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InterventIonal

neuroradIology

InterventIonal

neuroradIology

Edited by

robert W. Hurst

Hospital of the University of Pennsylvania Philadelphia, Pennsylvania, USA

robert H. rosenwasser

Thomas Jefferson University Philadelphia, Pennsylvania, USA

Philadelphia, Pennsylvania, USA robert H. rosenwasser Thomas Jefferson University Philadelphia, Pennsylvania, USA
Philadelphia, Pennsylvania, USA robert H. rosenwasser Thomas Jefferson University Philadelphia, Pennsylvania, USA

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Library of Congress Cataloging-in-Publication Data

Interventional neuroradiology / edited by Robert W. Hurst, Robert H. Rosenwasser. p. ; cm. Includes bibliographical references.

ISBN-13: 978-0-8493-9562-8 (hardcover: alk. paper)

ISBN-10: 0-8493-9562-3 (hardcover: alk. paper)

1. Nervous system—Interventional radiology. I. Hurst, Robert W. II. Rosenwasser, Robert H.

[DNLM: 1. Cerebrovascular Disorders—radiotherapy. 2. Cardiovascular System—anatomy & histology. 3. Central Nervous System—blood supply. 4. Radiology, Interventional—methods. WL 355 I6074 2008]

RD594.15.I62 2008 616.8 0 04757—dc22

2007023346

To the mentors, students, and patients who have shown me how much there is to learn and all too often, how little time in which to accomplish it. To my wonderful wife Marilyn, and my children, Jonathan and Katherine, who make family the greatest happiness of my life. I must thank them for the commitment in time that has made this endeavor possible. —Robert W. Hurst

I would like to dedicate this book to my wife Deborah August, M.D., who has been my partner and pillar of strength and

supported me without hesitation in all my endeavors. In addition, I wish to express my gratitude to William A. Buchheit, M.D., my Neurosurgical Mentor and Friend, and the individual who supported the early concept of Endovascular Therapy for disorders

of the Nervous System

a man way ahead of his time.

—Robert H. Rosenwasser

Preface This book is intended to provide the clinical practitioner with background information and specific

Preface

This book is intended to provide the clinical practitioner with background information and specific descriptions of the anatomy, techniques, disorders, procedures, and decisions most commonly encountered in interventional neuro- radiology. Throughout the past decade, interventional neuroradiological techni- ques have revolutionized therapy for vascular disorders of the head, neck, and central nervous system. These procedures now provide noninvasive treatment for many of the most common neurological disorders and make possible treat- ment of numerous patients for whom there were no reasonable therapeutic options before. With progress, however, comes the requirement for increased knowledge and technical skill to deliver these treatments safely and effectively. Areas of fundamental knowledge in interventional neuroradiology cross the boundaries of classically delineated medical and surgical specialties, including neurosurgery, neuroradiology, and neurology. Required knowledge includes familiarity with neuroradiological imaging of vascular disease, knowledge of vascular anatomy, and thorough understanding of cerebrovascular disorders and their endovascu- lar treatments. Most importantly, skill in basic interventional techniques must be coupled with good clinical judgment in patient management and decision making. Recent rapid advances in neuroimaging mean that practitioners of interven- tional neuroradiology must have excellent diagnostic skills with noninvasive neuroimaging modalities to identify the presence of cerebrovascular disease, evaluate its effects, identify potential candidates for neurointerventional proce- dures, and document the effects of the treatment. Separate chapters on CT, MR, and ultrasonographic evaluation of cerebrovascular disease emphasize the cur- rent noninvasive evaluation of disorders that are of interest to neurointervention- alists. In addition, the authors have made every effort throughout the text to illustrate the integration of current neuroimaging into the performance and decision making associated with interventional neuroradiological procedures. As in all radiological- or surgical-based specialties, thorough understanding of pertinent anatomy is essential. For the neurointerventionalist, cerebrovascular anatomy is the workplace. Anatomic knowledge underlies the understanding of many, if not all, cerebrovascular disorders, provides routes of endovascular access, and defines the scope of treatment options. Chapters covering pertinent vascular anatomy of special importance to neurointerventional procedures have been included. These chapters are directed at key anatomic concepts as well as specific anatomic features of the head, neck, brain, and spine vasculature. It is through basic neurointerventional techniques that treatment is deliv- ered to the individual patient. No amount of theoretical understanding can overcome poor technique in an environment as unforgiving as the cerebrovas- cular system. Discussion of basic techniques with appropriate illustrations should prove useful for readers at all levels of experience, from students entering the field to experienced practitioners who may benefit from review or additional technical options. Coupled with anatomic and technical knowledge is the requirement for understanding the epidemiology, pathophysiology, and clinical features of the increasing numbers of cerebrovascular disorders that are now amenable to endovascular treatment. Recognized experts in the field have authored clinically oriented discussions of the most common conditions of interest to interventional neuroradiologists. Treatment discussions are illustrated with current images to emphasize pertinent technical and anatomic details. Extensive and current references are included to serve as a basis for further research.

vi

Preface

Perhaps most essential to successful neurointerventional practice is the requirement for correlating the appropriate application of knowledge and tech- nical skills to the care of patients. This book is designed to illustrate and emphasize the importance of integrating clinical information, knowledge of disease processes, and technical skill through the use of good clinical judgment to formulate and perform effective neurointerventional procedures.

Robert W. Hurst

Robert H. Rosenwasser

Contents Preface v   Contributors ix 1. Vascular Anatomy of the Head, Neck, and Skull

Contents

Preface

v

 

Contributors

ix

1.

Vascular Anatomy of the Head, Neck, and Skull Base Michele H. Johnson, Hjalti M. Thorisson, and Michael L. DiLuna

1

2.

Applied Neurovascular Anatomy of the Brain and Skull Randy S. Bell, Alexander H. Vo, and Rocco A. Armonda

23

3.

Vascular Anatomy of the Spine and Spinal Cord Armin K. Thron

39

4.

Intracranial Collateral Routes and Anastomoses in Interventional Neuroradiology David S. Liebeskind

57

5.

CT Imaging and Physiologic Techniques in Interventional Neuroradiology Ronald L. Wolf

87

6.

MR Angiography: Principles and Applications in Interventional Neuroradiology Neerav R. Mehta and Elias R. Melhem

113

7.

Ultrasonographic Imaging and Physiological Techniques in Interventional Neuroradiology Jaroslaw Krejza

135

8.

Techniques and Devices in Interventional Neuroradiology Jeffrey M. Katz, Y. Pierre Gobin, and Howard A. Riina

161

9.

Balloon Occlusion, Wada, and Pharmacological Testing Linda J. Bagley

183

10.

Endovascular Management of Tumors and Vascular Malformations of the Head and Neck Johnny C. Pryor, Joshua A. Hirsch, and Robert W. Hurst

195

11.

Dissections of the Carotid and Vertebral Arteries Qaisar A. Shah, Scott E. Kasner, and Robert W. Hurst

213

12.

Direct Carotid

Cavernous Fistula

231

Uday S. Kanamalla, Charles A. Jungreis, and Jeffrey P. Kochan

13.

Endovascular Management of Intracranial Aneurysms Darren Orbach, Tibor Becske, and Peter Kim Nelson

239

14.

Endovascular Treatment of Post-Subarachnoid Hemorrhage Vasospasm Jonathan L. Brisman, David W. Newell, and Joseph M. Eskridge

263

15.

Endovascular Management of Brain Arteriovenous Malformations John B. Weigele, Riyadh N. Al-Okaili, and Robert W. Hurst

275

viii

Contents

16. Endovascular Treatment of Acute Ischemic Stroke Mayur A. Paralkar, Alexandros L. Georgiadis, Adnan I. Qureshi, and Qaisar A. Shah

305

17. Endovascular Treatment of Extracranial Carotid Atherosclerotic Disease

311

Eric Sauvageau, Robert D. Ecker, Junichi Yamamoto, Ramachandra P. Tummala,

Elad I. Levy, and L. Nelson Hopkins

18. Stenting and Angioplasty for Intracranial Atherosclerotic Occlusive Disease Nabil M. Akkawi and Ajay K. Wakhloo

325

19. Endovascular Management of Dural Arteriovenous Fistulas J. Marc C. van Dijk, Robert A. Willinsky

335

20. Inferior Petrosal Sinus Sampling in the Diagnosis of Pituitary Adenomas Nicholas J. Patronas and Donald L. Miller

353

21. Endovascular Treatment of Spinal Vascular Malformations Mayumi Oka and Kieran Murphy

363

22. Percutaneous Vertebroplasty Mary E. Jensen

387

Index

411

Contributors Nabil M. Akkawi Division of Neuroimaging and Intervention, University of Massachusetts Medical School,

Contributors

Nabil M. Akkawi Division of Neuroimaging and Intervention, University of Massachusetts Medical School, Worcester, Massachusetts, U.S.A.

Riyadh N. Al-Okaili Department of Radiology, King Abdulaziz Medical City, Riyadh, Saudi Arabia.

Rocco A. Armonda Departments of Neurosurgery and Radiology, National Naval Medical Center, and Comprehensive Neurosciences Program, Uniformed Services University of Health Sciences, Bethesda, Maryland, U.S.A.

Linda J. Bagley Departments of Radiology and Neurosurgery, University of Pennsylvania Medical Center, Philadelphia, Pennsylvania, U.S.A.

Tibor Becske Departments of Neurology, Neurosurgery, and Radiology, New York University Medical Center, New York, New York, U.S.A.

Randy S. Bell Departments of Neurosurgery and Radiology, National Naval Medical Center, and Comprehensive Neurosciences Program, Uniformed Services University of Health Sciences, Bethesda, Maryland, U.S.A.

Jonathan L. Brisman Department of Cerebrovascular and Endovascular Neurosurgery, Winthrop University Hospital, Mineola, Long Island, New York, U.S.A.

Michael L. DiLuna Department of Neurosurgery, Yale University School of Medicine, New Haven, Connecticut, U.S.A.

Robert D. Ecker Department of Neurosurgery and Toshiba Stroke Research Center, Millard Fillmore Gates Hospital, Kaleida Health, University at Buffalo, State University of New York, Buffalo, New York, U.S.A., and Department of Neurological Surgery, U.S. Naval Hospital, Okinawa, Japan.

Joseph M. Eskridge Department of Interventional Neuroradiology, Seattle Neuroscience Institute, Seattle, Washington, U.S.A.

Alexandros L. Georgiadis Department of Neurology, Zeenat Qureshi Stroke Research Center, University of Minnesota, Minneapolis, Minnesota, U.S.A.

Y. Pierre Gobin Departments of Radiology and Neurosurgery, New York Presbyterian Hospital, Weill Medical College of Cornell University, New York, New York, U.S.A.

Joshua A. Hirsch Department of Interventional Neuroradiology and Endovascular Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, U.S.A.

L. Nelson Hopkins Department of Neurosurgery and Toshiba Stroke Research Center, Millard Fillmore Gates Hospital, Kaleida Health, University at Buffalo, State University of New York, Buffalo, New York, U.S.A.

Robert W. Hurst Departments of Radiology, Neurology, and Neurosurgery, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A.

Mary E. Jensen Departments of Radiology, and Neurosurgery, University of Virginia Health Systems, Charlottesville, Virginia, U.S.A.

x

Contributors

Michele H. Johnson Interventional Neuroradiology, Departments of Diagnostic Radiology and Surgical Otolaryngology, Yale University School of Medicine, New Haven, Connecticut, U.S.A.

Charles A. Jungreis Temple University Hospital, Temple University School of Medicine, Philadelphia, Pennsylvania, U.S.A.

Uday S. Kanamalla Temple University Hospital, Temple University School of Medicine, Philadelphia, Pennsylvania, U.S.A.

Scott E. Kasner Department of Neurology, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A.

Jeffrey M. Katz Department of Radiology, New York Presbyterian Hospital, Weill Medical College of Cornell University, New York, New York, U.S.A.

Jeffrey P. Kochan Temple University Hospital, Temple University School of Medicine, Philadelphia, Pennsylvania, U.S.A.

Jaroslaw Krejza Department of Radiology, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A.; Department of Nuclear Medicine, Medical University of Gdansk, Poland.

Elad I. Levy Department of Neurosurgery and Toshiba Stroke Research Center, Millard Fillmore Gates Hospital, Kaleida Health, University at Buffalo, State University of New York, Buffalo, New York, U.S.A.

David S. Liebeskind UCLA Stroke Center, University of California, Los Angeles, California, U.S.A.

Neerav R. Mehta University of Pennsylvania Medical Center, Philadelphia, Pennsylvania, U.S.A.

Elias R. Melhem University of Pennsylvania Medical Center, Philadelphia, Pennsylvania, U.S.A.

Donald L. Miller Department of Radiology, National Naval Medical Center and Department of Radiology, Uniformed Services University of Health Sciences, Bethesda, Maryland, U.S.A.

Kieran Murphy Department of Radiology, Division of Interventional Neuroradiology, Johns Hopkins University, Baltimore, Maryland, U.S.A.

Peter Kim Nelson Departments of Neurology, Neurosurgery, and Radiology, New York University Medical Center, New York, New York, U.S.A.

David W. Newell Department of Neurosurgery, Seattle Neuroscience Institute, Seattle, Washington, U.S.A.

Mayumi Oka Department of Radiology, Division of Interventional Neuro- radiology, Johns Hopkins University, Baltimore, Maryland, U.S.A.

Darren Orbach Departments of Neurology, Neurosurgery, and Radiology, New York University Medical Center, New York, New York, U.S.A.

Mayur A. Paralkar Department of Medicine, University of Medicine and Dentistry of New Jersey, Newark, New Jersey, U.S.A.

Nicholas J. Patronas Department of Radiology, National Institutes of Health Clinical Center, Bethesda, Maryland, U.S.A.

Johnny C. Pryor Department of Interventional Neuroradiology and Endovascular Neurosurgery, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, U.S.A.

Contributors

xi

Adnan I. Qureshi Department of Neurology, Zeenat Qureshi Stroke Research Center, University of Minnesota, Minneapolis, Minnesota, U.S.A.

Howard A. Riina Departments of Radiology and Neurosurgery, New York Presbyterian Hospital, Weill Medical College of Cornell University, New York, New York, U.S.A.

Eric Sauvageau Department of Neurosurgery and Toshiba Stroke Research Center, Millard Fillmore Gates Hospital, Kaleida Health, University at Buffalo, State University of New York, Buffalo, New York, U.S.A., and Department of Neurological Surgery, University of South Florida College of Medicine, Tampa, Florida, U.S.A.

Qaisar A. Shah Department of Neurology, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A., and Department of Neurology, University of Minnesota, Minneapolis, Minnesota, U.S.A.

Hjalti M. Thorisson Department of Diagnostic Radiology, Yale University School of Medicine, New Haven, Connecticut, U.S.A.

Armin K. Thron Department of Neuroradiology, University Hospital, RWTH Aachen University, Aachen, Germany.

Ramachandra P. Tummala Department of Neurosurgery and Toshiba Stroke Research Center, Millard Fillmore Gates Hospital, Kaleida Health, University at Buffalo, State University of New York, Buffalo, New York, U.S.A.

J. Marc C. van Dijk Department of Neurosurgery, University Medical Center, Groningen, Groningen, The Netherlands.

Alexander H. Vo Departments of Neurosurgery and Radiology, National Naval Medical Center, and Comprehensive Neurosciences Program, Uniformed Services University of Health Sciences, Bethesda, Maryland, U.S.A.

Ajay K. Wakhloo Division of Neuroimaging and Intervention, University of Massachusetts Medical School, Worcester, Massachusetts, U.S.A.

John B. Weigele Department of Radiology, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania, U.S.A.

Robert A. Willinsky Department of Medical Imaging, Toronto Western Hospital, Toronto, Ontario, Canada.

Ronald L. Wolf Department of Radiology, Neuroradiology Section, University of Pennsylvania Medical Center, Philadelphia, Pennsylvania, U.S.A.

Junichi Yamamoto Department of Neurosurgery and Toshiba Stroke Research Center, Millard Fillmore Gates Hospital, Kaleida Health, University at Buffalo, State University of New York, Buffalo, New York, U.S.A.

1

Vascular Anatomy of the Head, Neck, and Skull Base

Michele H. Johnson, Hjalti M. Thorisson, and Michael L. DiLuna

Interventional Neuroradiology, Departments of Diagnostic Radiology and Surgical Otolaryngology; , Department of Diagnostic Radiology; and , Department of Neurosurgery, Yale University School of Medicine, New Haven, Connecticut, U.S.A.

INTRODUCTION

The emphasis of this chapter is on the anatomy and anatomic variations of the vasculature of the head and neck beginning in the thorax at the level of the aortic arch and extending superiorly to the level of the skull base (vascular entrance through the dura). Selective catheterization is predicated on familiarity with these anatomic features. Cross-sectional (vascular) imaging, including CTA and MRA, has supplanted catheter studies for the purposes of pure diagnosis. Identifica- tion of the common and uncommon variations and their adjacent soft tissue relationships is important to the neurointerventionalist when assessing the cross- sectional imaging prior to therapeutic intervention. The anatomy of this region will be explored using a combination of CTA, MRA, and conventional angio- graphic images and case examples to demonstrate features important to the neurointerventionalist (1).

EMBRYOLOGY

The embryology of the aortic arch development is complex and beyond the scope of this chapter; how- ever, a few relevant embryologic considerations pro- vide a basis for understanding important normal variants that may have an impact on catheterization and image interpretation (2–6). The convexity of the aortic arch forms from the left fourth primitive aortic arch. The innominate or brachiocephalic artery (BCA), the left common carotid artery (LCCA), and the left subclavian artery (LSUB) arise sequentially from the aortic arch (from proximal to distal) (Fig. 1A). In the majority of cases, the LCCA arises distinctly sep- arate from the BCA; however, in approximately 20% of patients, the LCCA may arise in conjunction with the BCA in a bovine configuration (Fig. 1B) (7,8). In a small percentage of patients, the left vertebral artery may arise as a branch of the aortic arch (Fig. 1C). Even more rarely, the right vertebral artery may arise directly from the aortic arch (Fig. 1D, E) (9).

In rare cases, the arch is derived from the right primitive arch and the brachiocephalic vessels arise as a mirror image of the normal arrangement (Fig. 1F). More commonly, an aberrant right subclavian artery (RSUB) is present that is characterized by the right common carotid as the first branch from the aortic arch, followed by the LCCA, the LSUB, and finally the RSUB, which arises distally and proceeds toward the right behind the esophagus to give rise to the right vertebral artery and remaining subclavian artery branches (Fig. 1G). A focal dilatation of the aorta adjacent to the origin of the aberrant right subclavian is referred to as Kommerell’s diverticulum and may occasionally become aneurysmal and require surgical repair (Fig. 1H) (10,11).

AORTIC ARCH AND BRANCHES

The aorta arises from the heart and emerges from the pericardium in the superior mediastinum, where it forms the ascending aortic arch (AOA) anterior to the trachea at the level of the sternal manubrium. From this ascending arch arise three major branches: the BCA, the LCCA, and the LSUB (Fig. 1A). The BCA crosses obliquely cephalad into the right anterior to the trachea before bifurcating into the right common carotid artery (RCCA) and RSUB behind the sterno- clavicular joint. Fluoroscopic recognition of the head of the clavicle as the location of the bifurcation of the BCA can be a useful adjunct to selective catheter- ization of the RCCA and RSUB (Fig. 2). The anterior location of the RCCA in relationship to the RSUB can be exploited in the selective catheterization of the subclavian artery by turning the patient’s head toward the left and extending the arm to accentuate the sep- aration between these two vessels. The right vertebral artery arises from the RSUB just opposite the origin of the internal mammary (INM) artery. The left vertebral artery can arise directly from the aorta in 5% of cases (9). Additional subclavian branches include the ascending cervical artery, the thyrocervical trunk,

2

Johnson et al.

2 Johnson et al. Figure 1 ( A ) Normal LAO arch configuration. Note the typical

Figure 1 (A ) Normal LAO arch configuration. Note the typical configuration of the great vessels and the marked vertebral artery asymmetry (right > left). (B ) Bovine arch. Note the common origin of the BCA and the LCCA. The left vertebral artery is larger than the right. ( C ) LAO arch injection demonstrates the origin of the left vertebral artery from the aortic arch between the origins of the LCCA and the left SUB. Note the absence of vertebral originating from the left SUB. ( D ) Right vertebral artery arising from the arch demonstrated on posterior view of 3D CTA. (E ) Spontaneous aortic dissection in a patient with aberrant right subclavian and a bovine arch configuration. The patient presented with chest and right arm pain. Note the false lumen (FL) and the dissection flap ( arrows). ( F) Ehlers-Danlos with aberrant right subclavian, bovine origin, and multiple aneurysms ( arrows ). (G ) Right aortic arch with aberrant left subclavian and tracheal ring. Note the diverticulum of Komerell (arrows ). (H ) Massive oral bleeding. Aortic arch arteriogram demonstrates a normal arch confirguration; however, there is an increased distance between the BCA and RCCA and the LCCA (arrows ) secondary to mediastinal hematoma. ( I ) Massive oral bleeding is associated with extravasation of contrast from this left common carotid blow-out. ( J) Massive oral bleeding is associated with extravasation of contrast from this left common carotid blow-out. Abbreviations : BCA, brachiocephalic artery; LCCA, left common carotid artery; SUB, subclavian artery; RCCA, right common carotid artery; LAO, left anterior oblique.

right common carotid artery; LAO, left anterior oblique. Figure 2 ( A , B ) 3D

Figure 2 (A, B) 3D CTA demonstrates the normal relationships of the BCA as it bifurcates into the subclavian and carotid arteries on the right bifurcation. The BCA road-map image demonstrates the clavicle as a landmark for the bifurcation in the AP view. Abbreviation : BCA, brachiocephalic artery.

Chapter 1: Vascular Anatomy of the Head, Neck, and Skull Base

3

1: Vascular Anatomy of the Head, Neck, and Skull Base 3 Figure 3 Proximal subclavian branches

Figure 3 Proximal subclavian branches (AC) SUB injection demonstrates proximal branches supplying T2 vertebral tumor. (D ) The ascending cervical artery is a potential collateral source to the vertebral artery. Abbreviation : SUB, subclavian artery.

vertebral artery. Abbreviation : SUB, subclavian artery. Figure 4 Vertebral artery cervical branches. AP view (

Figure 4 Vertebral artery cervical branches. AP view (A) and lateral view ( B ) of the cervical vertebral artery demonstrate small muscular and vertebral body branches (arrows ).

and the costocervical trunk (Fig. 3A–C). These branches are important to identify in the analysis of pathologic processes of the lower neck as well as vascular malformations and other pathologic lesions involving the cervical and/or upper thoracic vertebral bodies and spinal cord.

VERTEBRAL ARTERIES

The vertebral arteries ascend posterior to the com- mon carotid between the longus colli and scalenus anterior muscles, entering the transverse foramen at C6. They traverse the transverse foramen of the cer- vical vertebral body between C6 and C2. After exit- ing the transverse foramen at C2, the vertebral artery proceeds posterolaterally through the transverse foramen of C2 and posteromedially between C1 and the occiput, before entering the foramen mag- num (1,4,5). The cervical ve rtebral artery provides small branches to supply the vertebral bodies and the adjacent cervical musculature (Fig. 4A, B). The cer- vical course is usually straight, although tortuosity

may limit distal microcatheterization and/or may lead to confusion when the transverse foramen is enlarged (Fig. 5). It is also important to recognize the potential for luminal narrowing and/or flow alteration within the vertebral artery as a conse- quence of normal head turning. This normal phe- nomenon may be accentuated by the presence of osteophytes encroaching on the artery within the transverse foramen (12). Provocative maneuvers dur- ing angiography or, alterna tively, during noninva- sive vascular imaging may demonstrate these findings, which may correlate with clinical hypoper- fusion symptoms such as lightheadedness or vertigo (Fig. 6A, B) (13,14). The left vertebral artery is dominant (larger and responsible for the majority of the posterior fossa flow) almost half of the time, while the right vertebral artery is dominant 25% of the time (12,15–17). No size or flow dominance is present in the remaining cases (12,15–17). Anastomoses exist at multiple levels with the external carotid artery (ECA), the thyrocervical trunk, and the costocervical trunk.

4

Johnson et al.

4 Johnson et al. Figure 5 Vertebral artery tortuosity versus dissection on CTA ( A ).

Figure 5 Vertebral artery tortuosity versus dissection on CTA ( A ). Note the tortuosity without dissection flap on the AP angiogram ( B).

without dissection flap on the AP angiogram ( B ). Figure 6 Syncope on head turning.

Figure 6 Syncope on head turning. (A) Left vertebral artery: neutral position. Note the compression of the cervical vertebral artery by uncovertebral joint degen- erative osteophytes accentuated on moderate ( B) and maximal (C) head turning.

