Saccular Middle Cerebral Artery Aneurysms

Transcription

From the Department of Neurosurgery
Helsinki University Central Hospital
University of Helsinki
Helsinki, Finland
Saccular Middle Cerebral Artery
Aneurysms:
State-of-the-Art Classification and Microsurgery
Ahmed Elsharkawy
Academic Dissertation
To be presented with the permission
of the Faculty of Medicine of the University of Helsinki
for public discussion in Lecture Hall 1 of Töölö Hospital
on May 30th, 2014, at 12:00 pm
Helsinki, 2014
Supervised by:
Associate Professor Mika Niemelä, M.D., Ph.D.
Department of Neurosurgery
Helsinki, Finland
Associate Professor Martin Lehečka, M.D., Ph.D.
Helsinki, Finland
Reviewed by:
Associate Professor Ville Vuorinen, M.D., Ph.D.
Turku University Hospital
Turku, Finland
Associate Professor Arto Haapanen, M.D., Ph.D.
Department of Radiology
University of Turku
Turku, Finland
To be discussed with:
Professor Uğur Türe, M.D.
Professor and Chairman
Yeditepe University School of Medicine
Istanbul, Turkey
Custos:
Professor Juha Hernesniemi, M.D., Ph.D.
Professor and Chairman
Helsinki, Finland
ISBN 978-952-10-9915-1 (paperback)
ISBN 978-952-10-9916-8 (PDF)
Helsinki University Print
Helsinki 2014
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For my family
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Author’s contact information:
Ahmed Elsharkawy
Faculty of Medicine
Tanta University
El-Bahr street, Tanta
Egypt
Mobile: +20 122 371 7100
email: [email protected]
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TABLE OF CONTENTS
Table of contents
Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
Abbreviations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
List of original publications. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
2. Review of literature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
2.1. Intracranial aneurysms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
2.1.1 Epidemiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .18
2.1.2. Pathobiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .18
2.1.2.1. Formation of intracranial aneurysms . . . . . . . . . . . . . . . . . .18
2.1.2.2. Genetics of intracranial aneurysms. . . . . . . . . . . . . . . . . . . .18
2.1.2.3. Histology of intracranial aneurysms . . . . . . . . . . . . . . . . . . .18
2.1.2.4. Morphology of intracranial aneurysms . . . . . . . . . . . . . . . . .19
2.1.3. Rupture of intracranial aneurysms . . . . . . . . . . . . . . . . . . . . . . . . . . .19
2.1.3.1. Risk factors for the rupture of intracranial aneurysms . . . . . . .19
2.1.3.1.1. Aneurysm-related risk factors . . . . . . . . . . . . . . . . . . . 19
2.1.3.1.1.1. Aneurysm size . . . . . . . . . . . . . . . . . . . . . . . . . . . . .19
2.1.3.1.1.2. Aneurysm morphology . . . . . . . . . . . . . . . . . . . . . . .19
2.1.3.1.1.3. Aneurysm location . . . . . . . . . . . . . . . . . . . . . . . . 20
2.1.3.1.2. Patient-related risk factors . . . . . . . . . . . . . . . . . . . . 20
2.1.3.1.2.1. Gender. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
2.1.3.1.2.2. Age. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
2.1.3.1.2.3. Medical status and living habits . . . . . . . . . . . . . . . . 20
2.1.3.2. Mechanism of rupture of intracranial aneurysms . . . . . . . . . .20
2.1.4. Subarachnoid hemorrhage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
2.1.4.1. Diagnosis of aneurysmal SAH. . . . . . . . . . . . . . . . . . . . . . . .21
2.1.4.2. Grading systems for SAH. . . . . . . . . . . . . . . . . . . . . . . . . . .21
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TABLE OF CONTENTS
2.1.4.3. Complications of aneurysmal SAH . . . . . . . . . . . . . . . . . . . .21
2.1.4.4. Management of aneurysmal SAH . . . . . . . . . . . . . . . . . . . . .21
2.1.4.5. Outcome after aneurysmal SAH . . . . . . . . . . . . . . . . . . . . . .22
2.1.5. Intracerebral hematoma from aneurysm rupture . . . . . . . . . . . . . . . . 22
2.1.5.1. Incidence of intracerebral hematoma after the rupture of IAs . .22
2.1.5.2. Management of ruptured IAs with ICH. . . . . . . . . . . . . . . . . .22
2.1.5.3. Outcome of ruptured IAs with ICH. . . . . . . . . . . . . . . . . . . . .23
2.1.6. Imaging of intracranial aneurysms . . . . . . . . . . . . . . . . . . . . . . . . . .23
2.1.6.1. Historical aspects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .23
2.1.6.2. Digital subtraction angiography . . . . . . . . . . . . . . . . . . . . .23
2.1.6.3. CT angiography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .23
2.1.6.4. MR angiography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .24
2.1.7. Treatment of intracranial aneurysms . . . . . . . . . . . . . . . . . . . . . . . . .24
2.1.7.1. Historical aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .24
2.1.7.2. Microsurgery. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .25
2.1.7.3. Endovascular treatment . . . . . . . . . . . . . . . . . . . . . . . . . . .25
2.2. Anatomy for MCA aneurysm microsurgery . . . . . . . . . . . . . . . . . . . . . 25
2.2.1. The middle cerebral artery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .25
2.2.1.1. Development of the middle cerebral artery. . . . . . . . . . . . . . .25
2.2.1.2. Segmental anatomy of the middle cerebral artery. . . . . . . . . .26
2.2.1.3. Cortical area of supply . . . . . . . . . . . . . . . . . . . . . . . . . . . .26
2.2.1.4. Branching pattern of the M1 segment . . . . . . . . . . . . . . . . . .26
2.2.1.5. Perforating branches . . . . . . . . . . . . . . . . . . . . . . . . . . . . .26
2.2.1.6. Early cortical branches . . . . . . . . . . . . . . . . . . . . . . . . . . . .27
2.2.1.7. Anomalies of the middle cerebral artery. . . . . . . . . . . . . . . . .27
2.2.2. The sylvian fissure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .27
2.2.2.1. Sylvian veins. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .28
2.2.2.1.1 Superficial sylvian veins. . . . . . . . . . . . . . . . . . . . . . . 28
2.2.2.1.2 Deep sylvian veins . . . . . . . . . . . . . . . . . . . . . . . . . . 28
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TABLE OF CONTENTS
2.2.2.2. Sylvian cistern . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .28
2.2.2.3. Perisylvian cortex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .28
2.2.2.4. Insula . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .28
2.3. Middle cerebral artery aneurysms (MCAAs) . . . . . . . . . . . . . . . . . . . . . 29
2.3.1. Incidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .29
2.3.2. Classification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .29
2.3.3. Clinical symptoms of MCAAs. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30
2.3.3.1. Unruptured MCAAs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .30
2.3.3.2. Ruptured MCAAs. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .30
2.3.4. Morphological features of MCAAs . . . . . . . . . . . . . . . . . . . . . . . . . . 30
2.3.5. Special subgroups of MCAAs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30
2.3.5.1. Giant MCAAs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .30
2.3.5.2. Fusiform MCAAs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .30
2.3.6. Treatment of MCAAs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .31
2.3.6.1. Historical aspects and background . . . . . . . . . . . . . . . . . . . .31
2.3.6.2. Microsurgical treatment. . . . . . . . . . . . . . . . . . . . . . . . . . .32
2.3.6.2.1. Microsurgical clipping . . . . . . . . . . . . . . . . . . . . . . . 32
2.3.6.2.1.1. Clipping of proximal MCAAs . . . . . . . . . . . . . . . . . . .32
2.3.6.2.1.2. Clipping of MCA bifurcation aneurysms . . . . . . . . . . .32
2.3.6.2.1.3. Clipping of distal MCAAs . . . . . . . . . . . . . . . . . . . . .33
2.3.6.2.2. Adjuncts to the surgical clipping of MCAAs . . . . . . . . . 33
2.3.6.2.2.1. Bypass surgery for complex MCAAs . . . . . . . . . . . . . .33
2.3.6.2.3. Evolution of surgical approaches to MCAAs . . . . . . . . . 33
2.3.6.2.3.1. Proximal control during MCAA surgery . . . . . . . . . . . 34
2.3.6.2.3.2. Classic surgical approaches for MCAAs. . . . . . . . . . . .35
2.3.6.2.3.3. Focused sylvian opening for MCAAs. . . . . . . . . . . . . .35
2.3.6.2.3.4. Contralateral approach for MCAAs . . . . . . . . . . . . . 36
2.3.6.3. Endovascular treatment . . . . . . . . . . . . . . . . . . . . . . . . . . .36
2.3.7. Outcome after treatment of MCAAs . . . . . . . . . . . . . . . . . . . . . . . . . 36
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TABLE OF CONTENTS
2.3.7.1. Angiographic outcome . . . . . . . . . . . . . . . . . . . . . . . . . . . .36
2.3.7.2. Clinical outcome . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .36
3. Aims of the study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38
4. Patients, materials and methods . . . . . . . . . . . . . . . . . . . . . . . . 39
4.1. Publication I . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 39
4.1.1. Images. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .39
4.1.2. Localization of the main MCA bifurcation . . . . . . . . . . . . . . . . . . . . . .39
4.1.3. Assigning MCAAs into subgroups . . . . . . . . . . . . . . . . . . . . . . . . . . 40
4.2. Publication II . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42
4.2.1. Images . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .42
4.2.2. Patients and aneurysms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .43
4.2.3. Morphological analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44
4.2.4. Topographical analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44
4.2.5. Statistical analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .45
4.3. Publication III . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
4.3.1. Surgical planning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .47
4.3.1.1. Importance and tools . . . . . . . . . . . . . . . . . . . . . . . . . . . . .47
4.3.1.2. Aneurysm localization . . . . . . . . . . . . . . . . . . . . . . . . . . . .47
4.3.1.3. Choosing the approach angle . . . . . . . . . . . . . . . . . . . . . . .47
4.3.2. Surgical technique . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48
4.3.2.1. Positioning and craniotomy . . . . . . . . . . . . . . . . . . . . . . . 48
4.3.2.2. Opening of the sylvian fissure . . . . . . . . . . . . . . . . . . . . . . .52
4.3.2.3. Clipping of the MCAA. . . . . . . . . . . . . . . . . . . . . . . . . . . . .52
4.3.2.4. Confirming the adequacy of clipping . . . . . . . . . . . . . . . . . .53
4.3.2.5. Closing the sylvian fissure . . . . . . . . . . . . . . . . . . . . . . . . . .53
5. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54
5.1. Distribution of MCA aneurysms (Publication I) . . . . . . . . . . . . . . . . . . . 54
5.2. Types of M1As (Publication I) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
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TABLE OF CONTENTS
5.3. Distance from ICA bifurcation (Publication II). . . . . . . . . . . . . . . . . . . . 55
5.4. Aneurysm dome projection (Publication II) . . . . . . . . . . . . . . . . . . . . . 55
5.5. Aneurysm wall (Publication II) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55
5.6. Aneurysm size (Publication II) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56
5.6.1. Dome size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .56
5.6.2. Neck size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .56
5.7. Morphological indices (Publication II). . . . . . . . . . . . . . . . . . . . . . . . . 57
5.7.1. Aneurysm height–width ratio vs. aneurysm size . . . . . . . . . . . . . . . . . 58
5.8. Trends in the rupture of MCAAs (Publication II) . . . . . . . . . . . . . . . . . . 58
5.8.1 Morphological trends . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58
5.8.2. Topographical trends. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .59
5.8.3. Independent risk factors for rupture . . . . . . . . . . . . . . . . . . . . . . . . . 60
5.9. Focused opening of the sylvian fissure for the management of MCAAs (Publication III) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
6. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
6.1. The main MCA bifurcation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63
6.1.1. “False” MCA bifurcation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .63
6.1.2. Angiographic identification of the main MCA bifurcation . . . . . . . . . . . 64
6.2. Four-group classification of MCAAs. . . . . . . . . . . . . . . . . . . . . . . . . . 64
6.3. Distribution of MCAAs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64
6.4. Morphological parameters of MCAAs . . . . . . . . . . . . . . . . . . . . . . . . 65
6.4.1. Aneurysm wall regularity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .65
6.4.2. The aspect ratio (AR) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .65
6.4.3. Bottleneck factor (BNF) and height–width ratio . . . . . . . . . . . . . . . . . 66
6.4.4. The neck size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66
6.4.5. Aneurysm size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66
6.5. Distribution of ruptured MCAAs . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
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TABLE OF CONTENTS
6.6. Focused opening of the sylvian fissure for the microsurgical management of
MCAAs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
6.6.1. Requirements for the focused sylvian opening . . . . . . . . . . . . . . . . . . .67
6.6.1.1. Accurate placement of the sylvian opening. . . . . . . . . . . . . . .67
6.6.1.2. Slack brain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68
6.6.1.3. High magnification (9x or more). . . . . . . . . . . . . . . . . . . . . 68
6.6.1.4. Understanding intraoperative anatomy . . . . . . . . . . . . . . . 68
6.6.2. Troubleshooting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68
6.6.2.1. Premature rupture of the MCAA . . . . . . . . . . . . . . . . . . . . . 68
6.6.2.2. Clips may get entangled in the small field . . . . . . . . . . . . . . .69
6.6.2.3. Confirming the aneurysm clipping . . . . . . . . . . . . . . . . . . . .69
6.6.2.4. Anatomical orientation may be lost in the narrow field . . . . . .69
6.6.2.5. Large ICH and/or massive SAH. . . . . . . . . . . . . . . . . . . . . . .69
6.6.2.6. Large/giant aneurysms needing vascular bypass . . . . . . . . . .70
6.6.3. Advantages of the focused sylvian opening . . . . . . . . . . . . . . . . . . . . .70
6.7. Limitations of the studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70
6.8. The present state of the management of IAs . . . . . . . . . . . . . . . . . . . . 70
6.9. Future trends . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71
7. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
List of supplementary videos of the focused sylvian opening for the microsurgical management of MCAAs . . . . . . . . . . . . . . . . . . . . . . . . . 74
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
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ABSTRACT
Abstract
Background and objectives
The middle cerebral artery (MCA) is the
most frequent location of unruptured intracranial aneurysms (IAs). The rupture of
IAs causes subarachnoid hemorrhaging
(SAH) with high rates of morbidity and
mortality. However, controversy remains
regarding which unruptured MCA aneurysms should be prophylactically treated
since treatment is not without risks. More
insight when deciding upon the management of MCA aneurysms and less risky
treatment options are still needed. Nevertheless, MCA aneurysms are typically
classified according to their location in
relation to the main MCA bifurcation despite the inconsistent and subjective nature of identifying this main branching
point. This study aimed to objectively
characterize the main MCA bifurcation as
a key factor for the more accurate classification of MCA aneurysms (publication I),
to statistically identify the topographical
and morphological characteristics of MCA
aneurysms which could predict an increased risk of rupture (publication II) and
to technically minimize the invasiveness
of the microsurgical treatment of MCA aneurysms (publication III).
Methods
Computerized tomography angiography (CTA) data from 1,009 consecutive
patients with 1,309 MCA aneurysms constituted the basis of this study. The angiographic definition of the MCA main
bifurcation (Mbif) as the starting point of
the insular trunks (M2s) was the basis of
its objective characterization (publication
I). The morphological and topographical
characteristics of MCA aneurysms were
examined and compared to the aneurysm
rupture status; then, univariate and multivariate logistic regression analysis were
performed to determine the independent
risk factors for rupture (publication II).
Moreover, based on the surgical experience of Professor Juha Hernesniemi, we
presented the basic principles and techniques for safely clipping MCA aneurysms
through a 10–15-mm focused opening of
the sylvian fissure (publication III).
Results
The 1,309 MCA aneurysms were classified after objectively determining the
Mbif, which was the most common location for MCA aneurysms harboring 829
(63%) aneurysms. The 406 proximal middle cerebral artery (M1) aneurysms comprised 242 (60%) aneurysms at the origin
of the early cortical branches (M1–ECBAs)
and 164 (40%) aneurysms at the origin of
the lenticulostriate arteries (M1–LSAAs).
There were only 74 (6%) aneurysms distal
to the Mbif.
At the time of presentation, more than
two-thirds of the MCA aneurysms (69%)
were unruptured and 31% were ruptured.
Most unruptured MCA aneurysms had a
size < 7 mm (78%), a smooth wall (80%),
a height–width ratio = 1 (47%) and were
located at the main bifurcation (57%).
Ruptured MCA aneurysms were primarily sized 7–14 mm (55%), had an irregular
wall (78%), a height–width ratio > 1 (72%)
and were located at the main bifurcation
(77%). In addition, 38% of MCA bifurcation
aneurysms, 74% of large aneurysms, 64%
of aneurysms with an irregular wall and
49% of aneurysms with a height–width
ratio > 1 were ruptured.
In our experience, the focused sylvian
opening technique for the microsurgical
11
ABSTRACT
management of MCA aneurysms resulted
in shorter operative times and less inadvertent brain and vessel manipulation.
Thus, it proved to be safe and effective for
the clipping of both ruptured and unruptured MCA aneurysms.
Conclusions
Image-based analysis of the angioarchitecture of MCA can objectively define the
main MCA bifurcation and helps in classifying MCA aneurysms more accurately.
The analysis of topographical and morphological characteristics of MCA aneurysms is important when deciding upon
their management, where their location
at the main MCA bifurcation, the wall irregularity and a less spherical geometry
equate to an increased risk of rupture.
Thus, the focused opening of the sylvian fissure is a practical, less invasive alternative to the classical wide sylvian opening for the microsurgical management of
most MCA aneurysms.
