management of Patients With
surprising finding. Unruptured Intracranial Aneurysms” from the American
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Factors which in a high percentage of responders (>70%) Heart Association/American Stroke Association [9] recom-
lead to the request for a preoperative DSA are: location of mend that due to its high sensitivity and specificity, even for
the aneurysm in the posterior circulation or paraclinoid smaller aneurysms, CTA can be considered as an initial diag-
aneurysms, non-saccular aneurysmal shape (fusiform or dis- nostic test for aneurysm detection and screening. However,
secting), infectious aneurysm etiology, maximum diameter the reconstruction methods may not accurately depict the
of the aneurysm >25 mm, possible perforators or efferent true neck/dome/adjacent small vessel anatomy, but CTA is
vessels arising from the aneurysm sac, intra-aneurysmal very useful in identifying mural calcification and thrombus,
thrombus, previous treatment of the aneurysm, bypass con- which can have a significant impact on treatment decisions
templated, and to assess the collateral circulation. All these [15, 26].
factors could be considered as characteristics of complex Several other advantages of CTA and MRA over DSA
aneurysms. This is an expected finding since a general con- have been recognized, including reduced cost, avoidance of
sensus among the cerebrovascular specialists exists wherein arterial injury and stroke, rapid acquisition, and retrospective
any angioanatomical feature indicating the presence of a manipulation of data. Furthermore, it is important to mention
complex aneurysm should lead to a more detailed workup, that both the radiation dosage and the volume of contrast

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
14 M. Sebök et al.

media is inferior with CTA than DSA (one-third to one-half Moreover, a surgeons’ experience plays a role in the
for a single CTA compared to a four-vessel DSA) [10, 15]. decision-­making regarding preoperative DSA, with experi-
The most appropriate use of the above-mentioned imag- enced surgeons (>100 aneurysms treated as main surgeon)
ing modalities, especially CTA and DSA, in guiding medical requesting preoperative DSAs less frequently. This effect is
decision-making for treatment of ruptured and unruptured especially pronounced in patients with unruptured
intracranial aneurysms, remains an issue of debate. aneurysms.

Limitations Appendix: Survey Questions

Our survey has several limitations, particularly with regard


to responder bias and generalizability. First, the survey was 1. In which country do you work?
distributed to participants of the EJCVC 2018 and therefore …………………………………………………
the results represent the current European and Japanese prac- 2. At which institution do you work? (if you want to
tice but might not be generalizable to other regions. Second, answer)
responses were voluntary and could lead to a selection bias …………………………………………………
for people with a particular interest and/or knowledge in 3. Which specialist are you?
these issues. Finally, 20% of all responders never treated an (a) neurosurgeon
aneurysm as a main surgeon, indicating a possible limited (b) neurointerventionist (interventional neuroradiologist)
experience in preoperative decision-making. Nonetheless, (c) hybrid surgeon
this subgroup of responders could have answered by using (d) neurologist
the decision-making algorithm of their working institution, (e) neurointensivist (Neuro Intensive Care)
which was the reason we included them in our analysis. (f) other: ………………………….
However, we adapted a crosstab of surgical aneurysm treat- 4. What is your position?
ment without preoperative DSA based on aneurysm location (a) chairman
and performed a calculation excluding the responders who (b) senior consultant (attending clinician)
never treated an aneurysm as main surgeon. The results do (c) junior consultant (attending clinician)
not show significant changes if one does not consider the (d) fellow
surgeons who never clipped an aneurysm (Tables 2 and 3). (e) resident
(f) other: ………………………………….
5. How many aneurysms have you treated in your
Conclusion career as main surgeon?
(a) none
There is still a high variability in the surgeons’ preoperative (b) 1–20
decision-making regarding the indication for DSA before (c) 20–100
clipping of intracranial aneurysms, except in case of rup- (d) 100–200
tured aneurysms with life-threatening hematoma, where (e) 200–500
most of the responders perform surgery without preoperative (f) >500
DSA. For MCA aneurysms, approximately 60% of respond- 6. How many patients with unruptured intracranial
Copyright © 2021. Springer International Publishing AG. All rights reserved.

ers perform microsurgery without preoperative DSA, regard- aneurysms are treated at your department per
less of rupture status. For aneurysms in locations other than year?
MCA, microsurgery is done without preoperative DSA in (a) <20
68% of unruptured and 73% of ruptured cases. (b) 20–50
The factors favoring the execution of a DSA before clip- (c) 50–100
ping are related to the complexity of the aneurysm: aneurys- (d) >100
mal shape (fusiform, dissecting), etiology (infectious), size 7. How many patients with ruptured intracranial aneu-
(>25 mm), possible presence of perforators or efferent ves- rysms are treated at your department per year?
sels arising from the aneurysm, intra-aneurysmal thrombus, (a) <20
previous treatment, location (posterior circulation or paracli- (b) <50
noid), and flow-replacement bypass contemplated for final (c) 50–100
aneurysm treatment. (d) >100

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
When Is Diagnostic Subtraction Angiography Indicated Before Clipping of Unruptured and Ruptured Intracranial Aneurysms… 15

8. Who takes the final decision for the type of (a) yes
treatment? (b) no
(a) interdisciplinary (boards or discussion of the case 16. Do you treat surgically unruptured MCA aneurysms
among neurosurgeons, neuroradiologists, without preoperative Digital Subtraction
neurologists) Angiography (DSA)?
(b) neurosurgeon (a) yes
(c) neurointerventionalist (interventional neuroradiologist) (b) no
(d) hybrid surgeon (c) I do not clip
(e) neurologist (d) I have not clipped yet
(f) neurointensivist (Neuro Intensive Care) 17. Do you treat surgically unruptured aneurysms in
(g) others: ………………………. other locations (i.e., not MCA-aneurysms) without
9. Do you (or surgeons at your institution) nowadays preoperative DSA?
treat surgically only aneurysms of the middle cere- (a) yes
bral artery (MCA)? (b) no
(a) yes (c) I do not clip
(b) no (d) I have not clipped yet
(c) I do not know 18. Do you treat surgically ruptured MCA aneurysms
10. Have you (or surgeons at your institution) treated without preoperative DSA?
surgically in the past also intracranial aneurysms in (a) yes
other locations (i.e., not MCA aneurysms)? (b) no
(a) yes (c) I do not clip
(b) no (d) I have not clipped yet
(c) I do not know 19. Do you treat surgically ruptured aneurysms in other
11. Does the neurosurgeon at your institution sometime locations (i.e., not MCA-aneurysms) without preop-
decide by himself to treat a MCA aneurysm surgi- erative DSA?
cally without having involved the neurointervention- (a) yes
ist in the decision-making? (b) no
(a) yes (c) I do not clip
(b) no (d) I have not clipped yet
(c) I do not know 20. Do you operate ruptured MCA aneurysms without
12. Does the neurosurgeon sometime decide by himself preoperative DSA in case of life-threatening
to treat an aneurysm in other locations (i.e., not MCA hematoma?
aneurysms) surgically without having involved the (a) yes
neurointerventionist in the decision-making? (b) no
(a) yes (c) I do not clip
(b) no (d) I have not clipped yet
(c) I do not know 21. Do you operate ruptured aneurysms in other
13. Does the neurointerventionist sometimes decide by locations (i.e., not MCA-aneurysms) without pre-
himself to treat an aneurysm endovascular without operative DSA in case of life-threatening
Copyright © 2021. Springer International Publishing AG. All rights reserved.

having involved the neurosurgeon in the hematoma?


decision-making? (a) yes
(a) yes (b) no
(b) no (c) I do not clip
(c) I do not know (d) I have not clipped yet
14. Have you at your institution good quality Computed 22. By preoperative DSA, do you always ask for tridi-
Tomography Angiography (CTA)? mensional rotational sequences?
(a) yes (a) yes
(b) no (b) no
15. Have you at your institution good quality Magnetic (c) I do not clip
Resonance Angiography (MRA) with at least 1.5 T or (d) I have not clipped yet
more?

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
16 M. Sebök et al.

23. Which of the following criteria influence your choice References


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Aneurysm-related factors
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Middle cerebral artery (MCA) distal (M3-M4 segments) Ο yes Ο no
3. Dammert S, Krings T, Moller-Hartmann W, Ueffing E, Hans FJ,
Carotid-posterior communicating artery (PCom) Ο yes Ο no
Carotid-anterior choroidal artery (ACho) Ο yes Ο no
Willmes K, Mull M, Thron A (2004) Detection of intracranial
Carotid-T Ο yes Ο no aneurysms with multislice CT: comparison with conventional angi-
Carotid-hypophyseal Ο yes Ο no ography. Neuroradiology 46:427–434. https://doi.org/10.1007/
Carotid-paraclinoidal (ophthalmic) Ο yes Ο no s00234-003-1155-1
Anterior cerebral artery (ACA) proximal (A1-A2 segments) Ο yes Ο no 4. Chappell ET, Moure FC, Good MC (2003) Comparison of com-
Anterior cerebral artery (ACA) proximal (A3-A4 segments) Ο yes Ο no
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Anterior projecting Ο yes Ο no
Posterior projecting Ο yes Ο no
Neurosurgery 52:624–631; discussion 630–1.
Superior projecting Ο yes Ο no 5. Burkhardt JK, Chua MH, Winkler EA, Rutledge WC, Lawton MT
Inferior projecting Ο yes Ο no (2019) Incidence, classification, and treatment of angiographically
Posterior circulation: posterior inferior cerebellar artery (PICA) Ο yes Ο no occult intracranial aneurysms found during microsurgical aneu-
Posterior circulation: others (anterior inferior cerebellar artery, superior cerebellar rysm clipping of known aneurysms. J Neurosurg 132:434–441.
artery, basilar artery, posterior cerebral artery) Ο yes Ο no
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Aneurysmal morphology
6. Dehdashti AR, Binaghi S, Uske A, Regli L (2006) Comparison of
Etiology:
Saccular Ο yes Ο no
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Fusiform Ο yes Ο no traction angiography in the postoperative evaluation of patients
Dissecting Ο yes Ο no with clipped aneurysms. J Neurosurg 104:395–403. https://doi.
Infective (i.e.: mycotic) Ο yes Ο no org/10.3171/jns.2006.104.3.395
Shape: 7. Kangasniemi M, Makela T, Koskinen S, Porras M, Poussa K,
Irregularity (bleb/ lobulation/daughter aneurysm) Ο yes Ο no
Hernesniemi J (2004) Detection of intracranial aneurysms with
Broad neck Ο yes Ο no
two-dimensional and three-dimensional multislice helical com-
Others Ο yes Ο no
Maximum diameter (single)
puted tomographic angiography. Neurosurgery 54:336–340; dis-
< 5mm Ο yes Ο no cussion 340–1.
>10 mm Ο yes Ο no 8. Menke J, Larsen J, Kallenberg K (2011) Diagnosing cerebral aneu-
>25mm Ο yes Ο no rysms by computed tomographic angiography: meta-analysis. Ann
Possible perforators arising from the aneurysm Ο yes Ο no Neurol 69:646–654. https://doi.org/10.1002/ana.22270
Efferent vessels arising from aneurysmal sac Ο yes Ο no
9. Thompson BG, Brown RD Jr, Amin-Hanjani S, Broderick JP,
Cockroft KM, Connolly ES Jr, Duckwiler GR, Harris CC, Howard
Calcification/atherosclerotic plaque of the aneurysm wall Ο yes Ο no
VJ, Johnston SC, Meyers PM, Molyneux A, Ogilvy CS, Ringer
Intra-aneurysmal thrombus Ο yes Ο no
AJ, Torner J (2015) Guidelines for the management of patients
Recurrence/previous treatment Ο yes Ο no with unruptured intracranial aneurysms: a guideline for health-
Computational fluid dynamic analysis based decision Ο yes Ο no care professionals from the American Heart Association/American
Patient-related factors Stroke Association. Stroke 46:2368–2400. https://doi.org/10.1161/
Patient age: str.0000000000000070
<40 Ο yes Ο no 10. Kouskouras C, Charitanti A, Giavroglou C, Foroglou N, Selviaridis
40-60 Ο yes Ο no
P, Kontopoulos V, Dimitriadis AS (2004) Intracranial aneurysms:
>60 Ο yes Ο no
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Clinical situation:
intraoperative findings. Neuroradiology 46:842–850. https://doi.
SAH Ο yes Ο no org/10.1007/s00234-004-1259-2
11. Sailer AM, Wagemans BA, Nelemans PJ, de Graaf R, van Zwam
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Cranial nerve deficit Ο yes Ο no