The vertebral arteries proceed through the dura at the level of the foramen magnum and join to form a common basilar artery. The posterior inferior cer- ebellar artery (PICA) is the largest, though frequently variable, branch of the vertebral artery and usually arises proximal to origin of the basilar artery. It can arise as a single trunk or in duplicate, and occasion- ally the vertebral artery can terminate as the PICA (18,19). There is a balance between distal branches of the PICA and hemispheric branches of the anterior inferior cerebellar artery (AICA) such that an AICA- PICA variant may be an absent PICA, with the PICA territory supplied by distal branches of the AICA, or vice versa (18–20). (Fig. 7A, B) The posterior spinal artery often arises from the vertebral artery at the level of the medulla oblongata

or may arise from the PICA, coursing posteriorly and dividing into anterior and posterior branches to anas- tomose with small perforators from the vertebral artery. The ascending cervical artery, posterior inter- costal arteries, and lumbar arteries may each contrib- ute collateral supply to the posterior spinal arteries at their respective levels. The anterior spinal artery arises from the distal end of the vertebral artery and descends anterior to the medulla oblongata, joining with its contralateral branch to descend as a single vessel, forming multiple anastomoses with similar segmental perforators (as the posterior spinal artery), to supply the anterior spinal cord to the filum termi- nale. The posterior meningeal artery arises from the cervical vertebral artery to supply the bone and dura of the posterior fossa (12). Multiple small spinal

Chapter 1: Vascular Anatomy of the Head, Neck, and Skull Base

5

1: Vascular Anatomy of the Head, Neck, and Skull Base 5 Figure 7 Distal vertebral artery

Figure 7 Distal vertebral artery variations. (A ) AP and ( B ) lateral vertebral ends in PICA. Vertebral artery fenestrations ( CE); T1-weighted sagittal MRI ( F) and AP (G ) and lateral ( H ) vertebral angiograms demonstrate an AVM fed by the ASA; AP ( I) and lateral (J ) views demonstrate the origin of PICA below the foramen magnum. Abbreviations : AVM, arteriovenous malformation; ASA, anterior spinal artery; PICA, posterior inferior cerebellar artery.

branches enter the vertebral canal through the inter- vertebral foramina to supply the spinal cord. Muscu- lar branches at the level of the lateral mass of C1 supply the deep cervical musculature.

COMMON CAROTID ARTERIES

The common carotid arteries proceed cephalad within the fibrous carotid sheath along with the internal jugular vein, the vagus nerve, and the ansa cervicalis. The common carotid arteries have no nor- mal branches before the carotid bifurcation, although rare variations may occur (Fig. 8A, B) (20). The ter- minal common carotid artery dilates to form the carotid bulb and bifurcates into the ICA and ECA. The bifurcation is typically located between the level of thyroid cartilage and the greater horn of the hyoid bone, although carotid bifurcations may lie either above or below this level (reported at the C1–C2 to the C6–C7 levels) (21,22). The anatomic level of the carotid bifurcation is more important when surgical rather than endovascular correction of carotid atherosclerotic disease is planned. The bifurcation is located between C3 and C5 in approximately 80% of patients, with the next common location at the C5–C6 level (13%) (22,23). The internal carotid artery (ICA) courses posterolateral to the ECA and then proceeds

medially to enter the carotid canal at the skull base (Fig. 8C, D).

External Carotid Artery

The ECA arises at the bifurcation of the common carotid artery in the neck and supplies the face, scalp, and dura primarily, with potential collateral contributions to the brain parenchyma and orbital contents (23). The ECA branches have many varia- tions. (Fig. 9). However, true ECA anomalies are rare, the most common being a so-called nonbifurcated common carotid artery, where the ECA branches arise separately from the common carotid trunk (24,25). Anomalous origin of the ECA from the aortic arch is also rarely encountered (26). The ECA courses anterolaterally from its initial position along the lat- eral pharyngeal wall as it passes beneath the posterior belly of the digastric and stylohyoid muscles and pierces the parotid fascia. The deep lobe of the parotid gland separates the ECA from the ICA (1,4, 5). Two schemes for categorizing the ECA branches according to cranial caudal or anterior and posterior locations have been proposed to pre- dict the vascular source of neovascularity or bleeding on the basis of cross-sectional imaging prior to inter- vention. In one scheme, the ECA branches are

6

Johnson et al.

6 Johnson et al. Figure 8 Cervical carotid variations. ( A ) Normal bifurcation, ( B

Figure 8 Cervical carotid variations. (A) Normal bifurcation, (B ) cervical loop, and (C ) ascending pharyngeal artery arise from the ICA. (D ) Hypoglossal artery with ICA occlusion. ( E ) Hypoglossal artery CT. ( F) Hypoglossal artery angiogram. ( G ) Fibromuscular dysplasia (FMD). Abbreviations : ICA, internal carotid artery.

(FMD). Abbreviations : ICA, internal carotid artery. Figure 9 ( A ) Lateral CCA injection reveals

Figure 9 ( A) Lateral CCA injection reveals a large facial artery (FAC) with dominant nasal supply compared with the smaller IMA contribution. Note the prominent nasal blush in this patient with epistaxis ( arrows ). ( B) Lateral CCA injection reveals a large IMA and smaller FAC in another patient. Rapid visualization of collateral circulation ( C ) from IMA to facial territory following FAC embolization and (D ) from FAC to IMA territory demonstrated in two different patients during embolization therapy for epistaxis. Abbreviations : CCA, common carotid artery; IMA, internal maxillary artery.

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1: Vascular Anatomy of the Head, Neck, and Skull Base 7 Figure 10 Terminal ECA branching.

Figure 10 Terminal ECA branching. Lateral view demonstrates the terminal branches of the ECA, the IMA, and the STA. Note the normal origins of the MMA and AMA from the IMA. Abbrevia- tions : ECA, external carotid artery; IMA, internal maxillary artery; STA, superficial temporal artery; MMA, middle meningeal artery; AMA, accessory meningeal artery; IMA, internal maxillary artery.

conceptually divided into three segments: (1) the lower cervical segment, (2) the middle segment (at the mandibular angle), and (3) the upper segment (in the area of the parotid gland). An alternative orga- nizational method is to consider the ECA branches as anterior and posterior branches. The anterior branches, listed in proximal to distal order, are the superior thyroid, lingual, and facial arteries. The posterior branches in proximal to distal order are the ascending pharyngeal artery (APA), occipital, and posterior auricular arteries. The branch order corresponds to the associated soft tissue structures, after which the vessels are named. The ECA termi- nates by bifurcating into the internal maxillary and superficial temporal arteries (Fig. 10A, B) (23).

Superior Thyroid Artery

The superior thyroid artery is usually the most prox- imal and anterior ECA branch and can be readily identified by the prominent thyroid blush after contrast injection. This artery may also arise from the carotid bifurcation or, occasionally, directly from the cervical common carotid artery (Fig. 11) (23,27). The superior thyroid artery arises from the anterior surface of the ECA and courses directly inferiorly alongside the gland to supply the superior pole of the thyroid gland and larynx. There is extensive collateralization with the contralateral superior

extensive collateralization with the contralateral superior Figure 11 Superior thyroid artery (SUT). The normal SUT (

Figure 11 Superior thyroid artery (SUT). The normal SUT (arrow ) is the first branch of the ECA and provides a dense arterial blush (*) to the richly vascular thyroid gland. Note the presence of multiple branches and the incidental anterior com- municating artery aneurysm. Abbreviation : ECA, external carotid artery.

thyroid artery and the inferior thyroid artery, which originates from the thyrocervical trunk. Rarely, injury to the artery may occur at the time of tracheostomy or laryngeal surgery, resulting in bleeding and/or pseu- doaneurysm formation (Fig. 12A, B).

Ascending Pharyngeal Artery

The APA is the first posterior ECA branch (23). Anteriorly directed APA branches supply the phar- ynx and eustachian tube. Posteriorly directed branches supply the tympanic cavity and preverte- bral muscles (Fig. 13A, B). The main trunk of the APA parallels the course of the ICA and can be occasionally mistaken for the ICA on ultrasound in the setting of internal carotid occlusion (a source of false-negative ultrasound screening examinations) (Fig. 14A, B) (28). The APA, in its location adjacent to the pharyngeal mucosal space, can be eroded by tumor and become the source of intractable bleeding (Fig. 15A, B). A small but clinically important branch vessel is the neuromeningeal branch, which supplies both the dura and lower cranial nerves. There are extensive anastomoses between the APA and the intracranial vasculature. These include rami anastomosing with the middle meningeal and accessory meningeal arteries of the external carotid circulation (23,29). There are also anastomoses with the internal carotid system via the inferior tympanic artery, which

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8 Johnson et al. Figure 12 Superior thyroid artery (SUT) pseudoaneurysm: peritracheal bleeding nine days after

Figure 12 Superior thyroid artery (SUT) pseudoaneurysm: peritracheal bleeding nine days after radical neck surgery, layngectomy, and tracheostomy. Oblique RCCA injection demonstrates faint blush from the distal SUT ( A) better seen on microcatheter injection (B ). It was successfully embolized with acrylic ( C). Abbreviation : RCCA, right common carotid artery. From Endovascular today and neurosurgical clinics .

From Endovascular today and neurosurgical clinics . Figure 13 Ascending pharyngeal artery. AP ( A )

Figure 13 Ascending pharyngeal artery. AP ( A) and lateral ( B ) angiograms of the normal APA that divides into an anterior (pharyngeal) and posterior division. Collaterals exist between the posterior division and the vertebral and between the anterior division and the internal carotid artery. (C ) Note the extensive neovascular supply ( arrows ) from the anterior division of the APA to this JNA. Abbreviations : APA, ascending pharyngeal artery; JNA, juvenile nasal angiofibroma.

anastomoses with the caroticotympanic artery of the petrous internal carotid. Other variable anastomoses may also exist between the APA and the vidian artery and inferolateral trunk. The APA may also anasto- mose with cervical branches of the vertebral artery via

the artery of the odontoid arch (Fig. 16). These poten- tial pathways of collateralization are extremely important to keep in mind during therapeutic embo- lization of the APA territory (23,29). Careful angio- graphic evaluation of t he APA branching pattern

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1: Vascular Anatomy of the Head, Neck, and Skull Base 9 Figure 14 Ultrasound pitfalls. (

Figure 14 Ultrasound pitfalls. ( AC) High-grade carotid stenosis misdiagnosed as ICA occlusion by ultrasound. An 80-year-old female had known bilateral carotid stenoses, which had previously been estimated at 90% on the right by ultrasound 5 months ago. Pulsed Doppler of right ICA (A ) shows increased peak systolic velocity and prominent diastolic flow. The more distal ICA could not be visualized, and the study reported RICA occlusion. By comparison, pulsed Doppler of the left ICA (B) shows a symmetric appearance of the diastolic flow on the left as compared with the right. A true occlusion of the RICA would demonstrate no diastolic flow in the ICA proximal to the occlusion. ( C ) A CTA 3D volume-rendered image with curved reformation confirms that the right ICA is severely narrowed, but patent. (D, E) APA mistaken for the ICA by ultrasound. Pulsed Doppler ultrasound ( D) image of a patient with congenital absence of the left ICA (same patient as shown in Fig. 32C–E) demonstrates an artery in the expected location of the ICA, which has low resistance flow. This vessel was mistaken for the ICA on initial ultrasound interpretation. A CTA 3D volume-rendered images shows the absent ICA ( E ). The APA lies parallel to the carotid sheath, and the presence of APA to ICA anastomoses lead to ‘‘internalization’’ of the waveform pattern, thus potentially causing confusion on ultrasound. Abbreviations: ICA, internal carotid artery; APA: ascending pharyngeal artery; RICA, right internal carotid artery.

pharyngeal artery; RICA, right internal carotid artery. Figure 15 APA extravasation (EXTRAV). ( A ) Lateral

Figure 15 APA extravasation (EXTRAV). (A) Lateral CCA injection demonstrates faint extravascular contrast in the region of the APA. (B ) Microcatheter injection reveals frank extravasation. (C ) Acrylic injection (CAST) resulted in cessation of bleeding. Abbreviations : APA, ascending pharyngeal artery; CCA, common carotid artery. From Endovascular today.

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10 Johnson et al. Figure 16 Artery of the odontoid arch. ( A ) Selective APA

Figure 16 Artery of the odontoid arch. (A ) Selective APA injection before embolization of skull base giant cell tumor (arrows ) demonstrates a midline vessel filling the vertebral artery from the APA. ( B) Note the vessel filling on the selective vertebral artery injection. Safe embolization requires the catheter to be positioned distal to the collateral branch. Abbreviation : APA, ascending pharyngeal artery.

branch. Abbreviation : APA, ascending pharyngeal artery. Figure 17 Lingual artery normal. ( A ) AP

Figure 17 Lingual artery normal. (A ) AP and ( B , C) lateral early- and late-phase images.

is imperative before therapeutic embolization is performed.

Lingual Artery

The lingual artery arises from the anterior surface of the ECA, loops upward, and proceeds anteriorly along the hyoid and deep into the hypoglossal muscle, to supply the ipsilateral tongue, sublingual gland, pharynx, and hyoid musculature (1,23). It may occasionally arise from a common trunk with the facial artery (Fig. 17). The lingual artery has a characteristic U-shape on AP and lateral views. Lingual artery injury, erosion, or laceration may result in pseudoaneurysm formation and massive bleeding (Fig. 18A, B).

Facial Artery

The facial artery is the third anteriorly oriented ECA branch. It ascends along the superior constrictor

muscle, passes deep into the stylohyoid and digastric muscles, and loops over the submandibular gland. It crosses the anterior as pect of the mandible and branches into the submental artery inferiorly, to supply the floor of mouth and submandibular gland. The facial artery and its superior branches course in an oblique fashion from the inferolateral aspect of the face, sup- plying the lips, face, palate, pharynx, and floor of the nasal cavity before terminating as the angular artery near the medial canthus of the eye (Fig. 19) (1,23).

Occipital Artery

The occipital artery is the second posteriorly oriented ECA branch, arising opposite the facial artery. It passes beneath the posterior belly of the digastric and sternocleidomastoid muscles providing muscular pen- etrating branches. It courses within the subcutaneous tissues of the posterior scalp and supplies the posterior

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1: Vascular Anatomy of the Head, Neck, and Skull Base 11 Figure 18 ( A )

Figure 18 (A) Massive oral bleeding. Axial CTA dem- onstrates radiation seeds in the tongue/floor of mouth on the left. A rounded collection of contrast is identified in the tongue consistent with a lingual pseudoaneurysm (arrow ). ( B) CTA coronal reconstruction demonstrates the pseudoaneurysm ( arrow ) and correlates with the

(C) AP external carotid arteriogram, where the pseu-

doaneurysm is identified as arising from the LIN.

(D) Lateral ECA arteriogram demonstrates the mark-

edly irregular lingual artery and the contrast extending into the pseudoaneurysm ( arrow ) arising from the irreg-

ular segment. Abbreviations : ECA, external carotid artery; LIN, lingual artery; FAC, facial artery.

carotid artery; LIN, lingual artery; FAC, facial artery. Figure 19 Facial artery nasal supply. ( A

Figure 19 Facial artery nasal supply. ( A) AP and ( B) lateral views of a FAC injection demonstrates marked vascular blush to the nasal arcade and a focal PSA in this patient with epistaxis. Abbreviations : FAC, facial artery; PSA, pseudoaneurysm.

skin, muscle, and meninges of the posterior fossa (1,24,30). Prominent muscular branches provide anasto- moses between the occipital and vertebral arteries, particularly in the setting of proximal stenosis or occlu- sion (Fig. 20A, B). It is important to recognize that meningeal branches pass intracranially through the hypoglossal and mastoid canals as well as through the jugular foramen. These branches can become enlarged in the setting of dural arteriovenous malformation (Fig. 21).

Posterior Auricular Artery

The posterior auricular artery arises from the poste- rior aspect of the ECA just above the level of the occipital artery (23). It may occasionally arise from or as a combined trunk with the occipital artery (30). The stylomastoid branch of the posterior auricular artery enters the styloma stoid foramen and sends branches to the chorda tym pani within the tympanic cavity, the mastoid, and the semicircular canals. The

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12 Johnson et al. Figure 20 Occipital artery. ( A ) Lateral selective occipital artery injection

Figure 20 Occipital artery. ( A) Lateral selective occipital artery injection demonstrates scalp branches and distal meningeal branches supplying a hypervascular meningioma ( arrows ). (B ) Lateral common carotid injection demonstrates prompt filling of the vertebral artery from muscular collaterals of the occipital artery. The anterior circulation fills via the posterior communicating artery in this patient with occlusive disease of the internal carotid artery. (C E ) OCC to vertebral muscular collaterals are demonstrated in this patient with left subclavian origin occlusion. ( C ) Illustrates reconstitution of the intracranial vertebral artery, while later phase lateral ( D) and AP (E) views demonstrate reconstitution of the cervical vertebral artery and distal subclavian. Abbreviation : OCC, occipital.

and distal subclavian. Abbreviation : OCC, occipital. Figure 21 Enlarged dural branches with dural arteriovenous

Figure 21 Enlarged dural branches with dural arteriovenous malformation. Lateral ECA arteriogram demonstrates an enlarged middle meningeal artery with shunting into the trans- verse sinus and middle meningeal vein. In addition, there are enlarged dural branches of the occipital artery shunting into the abnormal, distally occluded transverse sinus. Abbreviation : ECA, external carotid artery.

auricular branch supplies the scalp, the pinna, and the external auditory canal. A prominent but normal vascular blush is noted in the pinna after injection of the posterior auricular artery (Fig. 22). The stylo-

mastoid artery anastomoses with petrosal branches from the middle meningeal artery.

Superficial Temporal Artery

The ECA terminates within the parotid gland in the superficial temporal artery (STA) and the internal maxillary artery. From its origin within the parotid gland, the STA proceeds cephalad over the arch of the zygoma and divides into frontal and parietal branches. The STA is primarily a cutaneous artery supplying the anterior two-thirds of the scalp, the underlying cranium and musculature, and portions of the parotid gland, ear, and temporomandibular joint (1,23). Small local branches anastomose with the maxillary and facial artery branches of the upper portion of the face. The STA has a characteristic ‘‘hairpin’’ turn on angiography as it courses over the zygoma (Fig. 23). The superficial course of the STA renders it vulnerable to direct injury with resultant pseudoaneurysm formation. The pseudoaneurysms commonly present as pulsatile ‘‘lumps’’ on the fore- head or scalp following remote trauma (Fig. 24).

Internal Maxillary Artery

The internal maxillary artery courses deep to the neck of the mandible and enters the infratemporal fossa. It commonly passes horizontally between the heads of the medial and lateral pterygoid muscles and through the pterygomaxillary fissure into the pterygopalatine fossa (1,4,5,23). Three segmental divisions of the inter- nal maxillary artery are defined by the position of the artery relative to the pterygoid muscle. The first seg- ment gives rise to the inferior alveolar artery, which extends inferiorly along with the mandibular nerve to the mandibular foramen (Fig. 25). The middle and accessory meningeal arteries pass through the

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1: Vascular Anatomy of the Head, Neck, and Skull Base 13 Figure 22 PAA supplying AVM.

Figure 22 PAA supplying AVM. (A ) MRA 3D TOF axial source image demonstrates enlargement of the left pinna and increased signal intensity consistent with hypervascularity. Digital AP ( B) and early- and late-phase lateral ( C, D) views of a selective OCC artery injection demonstrates the PAA arising from the OCC (a normal variant) and a prominent blush with early venous drainage into the external jugular system secondary to a high-flow AVM of the pinna. Abbreviations : AVM, arteriovenous malformation; OCC, occipital; PAA, posterior auricular artery; TOF, time of flight.

PAA, posterior auricular artery; TOF, time of flight. Figure 23 Scalp AVM. ( A , B

Figure 23 Scalp AVM. ( A, B) AP and lateral selective STA angiograms demonstrate the enlarged feeders from the anterior division of the STA to an AVM of the scalp. Note the normal size of the STA posterior division and the early draining vein. Abbreviations : STA, superficial temporal artery. Abbreviation : AVM, arteriovenous malformation.

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14 Johnson et al. Figure 24 STA pseudoaneurysm. ( A , B ) Two patients with

Figure 24 STA pseudoaneurysm. ( A, B) Two patients with typical STA aneurysms ( arrows ) following direct trauma. Abbreviations : STA, superficial temporal artery; MMA, middle meningeal artery.

superficial temporal artery; MMA, middle meningeal artery. Figure 25 Internal maxillary artery. ( A , B

Figure 25 Internal maxillary artery. ( A, B) AP and lateral selective IMA injections demonstrate the three segments and the important branches. Abbreviations :

IMA, internal maxillary artery; MMA, middle meningeal artery; ACM, accessory meningeal artery; STA, super- ficial temporal artery.

foramen spinosum and ovale, respectively. The mid- dle meningeal artery has a characteristic curve as it exits the foramen spinosum that parallels the floor of the sella on lateral angiogram. The meningeal branches can be differentiated from the scalp branches by their straight rather than tortuous course. Remem- bering that ‘‘you can wrinkle your forehead, but you cannot wrinkle your dura’’ is a helpful key to differ- entiating these branches (Fig. 26). The middle menin- geal artery may be variable in size and may occasionally give rise to, or arise from, the ophthalmic artery (31). The deep auricular artery that supplies the external auditory canal and the anterior tympanic artery that supplies the tympanic membrane both arise from the first segment of the internal maxillary artery. The pterygoid segment (middle) is located in the high, deep masticator space and gives rise to masseteric, buccal, and deep temporal arteries. These supply the pterygoid and temporalis muscles and the lingual and buccal nerves. The third or sphenopala- tine segment of the internal maxillary artery lies within the pterygopalatine fossa and sends branches along with each nerve to the pterygopalatine ganglion

(Fig. 27). It terminates in multiple branches to the nasal cavity supplying both nasal wall and septum. The posterior superior alveolar artery supplies the palate and posterior wall of the maxilla. The infraor- bital artery passes through the infraorbital fissure along the orbital floor.

External Carotid Anastomotic Network

The importance of external carotid to internal carotid collaterals and potential anastomotic pathways cannot be overemphasized in the setting of disease and neurointervention (23,29,30,32). These interconnec- tions are dynamic and may change in appearance and flow rate during the interventional procedure, becoming most dangerous near the end of the proce- dure. The IMA has numerous extensive anastomoses with other ECA branches in the face. It is clinically relevant to appreciate the extensive collateral network between the lingual, facial, and internal maxillary artery branches. A complex hemodynamic balance exists between these pedicles. If a hypoplastic facial artery is present, large buccal and masseteric branches

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1: Vascular Anatomy of the Head, Neck, and Skull Base 15 Figure 26 Middle meningeal artery

Figure 26 Middle meningeal artery variations. The ophthalmic artery arises from the MMA in this patient. The reverse can also occur, posing potential problems for embolization. Abbreviations : MMA, middle menin- geal artery.

Abbreviations : MMA, middle menin- geal artery. Figure 27 IMA nasal arcade ( A ) AP

Figure 27 IMA nasal arcade ( A ) AP DSA injection into the distal ECA demonstrates the branches of the inter- nal maxillary artery and the nasal arcade ( arrows ). Note the STA and MMA arteries. ( B ) Magnified superselec- tive AP view better demonstrates the nasal arcade and prominent mucosal blush in this patient with epistaxis. Abbreviations : IMA, internal maxillary artery; DSA, dig- ital subtraction angiography; ECA, external carotid artery; STA, superficial temporal artery; MMA, middle meningeal artery.

will be present from the internal maxillary artery, and vice versa. During embolization therapy for epistaxis, it is not uncommon to appreciate anastomotic branches restoring proximal flow to an embolized territory (Fig. 28). External carotid to internal carotid anastomoses exist, and flow may proceed in either direction depend- ing on the location and nature of the diseased vascu- lature. The distal ethmoidal branches of the IMA anastomose with distal ethmoidal branches of the oph- thalmic artery. Thus the IMA, via these ethmoidal collaterals, may provide a supply route to the supra- clinoid ICA via reversal of flow through the ophthalmic artery. The vidian artery anastomoses with the petrous ICA. The artery of the foramen rotundum and the inferolateral trunk anastomose with the cavernous ICA. These ECA-ICA anastomoses vary to a significant degree among patients and offer a clinically significant

collateral pathway between the ECA and the ICA systems, seen most prominently in the setting of occlu- sive vascular disease (Fig. 29A, B) (23,29). With occlu- sion of the ECA, ICA branches may collaterally restore external carotid flow (Fig. 30) (23,29).

Internal Carotid Artery

The ICA enters the skull base through the carotid canal ascending anterior to the jugular bulb and pos- terior to the eustachian tube (1,4,5,33). The ICA pet- rous segment courses anteromedially to the tympanic cavity, giving rise to the caroticotympanic artery (to the tympanic cavity), the vidian artery, and small periosteal branches (34). The ICA courses superiorly, extending above the foramen lacerum to pierce the dura and enter the posterior aspect of the cavernous sinus (Fig. 31). The ICA is occasionally congenitally

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16 Johnson et al. Figure 28 Epistaxis: the importance of ophthalmic collaterals. ( A ) ICA

Figure 28 Epistaxis: the importance of ophthalmic collaterals. (A) ICA injection at the time of initial epistaxis embolization demonstrates normal terminal ophthalmic artery branches. ( BD) One month later, the patient presents with recurrent epistaxis, and sequential ICA images demonstrate reconstitution of the nasal arcade by ophthalmic collaterals. Abbreviation : ICA, internal carotid artery.

collaterals. Abbreviation : ICA, internal carotid artery. Figure 29 Extensive collaterals to the petrous, cavernous,

Figure 29 Extensive collaterals to the petrous, cavernous, and supraclinoid ICA from the branches of the internal maxillary artery. (A ) IMA to OPH to ICA ethmoidal collaterals. ( B) Vidian artery and inferolateral trunk to the petrous ICA. Note the occipital to vertebral artery muscular collaterals. Abbreviations : ICA, internal carotid artery; AMA, acessory meningeal; MMA, middle meningeal artery; OPH, ophthalmic artery.