12
ABBREVIATIONS
Abbreviations
2D
= two-dimensional
3D
= three-dimensional
AccMCA
= Accessory middle cerebral artery
AcomA
= Anterior communicating artery
AR
= Aspect ratio
ASDH
= Acute subdural hemorrhage
AVM
= Arteriovenous malformation
BNF
= Bottleneck factor
CI
= Confidence interval
CSF
= Cerebrospinal fluid
CT
= Computerized tomography
CTA
= Computerized tomography angiography
DCI
= Delayed cerebral ischemia
DMCA
= Duplicated middle cerebral artery
DSA
= Digital subtraction angiography
ECB
= Early cortical branch
EEL
= External elastic lamina
EFB
= Early frontal branch
ETB
= Early temporal branch
IA
= Intracranial aneurysm
ICA
= Internal carotid artery
ICG
= Indocyanine green
ICH
= Intracerebral hematoma
IEL
= Internal elastic lamina
ISAT
= International Subarachnoid Aneurysm Trial Study
ISH
= Intrasylvian hematoma
ISUIA
= International Study of Unruptured Intracranial Aneurysms
13
ABBREVIATIONS
IVH
= Intraventricular hemorrhage
LLSA
= Lateral lenticulostriate artery
LSA
= Lenticulostriate artery
M1
= Proximal middle cerebral artery
M1As
= Proximal middle cerebral artery (M1) aneurysms
M1–ECBA
= M1 segment early cortical branch aneurysm
M1–EFBA
= M1 segment early frontal branch aneurysms
M1–ETBA
= M1 segment early temporal branch aneurysm
M1–LSAA
= M1 segment lenticulostriate artery aneurysm
M2
= Insular trunk
M3
= M3 segment of MCA
M4
= M4 segment of MCA
M5
= M5 segment of MCA
Mbif
= Main middle cerebral artery bifurcation
MbifA
= Main middle cerebral artery bifurcation aneurysm
MCA
= Middle cerebral artery
MCAA
= Middle cerebral artery aneurysm
Mdist
= Distal middle cerebral artery
MdistA
= Distal middle cerebral artery aneurysm
MRA
= Magnetic resonance angiography
MRI
= Magnetic resonance imaging
OR
= Odds ratio
PcomA
= Posterior communicating artery
P
= Probability value
SAH
= Subarachnoid hemorrhage
SD
= Standard deviation
SF
= Sylvian fissure
SMC
= Smooth muscle cells
SPS
= Sphenoparietal sinus
14
ABBREVIATIONS
SSV
= Superficial sylvian vein
STA
= Superficial temporal artery
TH
= Temporal horn
US
= Ultrasonography
15
LIST OF ORIGINAL PUBLICATIONS
List of original publications
This thesis is based on the following publications, referred to in the text by their Roman numerals:
I.
Elsharkawy, A., M. Lehecka, M. Niemela, R. Billon-Grand, H. Lehto, R. Kivisaari
and J. Hernesniemi. “A New, More Accurate Classification of Middle Cerebral
Artery Aneurysms: Computed Tomography Angiographic Study of 1,009 Consecutive Cases with 1,309 Middle Cerebral Artery Aneurysms.” Neurosurgery 73,
no. 1 (2013): 94-102.
II.
Elsharkawy, A., M. Lehecka, M. Niemela, J. Kivelev, R. Billon-Grand, H. Lehto, R.
Kivisaari and J. Hernesniemi. “Anatomic Risk Factors for Middle Cerebral Artery
Aneurysm Rupture: Computed Tomography Angiography Study of 1,009 Consecutive Patients.” Neurosurgery 73, no. 5 (2013): 825-37.
III.
Elsharkawy, A., M. Niemela, M. Lehecka, H. Lehto, B. R. Jahromi, F. Goehre, R.
Kivisaari and J. Hernesniemi. “Focused Opening of the Sylvian Fissure for Microsurgical Management of MCA Aneurysms.” Acta Neurochirurgica 156, no. 1
(2014): 17-25.
The original publications have been reproduced with the permission of the copyright
holders.
16
1. INTRODUCTION
1. Introduction
Intracranial aneurysms (IAs) are focal
dilatations of intracranial arteries, usually
at their branching points. Most IAs remain
asymptomatic and never rupture. When
an IA ruptures, arterial bleeding typically causes a subarachnoid hemorrhage
(SAH). A patient with SAH usually complains of the sudden onset of the worst
headache in his/her life accompanied by
nausea and vomiting if consciousness
was not lost at onset. Risk factors associated with the rupture of IAs include both
aneurysm- as well as patient-related factors. The advancement of neurovascular
imaging techniques have allowed for the
increasing frequency of the discovery of
incidental unruptured IAs. This provides
an opportunity for their treatment before
rupture, although prophylactic treatment
is not without risks. Therefore, the management or treatment decisions should
be made individually after weighing treatment risks against the natural course of
the disease.28, 53, 128, 129, 143, 286
The middle cerebral artery (MCA) harbors around one-third of all IAs. MCA aneurysms (MCAAs) are classically divided
into three groups: proximal middle cerebral artery aneurysms (M1As), main middle cerebral artery bifurcation aneurysms
(MbifAs) or distal middle cerebral artery
aneurysms (MdistAs). Each group has
distinct anatomic features which have an
impact on clinical management. The MCA
is easily accessible by surgery, while its
angioarchitecture is usually troublesome
for endovascular navigation. In addition,
MCA aneurysms are often broad necked
and incorporate branches at the neck,
which challenges endovascular coiling
more than surgical clipping. This favors
clipping as the most adequate treatment
for most MCA aneurysms.34-36, 42, 117, 209, 269,
273, 291
This study is based on computerized tomography angiograghy (CTA) data from
1,009 consecutive patients with 1,309 MCA
aneurysms diagnosed between 2000 and
2009 at the Department of Neurosurgery
at Helsinki University Central Hospital. We
present an angioarchitecture-based technique for distinguishing the main MCA
bifurcation from other branching points
along the MCA as the key to the accurate
classification of MCAAs. We also analyze
topographical and morphological characteristics of MCAAs and relate these characteristics to aneurysm rupture. Moreover, based on the surgical experience of
Professor Juha Hernesniemi, we present
the basic principles and techniques for
the microsurgical management of MCAAs
through a focused opening of the sylvian
fissure. This represents a technical innovation which minimizes brain and vessel manipulation as well as operative time, while
still maintaining accuracy and safety.
17
2. REVIEW OF LITERATURE
2. Review of literature
2.1. Intracranial aneurysms
2.1.1 Epidemiology
Intracranial aneurysms (IAs) are acquired lesions with an incidence of 1–5%
in adults and a lower incidence in the pediatric population. The risk of having IAs
is 2–4 times higher in families with two or
more members with a history of IAs. Most
IAs are sporadic and only less than 10%
of patients have a family history of aneurysms. Around one-third of all patients
with IAs have multiple aneurysms.35, 36, 47,
113, 119, 220, 222, 225, 226, 232, 292
Although the incidence of IAs is similar worldwide, their rupture rates are different. The incidence of aneurysmal SAH
in most populations is 6–10 cases per
100,000 person-years; in Finland, Japan
and northern Sweden, the incidence is
10–16 cases per 100,000 person-years.
This higher incidence may be due to environmental or genetic factors, but still remains unknown.151, 194, 231, 240, 243, 270, 275
2.1.2. Pathobiology
2.1.2.1. Formation of intracranial
aneurysms
Although it is generally accepted that
IAs are acquired lesions, the actual mechanism of their formation is unknown. Possible mechanisms include direct vascular
trauma, infection, hemodynamic stress,
inflammation and/or arterial wall degeneration. Understanding of the mechanisms behind the formation of IAs could
provide an opportunity for the devel-
18
opment of pharmacological therapy for
IAs.12, 27, 63, 66-68, 109, 154, 156, 260
Inflammation has been found to have
a principal role in the process of IA formation and subsequent rupture. Aspirin,
through its anti-inflammatory effects, was
found to be effective in decreasing the
risk of SAH without increasing the risk of
intracerebral hemorrhage. Aspirin might
be a promising prophylactic drug against
IA growth and rupture.22, 23, 74, 96
2.1.2.2. Genetics of intracranial
aneurysms
Many genetic studies have aimed to
determine if some genetic variants predispose individuals to the development
of IAs. Multinational genome-wide association studies13, 295 have defined five loci
with strong statistical evidence and another 14 loci with suggestive evidence of
an association with IAs. 5q26 is one suggestive risk locus for IAs which was also
found to be associated with a risk of high
systolic blood pressure. In addition, 9p21,
which is a general cardiovascular risk locus, was found to be a strong risk locus for
IAs. This overlapping genetic background
suggests that the formation of IAs might
be a part of generalized vasculopathy
rather than a separate disease.70, 71
2.1.2.3. Histology of intracranial
aneurysms
The wall of cerebral arteries is composed of three histologic layers: tunica intima, tunica media and tunica adventitia.
The tunica intima and tunica media are
separated by the internal elastic lamina
(IEL). The wall of cerebral arteries differs
from that of extracranial arteries in that
it lacks the external elastic lamina (EEL)
normally present in extracranial arteries
between the tunica media and the tunica
adventitia. Additionally, cerebral arteries
have fewer smooth muscle cells (SMC) in
the tunica media and in IEL than extracranial arteries. Moreover, at the bifurcation
of cerebral arteries—the typical location
for the formation of IA—the tunica media consists mainly of collagen arranged
in such a way that it increases resistance
to mechanical stress. The walls of IAs lack
elastic laminas.55, 67, 173, 230
In Helsinki, Frösen et al.67 identified four
histological wall types for IAs: type A, an
endothelialized wall with linearly organized SMC; type B, a thickened wall with
disorganized SMC; type C, a hypocellular
wall; and type D, an extremely thin thrombosis-lined hypocellular wall. These types
probably reflect consecutive stages (A
through D) of degeneration suggesting a
dynamic nature to the IA wall. Other factors, such as complement activation and
protein kinases, are involved in IA growth
and rupture.156, 260
2.1.2.4. Morphology of intracranial aneurysms
Morphologically, IAs are classified as either saccular aneurysms when the protrusion is pouch-like or fusiform aneurysms
when the whole arterial segment is dilated without a definite base or neck. Most
IAs (97%) are saccular and arise at arterial
branching sites.34, 36
2.1.3. Rupture of intracranial
aneurysms
2.1.3.1. Risk factors for the rupture of intracranial aneurysms
Most IAs remain clinically silent until
they rupture, causing SAH with a high
morbidity and 30–50% mortality. Several
patient- and aneurysm-specific characteristics have been examined as possible
predisposing factors for the rupture of IAs.
2.1.3.1.1. Aneurysm-related risk factors
2.1.3.1.1.1. Aneurysm size
Although aneurysm size has traditionally been considered a risk factor for the
rupture of IAs, a single threshold value for
an increased rupture risk has not been defined. Many studies have reported a significantly higher risk of rupture for saccular IAs larger than 10 mm than for smaller
aneurysms.2, 288 The largest study on unruptured saccular IA—the International
Study of Unruptured Intracranial Aneurysms (ISUIA)—reported that the rupture
rate for aneurysms smaller than 7 mm was
significantly lower than for those larger
than 7 mm.287 However, in clinical experience, it is obvious that many small aneurysms do rupture. According to the Helsinki Aneurysm Database, which includes
data from more than 9,000 patients, 33%
of all ruptured aneurysms were smaller
than 7 mm in size.
2.1.3.1.1.2. Aneurysm morphology
Some morphological characteristics
of IAs, such as the presence of daughter
sacs and the aspect ratio (the ratio of the
fundus depth to the neck width, AR), have
been found to be associated with the risk
of rupture. Although several hypotheses have been postulated to explain this
association, the underlying mechanism
is still unproven. Histological studies are
still needed to explain the relationship
between the morphological characteristics of IAs and their rupture. In addition,
large-scale clinical studies are needed
to evaluate the predictive value of other
19
morphological variables related to the risk
of rupture.9, 98, 189, 213, 264, 265, 279
tiple IAs and for the rupture of small-sized
IAs.193, 200
2.1.3.1.1.3. Aneurysm location
Smoking and high alcohol consumption
are the principal lifestyle risk factors associated with aneurysmal SAH.53, 130, 133, 146,
220, 231, 280
Moreover, cocaine use has been
found to be significantly associated with
aneurysmal SAH.19
Posterior circulation aneurysms and
aneurysms arising from the posterior
communicating artery (PcomA) have a
higher risk of rupture relative to anterior
circulation aneurysms.220, 287 Among anterior circulation aneurysms, anterior communicating artery (AcomA) aneurysms
have been reported to have the highest
rupture rate132, while, in a large sample
of Finnish patients, MCAAs had the lowest rupture rate. In Finland, close to 50%
of unruptured IAs are located along the
MCA.115
2.1.3.1.2. Patient-related risk factors
2.1.3.1.2.1. Gender
IAs are more frequently diagnosed in
women than in men. Furthermore, aneurysmal SAH is more common in women.220
IAs in women carry a higher risk of rupture especially after menopause, which
is probably related to the effects of estrogen on the vascular wall.38, 93, 150, 167, 185, 220, 244
2.1.3.1.2.2. Age
The annual rupture risk of IAs is 1.1% in
the Finnish population. This risk increases
cumulatively with age to peak between
40–65 years of age.131 In patients with
a family history of SAH, IAs rupture at a
younger age.193
2.1.3.1.2.3. Medical status and living
habits
Hypertension is the most frequently reported health condition associated with
the formation of IAs and their subsequent
rupture.19, 52, 53, 120, 122, 129, 220 Hypertension
was also found to be a risk factor for mul-
20
2.1.3.2. Mechanism of rupture of
intracranial aneurysms
The exact mechanism which causes the
rupture of IAs is still unknown. However, it
is generally accepted that rupture occurs
when the intra-aneurysmal hemodynamic stress surpasses its wall resistance. IAs
increase in size through real growth rather than by stretching which attenuates
the wall.31, 265 Thus, aneurysm size might
depict only the degree of wall growth,
but not its strength. Wall morphology, on
the other hand, correlates more strongly
with the quality of wall growth and its resistance to rupture.
2.1.4. Subarachnoid hemorrhage
SAH is a neurologic emergency resulting from the extravasation of blood into
the subarachnoid space. The rupture of
an IA is the main cause of nontraumatic SAH, accounting for around 80% of all
cases. Aneurysmal SAH is a catastrophic
condition responsible for 2–5% of all new
strokes. The mean age at presentation
is 55 years with an increasing incidence
with age. Women are at a 1.6 times higher
risk for aneurysmal SAH than men. Other
causes for SAH include trauma, arteriovenous malformation (AVM) and Moyamoya
disease. The prognosis for nonaneurysmal
SAH is relatively good.18, 59, 116, 121, 140, 163, 177, 178,
180, 196, 199, 227, 245, 270, 282
2.1.4.1. Diagnosis of aneurysmal prediction of clinical management outcomes.1, 26, 57, 114
SAH
The accurate diagnosis of aneurysmal
SAH is important for the early initiation
of treatment. Clinically, patients typically complain of the sudden onset of the
worst headache in his/her life accompanied by nausea, vomiting, neck pain and/
or photophobia. Physical examination
may reveal stiffness in the neck, retinal
hemorrhage and/or a wide scope of neurological deficits ranging from focal cranial nerve affection (such as third nerve
palsy with PComA aneurysms) to loss of
consciousness with severe SAH or adjoining intracerebral hematoma (ICH). Plain
computerized tomography (CT) of the
head is highly sensitive (95–100%) in the
detection of SAH on the first day. Lumber
puncture is indicated only when a head
CT is negative for SAH, yet the clinical presentation is highly suggestive. In this case,
cerebral angiography will be needed to
fully identify the source of SAH.20, 212, 235
2.1.4.3. Complications of aneurysmal SAH
After rebleeding, the vasospasm of
cerebral vessels is the second leading
cause of mortality in patients surviving
the initial ictus from the rupture of an
IA. Cerebral vasospasm is detected angiographically in up to 70% of all cases of
aneurysmal SAH. Around 30% of patients
with angiographic vasospasm are clinically symptomatic. Clinical symptoms include the sudden or insidious onset of a
decreasing level of consciousness, affected speech and/or motor deficits. Other
neurological complications of aneurysmal
SAH include hydrocephalus and seizures.
Nonneurological complications include
hypernatremia, pulmonary edema, cardiac arrhythmia, myocardial infarction, renal
dysfunction and hepatic dysfunction.89, 94,
95, 103, 139, 241
2.1.4.2. Grading systems for SAH
2.1.4.4. Management of aneurysmal SAH
There are several grading systems for
describing the clinical condition of patients with SAH and for portraying the
radiological features of the extravasated
blood. The most commonly used clinical
grading scales are the Hunt and Hess scale
and the World Federation of Neurological
Surgeons scale. The Fisher grading system—grade 1: no hemorrhage evident;
grade 2: diffuse or vertical layer of SAH <
1-mm thick; grade 3: localized clot and/
or vertical layer of SAH ≥ 1-mm thick; and
grade 4: intracerebral or intraventricular
clot with or without diffuse SAH—is the
standard radiologic scale used to classify
the CT appearance of SAH and any accompanying intraventricular or parenchymal
hemorrhages. Both clinical and radiological grades of patients with SAH help in the
In addition to the prevention of rebleeding, the main goal of treatment for
patients with ruptured IAs is to manage
the complications associated with SAH, in
particular, vasospasm. For vasospasm prophylaxis, oral nimodipine is traditionally
administered and prescribed to patients
for three weeks once aneurysmal SAH is
diagnosed. The use of nimpodipine was
associated with a 40% reduction in poor
outcomes after an aneurysmal SAH. Other drugs, such as magnesium sulphate
and statins, are occasionally used, but
with fewer reported benefits. The use
of triple-H therapy (hypervolemia, hemodilution and hypertension) is more
controversial and is usually reserved for
symptomatic patients. Endovascular me-
21
chanical and/or pharmacological angioplasty are increasingly being used to treat
cerebral vasospasm. Other neurological
and nonneurological complications of
SAH are managed accordingly.33, 41, 43, 46, 54,
78, 290
2.1.4.5. Outcome after aneurysmal SAH
The outcome after the rupture of IAs is
still dismally associated with significant
morbidity and fatality in up to half of all
patients. Around one-third of those who
initially survive the aneurysmal SAH ictus suffer from poor outcomes despite all
available treatment modalities; many of
them die earlier than their peers in longterm follow-up. Delayed cerebral ischemia
(DCI) is the most important cause of morbidity and mortality in these patients. The
treatment modality—in this case, either
surgical clipping or endovascular coiling
of the ruptured aneurysm—does not affect the incidence of the development of
vasospasm or other complications associated with aneurysmal SAH.18, 37, 59, 107, 116, 121,
140, 177, 180, 188, 196, 199, 227, 247, 270, 282
2.1.5. Intracerebral hematoma from aneurysm rupture
2.1.5.1. Incidence of intracerebral
hematoma after the rupture of
IAs
Intracerebral hematoma (ICH) is detected in up to 20% of initial CT scans of
patients with ruptured IAs. The most frequent locations where ruptured IAs are
associated with ICH are the MCA and the
AComA. More than half of all ruptured
MCAAs are associated with ICH and/or intrasylvian hematoma (see Figure 1).3, 136, 201,
259
22
Figure 1.
Axial plane CT of a brain showing a right-side intracerebral hematoma resulting from the rupture of an MCAA.
There is a noticeable effacement of the lateral ventricle on
the right side with a midline shift to the left side.
2.1.5.2. Management of ruptured
IAs with ICH
There is still some controversy regarding the adequate management of patients with a massive ICH caused by the
rupture of an IA. It has been reported that
the surgical evacuation of ICH without the
clipping of the ruptured IA was associated
with a 75% mortality rate, while combining aneurysm obliteration with ICH evacuation resulted in a 29% mortality rate.