Clinical mass effect Ο yes Ο no WH (2014) Diagnosing intracranial aneurysms with MR angiog-
Radiological mass effect Ο yes Ο no raphy: systematic review and meta-analysis. Stroke 45:119–126.
Previous SAH Ο yes Ο no
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Others: ………………………………………………………………… Ο yes Ο no
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Bypass contemplated Ο yes Ο no Radiology 217:361–370. https://doi.org/10.1148/radiology.217.2.r
Visualization of possible donor artery (e.g. STA) Ο yes Ο no 00nv06361
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Collateral circulation Ο yes Ο no
preservation in intracranial aneurysm surgery: an overview with
Others……………………………………………………………………………. Ο yes Ο no
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org/10.4068/cmj.2017.53.1.47

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
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Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Current Strategies in the Treatment
of Intracranial Large and Giant
Aneurysms

Matthias Gmeiner and Andreas Gruber

Introduction demographics (age), and aneurysm morphology can be


applied [6, 7].
Very large and giant intracranial aneurysms are defined as Both reconstructive (clipping, coiling, stent-assisted coil-
aneurysms with a diameter >20 mm and >25 mm [1] ing, flow diversion [FD]) and deconstructive techniques
respectively. Giant aneurysms constitute approximately (parent artery occlusion [PAO], PAO in conjunction with
2–5% of all intracranial aneurysms [2–4]. The natural his- bypass surgery, and strategies of flow modification) are
tory of these lesions is poor, with reported mortalities rang- available for the treatment of cerebral aneurysms [8]. The
ing from 66–80%. The worst outcomes have been observed aim of this paper is to review the current literature on the
in untreated posterior circulation giant aneurysms [3–5]. management of very large and giant aneurysms and to
The majority of patients harboring very large and giant describe representative cases—treated by the senior author,
intracranial aneurysms (50–80%) present with thromboem- who has been dually trained and is cross-experienced in both
bolic events or symptoms of mass effect [3, 6], whereas microsurgical and endovascular techniques—to illustrate
subarachnoid hemorrhage (SAH) occurs in approximately possible treatment strategies.
20–30% [6].
In view of the poor natural course of these lesions, aggres-
sive treatment aiming for both aneurysm occlusion and relief Reconstructive Techniques
of mass effect has been recommended [6, 7]. The benefits of
active aneurysm therapy must be weighed against the inher- Reconstructive techniques are usually the preferred treat-
ent risks of treatment. Whereas surgical management carried ment strategy in the management of intracranial aneurysms,
a significant morbidity and mortality in the past [3], recent since these procedures do not compromise the patency of the
meta-analyses reported good clinical outcomes in as many as parent vasculature and in turn do not interfere with cerebral
80% of the patients when individualized treatment strate- blood flow distal to the aneurysm site. In the management of
gies—including both surgical and endovascular tech- very large and giant aneurysms, open surgical strategies of
niques—were adopted [2]. The risk-benefit assessment, direct aneurysm occlusion have proven technically difficult
however, will favor active therapy only when treatment is but often highly effective, whereas technically less challeng-
Copyright © 2021. Springer International Publishing AG. All rights reserved.

performed at high-volume cerebrovascular centers, where ing endovascular procedures, e.g., intrasaccular coil emboli-
the capacities of both neurosurgery and neurointervention zation, have proven ineffective in the long run. The role of
are available and individualized treatment concepts consid- more advanced endovascular strategies, e.g., FD stents and
ering anatomic location (cavernous vs. subarachnoid, ante- intra-aneurysmal FD, is still in the process of being defined.
rior circulation vs. posterior circulation), clinical presentation
(SAH vs. mass effect vs. incidental presentation), patient
Clipping and Clip Reconstruction

M. Gmeiner · A. Gruber (*) Direct surgical clip ligation of the neck with preservation of
Department of Neurosurgery, Kepler University Hospital, the parent vasculature remains the ideal reconstructive treat-
Linz, Austria ment strategy in the majority of very large and giant saccular
Johannes Kepler University (JKU) Linz, Linz, Austria aneurysms. Procedural outcomes usually depend on aneu-
e-mail: [email protected]; rysm morphology (calcifications, intrasaccular thrombus,
[email protected]

© The Author(s) 2021 19


G. Esposito et al. (eds.), Trends in Cerebrovascular Surgery and Interventions, Acta Neurochirurgica Supplement 132,
https://doi.org/10.1007/978-3-030-63453-7_3

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
20 M. Gmeiner and A. Gruber

complex anatomy), aneurysm location, parent artery caliber, with angiographic occlusion rates >90% 6 months after coil-
and perforator anatomy [4, 6, 9, 10]. ing had low rates (0.4%) of recurrent SAH within the subse-
In the management of very large and giant middle cere- quent 8 years [22]. In large and giant aneurysms, the reported
bral artery (MCA) aneurysms, direct surgical clipping is annual rebleeding rate of 1.9% after coil embolization was
considered the most effective and durable treatment, whereas substantially higher [23]. A retrospective study reporting
coiling was identified as an independent risk factor for outcomes after surgical or endovascular therapy of 184 very
retreatment in a recent study describing the management of large or giant aneurysms identified the following as risk fac-
106 large and giant MCA aneurysms [11]. Coiling of MCA tors for incomplete angiographic obliteration: (1) fusiform
aneurysms carries a higher recurrence risk even in smaller aneurysm morphology, (2) aneurysm location in the poste-
lesions. In detail, the recurrence risk following coil emboli- rior circulation, and (3) endovascular treatment (coiling or
zation of >7 mm MCA aneurysms was 17.5% [12], and that stent-assisted coiling) [24].
of MCA aneurysms ≥11 mm was 46% in recent publications
[13]. Long-term instability of MCA aneurysm occlusion was
reported in 3% of the patients receiving surgical clipping and Stent-Assisted Coiling
in >45% of the patients receiving intrasaccular coiling [14].
The success of direct clipping of very large and giant Intrasaccular coil embolisation has significant limitations in
aneurysms depends on the ability to soften the aneurysmal wide-necked aneurysms due to comparably lower packing
sac intraoperatively, usually achieved by temporary clipping densities and subsequently higher rates of recanalization.
of the parent vasculature or measures inducing transient car- Therefore, alternative techniques using so-called neck bridg-
diac standstill (i.e., pharmacologically induced hypodynamic ing devices have been introduced (Fig. 1d–f). The technique
standstill using Adenosine or electrically induced hyperdy- of stent-assisted coiling uses a stent—which per se is a non-­
namic standstill using rapid ventricular pacing). In cases of occlusive device—to provide a scaffold to hold the coils
extensive intrasaccular thrombosis, aneurysmotomy and within the aneurysmal sac [25]. Meta-analyses revealed that
subsequent thrombectomy under pharmacologic cerebropro- in patients harboring very large and giant aneurysms, occlu-
tection are required for successful clip reconstruction [6]. sion rates were significantly higher following stent-assisted
Multiple clips applied in different techniques (tandem clip- coiling [73%] when compared to coiling alone (59%) [26].
ping, stacked multiple clips, overlapping clips) are usually Of note, significantly higher treatment morbidities have been
required (Fig. 1a–c) [15, 16]. reported following stent-assisted coiling when compared to
regular intrasaccular coil embolization [27]. Stent-assisted
coiling has nowadays become a routine procedure that can be
Coil Embolization performed safely and effectively in expert hands. Since the
implanted device is endoluminal rather than intra-­
Coil embolization has proven ineffective in the treatment of aneurysmal, peri-interventional management of coagulation
very large and giant aneurysms. Low initial complete occlu- is of major importance and procedure-related complications
sion rates (10–60%) and high recanalization rates (56–90%) of in-stent thrombosis and subsequent distal thromboembo-
have been demonstrated in several studies [17, 18]. lism are still relevant issues. When compared to flow diver-
Mechanisms of recanalization include coil compaction, coil sion [FD], stent-assisted coiling of giant aneurysms has the
migration, and aneurysm regrowth [18, 19]. potential to further increase aneurysmal mass effect. It
In a previous study assessing the results of coil emboliza- should be pointed out that stent-assisted coiling of a giant
Copyright © 2021. Springer International Publishing AG. All rights reserved.

tion in patients with very large or giant aneurysms, the senior aneurysm can be a very expensive undertaking.
author reported a 71% complete or nearly complete angio-
graphic occlusion rate immediately after the intervention. Of
note, a single embolization served as definitive treatment for Flow Diversion
only 12.5% of the giant and only 31% of the very large aneu-
rysms in the long run [17]. In partially thrombosed aneu- Flow diverters have become an attractive alternative for the
rysms presenting with mass effect, selective coiling endovascular treatment of complex aneurysms in selected
reportedly resulted in continuous aneurysm growth in 18% cases [28–31] because the technique does not suffer from the
of the cases, whereas only 7% of the aneurysms decrease in aforementioned shortcomings of intrasaccular coil emboli-
size [20]. Coiling had little if any effect on the relief of symp- zation [17, 18, 20, 28]. Flow diverters initially received FDA
toms of mass effect. approval for the treatment of large and giant aneurysms
The current body of literature strongly suggests that the extending from the petrous to the superior hypophyseal seg-
initial angiographic occlusion rate after coil embolization is ment of the internal carotid artery [32] (Fig. 1g–i). Currently,
related to the risk of re-rupture [21]. Ruptured aneurysms however, a variety of aneurysms—including those p­ reviously

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Current Strategies in the Treatment of Intracranial Large and Giant Aneurysms 21
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Fig. 1 Reconstructive surgical and endovascular techniques. (a–c) ing site of the superior hypophyseal artery. Aneurysmal mass effect
Microsurgical clipping. Fifteen years after uneventful clipping of a resulted in optic nerve compression and subsequent visual field deficits.
7 mm left MCA bifurcation aneurysm, a 40 mm partially thrombosed The patient was treated by stent-protected coil embolization (f) and
aneurysm recurrence is detected on MRI (a). Since STA donor braches regained vision over the following months, an effect attributable to
were of insufficient caliber and three M2 branches were incorporated aneurysm shrinkage after embolization (A.G., procedure performed at
into the aneurysm sac, the decision was made to treat the aneurysm by the Medical University Vienna). (g–i) Flow diversion. Right ICA angio-
direct surgical clipping after temporary trapping, aneurysmotomy, and grams (g) demonstrate a very large intracavernous ICA aneurysm that
thrombectomy under pharmacologic cerebroprotection (b). resulted in partial ophthalmoplegia from mass effect and intracavernous
Intraoperative left ICA angiograms demonstrate sufficient aneurysm cranial nerve compression. The patient was treated by FD stenting (h),
obliteration (c) (A.G., procedure performed at the Kepler University which resulted in complete aneurysm occlusion (i) and delayed resolu-
Hospital Linz). (d–f) Stent-protected coil embolization. MRI (d) and tion of ophthalmoplegia due to post FD aneurysm shrinkage (A.G., pro-
right ICA angiograms (e) depict a 20 mm ICA aneurysm at the branch- cedure performed at the Medical University Vienna)