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1: Vascular Anatomy of the Head, Neck, and Skull Base 17 Figure 30 Restoration of ECA

Figure 30 Restoration of ECA flow. (A) Lateral CCA arteriogram demonstrates extravasation of contrast from the proximal ECA at the origin from the carotid bulb. Note the radiation seeds and the small occipital artery identified before embolization. ( B) Following par- tial embolization of the ECA and occlusion of the right CCA. Control arteriogram demonstrates filling of the ipsilateral vertebral artery with filling of a large muscular collateral with reconstitution of the occipital artery and retrograde filling of the ECA with continued extravasa- tion into the pharynx. Control of bleeding required particulate embolization for occlusion and disconnec- tion of the muscular collateral to the occipital artery. Abbreviations : ECA, external carotid artery; CCA, com- mon carotid artery.

ECA, external carotid artery; CCA, com- mon carotid artery. Figure 31 The dural ring. The ICA

Figure 31 The dural ring. The ICA enters the cavernous sinus dura, traverses the sinus and exits at the dural ring. This patient presented with SAH and demonstrates and ICA posterior wall aneurysm. The arrow marks the location of the dural ring on the conventional angiogram (A ) and on 3D CTA ( B ). The trigeminal artery is a primative communication between the cavernous carotid segment and the distal one-third of the basilar artery identified on conventional angiogram ( C) and on 3D CTA (D ). Abbreviation : ICA, internal carotid artery; SAH, subarachnoid hemmorhage.

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18 Johnson et al. Figure 32 ICA anomalies. ( A ) CT and ( B )

Figure 32 ICA anomalies. (A) CT and ( B) AP angiogram demonstrate the aberrant ICA with the characteristic lateral position of the ICA (arrow ) projecting into the middle ear cavity behind the tympanic membrane. The carotid canal is incomplete and the carotid is usually narrowed just distal to the middle ear segment. ( C) CT and (D, E ) CTA in agenesis of the ICA demonstrate absence (*) of the carotid canal in addition to the absence of the ICA. Abbreviation : ICA, internal carotid artery.

absent and can be differentiated from acquired occlu- sion by the absence of the carotid canal at the skull base (Fig. 32A, B) (35). Nomenclature varies, but the four-part division of the internal carotid, designated as C1–C4 and described in the radiology and surgical literature, is useful. The cervical segment (C1) begins proximally at the origin of the ICA with the CCA and extends cephalad to the external orifice of the carotid canal. The petrous segment (C2) traverses the carotid canal and enters the cavernous sinus (dura), where the cavernous segment (C3) begins. The cavernous seg- ment ends where the ICA pierces the dural roof of the cavernous sinus. The supraclinoid segment (C4) begins where the ICA exits the dural ring and enters the subarachnoid space, and it ends at the internal carotid bifurcation into anterior and middle cerebral artery branches (34,36). The supraclinoid segment passes medially to the anterior clinoid and below the optic nerve. Together, the C3 and C4 segments form the characteristic ‘‘S’’ shape seen on lateral and oblique angiographic views of the skull base. C1 does not normally provide any branches. C2 gives rise to three potential branches: the caroticotympanic branch supplying the middle and inner ear; the vidian artery, or the artery of the pterygoid canal,

which goes through the foramen lacerum; and the artery of the foramen rotundum (35,36). C3 gives rise to three trunks. The posterior trunk, or the meningo- hypophyseal trunk, branches into the tentorial artery (of Bernasconi and Casinari) supplying the tento- rium, the inferior hypophyseal artery supplying the posterior pituitary capsule, and the dorsal meningeal artery supplying the abducens nerve and the clivus (35,36). The lateral trunk, or inferior cavernous sinus artery, supplies the infero lateral cavernous sinus wall and region of the foramen ovale and spinosum. The medial trunk, or McConnel’s capsular artery, supplies the anterior and inferior pituitary capsules and is present in only 28% of the population (33,34,36). A pituitary blush is commonly identified on lateral internal carotid arteriograms. These small branches become important in the analysis of skull base tumors and provide potential anastomoses with external carotid branches in the setting of disease (Figs. 32 and 33) (33,34,36).

VEINS OF THE HEAD, NECK, AND SKULL BASE

The venous drainage of the face is predominantly super- ficial and empties into the external jugular drainage pathways (1,4,5). The supraorbital and supratrochlear

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1: Vascular Anatomy of the Head, Neck, and Skull Base 19 Figure 33 Cervical and facial

Figure 33 Cervical and facial veins. ( A) The proximal internal and external jugular veins are demonstrated as approached from the femoral route. ( B, C) Facial veins drain into the EJV. ( D , E) Nasal and facial structures may drain superiorly into the superior and or inferior ophthalmic veins. Abbreviations : EJV, external jugular vein; SOV, superior ophthalmic veins.

veins of the face join to become the angular vein and proceeds as the facial vein over the angle of the man- dible (1,4,5). The pterygopalatine venous plexus is located around and within the lateral pterygoid muscle. It may be recognized on CT as a focal area of irregular enhancement adjacent to the muscle. It is often identi- fied as a variation in the cerebral venous drainage pattern on cerebral angiography, receiving flow from the greater middle cerebral (sylvian) vein (Fig. 34A, C). The pterygopalatine venous plexus drains into a pair of maxillary veins, which lie deep in the neck of the mandible and join with the temporalis vein draining the temporal region of the face and scalp to form the retromandibular vein. The inferior ophthalmic vein travels with the infraorbital artery and drains into the cavernous sinus intracranially and the pterygopalatine venous plexus extracranially.

Occasionally, the facial veins will drain superi- orly into the ophthalmic veins and into the cavernous sinus as a normal variation in the absence of shunting (37). The retromandibular vein passes through the parotid gland and divides into anterior and posterior branches that drain into the internal and external jugular veins, respectively. The deep facial vein rep- resents the anastomosis between the pterygopalatine venous plexus and the facial vein. The anterior jugu- lar veins lie in the submental region extending infe- riorly to the suprasternal notch, where they communicate with the external jugular vein deep to the sternocleidomastoid muscle. The external jugular also receives the posterior auricular vein. The external jugular vein empties into the subclavian vein near the midpoint of the clavicle. The internal jugular vein originates from the jugular bulb receiving blood from

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20 Johnson et al. Figure 34 Prominent PVP ( A ) Axial CTA image demonstrates asymmetry

Figure 34 Prominent PVP (A) Axial CTA image demonstrates asymmetry of the PVP, prominent on the left ( arrows )—possible normal variant versus AVM. Digital subtraction images of the venous phase after ICA injection in AP ( B ) and lateral ( C) projections demonstrate a prominent sylvian (greater middle cerebral) vein ( arrows ) draining into an unusually large PVP (arrow ), which subsequently drains into the external jugular vein. This arrangement is a normal anatomic variant. Abbreviation : PVP, pterygopalatine venous plexus; AVM, arteriovenous malformation; ICA, internal carotid artery.

arteriovenous malformation; ICA, internal carotid artery. Figure 35 Veins at the skull base. ( A )

Figure 35 Veins at the skull base. ( A ) Late venous-phase DSA image in AP projection after arterial injection shows the normal course of the skull base venous sinuses. (B , C ) DSA images in AP and lateral projections demonstrate the course of the IPS, which is oriented medially and anteriorly. (D) DSA image in AP projection from another patient after right IJV injection demonstrates venous communication with contrast filling the right IPS and refluxing into the left IPS. Note the cavernous sinus filling. Abbreviations : DSA, digital subtraction angiography; IPS, inferior petrosal sinus; SIG, sigmoid sinus; IJV, internal jugular vein.

the sigmoid sinus and its first extracranial tributary, the inferior petrosal sinus (Fig. 35A–C) (37,38). It descends behind the ICA directly adjacent to the arch of C1, where it joins the subclavian vein to become the brachiocephalic vein. The left brachioce- phalic vein joins at the right of the second costal cartilage to become the superior vena cava.

SUMMARY

Knowledge of the normal and variant anatomy of the head, neck, and skull base is critical to the under-

standing of its vascular pathology and to the safe performance of diagnostic and therapeutic angiogra- phies. Correlation with cross-sectional imaging is use- ful in the anticipation of vascular supply and dangerous anastomoses.

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1. Johnson MH. Head and neck vascular anatomy. Neuro- imaging Clin N Am 1998; 8:119–141.

2. Langman J. Medical Embryology. 3rd ed. Baltimore, MD:

William & Wilkins, 1975.

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Haughton VM, Rosenbaum AE. The normal and anoma- lous aortic arch and brachiocephalic vessels. In: Newton

Angiography, vol 2. Great Neck, NY: Mosby, 1974:1145–

branches and high division of the internal carotid artery. Okajimas Folia Anat Jpn 1986; 63(1):37–43.

TH, Potts GN, eds. Radiology of the Skull and Brain:

21. Lo A, Oehley M, Bartlett A, et al. Anatomical variations of the common carotid artery bifurcation. ANZ J Surg 2006;

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adults: implications for geometric risk of atherosclerosis. Stroke 2005; 36:2450–2456.

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variant in humans: clarification of a common misnomer. AJNR Am J Neuroradiol 2006; 27(7):1541–1542.

26. Cakirer S, Karaarslan E. Aortic arch origin of the left external carotid artery. AJNR Am J Neuroradiol 2003; 24

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of the right vertebral artery: review of the literature and case report of right vertebral artery origin distal to the left subclavian artery. AJNR Am J Neuroradiol 1999; 20

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29. Mishkin MM, Schreiber MN. Collateral circulation in Newton TH and Potts DG, eds. Angiography. Radiology of the Skull and Brain, vol 2, book 4. St Louis, MO: Mosby

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2

Applied Neurovascular Anatomy of the Brain and Skull

Randy S. Bell, Alexander H. Vo, and Rocco A. Armonda

Departments of Neurosurgery and Radiology, National Naval Medical Center, and Comprehensive Neurosciences Program, Uniformed Services University of Health Sciences, Bethesda, Maryland, U.S.A.

INTRODUCTION

Advances in imaging and materials technology have expanded the array of pathologies treatable through less invasive endovascular approaches. The resultant benefit to the patient manifested by increased inter- ventional success rates and reduced morbidity and mortality cannot be overstated. However, the utility of even the most advanced biplanar machine with 3D rotational capabilities is limited without a thorough understanding of the craniocerebral angiographic anatomy. This understanding must, of necessity, include the significant arterial anastomoses and col- lateral circulatory patterns that should be considered during any intervention. Collateral circulation may prevent significant neurologic deficit should parent artery occlusion (PAO) be required. That said, known circulatory anastomoses could result in infarct distal to the area of embolization or PAO. The purpose of this chapter is to provide an in-depth review of the normal cerebrovascular angiographic anatomy as well as the significant internal, external, and vertebrobasi- lar anastomoses. Additionally, high-quality gross ana- tomic specimens will be shown with the basic angiogram to emphasize the importance of surround- ing neurologic structures. The importance of the con- tribution of individual anatomy in the formulation of any treatment plan will also be emphasized. Because thorough reviews of anatomic variants have been provided elsewhere (1–5), only brief descriptions will be highlighted where considered relevant.

INTERNAL CAROTID ARTERY

The internal carotid artery (ICA) originates from the common carotid artery in the neck at the approximate level of the fourth cervical vertebrae. Though several segmental naming schemes exist, this chapter will refer to that provided by Rhoton (5). The cervical segment (C1) ascends to the base of the skull without producing any branches (Fig. 1B). It enters the skull through the carotid canal to become the horizontal petrous portion (C2). This segment is seen as the first medial turn on a standard anterior-posterior (AP) projection and as the

first anterior turn on a lateral projection (Fig. 1A). The vidian and caroticotympanic branches originate from this segment. The artery then takes a 908 superior turn at the foramen lacerum and becomes the cavernous portion (C3). The segment is manifested as a double arterial density on a standard AP projection and as an anteriorly projecting hairpin turn on a lateral projec- tion. Branches within this segment include the menin- gohypophyseal trunk, the inferolateral trunk, and McConnell’s capsular arteries. The ophthalmic artery may occasionally originate from this segment. The meningohypophyseal trunk gives rise to the tentorial artery of Bernasconi and Cassinari [important during embolization of tentorial meningiomas or tentorial arteriovenous malformation (AVM) (Figs. 2 and 3)], the dorsal meningeal artery, and the inferior hypophy- seal artery. The artery then progresses caudally and laterally as it exits the cavernous sinus and enters the subarachnoid space through an inner and outer dural ring to become the supraclinoid segment (C4). The ophthalmic, superior hypophyseal, posterior commu- nicating, and anterior choroidal arteries arise from this segment (Fig. 4). The internal carotid then bifurcates into the anterior and middle cerebral arteries (MCAs).

The Ophthalmic Artery

The ophthalmic artery arises from the anterior wall of the ICA as its first intradural branch (Fig. 4). In 8% of cases, the artery may arise from within the cavernous sinus (5). It then travels in an anterior direction and enters the orbit through the optic canal along with the optic nerve. A recurrent meningeal branch may inter- mittently arise from the orbital portion of the ophthal- mic artery, traveling back through the superior orbital fissure to supply the meninges in that area. It continues forward and gives rise to the anterior and posterior ethmoidal arteries. The remaining terminal branches of the ophthalmic artery are the central retinal, lacrimal, long and short ciliary, supraorbital, medial palpebral, infratrochlear, supratrochlear, and dorsal nasal arte- ries (5). Significant collateral circulation exists between the ophthalmic artery and the internal maxillary (long sphenopalatine communication via the ethmoidal

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24 Bell et al. Figure 1 AP ( A ) and lateral ( B ) angiogram

Figure 1 AP (A) and lateral ( B ) angiogram of the ICA. The segmental scheme of Rhoton is provided. C1 extends from the carotid bifurcation to its entrance into the carotid canal. C2 extends from this point, through the petrous bone, to the foramen lacerum. C3 constitutes the intracavernous segment. The supracli- noid segment (C4) continues from the cavernous sinus to the ICA bifurcation. Abbreviation : ICA, internal carotid artery.

bifurcation. Abbreviation : ICA, internal carotid artery. Figure 2 T1-weighted axial MRI through the rostral

Figure 2 T1-weighted axial MRI through the rostral midbrain. A tentorial AVM is shown. The black arrow (Figure 3) indicates the location of the tentorial artery of Bernasconi and Cassinari within the paramesencephalic cistern.

arteries), the middle meningeal (via the ethmoidal arteries), and the superficial temporal artery (via the lacrimal and zygomatic-orbital arteries) (1,2).

The Posterior Communicating Artery

The posterior communicating artery arises from the posteromedial aspect of the ICA (Figs. 4, 5, and 13). It terminates at the posterior cerebral artery (PCA) and is the boundary between the P1 and P2 segments of that artery. In approximately 22% of cases, the posterior communicating artery is larger than the PCA or fails to fuse with the PCA and becomes the dominant

PCA or fails to fuse with the PCA and becomes the dominant Figure 3 Lateral angiographic

Figure 3 Lateral angiographic projection of the right ICA. The black arrow again indicates the location of the tentorial artery. Note the venous outflow to the superior sagittal sinus. Abbrevia- tion : ICA, internal carotid artery.

circulation to the PCA territory (1,4,5). Anatomically, it courses below the edge of the tentorium just superior to the third cranial nerve (Fig. 5). There are multiple small perforating arteries that arise from the posterior communicating artery. The largest of these arteries is called the premamillary artery (1,5). The perforating arteries are divided into anterior and posterior perfo- rating arteries. The anterior perforators supply neuro- logic tissue within the posterior limb of the internal capsule, the anterior thalamus, the posterior hypothal- amus, and the anterior one-third of the optic tract, while the posterior perforators penetrate the rostral midbrain and supply the subthalamic nucleus (1).

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2: Applied Neurovascular Anatomy of the Brain and Skull 25 Figure 4 Lateral angiogram of the

Figure 4 Lateral angiogram of the C4 segment of the ICA. Note the anterior course of the ophthalmic artery as it passes through the optic canal with the optic nerve. The black arrow identifies the course of the artery as it passes superior to the optic nerve. Significant terminal branches are noted. The posterior communi- cating and anterior choroidal arteries are also easily seen in this view. Abbreviations: ICA, internal carotid artery; AchA, anterior choroidal artery; pCom, posterior communicating artery; LA, lac- rimal artery; CrA, central retinal artery; PeA, posterior ethmoidal artery; AeA, anterior ethmoidal artery.

posterior ethmoidal artery; AeA, anterior ethmoidal artery. Figure 5 Gross anatomic specimen from Rhoton. The branches

Figure 5 Gross anatomic specimen from Rhoton. The branches of the ICA are viewed in an axial plane from below. Note the location of the CN III with respect to the PCoA. and the AChA. The cisternal segment of the AChA can be seen traveling toward the temporal horn of the lateral ventricle and the choroid plexus within. The M1 segment of the MCA is also shown with numerous lenticulostriate arteries traveling superiorly through the anterior perforated substance to supply portions of the basal ganglia. Abbreviations : ICA, internal carotid artery; AChA, anterior cho- roidal artery; PCoA, posterior communicating artery; CN III, third cranial nerve; LentStrA, lenticulostriate arteries; MCA, middle cerebral artery. Source : From Ref. 5.

The Anterior Choroidal Artery

The anterior choroidal artery is the last named branch arising from the ICA prior to its bifurcation (Figs. 4 and 5). It travels in a posterolateral direction toward the choroidal point and the choroid plexus of the temporal horn of the lateral ventricle. The artery is

of the temporal horn of the lateral ventricle. The artery is Figure 6 Lateral angiogram, arterial

Figure 6 Lateral angiogram, arterial phase, of the ICA. The branches and segments of the ACA are delineated. The A1 segment extends from the carotid bifurcation to the anterior communicating artery. The A2–A5 segments are then named based on their location with respect to the corpus callosum. The anterior and posterior internal parietal arteries are not well visualized on this injection. Abbreviations : ACA, anterior cerebral artery; ICA, internal carotid artery; A1, precommisural segment; A2, infracallosal segment; A3, precallosal segment; A4, supra- callosal segment; A5, posterocallosal segment; FpA, frontopolar artery; AntIFA, anterior internal frontal artery; CmA, callosomar- ginal artery; MidIFA, middle internal frontal artery; PostIFA, pos- terior internal frontal artery; PeriA, pericallosal artery; PcA, precentral artery.

broken into the cisternal (within the subarachnoid cisterns) and plexal (within the lateral ventricles and choroids plexus) segments. Small perforating vessels arise from the cisternal segment and are not visualized on a lateral angiogram. These arteries supply the optic tract, the cerebral peduncle, the mesial temporal lobe, and the lateral geniculate body.

The Anterior Cerebral Artery

The anterior cerebral artery (ACA) can be broken down into five anatomic segments on the basis of its location with respect to the underlying corpus cal- losum (Figs. 6 and 7). The A1 segment, or the pre- communicating segment, extends from the ICA bifurcation to the anterior communicating artery. Usually, small perforating branches feed the optic chiasm, hypothalamus, and anterior corpus callosum, though they are not typically visible on a normal four- vessel cerebral angiogram. The recurrent artery of Heubner may occasionally arise from this segment, though it primarily originates from A2 (Fig. 13). This artery is not commonly visualized on a basic

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26 Bell et al. Figure 7 Gross anatomic specimen, sagittal plane through the falx cerebri. The

Figure 7 Gross anatomic specimen, sagittal plane through the falx cerebri. The segments of the ACA are shown with surrounding neurologic structures (com- pare with Fig. 6). The ACA feeds the paracentral lobule, which is responsible for motor control of the contralateral leg. Abbreviation: ACA, anterior cerebral artery; Call- MargA, callosomarginal artery. Source: From Ref. 5.

Call- MargA, callosomarginal artery. Source : From Ref. 5. Figure 8 AP ( A ) and

Figure 8 AP ( A) and lateral ( B) injection of the ICA. The MCA segmental anatomy is shown. M1 starts at the ICA bifurcation and ends at the LI. M2 continues to the sharp (>90 8 on AP) turn at the CS. M3 travels over the frontal, temporal, and parietal Op to terminate as the distal, cortical M4 branches. Abbreviations : ICA, internal carotid artery; MCA, middle cerebral artery; LI, limen insula; CS, circular sulcus; Op, operculum.

diagnostic angiogram. The remaining postcommuni- cating segments include the infracallosal (A2), the precallosal (A3), the supracallosal (A4), and the post- erocallosal (A5). The A2 segment typically starts at the anterior communicating artery and extends to the bifurcation of the pericallosal and callosomarginal arteries. The frontopolar and orbitofrontal arteries arise from this segment. Subserved neurologic tissue includes the hypothalamus, septum pellucidum, ante- rior commisure, columns of the fornix, and portions of the basal ganglia. The A3 segment includes the callosomarginal and pericallosal arteries. The A4 and A5 segments involve the terminal branches of the ACA, including the arteries that provide collateral flow to certain areas within the MCA and PCA distributions (Fig. 8).

The Middle Cerebral Artery

The MCA originates from the internal carotid and travels in a course parallel to the floor of the middle cranial fossa. The artery partitions into four anatomic

segments, and like the other cerebral arteries organized in this fashion, the segments are based on surrounding cerebral anatomy rather than arterial branch points (Fig. 8A, B). The M1 segment extends from the ICA to the 908 turn that the artery takes at the limen insula (Figs. 8 and 9). The MCA bifurcation may occur prior to or after this point. The M1 segment is characterized by multiple small perforating arteries that feed the lentiform nuclei and the anterior limb of the internal capsule. These lenticulostriate arteries are divided into medial, intermediate, and lateral groups and originate from the superior wall of the M1 segment and travel through the anterior perforated substance to the deep hemispheric nuclei (Figs. 12 and 13). The M2 segment extends from the limen insula to the second turn of the artery at the circular sulcus. Although the M2 branches are distinguishable on a lateral angiogram, they appear as a group of double densities on an AP view. The gross anatomic lateral view of the insula clearly displays the complex arterial anatomy in this region (Fig. 11). The M3 segment specifically refers to the course of the vessels over the frontal, parietal, and

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2: Applied Neurovascular Anatomy of the Brain and Skull 27 Figure 9 Gross anatomic specimen, coronal

Figure 9 Gross anatomic specimen, coronal view of the brain. The MCAs are shown with surrounding anat- omy (compare with Fig. 8A). The single white area indicates the location of the limen insula. The double white arrow highlights the sharp turn of the MCA at the circular sulcus. Three white arrows approximate the location of the operculum. Abbreviations : PCA., poste- rior cerebral artery; LentNucl, lentiform nuclei; LentStrA, lenticulostriate arteries; MCA, middle cerebral artery; ACA, anterior cerebral artery. Source : From Ref. 5.

temporal opercula. The M4 segment refers to the terminal cortical branches (Fig. 10). It is important to remember that some of the distal MCA vessels feed non-eloquent cortex (i.e., the temporopolar artery); however, vessels feeding the central area bilaterally (primary motor cortex) and the angular area on the left could result in significant neurologic deficit should sacrifice occur. Specifically, sacrifice of the superior trunk of the MCA on the left could result in a Gerst- mann’s syndrome (right–left dissociation, acalculia, agraphia without alexia, finger agnosia), while sacrifice of the same artery on the right might result in asomatagnosia.

Anatomic Considerations

Aneurysms and other vascular malformations of the distal intracranial circulation present difficult treat- ment scenarios. As a general rule, aneurysms distal to the circle of Willis tend to rupture regardless of size (6,7) and therefore require treatment at the time of diagnosis. The possible exception may include the distal aneurysms that result from the aberrant high- flow state associated with AVMs (8,9). Although open surgery was advocated prior to the advent of endo- vascular treatment strategies, a combined approach is now often necessary. The following will examine the unique anatomic circumstances that must be consid- ered prior to treatment of distal intracranial circula- tion pathology.

The Anterior Cerebral Artery

The ACA and its branches supply the cortex within the interhemispheric fissure. Since this network includes the cingulate cortex and the paracentral lobule, clinical consequences from pathology in this area may manifest as lower extremity paresis or memory impairment (Fig. 7) (8,10,11). Surgica l approaches to vascular

(Fig. 7) (8,10,11). Surgica l approaches to vascular Figure 10 Late arterial phase injection, lateral view,

Figure 10 Late arterial phase injection, lateral view, of the ICA. The distal MCA vessels are shown with approximate named locations. The dense tangle of vessels approximates the location of the insula. Abbreviations : MCA, middle cerebral artery; Ofr, orbitofrontal artery; PreFr, prefrontal artery; PreCen, precentral artery; Cen, central artery; Ang, angular artery; OccTemp, tem- porooccipital artery; PostTemp, posterior temporal artery; Mid- Temp, middle temporal artery; AntTemp, anterior temporal artery; Tp, temporopolar artery.