Some neurointerventionists advocate for
the coiling of the ruptured aneurysm first
and, then, evacuating the ICH. We advocate for the removal of the ICH and clipping of the aneurysm in the same setting
to avoid time delays with an increased intracranial pressure. In addition, the combination of endovascular and surgical
treatments would expose the patient to
the risks associated with both treatment
modalities.3, 187, 254, 284
2.1.5.3. Outcome of ruptured IAs biplane DSA allowing for the rigorous
visualization of aneurysm’s morphologwith ICH
It can be expected that patients with
both ICH and SAH from ruptured IAs
would present with worse clinical grades
than patients with SAH only. The outcomes for patients with aneurysmal SAH
were found to be worse when the presenting CT scan showed that they were
associated with ICH. In one cooperative
study, it was reported that ICH was present in 90% of patients who died within 72
hours of the aneurysmal SAH ictus.3, 29, 105,
165, 166, 253
2.1.6. Imaging of intracranial
aneurysms
2.1.6.1. Historical aspects
Before cerebral angiography, the diagnosis of an IA could be confirmed only
during surgery or autopsy. Pneumoencephalography (introduced by Dandy in
1919) could also show some large aneurysms causing mass effects. Cerebral angiography was initiated in 1927 after Egas
Moniz revealed the shadows of cerebral
vessels on angiographic films after direct
exposure of the carotid artery. The percutaneous technique of cerebral angiography was thoroughly embedded in practice in 1944 by Engeset.64, 87, 278
2.1.6.2. Digital subtraction angiography
ical features and its relationship to the
surrounding vessels. The new flat-panel
DSA system provides high spatial resolution two- and three-dimensional images,
which enable the accurate visualization of
very small vessels as perforators.61, 99, 126, 153,
298
DSA, being an invasive procedure and
time consuming, has been increasingly
suspended from the primary diagnostics
of IAs since 2000 with the exception of
giant and complex aneurysms or when
endovascular therapy is planned. DSA can
be associated with complications such
as stroke, an allergic reaction to the contrast agent, bleeding from the puncture
site, renal failure and/or aneurysm rupture during the procedure. Moreover, DSA
does not provide clear data about the mural calcification, luminal thrombosis or the
relationship to bony structures at the base
of the skull, which are useful for surgical
planning.61, 92, 137, 229, 277
The use of noninvasive techniques, such
as CTA and magnetic resonance angiography (MRA), for the evaluation of cerebral
vasculatures have enabled the early diagnosis and treatment of ruptured IAs. These
noninvasive techniques are also useful for
the screening of certain groups at higher
risk for IAs. The sensitivity and specificity
of these noninvasive techniques are comparable to the gold standard of DSA.137, 175,
205, 239, 271, 285, 289
Digital subtraction angiography (DSA)
used to be the gold standard for the detection of IAs. Four-vessel angiography is
required in the presence of the possibility
of multiple aneurysms. Vascular anatomy
and aneurysm localization, shape and geometry can be well determined from DSA.
Three-dimensional (3D) rotational angiography is a useful addition to the standard
2.1.6.3. CT angiography
CTA is progressively replacing DSA as
the gold standard for the detection of IAs.
The actual scanning time is less than one
minute making it suitable for investigating
most patients with acute SAH. Mural calcifications, especially at the aneurysm neck,
23
can usually be identified with CTA, which
would affect the clinical management
and planning of treatment. CTA with a 3D
reconstruction of the vessels and bone
is very helpful for anatomical orientation
during the surgical management of IAs.
Unlike MRA, CTA is permissible in patients
with ferromagnetic clips or pacemakers.5,
7, 8, 14, 61, 137, 152, 271, 274
2.1.6.4. MR angiography
MRA with 3D reconstruction allows
for the rapid, detailed and noninvasive
assessment of intracranial vasculatures
without the need for ionizing radiation
or iodinated contrast material. MRA is
preferred for studying patients with renal
insufficiency or hypersensitivity to iodinated contrast materials. For some aneurysms with an immediate relation to the
base of the skull, such as intracavernous or
supraclinoid carotid aneurysms, MRA can
provide better morphological details of
the aneurysm than CTA. MRA is also ideal for noninvasive follow-up in aneurysm
patients after endovascular coiling.61, 152, 229
2.1.7. Treatment of intracranial aneurysms
2.1.7.1. Historical aspects
The first ancient record of an arterial
aneurysm is found in the Ebers papyrus
(2725 BC), where the ancient Egyptian
physician Imhotep tried to treat a bulging
extracranial aneurysm with a fire-glazed
instrument. There was a lapse in history until 117 BC, when Flaenius Rufus, an
Ephesian physician trained in Alexandria,
Egypt, gave the first available description
of the possible etiology of aneurysms
by considering them traumatic in origin.
There was another gap in history until
200 AD, when Galen, the famous Greek
physician, used the term “aneurysm” to
24
describe arterial lesions. For the following 1500 years, Islamic physicians almost
exclusively contributed to any increasing
knowledge of the origin of aneurysm and
their sites. In 1728, Lancisis provided the
modern definition of “aneurysm” as an expansion of a weekend artery.4, 138, 164, 208
According to Fox, the first documented
autopsy report of a ruptured IA dates back
to 1814, when Blackall presented a case of
SAH from a ruptured basilar artery aneurysm. Most autopsy case reports in the
first half of the 1800s comprised only large
or giant IAs since small ones were usually
missed. In 1851, Virchow began to diagnose small aneurysms in different parts of
the body. In 1891, Quincke introduced the
lumbar puncture as a useful test to verify
the presence or absence of SAH.64
The general trend in the historical progress of the surgical management of IAs
was to become more direct and more
effective. The surgical treatment of IAs
started in 1885, when Victor Horsley ligated the cervical carotid artery to induce
thrombosis within an epsilateral IA. Direct
surgery for IAs started in 1931, when Norman Dott wrapped a ruptured aneurysm
with a piece of muscle. Walter Dandy performed the first clipping of an internal
carotid artery (ICA) aneurysm in 1937.
Microsurgery for IAs began in the 1960s
and gradually led the surgical field mainly
due to the efforts of Yasargil. Surgery remained the only definitive treatment until
the early 1990s, when endovascular treatment became an alternative to clipping.32,
44, 168, 176, 182, 258, 269, 278
Trials to produce thrombosis inside systemic aneurysms by introducing a foreign
body or using thermal or electrical stimulation were initiated in the first half of the
19th century. Electrothermal coagulation
of an acutely ruptured IA was first report-
ed by Werner et al. in 1941. In 1963, Gallagher reported using pilojection to induce
the thrombosis of IAs. The first catheterization of cerebral vessels to occlude an IA
was reported in 1964 by Luessenhop and
Velasquez, who attempted to occlude a
ruptured carotid-ophthalmic artery aneurysm. In 1973, Serbinenko performed the
first successful balloon embolization of
an IA. The present era in the endovascular management of IAs using electrically
detachable coils was initiated in the early
1990s by Guglielmi.61, 72, 73, 82, 84, 170, 237, 238
2.1.7.2. Microsurgery
The principal goal of the surgical management of an intracranial aneurysm is to
completely and safely exclude the aneurysm from circulation. This entails clipping
the entire aneurysm neck while maintaining normal vascular patency and avoiding parenchymal injury. All other surgical
steps (including craniotomy, opening of
the arachnoid and brain retraction) are
intended to gain access to the aneurysm.
These steps are associated with some risks
which might affect the final surgical outcome.
The accumulation of neurosurgical experience, improvements in operating microscopes and the advancement of medical imaging have resulted in minimizing
the gain-access steps needed for the clipping of IAs while maintaining efficacy and
safety.
2.1.7.3. Endovascular treatment
Originally, endovascular coiling of intracranial aneurysms was restricted for
surgically inaccessible or difficult cases,
especially in posterior circulation or when
there was a medical contraindication for
surgery. After the publication of the initial
results of the International Subarachnoid
Aneurysm Trial (ISAT) study in 2002, which
recommended endovascular treatment,
management strategies have changed.
The endovascular coiling of intracranial
aneurysms became not only a “competitor” to microsurgical clipping, but became
the first choice of therapy in many hospitals across the globe.61, 77, 182
2.2. Anatomy for MCA
aneurysm microsurgery
2.2.1. The middle cerebral
artery
The MCA is the largest of the cerebral
arteries. The diameter of the MCA at its
origin is about 4 mm (range, 2.4–4.6 mm).
The MCA starts as the larger and the more
direct branch at the ICA bifurcation and
courses laterally below the anterior perforated substance within the sylvian fissure
(SF), where it gives rise to the lateral lenticulostriate arteries (LLSAs) and cortical
branches and, then, divides into its main
trunks. The MCA has a characteristic genu
at which it turns sharply posterosuperiorly to run over the insular surface. At the
peri-insular sulcus, the MCA branches turn
to run on the medial surfaces of the frontal, parietal and temporal opercula. The
MCA branches reach the cortical surface
after turning around the frontal, parietal
and temporal opercula.198, 218, 292
2.2.1.1. Development of the middle cerebral artery
Before the development of the insula
and sylvian fissure, the cortical branches
of the MCA ramify directly over the lateral
surface of the brain. With the start of insular development between the eighth and
the twelfth weeks of gestation, the MCA
branches follow the progressive invagination of the insula and the in-folding of the
overlying frontal, parietal and temporal
25
lobes and, thus, the MCA branches become folded and buried within the deep
part of the SF appearing only through the
lips of the superficial part of the SF.76, 198
2.2.1.2. Segmental anatomy of
the middle cerebral artery
The MCA is classically subdivided into
four segments: the sphenoidal (M1) segment extending from the ICA bifurcation
to the main MCA bifurcation where insular trunks (M2) begin and course over
the insula until the peri-insular sulcus,
where the opercular (M3) segments start
and continue until the lateral surface of
the brain in the SF and, then, continue as
cortical (M4) segments. The early cortical
branches are named the parasylvian (M4)
segments and the distal extensions are
called the terminal (M5) segments (see
Figure 2).219, 262, 293
2.2.1.3. Cortical area of supply
The MCA supplies the entire insular and
opercular surfaces and most of the lateral
surface of the hemisphere excluding the
occipital and frontal poles and the upper
margin of the hemisphere. It also supplies
the lateral part of the inferior surface of
the frontal and temporal lobes and the
temporal pole.198, 218
2.2.1.4. Branching pattern of the
M1 segment
There is evident variability in the number and dominance of divisions of the
proximal middle cerebral artery (M1).
There may be a single trunk with no primary divisions, a bifurcation, a trifurcation
or a quadrifurcation. The most common
branching pattern is the bifurcation seen
in 64–90% of hemispheres, where M1
ends in the superior and inferior divisions.
A balanced supply between both divisions
is seen in 18% of hemispheres, where the
superior division supplies the cortex from
the orbitofrontal to the posterior parietal
areas and the inferior trunk supplies from
the angular to temporopolar areas. The
inferior trunk is dominant slightly more
frequently than the superior trunk (32%
vs. 28%), where there is a shift in supply
from the dominant division towards the
other division’s area of supply. This will be
apparent in the clinical syndromes associated with division occlusion.56, 76, 124, 268
2.2.1.5. Perforating branches
The average number of LLSAs arising
from the MCA is 10 arteries (range of 1–21)
per hemisphere. The majority (80%) of
theses perforating branches arise from
the M1 segment of the MCA with the remaining stemming from the proximal
Figure 2.
Illustration showing the segmental anatomy
of the MCA on the left side.
1: M1, proximal segment; 2: M2, insular
trunks; 3: M3, opercular segments; 4: M4,
cortical segments; *: main bifurcation of the
MCA; 5: early cortical branch.
26
branches of the MCA and the proximal
insular trunks (M2s). The LLSAs penetrate
the anterior perforated substance to supply the internal capsule, the lateral aspect
of the anterior commissure, the dorsal aspect of the head of the caudate nucleus,
the lateral globus pallidus, the putamen
and the substantia innominata. The LLSAs
pursue an S-shaped course to enter the
anterior perforated substance unlike the
relatively direct course of the medial lenticulostriate arteries.186, 218, 228
2.2.1.6. Early cortical branches
According to Crompton, early cortical
branches (ECBs) arise from the M1 segment proximal to the main MCA bifurcation and traverse towards the cortex.30
These ECBs are divided into (a) early frontal branches (EFBs) and (b) early temporal
branches (ETBs) according to their area of
supply. Ture et al. found one to three ECBs
in 95% of hemispheres in their dissection
of 20 human cadaver brains. ETBs were
found three times more frequently than
EFBs.262 Yasargil argued that the misconception regarding the origin of large ECBs
as the main MCA bifurcation was the reason behind some reports of a very short
M1 segment of the MCA.292
anomalies include hypoplasia, aplasia and
fenestrations. These anomalies might be
associated with the formation of aneurysms.48, 69, 75, 90, 91, 110, 118, 134, 135, 145, 148, 155, 159, 181,
242, 246, 255, 263, 267, 276
2.2.2. The sylvian fissure
The SF is the most easily recognizable
feature on the lateral surface of the brain.
It is an important surgical corridor to the
central part of the base of the skull, the
circle of Willis and the basal surface of
the brain. The SF is classically described
as comprising superficial and deep parts.
The superficial part consists of a stem
and three rami (the anterior horizontal,
the anterior ascending and the posterior
rami). The stem extends for around 4 cm
on average behind the sphenoid ridge in
a medial to lateral direction between the
frontal and temporal lobes. The anterior horizontal and the anterior ascending
rami divide the inferior frontal gyrus into
the pars orbitalis, the pars triangularis and
the pars opercularis. The posterior ramus
lies between the frontal and parietal lobes
superiorly and the temporal lobe inferiorly. The average length of the posterior ramus is 7.5 cm.62, 252, 261
The deep part of the SF consists of the
2.2.1.7. Anomalies of the middle sphenoidal and operculoinsular compartcerebral artery
ments. The sphenoidal compartment lies
Although the branching pattern of the
MCA is highly variable, true anomalies of
the MCA are rare. The incidence of MCA
anomalies ranges from 0.6–3% in anatomic dissections30, 76, 124 and even less
frequently during angiography.149, 256 The
most commonly observed anomalies of
the MCA include the duplicated middle
cerebral artery (DMCA) which arises from
the ICA and the accessory middle cerebral
artery (AccMCA) which arises from the anterior cerebral artery. Other less frequent
behind the sphenoid wing between the
frontal and temporal lobes and contains
the M1 segment of the MCA. The operculoinsular compartment lies deep relative to the superficial rami of the SF and
contains the M2 and M3 segments of the
MCA. This operculoinsular compartment
is divided into two clefts: (1) the opercular
cleft which lies more superficial between
the frontoparietal operculum and the
temporal operculum and (2) the insular
cleft which lies deeper between the insula
27
and the medial aspect of the opercula.62,
252
2.2.2.1. Sylvian veins
Although there is considerable variation
in the drainage and branching pattern of
the sylvian veins, these veins are usually
grouped into superficial and deep veins
with significant anastomosis between
both groups. Careful study of the venous
anatomy and adequate dissection are required during transsylvian approaches in
order to obtain adequate working space
without sacrificing or overstretching the
sylvian veins.142, 217
2.2.2.1.1 Superficial sylvian veins
The superficial sylvian vein (SSV) (or the
superficial middle cerebral vein) is usually
enveloped in double layers of the arachnoid bridging the lips of the SF. The SSV is
most frequently recognized as one or two
main trunks. It is less common to find that
the SSV is absent or hypoplastic. The SSV
typically drains into the sphenoparietal
sinus (SPS) or directly into the cavernous
sinus.142, 217
2.2.2.1.2 Deep sylvian veins
The deep sylvian veins consist of insular
veins converging on a common trunk (the
deep middle cerebral vein) near the limen
insula. The deep middle cerebral vein
typically joins the anterior cerebral vein
to form the basal vein, or less frequently
drains into the SPS or the cavernous sinus.142, 197
2.2.2.2. Sylvian cistern
The sylvian cistern is the subarachnoid
space spreading into the deep part of the
SF. It contains the sylvian veins and the
MCA and its branches. The proximal end
of the sylvian cistern is separated from the
28
carotid cistern by a thick arachnoid band
around the origin of the MCA. The degree
of surgical difficulty for the transsylvian
approaches is affected by the width of the
sylvian cistern and the strength and the
transparency of the intrasylvian arachnoid bands. The width, length and depth
of the sylvian cistern are variable and the
intrasylvian arachnoid bands are normally
transparent and fragile, but can be thickened after meningitis or SAH, which also
stains the arachnoid.25, 292, 293
2.2.2.3. Perisylvian cortex
On the basal surface of the brain, the inferior wall of the SF is formed by the upper
surface of the planum polare of the superior temporal gyrus. The superior wall of
the SF is formed by the posterior orbital
gyrus, the posterior part of the lateral orbital gyrus and the pars orbitalis of the inferior frontal gyrus.281
On the lateral surface of the brain, the
inferior wall of the SF is formed by (from
anterior to posterior) the upper surface
of the planum polare, Heschl’s gyrus and
the planum temporale of the superior
temporal gyrus. The upper wall of the SF
is formed by (from anterior to posterior)
the pars orbitalis, the pars triangularis, the
pars opercularis and precentral gyrus of
the frontal lobe and postcentral and supramarginal gyri of the parietal lobe. The
pars triangularis of the inferior frontal gyrus marks the turn from the horizontal to
the lateral parts of the SF (see Figure 3).281
2.2.2.4. Insula
The base of the SF is formed by the insula which is a pyramid-shaped set of gyri
buried in the depth of the SF. It has an anterior surface and a lateral convex surface
which presents two faces: superolateral
and inferolateral. The insula is encircled
by the limiting sulcus which separates
Figure 3.
Illustration showing the perisylvian
cortex and the insula on the left side.