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
22 M. Gmeiner and A. Gruber

treated, acutely ruptured, small sized, located within the pos- sources indicate that all aneurysms that underwent FD stent-
terior circulation, as well as non-saccular lesions including ing either collapsed completely (in 90% of cases) or
fusiform, dissecting, and pseudoaneurysms—are treated decreased significantly in size (in 10% of cases) between 6
using FD techniques. For the time being, indications for FD and 18 months after the intervention, it is likely that the
treatment are unclear, and many procedures, especially those aforementioned mechanisms of post-FD stenting aneurysm
expanding FD indications from untreatable giant aneurysms expansion are transient in nature [38].
to comparably easy surgical cases, must still be considered A recent study reported a 95.2% complete occlusion rate
off-label uses of the device. in complex internal carotid artery aneurysms undergoing FD
Similar to stent-assisted coiling, FD stenting relies on an stenting in absence of hemorrhagic or ischemic cerebrovas-
endoluminal device creating an interface between the aneu- cular events [28]. In the same patient cohort, the complete
rysmal sac and the parent vasculature. Aneurysm occlusion aneurysm occlusion rate after 180 days was 73.6% [28, 40].
thereby occurs in a delayed fashion over weeks to months Other reports have demonstrated complete aneurysm occlu-
[23] by intra-aneurysmal flow modification, thrombus for- sions in as many as 76% of the giant aneurysms treated using
mation, and subsequent endothelial overgrowth of the aneu- FD stents. This success, however, came at the cost of compa-
rysm neck. Peri-interventional management of coagulation, rably higher treatment morbidities when compared to those
i.e., dual antiplatelet medication, is of major concern, and in of conventional coil embolization. In detail, the reported
turn FD stents have limited if any value in the management procedure-related mortality was 5% and the overall ischemic
of patients with acutely ruptured aneurysms [33]. Since stroke rate was 6%. Perforator strokes occurred in 3% and
intra-aneurysmal thrombosis occurs progressively over time patients with posterior circulation aneurysms were more
and intra-aneurysmal pressures will remain elevated even likely to be affected. In basilar artery aneurysms, perforator
after the initial angiographic occlusion—which is due to territory strokes were encountered in 14% [41]. The rates of
stagnant aneurysmal inflow rather than to aneurysm oblitera- post-procedural SAH or parenchymal hemorrhage were 3%
tion (“a flow diverter is not a pressure diverter”) [34]— each [29]. Aneurysm morphology may further influence the
patients managed using FD stents in the acute phase after success of FD treatment. Recent data indicate that permanent
aneurysmal SAH are still at risk for early rebleeding. complete aneurysm occlusion is less likely in aneurysms
Possible strategies to circumvent the problem of dual incorporating arterial side branches, i.e., in lesions where
anti-platelet medication for FD treatment in acutely ruptured major arteries arising from the aneurysm are jailed during
aneurysms include (1) techniques of intra-aneurysmal FD FD stent placement [42]. It should therefore be pointed out
and (2) staged procedures consisting of partial protective that the clinical safety of FD devices is still in a process of
coiling of the aneurysm dome in the acute phase followed by being defined [23]; e.g., a multicenter randomized care trial
later definitive FD treatment. Such staged procedures were and registry was recently halted due to safety and efficacy
both safe and effective in a recent series of 31 patients with concerns [43].
acutely ruptured intracranial aneurysms [35].
Unexplained cases of early post-interventional hemor-
rhages after FD treatment—occurring also in initially unrup- Deconstructive Techniques
tured aneurysms and with often fatal consequences under
dual anti-platelet medication—may also be explained by Deconstructive measures are indicated only in those cases
intrasaccular processes of active thrombus formation and where reconstructive treatment of cerebral aneurysms is
degradation affecting the integrity of the aneurysm wall [36– impossible or associated with unacceptable treatment mor-
Copyright © 2021. Springer International Publishing AG. All rights reserved.

38]. These mechanisms remain speculative, however, since bidities. As previously mentioned, these strategies include
any residual flow within the aneurysm may per se trigger [10, 44] therapeutic surgical or endovascular parent artery
further aneurysm growth or rupture [39]. In line with these occlusion (PAO), PAO in conjunction with flow replacement
findings, a recent study demonstrated significantly improved bypass surgery, was well as techniques of flow modification
occlusion rates in absence of post-interventional hemor- (e.g., deliberate basilar trunk occlusion to induce flow rever-
rhages in patients undergoing FD stenting in conjunction sal for the management of otherwise untreatable very large
with concomitant coiling when compared to FD treatment and giant basilar apex aneurysms).
alone (88.9% versus 61.5% complete occlusion rate, respec-
tively) [31].
Similar mechanisms may trigger early giant aneurysm Parent Artery Occlusion
growth after FD treatment. A recent retrospective study
found that 6 out of 45 aneurysms managed by FD stenting As demonstrated in Fig. 2a–c, PAO relies on competent
had increased >20% in size during the first 6 months and pro- crossflow via anterior and posterior communicating artery
duced symptoms of intracranial mass-effect [36]. Since other collaterals as well as leptomeningeal anastomoses. The

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Current Strategies in the Treatment of Intracranial Large and Giant Aneurysms 23
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Fig. 2 Deconstructive surgical and endovascular techniques. (a–c) STA–MCA double-barrel low-flow bypass revascularization (e) 48 h
Parent artery occlusion. Right ICA angiograms (a) demonstrate a giant before successful awake balloon test occlusion and subsequent endo-
intracavernous ICA aneurysm that exerted local mass effect and resulted vascular parent artery occlusion. The bypass in conjunction with pre-­
in complete right-sided ophthalmoplegia. The patient was managed by existent anterior communicating artery crossflow (f) was sufficient to
endovascular parent artery occlusion after successful balloon test occlu- revascularize the right hemisphere after therapeutic endovascular par-
sion. Left ICA angiograms (b) depict sufficient crossflow via the ante- ent artery sacrifice (A.G., procedure performed at the Medical
rior communicating artery to supply the right hemisphere after University Vienna). (g–i) Parent artery occlusion under venous high-­
therapeutic parent artery sacrifice (b). The intracavernous giant aneu- flow bypass protection. Right ICA angiograms depict a partially coiled,
rysm decreased in size significantly as depicted on follow-up MRIs (c) recurrent very large aneurysm of the right ICA at the branching site of
and the patient’s ophthalmoplegia gradually resolved over time (A.G., the superior hypophyseal artery, exerting progressive optic nerve com-
procedure performed at the Medical University Vienna). (d–f) Parent pression and resulting in right-sided visual loss (g). The patient was
artery occlusion under low-flow bypass protection. Right ICA angio- managed by saphenous vein high-flow bypass revascularization (h, i)
grams demonstrate a giant intracavernous ICA aneurysm (d) that followed by parent artery occlusion during the same procedure. The
became symptomatic by local cranial nerve compression and mani- patient recovered gradually but never regained vision in her right eye
fested in partial oculomotor nerve palsy. The patient was managed by (A.G., procedure performed at the Kepler University Hospital Linz)

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
24 M. Gmeiner and A. Gruber

safety and feasibility of this strategy is assessed during bal- the STA–MCA double-barrel technique (e.g., temporal and
loon test occlusions [BTO] in the awake patient prior to frontoparietal territories in cases of M1/M2 bifurcation
definitive surgical or endovascular vessel sacrifice. Many aneurysms), this may be difficult in cases of—single-bar-
surgeons, however, prefer revascularization in all cases that rel—high-flow revascularization. Recent publications have
require major vessel sacrifice [44]. PAO is often followed by reported a multiple reimplantation technique for the recon-
a significant reduction of aneurysm size and alleviation of struction of complex and giant MCA bifurcation aneurysms,
aneurysmal compressive mass effect (Fig. 2a–c). where the efferent M2 branches are serially reimplanted into
the saphenous vein donor graft [45]. The technical nuances
of indirect surgical aneurysm occlusion were addressed in a
 arent Artery Occlusion in Conjunction
P recent publication, describing 18 different bypass strategies
with Bypass Surgery for the treatment of 30 complex MCA aneurysms, all man-
aged with excellent surgical and clinical results [16].
In the vast majority of the cases, however, spontaneous col- Perforator occlusion in conjunction with PAO-induced
lateral crossflow is inadequate to provide sufficient hemi- thrombosis is always a major concern. A recent case series
spheric blood flow distal to the point of PAO. In these cases, describing the management of 141 giant aneurysms reported
cerebral revascularization is required prior to PAO. Generally thrombotic occlusion of perforators or branching arteries in
speaking, cerebral bypasses can be stratified according to 7% of the aneurysms receiving indirect treatment [10]. In
their function (flow replacement bypass, flow augmentation those cases, where complete surgical trapping or endovascu-
bypass), their donor grafts (pedicled, interpositional, in situ), lar coil embolization of the aneurysm is impossible due to
the sites of anastomosis (extracranial [EC]–intracranial [IC], delicate perforator anatomy, proximal or distal occlusions
EC–IC) and the flow provided (low-, intermediate-, and high may be performed. This strategy relies on intra-aneurysmal
flow) [44]. The revascularization technique selected for flow flow modification to reduce the risk of aneurysm rupture, to
replacement bypass surgery in the management of intracere- induce slow aneurysm thrombosis, and to preserve flow into
bral aneurysms depends on the treatment strategy chosen. In the perforating branches [10, 46]. In some cases, however,
cases in which bypass surgery is performed in conjunction postoperative aneurysm ruptures with devastating conse-
with surgical PAO during the same procedure (i.e., cases quences have been reported with this technique [47].
where neurologic assessment of the awake patient is not pos- Periprocedural ischemia due to prolonged temporary clip-
sible), high-flow bypass surgery is usually performed. It is ping times while suturing the anastomosis is another impor-
reasonable to “oversize” the bypass rather than to face isch- tant issue. The larger the caliber of the donor graft (i.e.,
emic complications due to insufficient low-flow bypass during high-flow bypass surgery), the larger—and thus more
revascularization (Fig. 2g–i). In those cases, however, where proximal—the recipient artery should be. In turn, the more
the therapeutic strategy involves cerebral revascularization proximal the recipient artery, (1) the larger the vascular terri-
1–2 days ahead of BTO and endovascular PAO, other bypass tory rendered ischemic during temporary clipping for sutur-
techniques (i.e., double barrel STA–MCA bypass in cases of ing the anastomosis, and (2) the more difficult and usually
anterior circulation aneurysms, OA–PCA or OA–PICA time-consuming the suturing of the anastomosis will be. To
bypasses in cases of posterior circulation aneurysms) may be overcome this problem, the technique of excimer laser-­
justified. The senior author has successfully performed this assisted non-occlusive anastomosis [ELANA] bypass was
technique in over 40 cases (Fig. 2d–f). Anterior and posterior introduced to provide high-flow revascularization without
communicating artery crossflow as well as leptomeningeal cross-clamping related distal ischemia or stroke. The role of
Copyright © 2021. Springer International Publishing AG. All rights reserved.

collaterals frequently contribute further to post PAO hemi- this technique, usually reserved for the most challenging
spheric revascularization. lesions, is still in a process of being defined [44, 48]. In many
The occlusion rates reported with indirect aneurysm treat- cases, originally considered suitable for the ELANA proce-
ment are high. A recent series described the management of dure, FD stenting and other innovative reconstructive endo-
82 patients with complex intracranial aneurysms using both vascular techniques have proven effective as well.
EC-IC and IC-IC bypasses and reported aneurysm oblitera-
tion rates of over 97% with low treatment-related morbidi-
ties [9]. Aneurysms managed by PAO in conjunction with Conclusion
bypass revascularization usually shrink in size over time. A
recent multi-center study observed an average delayed vol- Very large and giant intracranial aneurysms are among the
ume reduction of 55.2% in giant aneurysms treated by PAO most challenging pathologies in neurosurgery. Patients
and bypass revascularization [1]. harboring such lesions should be managed at high-volume
Whereas revascularization of multiple vascular territo- cerebrovascular centers by multidisciplinary teams trained
ries distal to the site of PAO is usually easily obtained using in all techniques of open and endovascular neurosurgery.