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28 Bell et al. Figure 11 Gross anatomic specimen of the arterial anatomy of the insula

Figure 11 Gross anatomic specimen of the arterial anatomy of the insula (compare with Fig. 8B). The opercular cortices have been retracted to show the insula and vessels. Abbreviations : SupTr, superior trunk; InfTr, inferior trunk. Source : From Ref. 5.

trunk; InfTr, inferior trunk. Source : From Ref. 5. Figure 12 AP angiogram of the ICA,

Figure 12 AP angiogram of the ICA, magnified view of the ICA bifurcation. The ML, IL, and LL arteries can be seen. Note the origin from the superior aspect of the MCA with a course through the anterior perforated substance to supply the lentiform nuclei. Abbreviations : ICA, internal carotid artery; MCA, middle cerebral artery; ML, middle lenticulostriate; IL, intermediate lenticulostri- ate; LL, lateral lenticulostriate.

pathology in this area are technically difficult and require extensive preoperative planning (6,8). Consid- erations include the possibility of disruption of venous drainage to the superior sagittal sinus from surgical exposure and retraction, the neurologic consequences to frontal lobe retraction, and variable anatomy. Endovascular treatments of distal ACA pathology are technically challenging because of vessel tortuosity and reduced distal vessel caliber. However, the possible neuropsychiatric consequences of open surgery can be avoided. Treatment with platinum coils of narrow-

can be avoided. Treatment with platinum coils of narrow- Figure 13 Gross anatomic specimen, anterosuperior view

Figure 13 Gross anatomic specimen, anterosuperior view of the ICA bifurcation (compare with Fig. 12). The small lenticulos- triate arteries are indicated by white arrows. The recurrent artery of Heubner can also be seen arising from the A2 segment of the ACA. Abbreviations : ICA, internal carotid artery; ACA, anterior cerebral artery; PCoA, posterior communicating artery; RecA, recurrent artery of heubner; MCABr, middle cerebral artery branches; FrontBr, frontal branch. Source : From Ref. 5.

necked, distal ACA saccular aneurysms alone is a rea- sonable approach because anterograde flow through the preserved parent artery may be possible. However, it may be necessary at times to sacrifice the parent artery when balloon remodeling or stent-assisted coiling of a wide-necked or fusiform aneurysm is not feasible (Fig. 14A, B). In this case, sufficient collateral circulation from the PCA circulation may be seen (Fig. 23). Parent artery occlusion (PAO) proximal to the pericallosal- callosomarginal artery bifurcation (A2–A3) may result in some or all of the neurologic consequences previously outlined. Occlusion distal to this vessel segment may be clinically silent secondary to the extensive collateral

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2: Applied Neurovascular Anatomy of the Brain and Skull 29 Figure 14 Magnified lateral ( A

Figure 14 Magnified lateral (A) and plane lateral injection of the ICA. An irregular dilation of the A3 segment of the ACA (A, black arrow ) is noted in a patient with traversing penetrating head trauma and subarachnoid hemorrhage. The treatment strategy included PAO using detachable platinum coils ( B, black arrow ). Abbreviation : ACA, anterior cerebral artery; PAO, parent artery occlusion.

circulation between the anterior and posterior cerebral circulation through the posterior pericallosal and sple- nial arteries. Kim et al. describe an elegant combined open surgical and endovascular approach to an A2 ane- urysm, where the distal artery arose from the aneurysm dome. In this case, a side-to-side pericallosal-pericallosal anastomosis was performed prior to unilateral endovas- cular PAO of the A2 segment. This anastomosis resulted in preservation of distal flow to both hemispheres and obliteration of the complex aneurysm (12).

The Distal Middle Cerebral Artery

The MCA supplies hemispheric structures, including the lentiform nuclei, the lateral aspect of the frontal, parietal, and temporal cortices, and the insular cortex. Clinical sequelae from arterial occlusion are largely based on which segment of which MCA (right or left) is occluded, with symptoms ranging from contrala- teral hemiparesis or hemianesthesia to aphasia and calculation difficulties. MCA bifurcation aneurysms are difficult to treat endovascularly because of the tendency toward wide- necked morphologies or because of bifurcation arteries distal to the aneurysm arising from the aneur- ysm dome. Fusiform aneurysms or giant MCA bifur- cation aneurysms may require PAO in combination with open surgical clipping and bypass (13,14). Weill et al. describe two cases of giant MCA trifurcation aneurysms that were successfully treated with EC-IC bypass and subsequent PAO. In these cases, the M1 segment was coil occluded in a patient with an intact circle of Willis, while the supraclinoid internal carotid was coiled in the patient with an absent anterior communicating artery (14).

Mycotic aneurysms that form in the distal MCA circulation may rupture and cause subarachnoid hem- orrhage, or they may resolve on antibiotics (15). Recurrent hemorrhage or interval angiographic enlargement may push the surgeon to intervene. Sev- eral studies have demonstrated successful obliteration of the distal aneurysm through endovascular occlu- sion (16–20). Sodium amytal injection has been used to determine whether parent artery occlusion (PAO) will be tolerated. However, this procedure’s low sensitiv- ity may not accurately reflect the lack of postocclusion neurologic deficit with a negative result. In cases of distal aneurysm formation in eloquent arterial terri- tories, it may be necessary to accept the possibility of neurologic deficit to reduce the risk of potentially fatal subarachnoid hemorrhage (Fig. 15 A, B). For M4 occlusions, collateral flow from the ACA may reduce the neurologic deficit that would occur from a central arterial occlusion (motor strip).

PERSISTENT CAROTICOBASILAR ANASTOMOSES

Persistent fetal circulatory patterns refer to anastomoses between the carotid and basilar arterial systems, includ- ing the persistent trigeminal, otic, hypoglossal, and proatlantal arteries (Fig. 16). These structures are pres- ent embryologically, normally recede through vessel atresia, and are associated with other vascular malfor- mations (21–26). The trigeminal artery is the most com- mon, occurring in 0.1% to 0.2% of the general population. This artery typically arises from the preca- vernous carotid and anastomoses with the distal basilar artery (Fig. 17). The persistent otic artery arises from the petrous portion of the carotid artery and terminates at

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30 Bell et al. Figure 15 Lateral angiogram ( A ) and magnified lateral angiogram of

Figure 15 Lateral angiogram ( A ) and magnified lateral angiogram of the ICA. The black arrows indicate the focal dilation of the distal MCA consistent with the presence of a mycotic aneurysm. Abbreviations : ICA, internal carotid artery; MCA, middle cerebral artery.

: ICA, internal carotid artery; MCA, middle cerebral artery. Figure 16 Lateral angiographic cartoon representation of

Figure 16 Lateral angiographic cartoon representation of the types of persistent caroticobasilar anastomoses. A fetal PCA (a) is shown, though this type is common enough to be considered a normal variant. The persistent trigeminal artery (b) originates from the cavernous segment of the ICA and terminates at the basilar artery. The persistent otic artery (c) originates from the petrous portion of the ICA and terminates at the proximal basilar artery. Both the persistent hypoglossal (d) and persistent proat- lantal (e) arteries arise from the extracranial ICA and terminate at the vertebral artery. C1 and C2 indicate the location of the first and second cervical vertebrae. Abbreviation : PCA, posterior cerebral artery; ICA, internal carotid artery.

the anterior inferior cerebellar artery (AICA) or basilar artery (1). There are less than five reported cases of this type in the literature. The persistent hypoglossal artery arises from the extracranial ICA, passes through the anterior condyloid foramen, and terminates at the distal basilar artery. The persistent proatlantal artery is a

basilar artery. The persistent proatlantal artery is a Figure 17 Diagnostic angiogram of the ICA, lateral

Figure 17 Diagnostic angiogram of the ICA, lateral projection. A persistent trigeminal artery is seen leaving the internal carotid in the cavernous (C3) segment and entering the basilar artery Note the filling of both the PCA and SCA circulation. Abbreviations :

ICA, internal carotid artery; PCA, posterior cerebral artery; SCA, superior cerebellar artery.

primitive anastomosis between the ICA or ECA and the cervical vertebral artery.

Anatomic Considerations

The presence of persistent caroticobasilar anastomoses should be ruled in or out before certain procedures. Wada testing is employed to localize language and memory dominance prior to partial or complete amygdalohippocampectomy. During this test, sodium amobarbital is injected into the ICA on one side to effectively anesthetize the ipsilateral hemisphere. Should a persistent caroticobasilar anastomosis exist, the target of the amobarbital would be the brain stem,

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2: Applied Neurovascular Anatomy of the Brain and Skull 31 Figure 18 Lateral common carotid artery

Figure 18 Lateral common carotid artery injection ( A) and selective, late arterial phase injection of the ECA ( B). The branches of the ECA are identified. Note the tortuous course of the distal vessels ( B) characteristic of external carotid vessels. The black arrow indicates the sharp turn the middle meningeal artery makes just after passing through the foramen spinosum. Abbreviations : ST, superior thyroid; L, lingual artery; F, facial artery; ECA, external carotid artery; ICA, internal carotid artery; AscP, ascending pharyngeal artery; IMax, internal maxillary artery; MMA, middle meningeal artery; Occ, occipital artery; STA, superficial temporal artery; d, distal.

potentially resulting in respiratory arrest, stroke, or death (3). In this case, it would be necessary to select the artery distal to the anastomosis to avoid this complication. The same principle applies to balloon test occlusion studies (27). Among the list of complications for carotid endarterectomy is the possibility of brain stem infarct from a fractured embolus that occurs during this procedure should a persistent hypoglossal artery be present (28,29). Though this complication has not yet been reported in the setting of carotid artery stenting, it should be considered if a persistent hypoglossal artery is present. In this case, the choice of stent length and position would be important. A Y-stent might be the optimal solution preserving flow routes to both eloquent vascular distributions.

EXTERNAL CAROTID ARTERY

The external carotid artery (ECA) originates from the common carotid artery in the neck. The named branches in order of origin are the superior thyroid, lingual, facial, ascending pharyngeal, occipital, poste- rior auricular, superficial temporal, and internal max- illary arteries (Fig. 18A). The ascending pharyngeal artery (APA) further bifurcates into pharyngeal and neuromeningeal trunks. The internal maxillary artery terminates in the middle meningeal, accessory menin- geal, and sphenopalatine arteries (Fig. 18B). Further terminal branch description will be given later in this text where relevant anastomoses apply.

Anatomic Considerations: The Ascending Pharyngeal Artery

The APA is unique because it provides anastomotic channels to the internal carotid, the vertebral artery, and other branches within the external carotid circula- tion (Fig. 19A) (1–4,30). It typically arises from the ECA, but it can occasionally arise from the proximal ICA or an aberrant posterior inferior cerebellar artery (PICA) (30–34). The APA starts as a common trunk and then bifurcates into pharyngeal and neuromeningeal trunks. The pharyngeal trunk terminates as the superior, mid- dle, and inferior pharyngeal branch, providing rich anastomotic connections to the internal maxillary artery (middle pharyngeal via the descending palatine artery and pterygovaginal artery via the accessory meningeal artery) and the ICA (superior pharyngeal via the inferolateral trunk and the recurrent artery of the foramen lacerum). As the name implies, this por- tion of the artery supplies the tissue of the oropharynx. Although the artery is often difficult to see on an external carotid angiogram, its clinical importance exceeds its size in certain circumstances. Specifically, the anastomotic channels previously described can cloud the results of test balloon occlusion of the ICA by providing collateral circulatory routes. These chan- nels also become important during the embolization of glomus jugulare, vagale, or tympanicum tumors sup- plied predominantly by this artery. The neuromeningeal trunk courses in a poster- osuperior direction toward the foramen magnum. Its

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32 Bell et al. Figure 19 ( A ) Cartoon angiographic representation of the ascending pharyngeal

Figure 19 ( A) Cartoon angiographic representation of the ascending pharyngeal artery and its anastomoses. (a) Middle pharyngeal artery to internal maxillary artery via the descending palatine artery. (b) Pterygovaginal artery (terminal branch of the superior pharyngeal artery) to internal maxillary artery via the accessory meningeal artery. (c) Superior pharyngeal artery to the ICA via the recurrent artery of the foramen rotundum and the inferolateral trunk. (d) Clival branches (terminal branches of the neuromeningeal trunk) to the ICA via the meningohypophyseal trunk. (e) inferior tympanic artery to ICA via the caroticotympanic branch. (f) Hypoglossal artery to the vertebral artery via the odontoid arch system. (g) Neuromeningeal trunk to the vertebral artery via the odontoid arch system. (h) Neuromeningeal trunk to the odontoid arch system. The odontoid arch then connects, at times, to the occipital artery. ( B) Selective vertebral artery injection. A direct anastomosis from the vertebral artery to the ECA via the APA is shown. Abbreviations : APA, ascending pharyngeal artery; NmT, neuromeningeal trunk; PhB, pharyngeal branch; CCA, common carotid artery; ECA, external carotid artery; Vert, vertebral artery; IMax, internal maxillary artery; dICA, distal internal carotid artery.

branches include the inferior tympanic, musculospi- nal, hypoglossal, and jugular arteries, with additional terminal branches to the internal auditory canal, the clivus, and the odontoid arch. Clinically relevant anastomoses occur between the hypoglossal and mus- culospinal arteries to the vertebral artery, the inferior tympanic branch to the ICA through the caroticotym- panic artery, lateral clival branches directly to the ICA, and ECA to ECA connections from the odontoid arch system to the occipital artery (1,4,30). An example of a direct anastomosis between the ascending pharyngeal and vertebral artery is given in Figure 19B.

THE VERTEBROBASILAR SYSTEM

The vertebral arteries typically arise from the subcla- vians bilaterally (V1). They proceed superiorly and dorsally to enter the foramen transversarium at the level of C6. The arteries subsequently travel to the arch of C1, giving off a variable number of small spinal muscular and segmental arteries (V2). Two characteristic right-angle turns are noted on both AP and lateral angiographic projections at C1 and C2 (V2) (Figs. 20A and 22), which have been described as a box on the AP projection. The artery then processes dorsally to the atlanto-occipital joint and travels in an

anterosuperior direction to enter the dura (V4). Prior to the vertebrobasilar junction, the artery gives off the anterior spinal artery (ASA) and posterior inferior cerebellar artery (PICA). The ASA supplies the ante- rior spinal cord, and the PICA supplies the lower brain stem, cerebellar tonsils, and the inferior aspect of the cerebellar hemispheres. The basilar artery then travels anterior to the brain stem, giving off the ante- rior inferior cerebellar artery (AICA), multiple small pontomesencephalic perforators, and the superior cer- ebellar artery (SCA) (Figs. 20 and 21). There are mul- tiple areas of collateral circulation between the SCA, AICA, and the PICA, and distal parent artery sacrifice in this area may be clinically silent (Fig. 23, white arrows). The AICA and PICA may, at times, arise from a common trunk (Fig. 22). This particular ana- tomic variant may alter the treatment plan in certain circumstances. The basilar artery subsequently bifur- cates within the crural cistern into the PCA.

The Posterior Cerebral Artery

The PCAs, like the MCA and ACA, are segmentally organized on the basis of the relevant surrounding anatomy (Figs. 23–25). The P1 segment starts at the basilar bifurcation and extends to the insertion of the

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2: Applied Neurovascular Anatomy of the Brain and Skull 33 Figure 20 Selective vertebral artery injection,

Figure 20 Selective vertebral artery injection, transmaxillary projection ( A) and gross anatomic specimen for comparison (B). Note the course of the vertebral and basilar arteries with respect to the brain stem and cranial nerves. Abbreviations : Vert, vertebral artery; PICA, posterior inferior cerebellar artery; AICA, anterior inferior cerebellar artery; B, basilar artery; SCA, superior cerebellar artery; PCA, posterior cerebral artery; CN, cranial nerve; C1, first cervical vertebrae; C2, second cervical vertebrae. Source : From Ref. 5.

C2, second cervical vertebrae. Source : From Ref. 5. Figure 21 Lateral angiogram of the vertebral

Figure 21 Lateral angiogram of the vertebral artery. Abbrevia- tions : Vert, vertebral artery; SmB, spinomuscular branch; PICA, posterior inferior cerebellar artery; B, basilar artery; AICA, ante- rior inferior cerebellar artery; SCA, superior cerebellar artery; PCA, posterior cerebral artery; C1, first cervical vertebrae; C2, second cervical vertebrae.

C1, first cervical vertebrae; C2, second cervical vertebrae. Figure 22 Transmaxillary projection of the vertebral

Figure 22 Transmaxillary projection of the vertebral artery. Note the bilateral absence of a true PICA, and a prominent bifurcation of the AICA characteristic of an AICA-PICA complex. Abbrevia- tions : PICA, posterior inferior cerebellar artery; AICA, anterior inferior cerebellar artery.

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34 Bell et al. Figure 23 Lateral projection of the basilar artery from a verte- bral

Figure 23 Lateral projection of the basilar artery from a verte- bral artery injection. Collateral circulatory pathways are shown with the segmental anatomy of the PCA. Note the filling of the internal parietal arteries from this injection via the splenial artery. The splenium of the corpus callosum is outlined by the splenial artery and the lateral and medial posterior choroidal arteries. The black arrow indicates the faint contrast blush within the posterior thalamoperforating arteries from the basilar apex and P1. The white arrows depict the collateral circulation of the distal cere- bellar vessels. Abbreviations : PCA, posterior cerebral artery; B, basilar artery; MpcA, medial posterior choroidal artery; LpcA, lateral posterior choroidal artery; S, splenial artery; CalcA, cal- carine artery; PoA, parietooccipital artery; IpA, internal parietal artery; CC, corpus callosum.

artery; IpA, internal parietal artery; CC, corpus callosum. Figure 24 Projection through the foramen magnum (Townes

Figure 24 Projection through the foramen magnum (Townes projection), vertebral artery injection. The segmental anatomy of the PCA is shown. P1 starts at the basilar artery and ends at the insertion of the posterior communicating artery. P2 is divided into a P2A within the crural cistern and P2P within the ambient wing cistern. P3 begins at the quadrigeminal plate cistern and ends at the origin of the calcarine and parietooccipital artery. The P4 segment includes the terminal cortical branches. The digitally subtracted shadow of a 7.62-mm bullet is seen (FB). Abbrevia- tions: PCA, posterior cerebral artery; AtA, anterior temporal artery; P2A, anterior segment; P2P, posterior segment; PtA, posterior temporal artery; PoA, parietooccipital artery; FB, foreign body.

artery; PoA, parietooccipital artery; FB, foreign body. Figure 25 Gross anatomic specimen of the medial

Figure 25 Gross anatomic specimen of the medial undersurface of cerebrum. The course and segmenta- tion of the PCA is shown. Note the course of the calcarine artery within primary visual cortex (Cuneus and Lingula). The brain stem can also be seen medial to the P2 segment. Perforating arteries from this seg- ment supply the lateral brain stem and optic tract. Abbreviations : PCA, posterior cerebral artery; ACA, anterior cerebral artery; ICA, internal carotid art- ery; CalcSulcus, calcarine sulcus; ParOccip, Sulcus- parietooccipital sulcus. Source : From Ref. 5.

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posterior communicating artery. The P2 segment is divided into the anterior (P2A) and posterior (P2P) on the basis of its cisternal location. The P2A starts at the posterior communicating artery and travels around the anterolateral aspect of the mesencephalon in the crural cistern. The P2P continues posteriorly within the paramesencephalic and ambient wing cisterns and ends at the quadrigeminal plate cistern. Small perfo- rating arteries, not well visualized on an angiogram, arise from this segment and supply the cerebral peduncles, brain stem, optic tracts, thalamus, choroids plexus, and hippocampus. The posterior temporal artery also emerges in this region. The P3 segment starts at the quadrigeminal cistern (tectal plate) and continues to the origin of the parieto-occipital and calcarine arteries (P4).

Anatomic Considerations: The Distal Posterior Cerebral Artery

Distal vascular anomalies in the posterior cerebral circulation are difficult entities to treat. The surgical approaches to the crural, paramesencephalic, ambient wing, and quadrigeminal plate cisterns are certainly elegant, but the associated morbidity may lend itself to a treatment strategy that incorporates a less inva- sive approach (7, 35–38). Patients with pathology in this region may present with hemiparesis (brain stem perforators or compression), homonymous hemianop- sia (compression of optic tract, infarction of calcarine cortex), and occasionally fourth nerve compression (Fig. 26) (7,39). The elegant nature of the neural tissue fed by the PCA system complicates the open surgical or endovas- cular repair of vascular abnormalities in this region. Surgical bypass followed by PAO is one successful approach to complicated PCA pathology. Endovascu- lar treatment without open surgery can reduce mor- bidity, but the often necessary PAO can result in additional deficit. There are diverging published opin- ions concerning where along the PCA circulation PAO is safe (36,40). Ciceri et al. treated 21 aneurysms in 20 patients with endovascular coil occlusion (36). The parent artery was preserved in 14 patients, and PAO was performed without preoperative test balloon occlusion. Though relatively successful with proximal PAO, the general recommendation posited by the authors was that occlusion distal to P2 could be tol- erated secondary to adequate distal collateral circula- tion provided by the posterior temporal, lateral posterior choroidal, medial posterior choroidal, and splenial arteries. Conversely, proximal PCA occlusion could be associated with brain stem infarct. However, Hallacq et al. occluded the parent artery in 10 patients with P2 segment aneurysms without postocclusion deficit, concluding that P2 occlusion was in fact safe.

THE CEREBRAL VEINS

It is convenient to think of the cerebral venous anat- omy as a construct of channels (sinuses) and veins organized into a deep and superficial system. The

and veins organized into a deep and superficial system. The Figure 26 Artists rendition of the

Figure 26 Artists rendition of the course of the distal PCA under the surface of the tentorium cerebelli. An aneurysm in this loca- tion could conceivably cause a fourth cranial nerve palsy sec- ondary to its proximity to that nerve. Abbreviation : PCA, posterior cerebral artery. Source : From Ref. 39.

sinuses receive the bulk of venous outflow from the brain and terminate in the internal jugular veins. The following will review the deep and superficial venous anatomy seen on normal angiographic studies.

The Superficial Venous System

The superior sagittal sinus is the large midline vein easily visualized on both AP and lateral angiographic projections (Fig. 27). It receives direct inflow from the hemispheres via the superficial frontal, parietal, and occipital cortical veins as well as extra-axial inflow from the diploic and meningeal veins. The superior anastomotic vein of Trolard is the largest of the cor- tical venous inflow tracts and is typically located in the middle third of the sinus. The superior sagittal sinus terminates at the torcular herophili at the con- fluence of the sinuses. Here the straight sinus and the superior sagittal sinus become the paired transverse sinuses. The straight sinus receives venous inflow from the inferior sagittal sinus, the vein of Galen, and meningeal veins from the tentorium. The trans- verse sinuses make a 90 8 turn under the asterion of the skull to become the sigmoid sinuses. On a lateral angiogram, the inferior anastomotic vein of Labbe and the superior petrosal sinuses can be seen draining into this area.

Figure 27 Lateral ( A ) and AP ( B ) projection, venous phase. Normal

Figure 27 Lateral (A) and AP (B) projection, venous phase. Normal venous anatomy is shown. Abbreviations : IJ, internal jugular vein; SigS, sigmoid sinus; TS, transverse sinus; SPS, superior petrosal sinus; SS, straight sinus; SSS, superior sagittal sinus; VoL, inferior anastomotic vein of Labbe; BVoR, basal vein of Rosenthal; TsV, thalamostriate vein; VoG, vein of Galen; IcV, internal cerebral vein; AfV, anterior frontal vein; MfV, middle frontal vein; PfV, posterior frontal vein; PrecV, precentral vein; VoT, superior anastomotic vein of Trolard; ApV, anterior parietal vein; PpV, posterior parietal vein.

ApV, anterior parietal vein; PpV, posterior parietal vein. Figure 28 Representation of the main cerebral venous

Figure 28 Representation of the main cerebral venous and sinus anatomy. Abbreviations : Ant, anterior; Post, posterior; Mid, middle; Cent, central; Med, medial; Precent, precentral; Pericall, pericallosal; Car, Carotid; Cav, cavernous; SphenPar, sphenoparietal; Sup, superficial; Sag, Sagittal; Inf, inferior; Paracent, paracentral; Cer, cerebral; Front, frontal; Bas, basal; Men, meningeal; Temp, temporal; Tent, tentorial; Occip, occipital; Post, posterior; Calc, calcarine; Lat, lateral; Str, straight. Source : From Ref. 5.

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2: Applied Neurovascular Anatomy of the Brain and Skull 37 Figure 29 Lateral injection of the

Figure 29 Lateral injection of the ICA. A direct CC fistula is shown. The cavernous sinus is best visualized during pathologic conditions. Note the cerebellar cortical venous reflux, making this particular CC fistula prone to causing subarachnoid hemorrhage. Abbreviations : CC, carotid cavernous; Pp, pterygoid venous plexus; IpS, inferior petrosal sinus; SpS, superior petrosal sinus; CavS, cavernous sinus; RV, retinal vein.

The base of the brain contains multiple venous sinuses that are clinically relevant. The cavernous sinus is a paired structure composed of multiple venous sinusoidal channels that anatomically encircle the sella turcica (Fig. 30). This structure is not overtly obvious on a normal angiogram, but becomes prom- inent in the setting of direct carotid cavernous fistulas (Fig. 29). Just posterior and inferior to this structure is the midline basal sinus. This sinus receives inflow from the superficial sylvian vein via the sphenopar- ietal sinus, and outflow from the superior petrosal sinus toward the sigmoid sinus.