1: pars orbitalis, 2: pars triangularis,
3: pars opercularis, 4: precentral gyrus, 5: postcentral gyrus, 6: supramarginal gyrus, 7: superior temporal
gyrus, 8: central insular sulcus, 9:
three short insular gyri, 10: two long
insular gyri.
the insula from the frontal, parietal and
temporal opercula. The limiting sulcus is
generally triangular consisting of a superior horizontal part under the frontoparietal operculum, an inferior diagonal part
under the temporal operculum and an
anterior part beneath the pars orbitalis.186,
252, 261, 281, 294
The central insular sulcus, which is the
deepest sulcus of the insula, splits the lateral surface of the insula into a larger anterior part with three short gyri and a smaller posterior part with two long gyri (see
Figure 3). The limen insula is an elevation
overlying the uncinate fasciculus at the
junction of the sphenoidal and the operculoinsular compartments of the SF. The
insular pole is formed by the convergence
of the short gyri lateral to the limen at the
lower anterior edge of the insula. The insular apex is the most prominent elevation on the insular convexity and the most
superficial point of the insula. It is located
above and behind the insular pole, usually
on the middle short gyrus. Numerous tiny
arteries run from the M2 and M3 branches
to supply the insula as well as the underlying external capsule and claustrum.252, 261,
294
2.3. Middle cerebral artery aneurysms (MCAAs)
2.3.1. Incidence
MCAAs represent 18–40% of all IAs and
are the most frequent lesion in patients
with multiple IAs. In Finland, the MCA is
the most common location for IAs, where
43% of all patients with IAs and 73% of all
patients with multiple IAs have at least
one MCAA. MCAAs are most frequently
located at the main MCA bifurcation.34-36,
104, 112, 221, 293
2.3.2. Classification
Because of the wide diversity of MCAA
morphology, etiology, size, location, projection and clinical presentation, the accurate classification of MCAAs is required
in order to tailor the proper clinical management strategy. For example, the size
of MCAAs can be small (<7 mm), medium
(7–14 mm), large (15–24 mm) or giant (≥25
mm). Morphologically, MCAAs can be saccular, fusiform, blister-like or extremely
dysmorphic. Topographically, MCAAs are
located either proximal, at or distal to the
main MCA bifurcation. The etiology of
most MCAAs is still not precisely defined,
29
although some are clearly traumatic, dissecting or infectious.49, 293, 299
2.3.3. Clinical symptoms of
MCAAs
2.3.3.1. Unruptured MCAAs
Currently, more MCAAs are diagnosed
incidentally during investigation for unrelated symptoms or in association with
other symptomatic aneurysms in patients
with multiple aneurysms. Large and giant
MCAAs can also be symptomatic from
mass effects, seizures or ischemic changes.224, 299
2.3.3.2. Ruptured MCAAs
The rupture of MCAAs typically leads
to SAH with the characteristic symptoms
and signs of meningeal irritation and/
or hydrocephalus. The clinical picture is
usually complicated by frequently associating ICH, intrasylvian hematoma (ISH)
or vasospasm which adversely affects
the eloquent brain cortex surrounding
the SF. Thus, homonymous hemianopsia,
hemiplegia and/or cortical sensory loss,
especially in the upper limb, can be found
either separate from or in association with
ruptured MCAAs. Moreover, motor, receptive or global aphasia may be found in a
patient with ICH from a ruptured MCAA
on the dominant side. The rupture of
MCAAs can be associated with convulsive
seizures more frequently than other IAs.64,
299
2.3.4. Morphological features of MCAAs
Aneurysm size, shape, wall irregularities and wall calcification are among the
morphological characteristics correlated
with the risk of aneurysm rupture and can
also affect the feasibility of surgical and/
30
or endovascular treatment. The rupture of
MCAAs is usually associated with a large
aneurysm size, a less spherical shape and
wall irregularity. MCAAs usually have
broad necks which frequently hinder simple endovascular coiling and increase the
risk of vascular compromise after surgical
clipping. The calcification of the aneurysm neck can also complicate surgical
clipping.39, 50, 88, 115, 162, 279
2.3.5. Special subgroups of
MCAAs
2.3.5.1. Giant MCAAs
Giant IAs (≥25 mm) are diagnosed most
frequently along the MCA, where they
represent 1–4% of all MCAAs. The intrasylvian anatomy is usually disturbed by
the giant MCAA which shifts the MCA and
its branches. Preoperative evaluation of
these giant aneurysms requires 3D reconstruction of angiographic data for a better understanding of the vascular anatomy. Although some giant MCAAs can be
successfully excluded from circulation by
simple clipping, the surgeon should be
ready for the possible need for aneurysmorrhaphy, vascular reconstruction and/
or vascular bypass procedures.50, 141, 147, 157,
158, 160, 221
2.3.5.2. Fusiform MCAAs
Fusiform intracranial aneurysms are
longitudinal, frequently circumferential
dilatations of the cerebral arteries typically affecting posterior circulation. Fusiform MCAAs are rare, but represent one
of the most challenging lesions for both
neurosurgeons and neurointerventionists. These aneurysms lack true necks and
their walls are usually calcified and atherosclerotic, while their lumens are usually partially thrombosed. Fusiform MCAAs
are usually large in size, affect a long seg-
ment of the MCA and cannot usually be
managed by simple microsurgical clipping or endovascular coiling. Aneurysm
wrapping, trapping with cerebral revascularization, stent-assisted coiling or other
complex treatment modalities are usually needed with higher rates of morbidity
and mortality.127, 160, 202, 299
2.3.6. Treatment of MCAAs
2.3.6.1. Historical aspects and
background
According to Fox, a total of 11 MCAAs
were found in 8 autopsy reports published in the 1800s. Most of these MCAAs
were of a large size and associated with
SAH. In 1918, Packard and Zabriskie performed decompression of a ruptured
MCAA. In 1928, Schmidt “enucleated” a giant MCAA. A variety of surgical approaches for MCAA were described, including
the frontolateral approach by Dandy in
1944, the temporal approach by Swain in
1948 and the frontal approach by Falconer in 1951. Despite all of these efforts, the
treatment of MCAAs during the first half
of the 20th century was associated with
high morbidity and mortality.64, 65
Petit-Dutaillis and Pittman presented
their experience with operating on nine
ruptured MCAAs between 1946 and 1954.
They performed neck occlusion for seven
MCAAs—five by clipping and two by ligature with silk suture. For the other two
cases, hematomas were evacuated without obliteration of the ruptured MCAAs.
They also reviewed the available literature
up to 1954 and found 76 cases of surgically managed MCAAs. The surgical procedures applied included occlusion of the
aneurysm neck (29), wrapping of the aneurysm with muscles (12), occlusion of the
parent artery (6), ligation of cervical carotid only (18), evacuation of ICH only (9) and
intracranial exploration only (2). From the
results of their own cases and that of the
reviewed literature, it could be concluded
that occlusion of the MCAA neck was the
procedure which yielded the most fruitful outcomes, with good results achieved
in 81% of cases, 6% resulting in morbidity and 14% resulting in mortality. On the
other hand, surgical exploration only and
evacuation of the ICH only were associated with the highest mortality rates—100%
and 91%, respectively.206
The results of the surgical treatment of
MCAAs started to improve in the second
half of the 20th century especially after
the adoption of microsurgical techniques.
Between 1967 and 1984, Yasargil operated on 231 MCAAs. The outcomes were
good in 86% of cases with 10% morbidity
and 4% mortality. There have also been
several other large reviews of the surgical management of MCAAs incorporating
hundreds of cases, such as the Hungarian
review of 289 patients by Pasztor et al., the
Japanese review of 413 patients by Suzuki
et al. and the Finnish review of 561 patients by Rinne et al. The results of these
large studies were comparatively satisfactory varying mainly due to the different
inclusion criteria for each.203, 221, 249, 293
Regli et al. studied two consecutive
samples of unruptured MCAAs prospectively managed according to a protocol
favoring endovascular coiling which considered surgical clipping only after the
failure of coiling trials or in the presence
of angio-anatomical contraindications
for endovascular coiling. The first sample, between 1993 and 1997, comprised
34 unruptured MCAAs. Out of these 34
MCAAs, 21 were primarily clipped since
their angio-anatomy excluded endovascular trials. Only 2 of the 13 MCAAs which
received trials for endovascular coiling
were successfully coiled. The remaining
31
11 MCAAs were clipped after the failure of
coiling trials. The second sample, between
1997 and 2000, comprised 40 unruptured
MCAAs. Out of these, 39 were considered
primarily for surgical treatment because
of the unfavorable angio-anatomy for
endovascular treatment. Only one case
had a favorable angio-anatomy for endovascular treatment and was successfully
coiled. They concluded that surgical clipping was the most adequate treatment
for unruptured MCAAs at that time.215, 216
In the last decade after tremendous advances in endovascular techniques and
devices, several relatively large studies of
the endovascular management of MCAAs
were published.16, 17, 40, 42, 79, 83, 106, 117, 169, 187, 195,
207, 209, 250, 273, 291, 297
2.3.6.2. Microsurgical treatment
2.3.6.2.1. Microsurgical clipping
Microsurgical clipping of MCAAs is still
the preferred treatment modality in most
centers due to the relatively straightforward surgical approach to these comparatively superficial aneurysms. In addition
to the major advantage of surgery which
provides effective and durable exclusion
of MCAAs, surgery also allows for the
management of the increased intracranial
pressure through evacuation of ICH, the
release of cerebrospinal fluid (CSF) and/or
hemicraniectomy.15, 51, 58, 86, 100, 183, 184, 224
The accurate preoperative localization
of the MCAA either at the main bifurcation or at another branching point has
important implications on surgical planning especially for ruptured aneurysms.
The different locations of MCAAs pose
distinct challenges to the neurosurgeon
and require peculiar surgical strategies.
Furthermore, the location of the MCAA affects the selection of the recipient vessel
for cerebral revascularization if indicated
32
in order to manage an inevitable vascular
compromise during the securing of the
aneurysm.
2.3.6.2.1.1.
MCAAs
Clipping
of
proximal
Proximal MCA aneurysms (M1As) are
especially challenging lesions because
of their intimate relation to LLSAs and/or
the ECBs. These perforators and cortical
arteries may arise from the M1 segment
or from the aneurysm neck itself. These
branches are quite easily damaged if severed during dissection, included with the
aneurysm during clipping or compressed
by the clip with subsequent thrombosis.
LLSAs, despite being very small in some
instances, irrigate eloquent areas of the
brain and, thus, damage to them could result in a poor clinical outcome. Moreover,
it is not unusual to find M1As embedded
in the brain parenchyma risking premature aneurysm rupture simply through
brain retraction.
Thus, for M1As, it is necessary to carefully study good-quality imaging and to
use high magnification to identify and
secure perforators and ECBs related to the
aneurysm before trying to clip it. Much
care should be taken when retracting the
brain to avoid the risk of premature rupture of the aneurysm if it is embedded in
the brain substance. The aneurysm neck
should be clipped before dissection of the
entire dome. In addition, it is advisable to
use the shortest possible clip to reduce
the risk of a postoperative kink in the
nearby small vessels.104, 123, 204, 292
2.3.6.2.1.2. Clipping of MCA bifurcation aneurysms
For MCA bifurcation aneurysms (MbifAs), it is important to dissect and expose
more of the aneurysm and the M2s to
make sure that a division from early refurcation of the M2s is not included with
the aneurysm in the clips. Occasionally, it
can be difficult to maintain both M2s patent without compromise while trying to
completely occlude the aneurysm neck.
In this instance, it is better to leave some
neck unclipped to avoid narrowing or occluding any of the M2s. The residual neck
can then be protected with another clip,
bipolar coagulation or just wrapping with
a piece of gauze. Clearing of the proper neck of the MbifA can be problematic
when one or both M2s are adherent to the
neck giving the neck a broader appearance. This may necessitate careful sharp
dissection of these branches from the
neck. It is also important to keep in mind
that the LLSAs may arise at or even distal
to the MCA bifurcation. Thus, care must
be taken not to include any perforator in
the clip.104
2.3.6.2.1.3. Clipping of distal MCAAs
The main challenge during surgery for
MdistAs is to localize the aneurysms, particularly when they are small and distal
to the M2–M3 junction or when the SF
is filled with SAH or ICH. Localization of
MdistAs requires more experience and
careful study of the preoperative angiography. Identification of the parent MCA
segment—either M2, M3 or M4—can
help to localize the aneurysm over the insula, under the opercula or on the brain
surface, respectively. The distance from
the MCA genu, the location in relation to
the associated ICH if present, the depth
of the aneurysm from the surface of the
brain and the relation to some craniometric points and skull sutures are some
of the data that can be obtained from
CTA and which can help during surgery.
Neuronavigation, intraoperative DSA or
intraoperative ultrasound might also be
considered.34
2.3.6.2.2. Adjuncts to the surgical
clipping of MCAAs
Although simple clipping is usually safe
and sufficient for the management of
most MCAAs, others require extra steps
to manage the additional challenges imposed by their giant size, intraluminal
thrombosis (see Figure 4), calcifications
(see Figure 5), branch incorporation and/
or complex anatomy. Aneurysmorrhaphy,
tandem clipping, vascular reconstruction,
cerebral revascularization, trapping and/
or wrapping may be valid options when
dealing with such difficulties.141, 224
2.3.6.2.2.1. Bypass surgery for complex MCAAs
When exclusion of an MCAA seems to
significantly risk the patency of the afferent or efferent MCA branches, cerebral
revascularization should be considered.
Before approaching a giant, fusiform,
thrombosed or complex MCAA incorporating one or more of the MCA branches,
the STA should be preserved and prepared early for possible STA–MCA anastomosis. This significantly reduces the time
of temporary clipping needed to perform
the anastomosis.174, 224, 236, 299
Aside from STA–MCA anastmomsis, revascularization options also include highflow bypass using a saphenous vein or
radial artery graft, MCA–MCA in-situ anastomosis and reanastomosis of the MCA after aneurysm excision. Bypass procedures
are skill-demanding and carry the risk for
ischemic complications; thus, they should
be considered only in extreme cases (see
Figure 6).147, 174, 224, 236, 299
2.3.6.2.3. Evolution of surgical approaches to MCAAs
The development of the microsurgical
management of MCAAs has been charac-
33
precise dissection. Even if the aneurysm
ruptured during dissection, the bleeding
is less troublesome so long as there is
proximal restriction of the blood flow. In
the early 1950s, vasodepressor drugs were
recommended in order to lower arterial
pressure during IA surgery. According to
Petit-Dutaillis and Pittman206, Olivecrona
was the first to use removable clips for the
temporary occlusion of MCA proximal to
the aneurysm neck.278
Figure 4.
Axial T2 MRI brain scan showing a partially thrombosed giant MCAA on the right side.
terized by minimizing not only the craniotomy size but also the area of the brain
exposed, vessel manipulation and sylvian
dissection.
2.3.6.2.3.1. Proximal control during
MCAA surgery
Proximal arterial control before aneurysm dissection is a fundamental principal of IA surgery. With proximal control,
the tension of the aneurysm wall is diminished which allows for the safe and
During surgery for MCAAs, proximal
control of the parent MCA was achieved
after dissecting the ICA in the carotid cistern and then following the MCA from its
beginning at the ICA bifurcation towards
the aneurysm. The accumulation of surgical experience, the use of high magnification and the availability of clear 3D images of the vascular anatomy with bony
landmarks from preoperative CTA all allowed for the safe targeting of the parent
MCA in order to achieve proximal control
just before the aneurysm neck. This can
eliminate, in most cases, the necessity of
starting the dissection from the ICA or to
widely open the sylvian fissure to define
the proximal MCA.34-36, 104, 293
If the exposed segment of the parent
MCA harbors numerous perforators or
Figure 5.
CTA images (A: axial, B: coronal, and C: sagittal) showing a calcified giant MCAA on the right side.
34
Figure 6.
DSA images showing examples of some cerebral revascularization techniques to compensate for vascular insufficiency after the trapping of complex MCAAs. A: STA-MCA bypass, B: Occipital artery – MCA bypass, C: High flow
bypass using a saphenous vein graft from the external carotid artery to the MCA on the right side.
is apparently calcified or atherosclerotic,
adenosine-induced cardiac arrest is an
alternative to temporary clipping to render the aneurysm softer. With adenosine
at the ready, some MCAAs can also be
clipped directly without achieving proximal control; but, additional care is needed
to avoid intraoperative rupture with concomitant risks.11, 85
2.3.6.2.3.2. Classic surgical approaches for MCAAs
The proximal sylvian approach involves
the splitting of the SF in a medial-to-lateral direction. The ICA is identified and
followed laterally along the M1 segment
until the aneurysm is encountered. The
advantage of this approach is that proximal control is achieved early and it allows
for exposure of the aneurysm neck before
the dome. The disadvantage is that it requires a relatively extensive dissection
which risks injury to banks of the SF and
increases the risk of vasospasm of the
MCA.104
The distal sylvian approach entails the
splitting of the SF in a lateral-to-medial
direction. The SF is opened laterally and
the M2s are followed proximally until the
aneurysm is encountered. The advantage
is that it requires less dissection. The disadvantage is that the aneurysm dome is
encountered before proximal control is
obtained.104
The superior temporal gyrus approach
implies a subpial dissection of the superior temporal gyrus with exposure of the
peripheral MCA branches and following
them proximally. This approach is usually reserved for situations when there is
a temporal ICH and/or the brain is swollen. The advantage of this approach is
the preservation of the sylvian veins and
minimizing the need for retraction. The
disadvantage is the violation of brain tissue and a theoretical increase in the risk
of epilepsy.104
2.3.6.2.3.3. Focused sylvian opening
for MCAAs
The focused sylvian opening means a
limited area of sylvian dissection is placed
directly over the suspected location of the
MCAA with the aim of exposing just the
aneurysm and the MCA around the aneurysm. The advantage of this method is
35
that it avoids extensive dissection which
carries the risk of injury to the banks of the
SF and sylvian veins. This also minimizes
the risk of an exacerbating vasospasm of
the MCA and its branches. This approach
also makes it possible to work just proximal to the neck to achieve proximal control and, at the same time, to dissect the
branches around the aneurysm before
neck clipping.51
2.3.6.2.3.4. Contralateral approach for
MCAAs
With careful preoperative analysis of the
vascular anatomy, some cases with bilateral MCAAs can be managed through a
unilateral approach which spares the patient a second craniotomy. The optimal
MCAA for clipping through a contralateral
craniotomy is an unruptured small M1 aneurysm projecting inferiorly or anteriorly
in an elderly patient with some brain atrophy. Some MCA bifurcation aneurysms
could also be managed from the contralateral side when the M1 segment is short
and the aneurysm projection is favorable.223, 224
2.3.6.3. Endovascular treatment
Until within the last decade, endovascular coiling was considered unsuitable for
the management of most MCAAs given
that they typically have broad necks with
arterial branches originating at their base
in addition to the unfavorable angioarchitecture of the MCA. The advancement of
endovascular techniques and the introduction of new microcatheters, remodeling balloons, stents and flow diverters
increased the feasibility of coiling many
previously challenging MCAAs. Although
these novel techniques and devices enabled interventionists to overcome some
obstacles such as the unfavorable fundusto-neck ratio of some MCAAs and diffi-
36
cult angioarchitecture of the MCA, they
are still limited in their ability to manage
other difficulties, in particular, a partially
thrombosed aneurysm or a branch originating from the aneurysm neck.21, 111, 125, 204
Although the safety and durability of
new endovascular devices have not yet
been proven and the use of antiplatelet agents with stents and flow diverters
presents challenges especially for ruptured cases, the endovascular treatment
of MCAAs is gaining popularity in many
centers as the first-line treatment option,
leaving only complex MCAAs requiring
surgery.16, 24, 79, 127, 144, 187, 209, 250, 296, 297
2.3.7. Outcome after treatment of MCAAs
2.3.7.1. Angiographic outcome
The rates for angiographic obliteration
of MCAAs after surgical management
ranges from 97–99% complete obliteration, up to 3% complete obliteration with
neck remnants and around 1% incomplete obliteration of the aneurysm sac.