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Current Strategies in the Treatment of Intracranial Large and Giant Aneurysms 25

In view of the poor natural history, active management 11. Park W, Chung J, Ahn JS, Park JC, Kwun BD (2017) Treatment of
large and giant middle cerebral artery aneurysms: risk factors for
using ­multiprofessional individualized approaches [4, 6, 7, unfavorable outcomes. World Neurosurg 102:301–312
9–11, 15, 16, 44–46, 48–50] is required to achieve com- 12. Kadkhodayan Y, Delgado Almandoz JE, Fease JL, Scholz
plete aneurysm occlusion, relief of mass effect, and oblit- JM, Blem AM, Tran K, Crandall BM, Tubman DE (2015)
eration of the embolic source with acceptable treatment Endovascular treatment of 346 middle cerebral artery aneurysms:
results of a 16-year single-center experience. Neurosurgery
morbidities [7]. Microsurgical and endovascular tech- 76:54–60; discussion 60–1.
niques are complementary rather than competitive strate- 13. Iijima A, Piotin M, Mounayer C, Spelle L, Weill A, Moret J (2005)
gies that can ideally be combined in hybrid procedures. Endovascular treatment with coils of 149 middle cerebral artery
Both microsurgery [6, 7, 15, 16] and neurointervention are berry aneurysms. Radiology 237:611–619
14. Smith TR, Cote DJ, Dasenbrock HH, Hamade YJ, Zammar SG, El
still improving in technique and outcome. With an increas- Tecle NE, Batjer HH, Bendok BR (2015) Comparison of the effi-
ing endovascular caseload, neurosurgeons working in the cacy and safety of endovascular coiling versus microsurgical clip-
field of cerebrovascular disease may find themselves in a ping for unruptured middle cerebral artery aneurysms: a systematic
“low case scenario” in the near future, where innovative review and meta-analysis. World Neurosurg 84:942–953
15. Lawton MT (2010) Seven aneurysms. Tenets and techniques for
strategies of surgical training—including haptic and vir- clipping. Thieme, New York, NY
tual models of simulation [51]—will be of major impor- 16. Tayebi Meybodi A, Huang W, Benet A, Kola O, Lawton MT
tance to maintain the current levels of technical skill and (2017) Bypass surgery for complex middle cerebral artery aneu-
procedural quality. rysms: an algorithmic approach to revascularization. J Neurosurg
127:463–479
17. Gruber A, Killer M, Bavinzski G, Richling B (1999) Clinical and
Conflict of Interest The authors declare that they have no conflict of angiographic results of endosaccular coiling treatment of giant and
interest or a financial disclosure. very large intracranial aneurysms: a 7-year, single-center experi-
ence. Neurosurgery 45:793–803; discussion 803–4.
18. Wang B, Gao BL, Xu GP, Xiang C, Liu XS (2015) Endovascular
embolization is applicable for large and giant intracranial aneu-
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Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Computational Fluid Dynamics
for Cerebral Aneurysms in Clinical
Settings

Fujimaro Ishida, Masanori Tsuji, Satoru Tanioka,


Katsuhiro Tanaka, Shinichi Yoshimura,
and Hidenori Suzuki

Introduction (Materialise Japan, Kanagawa, Japan) to extract aneurysm


geometry as stereolithography (STL). The STL file is inte-
Computational fluid dynamics (CFD) is a computational sci- grated into 3-matic (Materialise Japan, Kanagawa, Japan) and
ence which connects experiment and theory. Therefore, it is geometry in the region of interest is segmented. In addition,
important to understand the need of validation and verifica- the geometry is remeshed by a triangle measuring 0.25 mm at
tion of CFD for cerebral aneurysms when the hemodynamic the maximum length for correction of a distortion comprising
results are applied to surgical decision-making in clinical the STL. The fluid domain is meshed using ANSYS ICEM
settings. CFD (ANSYS Inc. Canonsburg, Pennsylvania) to create tet-
CFD for a cerebral aneurysm using the patient-specific rahedral elements that are established as 0.6 mm at maximum
geometry model was first reported by DA Steinman et al. in and 0.1 mm at minimum using the Octree’s method. On the
2003 [1], and it has been revealing that hemodynamics con- geometry surface, six prism layers are added with total
tributes to understanding aneurysm pathology including ini- heights of 0.148 mm. The inlet is prolonged vertically at the
tiation, growth, and rupture [2–10]. On the other hand, CFD surface to establish fully developed laminar flow according to
has not permeated into a clinical setting of cerebral aneu- Poiseuille’s law.
rysms due to several limitations including analysis time and Numerical modeling is performed using ANSYS CFX
complicated process. Therefore, we present our practical (ANSYS Inc. Canonsburg, Pennsylvania). For the fluid
application of CFD for the treatment planning of cerebral domain, 3D laminar flow fields are obtained by solving the
aneurysms. continuity and Navier-Stokes equations, and discretization is
made by the finite volume method. Blood is assumed to be
an incompressible Newtonian fluid with a density of 1056 kg/
CFD Process for Cerebral Aneurysms m3 and a viscosity of 0.0035 Pa s. Typical flow waveform of
phase-contrast MR imaging is scaled to the inlet and a flow
The CFD process for cerebral aneurysms is the following [2, rate is proportional to achieve a physiological wall shear
11, 12]: the digital imaging and communication in medicine stress (WSS). Traction-free boundary conditions are applied
(DICOM) datasets of 3D CT angiography and 3D rotational to the outlets. The time steps are 0.0001 s and transient anal-
Copyright © 2021. Springer International Publishing AG. All rights reserved.

angiography are loaded into Mimics Innovation Suite ysis with an initial value specification is performed.

F. Ishida (*) · M. Tsuji · S. Tanioka · K. Tanaka


Department of Neurosurgery, Mie Chuo Medical Center, NHO, Rupture Status
Tsu, Japan
e-mail: [email protected] A lot of CFD studies were reported regarding the rupture
S. Yoshimura status of cerebral aneurysms. Compared with unruptured
Department of Neurosurgery, Hyogo College of Medicine, aneurysms, ruptured aneurysms had significant characteris-
Hyogo, Japan
tics such as low WSS [12–15], high oscillatory shear index
H. Suzuki (OSI) [12, 14], low aneurysm formation indicator (AFI)
Department of Neurosurgery, Mie University Graduate School of
[12], prolonged relative residence time (RRT) [16], complex
Medicine, Tsu, Mie, Japan

© The Author(s) 2021 27


G. Esposito et al. (eds.), Trends in Cerebrovascular Surgery and Interventions, Acta Neurochirurgica Supplement 132,
https://doi.org/10.1007/978-3-030-63453-7_4

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
28 F. Ishida et al.

flow pattern, unstable flow pattern [17], and high oscillatory bral angiogram early after coil embolization, and lower
velocity index [18]. Among these hemodynamic parameters, packing density.
low magnitude of WSS is the most noticeable hemodynamic A number of authors reported hemodynamic risk fac-
characteristic associated the rupture status. Since the magni- tors associated with coiled aneurysms. High WSS
tude of WSS was quantified as time-averaged value, spatial observed near the remnant neck of partially coiled aneu-
minimum and maximum values on the dome, normalized rysms are more likely to have recanalization [20].
WSS and low shear area ratio, we should recognize that the However, since the geometry of neck remnant is obtained
distribution of low WSS would be an unchanged observa- only after coiling, it is impossible to predict the recur-
tion. However, comparison of the magnitude of WSS in clin- rence risk as presurgical decision-­making based on this
ical practice should be carried out as an optimal quantification. method. In a clinical setting, it is desirable that hemody-
For instance, time-averaged WSS would be allowed to inves- namic evaluation using presurgical geometry models can
tigate the rupture status of multiple cerebral aneurysms in a predict recanalization of coiled aneurysms. Sugiyama
patient with subarachnoid hemorrhage. In particular, mirror et al. demonstrated the correlations between the hemody-
aneurysms are a useful disease model to predict the rupture namics before coil embolization and the outcomes after
site of an aneurysm. On the other hand, normalized WSS treatment for basilar tip aneurysms [21]. In their study,
would be recommended for measuring WSS of aneurysms at aneurysmal inflow rate coefficient (AIRC) was calculated
different locations. by the following equation:
Qa
AIRC =
Qb
Hyperplastic Remodeling of Aneurysm Wall
where Qa and Qb were the aneurysmal inflow rate and the
Ku described OSI that was a hemodynamic parameter to basilar artery flow rate, respectively.
evaluate fluctuation of WSS vectors in 1985 [19]. The stud- In 57 basilar tip aneurysms, AIRC was significantly
ies using the pulsatile flow data in a Plexiglas model and higher in the recanalized group and correlated to the
intimal plaque thickness in five human carotid bifurcations types of basilar bifurcation configuration. Although it
revealed that oscillations in the direction of wall shear may was sensible to make a decision for coil embolization
enhance atherogenesis. Aside from OSI, RRT and AFI can based on these findings, packing density should be con-
also evaluate oscillation of WSS vectors. These hemody- sidered simultaneously. Therefore, CFD using porous
namic parameters were examined regarding hyperplastic media modeling was developed to predict recurrence of
remodeling of aneurysm wall. Since these hemodynamic coil embolization. Umeda et al. calculated residual flow
parameters showed similar distribution to high oscillatory volume (RFV) to quantify the residual aneurysm vol-
WSS vector (Fig. 1), we can use any of these variables as the ume after simulated coiling, which has a mean fluid
preoperative predictor of thick aneurysm wall. In addition, domain above 1.0 cm/s [22]. In 37 unruptured cerebral
we should recognize that a high OSI region corresponds to a aneurysms, the recurrence group had significantly larger
low WSS region. RFV than the stable group. Receiver-operating charac-
The prediction of hyperplastic remodeling lesions using teristic (ROC) curve analyses showed that the cut-off
CFD [6, 11, 16] would contribute to avoiding intraoperative value of RFV was 20.4 mm 3 and that the area under the
risks such as inadequate temporary clipping and obstruction ROC curve was 0.86. Although this study was retrospec-
of small branches (Fig. 2). tive, these findings could be applied to indicate a target
Copyright © 2021. Springer International Publishing AG. All rights reserved.

packing density. In addition, CFD using double porous


media modeling was developed to simulate stent-
Recurrence of Coiled Aneurysms assisted coiling (Fig. 3) [23]. Since these porous media
modeling have discrepancies between actual distribu-
Coil embolization of cerebral aneurysms is widely used; tion of placed coil and expanded strut in the aneurysm,
however, recanalization and re-treatment occur more often large-scale clinical studies are required to confirm the
compared with surgical clipping. Several risk factors for accuracy of the prediction for recurrence of coiled
recanalization and re-treatment have been reported, such as a aneurysms.
large aneurysm, wide neck width, minor recurrence on cere-

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Computational Fluid Dynamics for Cerebral Aneurysms in Clinical Settings 29

a b

0 0.5 0 50 [1/Pa]

c d

–1 1 0 20 [Pa]

Fig. 1 Comparison of hemodynamic parameters to evaluate the fluc- similar distribution to prolonged RRT and low WSS; (d) visualization
tuation of WSS vector in a patient of ruptured middle cerebral artery of WSS, in which high OSI, prolonged RRT and low AFI regions are
aneurysm: (a) visualization of OSI, showing high OSI near the neck; depicted in the low WSS area
Copyright © 2021. Springer International Publishing AG. All rights reserved.

(b) visualization of RRT; (c) visualization of AFI, in which low AFI has

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
30 F. Ishida et al.

a b c

0 0.5 0 0.5 0 20 [Pa]

d e f

Fig. 2 Seventy-six-year-old man with unruptured left internal carotid (d, e) intraoperative photography, demonstrating atherosclerotic lesions
artery-anterior choroidal artery bifurcation aneurysm: (a, b) visualiza- of the parent artery (white arrow) and at the backside of the aneurysm
tion of OSI, showing high OSI at the parent artery (white arrow) and the neck (black arrow), respectively, which correspond with high OSI
backside of the aneurysm neck at which anterior choroidal artery arises regions; (f) aneurysm clip is applied with an intended space to keep
(black arrow); (c) visualization of time-averaged WSS, showing distri- blood flow of the anterior choroidal artery
bution of low WSS (white arrow) which is similar to that of high OSI;
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Computational Fluid Dynamics for Cerebral Aneurysms in Clinical Settings 31

a b c

Fig. 3 Seventy-nine-year-old woman with left internal carotid artery-­ double porous media setting, one of which is a porous media setting for
posterior communicating artery bifurcation aneurysm: (a) 3D surface the coiled aneurysm and another of which is that for an intracranial
rendering image of rotational angiography; (b) angiography after stent-­ stent (arrow), to evaluate the hemodynamic changes of stent-assisted
assisted coiling of the aneurysm with a packing density of 35.9%; (c) coiled aneurysm. Residual flow volume (pink domain) is 62.3 mm3,
head CT revealing subarachnoid hemorrhage 19 months after the coil- which is larger than the cut-off value to predict the recurrence of coiled
ing; (d) left internal carotid artery angiography revealing the recanali- aneurysms
zation of the coiled aneurysm; (e) retrospective CFD findings using
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
32 F. Ishida et al.