The Deep Venous System

The deep venous structures are also easily visible on a lateral angiogram. The basal veins of Rosenthal become visible within the crural cisterns (Figs. 27A and 28). They receive flow from the deep middle cerebral veins and the anterior cerebral veins (Fig. 28). They subse- quently course within the paramesencephalic and ambient wing cisterns with the PCA to finally end at the vein of Galen. The vein of Galen also receives venous drainage from the internal cerebral veins. This paired venous outflow receives predominant feeders from the thalamostriate veins (Fig. 27A), the anterior caudate veins, and the anterior septal veins lining the

caudate veins, and the anterior septal veins lining the Figure 30 AP projection of an ICA

Figure 30 AP projection of an ICA injection. A direct CC fistula is shown. The cavernous sinus clearly outlines the sella turcica in this view. Abbreviations : CC, carotid cavernous; ST, sella turcica; CavS, cavernous sinus; Pp, pterygoid plexus.

lateral ventricles. The internal cerebral veins course within the velum interpositum with the medial pos- terior choroidal arteries and terminate at the vein of Galen. The vein of Galen then empties into the straight sinus.

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40. Hallacq P, Piotin M, Moret J. Endovascular occlusion of the posterior cerebral artery for the treatment of p2 seg- ment aneurysms: retrospective review of a 10-year series. AJNR Am J Neuroradiol 2002; 23(7):1128–1136.

3

Vascular Anatomy of the Spine and Spinal Cord

Armin K. Thron

Department of Neuroradiology, University Hospital, RWTH Aachen University, Aachen, Germany

INTRODUCTION

Because of progress in microneurosurgery and inter- ventional neuroradiology, intramedullary spinal vas- cular lesions have become more and more accessible and treatable. Unfortunately, a lack of knowledge about spinal vascular anatomy is evident in many conferences with neurologists and sometimes even with neurosurgeons and neuroradiologists. This lack of knowledge might be a reason for unsatisfactory clinical results in the treatment of spinal vascular diseases by invasive therapeutic techniques. Further- more, magnetic resonance imaging (MRI) and mag- netic resonance angiography (MRA) of blood vessels in and around the spinal cord have substantially improved. To provide a correct anatomical interpreta- tion of the demonstrated blood vessels, knowledge of the anatomy of spinal cord blood vessels is the first prerequisite. At the end of the 19th century, Kadyi (1) gave the most precise and detailed anatomical descrip- tion of these blood vessels. His work was published in 1889, seven years after the first extensive and compre- hensive study performed by Adamkiewicz (2). This chapter deals with the essentials of spine and spinal cord blood vessel anatomy (in parts adapted from 3), outlines the possibilities of identify- ing these vessels on tomographic images, and illus- trates the main problems and pitfalls in the anatomical evaluation of spinal vascular malformations.

ARTERIAL BLOOD SUPPLY

Sources of Arterial Blood Supply to the Spine and Spinal Cord

The blood supply to the vertebral body, the paraspinal muscles, the dura, the nerve root, and the spinal cord is derived from segmental arteries (Fig. 1). These vessels persist as intercostal and lumbar arteries in the majority of the thoracolumbar region. Several segments in the upper thoracic region have a common feeder, which is the supreme intercostal artery. Following intrauterine vascular rearrangements, longitudinal arteries are established in the cervical region. On each side, three vessels are potential

sources of spinal blood supply, namely, the vertebral artery, the deep cervical artery, and the ascending cervical artery. In the sacral and lower lumbar region, sacral arteries and the iliolumbar artery (supplying the L5 level) derived from the internal iliac arteries are the most important supply to the caudal spine. Generally, the segmental arteries supply all the tissues on one side of a given metamere, with the exception of the medulla. A spinal branch of the posterior intercostal artery enters the vertebral canal through the intervertebral foramen and regularly divides into three branches: an anterior and a poste- rior artery of the vertebral canal, which supply the spinal column, and a radicular artery, which supplies the dura and nerve root at every segmental level. The hemivertebral blush, resulting from injection of a segmental artery, may help in identifying the artery. At the thoracic level, the artery is named according to the number of the rib under which it courses. The segmental arteries are connected across the midline and between levels above and below, through highly effective anastomoses (Figs. 2 and 7). At certain segmental levels, this radicular artery has persisted as a radiculomedullary artery, which means that it follows the anterior and/or posterior nerve roots to form and supply the superficial spinal cord arteries (Fig. 1). The number of these radiculome- dullary arteries is reduced during an embryonic trans- formation process. From 2 to 14 (on average 6) anterior radiculomedullary arteries persist as a result of this ontogenic reduction of feeding vessels. The posterior radiculomedullary arteries are reduced less drastically from 11 to 16 vessels. Figure 3 demonstrates schemat- ically the typical potential sources of arterial supply to the anterior axis of the spinal cord.

Extra- and Intraspinal Extradural Anastomoses

1. An extraspinal system connects the neighboring segmental arteries longitudinally. The vessels course on the lateral aspect of the vertebra or transverse process (Figs. 1, 2, and 7). This system is highly developed in the cervical region where the vertebral artery and the deep cervical and

40

Thron

40 Thron Figure 1 Blood supply of the spinal column and spinal cord. ascending cervical arteries

Figure 1 Blood supply of the spinal column and spinal cord.

ascending cervical arteries form the most effective longitudinal anastomoses. 2. The intraspinal extradural system is mainly a transverse anastomosis, but it also has longitudi- nal interconnections. The retrocorporeal and arteries are the relevant vessels for the supply of bone and dura (Figs. 1, 2, and 7). These anasto- moses provide an excellent collateral circulation and therefore numerous segmental arteries can be visualized by injection of one segmental artery (Fig. 2).

The extra- and intraspinal anastomoses protect the spinal cord against ischemia when pathologies, such as arteriosclerotic disease of the aorta, cause focal vessel occlusion.

Radicular Supply and Superficial Spinal Cord Arteries

Several nomenclatures and classifications have been used to describe spinal cord arteries. This variation is an ongoing cause of misunderstanding. A recent clas- sification proposed by Lasjaunias et al. (4) differen- tiates three types of spinal radicular arteries: radicular, radiculopial, and radiculomedullary. The first type of spinal radicular artery is a small branch present at every segmental level, which is restricted to the supply of the nerve root. The second type supplies the nerve root and superficial pial plexus (e.g., posterior radicular artery). The third type supplies the nerve root, pial plexus, and medulla. This classification may offer some advantages to the interventional neuroradiologist when compared

with classical differentia tions because it stresses the importance of the anterior supply for the gray matter of the spinal cord parenchyma. From an ana- tomical and linguistic point of view, however, it is not a clear-cut differentiation because anterior and pos- terior radicular arteries share in the blood supply of the medulla and the posterior radicular arteries do contribute to the supply of the central gray matter, especially of the posterior horn. We therefore suggest only a slight modification of the older anatomical classification with the follow- ing differentiation of spinal radicular arteries:

radicular arteries supplying only the nerve root and the dura mater, but not the spinal cord; anterior radiculomedullary arteries in which the per- sistent medullary branch runs with the anterior nerve root to join the longitudinal trunk, which has been called the anterior spinal artery (Figs. 1 and 3); and posterior radiculomedullary arteries in which the per- sistent medullary branch accompanies the posterior nerve root and joins the longitudinal systems of posterolateral and/or posterior spinal arteries. The first lies laterally and the second medially to the posterior root entry zone. These longitudinally ori- ented vessels are not continuous and may replace each other (Figs. 1, 6, 7C, D, and 8C).

As has already been mentioned, the anterior radiculomedullary supply is reduced to an average of 6 radiculomedullary arteries (Fig. 3), whereas from 11 to 16 posterior radiculomedullary arteries persist after embryonic life.

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Chapter 3: Vascular Anatomy of the Spine and Spinal Cord 41 Figure 2 Extra- and intraspinal
Chapter 3: Vascular Anatomy of the Spine and Spinal Cord 41 Figure 2 Extra- and intraspinal

Figure 2 Extra- and intraspinal extradural anastomoses. Selec- tive injection in the first lumbar artery on the left opacifies homo- lateral arteries as well as contralateral vessels. The typical hexagonal configurations of the retrocorperal intraspinal anasto- mosis ( small arrows ) as well as the extraspinal pretransverse and anterolateral anastomoses ( large arrows ) are demonstrated. The injected artery gives rise to an anterior radiculomedullary artery (arrowheads ), probably the Adamkiewicz artery. Note the hemi-

vertebral blush corresponding to the injected artery. Figure 3 Sources of supply to the anterior spinal artery.

The thoracolumbar enlargement is the region where the dominant anterior radiculomedullary artery ( arteria radicularis magna , or Adamkiewicz artery ) arises. However, in this region several posterior rad- iculomedullary arteries may also be large-sized ves- sels, which furnish blood supply to this area. They are connected to the anterior spinal artery through two anastomotic semicircles, called the arcade of the cone (Figs. 3 and 6A). The superficial distribution of blood to the spinal cord is achieved by the above-mentioned anterior and posterior longitudinal vessels, which have been named anterior and posterior/posterolateral spinal arteries. Both systems supply a superficial network of smaller pial arteries that covers the spinal cord, termed the vasocorona (Figs. 8 and 9). The anterior

spinal artery may be small or absent as a continuous tract in the upper thoracic and upper cervical regions of the spinal cord (Figs. 3 and 4). The main source of arterial supply to the cord is the anterior spinal artery (ventral axis), with a multi- segmental distribution of blood and a distinct territory of supply. It gives rise to the hemodynamically impor- tant central (centrifugal) system, which supplies the major part of the gray matter. Additionally, there are branches to the pial system on the anterior and lateral surface, supplying the ventral two-thirds of the vaso- corona (Figs. 8 and 9A). The posterior/posterolateral spinal arteries distribute blood to the dorsal one-third of the

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42 Thron Figure 4 Anterior spinal artery in the cervical spinal cord. The pattern of supplying

Figure 4 Anterior spinal artery in the cervical spinal cord. The pattern of supplying vessels varies considerably, especially in the upper spinal cord. ( A ) Photograph of an injected specimen. Plexiform pattern of arterial supply in the upper cervical levels, without formation of a midline anterior spinal artery. ( B) X-ray film in AP view. The anterior spinal artery is formed by a large unilateral descending branch from the left vertebral artery (arrow ) and is reinforced by a large anterior radiculomedullary artery at the C5 level on the right. The small descending branch coming from the right vertebral artery ( arrowhead ) ends in this network of small tortuous superficial arteries. Source : From Ref. 13.

vasocorona, and in this way they share with central artery branches in the supply of the posterior horn and marginal parts of the central gray matter (Fig. 9A). The posterior/posterolateral arteries do not have such a distinct territory of supply as the anterior spinal artery, which means that they predominantly reinforce the rope ladder–like network of posterior pial arteries (Fig. 8C).

ladder–like network of posterior pial arteries (Fig. 8C). Figure 5 Demonstration of an anterior radiculomedullary

Figure 5 Demonstration of an anterior radiculomedullary feeder to the cervical spinal cord by injecting the costocervical trunk on the left. The ascending and descending branches ( arrowheads ) are forming the anterior spinal artery at this level.

Differences in Arterial Supply of the Spinal Cord Depending on Regions

Cervical Region

One of the ventral radicular feeders between C5 and C8 is often distinctly larger (400–600 m m) than the others and was termed the artery of the cervical enlargement by Lazorthes (5,6). It is more often derived from the deep and ascending cervical arteries than from the vertebral artery (Figs. 3 and 5). There- fore, these vessels that originate from the thyrocer- vical and costocervical trunks, respectively, must be demonstrated on angiography for diagnostic and interventional procedur es. The average number of anterior radicular feeders to the cervical medulla is 2 to 3. The ventral feeders to the upper cervical cord, originating from the intracranial section of the verte- bral artery, may be very small. Their demonstration on angiography is often impossible. If there are two descending branches from both vertebral arteries, the smaller or rudimentary vessel does not join the main

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Chapter 3: Vascular Anatomy of the Spine and Spinal Cord 43 Figure 6 X-ray film (AP

Figure 6 X-ray film (AP view) of a contrast-injected human spinal cord specimen with arterial filling. ( A ) Lumbar and ( B ) thoracic regions. Note the different calibers of the anterior ( large arrowheads ) and posterior radiculomedullary feeders ( small arrowheads ) and of the anterior spinal artery ( small arrows ) at different spinal cord levels. The important supply coming from the ‘‘artery of the lumbar enlargement’’ is obvious as well as its connection with the posterior arteries around the cone (arcade of the cone) ( black arrow ). The system of posterior/posterolateral arteries is discontinuous; the largest posterior radiculomedullary feeder enters below and contralateral to the artery of Adamkie- wicz in this specimen ( oblique arrowhead ). Source : From Ref. 13.

midline trunk but ends separately as a large central artery (Figs. 3 and 4). Duplication of the anterior spinal artery over some distance is frequent in this region; a pseudo- island formation and even a net-like plexiform pattern of arteries may be observed. Continuity of an anterior spinal artery may not exist. All these variations have to be regarded as a state more closely related to the embryonic (or ontogenetic) condition (Fig. 4). A descending branch from the vertebral artery or posterior inferior cerebellar artery (PICA) constitutes

the posterior system of the upper cervical region. The vessel may have a large caliber and originates in a lateral position (lateral cervical artery) (7). The number of central arteries in the cervical enlargement is about 6/cm. They take a horizontal course.

Thoracic Region

Occasionally, one segmental artery branches and sup- plies two intercostal spaces. In this case, the dorsal and spinal branch of one of the two segments may not be seen. Therefore, a small posterior intercostal artery, from which the spinal branch of this metamere arises, must be looked for. This procedure may be crucial, for example when searching for the site of a dural arterio- venous fistula. The upper and midthoracic regions are mostly supplied by small radicular arteries (200–400 m m), mak- ing angiographical demonstration difficult (Fig. 3). In addition, the ventral anastomotic tract (anterior spi- nal artery) may be discontinuous throughout these regions. The pial system plays an important role in this spinal cord region, which has relatively less gray matter and more white matter tracts (Figs. 9A and 10A). On the posterior surface of the cord, the longi- tudinal tracts may run in posterior/posterolateral positions, thus indicating the functional identity of these vessels (Figs. 6 and 8C). The number of central arteries is only 2 to 3/cm for this region. This fact explains the prevalence of steeply ascending and descending central artery branches (Fig. 10A). As pointed out earlier, the impression of an intrinsic longitudinal anastomosis on sagittal images was not confirmed on coronal images of our microangiographic studies.

Thoracolumbar Region and Cauda Equina

One of the ventral feeders between T9 and L1 (excep- tionally at L2 or L3) is always dominant (80–100 m m) and is therefore called the artery of the lumbar enlargement (Lazorthes) or the great radicular artery (Adamkiewicz) (Figs. 3 and 6). Below its level of entrance, additional significant ventral feeders are unusual. Supply to the posterior system in this region often includes two equally large dorsal feeders (400– 500 mm) that enter the spine above or below the great radicular artery (Fig. 6). The ventral and dorsal systems are connected to each other around the conus (arcade of the cone, rami anastomotici arcuati ) (1). This pattern may constitute a significant anastomosis, comparable to the circle of Willis. The densest concentration of central arteries is found in the thoracolumbar enlargement, where 6 to 8 vessels/cm can be counted on microangiograms (Fig. 8B).

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44 Thron Figure 7 Angiographical demonstration and identification of spinal cord arteries. ( A , B

Figure 7 Angiographical demonstration and identification of spinal cord arteries. ( A , B) Selective injection of the 11th intercostal artery with normal findings. ( A ) Frontal view. Typical hairpin configuration and midline position of the anterior radiculomedullary and anterior spinal arteries [small ascending and larger descending branch at this level ( arrowheads )]. Note the extra- and intraspinal longitu- dinal and transverse anatomoses ( arrows ) and the hemi- vertebral blush. ( B ) Lateral view. Anterior location of the artery demonstrated in ( A) (arrowhead ). The lateral projec- tion is very helpful to differentiate the anterior or posterior position of the artery with certainty, which may be difficult in cases of scoliosis, and especially AVMs. (C , D ) Injection of the ninth intercostal artery in case of an intraspinal tumor. (C ) Frontal view. The segmental artery gives rise to an anterior ( arrowhead ) and posterior (arrow ) spinal cord sup- plying artery. Note the different positions of the ‘‘hairpin curve’’ and of the descending branches. (Displacement of the anterior and posterior spinal arteries below the level of the injection and the equal size of both vessels are due to an intraspinal neurinoma.) ( D) Lateral view. The anterior (arrowhead ) and posterior positions ( arrow ) of the anterior and posterior spinal artery can be distinguished. Abbrevia- tion : AVM, arteriovenous malformation.

Intrinsic Spinal Cord Arteries

The arteries directly supplying the spinal cord are

central (or sulcal) arteries originating from the anterior spinal artery and perforating branches arising from the pial network which covers the spinal cord.

The first type of perforating arteries constitutes a centrifugal system. Each central artery (inner vessel diameter, 100–250 m m) penetrates the parenchyma to the depth of the anterior fissure, courses to one side of the cord, and branches mainly within the gray matter. The second type of perforating arteries arises from the pial covering of the cord (vasocorona) and penetrates the white matter tracts from the periphery (centripetal

system). These vessels are numerous, with a diameter of up to 50 mm. Both types of intrinsic artery and their region of supply can be appreciated on the axial section of the microangiogram demonstrated in Fig- ures 8, 9A, and 10A.

Superficial and Intrinsic Arterio-Arterial Anastomoses

Arterio-arterial anastomotic interconnections are fre- quent in the spinal cord. The anterior spinal artery may be regarded as the largest and most constant longitudinal anastomo- sis (Figs. 3 and 6). The posterior systems are not constantly devel- oped or continuous. They include longitudinal and

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Chapter 3: Vascular Anatomy of the Spine and Spinal Cord 45 Figure 8 Anterior spinal artery,

Figure 8 Anterior spinal artery, intrinsic arteries, and pial plexus demonstrated on microangiograms of the lumbar spinal cord. The spinal cord has been cut into three coronal sections, each 2 to 3 mm thick; section length, 2.5 cm. ( A ) Anterior coronal section. Numerous transverse and oblique branches from the anterior spinal artery (arrow ) supply the anterior part of the superficial pial plexus called ‘‘vasocorona.’’ (B ) Middle coronal section. The central arteries, derived from the anterior spinal artery, course to one side of the cord and branch mainly within the gray matter. From the surface of the spinal cord, perforating branches of the vasocorona penetrate and supply the outer rim of fiber tracts and parts of the posterior horn. ( C) Posterior coronal section. The larger posterolateral ( arrows ) and smaller posterior spinal arteries (arrowheads ) form a rope ladder–like network, supplying the posterior part of the vasocorona. The posterolateral arteries are running laterally, the posterior arteries medially of the posterior roof entrance zone. Source : From Ref. 13.

transverse components and serve as anastomotic path- ways and distribution channels, at least over some segments (Figs. 6 and 8C). The arcade of the cone has an anastomotic func- tion, comparable to that of the circle of Willis. Superficial interconnections between two or sev- eral central arteries exist predominantly in the tho- racic region. They run immediately deep and parallel to the anterior spinal artery at the entrance of the anterior fissure within the pial system (Fig. 10A). Additionally, there are horizontal anastomoses between central artery branches and the superficial systems, especially in a centroanterolateral or centro- posterolateral direction. However, they do not seem to

play an important role in the plasticity of blood sup- ply to the spinal cord. The most important observation to note is that we could not demonstrate an intrinsic longitudinal anastomoses between the ascending and descending branches of the central arteries within the spinal cord parenchyma (13), as was assumed by Adamkiewicz (2) and Fazio and Agnoli (8).

VENOUS DRAINAGE

The pattern of venous drainage deviates substantially from that of the arteries. Their arrangement will be

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46 Thron Figure 9 Comparison between intrinsic spinal cord arteries and veins demonstrated on microangiograms of

Figure 9 Comparison between intrinsic spinal cord arteries and veins demonstrated on microangiograms of axial sections of 2-mm thickness. (A ) Arteries at different levels of the spinal cord (anterior spinal artery, arrow ; posterior/posterolateral spinal arteries at both sides of the posterior root entry zone, small arrowheads ). The central arteries (large arrowhead ) are the predominant intrinsic feeders at the level of the cervical and lumbar enlargements. They run within the anterior fissure and continue either to the right or left side of the hemicord as a centrifugal system. The perforating branches are the predominant feeders of the thoracic spinal cord. They originate from the superficial vasocorona as a centripetal system, and their territory of supply can very well be differentiated from the system of central arteries. (B) Veins at different levels of the spinal cord. Radial and central veins are of almost equal size and drain to the pial covering of the spinal cord (anterior and posterior median spinal veins, arrows ). Source : From Ref. 13.

described in the direction of venous drainage from the spinal cord parenchyma to the epidural plexus.

Intrinsic Veins

Radial veins drain the blood of the spinal cord paren- chyma. They show a horizontal, radial, and symmet- rical course in most parts of the spinal cord (Fig. 9B). Only in the lower thoracic cord, from the lower lumbar enlargement to the conus medullaris, are the

sulcal veins (100–250 mm) larger than the numerous radial veins.

Superficial Veins

At the level of the spinal pia mater, blood is accumu- lated in essentially two longitudinal collectors: the an- terior and posterior median spinal veins (Figs. 10–14). The anterior midline vein is located under the anterior spinal artery (Fig. 11C). It has its largest caliber lumbo- sacrally. In about 80% of cases, it runs together with the

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Chapter 3: Vascular Anatomy of the Spine and Spinal Cord 47 Figure 10 Comparison between intrinsic

Figure 10 Comparison between intrinsic spinal cord arteries and veins demonstrated on micro- angiograms of sagittal sections through the mid- line of the spinal cord (section length, 2.5 cm; thickness, 2 mm). (A) Arteries at a lower thoracic level. Anterior spinal artery (large arrow) with loss of contrast filling in small sections. The ascending course of the central arteries with more vertical than horizontal arborization within the gray matter is demonstrated. The impression of an intrinsic longitudinal anastomosis is not supported by coronal images. Compare the small perforating arteries of the posterior columns, originating from the pial network of the vasocorona. (B) Veins at a lower thoracic level. Anterior median vein (arrow) and posterior median vein (double arrow) with loss of contrast filling in sections. The sulcal veins are less numerous but larger than the pos- terior veins. Several of them join to form a com- mon stem (arrowhead). The different pattern of intrinsic arterial supply and venous drainage at approximately the same spinal cord level is well demonstrated in this comparison. Source: From Ref. 13.

filum terminale as a sometimes very large terminal vein to the end of the dural sac. The venous longitu- dinal system on the anterior and posterior surfaces of the cord is more variable in course, size, and localiza- tion than the anterior spinal artery (Fig. 11). The lon- gitudinal midline veins are not always continuous tracts and may be replaced by secondary systems of smaller caliber. The posterior median spinal vein takes a course independent from the posterolaterally located arteries and is especially large above the thoracolumbar enlargement. Varicose convolutions are frequent (Figs. 11B and 14B). The posterior veins of the thoracolumbar enlargement are undoubtedly the medullary vessels of largest caliber (up to 1.5 mm in diameter) and are rarely matched by superficial cervical veins. These are the vessels most likely to be seen on MR images (Figs. 13A and 14A). The vessels are part of a pial

vascular network, which has been called the venous plexus of the pia mater (9), the coronal pial plexus (10,11), or the venous pial plexus (12).

Intraparenchymal Venous Anastomoses

These anastomoses are quite common. However, they are not distributed uniformly over the length of a spinal cord. They are of two types. Anastomoses of the first type are complex and connect central and peripheral branches (sulcal and radial veins 100–200 mm in diameter). They are very frequent and drain to smaller veins of the superficial pial plexus. More important are anastomoses of the second type, which are transmedullary midline anastomoses from 300 to 700 m m in diameter, connecting the median veins on both sides of the cord. They do not

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48 Thron Figure 11 Superficial spinal cord veins. ( A ) Photograph of the dorsal aspect

Figure 11 Superficial spinal cord veins. (A ) Photograph of the dorsal aspect of a spinal cord specimen following ink injection into the veins at cervical and thoracic levels. The posterior median vein has a variable size at different levels. Three large radiculomedullary veins (arrows ) and some smaller ones can be seen. (B ) X-ray film (AP view) of a contrast-injected thoracolumbar spinal cord specimen. There is much tortuosity mainly of the posterior spinal cord veins (posterior venous plexus). Three large radiculomedullary veins accompany lumbar or sacral nerve roots to reach the epidural space ( arrows ). (C) Photograph of an injected spinal cord specimen with filling of the ventral veins at the thoracic level. Note the hairpin configuration of the AMV, where it continues as RV. This configuration is very similar to the arterial one. The nonfilled anterior spinal artery is running beside or over the vein ( arrow ). Abbreviations : AMV, anterior median vein; RV, radicular vein.

receive tributaries from the intrinsic vessels. Because of their size, they are not only seen on microangio- grams (Fig. 13B) but may also be seen on angiography or MRI (Fig. 13A). Through these large anastomoses, blood can easily be directed from one side of the cord to the other (13).

Differences in the Venous Drainage Depending on Spinal Cord Region

Cervical Region

Radial symmetry of intrinsic veins is very pronounced in the cervical spinal cord. Transmedullary midline anastomoses are also very frequent, but they are of

smaller caliber in the upper cervical region than those in the lower cervical and upper thoracic regions. The anterior median vein was frequently larger than the posterior median vein in our material. Both veins connect to the brain stem veins and basal sinuses around the foramen magnum. Additionally and pre- dominantly radicular outflow to the epidural plexus occurs at many levels (Fig. 11A).

