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Gianni Boris Bradac

Cerebral
Angiography
Normal Anatomy and
Vascular Pathology
Second Edition

123


Cerebral Angiography


Gianni Boris Bradac

Cerebral Angiography
Normal Anatomy and Vascular
Pathology
Second Edition


Gianni Boris Bradac, MD
Past director of Neuroradiology
Professor Emeritus of Neuroradiology
Department of Neuroscience
University of Turin
Ospedale Molinette
Turin
Italy
With the collaboration of


Edoardo Boccardi MD
Director of Neuroradiology
Ospedale Niguarda “Ca Granda”
Milan
Italy

ISBN 978-3-642-54403-3
ISBN 978-3-642-54404-0
DOI 10.1007/978-3-642-54404-0
Springer Heidelberg New York Dordrecht London

(eBook)

Library of Congress Control Number: 2014937448
© Springer-Verlag Berlin Heidelberg 2014
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Preface

This is a revised and enlarged edition of Cerebral Angiography published in
2011. The first part of the book describes the normal anatomy of the cerebral
arteries, with attention given to their embryological development, and its possible anomalies, their morphological aspect, their function, and their vascular
territories. The intraorbital and extracranial vascularization is also considered. One chapter is dedicated to the embryological development and to the
normal anatomy of the intra- and extracranial veins. This first part of the book
will serve as a basis for the correct interpretation of pathological processes
and their clinical relevance, which will be covered in the second part of the
book. Among the pathologies considered are vascular abnormalities, including aneurysms; the different types of angiomas and fistulas; atherosclerotic
and non-atherosclerotic stenosis and occlusion of the cerebral vessels; venous
thrombosis and other correlated venous pathologies; and intraorbital and
extracranial vascular malformations. The pathogenesis of the pathological
processes and their different morphological and dynamic aspects, influencing
the clinical aspects and the therapy, are described. While the emphasis
throughout is on the diagnostic value of cerebral angiography, many examples of endovascular treatment in different pathological situations are also
presented, with discussion about indications, risks, and results.
We hope that this edition, also, will be of practical use for all the physicians involved in the study of the cerebral vessels and treatment of vascular
pathology.

Historical Aspects
In July 1927, Prof. Egas Moniz, director of the neurological clinic in Lisboa,

presented at the congress of the Neurological French Society in Paris his first
experiences with a method to study the cerebral vessels that he called
“L’encephalographie arterielle.” The interest for this new method called later
“cerebral angiography” was great. Among the several neurological authorities present in the congress, we report the comment of Prof. Babinski:
Le radiographies qui vient de presenter E. Moniz sont remarquables. Si les observations ulterieures établissent définitivement que les injections auxquelles il a recours
sont inoffensives, tous les neurologistes seront reconnaissants a notre éminent collégue de leur avoir procuré un nouveau moyen pouvant permettre de localiser des
tumeurs intracraniennes dont le siège est souvent si difficile a déterminer.

v


vi

Preface

Since then, great progresses have been made, starting with the introduction of the catheter technique (Seldinger 1953), the subtraction (Ziedses des
Plantes 1963) followed by the introduction of more and more suitable catheters, guide wires, and less toxic contrast media. All these aspects along with
the improved technological equipment have characterized the evolution of
the cerebral angiography which has become a very important neuroradiological diagnostic method. Certainly, the evolution of new methods such as
angio-CT, angio-MR, and ultrasounds allows to replace today in many cases
cerebral angiography. However, every time the diagnosis is not sufficiently
clear or finer details are required to understand the clinical symptoms or to
plan the therapy, especially when an endovascular approach is considered,
angiography remains today the method of choice.

References
Babinski J (1927) Revue Neurologique 34:72
Moniz E (1927) Revue Neurologique 34:72
Seldinger SI (1953) Acta Radiol (Stock) 39:368
Ziedses des Plantes BG (1963) Acta Radiol Diagn 1:961


Turin, Italy

G.B. Bradac


Acknowledgements

This book reflects the work done and the experience gained in the
Neuroradiological Units at the Molinette Hospital of Turin University, at
Niguarda Hospital in Milan, and Santa Croce Hospital in Cuneo. It would not
have been possible without the involvement of the members (doctors, technologists, nurses, etc.) working in different times in these units as well as
the members of the anesthesiological, neurosurgical, maxillary surgery,
otolaryngology and stroke units.
To all these persons we would like to express our sincere thanks.
We are especially grateful to M. Coriasco, B.Sc. (clinical technologists)
for his help with the technical aspects concerning the manuscript and for the
image processing to improve the quality of the figures, Mr. G. Hippmann for
his effort to correctly represent the schematic drawings and Mr. P. Prejith for
his work in the preparation of this 2nd edition.
Finally we would like to express our gratefulness to all members of
Springer-Verlag, especially C.D. Bachem, Mr. G. Karthikeyan, Dr. U. Heilmann
and Dr. Freyberg.
G.B. Bradac
E. Boccardi

vii


Contents


1

Aortic Arch and Origin of the Cranial Cerebral Arteries. . . .

1

2

Carotid Artery (CA) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1 Cervical Segment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2 Petrous Segment of ICA . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3 Cavernous Segment of ICA . . . . . . . . . . . . . . . . . . . . . . . . .
2.4 Supraclinoid Segment of ICA . . . . . . . . . . . . . . . . . . . . . . .
2.4.1 In the Ophthalmic Segment Arise the Ophthalmic
Artery and Superior Hypophyseal Arteries . . . . . . .
2.4.2 In the Communicating Segment Arises the PcomA . .
2.4.3 In the Choroidal Segment Arise the Anterior
Choroidal Artery and Often Perforators
Directly from the ICA . . . . . . . . . . . . . . . . . . . . . . .
2.5 Congenital Anomalies of the ICA . . . . . . . . . . . . . . . . . . . .