Conclusions 10. Tsuji M, Ishikawa T, Ishida F, Furukawa K, Miura Y, Sano T,


Tanemura H, Umeda Y, Shimosaka S, Suzuki H (2017) Stagnation
and complex flow in ruptured cerebral aneurysms: a possible asso-
This review describes the practical application of CFD to ciation with hemostatic pattern. J Neurosurg 126:1566–1572
treatment planning of cerebral aneurysms. Several hemody- 11. Furukawa K, Ishida F, Tsuji M et al (2018) Hemodynamic charac-
namic parameters have valuable aspects not only in an endo- teristics of hyperplastic remodeling lesions in cerebral aneurysms.
PLoS One 13:e0191287
vascular treatment but also in a direct clipping. Although 12. Miura Y, Ishida F, Umeda Y, Tanemura H, Suzuki H, Matsushima
prospective trials are needed to evaluate the rupture risk of S, Shimosaka S, Taki W (2013) Low wall shear stress is indepen-
unruptured cerebral aneurysms determined using CFD, dently associated with the rupture status of middle cerebral artery
recent knowledge of hemodynamics of cerebral aneurysms aneurysms. Stroke 44:519–521
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Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Microneurosurgical Management
of Posterior Inferior Cerebellar Artery
Aneurysms: Results of a Consecutive
Series

Mattia Del Maestro, Sabino Luzzi, and Renato Galzio

Introduction spective study is to analyze the results of 25 PICA aneurysms


surgically treated, mainly focusing on the choice of the
PICA aneurysms are rare. Their incidence accounts for approach and technical nuances.
0.49–3% of all intracranial aneurysms [1–3]. However,
they are most common within the posterior circulation
ones after those of the basilar tip. Most are left-sided due to Materials and Methods
the prevalence of the vertebral artery. The saccular geome-
try is usually the most frequent, but dissecting or fusiform Between 2008 and 2018, 25 patients harboring 25 PICA
aneurysms are also relatively more common than in other aneurysms were surgically treated by the senior author
cerebral arteries [2, 3]. PICA has a complex and variable (R.G.) at two institutions: San Salvatore City Hospital,
course among all of the intracranial arteries, it has a small L’Aquila, Italy, and Foundation IRCCS Policlinico San
diameter, projecting along the brainstem and cerebellum. Matteo, Pavia, Italy. Only patients harboring saccular aneu-
According to Lister et al., five segments are classically rysms were selected and retrospectively reviewed. Aneurysms
described [4]. Because of the proximity to the lower cranial were classified according to the five PICA segments reported
nerves and frequent involvement of perforating arter- by Lister et al. [4]. Proximal aneurysms were defined as
ies from the proximal segments, both microsurgical and those arising from the vertebral artery-PICA junction to the
endovascular treatment of PICA aneurysms are tonsillo-medullary segment, the remnants being been con-
challenging. sidered as distal. Factors affecting the choice of the approach
In 1953, Rizzoli and Hayes first reported successful surgi- were also analyzed. Overall neurological outcome was
cal treatment of a PICA aneurysm operated in 1947 [5, 6]. reported as good, moderate, severe, and death, on the basis of
Since then, several reports on the surgical management of an mRS score of 0–2, 3–4, 5, and 6, respectively. The out-
PICA aneurysms were published, but only a few of them come evaluation was also reported according to the clinical
were based on a large patient’s cohort. The aim of this retro- onset and the involved PICA segment. The angiographic out-
come was evaluated on the basis of the complete exclusion of
the aneurysm at the sixth-month follow-up.
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Del Maestro M. (*)


PhD School in Experimental Medicine, Department of Clinical-­
Surgical, Diagnostic and Pediatric Sciences, University of Pavia, Results
Pavia, Italy
Neurosurgery Unit, Department of Surgical Sciences, Fondazione Nineteen patients were females and the average age was
IRCCS Policlinico San Matteo, Pavia, Italy
43 years (range 18–69). Nine patients suffered from hyper-
e-mail: [email protected]
tension, two from diabetes, three from hypercholesterolemia,
Luzzi S. · Galzio R.
and one from obesity. Nineteen patients were smokers. In one
Neurosurgery Unit, Department of Surgical Sciences, Fondazione
IRCCS Policlinico San Matteo, Pavia, Italy patient, familiar history of aneurysms was found. Admission
computed tomography (CT) angiography and digital sub-
Neurosurgery Unit, Department of Clinical-Surgical, Diagnostic
and Pediatric Sciences, University of Pavia, Pavia, Italy traction angiography (DSA) were performed by default in all
e-mail: [email protected] patients. A contrast-enhanced MRI was performed in all large

© The Author(s) 2021 33


G. Esposito et al. (eds.), Trends in Cerebrovascular Surgery and Interventions, Acta Neurochirurgica Supplement 132,
https://doi.org/10.1007/978-3-030-63453-7_5

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
34 Del Maestro M. et al.

Table 1 Demographic and clinical presentation brain arteriovenous malformations [7–15]. But we strongly
Patients believe that neurovascular training is the most important tool
No. of Ruptured Unruptured by far to improve the technique and avoid complications [16]
Patients aneurysms aneurysms Exclusion of the aneurysm was achieved in 23 cases treated
[no. 25] [no. 15] [no. 10]
by clipping. Two complex aneurysms underwent to an in situ
Gender
Females 19 (76%) 11 8 PICA-PICA bypass before the trapping. Table 2 reports the
Males 6 (24%) 4 2 overall data about the surgical management of the present
Age: mean 43 years old series (Tab. 2). Neuronavigation and endoscope-assisted
(18–69) techniques were commonly employed, the latter being been
Comorbidities useful for both the aneurysms having a huge blind spot and
Hypertension 9 7 2 those very close to perforating arteries. Micro-Doppler
Diabetes 2 2 1 (20 MHz System, Mizuho Medical Co., Ltd., Tokyo, Japan)
Hypercolesterolemia 3 2 –
ultrasound-based evaluation of the flow was implemented.
Obesity 1 1 –
Smokers (76%) 19 16 3
Indocyanine green video angiography (Flow 800 Infrared
Clinical presentation Module, OPMI Pentero 800, Zeiss, Oberkochen, Germany)
Ruptured Aneurysms 15 and fluorescein angiography (Yellow 560 Fluorescence
 SAH Module, Kinevo 900, Zeiss, Oberkochen, Germany) were
 Hunt Hess scale I–III 11 also introduced since 2009 and 2018, respectively. Sixth-­
 Hunt Hess scale IV 3 month postoperative DSA was available in all but one patient.
 Hunt Hess scale V 1 Total exclusion of the aneurysm was achieved by means of
 Cerebellar life 4 a single procedure in 22 cases. In three cases, a remnant was
threatening
hematoma revealed imposing a redo surgery. No recurrences occurred
Unruptured Aneurysms 10 during the follow-up.
 Vertigo and gait 3 A good overall outcome was achieved in all but one
instability unruptured aneurysm and in 60% of those ruptured. A mod-
 Asymptomatic 7 erate outcome was observed in 16% of patients, whereas a
severe outcome occurred in one patient who suffered by a
permanent deficit of the lower cranial nerves. One patient,
and giant aneurysms to reveal intraluminal thromboses. In 15 having a giant ruptured proximal PICA aneurysm, died.
aneurysms (72%) subarachnoid hemorrhage (SAH) was the Table 3 reports the overall outcome of the present
onset, four of which being been associated with a life-threat- series (Tab. 3).
ening cerebellar hematoma. Three giant aneurysms presented
with vertigo and gait ­instability and seven further aneurysms
were incidental. Table 1 summarizes demographics and Illustrative Cases
clinical presentation data of the present series (Tab. 1) Nine
aneurysms were small (<7 mm), 11 medium (7–14 mm), Case 1 The case of a medium VA-PICA aneurysm is
two large (15–24 mm) and three giant (>25 mm). Nineteen reported (Fig. 1). A 35-year-old patient had an incidental
aneurysms were proximal and, among these, ten involved finding of a left VA-PICA unruptured aneurysm after a mild
the VA-PICA junction. Six involved the anterior-medullary traumatic brain injury (Fig. 1a). CT angiography and DSA
Copyright © 2021. Springer International Publishing AG. All rights reserved.

segment and three the lateral-­medullary segment. Of the demonstrated the involvement of PICA (Fig. 1b, c). A left
remaining distal aneurysms, two were located on the tonsillo- far-lateral transcondylar approach was performed and the
medullary segment, one on the telovelotonsillary segment, aneurysm was clipped (Fig. 1e, f). Postoperative CT angiog-
and one on the cortical segment. Peculiar patient character- raphy documented the complete exclusion of the aneurysm
istics involving PICA segment and bony anatomy were the with a preserved flow into the left PICA (Fig. 1g). Patient
main factors influencing the choice of approach. Far-lateral had a good recovery (mRS 1).
approach was the approach of choice for all proximal aneu-
rysms, while median or paramedian suboccipital approaches
were used for distal ones. An early surgery (within 24 h) Case 2 The case of a giant distal PICA aneurysm is reported
was performed in all ruptured aneurysms. Since 2012, in all (Fig. 2). A 64 years-old patient suffering from a severe head-
elective cases, intraoperative neurophysiological monitoring ache and dizziness underwent to an MRI showing a giant
involving somatosensory, motor, and brainstem auditory- thrombosed aneurysm causing a right cerebellar compres-
evoked potentials was implemented, adopting a defined sion (Fig. 2a). CT angiography and DSA demonstrated the
protocol that is also used in all intracranial aneurysms and involvement of the distal PICA (Fig. 2b, c). A median suboc-

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Microneurosurgical Management of Posterior Inferior Cerebellar Artery Aneurysms: Results of a Consecutive Series 35

Table 2 Overall data of the surgical management


Aneurysms
Aneurysms no. Approach Treatment
Size
Small (<7 mm) 9 9 Clipping
Medium (7–14) 11 11 Clipping
Large (15–24) 2 1 Clipping
1 Trapping + PICA-PICA by-pass
Giant (>25 mm) 3 2 Clipping
1 Trapping + PICA-PICA by-pass
Anatomical distribution
VA-PICA 10 Far lateral
Anterior medullary 6 Far lateral
Lateral medullary 3 Paramedian suboccipital
Tonsillomedullary 2 Paramedian suboccipital
Telovelotonsillary 1 Median suboccipital
Cortical 1 Median suboccipital

Table 3 Overall patient outcomes about distal aneurysms at all, this aspect has to be probably
mRS Ruptured aeurysms Unruptured aneurysms
related to the thinner walls of the distal ones [24–26]. The
Proximal Distal Proximal Distal well-known risk of rebleeding of ruptured PICA aneurysms,
0 – 1 3 1 up to 78%, imposes an early treatment. In this series, all hem-
1 2 3 4 – orrhagic patients underwent surgery within 24 hours and, for
2 4 1 – – patients with an impending-life hematoma, the indication for
3 3 – 1 – surgery was mainly based upon an evidence-­based manage-
4 1 – – – ment algorithm about intracerebral hemorrhages reported
5 1 – – – by our group [27]. Regardless of the clinical onset, all the
6 1 – – –
patients underwent CTA and DSA. A 4- or 6-vessel DSA
is recommended for all PICA aneurysms, depending by the
cipital approach was performed and the aneurysm was need for flow replacement, is recommended for all PICA
clipped after thrombectomy, the indocyanine green video aneurysms, also because of the well-­known risk to miss very
angiography confirmed the patency of the PICA (Fig. 2d–g). distal ones [28]. Indeed, one of the authors reported a very
Postoperative CT and CT angiography documented the com- rare case of an extra-cranial small aneurysm of the PICA
plete exclusion of the aneurysm (Fig. 2h, i). Patient had a which was initially missed by CT angiography. The labyrinth
good recovery (mRS 0). of neurovascular bundles present in the posterior fossa makes
the surgical exposure of PICA aneurysms really challenging.
A careful preoperative evaluation of the patient’s vascular and
Discussion bony anatomy is needed to tailor any approach, especially
to assess the relationships between VA-PICA complex, the
Historically speaking, posterior circulation aneurysms were jugular tubercle, and the occipital condyle. The choice of the
Copyright © 2021. Springer International Publishing AG. All rights reserved.

always considered a tough dare for surgeons. In 1829, correct surgical approach has to be considered the crossroads
Cruvelhier reported the first description of a spherical aneu- in the microsurgical treatment of these aneurysms. In this
rysm arising from the PICA-vertebral junction [17]. series, 19 proximal aneurysms were exposed through a far-
Afterward, in 1854, Fernet reported the first case of a distal lateral approach without drilling of the condyle in most cases.
PICA aneurysms [1]. The rarity of PICA aneurysms justifies Conversely, Bertalanffy et al. used the transcondylar approach
the few large series reported [18–21]. Still today, with 146 as a rule [29]. Ambrosio et al. suggest the routine use of the
cases, that of Peerless and Drake remains the largest ever extreme-­lateral approach to reach the proximal PICA from a
reported series about PICA aneurysms. In these aneurysms, corridor remaining below the lower cranial nerves [30].
the need for treatment is dictated by their high risk of rup- In the elective treatment of proximal PICA aneurysms,
ture, high mortality, and the usual younger age of the affected the use of the endoscope as an adjuvant tool has to be
patients [19]. The mean reported age range is from 44.6– ­considered. Our group have already stressed the importance
51 years [22, 23]. The average age was slightly lower in the of endoscope-assisted techniques in the treatment of several
present series, with a prevalence of female sex. neurosurgical pathologies [31, 32], but particularly in aneu-
Interestingly, all but one of the distal aneurysms were rup- rysm surgery where, often, the endoscope view allows spar-
tured, three of which of small size. Indeed, as already reported ing perforating branches within blind spots.