Angiographic obliteration of MCAAs after
endovascular management ranges from
29–80% complete obliteration, 12–48%
complete obliteration with neck remnants
and up to 43% incomplete obliteration of
the sac. There is around a 4% rate of technical failure and retreatment after the endovascular treatment of MCAAs.16, 17, 25, 42, 83,
86, 111, 117, 169, 183, 187, 192, 195, 209, 221, 224, 249, 250, 269, 272, 293
2.3.7.2. Clinical outcome
Although the reported angiographic
outcome after the surgical management
of MCAAs is superior to that after endovascular treatment, the recorded clinical
outcomes after both modalities are comparable. Knowing that most endovascular
series were selective for favorable MCA
cases while the surgical series were almost always nonselective including even
complex cases, demonstrates how efficient the surgical management of MCAAs
is.16, 17, 25, 42, 83, 86, 111, 117, 169, 183, 192, 195, 209, 221, 224, 249,
250, 269, 272, 293
For ruptured MCAAs, the outcome after endovascular treatment is reported to
be good in 48–100% of cases and poor in
up to 52% of cases with a mortality rate
of up to 14%. The outcome after the surgical treatment of MCAAs is recorded to
5–45% with a mortality rate of up to 13%.
For unruptured MCAAs, the outcome after endovascular treatment is reported to
up to 5% of cases with a mortality rate of
up to 3%. The outcome of surgical treatment is recorded to be good in 88–100%
of cases and poor in 4–12% of cases with
a mortality rate of up to 2%.16, 17, 25, 42, 83, 86, 111,
117, 169, 183, 192, 195, 209, 221, 224, 249, 250, 269, 272, 293
The wide variation in the reported patient outcomes after both treatment mo-
dalities is not only related to the appropriate selection of the treatment modality or
the operator proficiency, but also to specific patient and aneurysm factors. Patient
age, clinical condition at presentation
and medical comorbidities, as well as aneurysm rupture status, size and complex
morphology are among the many factors
which strongly influence the incidence of
intraprocedural complications, morbidity
and mortality.16, 17, 25, 42, 83, 86, 111, 117, 169, 183, 192, 195,
209, 221, 224, 249, 250, 269, 272, 293
Although the immediate postoperative outcomes after MCAA surgery match
those of other anterior circulation aneurysms, long-term follow-up indicates
that MCAA patients often fare worse due
to more persistent deficits (e.g., motor,
speech and/or visual fields) and/or late
onset epilepsy. The MCA lacks sufficient
collaterals and, thus, is less forgiving than
the remaining anterior circulation. This
vulnerability demands extreme care in order to reduce vascular and parenchymal
manipulation during MCAA surgery. 221
37
3. AIMS OF THE STUDY
3. Aims of the study
I.
To describe an objective angioarchitecture-based technique for defining the
main MCA bifurcation from other branching points along the MCA as a key
for the classification of MCAAs, and to present a four-group classification of
MCAAs as an extension of the classic three-group classification to help recognize the branching pattern of the MCA and to facilitate the accurate classification of MCAAs.
II.
To study the topographical and morphological characteristics of saccular
MCAAs in a large consecutive study and to determine which of these characteristics might predict the rupture tendency of these lesions.
III.
To outline the basic strategy and techniques for the microsurgical management of MCAAs through a focused opening of the SF and to explain simple
practical strategies for managing any possible difficulties encountered during
the clipping of MCAAs.
38
4. PATIENTS, MATERIALS AND METHODS
4. Patients, materials and methods
This study (Publications I & II) relies on
retrospective data from the Helsinki Intracranial Aneurysm Database, which
includes more than 9,000 patients with
IAs who have been referred to the Department of Neurosurgery at the Helsinki University Central Hospital (catchment
area of 1.8 million people) since 1937. We
identified 1,124 consecutive patients with
MCAAs diagnosed between the years
2000 and 2009. We excluded 115 patients
from the study due to the lack of an adequate CTA (n = 98) or those who had
nonsaccular MCAAs (n = 17). The remaining 1,009 patients with a total of 1,309 saccular MCAAs had adequate cerebral CTAs.
Publication III is based on the surgical
experience of Professor Juha Hernesniemi
over the past 13 years using a refinement
of a microsurgical technique for the management of MCAAs, specifically focused
on the microsurgical clipping of more
than 1,000 MCAAs.
Table 1.
Division of MCAAs into four subgroups.
4.1. Publication I
4.1.1. Images
For each of the 1,009 patients, pretreatment CTA images were examined and
measured on screen (AGFA, IMPAX DS
3000). The MCAAs were identified in each
patient and classified according to the location of the aneurysm neck in relation
to the main MCA bifurcation (see Figures
7–12). MCAAs were placed into one of
four groups: (1) M1 segment lenticulostriate artery aneurysms (M1-LSAAs); (2) M1
segment early cortical branch aneurysms
(M1-ECBAs); (3) main MCA bifurcation aneurysms (MbifAs); and (4) distal MCA aneurysms (MdistAs). The M1-ECBAs comprised M1 segment early frontal branch
aneurysms (M1-EFBAs) and M1segment
early temporal branch aneurysms (M1-ETBAs) (Table 1).
4.1.2. Localization of the
main MCA bifurcation
For the localization of the main MCA
bifurcation, we first checked the MCA
branches in sagittal views of the CTA at
the insular level. The M2s were identified
M1–LSAAs
Aneurysms arising on the main trunk (M1) of the MCA, between the
ICA bifurcation and the main MCA bifurcation, at the origin of lenticulostriate arteries
M1–ECBAs
Aneurysms
arising M1–EFBAs
on M1 at the origin of
ECBs
M1–ETBAs
Aneurysms arising at
the origin of EFB
Aneurysms arising at
the origin of ETBs
MbifAs
Aneurysms at the main MCA bifurcation
MdistAs
Aneurysms distal to the main MCA bifurcation on the M2, M3 or M4
segments
39
based on their posterior–superior direction and their course along the insular
surface. These trunks were then followed
in the proximal direction until the point
where they met. This convergence point
of the M2s was defined as the main MCA
bifurcation. The examination of the sagittal views was, then, correlated with the
axial and coronal views for confirmation
of the finding. In some cases with difficult
branching and looping patterns, 3D reconstruction was necessary (see Figure 7).
4.1.3. Assigning MCAAs into
subgroups
the CTA. The aim was to check whether
these branches were cortical or insular.
Correlation with the axial and coronal
views and, at times, 3D reconstructions
were necessary. Once the nature of the
branching vessels was established, we
examined the relationship between the
origins of these branching vessels (i.e., the
aneurysm base) with respect to the main
MCA bifurcation (the primary meeting
point of the M2s). Based on this information, each aneurysm was assigned into
one of the subgroups (see Table 1 and Figures 7–12).
The course and direction of the branches originating at the neck of the aneurysm
were first inspected in the sagittal view of
Figure 7.
CTA images (A: sagittal, B: coronal, C: axial and D: 3D reconstruction) illustrating an early cortical branch aneurysm
(white arrow) arising at the origin of an early frontal branch (green arrow) proximal to the main MCA bifurcation (yellow
arrow) which shows the frontal (red arrow) and temporal (blue arrow) M2s. The accompanying diagrams (E, F and G)
display how the angioarchitecture can help identify the main MCA bifurcation from the other branching points along
the MCA. In the sagittal view (E), the M2s (frontal in red and temporal in blue colors) have a characteristic upward and
posterior course, which helps in their identification. Following the M2s backward until they meet at a single point will
localize the main MCA bifurcation. It is important to recheck in the coronal (F) and axial views (G).
40
Figure 8.
CTA images (A: axial, B: coronal, C: sagittal and the corresponding 3D reconstruction views (D, E and F, respectively) illustrating an early cortical branch aneurysm (white arrows) arising at the origin of a large early frontal cortical branch (green
arrow) just proximal to the right MCA genu. This type of aneurysm can be subjectively misclassified as an MCA bifurcation
aneurysm, especially in coronal views; but, in the sagittal and axial views, the frontal branch (green arrow) is seen running
anteriorly away from the insula. In addition, the right MCA bifurcation (yellow arrow) is clearly seen distal to the genu
yielding the frontal (red arrow) and temporal (blue arrow) M2s.
Figure 9.
CTA images (A: axial, B: coronal,
C: sagittal and D: 3D reconstruction) illustrating an aneurysm
(white arrow) arising at the main
MCA bifurcation (yellow arrow)
which yields frontal (red arrow)
and temporal (blue arrow) M2s.
Notice the frontal cortical branch
(green arrow) arising from the
frontal M2 (red arrow). The MCA
main bifurcation (yellow arrow)
is located proximal to the genu.
41
Figure 10.
CTA images (A: axial, B: coronal and C: sagittal) illustrating an early cortical branch aneurysm (white arrow) arising at the
origin of an early frontal branch (green arrow) proximal to the main MCA bifurcation (yellow arrow) which yields frontal
(red arrow) and temporal (blue arrow) M2s. The MCA main bifurcation (yellow arrow) is located distal to the genu.
Figure 11.
CTA images (A: axial, B: coronal, C:
sagittal and D: 3D reconstruction)
illustrating an early cortical branch
aneurysm (white arrow) arising
at the origin of an early temporal
branch (green arrow) proximal to
the main MCA bifurcation (yellow
arrow) which yields frontal (red
arrow) and temporal (blue arrow)
M2s. The MCA main bifurcation
(yellow arrow) is located at the
genu.
4.2. Publication II
4.2.1. Images
For each of the 1,009 patients, pretreatment CT and CTA images were assessed
and measured on screen (AGFA, IMPAX
DS 3000) for the morphological and topographical variables of MCAAs. The mor-
42
phological variables comprised aneurysm
wall regularity, size, neck width, AR, bottleneck factor (BNF) and height–width ratio. The topographical variables included
the aneurysm location along the MCA,
side, distance from the ICA bifurcation
and dome projection in the axial and coronal CTA views.
Figure 12.
CTA images (A: axial, B: coronal and C: sagittal) illustrating a distal MCAA (white arrow) arising at the takeoff of a frontal
cortical branch (green arrow) from the left frontal M2 (red arrow) distal to the main MCA bifurcation (yellow arrow) which
yields frontal (red arrow) and temporal (blue arrow) M2ss. The MCA main bifurcation (yellow arrow) is located proximal
to the genu.
4.2.2. Patients and aneurysms
The mean age of patients at the time of
diagnosis was 55 ± 11 years (range 13–89
years). There was a clear female predominance with a female-to-male ration of
2.2:1 (690/319). In 466 (46%) patients,
there were multiple aneurysms. Multiple
MCAAs were seen in 246 (24%) patients,
unilateral in 59 patients and bilateral in
187 patients (see Table 2). There were 407
(31%) ruptured and 902 (69%) unruptured
MCAAs. There were more MCAAs on the
right side than on the left side (56% vs.
44%) and more aneurysms in women
than in men (905 vs. 404). However, these
differences were not statistically significant. The demographic characteristics of
the patients are presented in Table 3.
Table 2.
Patients and aneurysms.
No (%)
Single aneurysm Patients with only a single MCAA
patients
543 (54%)
Multiple aneurysm Patients with a single MCAA + one or more 220 (22%)
patients
associated aneurysms outside the MCA
Patients with multiple MCAAs without oth- 142 (14%)
er associated aneurysms
Patients with multiple MCAAs + one or more 104 (10%)
associated aneurysms outside the MCA
Total number of patients
1,009
43
Table 3.
Demographic characteristics of 1,009 patients with 1,309 MCAAs.
MCAAs (1,309)
Unruptured
(902)
Ruptured (407)
55 (13–83)
54 (24–89)
Aneurysms in men, n (%)
265 (66%)
139 (34%)
Aneurysms in women, n (%)
637 (70%)
268 (30%)
Right, n (%)
494 (67%)
238 (33%)
Left, n (%)
408 (71%)
169 (29%)
Age of patient (yrs)
Mean (range)
Sex (319 men + 690 women)
Side of the aneurysm
4.2.3. Morphological analy- 4.2.4. Topographical analysis
sis
The aneurysm wall was evaluated as either smooth (one regular pouch without
protrusions) or irregular (with protrusions
or secondary pouches). In each MCAA, we
measured (on screen under 4× magnification) the aneurysm height (maximal orthogonal distance from the dome to the
neck), width (maximal diameter perpendicular to the height) and neck width (the
minimum diameter of the neck plane).
According to the aneurysm size (the maximum cross-sectional diameter), MCAAs
were divided into four subgroups: small
(<7 mm), medium (7–14 mm), large (15–24
mm) and giant (≥25 mm). The AR (defined
as the aneurysm height to aneurysm neck
width), the BNF (defined as the aneurysm
width to neck width) and the aneurysm
height–width ratio were calculated.
44
Depending on the location of the aneurysm neck, the MCAAs were divided into
three groups: (1) M1As, (2) MbifAs and (3)
MdistAs.
The distance from the ICA bifurcation to
the proximal neck was measured for 1,128
MCAAs (in the remaining 181 MCAAs,
anatomy was distorted by large intracerebral hematoma caused by the rupture
of either the MCAA or other associated
aneurysm). The main projection of the
MCAA in the axial and coronal views was
recorded; in the coronal CTA views, the
aneurysm dome was categorized as superior (towards the frontal lobe), inferior (towards the temporal lobe) or neutral (neither superior nor inferior projection); in
the axial CTA views, the aneurysm dome
was categorized as anterior (in front of the
MCA), posterior (behind the MCA) or neutral (neither anterior nor posterior projection). The aneurysm projection was also
confirmed from sagittal CTA views (see
Figures 13–17).
4.2.5. Statistical analysis
For univariate analysis, we used the chisquare test for categorical variables, Student’s t-test for parametric continuous
variables and Mann-Whitney U test for
Figure 13.
illustrating a small-size MCAA (arrow) arising at the origin of the early
cortical branch from the M1 segment
(M1-ECBAs) on the left side. The aneurysm dome is almost spherical and
has a regular contour (D). The aneurysm dome is projecting superiorly in
the coronal view (B) and anteriorly in
the axial view (A). The aneurysm was
diagnosed incidentally.
Figure 14.
CTA images (A: axial, B: coronal and
C: sagittal) illustrating a small-size
MCAA (arrow) arising at the main
MCA bifurcation (MbifA) on the right
side. The aneurysm dome is almost
spherical and has an irregular contour. The dome is projecting inferiorly
in the coronal view (B) and is neutral
in the axial view (A). The aneurysm
was ruptured and the CT (D) showed
a SAH, an intraventricular hemorrhage and a massive right-side frontotemporal intracerebral hematoma.
45
Figure 15.
sagittal and D: 3D reconstruction) illustrating a large-size MCAA (arrow)
arising at the main MCA bifurcation
(MbifA) on the right side. The aneurysm dome is almost oval and has
an irregular contour (D). The dome
is projecting inferiorly in the coronal
view (B) and posteriorly in the axial
view (A). The aneurysm was diagnosed incidentally.
Figure 16.
CTA images (A: axial, B: coronal and
C: sagittal) illustrating a large-size
MCAA (arrow) arising at the main
MCA bifurcation (MbifA) on the left
side. The aneurysm dome is almost
oval and has an irregular contour.
The dome is projecting inferiorly in
the coronal view (B) and anteriorly
in the axial view (A). The aneurysm
was ruptured and the CT (D) showed
a SAH and a left-side temporal intracerebral hematoma.
nonparametric continuous variables. In
the univariate analysis, we included size,
AR, BNF, height–width ratio, wall regularity, location, side, projections and distance
from the ICA. A probability value (p) < .05
was considered statistically significant. Pa-
46
rameters having a statistically significant
association with rupture status in univariate analyses were included in multivariate logistic regression analyses to further
assess interdependence.6, 162 To calculate
the odds ratio (OR), we used binary logis-
Figure 17.
illustrating a medium-size MCAA
(arrow) arising at a branching point
along the M2 segment (MdistA) on
the right side. The aneurysm dome
is almost oval and has a regular
contour (D). The dome is projecting
superiorly in the coronal view (B) and
posteriorly in the axial view (A). The
aneurysm was diagnosed incidentally.
tic regression analysis. All statistics were
carried out using SPSS (version 17.0, SPSS,
Chicago, Illinois).
4.3. Publication III
4.3.1. Surgical planning
4.3.1.1. Importance and tools
An appropriate surgical plan is key to diminishing brain and vessel manipulation
by eliminating unnecessary intraoperative navigation and by selecting the most
direct and safest approach for MCAAs. In
our practice, CTA with 3D reconstruction
is the basis for planning surgery based on
the patient-specific MCA anatomy and aneurysm-specific topography, morphology
and rupture status.
4.3.1.2. Aneurysm localization
From imaging, we recognize the specific segment or angle of the sphenoid
ridge directly overlying the aneurysm.
Intraoperatively, an aneurysm can be ac-
curately localized along the SF based on
the corresponding segment or angle of
the sphenoid ridge (see Figure 18). In addition, some easily identifiable features
of superficial sylvian veins and/or cortical MCA branches are sometimes used as
surface landmarks in order to localize the
aneurysm along the SF. Furthermore, the
distance of the aneurysm from the MCA
genu, which lies immediately beneath the
pars triangularis281, helps to localize the
aneurysm. Neuronavigation is generally
used only in some distal MCAAs where
the lack of good intraoperative anatomical landmarks can make localization of
these aneurysms otherwise very difficult.
4.3.1.3. Choosing the approach
angle
Free-handling of the 3D reconstruction
of CTA data helps to select the approach
angle which provides the most favorable
surgical view of the clipping field (see
Figure 19) without the aneurysm dome
obstructing the way. For a ruptured aneurysm, the angle of the approach must be
47
Figure 18.
Illustration of a segmentation of the sphenoid ridge to facilitate its use as a surface landmark to localize MCAAs.