9
9
10
10
12

3


External Carotid Artery. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1 Superior Thyroid Artery . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2 Lingual Artery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.3 Facial Artery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.4 Ascending Pharyngeal Artery . . . . . . . . . . . . . . . . . . . . . . .
3.5 Occipital Artery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.6 Posterior Auricular Artery . . . . . . . . . . . . . . . . . . . . . . . . . .
3.7 Internal Maxillary Artery . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.7.1 Proximal Branches . . . . . . . . . . . . . . . . . . . . . . . . .
3.7.2 Masticator Space . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.7.3 Distal IMA. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.7.4 The Terminal Branch . . . . . . . . . . . . . . . . . . . . . . . .
3.8 Superficial Temporal Artery . . . . . . . . . . . . . . . . . . . . . . . .
3.9 Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.9.1 Vascular Malformations . . . . . . . . . . . . . . . . . . . . .
3.9.2 Hemangiomas . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.9.3 Juvenile Angiofibromas . . . . . . . . . . . . . . . . . . . . . .
3.9.4 Paragangliomas (Chemodectomas) . . . . . . . . . . . . .
3.9.5 Meningiomas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.9.6 General Considerations in Endovascular
Treatment in the ECA Area . . . . . . . . . . . . . . . . . . . .

12
18

19
21
27
27
28

28
29
32
32
32
34
36
37
37
38
38
38
39
43
43
45
47

ix


x

Contents

4

Anterior Cerebral Artery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1 Precommunicating Segment . . . . . . . . . . . . . . . . . . . . . . . .
4.2 Distal Segments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

4.2.1 Infracallosal Segment . . . . . . . . . . . . . . . . . . . . . . .
4.2.2 Precallosal Segment . . . . . . . . . . . . . . . . . . . . . . . .
4.2.3 Supracallosal Segment . . . . . . . . . . . . . . . . . . . . . .
4.2.4 Cortical Branches . . . . . . . . . . . . . . . . . . . . . . . . . .
4.3 Anatomical Variations . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.4 Vascular Territories . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.5 Angiogram . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

55
55
56
56
56
57
57
58
60
61

5

Middle Cerebral Artery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.1 M1 Segment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.2 M2, M3, and M4 Segments . . . . . . . . . . . . . . . . . . . . . . . . .
5.3 Anatomical Variations . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.4 Vascular Territories . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.5 Angiogram . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

67
67

68
72
72
77

6

Extra- and Intracranial Vertebrobasilar Sector . . . . . . . . . . . .
6.1 Extracranial Sector . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
6.1.1 Branches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
6.2 Intracranial Sector . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
6.2.1 Branches of the VA . . . . . . . . . . . . . . . . . . . . . . . . .
6.2.2 Branches of the Basilar Artery . . . . . . . . . . . . . . . .
6.2.3 Cortical–Subcortical Branches
of the Cerebellar Arteries . . . . . . . . . . . . . . . . . . . . .
6.2.4 Variants of Vertebral and Basilar Arteries . . . . . . . .

79
79
79
80
80
83
87
88

7

Posterior Cerebral Artery. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.1 P1 Segment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

7.2 P2 Segment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.3 P3 Segment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.4 P4 Segment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.5 Anatomical Variations . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.6 Vascular Territories . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7.7 Angiogram . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

95
95
97
97
97
98
98
100

8

Vascular Territories . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

105

9

Cerebral Veins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
9.1 Supratentorial Cerebral Veins . . . . . . . . . . . . . . . . . . . . . . .
9.1.1 The Superficial System . . . . . . . . . . . . . . . . . . . . . .
9.1.2 The Deep System. . . . . . . . . . . . . . . . . . . . . . . . . . .
9.2 Infratentorial Cerebral Veins (Veins of the Posterior Fossa) . . .
9.2.1 Superior Group . . . . . . . . . . . . . . . . . . . . . . . . . . . .

9.2.2 Anterior Petrosal Group . . . . . . . . . . . . . . . . . . . . .
9.2.3 Posterior Tentorial Group . . . . . . . . . . . . . . . . . . . .
9.3 Dural Sinuses. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
9.3.1 Superior Sagittal Sinus (SSS) . . . . . . . . . . . . . . . . .
9.3.2 Inferior Sagittal Sinus (ISS) . . . . . . . . . . . . . . . . . .

109
110
110
112
119
120
121
124
124
125
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Contents

xi

9.3.3 Straight Sinus (SS) . . . . . . . . . . . . . . . . . . . . . . .
9.3.4 Occipital Sinus (OS), Marginal Sinus (MS) . . . .
9.3.5 Transverse Sinus (TS) . . . . . . . . . . . . . . . . . . . . .
9.3.6 Sigmoid Sinus (SiSs) . . . . . . . . . . . . . . . . . . . . . .
9.3.7 Superior Petrosal Sinus (SPS) . . . . . . . . . . . . . . .
9.3.8 Inferior Petrosal Sinus (IPS) . . . . . . . . . . . . . . . .
9.3.9 Sphenoparietal Sinus (SpS) . . . . . . . . . . . . . . . . .