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
36 Del Maestro M. et al.

Fig. 1 CT angiography and DSA revealing a VA-PICA unruptured documenting the complete exclusion of the aneurysm with a preserved
regular aneurysm (a–c). Left far-lateral transcondylar approach and flow into the left PICA (f, g)
clipping of the aneurysm (d, e). Postoperative CT and CT angiography
Copyright © 2021. Springer International Publishing AG. All rights reserved.

Fig. 2 MRI angiography showing a giant thrombosed aneurysm caus- and virtual videoangiography with indocyanine green (d–g).
ing a right cerebellar compression (a). CT angiography and DSA dem- Postoperative CT and CT angiography documenting the complete
onstrating the involvement of the distal PICA (b, c). Median suboccipital exclusion of the aneurysm (h, i)
approach, exposure of the thrombosed aneurysm, dissection, clipping

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Microneurosurgical Management of Posterior Inferior Cerebellar Artery Aneurysms: Results of a Consecutive Series 37

The six aneurysms arising from the distal PICA were technical nuances. World Neurosurg 116:e340–e353. https://doi.
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Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
Posterior Circulation Aneurysms:
A Critical Appraisal of a Surgical Series
in Endovascular Era

Sabino Luzzi, Mattia Del Maestro, and Renato Galzio

Introduction Materials and Methods

Posterior circulation aneurysms have a worse natural his- Collected data concerned demographics, clinical onset,
tory than anterior aneurysms, mainly because of their the prevalence of site and size, approaches, and outcome of
higher risk of rupture and poor outcome [1]. This aspect 149 patients surgically treated because they harbored one or
imposes the need for treatment in most cases, especially in more posterior circulation aneurysms have been retrospec-
younger patients. The advent of the endovascular era and tively reviewed. All the patients were operated on by the
its constant refinement through the continuous improve- senior author (RG) in three different hospitals over a period
ment of the devices has dramatically changed the treat- of 28 years between January 1990 and December 2018.
ment standard for many but not all of the posterior circle Aneurysms were classified as proximal and distal. The prox-
aneurysms. Exceptions are aneurysms involving the distal imal ones involved vertebral artery (VA), basilar artery (BA),
segments of the cerebellar arteries, most basilar tip aneu- and the proximal segments of the posterior cerebral artery
rysms, and the giant ones for which microneurosurgery (PCA) and cerebellar arteries. The remaining sites were con-
remains a rational option. The aim of this study is a critical sidered as distal. For outcome evaluation, the patients were
appraisal of the overall results of a retrospective surgical divided in to two groups: <65 and ≥65 years old.
series aimed to identify those posterior circulation aneu- The Angiographic outcome was evaluated based on the com-
rysms for which microneurosurgery still today maintains a plete exclusion of the aneurysm at a six-month follow-up.
key role. The Neurological overall outcome was reported according to
patients’ age, clinical onset, and site, and size of the aneu-
rysms. Glasgow Outcome Score (GOS) 1 and 2 were consid-
ered as “good recovery,” whereas GOS 3, 4, and 5 were
considered as “moderate disability,” “severe disability,” and
“death-vegetative state,” respectively.

Results
Copyright © 2021. Springer International Publishing AG. All rights reserved.

S. Luzzi (*) · R. Galzio


Neurosurgery Unit, Department of Clinical-Surgical, Diagnostic
and Pediatric Sciences, University of Pavia, Pavia, Italy Patients Demographics and Clinical Data
Neurosurgery Unit, Department of Surgical Sciences, Fondazione
IRCCS Policlinico San Matteo, Pavia, Italy Average patient age was 56.7 ± 14.2 years. Admission
e-mail: [email protected]
contrast-­enhanced computed tomography (CT) angiogra-
M. Del Maestro phy was the rule for all patients. Preoperative digital sub-
Neurosurgery Unit, Department of Surgical Sciences, Fondazione
IRCCS Policlinico San Matteo, Pavia, Italy traction angiography (DSA) was performed in all
unruptured or complex aneurysms. In elective cases, the
PhD School in Experimental Medicine, Department of Clinical-­
Surgical, Diagnostic and Pediatric Sciences, University of Pavia, need for a balloon test occlusion (BTO) was assessed on a
Pavia, Italy case-by-case basis. A contrast-enhanced MRI was per-
e-mail: [email protected] formed in all very large and giant aneurysms to reveal

© The Author(s) 2021 39


G. Esposito et al. (eds.), Trends in Cerebrovascular Surgery and Interventions, Acta Neurochirurgica Supplement 132,
https://doi.org/10.1007/978-3-030-63453-7_6

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
40 S. Luzzi et al.

Table 1 Site and Size Prevalence of Posterior Circulation Aneurysms


N (%) Size
Regular Large (13–24 mm) Giant
Small (7 mm) (7–12 mm) N (%) (25 mm)
Site N (%) N (%) N (%)
Proximal Basilar tip + PCA (P1) + SCA 91 (58%) 17 (18.7%) 57 (62.6%) 7 (7.7%) 10 (11%)

Midbasilar trunk + proximal AICA 9 (5.7%) 2 (22.2%) 4 (44.4%) 2 (22.2%) 1 (11.1%)


VB Junction 10 (6.4%) 2 (20%) 5 (50%) 2 (20%) 1 (10%)
VA (V4) + proximal PICA (anterior + lateral 27 (17.2%) 5 (18.5%) 16 (59.3%) 3 (11.1%) 3 (11.1%)
medullary segment)
Distal PCA (P2-P3) 7 (4.5%) 1 (14.3%) 2 (28.6%) 1 (14.3%) 3 (42.9%)
Distal SCA 3 (1.9%) – 1 (33.3%) 1 (33.3%) 1 (33.3%)
Distal AICA 4 (2.5%) 2 (50%) 1 (25%) – 1 (25%)
Distal PICA (tonsillo-­medullary 6 (3.8%) – 2 (33.3%) 2 (33.3%) 2 (33.3%)
+ telovelotonsillar + cortical segment)
Tot. 157 29 (18.5%) 88 (56.1%) 18 (11.5%) 22 (14%)
PCA (P1) proximal segment of the posterior cerebral artery, SCA superior cerebellar artery, AICA anterior inferior cerebellar artery, VB junction,
vertebro-basilar junction, VA (V4) intradural segment of the vertebral artery, PICA posterior inferior cerebellar artery, PCA (P2-P3) distal segments
of the posterior cerebral artery

eventual intraluminal thromboses. In 98 patients, a hemor- and giant aneurysms. Al-Mefty’s combined petrosal
rhagic onset occurred. The Average admission Hunt-Hess approach [3] was employed for the midbasilar trunk and
score was 2.17 ± 0.8 and the mean Fisher grade was proximal anterior inferior cerebella artery (AICA). The Far-
1.9 ± 0.8. One hundred thirty-seven aneurysms were clas- lateral retrocondylar approach was the corridor of choice
sified as proximal and 20 as distal. Table 1 reports the for aneurysms involving VB junction, VA, and the proximal
prevalence of proximal and distal posterior circulation PICA, although the transcondylar variant was rarely neces-
aneurysms according to site and size (Table 1). About rup- sary. Regarding the distal localizations, a subtemporal
tured aneurysms—apart from rare cases of young patients trans-tentorial approach was commonly used to treat P2-P3
having an impending life hematoma, for whom the indica- PCA aneurysms. Conversely, aneurysms involving the dis-
tion for surgery was based mainly upon an evidence-­based tal segments of AICA, SCA, and PICA were elegantly
management algorithm about intracerebral hemorrhages treated by a retrosigmoid route.
reported by our group [2]—mainly patients with an admis-
sion Hunt-Hess score of 1–3 underwent surgery. In 92% of  irect vs. Indirect Treatment
D
cases, an early surgery (within 24 h) was performed. One In all but three aneurysms a direct treatment was possible. A
hundred fifty-seven aneurysms were consecutively oper- total of 128 aneurysms were successfully clipped. Trapping
ated on; six patients had two aneurysms and one patient was the solution to aneurysms that were not amenable for
harbored three different aneurysms. In three cases, two dif- clipping, under two conditions: if the patient tolerated the
ferent procedures were performed on the same patient. A BTO, and the aneurysms were far distal having no need for
total of 152 procedures were performed. revascularization. In one elective case of complex giant pos-
terior projecting basilar tip aneurysm, an extracranial to intra-
Copyright © 2021. Springer International Publishing AG. All rights reserved.

cranial (EC-IC) occipital artery (OA)—right P3 PCA bypass,


Surgery with a radial artery graft, was performed. In two other elective
patients, an intracranial to intracranial (IC-IC) PICA-PICA in
Approach Selection situ bypass was carried out preceding, in both cases, the trap-
Approaches were selected according to site and angioarchi- ping of a complex VB junction aneurysm. Table 2 reports the
tecture. Pterional and cranio-orbitary approaches were uti- types of treatment and the surgical techniques comprehen-
lized to basilar tip, proximal (P1) PCA, and superior sively employed in the current series (Table 2).
cerebellar artery (SCA). For these aneurysms, pterional
approach was usually “extended” to comprehend wide  emporary Clipping and Neurophysiological
T
drilling of the lesser sphenoid wing, a large opening of the Monitoring
sylvian fissure, an extradural or intradural anterior clinoid- In the present series, the anesthesia protocol used by our
ectomy, and an intradural posterior clinoidectomy. Cranio- group was specifically designed to allow the intraoperative
orbitary corridors were preferentially employed in large neurophysiological monitoring during neurovascular surgery

Trends in Cerebrovascular Surgery and Interventions, edited by Giuseppe Esposito, et al., Springer International Publishing AG, 2021. ProQuest Ebook Central,
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Music Has Grown Up
CHAPTER XVIII
Bach—The Giant