Thoracic Region

The greatest concentration of large transmedullary anastomic veins is found in the cervicothoracic region (1–2/cm) followed by the mid- and lower thoracic levels (Fig. 14B), where they are more widely

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Chapter 3: Vascular Anatomy of the Spine and Spinal Cord 49 Figure 12 DSA of an

Figure 12 DSA of an artery of Adamkiewicz with arterial and venous phase. ( A) Typical hairpin course between the anterior radiculomedullary artery and the descending branch of the ante- rior spinal artery. ( B) Venous phase showing the radiculomedul- lary vein coincidentally at the same level. The configuration between midline and radiculomedullary veins is the same. This configuration is important to know for the interpretation of angio- grams in case of an AVM with early venous filling or of spinal MRAs with insufficient time resolution. Abbreviations : DSA, dig- ital subtraction angiography; AVM, arteriovenous malformation. Source : Courtesy of Prof. G. Schroth, Berne, Switzerland.

Source : Courtesy of Prof. G. Schroth, Berne, Switzerland. Figure 13 Venous midline anastomoses. ( A

Figure 13 Venous midline anastomoses. ( A ) T1- weighted sagittal MRI following injection of the contrast medium. Demonstration of a large intramedullary mid- line anastomosis between the anterior and posterior midline veins in a normal subject ( arrow ). Source :

Courtesy of Prof. D. Petersen, Lbeck, Germany. ( B) Transparenchymal anastomosis near the medullary cone with a caliber of 0.7 mm (arrows ). Microangiogram of a midsagittal cut with venous filling (same specimen as in Fig. 10B). Note the larger caliber of the anterior vein at the level of the cone compared with the posterior vein. Source : From Ref. 13.

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50 Thron Figure 14 Superficial spinal cord veins in the lumbar spinal cord and cauda equina.

Figure 14 Superficial spinal cord veins in the lumbar spinal cord and cauda equina. ( A ) MRI of T1-subtraction image. The anterior median vein is running together with the filum terminale to the end of the caudal sac ( arrowheads ), which can be an abnormal arterialized vein or a normal variant as is shown in ( B , C). (B) X-ray film of an injected specimen in lateral projection. Tortuous posterior venous plexus at the level of the lumbar enlargement (small arrows). The anterior median vein ( arrowhead) continues as a terminal vein (vein of the filum terminale). Several transmedullary anastomoses can be assumed in this projection radiography ( small arrowheads ). (C ) Microangiogram of the cone with a large terminal vein ( arrowhead ). Source : (B ) and ( C ) from Ref. 13.

separated. Anterior and posterior median veins are mostly of equal size.

Lumbar Region

In this region, sulcal veins may be considerably larger than radial veins (Fig. 9B). The posterior median spi- nal vein is particularly large above the thoracolumbar enlargement (Fig. 14B), frequently forming varicose convolutions (the so-called posterior venous plexus). The anterior median spinal vein reaches its maximum caliber in this region, and it is important to note that the vein of the filum terminale is the continuation of this anterior median vein (Fig. 14). Alternatively, the anterior vein can follow a sacral nerve root to reach the sacral epidural space (Fig. 11B). The midline veins

of the thoracolumbar enlargement are the largest blood vessels of the spinal cord (Figs. 13 and 14). When demonstrated on contrast-enhanced MRI stud- ies, or CT myelography, they should not be mistaken for spinal cord arteries.

Radiculomedullary Veins and the Transdural Course

The superficial venous blood collectors drain into the epidural venous plexus through radicular veins (Fig. 11). The transition of the midline vessel to the radicular vein forms a hairpin course, similar to the arterial configuration (Fig. 11). Therefore, on angio- graphic images, the vein might be mistaken for an

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Chapter 3: Vascular Anatomy of the Spine and Spinal Cord 51 Figure 15 AVM at the

Figure 15 AVM at the level of the cone, supplied by two posterolateral feeders and the anterior spinal artery. ( A ) MRA showing the malformation as a whole and the main drainage into a considerably enlarged terminal vein ( arrow ). ( B) Unsubtracted angiogram. Typical midline position of the anterior spinal artery. Supply from this vessel is mostly running through the arcade of the cone ( arrowheads ) to the posterior surface. (C E ) DSA. Note the somewhat different hairpin configurations of anterior and posterolateral feeders in AP view (arrowheads). The largest part of the nidus is lying posteriorly ( arrows ). ( F) Horizontal interconnections (black arrows ) between the posterolateral tracts ( arrowheads ) are visualized with increasing peripheral resistance during embolization.

artery (Fig. 12), particularly when an arteriovenous malformation (AVM) with early venous filling is present. For the same reason, it may be impossible to distinguish an anterior spinal artery from an ante- rior spinal vein on magnetic resonance images as long

as no sufficient time-resolved MRA is available. From an anatomical point of view, the number of venous outlets is high. In some studies, on average 25 rad- icular veins were counted on the anterior and poste- rior surfaces of the cord (14,15). However, purely

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52 Thron Figure 16 SDAVF T5 level. The AV shunt is at the level of the

Figure 16 SDAVF T5 level. The AV shunt is at the level of the dura mater (arrow ) and is directed at two veins coming from upward and downward. The mass of dilated veins resembles an AVM, but no spinal cord artery is involved. Abbreviations : DSA, digital subtraction angiography; SDAVF, spinal dural arterio- venous fistula; AVM, arteriovenous malformation.

radicular veins might have been included in this number. If smaller veins (<250 m m in diameter) are excluded, the number of radiculomedullary veins draining the spinal cord is from 6 to 11 for the anterior and from 5 to 10 for the posterior systems (1,16). These latter studies are in agreement with a study performed by Jacobs (17). In addition, Moes and Maillot (18) described fibrotic radicular veins at thoracic levels. These veins may contribute to the vulnerability of the spinal venous system, such as in the chronic impair- ment of venous drainage in Foix and Alajouanine disease (19) as a late complication of dural arterio- venous fistula (AVF) (20). The transdural course of radicular veins exhibits special features (3). The presence of venous valves described by Oswald (21) could not be confirmed in later studies. Instead, an oblique and zigzag course with considerable narrowing of the lumen was first described by Tadie et al. (22). They concluded that this configura- tion might act as an anti-backflow system, protecting the spinal cord against high pressure in the extraspinal veins. A study performed by Otto (23) is in agreement with their findings, although this arrangement did not always prevent reflux from the epidural plexus to the superficial spinal cord veins when a contrast medium was injected in the postmortem specimen (23).

Extradural Venous Spaces and the Extraspinal Venous System

The extradural plexus, well demonstrated by spinal contrast venography, extends as a continuous system from the sacrum to the skull base. It drains the spinal cord and surrounding structures. Drainage of blood from the spine (including spinal cord) occurs through the internal and external venous vertebral plexus and also extends as a contin- uous system from the sacrum to the base of the skull. They are identifiable as anterior and posterior sys- tems; the anterior internal vertebral plexus is larger than the posterior internal system. The external sys- tems run anterior to the body of the vertebrae (ante- rior external plexus), while the posterior external plexus lies posterolateral to the vertebral bodies. This valveless system is connected with the azygos and hemiazygos venous systems by intercostal or segmental veins and in the cervical region with the vertebral and deep cervical veins. The segmental veins in the lumbar region are connected by the ascending lumbar vein, joining the azygos (right side) and hemi- azygos veins (left side) (3).

ANATOMICAL EVALUATION OF AVMs

Some important problems and pitfalls in the clinical application of blood vessel anatomy concerning spinal AVMs should be mentioned and explained. They are illustrated in Figures 15–19.

1. Prior to a therapeutic intervention, it is essential to identify the feeders of a spinal AVM from both the anterior and posterior circulation. Figure 15 illus- trates the different configuration of the hairpin curve in anterior and posterior radiculomedullary arteries. Nevertheless, it is essential to have a lateral projection for a definite identification.

2. Spinal dural arteriovenous fistulas (SDAVFs) may look very similar to AVMs (Fig. 16). But as long as no typical radiculomedullary artery is involved, the arteriovenous (AV) shunt is much more likely situated at the level of the dura mater.

3. Discrimination between a perimedullary fistula (fistulous type of an AVM) and a SDAVF may be difficult if the arterialized vein looks like an anterior radiculomedullary feeder with a hairpin curve (Fig. 17). This event is not rare in SDAVF at lower lumbar levels when the arterialized vein is one of the large lumbar veins shown in the postmortem specimen of Figure 11B. To avoid misinterpretation, careful analysis of the vessel anatomy in the region of the intervertebral fora- men is important as well as a look at the further course of the vessel on the spinal cord surface on later images (Fig. 17C). If you are unable to iden- tify an AV shunt (fistula) on or within the spinal cord, ask yourself whether the intradural blood vessels as a whole could not be veins (Fig. 17).

4. Spinal cord supplying arteries and a SDAVF may be observed at the same level and same side as

Figure 17 DSA of a SDAVF at the L3 level ( arrowhead ). ( A

Figure 17 DSA of a SDAVF at the L3 level ( arrowhead). (A ) The blood vessel that is opacified first resembles a radiculomedullary artery. It runs upward to the cone and lumbar enlargement and exhibits a narrow curve. ( B) Anterior position of the blood vessel in the lateral view. (C ) Filling of typical veins on the later image in the AP view confirms that the whole of intradural vessels are veins. The configuration of a radiculomedullary vein can be very similar to that of an artery (compare Figs. 11 and 12). Abbreviations : DSA, digital subtraction angiography; SDAVF, spinal dural arteriovenous fistula.

angiography; SDAVF, spinal dural arteriovenous fistula. Figure 18 DSA of a SDAVF with an anterior radiculo-

Figure 18 DSA of a SDAVF with an anterior radiculo- medullary artery entering at the same foramen. ( A ) AP view. The artery ( arrowheads ) is partially superimposed by the enlarged veins ( arrow ). ( B) The lateral view demon- strates the anterior position of the artery ( arrowheads ) and the posterior position of the mass of veins (arrow ). Abbre- viations : DSA, digital subtraction angiography; SDAVF, spinal dural arteriovenous fistula.

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54 Thron Figure 19 AVM of the filum terminale (DSA, AP views). ( A ) The

Figure 19 AVM of the filum terminale (DSA, AP views). ( A ) The anterior spinal artery ( black arrows ) is not unusually enlarged, but it continues without a change in caliber below the level of a cone in normal position. ( B ) At the L4 level, a second blood vessel is opacified that is a little bit larger than the artery and runs in upward direction (artery, black arrow ; arterial- ized terminal vein, arrowheads ). The clinical signifi- cance of this small AV shunt ( white arrow ) was considerable. Abbreviations : AVM, arteriovenous mal- formation; DSA, digital subtraction angiography.

demonstrated in Figure 18. They are better dis- criminated on lateral views.

5. If an anterior or posterior spinal artery seems to be too large for the region to be supplied or if it extends below the level of the cone, it should be followed caudally. This is the only way not to miss the small AVMs of the filum terminale (Fig. 19).

ACKNOWLEDGEMENT

Special thanks to Walter Korr, RWTH Aachen Univer- sity, for technical assistance in the computer graphic design of Figs. 1 and 3.

REFERENCES

¨

1. Kadyi H. U ber die Blutgefa¨ ße des menschlichen Ru¨ cken- markes. Lemberg: Grubnowicz u Schmidt, 1889.

2. Adamkiewicz A. Die Blutgefa¨ ße des menschlichen Ru¨ ck- enmarkes. II.Teil: Die Gefa¨ ße der Ru¨ ckenmarkoberfla¨ che. Sitzungsberichte der Akademie der Wissenschaften in

Wien, Mathematisch-Naturw issenschaftliche Klasse 1882; 85:101–130 (abstr 3).

3. Thron A. Vascular anatomy of the spine. In: Byrne James, ed. Interventional Neuroradiology. Oxford: Oxford Uni- versity Press, 2002.

4. Lasjaunias P, Berenstein A, ter Brugge K. Surgical Neuro- angiography. Volume1: Clinical Vascular Anatomy and Variations. 2nd ed. New York: Springer, 2002.

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Lazorthes G, Poulhes J, Bastide G, et al. La vascularisation arte´ rielle de la moelle. Recherches anatomiques et appli- cations a` la pathologie medullaire et a` la pathologie aortique. Neuro-Chirurgie 1958; 4:3–19.

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Lazorthes G, Gonaze A, Djindjian R. Vascularisation et circulation de la moelle epinie` re. Paris: Masson, 1973.

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Lasjaunias P, Vallee B, Person H, et al. The lateral spinal artery of the upper cervical spinal cord. J Neurosurg 1985;

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Fazio C, Agnoli A. The vascularization of the spinal cord. Anatomical and pathophysiological aspects. Vasc Surg 1970; 4:245–257.

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Tveten L. Spinal cord vascularity. The venous drainage of the spinal cord in the rat. Acta Radiol Diagn 1976; 17:653–662.

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Gillilan LA. Veins of the spinal cord. Neurology 1970;

20:860–868.

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Turnbull JM, Breig A, Hassler O. Blood supply of cervical spinal cord in man; a microangiographic cadaver study. J Neurosurg 1966; 24:951–965.

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Crock HV, Yoshizawa H. The blood supply of the verte- bral column and spinal cord in man. Wien, New York:

Springer, 1977.

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Thron AK. Vascular anatomy of the spinal cord. Wien, New York: Springer, 1988.

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Jellinger K. Zur Orthologie und Pathologie der Ru¨ cken- markdurchblutung. Wien, New York: Springer, 1966.

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von Quast H. Die Venen der Ru¨ ckenmarkoberfla¨ che. Gegenbaurs Morphologisches Jahrbuch 1961; 102:33–64.

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Suh TH, Alexander L. Vascular system of the human spinal cord. Arch Neurol Psychiat 1939; 41:659–677.

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Jacobs T. Venae radiculares. Anatomische Untersuchungen zur veno¨ sen Drainage des menschlichen Ru¨ ckenmarkes.

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Thesis. Medizinische Fakulta¨ t der Rheinisch-Westfa¨ lischen Technischen Hochschule Aachen, 1996.

18. Moes P, Maillot C. Les veines superficielles de la moelle epinie` re chez l’homme. Essai de systematisation. Archives d’Anatomie, d’Histologie et d’Embryologie Normales et

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Expe´ rimentales. Extrait du tome 64. Paris, Colmar: E di- tions Alsatia, 1981:5–110.

19. Foix Ch, Alajouanine TH. La mye` lite ne´ crotique subaigue. Rev Neurol 1926; 33:1–42.

20. Thron A, Koenig E, Pfeiffer P, et al. Dural vascular anoma- lies of the spine—an important cause of progressive myel- opathy. In: Cervos-Navarro J, Ferszt R, eds.Stroke and Microcirculation. New York: Raven Press, 1987.

21. Oswald K. Untersuchungen u¨ ber das Vorkommen von Sperrmechanismen in den Venae radiculares des Men- schen. Thesis. Berlin, 1961.

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anti-reflux des veines de la moelle. Neuro-Chir 1979;

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23. Otto J. Morphologie des Sperrmechanismus am Dura- durchtritt der Venae radiculares des Menschen. Neuro- radiologische und histologische Befunde. Thesis. Medizinische Fakulta¨ t der Rheinisch-Westfa¨ lischen Tech- nischen Hochschule Aachen, 1990.

4

Intracranial Collateral Routes and Anastomoses in Interventional Neuroradiology

David S. Liebeskind

UCLA Stroke Center, University of California, Los Angeles, California, U.S.A.

INTRODUCTION

Collateral circulation in the brain compensates for obstruction to arterial inflow or venous drainage (1). Descriptions of collateral vessels date back to the founding of neurology. Centuries after Sir Thomas Willis described arterial collaterals and their potential significance in disease, angiography illustrated the influential role of these routes. Hemodynamic studies later emphasized the critical impact of collaterals, yet subsequent imaging advances diverted attention away from angiography, seeking neuroprotection and targeting tissue ischemia. In the routine clinical practice of interventional neuroradiology, arterial and venous intracranial collaterals are influential factors in the diagnosis, treatment, and prognosis of various cerebrovascular disorders. Knowledge of collateral anatomy and patho- physiology may expand our understanding of numer- ous disorders. Correlative studies of imaging features and angiography may facilitate diagnosis and broaden perspectives on novel treatment strategies. This chap- ter reviews current knowledge of arterial and venous collaterals, emphasizing the specific implications of collaterals in various disorders.

ANATOMY

The anatomy of intracranial collaterals greatly influ- ences the capacity of these channels to provide alter- native blood flow routes across different regions, with collateral capacity primarily determined by luminal caliber. A description of arterial collateral anatomy may be subdivided between common routes, includ- ing Willisian collaterals at the circle of Willis or leptomeningeal anastomoses, and atypical circuits that may develop in response to particular lesions. Similarly, venous collateral anatomy may be described through the typical anastomotic routes and the atypical, a category in which the diversity and complexity of routes is enormous. Some connec- tions such as the posterior communicating artery (PCoA) represent embryonic remnants, whereas other routes form only in response to disease. There

are also numerous collateral extracranial-intracranial (EC-IC) routes, not discussed herein, for both arterial and venous flow diversions. Much of the knowledge regarding the anatomy of intracranial collaterals stems from historical descriptions over the last few hundred years. Only recently, with the advent of angiography and modern imaging techniques, have the functional correlates of these blood flow routes been established. Prior reports have classified collateral routes as pri- mary or secondary functional routes on the basis of anatomical location, yet this classification may be oversimplified, as great variability exists. The knowl- edge of intracranial collateral anatomy in humans is particularly important in understanding ischemic stroke and other clinical cerebrovascular disorders, as there are considerable differences in anatomy that may preclude successful translation of therapeutic approaches studied in animals (2). Species differences in the configuration of collaterals may also be com- pounded by differences in collateral anatomy among various individuals or populations. The circle of Willis provides numerous potential routes for blood flow diversion (Fig. 1). All of the Willisian segments, including the anterior communi- cating artery (ACoA), the proximal anterior cerebral artery (ACA), the PCoA, and the proximal posterior cerebral artery (PCA), may facilitate flow diversion in either direction depending on intraluminal pressure gradients. All of these segments may also be atretic or hypoplastic, yet they retain the ability to develop significant blood flow capacity and luminal expan- sion. These arterial segments are relatively closely matched in size and vessel wall characteristics with respect to their parent arteries. This configuration allows for interhemispheric collateral flow or compen- sation for gradients that may develop between the anterior and the posterior circulations. Much empha- sis has been placed on the anatomy of the PCoA (3,4). Various terms, including persistent or fetal PCoA anatomy, have been used to differentiate the status of this segment on the basis of diameter measure- ments at autopsy or on imaging studies, such as magnetic resonance angiography (MRA), where the status of this vessel or dominance is described in

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58 Liebeskind Figure 1 Schematic illustration of the circle of Willis and potential Willisian collaterals, including

Figure 1 Schematic illustration of the circle of Willis and potential Willisian collaterals, including ACoA (a), proximal ACA (b), PCoA (c), and proximal PCA (d). Abbreviations : ACoA, anterior communicating artery; ACA, anterior cerebral artery; PCoA, posterior communicating artery; PCA, posterior cerebral artery.

relation to the proximal PCA. Descriptive terms of the opposite situation, in which there has been involution of the PCoA’s embryonic origin from the internal carotid artery (ICA) resulting in a hypoplastic PCoA, have questionable validity, as even small-diameter remnants may once again provide blood flow if the need arises. Arterial patterns at the circle of Willis have been categorized by citing the prevalence of certain configurations, but such descriptive data are also questionable, as anatomy may change with dis- ease and age or vary among populations. The leptomeningeal anastomoses bridging distal reaches of the major cerebral arteries are small (* 50–400 m m) arteriolar connections that allow for retrograde perfusion of adjacent territories (Fig. 2) (5,6). Such connections display variable configura- tions, including end-to-end anastomoses, end-to-side connections, and azygous variants (6). These arteriolar anastomoses adjoin the middle cerebral artery (MCA) with both the ACA and the PCA. Anastomoses from the ACA potentially feed the superior or anterior divisions of the MCA, with most of the posterior or inferior division MCA collateral flow arising from the PCA. Such connections are relatively sparse between the ACA and the PCA. The seminal work of Vander Eecken and Adams on 20 human cadavers delineated the principal characteristics of leptomeningeal anasto- moses, illustrating considerable variability in the size, number, and location of these collaterals (6). Such

size, number, and location of these collaterals (6). Such Figure 2 Schematic illustration of principal supratentorial

Figure 2 Schematic illustration of principal supratentorial lep- tomeningeal anastomoses in the brain, including ACA-MCA (a) and PCA-MCA (b) routes. Abbreviations : ACA, anterior cere- bral artery; MCA, middle cerebral artery; PCA, posterior cerebral artery.

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great variability likely influences the results of any particular anatomical study and accounts for much controversy in correlative studies of collateral function with age. Anastomoses also converge over the cere- bellar convexities, where the distal branches of the posterior inferior cerebellar arteries (PICAs), anterior inferior cerebellar arteries, and superior cerebellar arteries (SCAs) meet (Fig. 3). Because of the symmetric anatomy of posterior fossa structures, such anastomo- ses may allow for collateral flow between cerebellar hemispheres and from proximal to distal aspects of the basilar distribution. In cases in which flow demands and pressure gradients exceed the capacity of primary arterial routes and Willisian or leptomeningeal collaterals, atypical routes of collateral flow may develop. Some collateral routes may utilize the paths of normal variants, such as azygous connections between the ACAs. The anterior and posterior choroidal arteries may distribute blood flow in either direction between the anterior and posterior circulations. In cases of moyamoya, this choroidal network is commonly recruited. Other moyamoya arterioles pervade sub- cortical structures, meandering around occluded MCAs. Anastomoses may shunt flow between the PCA and the SCA at the tentorial edge. More unusual arterial collateral routes may also arise, commonly in association with prominent EC-IC collaterals. Atypical collaterals can be demonstrated in almost any config- uration, limited to an extent solely by physical barriers such as the falx or tentorium.

solely by physical barriers such as the falx or tentorium. Figure 3 Schematic illustration of cerebellar

Figure 3 Schematic illustration of cerebellar anastomoses, demonstrating potential collateral flow between SCA (a), AICA (b), and PICA (c). Abbreviations : SCA, superior cerebellar artery; AICA, anterior inferior cerebellar artery; PICA, posterior inferior cerebellar artery.

Venous collateral anatomy is best understood in light of typical venous flow patterns (Fig. 4) (7,8). Venous drainage is balanced by superficial and deep systems, with the transcerebral veins allowing for potential shunting in either direction. The superficial system, including the cortical veins and superior sagittal sinus, typically empties the majority of out- flow toward the right transverse and sigmoid sinuses and into the jugular. The anastomotic veins of Trolard and Labbe´ shunt flow across the cerebral hemisphere to drainage pathways with lower pressures. Similarly, cortical veins share connections, allowing for diver- sion of flow. The deep system includes the choroid plexuses and draining veins of the thalami, striatum, periventricular white matter, limbic regions, and ros- tral brain stem. Larger emissaries of this system include the basal veins, vein of Galen, and straight sinus. The deep system may drain via the straight sinus and into the left transverse system or, alterna- tively, send flow anteriorly toward the basal veins. Numerous anastomoses abound toward the inferior surface of the brain, allowing for drainage of the deep system. The deep middle cerebral vein, inferior and superior petrosal sinuses, and the basilar plexus may shuttle flow across these regions. Because of the vari- ability in venous outflow patterns and potential anas- tomoses to relieve focal venous hypertension, minimal attention has been placed on systematic characteriza- tion of venous collateral anatomy.

systematic characteriza- tion of venous collateral anatomy. Figure 4 Schematic illustration of intracranial venous

Figure 4 Schematic illustration of intracranial venous anatomy and typical collateral routes, including vein of Trolard (a), vein of Labb (b), deep middle cerebral vein (c), superior petrosal sinus (d), pterygoid plexus (e), inferior petrosal sinus, and basilar plexus (f).

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60 Liebeskind Figure 5 Right ICA injection on angiography, demonstrating Willisian and leptomeningeal collateral flow

Figure 5 Right ICA injection on angiography, demonstrating Willisian and leptomeningeal collateral flow in acute stroke due to left ICA occlusion. Abbreviation : ICA, internal carotid artery.

EPIDEMIOLOGY

The epidemiology of intracranial collaterals has occa- sionally been broached in the literature, citing varia- tions in Willisian anatomy or unfounded theories related to collateral development in different cohorts, such as the elderly. Most of these studies have used anatomical data based on autopsy series. Unfortu- nately, this approach of using anatomical postmortem data to describe potential collateral function does not make sense when one considers the dynamic changes in collateral flow that take place during life. Studies of Willisian configuration in normal individuals are also limited, as collaterals are irrelevant in the absence of disease. Functional assays such as angiographic dem- onstration of collateral flow during particular clinical scenarios, such as acute ischemic stroke, provide fur- ther information (Fig. 5), yet serial changes or a reflec- tion of collateral development may still go unresolved. Other reports in the literature have extrapolated find- ings on coronary or peripheral arterial collaterals to the cerebral circulation , without validation. Much speculation has addressed the influence of age on collateral flow, yet considerable variability with intra- cranial collaterals likely occurs with increasing age (9). There is scant epidemiological data on arterial collat- eral flow, via Willisian or leptomeningeal routes, even within a specific disease state, and the epidemiology of venous collaterals is unknown.