9.3.10 Cavernous Sinus (CS) . . . . . . . . . . . . . . . . . . . . .
9.3.11 Superior Ophthalmic Vein (SOV) . . . . . . . . . . . .
9.3.12 Inferior Ophthalmic Vein (IOV) . . . . . . . . . . . . .

125
127
127
128
128
128
130
130
133
133

10

Extracranial Venous Drainage . . . . . . . . . . . . . . . . . . . . . . . . . .
10.1 Orbital Veins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
10.2 Facial Veins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
10.3 Retromandibular Vein . . . . . . . . . . . . . . . . . . . . . . . . . . .
10.4 Posterior Auricular and Occipital Veins . . . . . . . . . . . . . .
10.5 Deep Cervical Vein . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
10.6 Venous Plexus of the Vertebral Artery . . . . . . . . . . . . . . .
10.7 Emissary Veins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
10.8 Diploic Veins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
10.9 Internal Jugular Vein . . . . . . . . . . . . . . . . . . . . . . . . . . . .

135
135

135
136
136
136
136
136
137
137

11

Aneurysms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
11.1 Incidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
11.2 Type and Location . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
11.3 Macroscopic Appearance . . . . . . . . . . . . . . . . . . . . . . . . .
11.4 Pathogenesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
11.5 Clinical Presentation . . . . . . . . . . . . . . . . . . . . . . . . . . . .
11.6 Aneurysm Location . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
11.6.1 Extracranial ICA Aneurysms . . . . . . . . . . . . . . .
11.6.2 Petrous Segment ICA Aneurysms . . . . . . . . . . .
11.6.3 ICA Paraclinoid Aneurysms . . . . . . . . . . . . . . .
11.6.4 Aneurysms of the Communicating
and Choroidal Segments . . . . . . . . . . . . . . . . . .
11.6.5 Aneurysms of the Carotid Bifurcation . . . . . . . .
11.6.6 Anterior Cerebral Artery Aneurysms . . . . . . . . .
11.6.7 MCA Aneurysms . . . . . . . . . . . . . . . . . . . . . . . .
11.6.8 Aneurysms of the Posterior Circulation . . . . . .
11.7 Dissecting Aneurysms . . . . . . . . . . . . . . . . . . . . . . . . . . .
11.8 Fusiform and Giant Aneurysms . . . . . . . . . . . . . . . . . . . .
11.9 Diagnosis and Treatment . . . . . . . . . . . . . . . . . . . . . . . . .

11.10 Unruptured Aneurysms . . . . . . . . . . . . . . . . . . . . . . . . . .
11.11 Negative Angiograms in Patients with SAH . . . . . . . . . .
11.12 Vasospasm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
11.13 Aneurysms in Children . . . . . . . . . . . . . . . . . . . . . . . . . .

139
139
139
139
139
140
141
141
141
141
142
143
147
147
148
156
160
162
163
164
164
166

Vascular Malformations of the Central Nervous System . . . . .
12.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

12.2 Classification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

167
167
167

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Contents

12.3

Arteriovenous Malformations . . . . . . . . . . . . . . . . . . . . .
12.3.1 Pathogenesis and Pathology . . . . . . . . . . . . . . . .
12.3.2 Incidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
12.3.3 Clinical Relevance . . . . . . . . . . . . . . . . . . . . . . .
12.3.4 Location . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
12.3.5 Diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
12.3.6 Treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Cavernous Malformations (Cavernomas) . . . . . . . . . . . .
12.4.1 Pathology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
12.4.2 Incidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
12.4.3 Location . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
12.4.4 Diagnosis and Clinical Relevance . . . . . . . . . . .
Capillary Malformations (Telangiectasias) . . . . . . . . . . .
Developmental Venous Anomaly (DVA) . . . . . . . . . . . . .
12.6.1 Pathology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

12.6.2 Incidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
12.6.3 Diagnosis and Clinical Relevance . . . . . . . . . . .
Central Nervous System Vascular Malformation:
Part of Well-Defined Congenital
or Hereditary Syndromes. . . . . . . . . . . . . . . . . . . . . . . . .
12.7.1 Rendu–Osler Syndrome
(Hereditary Hemorrhagic Telangiectasias) . . . .
12.7.2 Sturge–Weber Syndrome
(Encephalotrigeminal Angiomatosis) . . . . . . . .
12.7.3 Wyburn–Mason Syndrome . . . . . . . . . . . . . . . .
12.7.4 Klippel–Trenaunay–Weber Syndrome . . . . . . . .
Arteriovenous Shunts Involving the Vein of Galen . . . . .

190
192
192
192

13

Dural Arteriovenous Fistulas . . . . . . . . . . . . . . . . . . . . . . . . . . . .
13.1 Incidence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
13.2 Pathology and Pathogenesis. . . . . . . . . . . . . . . . . . . . . . .
13.3 Clinical Relevance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
13.4 Location . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
13.5 Diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
13.6 Classification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
13.7 Situations Deserving More Detailed Consideration . . . .
13.8 DAVFs in Pediatric Patients. . . . . . . . . . . . . . . . . . . . . . .


199
199
199
200
200
200
200
201
238

14

Arteriovenous Fistulas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
14.1 Carotid–Cavernous Fistulas . . . . . . . . . . . . . . . . . . . . . . .
14.1.1 Clinical Presentation . . . . . . . . . . . . . . . . . . . . .
14.1.2 Diagnosis and Treatment . . . . . . . . . . . . . . . . . .
14.2 Vertebral Arteriovenous Fistulas . . . . . . . . . . . . . . . . . . .
14.2.1 Clinical Presentation . . . . . . . . . . . . . . . . . . . . .
14.2.2 Diagnosis and Treatment . . . . . . . . . . . . . . . . . .