CTA images (A: axial and B: 3D reconstruction) of the sphenoid ridge. The angulation pattern of the sphenoid ridge varies
between patients, but is generally an anteriorly convex arc beginning medially at the tip of the anterior clinoid process and
ending laterally at the lateral wall of the middle fossa. Two points (angles) can usually be identified where there is a prominent change in the direction of its sloping. At its medial segment (green), the sphenoid ridge slopes mainly from posterior
to anterior until the medial angle (arrow) at the base of the anterior clinoid process. For the middle segment (blue), the
sloping becomes more medial to lateral until the lateral angle (arrow head). At the lateral segment (red), the ridge slopes
mainly from anterior to posterior.
From the axial views and 3D reconstruction of a CTA, we identify the specific segment or angle of the sphenoid ridge directly overlying the aneurysm. Intraoperatively, the aneurysm can be accurately localized along the sylvian fissure based on
the corresponding segment or angle of the sphenoid ridge. Even after a part of the sphenoid wing is removed by drilling,
the underlying dura maintains its original angulation pattern and can still guide localization of the aneurysm.
planned so that the rupture site is not accidentally exposed before proper proximal
control has been established. The selected angle of the approach can be obtained
by changing the placement of the sylvian
opening in relation to the aneurysm location (see Figures 20–22 and Videos 1–3).
4.3.2. Surgical technique
4.3.2.1. Positioning and craniotomy
The patient is positioned supine with
the head elevated above the heart level
(10–20 cm). The head is mildly extended, rotated to the contralateral side and
slightly tilted laterally. The head rotation
Figure 19.
Illustration showing the clipping
field for different types of MCAAs.
The clipping field includes the
parent MCA, the aneurysm base
and the branches at the aneurysm
base.
ECB: early cortical branch, LSA:
lenticulostriate artery, ICA: internal carotid artery, M1: proximal
middle cerebral artery, M2: insular
trunk and MCA: middle cerebral
artery.
48
Figure 20.
Illustrative case of the placement of the sylvian opening for a middle cerebral artery bifurcation aneurysm.
CTA images (A: axial, B: coronal, C: sagittal and D: 3D reconstruction) illustrating a 10-mm MCA bifurcation aneurysm
(white arrow) on the right side. The relationship of the aneurysm to the medial angle of the sphenoid ridge in the axial view
(A) and in the 3D reconstruction (D) helps to intraoperatively localize the aneurysm along the sylvian fissure. The height of
the aneurysm relative to the sphenoid wing in the coronal (B) and sagittal (C) views helps to adjust the angle of the intrasylvian dissection (frontal versus temporal) to reach the clipping field directly. Free-manipulation of the 3D reconstruction
is used to preview the clipping field from different angles. The surgical view of the clipping field through a direct angle
(E, see also the green arrow in D) is less favorable than that through a more oblique angle (F, and the yellow arrow in D).
Thus, for a more favorable surgical view of the clipping field, the sylvian opening is placed more laterally (* in D). G is an
intraoperative photograph showing the surgical view of the clipping field obtained through the focused sylvian opening. H
is an intraoperative photograph showing the size of the sylvian opening. See also Video 1.
An: aneurysm base, FL: frontal lobe, M1: proximal middle cerebral artery, M2: insular trunk and TL: temporal lobe.
49
Figure 21.
Illustrative case showing the placement of the sylvian opening for a middle cerebral artery bifurcation aneurysm.
CTA images (A: axial, B: coronal, C: sagittal and D: 3D reconstruction) demonstrating an 11-mm MCA bifurcation aneurysm
(white arrow) on the right side. The relationship of the aneurysm to the medial angle of the sphenoid ridge in the axial
view (A) and in the 3D reconstruction (D) helps to intraoperatively localize the aneurysm along the sylvian fissure. The
height of the aneurysm relative to the sphenoid wing in the coronal (B) and sagittal (C) views helps to adjust the angle
of the intrasylvian dissection (frontal versus temporal) to reach the clipping field directly. Free-manipulation of the 3D
reconstruction is used to preview the clipping field from different angles. The surgical view of the clipping field through a
direct angle (E, see also the green arrow in D) is more favorable than that through a more oblique angle (F, and the yellow
arrow in D). Thus, for a more favorable surgical view of the clipping field, the sylvian opening is placed directly (* in D) over
the clipping field. G is an intraoperative photograph showing the surgical view of the clipping field obtained through the
focused sylvian opening. See also Video 2.
An: aneurysm base, M1: proximal middle cerebral artery and M2: insular trunk.
50
Figure 22.
Illustrative case showing the placement of the sylvian opening for a ruptured middle cerebral artery aneurysm.
CT images (A: axial and B: coronal) illustrating a temporal intracerebral hematoma (black arrow) on the right side. The CTA
images (C: axial, D: coronal, E: sagittal and F: 3D reconstruction) reveal a ruptured 8-mm MCA bifurcation aneurysm (white
arrow) on the right side as the cause of the temporal intracerebral hematoma with a bleb on the anterior medial inferior
wall of the aneurysm dome representing the suspected rupture site. The relationship of the aneurysm to the medial angle
of the sphenoid ridge in the axial view (C) and in the 3D reconstruction (F) helps to intraoperatively localize the aneurysm
along the sylvian fissure. The height of the aneurysm relative to the sphenoid wing in the coronal (D) and sagittal (E)
views helps to adjust the angle of the intrasylvian dissection (frontal versus temporal) to reach the clipping field directly.
Free-manipulation of the 3D reconstruction is used to preview the clipping field from different angles.
51
Figure 22. Continued
The surgical view of the clipping field through an anterior direct angle (G, see also the green arrow in F) is adequate for clipping, but being close to the suspected rupture site (red mark in G) risks premature intraoperative rebreeding. Approaching
the clipping field from the lateral direction (F, and the yellow arrow in D), in addition to providing a favorable surgical view
of the clipping field, avoids the early exposure of the suspected rupture site (red mark in H), thus decreasing the associated
risk of early intraoperative rebleeding. Thus, for a safer surgical approach, the sylvian opening is placed more laterally (* in
F). I is an intraoperative photograph showing the surgical view of the clipping field obtained through the focused sylvian
opening. The photograph was taken immediately after clipping of the aneurysm neck before removal of the temporary
clip. The yellow dotted line outlines the aneurysm hidden by the temporal lobe with the suspected rupture site (red lines)
situated on the opposite side from the approach to the clipping field. See also Video 3.
M1: proximal middle cerebral artery and M2: insular trunk.
(15–45 degrees) depends on how proximal or distal the opening of the SF is
planned. The more distal the opening, the
more the head needs to be rotated. The
degree of head extension depends on
the height of the aneurysm in relation to
the skull base. The higher the aneurysm,
the more the head needs to be extended.
The details of the lateral supraorbital approach used in almost all MCAA surgeries
have been previously published.102 For giant MCAAs, pterional craniotomy is often
used. For distal MCAAs, craniotomies are
tailored according to the location and size
of the aneurysm.
4.3.2.2. Opening of the sylvian
fissure
The sylvian opening is placed according
to both the aneurysm location and the
chosen approach angle. Under high magnification (9x or more) of the operating
microscope, the two arachnoid layers (the
layer covering the SF and the layer limiting the sylvian cistern) are incised (usually
on the frontal side of sylvian veins) with a
sharp needle. Through this incision using
water dissection190, the SF is expanded
followed by sharp dissection with intermittent use of bipolar forceps and microscissors. Our strategy is to open a small
window in the two arachnoid layers and,
then, go deep into the sylvian cistern from
52
where the window is extended from the
inside out. In addition to being fast, this
technique helps in maintaining the proper dissection plane, especially in patients
with tight SF (see Video 2).
The size of the sylvian opening should
allow for the free exchange of microsurgical instruments and clips while sustaining
good visual control. The size of the opening varies according to aneurysm size
and location, but a 10–15 mm opening is
usually sufficient. If needed, the sylvian
opening can be extended at any stage
during the surgery. Retractors are seldom
used since sufficient retraction is usually
achieved with small cottonoids and with
the suction tip.
4.3.2.3. Clipping of the MCAA
From the sylvian opening, the clipping
field is approached by dissecting in the direction designated from the preoperative
imaging. Following the M3 or M2 branches towards the aneurysm is not obligatory.
However, if imaging shows some branches between the sylvian opening and the
aneurysm, following these branches may
help, but is not necessary. Once the clipping field is reached, a perforator-free
area of the parent MCA just proximal to
the aneurysm neck is prepared for temporary clipping. During temporary clipping,
the aneurysm neck is dissected free from
the surrounding branches. After initial
clipping of the neck, temporary clips are
carefully removed, and the neck occlusion
and vessel patency are checked. Bipolar
reshaping of the aneurysm neck and/or
the exchange of clips might be needed to
achieve satisfactory results.
4.3.2.4. Confirming the adequacy of clipping
The accuracy of the final clipping is confirmed by indocyanine green (ICG) angiography and/or Doppler ultrasonography
(US). In some cases, intraoperative DSA is
needed, especially for giant aneurysms or
in bypass surgery.
4.3.2.5. Closing the sylvian fissure
After verifying the proper clipping,
hemostasis is ensured and papaverine
is applied to the clipping field; then, the
sylvian banks are approximated with glue
injection (see Video 4).
Microsurgical videos
We have selected and edited demonstrative videos illustrating the microsurgical treatment of MCAAs in different locations through the focused opening of
the SF technique (see section 8 for a list of
eight supplementary videos on the microsurgery of MCAAs).
53
5. RESULTS
5. Results
5.1. Distribution of MCA
aneurysms (Publication I)
The number of aneurysms located at
MbifAs (829 or 63%) was double the number of aneurysms arising along M1As (406
or 31%). MdistAs were the least frequent
type, representing only 74 (6%) aneuLocation
rysms. The rupture state of the aneurysms
affected their distribution—among 407
ruptured MCAAs, 315 (77%) were found at
the main MCA bifurcation compared with
514 (57%) from 902 unruptured MCAAs.
Table 4 and Figure 23 show the distribution of 1,309 aneurysms along the MCA.
Ruptured
Unruptured
Total
n
n
n (%)
(%)
(%)
Proximal MCA (M1As)
80 (20%)
326 (36%)
406 (31%)
MCA bifurcation (MbifAs)
315 (77%)
514 (57%)
829 (63%)
Distal MCA (MdistAs)
12 (3%)
62 (7%)
74 (6%)
Total
407
902
1,309
Table 4.
Distribution of
1,309 MCAAs.
Figure 23.
Illustration showing the distribution of 1,309 MCAAs along the MCA
following the four-group classification in the present studies.
54
5. RESULTS
5.2. Types of M1As (Publi- 5.4. Aneurysm dome procation I)
jection (Publication II)
Among 406 M1As, 242 (60%) aneurysms
arose at the origin of the ECBs (M1–ECBAs). The remaining 164 (40%) M1As were
not associated with the ECBs, but rather
with lenticulostriate arteries (M1–LSAAs).
Of the 242 M1–ECBAs, 178 were found at
the origin of early frontal branches (M1–
EFBAs) and 64 at the origin of early temporal branches (M1–ETBAs) (see Table 5).
In the axial CTA view, the dome was
most commonly projecting anteriorly in
586 (45%) MCAAs. In the coronal CTA view,
the dome was most commonly projecting
inferiorly in 730 (56%) MCAAs. The differences in dome projections between ruptured and unruptured MCAAs are shown
in Table 6.
5.5. Aneurysm wall (Pub5.3. Distance from ICA bi- lication II)
furcation (Publication II)
The mean distance for all M1 aneurysms
(M1–ECBAs and M1–LSAAs) from the ICA
bifurcation was 12.5 ± 3.7 mm (range 1–20
mm), for MbifAs from the ICA bifurcation
was 18.2 ± 4.5 mm (range 7–33 mm) and
for distal MdistAs from the ICA bifurcation
was 25.5 ± 10 mm (range 10–65 mm) (see
Table 6).
All 1,309 MCAAs included in the study
were saccular. A smooth aneurysm wall
was seen in 810 (62%) aneurysms and
an irregular wall was seen in 499 (38%)
aneurysms. A smooth wall was more frequently associated with unruptured rather than ruptured aneurysms (89% vs. 11%,
respectively). An irregular wall, on the other hand, was more frequently associated
with ruptured rather than unruptured aneurysms (64% vs. 36%) (see Table 7).
Table 5.
Subdivision of 406 M1 segment aneurysms.
Type of M1As
Ruptured
Unruptured
Total
n
n
n (%)
(%)
(%)
45 (56%)
197 (60%)
242 (60%)
M1–EFBAs
41 (51%)
137 (42%)
178 (44%)
M1–ETBAs
4
60
(18%)
64 (16%)
M1–ECBAs
(5%)
M1–LSAAs
35 (44%)
129 (40%)
164 (40%)
Total
80
326
406
55
5. RESULTS
Table 6.
Topographical findings for 1,309 MCAAs.
M1As
MbifAs
MdistAs
Ruptured
Unruptured
Ruptured
Unruptured
Ruptured
Unruptured
80 (20)
326 (80)
315 (38)
514 (62)
12 (16)
62 (84)
Anterior
46 (58)
164 (50)
133 (42)
212 (41)
4 (33)
27 (44)
Posterior
27 (34)
100 (31)
135 (43)
202 (39)
8 (67)
25 (40)
7 (9)
62 (19)
47 (15)
100 (19)
0
10 (16)
Superior
40 (50)
143 (44)
56 (18)
144 (28)
8 (67)
31 (50)
Inferior
32 (40)
156 (48)
218 (69)
297 (58)
4 (33)
23 (37)
Neutral
8 (10)
27 (8)
41 (13)
73 (14)
0
8 (13)
Distance
from ICA to
aneurysm;
Mean (in
mm)
13.5
12.4
17.8
18.4
24.4
25.6
n (%)
Projection
in axial CTA;
n (%)
Neutral
Projection
in coronal
CTA; n (%)
5.6. Aneurysm size (Publication II)
5.6.1. Dome size
The mean size for all ruptured and unruptured MCAAs was 10 mm (range 1–41
mm) and 5 mm (range 1–51 mm), respectively. The majority of unruptured aneurysms (n = 706, 78%) were small (<7 mm)
and most ruptured aneurysms (n = 224,
55%) were of a medium size (7–14 mm).
Large (15–24 mm) and giant (≥25 mm) aneurysms were infrequent, found in only
56
63 (15%) ruptured and 31 (3%) unruptured
MCAAs.
5.6.2. Neck size
The mean neck width was similar for all
aneurysm locations. However, ruptured
aneurysms tended to have somewhat
larger necks than those which remained
unruptured (mean 5 mm and 3 mm, respectively) (see Table 7).
5. RESULTS
Table 7.
Morphological findings for 1,309 MCAAs.
M1As
MbifAs
MdistAs
Ruptured
Unruptured
Ruptured
Unruptured
Ruptured
Unruptured
80 (20)
326 (80)
315 (38)
514 (62)
12 (16)
62 (84)
8.9 (2–28)
4.8 (1–51)
10 (1–41)
5.6 (1–33)
6.8 (2–12)
3.6 (1–14)
Small (<7),
n (%)
30 (38)
280 (86)
84 (26)
368 (72)
6 (50)
58 (94)
Medium
(7–14), n
(%)
40 (50)
34 (10)
178 (57)
127 (25)
6 (50)
4 (6)
Large (15–
24), n (%)
9 (11)
6 (2)
48 (15)
14 (3)
0
0
Giant
(≥25), n
(%)
1 (1)
6 (2)
5 (2)
5 (1)
0
0
Irregular
wall, n (%)
54 (68)
48 (15)
258 (82)
123 (24)
6 (50)
10 (16)
Smooth
wall, n (%)
26 (33)
278 (85)
57 (18)
391 (76)
6 (50)
52 (84)
Neck width,
mean (in mm)
4.5
3.2
4.7
3.7
3.9
2.7
Aspect ratio
1.9
1.3
2.2
1.4
1.7
1.2
Bottleneck
factor
1.5
1.2
1.6
1.3
1.6
1.1
Height–width
ratio
1.3
1.1
1.4
1.1
1.1
1.1
n (%)
Aneurysm
size (range)
(in mm)
Aneurysm
size groups (in
mm)
Aneurysm
wall
5.7. Morphological indices (Publication II)
MCAAs had a mean AR of 1.6 ± 0.9, a
mean BNF of 1.4 ± 0.6 and mean height–
width ratio of 1.2 ± 0.4. Aneurysms were
divided into three groups based on the
height–width ratio: (a) height–width ratio < 1, i.e., wide and shallow oval-shaped
aneurysms; (b) height–width ratio = 1, i.e.,
spherical aneurysms; and (c) height–width
ratio > 1, i.e., elongated oval-shaped aneurysms. The rupture rates for these three
57
5. RESULTS
Table 8.
Rupture rate according to the height–width ratio.
Height–width ratio <1
Height–width ratio = 1
Height–width ratio >1
Aneurysms, n
239
470
600
groups were 28%, 10% and 49%, respectively. Spherical aneurysms were least
likely to rupture (see Table 8).
5.7.1. Aneurysm height–
width ratio vs. aneurysm size
We performed further analysis where
the height–width ratio was plotted (horizontal axis) against aneurysm size (vertical
axis), which is the most frequently reported morphological index associated with
the rupture of IAs. The two-dimensional
scatter plot is shown in Figure 24, in which
the Lowess curve shows the relationship
between aneurysm size and the height–
width ratio. It shows a generally linear correlation between the height–width ratio
and aneurysm size except for a characteristic local minimum at a height–width
Ruptured aneurysms, n (%)
68 (28%)
47 (10%)
292 (49%)
ratio of 1, i.e., for spherical aneurysms.
More than half (53%) of the 826 small-size
MCAAs had a height–width ratio value of
1, which was associated with a low rupture rate (10%).
5.8. Trends in the rupture
of MCAAs (Publication II)
5.8.1 Morphological trends
Univariate analysis of the morphological and topographical variables of MCAAs
exposed certain differences between ruptured and unruptured MCAAs. Ruptured
MCAAs were larger (9.7 mm vs. 5.2 mm, p
< .001), with a wider neck (4.6 mm vs. 3.4
mm, p < .001), and they had a larger AR
(2.1 vs. 1.4, p < .001), BNF (1.6 vs. 1.3, p <
.001) and height–width ratio (1.3 vs. 1.1,
Figure 24.
Scatter plot with the
Lowess curve (red)
showing the relationship between aneurysm
size and the height–
width ratio.
58
5. RESULTS
Table 9.
Univariate analysis of morphological and topographical characteristics of MCAAs.