PATHOPHYSIOLOGY

The pathophysiology of collateral circulation in the brain has largely been unexplored. Much of the knowledge regarding arte rial collaterals has been extrapolated from studies of collateral circulation in other vascular beds or in animal models in which vast differences exist with respect to collateral anatomy. Venous collateral pathophysiology remains virtually completely unknown. Most of the very few studies of

collateral flow in humans relate to anatomical patterns and resultant blood flow, yet very little is known about collateral recruitment. The process of arterio- genesis, or the recruitment and development of pre- existing arterioles to accommodate significant flow changes, must be distinguished from angiogenesis, the de novo growth of vessels (10). Features of both may be simultaneously involved with various cere- brovascular disorders, yet the role of these processes is quite distinct. Furthermore, although arterial collat- erals may be emphasized in acute ischemic stroke, there are likely changes that take place in the venous system as well. Similarly, failure of venous collateral- ization in cerebral venous thrombosis (CVT) may ultimately affect arterial inflow, leading to ischemia. As a result, the arterial and venous components must be considered in concert. Venogenesis, the venous counterpart of arteriogenesis, is assumed to be similar to the pathophysiological events that accompany the arterial process. Time is also a critical variable, as the capacity of collaterals to adapt to blood flow derange- ments changes with time. The particular role or influ- ence of collaterals in specific disorders is considered in subsequent sections of this chapter. With all of these entities, however, it remains important to distinguish the presence of collaterals at a specific time point versus the development or collateralization process itself.

The presence or extent of collaterals defined on angiography or imaging reflects the result of an adap- tive process responding to significant blood flow alterations. The process of collateralization may be best studied in cases in which collaterals are subopti- mal or in cases with progressive ischemia or conges- tion, allowing for investigation over a prolonged time course. In cases of acute stroke with exuberant collat- erals, the process may be obviated or fully realized. The pathophysiology of arteriogenesis has been estab- lished in the peripheral and coronary circulations (11,12). Arteriogenesis is principally mediated by

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Routes and Anastomoses in Interventional Neuroradiology 61 Figure 6 Table summary of the critical differences between

Figure 6 Table summary of the critical differences between arteriogenesis and angiogenesis and implications in acute cerebral ischemia.

increased fluid shear stress due to mechanical forces that accompany pressure gradients across anastomotic vessel segments. Inflammation plays a key role, incited by cytokine upregulation and macrophage infiltration due to mechanical events at the anastomo- ses (13). Vascular remodeling allows for potential expansion of the anastomotic vessel radius, thereby increasing flow and alleviating fluid shear stress. This process has considerable differences with respect to angiogenesis (Fig. 6). Arteriogenesis may rapidly cul- minate in dramatic increases in blood flow, whereas angiogenesis is a local phenomenon that increases permeability and relatively fragile capillary growth without the capacity for significant increases in blood flow. Angiogenesis in the brain occurs in perilesional areas around arteriovenous malformations, tumors, and stroke (14). Recently, the potential for angiogen- esis and concomitant neurogenesis has been the focus of investigation in studies of stroke recovery or restor- ative neurology. The potentially beneficial role of inflammation in cerebral arteriogenesis has yet to be established. In other arterial beds, inflammation simultaneously promotes atherosclerosis and corre- sponding arteriogenesis. Very recently, genetic upre- gulation of the actin-binding Rho-activating protein triggered by mechanical factors at anastomotic sites has been discovered (15). Although the basic vascular pathophysiology of arteriogenesis and collateraliza- tion is likely to be similar, the anatomy of intracranial collaterals and resultant pathophysiology may be quite distinct (16). Willisian collaterals allow for prompt flow diver- sion across relatively small distances between arterial territories. Pressure differentials allow for potential circuits to open, causing flow to course toward the ischemic vessel or territory. The diameter of these connections may be quite variable across individuals, likely reflecting developmental variation and subse- quent evolving changes during life. Willisian collater- alization and the appearance of the circle of Willis is therefore a dynamic process (17). Leptomeningeal anastomoses may also evolve in response to environmental stressors, yet the nature of leptomeningeal collateral perfusion is quite complex. The elongated pathways bridging arterial territories provide blood flow via a limited number of distal anastomoses that perfuse the ischemic territory in a

retrograde fashion. Such reverse arterial flow via selective daughter branches is extremely unusual (Fig. 7), unlike other blood flow routes in the systemic circulation. This pattern of blood flow violates the major hemodynamic principal of Murray’s law, where flow is configured in a manner that is energy efficient (18). It remains unknown whether the distal arterial tree adapts to conform to this ideal mode of blood flow by constricting adjacent daughter arteries. The resulting slow flow is largely diverted toward the parent occluded arterial segment. Intravascular deox- ygenation likely occurs because of slow flow past ischemic endothelium and neighboring ischemic brain parenchyma (19).

endothelium and neighboring ischemic brain parenchyma (19). Figure 7 Diagram of retrograde leptomeningeal flow in the

Figure 7 Diagram of retrograde leptomeningeal flow in the setting of MCA occlusion (a), illustrating anastomotic inflow via isolated distal segments (b, c) and predominant flow toward the trunk of the occluded parent artery (d). Abbreviation : MCA, mid- dle cerebral artery.

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In response to ischemia, the microcirculation adapts through loss of flow heterogeneity to accommo- date maximal oxygen extraction (20). Low-perfusion hyperemia, the expansion of cerebral blood volume (CBV) despite diminished blood flow due to arterial occlusion, relies heavily on the venous system (9). The mechanisms underlying venous engorgement remain unclear, but progressive expansion of the venous bed downstream from the ischemic arterial territory has been well documented (9). A critical and potentially influential question addresses what leads to the demise of this compensatory mechanism. Cerebral venous steal, reduction of the critical pressure gradient to maintain collateral arterial inflow, and the venoarterial reflex have been postulated as potential factors (21). These factors may also be important in the process of arterialization of the venous system that accompanies other cerebrovascular disorders. Paradoxically, much of the vascular pathophysi- ology relating to cerebral hemodynamics and intra- cranial collateral flow was uncovered more than 25 years ago. Although angiography was pivotal in these investigations, it was subsequently replaced by more noninvasive imaging modalities. The unrealized hopes of neuroprotection and isolated focus on the ischemic cascade without consideration of blood flow diverted attention away from hemodynamics and vascular pathophysiology that interventional neuro- radiologists often observe in the angiography suite.

CLINICAL CORRELATES

The clinical features associated with collateral circu- lation are often manifested as a dramatic minimization of symptoms despite severe obstruction to normal blood flow. Examples of this phenomenon include asymptomatic acute occlusion of the MCA or clini- cally silent occlusion of the ICA. Similar events may occur even more frequently with venous collateraliza- tion. For instance, CVT involving the principal dural sinuses may go undetected (Fig. 8). Such examples of collateral ability to ameliorate or minimize clinical symptoms are often recognized only when dynamic changes cause transient loss of this ability. In such situations, wide fluctuations in symptoms or neuro- logical deficits may be apparent. These fluctuations are most commonly observed during the very early stages of acute ischemia, during the first minutes and hours after presentation. In cases of MCA ischemia triaged in the prehospital setting as soon as 15 minutes after symptom onset, deficits are often quite minimal, followed by considerable changes and often devastat- ing consequences at later time points. Certain clinical features may also be described with specific disorders. Collateral failure may occur during subacute stroke despite previously sustained perfusion and no appar- ent blood pressure or hemodynamic changes. In a similar fashion, the limb-shaking transient ischemic attacks (TIAs) of moyamoya may represent only tran- sient collateral failure. Referred auditory phenomena or bruits may indicate venous collateralization. Many of these clinical features are often suspected to be

Many of these clinical features are often suspected to be Figure 8 CTV demonstrating transverse and

Figure 8 CTV demonstrating transverse and sigmoid sinus thromboses ( arrows ) with isolated headache. Abbreviation :

CTV, computed tomographic venography.

mediated by collaterals, yet imaging or angiography is often required to substantiate these claims.

IMAGING

Unlike the principal arterial and venous routes in the brain, imaging of collaterals evades most current techniques (22), partly because when disease alters the normal pathways for blood flow, collaterals will develop via numerous trajectories. Furthermore, col- lateral anastomoses tend to be diminutive, as they are recruited only as they are needed. As a result, the goal of imaging collaterals often follows an indirect path where much is inferred on the basis of vascular distributions and the oxymoronic objective of attempt- ing to see what cannot be seen. There is no ideal imaging modality for demonstration of collaterals. Although conventional angiography has been ex- tremely influential in characterization of collaterals and angiographic correlation is often used to substan- tiate noninvasive markers of collateral flow, there remain qualitative aspects of collateral perfusion that evade angiography. As a result, imaging characteriza- tion of intracranial collaterals is founded on integra- tion of findings from various studies. Each modality brings a specific advantage or limitation. For instance, MRA may fail to demonstrate flow in a functional ACoA if a specific threshold is not met. In contrast, computed tomographic angiography (CTA) may dem- onstrate fairly extensive leptomeningeal collaterals, yet the flow in these segments may be quite minimal

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Routes and Anastomoses in Interventional Neuroradiology 63 Figure 9 CTA source images depicting contrast opacification

Figure 9 CTA source images depicting contrast opacification of leptomeningeal vessels (arrows ) in the setting of acute left MCA occlusion. Abbreviations : CTV, computed tomographic venogra- phy; MCA, middle cerebral artery.

(Fig. 9). Differences inherent to each modality may accentuate flow or anatomical patency to varying degrees. For most of the clinical disorders encoun- tered in interventional neuroradiology that are described in this chapter, angiography remains para- mount for definitive characterization of collateral flow. Whereas Willisian routes are more easily depicted with various imaging modalities, leptome- ningeal collaterals are more difficult to delineate. Many of the noninvasive imaging correlates beyond definition of collaterals on conventional angiography have been described and are based on findings in acute ischemic stroke. Extrapolation from acute ische- mia to other variants, such as near occlusion or recurrent ischemia border ing on critical perfusion thresholds, has provided insight into other clinical scenarios where arterial collaterals are pivotal (22). Paradoxically, the acute ischemic stroke imaging find- ings of collateral perfusion may even have valuable information related to venous collateral system as well. For instance, imaging of congested venous drain- age in low-perfusion hyperemia may be similar to the findings noted in CVT. Imaging of collaterals is best described by distributions, direct visualization of the anatomical structures th emselves, and functional aspects including perfusion. The advent and increas- ingly routine clinical application of multimodal CT and MRI, incorporating parenchymal images, some extent of angiographic depiction of proximal lesions and corresponding collateral circulation, as well as perfusion may be gleaned.

The vascular distributions of arterial or venous collaterals mirror normal patterns of arterial supply or venous drainage. For instance, the borderzones of the MCA territory are based on the normal pattern for the periphery of blood flow in this artery. Unfortunately, these boundaries shift on the basis of variations in normal anatomy and with disease. In general, regions deep within the expected primary vascular distribu- tion are collateral poor, whereas those at the periphery are collateral rich. The extreme variability of venous collateral anatomy makes it quite difficult to infer such distributions. CT or MRI parenchymal sequences may demonstrate patterns suggestive of collateral recruitment. Insular vulnerability in MCA occlusion suggests collateral salvage of more peripheral cortical regions (Fig. 10). Similarly, borderzone infarcts may suggest collateral hemodynamic insufficiency. Direct visualization or imaging of Willisian routes may be feasible with most diagnostic modal- ities. The short segmental collaterals at the circle of Willis may be demonstrable with transcranial color- coded Doppler ultrasonography, CTA, MRA, and conventional angiography. In the setting of acute ischemic stroke, Willisian flow patterns reflect changes that took place shortly after arterial occlusion.

changes that took place shortly after arterial occlusion. Figure 10 CT in acute right MCA stroke

Figure 10 CT in acute right MCA stroke with isolated hypoden- sity of the insular region (arrows ). Abbreviations : CT, computed tomography; MCA, middle cerebral artery.

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Once flow is restored with proximal recanalization, such diversion of flow and the pattern of Willisian collaterals may change abruptly. Changes in Willisian flow with apparent arterial diameter expansion may also be evident in serial imaging of cases with chronic hypoperfusion or ischemia (17). Leptomeningeal col- laterals may be evident on conventional angiography and CTA, and only in rare circumstances with MRA. The slow flow in leptomeningeal collateral routes precludes adequate visualization of these segments with MRA. CTA source images may provide an indi- cation of the extent of leptomeningeal collaterals when viewed in axial format. The ability to depict venous collaterals is analogous to demonstration of leptome- ningeal arterial collaterals: conventional angiography and CTA may illustrate these channels, yet MRA or magnetic resonance venography (MRV) is limited. On review of parenchymal sequences, venous collaterals may be seen as engorged or dilated structures with prominent flow voids. Such an appearance may indicate the presence of a peripherally situated arte- riovenous malformation ( Fig. 11). Conventional angiography may easily demonstrate the presence of arterial or venous collateral routes, with some infor- mation regarding functional capacity evident by the temporal appearance of delayed opacification or washout. Such images provide a link between the

or washout. Such images provide a link between the Figure 11 MRI evidence of flow voids

Figure 11 MRI evidence of flow voids (arrows ) associated with a previously undiagnosed CAVM. Abbreviation : CAVM, cerebral arteriovenous malformation.

anatomical information o f vessel appearance and functional aspects of resultant perfusion. Aside from demonstrating the presence of col- lateral routes, imaging may also provide some insight into the functional aspects or capacity of collaterals. Various modalities may characterize features of col- lateral blood flow and nutrient or oxygen exchange. The amount of flow in various Willisian collaterals may be estimated from transcranial Doppler (TCD); however, velocity measures alone may be deceiving, as diameter changes may accompany collateral recruitment. In contrast to the previous discussion regarding direct visualization of collaterals, MRA or MRV may have an advantage over CTA or computed tomographic venography (CTV): MRA or MRV accentuates flow characteristics rather than anatomy. Therefore, standard time-of-flight (TOF) MRA may provide very useful information regarding capacity of specific collateral routes. Conventional MRI sequen- ces may provide some subtle, yet very useful, findings related to collateral flow. Fluid-attenuated inversion recovery (FLAIR) MRI vascular hyperintensity (FVH) may be evident in distal aspects of an occluded artery because of slow, retrograde leptomeningeal collateral filling of the artery (Fig. 12) (23,24). Deoxygenation in such distal arterial segments may be evident with gradient-recalled echo (GRE) sequences (19). Such signal loss on GRE associated with deoxygenation may also be observed in draining veins from the ischemic territory in stroke or in engorged venous

from the ischemic territory in stroke or in engorged venous Figure 12 Slow, retrograde leptomeningeal collateral

Figure 12 Slow, retrograde leptomeningeal collateral filling of the left MCA demonstrating FVH ( arrows ). Abbreviations : MCA, middle cerebral artery; FVH, FLAIR MRI vascular hyperintensity.

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Routes and Anastomoses in Interventional Neuroradiology 65 Figure 13 GRE prominence of the draining basal vein

Figure 13 GRE prominence of the draining basal vein ( arrow) suggesting deoxygenation in the setting of acute stroke. Abbre- viation : GRE, gradient-recalled echo.

collaterals because of thrombosis (Fig. 13). Recent developments in MRI have capitalized on the ability to encode spatial or directional information with phase-contrast (PC) MRA techniques, or selective labeling of specific arterial inflow routes with selective arterial spin-labeled (SASL) perfusion (25). Arterial spin-labeled perfusion MRI may reveal delayed arte- rial transit effects because of slow, leptomeningeal flow supplying the periphery of an ischemic lesion. Commonly used contrast-bolus perfusion techniques with CT or MRI also provide important information

regarding collateral flo w. Both modalities demon- strate delay and dispersion of contrast passage that are characteristic of collateral flow (Fig. 14). CBV is often elevated, and microcirculatory changes may be evident if one analyzes the tissue concentration curves in detail. When considering perfusion imaging tech- niques, one must remember that specific patterns may change rapidly with time and that certain perfusion findings may have different implications in acute versus chronic settings. During chronic phases, spe- cific perfusion abnormalities may be better tolerated.

DISORDERS

Arterial and venous disorders affecting the brain invar- iably involve some element of collateral circulation. Collaterals may serve a compensatory role to sustain oxygen and nutrient delivery scaled to metabolic demand, or these alternative blood flow routes may maintain homeostasis through relief of venous conges- tion. These beneficial roles are complemented by potentially detrimental aspects. For instance, collateral arterial feeders and venous routes may hinder treat- ment of arteriovenous malformations as these channels proliferate because of humoral and mechanical influ- ences. Although the extent of collaterals may only marginally influence current clinical decision making, the goals of revascularization procedures or treatments are often synonymous with collateralization. Similar- ities exist in the anatomy of collateral routes and related pathophysiology, yet the role of collaterals is best understood within the context and following dis- cussion of specific cerebrovascular disorders.

Ischemic Stroke

Collaterals play a crucial role in acute ischemic stroke (1,22,26). Although not all strokes are associated with thromboembolic occlusion of an intracranial artery or arteriole, ischemia in an arterial territory or bed is universal. Progressive stenosis of a proximal artery may also incite ischemia and elicit collateral recruit- ment. The degree or extent of collateral compensation varies, as distal cortical branch occlusions or lacunar strokes have limited collateral routes to balance

or lacunar strokes have limited collateral routes to balance Figure 14 Schematic illustration of the normal

Figure 14 Schematic illustration of the normal tissue concentration curve (A) and the delay and dispersion associated with collateral flow ( B) in the setting of acute stroke.

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diminished antegrade flow. The vast knowledge re- garding intracranial arterial collateral pathophysiol- ogy has been garnered from clinical observations and imaging correlates during acute or subacute cerebral ischemia. During these dynamic early stages of collat- eral adaptation to ischemia, patients often undergo various imaging studies, including angiography. At later stages, a more stable balance between residual antegrade flow and collaterals develops. As a result, some of the observations regarding collaterals in acute ischemic stroke may be relatively unique, precluding translation of these observations to other clinical set- tings. The critical role of collaterals is accentuated by the impressive impact of collateral perfusion on recan- alization and the fallacy of neuroprotection without blood flow to the penumbra beyond the occluded vessel segment (2). Great emphasis has duly been placed on proximal recanalization; however, such approaches are often futile, and sustenance of the penumbra via collaterals may be the only viable ther- apeutic option. To capitalize on potential collateral therapeutic interventions, attention must be focused on integration of the wealth of clinical, imaging, and angiographic data, which are often collected during early stages after symptom onset (Fig. 15). Collateral pathophysiology in acute stroke may be ideally described in the setting of MCA occlusion. As soon as distal intraluminal arterial pressure beyond the clot plummets because of failure of ante- grade flow, collaterals are recruited. Ischemia associ- ated with a large pressure gradient, and not hypoxia, is the principal driving force that encourages blood flow to traverse the leptomeningeal anastomoses between the distal reaches of the ACA and the PCA and into the MCA field. Augmented flow in these small anastomoses causes a dramatic rise of fluid

shear stress and resultant vascular remodeling because of arteriogenesis. Upregulation of various cytokines and macrophage invasion leads to perme- ability derangements in these areas at the far periph- ery of the ischemic field. Eventually, this process leads to an increase in the radii of these small collateral routes. Release of angiotensin II and neuropeptide Y may cause systemic hypertension, yet ironically the relatively intact vasoconstrictive capacity of these dis- tal arterioles may offset attempted hypertension- mediated increases in flow. Retrograde MCA flow is highly energy inefficient, and even slight reductions in the driving pressure gradient may cause collateral failure. CBV elevations, principally due to venous engorgement and loss of flow heterogeneity in the microcirculation, allow for optimal oxygen and nutri- ent extraction. Eventually, however, a series of detri- mental events may ensue, where CBV drops and collateral failure is manifest. The triggers for failure of such beneficial early stages of CBV elevation that has been termed low-perfusion hyperemia remain unclear. Unless correlative imaging or angiographic stud- ies are acquired, the dynamic clinical fluctuations due to collateral flow during acute ischemic stroke may go unfounded. Rapid changes in head positioning and dramatic increases in volume due to fluid boluses may produce profound changes and even normalization of the neurological examination, despite persistent arte- rial occlusion. Unfortunately, such changes may be transient, as sudden deterioration due to collateral failure may also occur. This paradigm is most worri- some when early hemodynamic improvement deters the clinician from intravenous thrombolysis within three hours and subsequent deterioration occurs well beyond this limited therapeutic window.

occurs well beyond this limited therapeutic window. Figure 15 Diffusion-weighted imaging ( A ), time-to-peak

Figure 15 Diffusion-weighted imaging ( A), time-to-peak PWI map (B), and angiogram ( C) in acute left MCA occlusion. Abbreviation :

MCA, middle cerebral artery.

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Routes and Anastomoses in Interventional Neuroradiology 67 Figure 16 Acute left MCA occlusion on MRA (

Figure 16 Acute left MCA occlusion on MRA (A) with unrevealing diffusion-weighted imaging ( B ) despite extensive time-to-peak abnormalities on perfusion- weighted imaging (C). Abbreviations: MCA, middle cere- bral artery; MRA, magnetic resonance angiography.

Case 1

A 92-year-old woman presented with acute onset of right hemiparesis and aphasia. Emergent MRI was acquired, and it revealed occlusion of the left MCA without diffusion-weighted imaging evidence of tis- sue injury (Fig. 16). FVH illustrated slow, retrograde collateral filling of the left MCA (Fig. 17). After 20 minutes in supine position during the MRI, her neurological deficits completely resolved. On return to the ER, she sat upright and her prior deficits of aphasia and hemiparesis recrudesced. Robust lepto- meningeal collaterals were evident on angiography (Fig. 18), and after complete recanalization with mechanical thrombectomy her exam normalized again. Her transient collateral failure associated with changes in head positioning prompted the decision to proceed with thrombectomy. This case demonstrates that collaterals may avert tissue injury despite abrupt cessation of arterial flow and that vigorous collaterals may be evidenced even with advanced age. Almost every imaging modality provides some information regarding collateral flow in acute ischemic stroke. TCD ultrasonography may exhibit flow diver- sion at the circle of Willis during acute MCA occlusion; increased velocities in other arterial segments may

signify collateral flow. Transcranial color-coded ultra- sonography may also provide direct visualization of such Willisian correlates. Often, the most demonstrable indirect evidence of collateral flow is loss of the insular ribbon on noncontrast CT. This finding suggests col- lateral preservation of the remainder of the MCA field. Infarct growth in the setting of persistent occlusion is also partially a reflection of collateral failure. MRI offers several further facets of collateral flow in acute stroke. FVH in distal segments of the MCA or occluded vessel is due to slow, retrograde leptomeningeal col- lateral flow (23,24). As the days from symptom onset lapse, this finding subsides because of stabilization or equilibration of collateral flow with infarct growth. Correlation with conventional angiography proves that FVH is not due to thrombosis itself. GRE MRI sequences may depict deoxygenation in distal lepto- meningeal collaterals, in draining veins, and in the ischemic tissue as well. Permeability derangements at the borderzones associated with collateral recruitment may also be depicted as subarachnoid hyperintensity on FLAIR (Fig. 19) or with dedicated permeability imaging techniques. Collateral perfusion is most readily identified on perfusion CT or MRI techniques. The footprints of collateral perfusion are evident as prolongation in time-to-peak contrast bolus, elevated

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68 Liebeskind Figure 17 FVH in the distal left MCA ( arrow ) reflecting predom- inantly

Figure 17 FVH in the distal left MCA ( arrow ) reflecting predom- inantly PCA to MCA collateral flow. Abbreviations : FVH, FLAIR MRI vascular hyperintensity; MCA, middle cerebral artery; PCA, posterior cerebral artery; MCA, middle cerebral artery.

mean transit times, augmented CBV, and microcircu- latory measures demonstrating loss of flow heteroge- neity. These individual parameter maps may be generated with either CT or MRI perfusion techniques.

Other imaging techniques, such as single-photon emission computed tomography (SPECT) or positron emission tomography (PET), may provide additional hemodynamic or even metabolic information related to collateral perfusion, yet such approaches are often cumbersome or impractical in the setting of acute ischemic stroke. The utility of such perfusion imaging studies to depict regions dependent on collateral flow gave rise to the development of mismatch as an imag- ing surrogate of salvageable penumbra. Various defi- nitions or iterations of mismatch have been developed to ideally select candidates for therapeutic intervention while minimizing risk. Although in the literature much emphasis has been placed on imaging identification of mismatch, incredibly few have substantiated the basis of this approach addressing the actual source of collat- eral perfusion. Furthermore, it is often forgotten that such imaging techniques provide only a snapshot in time of an extremely dynamic process that may radi- cally differ within minutes. Others have attempted to utilize noninvasive angiographic depictions of collat- eral flow. CTA source images may provide some indi- cation for the extent of collateral perfusion, yet the prolonged imaging acquisition obliterates temporal information related to flow in order to achieve more anatomical images. MRA may fail to demonstrate leptomeningeal collaterals, yet ipsilateral changes in the PCA may be indicative of PCA to MCA collateral flow in acute stroke (Fig. 20). Such changes may include prolongation or extension of the apparent PCA course on MRA reconstructions, or increases in the apparent PCA diameter (27). Ultimately, definitive proof of collateral supply depends on conventional angiography (28). However, correlation of angio- graphic findings with the often subtle noninvasive imaging findings noted above provides important information in other cases when angiography is not available or for ongoing imaging research related to collateral circulation. Angiography may reveal flow

to collateral circulation. Angiography may reveal flow Figure 18 Retrograde leptomeningeal collateral filling of

Figure 18 Retrograde leptomeningeal collateral filling of the left MCA territory demonstrated with angiography on a left common carotid artery injection. Abbreviation :

MCA, middle cerebral artery.