241
241
241
241
244
244
244

15


Ischemic Stroke. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
15.1 Pathology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
15.2 Location . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

247
247
248

12.4

12.5
12.6

12.7

12.8

167
167
168
168
169
169
182
186
186
186
188
188
189

190
190
190
190

190
190


Contents

xiii

15.3
15.4

Mechanisms Leading to Ischemia . . . . . . . . . . . . . . . . . .
Mechanism of Ischemia of the Anterior Circulation . . . .
15.4.1 Carotid Artery . . . . . . . . . . . . . . . . . . . . . . . . . .
15.4.2 Middle Cerebral Artery . . . . . . . . . . . . . . . . . . .
15.4.3 Anterior Choroidal Artery . . . . . . . . . . . . . . . . .
15.4.4 Anterior Cerebral Artery . . . . . . . . . . . . . . . . . .
15.4.5 Lacunar Infarcts in the Anterior Circulation . . .
Posterior Circulation . . . . . . . . . . . . . . . . . . . . . . . . . . . .
15.5.1 Subclavian and Innominate Arteries . . . . . . . . .
15.5.2 Vertebral Artery . . . . . . . . . . . . . . . . . . . . . . . . .
15.5.3 Basilar Artery . . . . . . . . . . . . . . . . . . . . . . . . . . .
15.5.4 Cerebellar Arteries . . . . . . . . . . . . . . . . . . . . . . .
15.5.5 Border-Zone Infarcts . . . . . . . . . . . . . . . . . . . . .
15.5.6 Posterior Cerebral Artery . . . . . . . . . . . . . . . . . .

Changes in the Venous Sector . . . . . . . . . . . . . . . . . . . . .
Collateral Circulation. . . . . . . . . . . . . . . . . . . . . . . . . . . .
15.7.1 Collateral Circulation Between
Intracranial Arteries . . . . . . . . . . . . . . . . . . . . . .
15.7.2 Collateral Circulation Between Extracranial
and Intracranial Arteries . . . . . . . . . . . . . . . . . .
15.7.3 The Vertebrobasilar Sector Deserves a Few
More Considerations . . . . . . . . . . . . . . . . . . . . .

248
249
249
255
266
266
268
269
269
270
270
275
276
278
285
286

16

Spontaneous Dissection of Carotid and Vertebral Arteries . .
16.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

16.2 Pathology and Pathogenesis. . . . . . . . . . . . . . . . . . . . . . .
16.3 Location . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
16.4 Morphological Diagnostic Appearance . . . . . . . . . . . . . .
16.5 Clinical Relevance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
16.6 Treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
16.7 Dissection and Dissecting Aneurysms in Children . . . . .

289
289
289
290
290
291
294
296

17

Other Nonatherosclerotic Vasculopathies. . . . . . . . . . . . . . . . . .
17.1 Great Variety of Diseases . . . . . . . . . . . . . . . . . . . . . . . . .
17.2 Cerebrovascular Fibromuscular Dysplasia . . . . . . . . . . .
17.2.1 Pathology and Etiopathogenesis . . . . . . . . . . . .
17.2.2 Diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
17.2.3 Clinical Relevance . . . . . . . . . . . . . . . . . . . . . . .
17.3 Moyamoya Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
17.3.1 Pathology and Etiopathogenesis . . . . . . . . . . . .
17.3.2 Diagnosis and Clinical Relevance . . . . . . . . . . .
17.4 Takayasu’s Arteritis . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
17.5 Sneddon’s Syndrome . . . . . . . . . . . . . . . . . . . . . . . . . . . .
17.6

Reversible Cerebral Vasoconstriction
Syndrome (RCVS) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
17.7 Primary Angiitis of the CNS (PACNS) . . . . . . . . . . . . . .
17.8 Autosomal Dominant Arteriopathy
with Subcortical Infarct and Leucoencefalopathy
(CADASIL) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
17.9 Migraine and Stroke . . . . . . . . . . . . . . . . . . . . . . . . . . . .

305
305
305
306
306
309
309
310
310
310
312

15.5

15.6
15.7

286
287
288

314

314

315
315


xiv

Contents

18

Cardiac Diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

317

19

Arterial Occlusive Diseases in Children . . . . . . . . . . . . . . . . . . .

321

20

Cerebral Venous Thrombosis . . . . . . . . . . . . . . . . . . . . . . . . . . . .
20.1 Etiopathogenesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
20.2 Location . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
20.3 Diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

323

323
323
324

21

Association of Venous Sinus and IJV Stenosis
and Some Clinical Pathological Condition . . . . . . . . . . . . . . . .

331

22

Considerations About Intracranial Hemorrhages . . . . . . . . . .

333

23

Vascular Pathology Involving the Intraorbital Vessels. . . . . . .