Bach and Handel rescued the Germans from the reputation of being
musical barbarians, for Germany had not had a Lully or a Palestrina!
But just in time, Bach and Handel entered and Bach carried
composition to maturity and religious musical art to its highest
point, while Handel was one of the foremost opera and oratorio
composers of his day.
And indeed not until Mozart’s day did the Italians think that
Germany was anything but barbarous, not in fact until they were
outranked in Italian Opera by a German.
Of all the unassuming men of genius Johann Sebastian Bach
(1685–1750) is the most lovable. Never did he seem to realize that he
was doing anything, but the will of God, never did he seem to care
what people thought of his work, but went on composing, supporting
twenty children, often with so little money that he tutored and played
at funerals to eke out a living. In his life there was little glitter. Bach
was a saint, if there was ever a saint. Although some few admired
Bach during his lifetime, it was not until one hundred years after his
death that his works were known and that he received the fame he
deserved.
The Bach family for six generations were musicians, beginning
with his grandfather “to the 5th power,” Veit Bach, a Thuringian
baker in the 16th century whose pleasure “was to use a small zither,
which he took with him to play, while the mill was moving.” All his
descendants became musicians down to and beyond Johann
Sebastian.
The Bachs were great family lovers and every year they held
reunions, at which all of the different members living in various parts
of Germany, met together and enjoyed a jolly time singing and
playing.
Sebastian was born in 1685 in Eisenach, the town where Martin
Luther wrote his stirring chorales. His father Ambrosius began very
early to teach him music, the family profession, and Sebastian
started with the violin.
But the poor little boy lost both father and mother when only ten
years of age, and he was left to be brought up by his elder brother,
Johann Christopher. Sebastian was passionately fond of music and
although Christopher taught him to play the clavier, nevertheless this
sad little tale is told:
Sebastian had seen Christopher with a book of music including
pieces by Froberger, Pachelbel, Buxtehude, and others. Sebastian
was very anxious to get it and play bits from it. Christopher forbade
him to touch it and put it away in a cupboard, which fortunately had
a lattice door, for Sebastian, every night during the full moon,
(because he did not dare to use a candle), copied the book note for
note. When Christopher discovered this, the little lad was soundly
scolded and was witness to Christopher’s burning it before his poor
eyes!
It did not seem to daunt him, for from this time on, he copied the
great works whenever he could.
It became necessary for Sebastian to earn money to save
Christopher’s purse, and in 1700 he became a choir boy at St.
Michael’s in Lüneburg, where he received lessons without paying for
them. He was happy here, with a library where he could copy music
to his heart’s content, and every vacation he went on foot to
Hamburg to learn of the great organist, Reinken. He visited too the
court of Celle where he heard Couperin’s music, which no doubt
helped to develop his style.
Soon he left Lüneburg and went to Saxe-Weimar where he entered
the orchestra of Prince Johann Ernst. But his interest was in the
church and when he was eighteen he tried for the post of organist in
the Church at Arnstadt. He played so delightfully, despite his youth,
that he was accepted at the first hearing!
He composed many works here and learned much about the organ,
that was to be valuable to him and to us. He was well liked, too, and
his playing was enjoyed. Nevertheless, his interest in others was so
great, that he decided to go to see Buxtehude in Lübeck, and he was
so interested in the master’s art that he forgot about his church in
Arnstadt and stayed four months instead of one! When he returned
he was severely reprimanded. Later, he received a second reprimand
which is of tremendous interest for he was accused of “interspersing
the chorale with many strange variations and tones, to the confusion
of the congregation.” He was charged with the crime of being
original!
Due to this lack of sympathy, he accepted a post as organist at
Mühlhausen in 1707 and later in the year married his cousin, Maria
Barbara, with great rejoicings. They had seven children, two of whom
were the famous Wilhelm Friedemann and Karl Philip Emanuel.
The next year he became Concertmaster (first violinist), to the
Duke of Weimar and remained there until 1718. This was a very
fruitful composing period, for he had no money worries. He studied
the Italian masters, especially Vivaldi, and wrote some excellent
cantatas. However, he went soon to the Prince of Anhalt-Cothen, as
Court Choir Master.
He made concert trips from here to Dresden and Leipsic, and it
was in Dresden that he challenged the proud Marchand, the French
organist, to a public improvisation contest on a theme, new to both
of them. But the contest never took place, because, unknown to Bach,
Marchand heard him play and when the time for the contest came,
Marchand had left town hurriedly in an early post-chaise. And
strange as it may seem, Emperor Frederick I gave Marchand one
hundred ducats and Bach got nothing!
Bach’s new patron was a fine man and a Protestant and gave Bach
every chance. At Weimar, he had become well known for his religious
works and beautiful playing. But, as he had no organ, he wrote music
for harpsichord, violin, chamber music and the orchestra, which was
far from “grown up.” Here, too, he wrote the Brandenburg Concertos
and the first part of his epoch-making work The Well-tempered
Clavichord (48 Preludes and Fugues, 1722) which he finished in
1744. It is still the greatest work of its kind. In it he reaches the
highest point of contrapuntal writing.
In 1720, while Bach was traveling with the Prince, his wife died.
After a year and a half he married a charming singer, Anna
Magdalena Wulkens, one of his pupils. They had twelve children and
lived very happily. The lovely little tunes that he wrote for Anna
Magdalena and his children have come down to us and many of us
have played them in the first years of our music study. Isn’t it
wonderful to think that the great Bach, who wrote some of the
masterpieces of the world, could also write simple little Minuets and
Preludes that any child can play?
But with all Bach’s comfort he missed an organ! Deep in his soul,
he craved the making of religious music—it was part of his thinking.
His religious ideas tied up with his music, were his life. So we see this
saint leaving happiness at Cothen for an ill-paid post in Leipsic, as
Cantor (1723) at the school of St. Thomas, where, succeeding Johann
Kuhnau, he stayed the rest of his life and wrote his greatest works.
Bach wrote to a friend that he thought a long while before leaving
his “gracious, music loving and discriminating Prince ... but it
happened that my master married a ... princess who ... weaned my
master from the loving interest he had ... toward our glorious art.
And so God arranged that the post of Cantor at St. Thomas’ should
fall vacant.... I took three months to consider the future and was
induced to accept, as my sons were studious and I was desirous ... of
gratifying their bent by entering them in the school ... and thus, in
the name of the Most High, I ventured and came to Leipsic.”
Note, dear reader, the nobility, spirituality and sweetness here,
thinking of his children and not of his career!
He struggled against the unsympathetic town council, the school,
and lack of money. He wrote to his friend Erdman, “My present
income averages $700. When funerals are numerous I make more,
but if the ‘air is healthy’ then my income falls. During the past year I
have earned $100 less, owing to the small number of deaths.”
In 1732 he wrote one of his few attempts at comedy.—the Coffee
Cantata set to music on a text by Picander. Leipsic had become a
slave to the new luxury, coffee, and in this Picander found material
for a satire.
Besides his regular work, he had to teach dull, undisciplined
pupils, attend to services in four churches, and be satisfied with the
few singers and players he found for the performances he directed.
Yet, fed with the spirit of love that was within him, he was happy
and his home was a center of joy. He never became too sad until he
lost his sight three years before his death. Even then he dictated his
compositions and conquered discouragement!
Bach’s life was made happier when Philip Emanuel became Court
musician and clavier player to Frederick the Great, and he talked so
much of his father that Bach was invited to Potsdam.
When Frederick the Great, who was playing the flute in his
orchestra, heard that Bach was in Potsdam, he put down his flute
and interrupted the concert saying, “Gentlemen, old Bach has
arrived.” Bach appeared in his traveling clothes and was invited to
improvise a fugue in six parts, which he did to the great admiration
of all.
Yet many felt that his writings were lacking in charm! This was no
doubt because people were getting accustomed to the Italian
melodies which had become popular in Germany. Furthermore,
when he wrote “The Art of Fugue” his son could sell but thirty copies
and finally sold the plates for the mere cost of the metal! Students
are grateful that copies of this work were saved, for it is still the
greatest authority on fugue writing.
In 1749, Bach underwent an operation on his eyes but lost his sight
and in 1750 died of apoplexy. So little was he appreciated that his
grave was destroyed in the renovation of the Johanneskirche
grounds. His supposed remains were discovered in 1894 and re-
interred one hundred and forty-four years after his death. But—what
remains of Bach, no known or unknown grave can bury.
A quarter of a century after Bach’s death, Mozart said, on hearing a
Bach Cantata, “At last I have heard something new and have learned
something.” Then later Mendelssohn re-discovered him, and
Schubert, too, helped to bring him to the world’s notice. And not
until 1850, a century after his death, was the Bach Society formed to
honor Bach, the corner-stone of modern music.
Bach was a stalwart man with fine deep eyes, broad forehead and a
grave face, lit with kindly humor. He had dignity and calm, was
always courteous, and criticised only his pupils whom he wanted to
help. When asked one time, how he played so well, he remarked, “I
always have had to work hard.” He could stand no one who was
pretentious and conceited. He wanted his rights but never boasted.
One year besides fulfilling his other duties he wrote a cantata every
Sunday! He wrote them as a preacher writes sermons. They had to be
done and he never neglected his duty.
Bach was a devoted father and husband and his home was one of
the happiest of any great genius. Many of his children were musical
and he said that he had an orchestra in his own home!
Even his little half-witted son had genius and during the last years
of Bach’s life when the dear old man had become blind, the little boy
sat at the clavier, Bach’s favorite instrument, and improvised to the
joy of his father.
Bach’s Works

It is impossible to describe in words just what Bach accomplished,


so surpassing in beauty are his best works.
He brought the art of polyphonic writing to its highest and most
sublime point. His value to the student cannot be exaggerated, for he
is the musical Bible to all who would be musicians.
The organ was the core of his musical thinking and it is in the
things which center about the organ that his art is loftiest.
Although he was most ingenious in writing counterpoint, he was
never dry and tricky as were other writers. His subjects were always
original and his melodic line always of rare beauty.
His works are most varied: fugues, motets, cantatas, passions,
oratorios, concertos, sonatas and suites. He was a radical in his day,
for he threw over conventional notions of harmony as to proper keys
and insisted upon a new system of tuning the clavier, so as to use the
whole range of tones. The “Well-tempered Clavichord,” two groups of
24 Preludes and Fugues in 24 keys, was the outcome of this. It was so
called because it was written to show the possibilities of a clavier (or
clavichord) tuned according to an idea of his, enabling one to play in
all keys. This was one of the greatest discoveries in the whole story of
music, for it made possible all the music which has followed. The
keyboard was divided into equal half-steps. This made twelve half-
steps within each octave and thus all the intervals became fixed, and
modulation from key to key was possible. Heretofore, if one went
from one key to another, the instrument sounded out of tune, but
now instruments were tuned, as we glibly say, “to scale.”
He invented a new fingering in which the thumb and little finger
were used for the first time. We wonder why the thumb had been
snubbed!
The pianoforte was just coming into prominence in Bach’s day but
he preferred the clavier, on which he felt he could play with more
expression.
He developed the fugue to its highest point. A fugue is an enlarged
canon in which the fragments of theme or melody are taken up and
answered by two, or more, voices. One voice declares the subject and
the answer is repeated usually in the dominant key a fifth above,
while the first voice gives the counter-subject. There are various
kinds of fugues, depending on their construction. After the voices
have all entered, separated sometimes by little passages called
“episodes,” a section in which the subject is freely developed comes,
and then the stretto, in which all the parts enter racing and
overlapping, building up to a climax; then follows the cadence or
ending.
To write a noble or lofty fugue, neither dry nor pedantic, takes art
to the nth power! Bach had the art that touched Heaven’s borders! In
truth you can safely divide fugues into two classes—Bach’s and all
others!
None of Bach’s works were published until he was forty years old,
and most of them not until long after his death, and many of his
manuscripts were lost and never published at all.
The list of his works is stupendous; the Bach Gesellschaft (Bach
Society, 1850) published them in sixty volumes! Among them were
the 48 Preludes and Fugues (The Well-tempered Clavichord
Collection); 12 Suites; many Inventions in 2 and 3 parts; partitas; 12
concertos for 1, 2, 3 and 4 claviers with orchestra; many sonatas and
concertos for violin, flute, viola da gamba, clavier, and orchestra;
several overtures for orchestras; vocal works; 200 motets and
cantatas; 5 Passions, of which the greatest are the St. Matthew and
the St. John; 5 masses of which his B Minor Mass is a world
masterpiece; oratorios; magnificats; many organ works, and old
German chorales harmonized for voices.
When you can, try to hear Wanda Landowska play Bach
compositions on the harpsichord. It is a glimpse into the beauty of
the saintly Bach.
Also try to hear the great Bach Festival, directed by Frederick
Wolle held yearly in Bethlehem, Pennsylvania, in the Moravian
Church.
In a list of great men, Bach would be classed with Euripides,
Sophocles, Shakespeare, Milton, da Vinci, Michael Angelo and
Goethe.
Bach did not write for people, he wrote for his own soul. He never
seemed able to write theatric music, for his was the drama of the
spirit. Always, his music was the result of his musings, the
confessions of his ideals. So he attained a loftiness, grandeur and
sublimity far removed from even some of the most dramatic writers.
Bach’s Sons