MCAAs (n = 1,309)
p
OR for
rupture
95% CI for
OR
Unruptured
(n = 902)
Ruptured
(n = 407)
Dome size (mean± SD) (in mm)
5.2 ± 4.6
9.7 ± 5.2
<.001
1.22
1.19–1.26
Neck size (mean± SD) (in mm)
3.4 ± 2
4.6 ± 2.23
<.001
1.32
1.24–1.41
AR (mean± SD)
1.4 ± 0.7
2.1 ± 1
<.001
3.38
2.80–4.07
BNF (mean± SD)
1.3 ± 0.6
1.6 ± 0.7
<.001
2.91
2.28–3.71
Height–width ratio (mean± SD)
1.1 ± 0.3
1.3 ± 0.4
<.001
6.12
4.35–8.62
1.01
0.99–1.04
Wall regularity, n (%)
<.001
Smooth
721 (89)
89 (11)
Irregular
181 (36)
318 (64)
Location of the aneurysm, n (%)
<.001
M1
326 (80)
80 (20)
Mbif
514 (62)
315 (38)
Mdist
62 (84)
12 (16)
16.71 ± 6.13
17.13 ± 4.64
Distance from ICA, (mean ± SD) (in
mm)
Projection in the axial view, n (%)
.33
.02
Neutral
172 (76)
54 (24)
Anterior
403 (69)
183 (31)
Posterior
327 (66)
170 (34)
Projection in the coronal view, n (%)
.002
Neutral
108 (69)
49 (31)
Inferior
476 (65)
254 (35)
Superior
318 (75)
104 (25)
p < .001). An irregular aneurysm wall was
much more common in ruptured than unruptured MCAAs (78% vs. 20%, p < .001).
5.8.2. Topographical trends
MCA bifurcation aneurysms had a higher rupture rate than M1 or distal MCA an-
eurysms (38% vs. 20% vs. 16%, respectively, p < .001). In the axial CTA view, a neutral
projection of the aneurysm dome was related to a lower rupture rate than anterior
and posterior projections (24% vs. 31% vs.
34%, respectively, p = .02). In the coronal
CTA view, a superior projection of the aneurysm dome was associated with a low-
59
5. RESULTS
Table 10.
Multivariate analysis of morphological and topographical characteristics of MCAAs
p
OR for rupture
95% CI for OR
Aneurysm size
.86
1.01
0.92–1.11
Neck size
.19
1.13
0.94–1.34
AR
.70
1.18
0.51–2.70
BNF
.42
1.44
0.59–3.54
Height–width ratio
.04
3.44
1.07–11.05
<.001
8.39
6.13–11.49
Wall regularity (Irregular vs.
smooth)
Location of the aneurysm
.04
Mbif vs. M1
.01
1.56
1.09–2.23
Mdist vs. M1
.78
1.12
0.52–2.4
Projection in the axial views
.55
Anterior vs. neutral
.47
1.18
0.75–1.84
Posterior vs. neutral
.28
1.29
0.82–2.04
Projection in the coronal views
.43
Inferior vs. neutral
.32
0.78
0.49–1.27
Superior vs. neutral
.20
0.71
0.42–1.2
er rupture rate than the neutral and the
inferior projections (25% vs. 31% vs. 35%,
respectively, p = .002). The distance from
the ICA along the MCA did not differ between ruptured and unruptured MCAAs
(16.7 mm vs. 17.1 mm, p = .33) (see Table 9).
5.8.3. Independent risk factors for rupture
Multivariate analysis of the morphological and topographical variables revealed
that a greater height–width ratio (p = .04),
60
an irregular wall (p < .001) and the location at the main MCA bifurcation (p = .01)
were associated with MCAA rupture. The
aneurysm size (p = .86), neck size (p = .19),
AR (p = .70), BNF (p = .42), projection in
the axial views (p = .55) and projection in
the coronal views (p = .43) were no longer
statistically significant (see Table 10). The
relationship between the three independent rupture risk factors and the different
size groups of MCAAs is presented in Table 11 and Figure 25.
5. RESULTS
Table 11.
Size groups of MCAAs and the associated rupture risk factors.
Total
aneurysms, n
(%)
Ruptured
aneurysms,
n (%)
Mean height–
width ratio ±
SD (in mm)
Wall
irregularity,
n (%)
Location at the
MCA bifurcation,
n (%)
Size groups
Small (<7 mm)
826
120 (15)
1.1 ± 0.30
156 (19)
452 (55)
Medium (7–14 mm)
389
224 (58)
1.3 ± 0.44
272 (70)
305 (78)
Large (15–24 mm)
77
57 (74)
1.4 ± 0.40
62 (81)
62 (81)
Giant (≥25 mm)
17
6 (35)
1.3 ± 0.88
9 (53)
10 (59)
Figure 25.
Prevalence of three independent risk factors for the
rupture of MCAAs in different
size groups and the associated rupture rates.
5.9. Focused opening of
the sylvian fissure for the
management of MCAAs
(Publication III)
The focused opening of the SF for the
microsurgical management of MCAAs has
proved to be safe and effective for the
clipping of both ruptured and unruptured
MCAAs. This included MCAAs with different levels of surgical difficulties due to the
variable complexity of the MCA anatomy,
the specific aneurysm topography and
morphology and various consequences
of aneurysm rupture (see Table 12).
61
5. RESULTS
Table 12.
Findings in 407 consecutive ruptured MCAAsa.
Cases, n (%)
Aneurysm location
M1–LSAAs
35
M1–ECBAs
45
MbifAs
315
MdistAs
12
Preoperative CT findings
Fisher gradeb
Grade 1
15 (4)
Grade 2
47 (12)
Grade 3
120 (29)
Grade 4
225 (55)
Frontal
41 (10)
Temporal
165 (41)
Moderate
60 (15)
Severe
35 (9)
ICH
IVHc
ASDH
32 (8)
Hydrocephalus
d
Moderate
109 (27)
Severe
19 (5)
a
These 407 consecutive ruptured MCA aneurysms were diagnosed between 2000 and 2009.7
b
The Fisher grading system for SAH.57
c
Moderate means there is blood inside the ventricles but no distension. Severe mans that the
ventricles are distended with blood.
d
Hydrocephalus was diagnosed when the size of both temporal horns (TH) was ≥2 mm in width
୊ୌ
or when
> 50% (where FH is the largest width of the frontal horns and ID is the internal
୍ୈ
diameter from inner table to inner table at this level). Hydrocephalus was considered moderate
୊ୌ
୊ୌ
when (2 mm ≤ TH < 4 mm and 50% ≤ < 70%) and severe when (TH ≥ 4mm or ≥ 70%).
୍ୈ
62
୍ୈ
6. DISCUSSION
6. Discussion
To date, this is the largest anatomical
study of MCAAs altogether comprising
1,309 MCAAs. Compared to cadaveric
studies, anatomic studies based on modern imaging methods such as CTA, such as
that used in our study, allow for a much
larger sample size, less selection bias, better reproducibility of the measurements
and, thus, more reliable statistical analysis.
6.1. The main MCA bifurcation
The main MCA bifurcation can simply
be defined as the branching point where
the M2s originate. The large anatomical
variation in size, length and branching
pattern of the M1 segment has posed difficulties in defining the M1–M2 junction,
i.e., the main MCA bifurcation.
Distinguishing the main MCA bifurcation is key to the sound classification and
grouping of MCAAs. Inconsistency in defining the main MCA bifurcation has led
to a wide range in the reported lengths
of M1 segments and large differences in
the reported frequencies of MCAA subgroups. Despite many previous reports on
the standard MCA anatomy, the definition
of the main MCA bifurcation has been
rather subjective and has varied between
different authors. Some have used the
relation to certain anatomical landmarks
such as the MCA genu, the limen insulae
or the LSAs, while others have relied on
the size of the branching vessels.35, 36, 80, 112,
186, 198, 204, 266, 292
It has also been common to
accept a branching point close to the MCA
genu giving rise to the largest branches as
the main MCA bifurcation. This has often
been the case in patients with aneurysms
in particular. This incongruity in the iden-
tification of the main MCA bifurcation led
us to design this study, where we used
a large patient population and modern
CTA to specify the main MCA bifurcation
based on vascular anatomy.
Previously, the identification of the main
MCA bifurcation was often based on the
origin of LLSAs, the genu of the MCA, the
limen insulae and the size of the originating branches.30, 198, 251, 292, 293 Although
sound in theory, we have found that these
methods are often problematic. The LLSAs should be found proximal to the main
MCA bifurcation.251, 292 This definition can
be used well in autopsy studies. However,
on CTA or DSA images, LLSAs are typically
not visible. Using the genu of the MCA in
order to define the main MCA bifurcation
is also inaccurate. The relation of the main
MCA bifurcation to the genu of MCA varies, and has been found to be proximal to
the genu in 82% of cases, at the level of
genu in 8% of cases and distal to the genu
in 10% of cases.251 Finally, the size of the
originating branches varies highly and a
large cortical branch originating from the
M1 segment can be easily mistaken for an
M2.262
6.1.1. “False” MCA bifurcation
The classic reason for the incorrect
identification of the main MCA bifurcation is the presence of large ECBs close to
the MCA genu which may resemble the
post-bifurcation M2s.262 This can result
in misinterpreting their origin (false early
bifurcation) as the main MCA bifurcation.
ETBs are usually less of a problem given
that their size decreases the closer they are
to the genu of the MCA.251 For EFBs0, there
63
6. DISCUSSION
is no such correlation between their size
and proximity to the MCA genu. This explains why some aneurysms arising close
to the MCA genu at the origin of a large
EFB could be easily confused for MbifAs
and why the distribution of MCAAs has
varied significantly in previous reports.
6.1.2. Angiographic identification of the main MCA bifurcation
We based our technique for the classification of MCAAs on the only angiographically evident anatomical definition of the
main MCA bifurcation that all previous
reports shared: the origin of the insular
trunks (M2s). Our assumption was to use
the meeting point of the M2s as an objective hallmark for defining the main
MCA bifurcation. The identification of the
M2s was possible due to the 3D nature of
modern CTA data with multiple viewing
directions. This technique proved to have
a greater interobserver agreement than
any of the previous methods we initially
applied.
6.2. Four-group classification of MCAAs
In our previous MCA publications34-36,
, we have followed the traditional
classification of MCAAs into three groups:
proximal (M1As), bifurcation (MbifAs) or
distal (MdistAs) aneurysms. Recognizing
the importance and the deceptive appearance of the early cortical branches,
we extended this classic three-group classification into a four-group classification
by subdividing M1 aneurysms into M1–
ECBAs and M1–LSAAs. This proved to be
practical and helped to focus our attention to this previously underrepresented
101, 115, 221
64
group of aneurysms arising at the origin
of the ECBs.
6.3.
Distribution
MCAAs
of
Most MCAAs are located close to the
MCA genu either at the main MCA bifurcation, the origin of the ECB or the proximal branching of the M2s. Discrimination
between these branches and, hence, the
classification of the MCAAs was possible using our technique. Difficulties
arose when the course of the MCA was
disturbed due to a large ICH, as was the
case in 51% of our ruptured aneurysms. In
these situations, a more careful analysis of
the different CTA views with the additional help of a 3D reconstruction is needed.
We used only CTA data in this study, but
the same principle could also be applied
with magnetic resonance angiography
(MRA) or modern rotational DSA.
In agreement with previous publications, the present study revealed that the
main MCA bifurcation is the most common location for aneurysms along the
MCA.35, 36, 104, 112, 221, 293 The proportion of
main MCA bifurcation aneurysms (63%)
was twice that for M1 aneurysms (31%).
The two most important reasons for the
differences in the distributions when compared to previous studies are (a) how the
main MCA bifurcation has been defined
and (b) the size of the studies. As mentioned previously, definitions have varied
between the different studies and this
was a major reason for the wide variation
in the reported distributions for MCAAs.
The sample size is certainly important especially in the case of rare locations such
as distal MCAAs. In smaller studies, these
aneurysms have not been always seen
(see Table 13).
6. DISCUSSION
Table 13.
Distribution of MCAAs in select previous studies.
No. of MCAAs
M1As
MbifAs
MdistAs
Yasargil, 1984293
184
22 (12%)
152 (83%)
10 (5%)
Rinne, 1996221
690
108 (16%)
557 (81%)
25 (4%)
1,704
241 (14%)
1,385 (81%)
78 (5%)
100
61 (61%)
39 (39%)
-
Huttunen, 2010115
1,055
133 (13%)
867 (82%)
55 (5%)
Present work49
1,309
406 (31%)
829 (63%)
74 (6%)
Dashti, 200734-36
Ulm, 2008266
Among the 242 (18%) MCAAs arising at
the origin of M1–ECBAs, there were 106
(8%) MCAAs located at the origin of large
EFBs (measuring ≥ half the diameter of the
M1). Such M1 aneurysms are easily misclassified as MCA bifurcation aneurysms.
6.4. Morphological parameters of MCAAs
6.4.1. Aneurysm wall regularity
In previous studies, aneurysm wall irregularity and the presence of protrusions
have been associated with an increased
risk of rupture.10, 88, 234 These protrusions
may develop from a weak scar at a previous rupture site.179, 248 In the present study,
the rupture rate of MCAAs with irregular
walls was six times higher than that of
MCAAs with smooth walls (64% vs. 11%,
respectively). Since this was a retrospective study, the shape of ruptured MCAAs
could have been modified by the rupture.
Some studies, however, indicate that nei-
ther the size nor the shape of aneurysms
are much affected by rupture.10, 213, 265
In one previous study, 96% of ruptured
MCAAs (including traumatic and fusiform
aneurysms) were irregular.221 In our series
of only saccular MCAAs, the frequency of
wall irregularity in ruptured aneurysms
was lower but still four times higher than
in unruptured aneurysms (78% vs. 20%).
The association between irregular wall
and aneurysm rupture was also seen in
our multivariate model.
6.4.2. The aspect ratio (AR)
It is frequently reported that the AR (aneurysm height to aneurysm neck width)
is significantly higher in ruptured than in
unruptured aneurysms.189, 233, 265, 279 The AR
has been suggested as a reliable predictor for aneurysm rupture in all locations
including the MCA. 265 Active treatment
has even been advised in aneurysms with
a high AR regardless of their maximum
size.279 The practical problem has been to
identify a threshold value for the AR which
65
6. DISCUSSION
would predict an increased rupture risk.
Some authors have suggested a threshold
value of 1.6.265 In the present study, the
rupture rate for MCAAs at AR = 1.6 was
only 58%. Thus, increasing the threshold
value would increase the specificity, but
at the cost of decreasing the sensitivity. In
the multivariate analysis, the AR was not
a statistically significant predictor for aneurysm rupture. Based on our results, we
would suggest using caution in applying
the AR as the sole indicator for selecting
unruptured MCAAs for treatment.
6.4.3. Bottleneck factor
(BNF) and height–width ratio
Two other morphological indices have
been reported as related to aneurysm rupture—namely, the BNF (aneurysm width
to neck width) and the height–width ratio.108 In our study, both the BNF as well as
the height–width ratio were higher in ruptured than in unruptured MCAAs. However, in our multivariate model, only the
height–width ratio remained statistically
significant.
In this study, the rupture rate of spherical aneurysms (height–width ratio = 1)
was lower than that of the more oval
aneurysms (height–width ratio ≠ 1). Furthermore, wide oval-shaped aneurysms
(height–width ratio < 1) had a lower rupture rate than elongated oval-shaped aneurysms (height–width ratio > 1). It has
been claimed that the geometry of IAs
affects their growth and rupture through
influencing the intra-aneurysmal hemodynamics and, ultimately, the wall shear
stress.97, 109, 264 Aneurysm geometry, however, might be just a visual representation
of the health of its wall. A more spherical
shape could reflect a rather healthy wall
growing evenly in all directions, while a
66
less spherical shape could denote some
pathological changes affecting wall
growth in one or more directions. To test
the validity of this hypothesis, we have already initiated further research projects
correlating aneurysm morphology with
histopathology.
6.4.4. The neck size
MCAAS are usually broad necked and
frequently have a branch (or branches) originating at their base.125, 204 In our
study, the neck size in ruptured MCAAs
seemed larger than in unruptured aneurysms (mean 5 vs. 3 mm), but it was not
a significant risk factor for rupture. The
neck–fundus ratio was a little higher in
M1 and distal MCA aneurysms (0.87 vs.
0.89, respectively) than in Mbif aneurysms
(0.79). The broad neck affects the aneurysm shape and the possibilities for occlusive treatment. A large neck–dome ratio is
a clear disadvantage especially for endovascular treatment.125, 204
6.4.5. Aneurysm size
General experience demonstrates that
aneurysm size affects its rupture risk.2,
132, 189, 283, 287, 288
In the present study, smallsized (<7 mm) MCAAs seldom ruptured
(15%), while large (15–24 mm) MCAAs
had the highest rupture rate (74%). Medium-sized (7–14 mm) MCAAs accounted
for the largest total number of ruptured
MCAAs (by virtue of their prevalence).
In this study, aneurysm size was identified as a risk factor for rupture in our univariate analysis, but it did not emerge as
an independent risk factor in the multivariate model. The relationship between
aneurysm size and the three independent
risk factors for rupture (irregular wall, lo-
6. DISCUSSION
cation at MCA bifurcation and less spherical geometry) determined the result of
the univariate analysis. These three independent risk factors were less frequent in
small MCAAs and most common in large
MCAAs (see Table 11 and Figure 19).
Unlike the analysis from some previous studies, we included even very small
MCAAs in our dataset (32% were ≤3 mm).
This resulted in a smaller mean size for
all MCAAs (mean = 6.6 mm) compared
to some previous studies (mean = 9.7
mm).266 The difference was evident for
both ruptured and unruptured MCAAs
(9.7 mm and 5.2 mm in our study vs. 12.3
mm and 7.5 mm in a study by Ulm et al.266).
Interestingly, two-thirds of the ruptured
MCAAs were ≤10 mm in size. This is congruent with a study by Forget et al.60 who
found that 69% (20 of 29) of the ruptured
MCAAs were ≤10 mm.
6.5. Distribution of ruptured MCAAs
The main MCA bifurcation was associated with a significantly higher aneurysm
rupture rate than other locations (38% for
MbifAs vs. 20% for M1As vs. 16% for MdistAs). Having the highest rates for both the
formation of an aneurysm and rupture at
the main MCA bifurcation suggests that
both events may be caused by the same
factors, possibly hemodynamic features
related to the flow direction and pressure
distribution along the MCA.
6.6. Focused opening of
the sylvian fissure for the
microsurgical management of MCAAs
Well-established surgical techniques
should not be considered too classic or
routine to be discussed, since continuous
improvements to imaging, operating microscopes and surgical instruments, along
with the accumulation of surgical experience, offer opportunities for technical
innovations to decrease surgical invasiveness and improve outcomes.
6.6.1. Requirements for the
focused sylvian opening
The main technical requirements for
pursuing a focused sylvian opening for
the microsurgical management of MCAAs
include (i) planning and the accurate
placement of the sylvian opening, (ii) a
slack brain, (iii) the use of high magnification and (iv) a complete understanding of
the microanatomy of the clipping field.