335

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

339

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

371



1

Aortic Arch and Origin
of the Cranial Cerebral Arteries

In the study of the normal aortic arch and
brachiocephalic arteries and of their possible
variants, some short considerations about the
embryogenesis are necessary.
An important aspect in the embryological
development of the cerebrovascular system, as
pointed out by Streeter (1918), is that it is not an
independent process but it is linked to the progressive development of the brain to which the
vascular structure continuously adapts.
The vascular structures develop from primitive vascular arches (Congdon 1922; Padget
1948; Haughton and Rosenbaum 1974). These
are longitudinal vessels arising on each side from
the ductus arteriosus having an ascending course
forming the primitive ventral (ascending) paired
aorta. The vessels then bend dorsally continuing
caudally in the paired primitive descending aorta.
From these arches arise the brachiocephalic arteries. In the embryogenesis, six arches in different
phases develop and progressively disappear. The
final normal aortic arch is characterized by the
persistence of the left fourth primitive ventral
arch from which arise (right to left) the brachiocephalic trunk (innominate artery), the left common carotid artery, and the left subclavian artery.
From the brachiocephalic trunk arise the right
common carotid artery and the subclavian artery,

giving off the right vertebral artery. The left vertebral artery arises from the left subclavian artery
(Figs. 1.1, 1.2, and 1.3).

Considering the embryogenesis of the brachiocephalic arteries, from each common carotid
artery arises the external carotid artery which
supplies the extracranial and meningeal territories and the internal carotid artery (ICA) which
divides intracranially into a cranial (anterior) and
caudal (posterior) division (Padget 1944, 1948;
Lazorthes 1961 Kier 1974; Lazorthes et al. 1976).
From the cranial division arise progressively the
anterior choroidal, the anterior cerebral, and the
middle cerebral arteries responsible for the supply of the cerebral hemispheres. From the caudal
division arises the posterior communicating
artery (Pcom A) which gives off at its distal end
the medial posterior choroidal artery and a
mesencephalic–diencephalic branch from which
arises the lateral posterior choroidal artery. In the
further evolution, the PcomA continues in the
posterior cerebral artery (PCA) which progressively extends supplying the posterior part of the
cerebral hemisphere. The PcomA (pars carotica
of PCA) is connected with bilateral longitudinal
channels (BLC) closely placed on the surface of
the primitive brainstem forming the primitive
duplicated basilar artery (BA) which later fuse
together in the median BA. The cranial part of
these longitudinal channels will become the P1
segment (pars basilaris of the PCA). Also at this
stage of the evolution, the primary ICA is connected with the BLC through transitory arteries
(trigeminal, otic, hypoglossal, and proatlantal)


G.B. Bradac, Cerebral Angiography,
DOI 10.1007/978-3-642-54404-0_1, © Springer-Verlag Berlin Heidelberg 2014

1


2

1

Aortic Arch and Origin of the Cranial Cerebral Arteries

BA

ICA

ECA

VA

TCT

CCA

SA
SA

Fig. 1.1 Drawing showing the aortic arch, the extra- and
intracranial cerebral arteries. Subclavian artery (SA).
Thyrocervical trunk (TCT). Common carotid artery

(CCA). Vertebral artery (VA). Internal carotid artery
(ICA). External carotid artery (ECA). Basilar artery (BA).
Circle of Willis

which normally disappear (see Sect. 2.5).
The flow is directed from cranial to caudal. To the
proximal part of the BA converge the two vertebral arteries (VAs) formed by longitudinal anastomotic channels connected proximally with the
subclavian artery. The connection of the VAs
with the BA leads to an inversion of the flow
which is now from caudal to cranial.

Fig. 1.2 Normal aortic arch, magnetic resonance imaging (MRI) angiography. Brachiocephalic trunk (BR), from
which arise the right common carotid artery (RC) and
right subclavian artery (RS). Common left carotid artery
(LC), left subclavian artery (LS). Normal origin of both
vertebral arteries (VA). The bifurcation of the two common carotid arteries is well demonstrated

From the vertebral and basilar arteries arise
the vessels supplying the brainstem and cerebellum. The cerebellar arteries are the latest to
develop due to the late development of the
cerebellum.
At the 6–7 weeks of the fetal development (De
Vriese 1905; Padget 1944–1948), at the base of
the cerebrum, both carotid and basilar arteries are
connected to each other by the way of the small
anastomotic circle called “circle of Willis”
(Willis 1684). Both anterior cerebral arteries are


1


Aortic Arch and Origin of the Cranial Cerebral Arteries

3

AcomA

A1

C

P
DS

PcomA

M1

PCA
P1
BA

Fig. 1.4 The circle of Willis. Internal carotid artery (C),
first segment of anterior cerebral artery (A1), first segment
of middle cerebral artery (M1). Basilar artery (BA), first
segment of posterior cerebral artery (P1), posterior cerebral artery (PCA), anterior communicating artery
(AcomA), posterior communicating artery (PcomA), pituitary gland (P), dorsum sellae (DS)

Fig. 1.3 Normal aortic arch angiogram with typical origin of the left and right common carotid arteries (LC, RC).
Subclavian arteries (RS, LS), asymmetry of the vertebral

arteries (VA). That of the left is hypoplastic

linked by the anterior communicating artery, and
each carotid artery is connected through the posterior communicating artery with the respective
PCA (Fig. 1.4).
This is a natural well-constructed security
system. Its functional value, however, is somewhat unpredictable owing to the many variants

present. According to several authors (De Vriese
1905; Padget 1944–1948; Lazorthes 1961;
Lazorthes et al. 1976) the variants of the circle of
Willis occur in the postnatal period and through
the life due to hemodynamic changes such compression of the carotid and vertebral arteries by
movements of the head and neck.
Variants: Owing to the complexity of the
embryonic process, minor variants are the rule.
However, these are not recorded in the literature
as variants or anomalies. This definition is
reserved to more or less complex changes (Lie
1968; Klinkhamer 1969; Haughton and
Rosenbaum 1974; Beigelman et al. 1995; Morris
1997; Osborn 1999; Mueller et al. 2011). Among
the most frequent and more simple anomalies,
there are those characterized by the common origin of the left common carotid (LC) and the brachiocephalic trunk or by the origin of the LC
from the brachiocephalic trunk. The vertebral
artery, commonly that of the left, may originate
from the aortic arch. In these cases, the left vertebral