Bach’s sons reached great eminence. The eldest was Wilhelm


Friedemann (1710–1784), an unusually talented man on whom the
father built great hopes. But while Friedemann inherited his father’s
musical talent he did not have his character, and was looked upon as
a disgrace to the family on account of his dissolute ways. He was the
greatest organist of his time and most of his compositions, which
were considered very fine, have been lost to the world, for he did not
take the trouble even to write them down, but played them from
memory.
The third son, Karl Philip Emanuel (1714–1788), although trained
to be a lawyer, could not resist the urge of music, and after going
through two universities decided to become a musician to Frederick
the Great. He was “general manager” of all the music at court until
the Seven Years’ War put an end to his position after almost thirty
years’ service. He then spent the rest of his life in Hamburg. As
composer, conductor, teacher and critic his influence was great. He
was loved and respected by the whole city. In his day he was
regarded as being as important as his father, but we know that he
was not in the same class, although he was the greatest of his
contemporaries. He did not imitate his father’s style but developed
the sonata into the form that Haydn, Mozart and Beethoven
perfected. He was an innovator, not only in form, but in the
treatment of melody and harmony. His best sonatas were written at
the court of Frederick the Great.
In the growth of music he is the link between his immortal father
and Haydn. Haydn was more gifted than he and made the seeds
planted by Philip Emanuel blossom luxuriantly.
Johann Christoph (1732–1795) was an upright, modest, amiable
man, and a splendid musician keeping up the family traditions.
Johann Christian (1735–1782), the youngest of those who outlived
the father, might be called the Italian Bach, because he went to Italy
in 1754, became organist of the Milan Cathedral, and wrote vocal
music in the Neapolitan style. He left his position as organist,
married an Italian prima donna, wrote many operas and spent the
last twenty years of his life in London, as director of concerts.
Curious as it may seem, the great and gifted Bach family died out
in 1845, with a grandson of Johann Sebastian. Out of twenty children
there seems not to have been one to carry the line to the present day.
CHAPTER XIX
Handel and Gluck—Pathmakers

George Frederick Handel—Master of Oratorio


(1685–1759)

In the last chapter we saw Bach rescue music from the danger of
emptiness and frivolity, by perfecting polyphonic music and
dignifying church music as it had not been since Palestrina.
Bach and Handel were alike in that they were both born in
Germany when music, especially opera, had become mechanical and
full of set rules. They were both Lutherans and Thuringians. They
worked about the same time, and tried to encourage the hearts and
minds of their country, torn by the Thirty Years’ War; both were
polyphonic masters; both organists. Bach attached himself to
Frederick the Great, the protector of the faith, and Handel went to
England, where there was liberty of thought; and both, died blind
and of apoplexy.
The differences, with so many similarities, are most interesting.
Bach, modest, retiring, was always a German subject; Handel
became an English subject. Bach was a homebody with twenty
children; Handel was a traveler and never married. Bach wanted
only to satisfy himself; Handel, to satisfy the public. Bach was
humble, Handel arrogant. Bach seldom fought for his rights, while
Handel would dismiss even his masters. Bach cared little for
applause, but Handel could not live without it. Bach was devoted to
the lyric, Handel to the epic. Handel is usually (not always) heroic,
Bach is usually religious (not always, of course). Handel is popular,
easy to understand; Bach is deep, coming from the soul, and it takes
more thought than the crowd is always willing to give to appreciate
this giant.
Handel achieved great worldly success, and treated nobles as
equals. Poor Bach worked contentedly in an humble position and
struggled for money and profited by “bad air.” (See page 248.)
Bach demanded faith and love of art, Handel demanded ready
ears. Bach never intended to make music, he only wanted to express
his devotion in the best medium he had; Handel wanted fame and
riches and the approval of the crowd. Handel died rich and Bach died
poor.
George Frederick Handel (1685–1759) who wrote the immortal
oratorio Messiah, and one of the greatest opera composers of his
time, was born in Halle, Saxony. His father was a barber, but
managed to get the title “Chamberlain to the Prince of Saxe-
Magdeburg.”
Handel’s father wished him to study law, but George Frederick did
not like the idea and besides he showed great musical gifts. One day
when he was a little boy, he found hidden in the attic, a clavichord
upon which he secretly played every chance he had.
Not long after this “find,” something most important happened.
His father was going to Weissenfels to the Duke’s castle and had no
intention of taking George Frederick with him. So, Father Handel
seated himself in the coach, taking things comfortably, when he
spied little George Frederick dashing along by the great wheels. He
paid no attention to him, but after going a mile and realizing that the
little boy was still following, he called out “What do you want?” “I
want to go with you,” answered Handel, and although his father was
quite annoyed, George Frederick’s will, as always, prevailed and he
went with his father! At the court the Duke saw, very quickly, how
gifted the little Handel was. His father relented and on his return to
Halle, George Frederick was given instruction on the organ,
harpsichord and in composition with Zachau, and taught himself the
oboe and violin, greedily mastering all the music he could find.
Although he studied music he seems to have respected his father’s
wishes and studied law and even after his father died in 1697, he
continued, but later gave it up for music. At seventeen he entered the
University, and studied, besides music, the literary classics which
were of great use to him later.
On leaving the University he went to Hamburg, the musical center
of Germany, where he heard Keiser’s works and received good advice
from Johann Mattheson, the composer, tenor and conductor, who
later engaged George Frederick in a duel.
The quarrel came about in this way: Handel was to lead
Mattheson’s opera, Cleopatra, in order to relieve Mattheson, who
sang the part of Antonio. After Antonio was “killed,” Mattheson
being free to lead, entered the orchestra pit to take Handel’s place as
leader. Handel was infuriated. They met later and fought a duel in
which Handel was saved by a large metal button which snapped
Mattheson’s rapier! What a little thing a button is and what it did for
music!
Handel’s first four operas were written here for the Hamburg
stage. But Almira (1705) is the only one ever heard now.
Handel in Italy

Next he visited Florence, Rome and Venice during which time he


had the happiest three years of his life. He composed a cantata, an
oratorio and other works; he learned much of melody and sweet
flowing music, which softened his dry, stiff use of German
counterpoint, and he gathered material for his later London work.
An amusing story is told of him in Venice. There was a carnival
going on and Handel went to it. At one of the costume balls, he sat
down to a harpsichord uninvited and began improvising, thinking
that no one would know him. A gorgeously garbed figure dashed
through the crowd to his side, and almost overcome by the music,
gasped, “This is either the Devil or the Saxon.” (Handel was called
“The dear Saxon”—“Il cáro Sarsone” in Italy.) It was Domenico
Scarlatti’s first meeting with Handel, and forever after they remained
warm friends.
In Vienna he met Steffani (Chapel Master) who persuaded him to
go to Hanover and after a short time, the Elector, who became
George I of England, appointed him Chapel Master and gave him
permission to go to England for a visit before taking up his new
work.
This visit was the turning point in Handel’s career, for later he
became an English subject and he—but we must not get ahead of our
story!
Handel in England

Handel went to England about fifteen years after the death of


Purcell, “The Orpheus of England.” Handel was quick to see Purcell’s
good points and modelled his first English work to celebrate the
Peace of Utrecht, on Purcell’s Te Deum.
After arriving in London he wrote Rinaldo with an Italian libretto
in fourteen days! He was the speed maniac of the 17th and 18th
centuries. His librettist said of him, “Mr. Handel barely allowed me
time to compose my verses.” Later he arranged Rinaldo for
harpsichord and all England played it, especially the lovely aria
Lascia ch’io Piango (Let Me Weep).
Yet Handel doesn’t seem to have made money out of Rinaldo,
which brought the publisher, Walsh, $10,000, about which Handel
said, “My dear fellow, the next time you shall compose the opera and
I will publish it.” (History of Music, by Paul Landormy.)
Later, he became the guest of the Duke of Chandos, at whose
house he wrote at least sixteen compositions.
King George had been very angry with Handel for leaving Hanover
and remaining in England, but forgave him later, and Handel was
made Director of the Royal Academy of Music which the King
founded in 1719. Among Handel’s duties were the getting of the
artists for the operas. This meant much to him and allowed him to
travel all over Europe. He composed operas almost as people wrote
their letters, for in eight years he produced eleven successful operas!
Think of that for work!
Handel and His Rivals

But—he had a rival, Battista Buononcini, protégé of the mighty


Duke of Marlborough, and a musical war raged in London. John
Byrom, a humorist of the day wrote:
Some say, as compared to Buononcini
That Mynheer Handel’s but a ninny
Others aver that he to Handel
Is scarcely fit to hold a candle.
Strange all this difference should be
’Twixt tweedledum and tweedledee.

Handel won, however, and Buononcini left England. In 1729,


another opera venture was started, an Italian opera society, of which
Handel was made the Director. Off he went to Dresden and brought
back Senesino, a tenor, and other famous singers. But Handel did
not get along well with his singers and subordinates. He was too
high-handed and because of his quarrels the opera was given up! On
one occasion he dragged the singer, Cuzzoni, to the window and
threatened to throw her out if she did not sing the way he wished.
Various other reasons were given too,—one, the dispute between
Cuzzoni, who was called the “Golden Lyre” and another soprano,
Faustina, the wife of Hasse, a rival conductor. Colley Cibber, a critic
of the time said: “These costly canary birds contaminate the whole
music loving public with their virulent bickerings. Cæsar and
Pompey did not excite the Romans to more violent partisanship than
these contentious women.”
And now we see Handel bankrupt and superseded in another
theatre by his two rivals, Porpora and then Hasse (1699–1783) of
Hamburg. However, they too were unsuccessful.
On went Handel, writing operas and oratorios and conducting at
special functions. His health snapped, but his will was so powerful
that this forceful man recovered, and presented two more operas,
which were not successful. In spite of all his failures and lack of tact,
he had faithful friends who arranged a successful benefit concert in
1738 for him. At about the same time a statue was erected in
Vauxhall Gardens, an honor never before paid to a living composer!
He composed, while writing for the stage all these years, twelve
sonatas for violin or flute with figured bass, thirteen sonatas for two
violins, oboes or flutes and bass, six concerti grossi, twenty organ
concertos and twelve concertos for strings, many suites, fantasies
and fugues for harpsichord and organ. It is difficult to understand
how one brain could do all this!
Handel Forsakes Opera

After his ill success with the Italian Opera House, he gave up
writing operas and devoted himself to oratorios. In thirteen years
(1739–1752) he wrote nineteen. Among these are Saul in which is the
famous “Dead March,” Joseph, and many other important ones, but
towering over all The Messiah, and Heracles, which Romain Roland
says is “one of the artistic summits of the 18th century.”
They are not all oratorios, for Heracles and several others are not
religious in subject, but are dramatic epics.
Handel’s sight failed him, but even this did not stop his torrential
activity to his death in 1759.
He had become an English subject, so was buried with pomp at
Westminster Abbey.
He was loved even though he was fiery of temper, and had a will
that no one could conquer.
His music is full of his gusts of feeling but always correct and his
art perfect. In his work he always held himself under great control
and it mirrors his power and balance. He loved wind instruments
and people often considered his music noisy!
He wrote forty-two operas, two passions, ninety-four cantatas, ten
pasticcios, serenatas, songs and the instrumental works mentioned
above. The famous Handel Largo comes from one of his operas,
Xerxes, and was an aria Ombra mai fu (Never was there a Shadow).
Handel used counterpoint, but always knew when to unbend and
use delightful flowing melody, so he became popular.
Other men, Hasse, Telemann and Graun, contemporaries of
Handel, followed the popular Italian models but without Handel’s
genius for melody and sublimity, and were never heard of after their
own generation had passed away.
Handel’s Messiah, which he wrote in twenty-four days, was first
given in Dublin. It took the people by storm and when the king heard
it, thrilled by the “Hallelujah Chorus,” he rose to his feet, and since
then it is the custom to stand during that number. It has become the
Christmas Oratorio and is sung in churches and societies all over the
world. It has lost none of its first popularity among the people and is
loved as few works have ever been. It thrills because it is sincere, big,

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