6.6.1.1. Accurate placement of
the sylvian opening
The sylvian opening is usually placed
directly over the clipping field such that
there is a short perpendicular path to the
clipping field. Sometimes, the relation of
the aneurysm dome to the clipping field
necessitates choosing a more oblique
path in order to achieve safer access and/
or a more favorable surgical view. This
is usually possible by placing the sylvian opening either a little more proximal
or more distal along the SF. In particular,
for ruptured MCAAs, the approach angle
should be such that the aneurysm dome
and rupture site remain hidden and untouched until proximal control has first
67
6. DISCUSSION
been established. Free-handling of the
3D reconstruction of the CTA data is very
helpful in choosing the possible approach
angles. For some unruptured MCAAs, the
SF can be opened directly over the aneurysm (see Videos 4 and 5).
6.6.1.2. Slack brain
With a relaxed brain, an MCAA can be
approached and clipped through a small
sylvian opening with little or no brain
retraction. Moreover, excessive removal
of the skull base is not needed when the
brain is soft and there is sufficient room
to maneuver. Achieving a relaxed brain
requires adequate neuroanesthesia techniques214, good venous outflow by elevating the head above the heart level without excessive tilt and the intraoperative
release of CSF.
6.6.1.3. High magnification (9x or
more)
High magnification improves safety and
precision when operating in small, narrow
and deep gaps. With better visual control
and a smaller operative field, the chance
for accidental injuries decreases. For the
small sylvian opening, we recommend
using the highest available magnification
to save small perforators. The drawback
of high magnification is the difficulty in
anatomical orientation. This can be overcome by careful study of preoperative angiograms—in particular, 3D reconstructions—and experience.
6.6.1.4. Understanding intraoperative anatomy
The complex anatomy of the MCA together with operating under high magnification through a narrow sylvian opening
require good recognition of the intraoperative patient-specific anatomy, especially
the surgical view of the clipping field. One
68
needs to know the locations of all vascular
structures, including the branches hidden
by the aneurysm dome. Again, preoperative planning and 3D images can help
to avoid branches being caught inside
the clip or accidentally injuring branches
during the clipping of the aneurysm neck.
Moreover, preoperative images should be
checked for calcifications in the parent
MCA or in the aneurysm, since they may
affect the use of temporary or permanent
clips at these sites.
It is important to accurately classify
MCAAs before surgery as special considerations are required for different types of
MCAAs.34-36, 49, 160
6.6.2. Troubleshooting
In this section, we present some of the
typical problems which can be encountered during the microsurgical clipping of
MCAAs through a small sylvian opening,
and recommend simple practical strategies on how to manage these difficulties.
6.6.2.1. Premature rupture of the
MCAA
Most premature aneurysm ruptures occur during the dissection and clipping of
the aneurysm.161 Bleeding can usually be
controlled with suction and/or compression of the bleeding site with a small cottonoid, followed by temporary clipping
of the already identified parent artery. If
bleeding is so profuse that suction fails to
clear the operative field, intravenous adenosine can be used to induce a short cardiac arrest, during which the operative field
is cleared and a temporary clip is placed
on the parent MCA or the aneurysm neck
is directly clipped.171, 191, 214 It is important
not to hurry and to avoid applying clips
blindly, since this may result in the further
6. DISCUSSION
tearing of the rupture site or occlusion of
adjacent branches.
ter clipping to enable better inspection of
the entire clipping field.
A spare suction line and adenosine
should be kept ready before opening the
SF, especially for ruptured aneurysms and
when the aneurysm dome is obstructing
the view towards the clipping field. In our
experience, temporary clipping of the parent MCA before dissecting and clipping of
the aneurysm neck significantly decreases
the incidence of premature rupture.
Although visual inspection can detect
some aneurysm remnants or vessel compromise (see Video 7), it is not sufficient.172,
257
ICG provides for the safe and rapid assessment of the clipping, and its resolution is high enough to assess even small
perforators. However, visualization is limited to the exposed vessels and can be diminished by atherosclerosis in the vessel
wall and blood clots in the subarachnoid
space.81, 210, 211 Doppler US detects flow in
larger arteries, and intraoperative DSA is
especially helpful for giant aneurysms and
bypass surgery.
6.6.2.2. Clips may get entangled
in the small field
The temporary and permanent clips can
get entangled when applied close to each
other in such a small surgical field. Careful
selection of the shape of the temporary
clips—that is, curved versus straight—
provides more room for permanent clips.
In addition, inserting a small cottonoid
between adjacent clips can help during
the exchange of clips (see Videos 1 and
6). We prefer short clip applicators when
operating on most MCAAs, since the clips
are easier to manipulate with short applicators when working close to the surface.
6.6.2.3. Confirming the aneurysm clipping
Clipping is ideal when the entire aneurysm is excluded from circulation while all
of the surrounding arteries are left patent.
The best time to confirm the adequacy of
the clipping is during surgery. After the
initial clipping, the clipping field is visually explored for any vessel compromise
and/or aneurysm neck remnants. The clip
can then be reapplied or exchanged, and
extra clips are added if necessary. The aneurysm can be reshaped by bipolar coagulation (see Video 6), and pulled carefully deeper into the clip with suction or
microforceps (see Videos 1 and 7). In large
aneurysms, the dome can be resected af-
6.6.2.4. Anatomical orientation
may be lost in the narrow field
Maintaining full anatomical orientation
is necessary during all steps of arachnoid dissection and aneurysm clipping.
Misplacement of the arachnoid opening
or unexpected findings can disturb anatomical orientation. Rechecking images,
especially 3D reconstructions, instead of
searching blindly inside the SF, can readjust orientation and improve the pairing
of operative findings with the imaging
data (see Video 6).
6.6.2.5. Large ICH and/or massive
SAH
It is safer to evacuate an ICH after securing the ruptured aneurysm (see Video 3).
Fenestration of the lamina terminalis and/
or opening the Liliequist membrane and
the basal cisterns are effective in releasing
CSF and relaxing the brain early before
opening the SF (see Video 7). However, if
despite all efforts the brain remains tight,
a small portion of the ICH far away from
the aneurysm dome can be removed
through a small cortisectomy even before
securing the aneurysm.
69
6. DISCUSSION
When the sylvian cistern is full of blood
clots, the initial steps of the dissection can
be very tedious. Visualization through the
blood-filled arachnoid can be improved
with profuse water irrigation of the subarachnoid space using a handheld syringe. After SAH, the arachnoid bands often become opaque and tougher, making
their dissection more difficult. Sharp dissection decreases the risk of injury to the
structures of the SF and/or the premature
rupture of the aneurysm.
6.6.2.6. Large/giant aneurysms
needing vascular bypass
When vascular compromise of the MCA
is anticipated, revascularization should be
considered. In such situations, the superficial temporal artery (STA) is preserved and
prepared for possible bypass.147 The SF is
initially opened locally overlying the clipping field and, then, the opening can be
easily extended as much as needed. The
clipping field is evaluated for the possibility and safety of direct clipping of the
aneurysm; but, when not possible, the
MCAA is trapped after performing a bypass (see Video 8).
6.6.3. Advantages of the focused sylvian opening
The compilation of temporary and definite clipping in one small surgical field under high magnification results in benefits
such as less invasiveness, but also speed
and safety. Being close in the same field,
the time needed for the clip exchange is
minimized, thus shortening the temporary
clipping time. In addition, while gradually
removing a temporary clip, the clipping
field can be concurrently checked for any
potential bleeding. A small surgical field
makes it easier and more practical to continue operating under high magnification,
ensuring better visual control throughout
70
the surgery. The limited sylvian dissection,
with the most direct and safest approach
to the MCAA, saves operating time and
decreases the risk of iatrogenic injury to
the surrounding neurovascular structures
(see Videos 1–8).
6.7. Limitations of the
studies
Reports addressing aneurysm rupture
risk factors, including this report, have
inherent limitations in not including all
possible rupture risk factors given that
some have not yet been identified. Therefore, integration rather than contradiction
should be practiced when interpreting
the results.
The evidence from all reports on risk
factors for aneurysm rupture is still insufficient to definitively characterize those
aneurysms which will certainly rupture.
There is no simple cut-off value for any
of the aneurysm-related characteristics
(such as size) which would subdivide unruptured MCAAs into those which need
to be actively treated and those which
should be left untouched.
6.8. The present state of
the management of IAs
In 1996, Drake, Peerless and Hernesniemi
said, “We continue to enjoy placing the
perfect clip around the base of those
deadly sacks.”45 Although both neurosurgeons and neurointerventionists praise
the way they manage IAs and do their best
to improve their results, patients usually
have their own preferences and needs.
Patients with SAH and those carrying unruptured IAs would be happy to be cured
without having their skulls opened; how-
6. DISCUSSION
ever, it is not always possible for patients
to choose their preference. In developing
countries, most patients with IAs cannot
afford the high cost of endovascular treatment. In addition, it is very dangerous for
patients with a space-occupying ICH from
a ruptured IA to postpone surgical evacuation of the ICH until the ruptured IA is
endovascularly coiled. On the other hand,
some very sick and elderly patient might
be generally unfit for surgery. Thus, both
treatment modalities are complementary
in helping patients to balance their preferences and needs.
6.9. Future trends
Around 2% of the whole population
harbors IAs which, in most cases, will not
rupture and usually remain asymptomatic throughout their life. The real fear
from IAs lies in the possibility of rupture.
Although rupture is not the classic fate
for IAs, it is the most catastrophic result,
which is associated with a 50% mortality
rate even with the best available management. Thus, it is not logical to screen the
entire population for IAs since most do
not have them. Furthermore, treating all
diagnosed IAs is unnecessary since most
of them will never harm the patients. Despite these factors, waiting to treat IAs
until they rupture is not justifiable, since,
by then, most patients would have been
lost or disabled. Research concerning IAs
is attempting to find innovative solutions
for these clinical dilemmas regarding the
diagnosis and management of IAs.
The identification of patients with IAs
is the cornerstone for initiating early clinical management before rupture. Imaging
the entire adult population—even in Finland—to identify all patients with IAs is
too expensive, time consuming and may
carry some risks of exposure to radiation
unless magnetic resonance angiography
(MRA) is used. Today, most unruptured
IAs are diagnosed either incidentally or
during the screening of relatives of patients with IAs. Indentifying the genetic
factors associated with IAs could make
screening for them as fast and as smooth
as a simple blood test, resulting in a higher percentage of patients with IAs being
identified early.
In addition to the simple diagnosis of
the presence of IAs, knowing the degree of resilience of the aneurysm wall
to rupture is also necessary. All available
data correlating the risk of rupture of IAs
to morphological and/or topographical characteristics are suggestive rather
than conclusive at this stage. Research is
currently being carried out to correlate
some morphological characteristics of IAs
with the histology of the IA wall in order
to determine more reliable indicators for
the state of health of the aneurysm wall.
Furthermore, transferring newly developed investigative tools, such as the new
ultra-high-field MRI, to the clinical setting
would probably enable us to examine the
aneurysm wall for weak spots. This would
allow for more reliability when classifying
IAs as either stable or rupture-prone.
At the present time, there is no management strategy for IAs that is 100% risk free.
Thus, IAs should be carefully selected for
treatment based on their risk of rupture.
The microsurgical management of IAs is
progressing by being less invasive, and
minimizing the size of craniotomy and the
area of exposure of the brain and normal
vessels. New endovascular techniques
and devices have enabled the management of some previously inoperable IAs,
while extending treatment to normal
innocent vessels when placing stents
and flow diverters into parent arteries.
Adopting healthier lifestyles by quitting
smoking, eliminating excessive alcohol
71
6. DISCUSSION
consumption and better controlling hypertension might prevent the development or growth of many IAs or decrease
the risk of IA rupture.
With progress in genetic studies, it
may become possible to develop targeted pharmaceutical therapies that would
reverse the process of IA formation. Advances in endovascular technology might
provide for the development of new
polymer-coated stents and flow diverters which do not require cotreatment
with antiplatelet drugs. Furthermore, it
is not impossible that some of today’s
science fiction would result in scientific
breakthroughs in the future, whereby we
witness nanorobots navigating throughout our cerebral arteries to treat IAs or
strengthen their walls.
72
7. CONCLUSIONS
7. Conclusions
I)
Studying the angioarchitecture of the MCA helps to define its branching pattern
and to accurately localize the main MCA bifurcation. Defining the main MCA bifurcation as the origin of M2s is practical for the study of preoperative angiograms.
Applying the four-group classification facilitates the accurate grouping of MCAAs
by keeping M1–ECBAs, the most frequently misclassified group of MCAAs, in mind.
This helps the neurosurgeon to improve the operative outcome.
II) The morphology and topography of MCAAs can be useful when estimating their
risk of rupture. The location at the main MCA bifurcation, the wall irregularity and a
less spherical geometry were independently associated with an increased rupture
rate. These risk factors were least prevalent in small MCAAs and most common in
large MCAAs which had the highest rupture rate.
III) The focused opening of the sylvian fissure for the microsurgical management of
MCAAs is a less invasive alternative to the classic wide opening of the sylvian fissure.
The main advantage of this technique is that it minimizes the area of the brain and
vessels manipulated, while maintaining the safety and efficacy of the procedure.
A 3D image-based anatomic orientation, a clipping field–focused surgical plan, a
slack brain and a high magnification are basic requirements for this approach.
73
LIST OF SUPPLEMENTARY VIDEOS
List of supplementary videos of the focused
sylvian opening for the microsurgical management of MCAAs
The supplementary CD includes eight videos showing the focused sylvian opening
for the microsurgical management of MCAAs. These videos contain the following:
1.
The clipping of an unruptured MCA bifurcation aneurysm through a laterally
placed focused sylvian opening on the right side (7:53 minutes).
2.
The clipping of an unruptured MCA bifurcation aneurysm through a directly
placed focused sylvian opening on the right side (8:04 minutes).
3.
The clipping of a ruptured MCA bifurcation aneurysm with a temporal intracerebral hematoma on the right side (7:37 minutes).
4.
The clipping of a bilateral unruptured M1–ECBA (8:48 minutes).
5.
The clipping of an unruptured distal MCA aneurysm on the right side (7:13 minutes).
6.
The clipping of an unruptured M1–LSAA on the right side (9:49 minutes).
7.
The clipping of a ruptured MCA bifurcation aneurysm with a SAH on the left side
(7:10 minutes).
8.
The clipping of a giant M1–ECBA on the left side (7:17 minutes).
All of the videos were recorded during microneurosurgical operations performed by
Professor Juha Hernesniemi on MCA aneurysms from 2011 to 2013 at the Department
of Neurosurgery, Helsinki University Central Hospital, Helsinki, Finland.
74
ACKNOWLEDGMENTS
Acknowledgments
This research was carried out at the Department of Neurosurgery, Helsinki University Central Hospital, where I worked as a Neurovascular Fellow under Professor Juha
Hernesniemi from 2010 to 2013. My work was financially supported by CIMO and the
Ehrnrooth Scholarships, which are gratefully acknowledged. I wish to express my gratitude to the following co-workers and friends for their support throughout this time.
I am deeply indebted to my fellowship mentor, Juha Hernesniemi, who assigned the
topic of my thesis and sketched the initial plan for this work. I am very grateful to him
for all of his advice and encouragement and his belief in me from the very start. His
words, “find your way,” ignited my mind and taught me to be independent whenever I
faced obstacles at the beginning of this work. His hard work and strong will were motivating forces for me, spurring me to increase my efforts, and have made him my hero.
Without his experience and innovations in the field of microneurosurgery, this work
would not have come to life.
I owe the deepest gratitude to my supervisor, Mika Niemelä, for his continuous support and invaluable guidance during my work. He saved me a lot of time by always
being available and by efficiently reviewing my work quickly. He pushed me forward
and set appropriate timelines, which kept the work on track without periods of deceleration. His good sense of humor, even when providing his constructive criticism,
improved the working atmosphere markedly. I am very appreciative of his intelligence
and his continual offers of help even before being asked.
I give my heartfelt thanks to my other supervisor, Martin Lehečka, for teaching me
how to write scientifically. He was quite patient and carefully read each of my early
manuscripts, providing valuable comments and suggestions which have greatly improved their readability. I certainly benefited from numerous lengthy discussions with
him, from which I adopted his scientific way of thinking. His insightful ideas markedly
improved all aspects of this work, and his experience and patience provided an initial
forward thrust to my work.
I am very grateful to my coauthors—Riku Kivisaari, Juri Kivelev, Felix Goehre and Romain Billon-Grand—for their valuable contribution to these studies and to each of the
manuscripts. I am especially thankful to Hanna Lehto for assisting me from the early
steps of my work. She provided me with the required database and helped me from
the start in my journey with statistics. I have benefited from her talent for expressing
complex ideas in a few simple words and with shortening sentences. She was the best
example for how a busy researcher could still help others. I gratefully acknowledge
Behnam Rezai, who, besides his input into this work, helped tremendously in all steps
of registration at the university and in the selection of the required courses. He made
many telephone calls to find answers for my frequent queries. Sharing my work with
such friends provided me with much strength.
I am also very thankful to the entire staff from neurosurgery and anesthesiology for
their friendly attitudes, which created such a pleasant working environment.
75
ACKNOWLEDGMENTS
I would like to acknowledge Virpi Hakala, Eveliina Salminen and Jessica Peltonen for
their efforts in managing all of the official documents required for my stay in Finland
and for completing my work.
I am very grateful to Ville Vuorinen and Arto Haapanen, the formal reviewers of my
thesis, for their excellent feedback and helpful comments all of which markedly improved this work. I would like also to sincerely thank Saruhan Cekirge for his informal
review and revisions. And, I gratefully acknowledge Vanessa Fuller for her skillful language revisions to my thesis.
My warmest thanks go to all of my friends, colleagues and the other neurovascular
fellows. In particular, I extend my gratitude to Amit Chakrabarty, Anna Piippo, Essam
Abdelhameed, Ferzat Hijazy, Hideki Oka, Hugo Andrade, Jouke van Popta, Makhkam
Makhkamov, Masaki Morishige, Miikka Korja, Minna Oinas, Tetsuaki Sugimoto and Zia
Akram for sharing funny moments and profound conversations which were very helpful in coping with the stress of our work.
Last, but not least, I would like to thank my parents, brothers, wife, sons and daughter
for their unlimited love and support which strengthened my resolve to complete this
work. I feel indebted to them all, especially my wife, Reham, who willingly accepted
carrying all of the responsibilities for our children and sacrificed her time and efforts in
order to allow me the time to concentrate so completely on my work. I cannot find the
words to express my gratitude.
In Helsinki, January 2014
76
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Saccular Middle Cerebral Artery Aneurysms

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