4


1

Aortic Arch and Origin of the Cranial Cerebral Arteries

Fig. 1.5 Aortic arch angiogram, showing the origin of the
left common carotid artery (LC) from the brachiocephalic
trunk. The left vertebral artery (VA) is well developed,
while that of the right is hypoplastic

Fig. 1.6 Aortic arch angiogram, showing the origin of the
left vertebral artery (VA) from the aortic arch. There is a
shifting of the origin of the left common carotid artery and
brachiocephalic trunk toward the heart owing to atherosclerotic elongation of the aortic arch

artery (LVA) arises from the aortic arch between
the origin of the left common carotid artery
(LCCA) and the left subclavian artery (LSA),
more rarely, distal to the LSA. A few cases of
origin of the right vertebral artery (RVA) from
the aortic arch have also been reported, distal to
the LSA or from the proximal RSA. The origin
of the vertebral artery, commonly that of the
right, from the common carotid artery can also
occur. More about variants of the VA are
described in Sect. 6.2.4.
Less frequent and more complex conditions
are the anomalous origin from the aortic arch

of all the brachiocephalic vessels in various

combinations and the aberrant subclavian
artery (more frequently that of the right) arising distal to the LSA, more rarely proximal or
close to it. Since the first description by
Kommerell in 1936, other authors have
described this anomaly (Akers et al. 1991;
Freed and Low 1997; Karcaaltincaba et al.
2009; Uchino et al. 2013b).
Extremely rare are other anomalies such as the
right aortic and the double aortic arch.
Angiographic studies are presented in
Figs. 1.5, 1.6, 1.7, 1.8, and 1.9.


1

Aortic Arch and Origin of the Cranial Cerebral Arteries

5

Fig. 1.7 Left aortic arch angiogram anomaly. The left
and right common carotid arteries (LC, RC) arise as a
common trunk. The right subclavian artery (RS) arises
distally with a separated or common origin with the left
subclavian artery (LS)

Fig. 1.8 Left aortic arch anomaly (angiogram). All vessels have a separate origin. The first to fill is the right common carotid artery (RC), followed by the left common
carotid artery (LC). Anomalous origin of the right subclavian artery (RS), probably located distally to the left subclavian artery (LS)

In the majority of the cases, these anomalies are asymptomatic, being discovered during
an angiographic study performed for a cerebral

pathology. However, the possibility of such
anomalies should be taken into account by the
angiographer. Infrequently, dysphagia can be
present, especially in cases of aberrant course of
the right subclavian artery and the right VA, due
to the course of the vessels, crossing the midline

in the retroesophageal space. Congenital heart
malformation can be associated. Furthermore, the
knowledge of these variants is useful in patients
in whom aortic arch, esophageal, or anterior neck
surgery is planned.
Some more aspects concerning the embryological development and its abnormalities involving the specific arteries are described later (see
Sects. 2.5, 2.4.1, 2.4.2, 2.4.3, 4.3, 5.3, 6.2.4, 7.5
and Chap. 3).


6

1

Aortic Arch and Origin of the Cranial Cerebral Arteries

a

Fig. 1.9 Right aortic arch anomaly associated with
anomalous origin of the brachiocephalic vessels. Aortic
angiogram. Right (a) and left (b) oblique view. On the left

oblique view (later phase), the more distal origin of the

left subclavian artery (LS) is visible


1

Aortic Arch and Origin of the Cranial Cerebral Arteries

Fig. 1.9 (continued)

b

7


2

Carotid Artery (CA)

2.1

Cervical Segment

Early in the embryogenesis, both primitive proximal ECA and ICA arise separately from the primitive third aortic arch: the ECA from its ventral
and the ICA from the dorsal part. The partial
involution of the aortic arch, on both left and
right sides, involving its segment distal to the origin of ICA, results in the formation of a common
trunk from which develops on each side the
common carotid artery (CCA). In the further evolution, the left CCA is annexed by the developped
left fourth aortic arch, and the right CCA from
the brachiocephalic trunk (Innominate Artery)

proximal remnant of the distally completely
regressed rigth fourth aortic arch. The common
carotid arteries run cranially in the carotid space,
surrounded by the three layers of the deep cervical fascia, called the carotid sheet. Approximately
at the level of the hyoid bone, usually between
the C4 and C6 vertebral bodies, each common
carotid artery divides into the internal carotid
artery (ICA) and external carotid artery (ECA).
Cases of a higher bifurcation, up to the first
cervical vertebra (Lie 1968), or lower, in the
upper thoracic levels (Vitek and Reaves 1973),
have been reported. The carotid sheet is a welldefined structure below the carotid bifurcation,
though it is incomplete or absent at the level
of the oral–nasal pharynx (Harnsberger 1995).
The infrahyoid segment of the carotid space contains the common carotid artery and depending
on the level of the bifurcation the proximal part