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Routes and Anastomoses in Interventional Neuroradiology 69 Figure 19 Subarachnoid hyperintensity on FLAIR due to

Figure 19 Subarachnoid hyperintensity on FLAIR due to increased permeability and contrast leakage at the leptomenin- geal borderzones. Abbreviation : FLAIR, Fluid-attenuated inver- sion recovery.

: FLAIR, Fluid-attenuated inver- sion recovery. Figure 20 Ipsilateral prominence of the PCA ( arrows )

Figure 20 Ipsilateral prominence of the PCA (arrows ) on MRA in the setting of acute right MCA occlusion. Abbreviations : PCA, posterior cerebral artery; MRA, magnetic resonance angiogra- phy; MCA, middle cerebral artery.

diversion via Willisian routes and leptomeningeal sources of perfusion during the arterial phase. Adjacent arteries such as the ACA or the PCA are initially visualized, followed by a momentary delay during transit through anastomoses beyond the resolution of conventional angiography, culminating with retro- grade filling of the MCA. Similarly, PICA to SCA anastomoses over the cerebellar convexities may bypass severe stenoses or occlusions of the basilar. The extent, but also the temporal features, of such filling patterns are important for adequate character- ization of collateral flow. Several scales have been developed to capture such information, incorporating the delay of collateral perfusion that may be prolonged well beyond the normal capillary filling and into the late venous phases (29,30) . Such prolongation of venous perfusion may also provide important infor- mation regarding the venous congestion associated with elevated CBV and the low-perfusion hyperemia of acute stroke. As most of the limited number of angiographic scales that capture information on collat- eral flow emphasize arterial filling, angiographic cor- relation with perfusion mismatch may be somewhat inaccurate. Following effective reperfusion due to recanalization and cessation of collateral dependence, all of these imaging or angiographic markers of collat- eral flow disappear. In fact, persistence of such markers of collateral flow may be indicative of incomplete reperfusion. Many of these imaging markers of collat- eral flow may be seen with other cerebrovascular disorders, but multimodal correlation is often best with the contemporaneous imaging approach unique to acute ischemic stroke. The reliance on angiography for validation of collateral supply largely limits observations on collat- eral flow in acute stroke to cases in which endovas- cular therapy is entertained or to the decreasing number of cases in which diagnostic conventional angiography is pursued. Collateral flow has been demonstrated as a strong predictor of favorable clinical outcome in intra-arterial thrombolysis and mechanical thrombectomy (31,32). Collateral flow does not appear to influence the success of proximal recanalization, yet ischemic injury may be lessened in tissue supplied by collaterals beyond the occlusion, or such regions may be sustained until partial restoration of antegrade flow is estab lished. Collateral flow may also thereby decrease the risk of hemorrhagic transformation. The pattern of collateral filling, such as Willisian diversion and configuration of potential ACA collateral flow in ICA occlusion, may have a substantial effect on outcome. The unusual filling pattern of retrograde arterial flow in the ischemic field may also determine the quality or effects of collateral perfusion (Fig. 21). Willisian collaterals have recently been used for delivery of endovascular therapy (33). The first endovascular device utilizing collaterals, NeuroFlo TM , is also currently being studied in clinical trials. The device employs augmentation of cerebral blood flow that accompanies titration of concomitant supra- and infrarenal artery aortic bal- loon inflation during acute stroke (Fig. 22). However, the mechanism of this approach remains to be eluci- dated. Once proximal recanalization or antegrade

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70 Liebeskind Figure 21 Frontal projection of a left ICA injection on angio- graphy demonstrating retrograde

Figure 21 Frontal projection of a left ICA injection on angio- graphy demonstrating retrograde filling of the MCA. Abbreviation :

ICA, internal carotid occlusion.

flow is restored, angiographic collaterals dissipate. In clinical practice, the appearance of robust collaterals on angiography may be deceiving in decision making. One may be compelled to forgo relatively risky inter- ventions to establish antegrade flow when collaterals are excellent. Unfortunately, when left untreated, many of these cases may be prone to collateral failure. Alternatively, the degree of collaterals may lessen stroke severity or clinical outcome even after failed recanalization. Despite these ostensibly critical impli- cations of collateral flow in acute stroke, collaterals are often regarded as only a curious finding on angiog- raphy in acute stroke. Most multicenter trials of endo- vascular therapy to date have considered collaterals only in post hoc analyses.

Ongoing investigations of collateral circulation in acute cerebral ischemia may elucidate important clinical features, imaging correlates, and undisclosed pathophysiology of collateral perfusion. Such studies may also provide relevant information for translation to the management of other cerebrovascular disor- ders. These findings may cease the unshakable failure of neuroprotection related to ongoing disregard for collateral perfusion and facilitate the development of collateral therapeutics (2,26). Endovascular therapy for proximal recanalization may be refined, allowing for collateral augmentation after failed recanalization and for prolonged windows of opportunity. The cal- culations of time is brain assuming a linear function may also be clarified through consideration of collat- erals and the ability to maintain tissue for prolonged periods of time. Revision of this concept may recog- nize that time is brain because collaterals may fail with time.

Intracranial Atherosclerosis

Although the intracranial arterial collateral circulation has been well described in acute ischemic stroke and in chronic extracranial occlusive disease, knowledge of collaterals in chronic intracranial occlusive disor- ders is largely limited to moyamoya. In chronic intra- cranial atherosclerotic disease, arterial stenosis may be isolated to a specific arterial segment, invoking a particular pattern of collateral development. Further- more, antegrade flow in that territory may not be viable via shorter segmental bypasses provided by the lenticulostriate collaterals of moyamoya. In con- trast to acute ischemic stroke, where complete or subtotal occlusion is common, a wide range in the degree of stenosis may be present with intracranial atherosclerosis. The influence of time or temporal features may be quite distinct, as the pace of intra- cranial atherosclerosis may allow for more consider- able collateral compensation (Fig. 23). Collateral flow should theoretically be inconsequential or nonexistent if the stenosis is not hemodynamically significant, exceeding luminal stenoses beyond 60% to 70%. Nevertheless, anecdotal descriptions relate collateral findings with even mild to moderate stenoses. The question remains whether such stenoses are actually hemodynamically significant because of factors beyond luminal stenosis. Collaterals with intracranial occlusive disease may be far more complex than in extracranial disease, as both lepto- meningeal and Willisian routes are commonly uti- lized. If one segregates focal intracranial lesions by potential collateral routes, a different balance may exist between leptomeningeal and Willisian collateral influences. For instance, leptomeningeal collaterals may be pivotal in MCA stenosis, whereas Willisian routes may provide retrograde flow distal to a basilar stenosis. These differences underscore the unique aspects of intracranial collaterals in atherosclerotic disease. Despite these potentially important aspects of collateral flow with intracranial atherosclerosis, the

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Routes and Anastomoses in Interventional Neuroradiology 71 Figure 22 Aortagram during placement and titration of

Figure 22 Aortagram during placement and titration of balloons on the NeuroFlo device for potential collateral augmentation in acute stroke.

for potential collateral augmentation in acute stroke. Figure 23 Frontal projection of an angiogram showing retro-

Figure 23 Frontal projection of an angiogram showing retro- grade collateral flow in severe atherosclerotic stenosis of the left MCA. Abbreviation : MCA, middle cerebral artery.

subject remains unexplored except for sporadic case series or isolated reports that skirt the topic. Several reasons for this lapse may exist. Intracranial athero- sclerosis has only recently been studied in a system- atic fashion in the Warfarin Aspirin Symptomatic Intracranial Disease (WASID) trial (34). The study was stopped prematurely on the basis of the futility of detecting a significant difference in treatment between warfarin and aspirin. A parallel investigation of noninvasive imaging correlates, the Stroke Out- comes and Neuroimaging of Intracranial Atheroscle- rosis (SONIA) study, demonstrated the relatively marginal performance of MRA and TCD for detection of angiographic stenoses in a multicenter setting (35). Willisian collaterals may be readily detected with such noninvasive techniques, yet leptomeningeal collater- als may require conventional angiography (Fig. 24). As a result, many clinicians have deliberated the role of imaging versus angiography and potential treat- ments for intracranial atherosclerosis. Only very recently has the potential impact of intracranial angio- plasty and stenting revived the consideration of conventional angiography and concomitant character- ization of collaterals. Future studies will likely need to heed the impact of collaterals on stroke risk and stenting for a given stenosis. Such analyses of collat- erals may reveal differences in the role of intracranial collaterals at various stages of disease. Specific collat- eral patterns, such as distal flow reversal in the basilar

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72 Liebeskind Figure 24 Frontal projection of a left ICA injection on angiography of concomitant ACA

Figure 24 Frontal projection of a left ICA injection on angiography of concomitant ACA and distal MCA stenoses ( arrows ), where ( A) represents early and (B ) later phases of angiogram. Abbreviations : ICA, internal carotid occlusion; ACA, anterior cerebral artery; MCA, middle cerebral artery.

ACA, anterior cerebral artery; MCA, middle cerebral artery. Figure 25 Angiography demonstrating retrograde leptomenin-

Figure 25 Angiography demonstrating retrograde leptomenin- geal filling of the MCA beyond a proximal stenosis. Abbreviation :

MCA, middle cerebral artery.

or leptomeningeal recruitment with MCA stenosis (Fig. 25), may be predicted on the basis of luminal stenosis or provide critical clinical information related to stroke risk. Similarly, the presence of beneficial

collateral flow may also be used in the future to decide when stenting is not indicated despite severe stenoses.

Moyamoya

Moyamoya is the quintessential model of collateral circulation in the brain. The term has been used to describe a severe multifocal steno-occlusive intracra- nial arterial disease that most frequently affects young women of Asian descent. Moyamoya syndrome refers to a similar pattern of predominantly proximal ante- rior circulation occlusive lesions and exuberant collat- eral formation that occurs in other cohorts or settings (Fig. 26) (36,37). Although much debate has focused on distinguishing this syndrome from the disease, the late-stage pathophysiology relating to collateral flow is same (37). The demographic and clinical features of moyamoya cases in the United States may be strik- ingly different than classic Asian descriptions (38). As an example, a moyamoya pattern may be seen in older patients with severe atherosclerotic disease because of numerous vascular risk factors. Imaging definitions have been used to describe a moyamoya pattern. Specific MRI criteria have arisen from conventional angiographic stages, delineating patterns that corre- late with disease progression. Unfortunately, many aspects continue to fuel debate. When unilateral or subtle findings are noted, many question the diagno- sis of moyamoya. Others resist usage of the term when the pathognomonic fine network of lenticulostriate collaterals is inapparent. Irrespective of the diverse range of conditions that has been reported in associ- ation with moyamoya, particular features are univer- sal, including initial diversion of flow through

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Routes and Anastomoses in Interventional Neuroradiology 73 Figure 26 TOF MRA illustrating multifocal anterior

Figure 26 TOF MRA illustrating multifocal anterior circulation occlusions in moyamoya syndrome. Abbreviation : TOF MRA, time-of-flight magnetic resonance angiography.

Willisian collateral routes and crucial recruitment of leptomeningeal collaterals to supply the vascular ter- ritory distal to the steno-occlusive lesions. Abnormal hemodynamics or particular flow patterns may pre- dispose to the development of stenotic lesions, and at later stages, further flow disturbances may lead to aneurysm formation. Moyamoya patterns have been described with various concomitant neurovascular lesions, including atypical aneurysms, vascular anomalies, and arteriovenous malformations (39,40). The clinical features of moyamoya syndrome have remained obscure, as these patients often present with diverse demographic backgrounds and various comorbidities and often have minimal clinical symp- toms due to well-developed leptomeningeal collater- als. Patients may present with migrainous headaches due to leptomeningeal dilatation, seizures, or TIAs. Sensory TIAs may be ascribed to migrainous events, yet these brief ischemic episodes may result from transient failure of parietal collaterals. After recover- ing from such brief symptoms, there is often little impetus to pursue further diagnostic studies. How- ever, devastating strokes, including hemorrhages, may occur. Imaging features, such as the ivy sign (Fig. 27), may be subtle, and vascular disease may go unsuspected unless a dedicated angiographic (non- invasive or conventional ) study is acquired (41). Because of such poor recognition of this disorder and the reliance on conventional angiography, angiog- raphers such as interventional neuroradiologists often encounter these patients. Although angiographic descriptions have often focused on the steno-occlusive lesions, angiography of collateral patterns is often dramatic and may be helpful in characterization of

is often dramatic and may be helpful in characterization of Figure 27 FLAIR depiction of the

Figure 27 FLAIR depiction of the ivy sign in moyamoya, demonstrating subtle hyperintensities of the subarachnoid space (arrows ). Abbreviation : FLAIR, Fluid-attenuated inversion recovery.

the disorder. Aside from the fine, lenticulostriate collaterals that bypass segmental occlusions of the MCA or the ACA, the PCA is often markedly enlarged or prominent, with vigorous leptomeningeal collater- als that supply the cerebral convexities. Progressive enlargement of the PCoA after proximal PCA stenosis follows obliteration of normal antegrade blood flow routes in the anterior circulation (17). Deep transcere- bral collaterals may be evident as medullary streaks on MRI (42,43). At later stages of the disorder, enlarge- ment of collaterals between the anterior and posterior choroidal arteries may herald intracerebral hemor- rhage (44). The lack of prospective studies of moyamoya, especially within the United States, has lead to a clinical quagmire where little knowledge has been garnered regarding treatment of patients with moya- moya. In general, once an imaging study or conven- tional angiography confi rms the diagnosis, most patients are referred to select vascular neurosurgeons for potential bypass or synangiosis (45). Medical treat- ment of moyamoya remains uncharted. The specific extent of collateral formation or perfusion derange- ments on noninvasive studies is rarely used to select candidates for intervention (46). Delineation of an exhausted oxygen extraction fraction on PET may be useful in guiding future standardized approaches (47). Intracranial angioplasty and stent placement has only rarely been described, perhaps because of the fear of

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dissection or perforation of the stenotic artery with presumed inflammatory infiltrates. The decision to proceed with EC-IC bypass or synangiosis may be influenced by angiographic features. Following revas- cularization of such cases, these patients may have limited clinical follow-up by neurologists, but neuro- radiologists may serially monitor them with multi- modal CT, MRI, or conventional angiography. Following revascularization, clinical symptoms of this progressive disorder may abate because of ade- quate collateral augmentation (48,49). Interestingly, focal revascularization also appears to improve global perfusion because of easing of demand on various collateral channels (50). Future studies may focus on moyamoya to model collateral flow in acute stroke or to further characterize the pathophysiology of collat- eral failure.

Extracranial Arterial Stenosis or Occlusion

Prominent pressure differentials exerted at the circle of Willis and resultant shifts in blood flow may occur with stenosis or occlusion of the extracranial carotid or vertebral arteries. Although alternative EC-IC routes of blood flow diversion are frequently noted, these changes are accompanied by shifts in blood flow in various Willisian segments. Unilateral carotid occlu- sion or even vertebral occlusion with a contralateral hypoplastic vertebral artery may elicit such changes.

Willisian segments are able to rapidly shunt flow to the potentially ischemic region or hemisphere. Sten- oses must exceed 60% to 70% before hemodynamic implications are evident, yet severe stenoses or occlu- sions are necessary to cause flow redistribution at the circle of Willis. Moderate stenoses of the extracranial ICA, for instance, may not be hemodynamically sig- nificant, but embolic risk may be high. As Willisian collaterals respond only during considerable intralu- minal pressure shifts, even severe, ulcerated carotid plaques may not elicit Willisian changes unless hemo- dynamically significant. Rapid downstream pressure changes due to plaque rupture and sudden carotid occlusion may not be adequately predicted on the basis of Willisian flow patterns unless the culprit lesion is hemodynamically significant at the baseline. More subtle changes may be evident with progressive stenoses, allowing Willisian segments such as the PCoA to grow with time (Fig. 28). The end-diastolic velocity of the CCA on duplex ultrasonography of carotid stenoses may be able to determine the hemo- dynamic significance of such lesions as correlated with Willisian collateral patterns (51). Once flow is restored, these changes may be readily reversed. For instance, rapid changes in collateral flow and cerebral blood flow distribution may occur after endovascular or surgical revascularization of extracranial stenoses (52,53). Carotid revascularization of stenosis contrala- teral to an occluded carotid may also improve ACoA flow to the contralateral hemisphere (54).

also improve ACoA flow to the contralateral hemisphere (54). Figure 28 Willisian collateralization ( A ,

Figure 28 Willisian collateralization (A , B) of the PCoA chronicled with TOF MRA. Abbreviations: PCoA, posterior communicating artery; TOF MRA, time-of-flight magnetic resonance angiography.

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A multitude of reports have described extensive extracranial occlusive disease with good clinical out- comes. Alternatively, in cases with rapid ICA occlu- sion due to thromboembolic disease, failure of Willisian segments to compensate for reduced blood flow may lead to devastating strokes. Time appears to be a critical factor—if stenoses or occlusions develop over a long period of time, almost any degree of occlusive disease may be tolerated (55). Even bilateral common carotid occlusion may be sustained with a good clinical course (40). The configuration of Willisian segments and metabolic demand of downstream terri- tories may determine the size, severity, and pattern of cerebral infarction (Fig. 29) (56,57). Presence of oph- thalmic flow reversal and leptomeningeal recruitment may signify relative insufficiency of Willisian segments (58). The specific Willisian segments may also differ- entially affect the pattern of cerebral ischemia. ACoA flow may determine the size and occurrence of border- zone infarction, whereas PCoA flow may be inconse- quential (57,59). Almost every diagnostic modality employed in prior reports has demonstrated that collateral compensation and downstream blood flow requirements may play a critical role in delineat- ing asymptomatic and symptomatic carotid occlu- sions (60). Prediction of recurrent stroke risk with symp- tomatic carotid occlusion has yielded conflicting results. Some have reported high-residual flow rates in other arterial segments and suggested that promi- nent collateralization via PCoA flow may identify patients at high risk for recurrent ischemia (61).

identify patients at high risk for recurrent ischemia (61). Figure 29 FLAIR demonstration of a relatively

Figure 29 FLAIR demonstration of a relatively small infarct in left ICA occlusion due to dissection and adequate collateral capacity. Abbreviations : FLAIR, Fluid-attenuated inversion recov- ery; ICA, internal carotid artery.

Improved oxygen extraction has been associated with increased collateral flow after carotid occlusion (62). However, after symptomatic carotid occlusion, recurrent stroke may not be offset by improved col- lateral flow alone (63). The size of the baseline lesion and subsequent demand likely influences the need for collateral blood flow via the circle of Willis. Differ- ences in technique and patient characteristics have likely influenced the results of numerous studies attempting to conclusively delineate the nature of this relationship (54,62,64). Angiographic definition of collateral flow patterns, including Willisian diver- sion, pial supply, and delayed venous opacification, may provide important information regarding ische- mic risk after symptomatic carotid occlusion. Brief angiographic evaluation of Willisian segments alone may not accurately predict misery perfusion on PET (64). As much controversy persists regarding the role of EC-IC bypass surgery, detailed evaluation of angio- graphic, hemodynamic, an d metabolic status with PET (Fig. 30) is currently being used to identify candidates for revascularization in the Carotid Occlu- sion Surgery Study (COSS) (65,66). It has also been suggested that the etiology of proximal ICA occlusion may influence outcome. ICA occlusion due to dissection may produce larger infarcts compared with progressive atherosclerotic disease due to the relative insufficiency of collaterals with rapid occlusion following dissection (67). The extent of Willisian collaterals after an occlusion due to dissection may also influence the likelihood for spon- taneous recanalization, as robust collaterals may hin- der reestablishment of patency in the proximal dissected segment. Various imaging techniques and provocative maneuvers have been used to assess not just stroke risk, but the need for shunting or other periprocedural interventions for carotid revascularization (25,68,69). The absence of ACoA or PCoA flow on angiography has been used to predict the need for shunting during carotid revascularization (70). Phase-contrast MRA, because of its ability to reflect not just the presence of flow but also direction, may be useful to predict changes that may occur with temporary carotid occlu- sion (71). Prediction of ischemia and the need for shunting may ideally be defined on the basis of non- invasive studies prior to revascularization.

Cerebral Venous Thrombosis

CVT is relatively uncommon, yet it is often considered the prototypical venous disorder. The cerebral venules and draining sinuses account for more than 60% to 80% of CBV; however, much of the complex physiology in the cerebral venous system remains unexplored. The diverse nature of CVT-associated predisposing condi- tions or prothrombotic states has attracted much atten- tion. In fact, most of the literature on CVT focuses on the thrombotic aspects, without considering venous flow patterns (Fig. 31). Several neurovascular lesions such as arteriovenous malformations or fistulas may have complex angioarchitecture that promote venous thrombosis, but venous collaterals are otherwise rarely

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76 Liebeskind Figure 30 Oxygen-15 PET data showing increased oxygen extraction fraction in the right hemisphere

Figure 30 Oxygen-15 PET data showing increased oxygen extraction fraction in the right hemisphere of a patient with carotid occlusion. Abbreviation : PET, positron emission tomography.

Abbreviation : PET, positron emission tomography. Figure 31 MRV illustration of prominent collateralization

Figure 31 MRV illustration of prominent collateralization in extensive CVT. Abbreviations : MRV, magnetic resonance veno- graphy; CVT, cerebral venous thrombosis.

considered. The remarkable distensibility and ability to compensate for pressure differentials within the cere- bral venous system have implications for every aspect of CVT from diagnosis to treatment. Thrombosis of a venous sinus or draining vein is offset by diversion of flow into neighboring channels. Unless considerable stasis ensues, the thrombus will remain isolated to the occluded segment until endog- enous thrombolytic mechanisms allow for recanaliza- tion. Venous pressure may rise in adjacent areas, but this rise is generally well tolerated. Areas of the brain with relative venous insufficiency may be prone to venous hypertension, with subsequent vasogenic edema, hemorrhage, and ultimately ischemia. Venous hypertensive hemorrhage is more common in areas with relatively poor venous collaterals even with small amounts of clot, whereas extensive thrombosis of several major dural sinuses may be inconsequential. Because of extreme variability in venous collateral networks, venous hemorrhage may be difficult to recognize on the basis of location alone, as the prin- cipal venous territories are often vague (8,72). Hem- orrhage confined to the deep territory of the vein of Labbe´ (Fig. 32) may be one of the few exceptions. The relative dominance of right- versus left-sided drainage of the superficial and deep venous territories

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Routes and Anastomoses in Interventional Neuroradiology 77 Figure 32 Intracerebral hemorrhage due to occlusion of the

Figure 32 Intracerebral hemorrhage due to occlusion of the left

vein of Labb .

influences venous hypertension and lesion location (8,72,73). The medullary or transcerebral veins may also divert flow in either direction between the super- ficial and deep systems. The clinical presentation and subsequent course of CVT is completely determined by collaterals (74). In fact, many CVT cases have been estimated to go undiagnosed likely because of considerable compen- sation by venous collaterals. Even though isolated cortical vein thrombosis may cause neurological def- icits in some individuals, the pursuit of this diagnosis is often tempered because it is generally considered a benign disorder due to collateral outflow. When patients present with CVT, headache, seizures, and focal neurological deficits may be noted. Sensory complaints, transient in many cases, may occur because of venous congestion of parietal regions with transverse or sigmoid sinus involvement. Some patients may describe ear fullness, bruits, or other auditory complaints associated with shunting of venous flow (Fig. 33). Dependent head positioning may elicit dramatic increases in symptoms or jugular venous distention. On occasion, a patient may present with an intracerebral hemorrhage of unclear etiology until venous thrombosis or prominent venous collat- eralization is noted. This broad spectrum of clinical manifestations and imaging presentation with hemorrhage has caused much confusion. Imaging correlates are extremely variable and best defined with MRI. Any angiographic technique (CTV, MRV, or conventional

MRI. Any angiographic technique (CTV, MRV, or conventional Figure 33 Prominent venous collaterals on CTV causing

Figure 33 Prominent venous collaterals on CTV causing audi- tory phenomena in CVT. Abbreviations : CTV, computed tomo- graphic venography; CVT, cerebral venous thrombosis.

angiography) can illustrate thrombotic occlusion and some degree of venous collateralization. MRI offers particular advantages, including demonstration of isolated cortical vein thromboses, prominence or dis- tention of medullary veins, and silent edema or dra- matic parenchymal lesions including hemorrhage that may easily resolve over time (56,75,76). MRI may also show mastoid fluid collection due to venous conges- tion and attempted outflow via collaterals (Fig. 34). Angiography has assumed a minimal role in diagnosis of CVT and is increasingly reserved for rescue treat- ment when patients deteriorate. Angiography may depict extensive venous col- laterals in cases of dural sinus thrombosis. Following thrombolysis or thrombectomy, such venous collater- als may resolve, but the time course may be protracted if thrombus is retained or stasis continues. Such resid- ual venous collaterals may persist indefinitely, caus- ing other clinical symptoms. Residual symptoms such as tinnitus or nystagmus may be partially due to collaterals. These seemingly detrimental manifesta- tions of distended venous collaterals offset the poten- tially high mortality rate of an otherwise relatively benign disorder.

Dural Arteriovenous Shunts