of the ICA, the proximal part of ECA, the Internal
Jugular Vein (IJV), portions of the cranial nerves
IX, X, XI, XII, the Sympatetic Plexus and Lymph
nodes. In the infrahyoid segment, the vessels run
in the so-called carotid triangle (Som et al. 2003a)
(Fig. 2.1) defined by the sternocleidomastoid
muscle, laterally and posteriorly, and by the superior belly of the omohyoid and the posterior belly
of the digastric muscle inferiorly and superiorly,
respectively. In the suprahyoid–infrahyoid segments, the ICA is accompanied by the IJV located
posterolaterally, the cranial nerves (IX, X, XI,
and XII), the sympathetic plexus, and the chain
of lymph nodes.
Near the skull base, the borders of the carotid

space (Harnsberger 1995) also called by others
(Som and Curtin 2003; Mukherji 2003) the retrostyloid parapharyngeal space can be so outlined: laterally, the parotid space; anteriorly and
medially, the parapharyngeal and retropharyngeal spaces, respectively; and posteriorly, the
perivertebral space (Fig. 2.2c).
The first segment of the ICA (carotid bulb)
is slightly enlarged, becoming smaller and narrower 1–2 cm distally. The bulb can be
enlarged, particularly in older, atherosclerotic
patients, and tortuosity of the distal segment is
frequent in very young and older patients. This
tortuosity can be congenital or related to dysplastic or atherosclerotic changes. At its origin, the ICA commonly lies posterior and
lateral to the ECA. More distally, it is medial to
the ECA (Fig. 2.2a, b) (see Chap. 3).

G.B. Bradac, Cerebral Angiography,
DOI 10.1007/978-3-642-54404-0_2, © Springer-Verlag Berlin Heidelberg 2014

9


10

2

ICA

D

IJV

ECA


H
CCA
OM

SCM

The mandibular artery is an embryonic remnant that usually divides into two branches: one
runs in the pterygoid canal, anastomosing with
the vidian artery; the other is more inferior, anastomosing with the pterygovaginal artery (see
also Sect. 3.7.3 and Fig. 3.27). This artery can
be especially involved in the vascularization of
angiofibromas (Fig. 3.20). Apart from the above
pathological situations, these branches are not
commonly visible on the angiogram.

2.3

S

Fig. 2.1 Drawing of the carotid triangle. Lateral-oblique
view. SCM sternocleidomastoid muscle, OM superior belly
of the omohyoid muscle, D posterior belly of the digastric
muscle, H hyoid bone, S sternum, CCA common carotid
artery, ECA proximal external carotid artery, ICA infra–
supra Hyoid internal carotid artery, IJV internal jugular vein

2.2

Petrous Segment of ICA


The ICA enters the base of the skull at the carotid
foramen, anteriorly to the jugular fossa and jugular
vein. It runs entirely in the petrous bone, first with
a vertical course for about 1 cm, then horizontally
medially and slightly upward. Through its course,
the ICA lies anteriorly medially and below the
tympanic cavity and cochlea. It emerges from the
petrous bone, near its apex, running above the
cartilage covering the foramen lacerum (Figs. 2.3
and 2.4) and enters the cavernous sinus.
There are two branches: the caroticotympanic
and mandibular arteries. The caroticotympanic
artery is an embryonic remnant that supplies the
middle ear cavity. There is possible anastomosis
with the tympanic branch of the ascending pharyngeal artery (APhA) (see also Sect. 3.4 and
Fig. 3.28). The caroticotympanic artery can be
involved in tumors of the skull base, particularly
in tympanojugular paragangliomas (Fig. 3.24d).

Carotid Artery (CA)

Cavernous Segment of ICA

This runs in the space formed by the separation of
a fold of the dura (Taptas 1982) into two layers: the
lateral one is the medial wall of the middle cranial
fossa; the other is medial and in close contact in its
inferior part with the periosteum of the sphenoid
bone (periosteal layer). This space, in which run the

ICA, venous channels, and nerves, has been called
by Taptas (1982) “the space of the cavernous sinus.”
This definition which distinguishes the space from
its contents is more appropriate than the commonly
used “cavernous sinus” (see also Sect. 9.3.10). In this
space, the ICA is directed first forward and upward,
then curving posteriorly and slightly medially to the
anterior clinoid process. In its course, laterally to
the sella turcica and pituitary gland from which is
separated by the medial layer of the dura, the artery
is surrounded by a venous plexus, and it has a close
relationship with cranial nerves III, IV, and VI and
the first and second branch of the trigeminal nerves.
The nerves run close to the lateral wall, attached to it
by dural sheaths. The latter can be connected, forming a thin, irregular inner layer adjacent to the external layer of the lateral wall (Umansky and Nathan
1982). Unlike the other nerves, cranial nerve VI
runs inside the cavernous space.
Due to its S-shaped course, the cavernous segment is also called the siphon, which schematically can be subdivided into three segments. The
segment called C5 is directed upward, the C4 is
horizontal, and the C3 is a posteriorly directed
curve up to the dural ring, through which the ICA
passes, entering the subarachnoid space (Figs. 2.3
and 2.4). There are two branches of the cavernous
segment: one is the meningohypophyseal trunk
(MHT), the other is the inferolateral trunk (ILT).


2.3 Cavernous Segment of ICA

11


a

b

c

MS

PPS

PS

ECA

CS

JV
ICA RPS

PVS

Fig. 2.2 (a) Common carotid angiogram, lateral view,
showing the course of the external and internal carotid
arteries. (b) Common carotid angiogram, AP view, showing the course of the external carotid artery (ECA, arrow),
first medially and more distally lateral to the internal carotid
artery (ICA). The dotted line corresponds to the axial plane
in (c). (c) Carotid space (CS), surrounded by the parotid

space (PS), the parapharyngeal space (PPS), the retropharyngeal space (RPS), and the perivertebral space (PVS).

Masticator space (MS). In the carotid space are indicated
the ICA (anteriorly) and jugular vein (JV, posteriorly),
together with cranial nerves IX, X, X1, and XII. In the
parotid space, the ECA runs posteriorly and the retromandibular vein anteriorly. The facial nerve runs laterally


12

2

Carotid Artery (CA)

recurrent meningeal artery of the ophthalmic
artery. One system can be dominant over the
other. Anastomoses are frequently present.
The ILT and MHT are very fine branches
(Fig. 2.5), not always recognizable on a lateral
angiogram. They can be dilated and well visible
when involved in the supply of pathological processes, especially meningiomas and dural arteriovenous fistulas (Figs. 3.25b, 13.7, 13.10, and 13.11).

2.4

Fig. 2.3 Petrous and cavernous portion of the ICA, lateral
carotid angiogram. Petrous portion (in red). Cavernous portion (in green). Dural ring proximal to the origin of the ophthalmic artery. C5, C4, and C3 correspond to the different
parts of the cavernous portion of the ICA. C2 and C1 define
the supraclinoid and subarachnoid ICA

• The MHT arises from the medial surface of the
C5 segment of the ICA. It gives off a branch supplying the neurohypophysis (inferior hypophyseal artery), which is recognizable on an
angiogram as a slight blush. It also gives off

dural branches for the clivus and tentorium
(clival and tentorial branches). The tentorial
branch has been called the artery of Bernasconi
and Cassinari (1957), who first reported its angiographic visualization. These dural branches
anastomose with meningeal branches of the contralateral ICA and inferiorly with clival branches
of the APhA. There are also possible anastomoses with branches of the middle meningeal artery.
• The ILT arise from the lateral surface of the
C4 segment; it supplies cranial nerves III, IV,
and VI and partially the ganglion Gasseri. It
gives off dural branches for the dura of the
cavernous sinus and adjacent area. In the supply of this area, there is a balance between the
ICA system, represented by the ILT, and
branches of the ECA, represented by the middle meningeal artery, accessory meningeal
artery, artery of the foramen rotundum, and

Supraclinoid Segment of ICA

This begins where the artery goes through the dura
and enters the subarachnoid space, running posteriorly, superiorly, and slightly laterally between
the anterior clinoid process laterally and the optic
nerve medially. The dural ring surrounding the
ICA, where the artery enters the subarachnoid
space, is closely adherent to the artery laterally, but
it is frequently less adherent medially, forming a
thin cavity (carotid cave). Aneurysms arising
below the dural ring (intracavernous aneurysms)
can, however, expand the cave and extend superiorly into the subarachnoid space (cave aneurysms)
(Kobayashi et al. 1995; Rhoton 2002).
At the level of the anterior perforated space
(APS), the artery divides into the anterior and

middle cerebral arteries. The supraclinoid segment can be subdivided into a proximal and distal
part, termed C2 and C1. From the origin of its
branches, the supraclinoid segment can be more
precisely subdivided as follows (Gibo et al. 1981a,
1981b): the ophthalmic segment, from the origin
of the ophthalmic artery to the origin of the posterior communicating artery (PcomA); the communicating segment, from the origin of the PcomA to
the origin of the choroidal artery; and the choroidal segment, from origin of the anterior choroidal
artery to the terminal bifurcation of the ICA.

2.4.1

In the Ophthalmic Segment
Arise the Ophthalmic Artery
and Superior Hypophyseal
Arteries

2.4.1.1 The Ophthalmic Artery
The ophthalmic artery (OA) arises on the superiormedial surface of the ICA, commonly very close


2.4

Supraclinoid Segment of ICA

13

b

a


d

c
Fig. 2.4 (a) Carotid angiogram, AP view. The lines
define the course of the petrous segment of the ICA, continuing into the cavernous segment. The end of the latter
cannot be precisely defined in the AP view. (b) CT angiography, coronal reconstruction, showing the course of

the petrous segment. (c) CT angiography, showing the
horizontal part of the petrous segment of the ICA running
above the foramen lacerum. (d) MRI, coronal view, sellar
and parasellar area, showing the course of the ICA in the
cavernous sinus. Cranial nerve III (arrowheads)

to the point where the ICA perforates the dura. It
runs below the optic nerve (Hayreh and Dass
1962a, b; Hayreh 1962) and enters, together with
the nerve, the orbita through the optic canal.
Initially, the artery runs inferolaterally to the optic
nerve (first segment), then crosses the nerve forming a bend below or above the nerve (second segment), and runs further medially and parallel to it
(third segment). It gives off three types of
branches: ocular, orbital, and extraorbital.
The ocular branches include the central retinal
artery and the ciliary arteries supplying partially
the optic nerve and the ocular bulb. These are the
first branches arising where the artery crosses the
nerve.

The orbital branches include the lacrimal
artery, which supplies the lacrimal gland and conjunctiva. An important branch, sometimes present, is the recurrent meningeal artery, which runs
backward and passes through the superior orbital

fissure, anastomosing with branches of the middle
meningeal artery (MMA). It can be involved in
the vascularization of basal meningiomas (Bradac
et al. 1990; Fig. 3.25), in dural arteriovenous fistulae (Fig. 13.10), and in the supply of angiofibromas and chemodectomas extending toward
the orbita and parasellar region (Fig. 3.20).
Anastomosis of the lacrimal artery with the
anterior deep temporal artery can be an important collateral circulation via the OA in occlusion


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