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The Ischemic
Penumbra
NEUROLOGICAL DISEASE AND THERAPY

Advisory Board

Gordon H. Baltuch, M.D., Ph.D.

Department of Neurosurgery
University of Pennsylvania
Philadelphia, Pennsylvania, U.S.A.

Cheryl Bushnell, M.D., M.H.S.

Duke Center for Cerebrovascular Disease
Department of Medicine, Division of Neurology
Duke University Medical Center
Durham, North Carolina, U.S.A.

Louis R. Caplan, M.D.

Professor of Neurology
Harvard University School of Medicine
Beth Israel Deaconess Medical Center
Boston, Massachusetts, U.S.A.

Mark A. Stacy, M.D.

Movement Disorders Center
Duke University Medical Center
Durham, North Carolina, U.S.A.

Mark H. Tuszynski, M.D., Ph.D.

Professor of Neurosciences
Director, Center for Neural Repair
University of California—San Diego
La Jolla, California, U.S.A.

Ajay K. Wakhloo, M.D., Ph.D.

Department of Radiology
University of Massachusetts Medical School
Worcester, Massachusetts, U.S.A.
 1. Handbook of Parkinson’s Disease, edited by William C. Koller
2. Medical Therapy of Acute Stroke, edited by Mark Fisher
3. Familial Alzheimer’s Disease: Molecular Genetics and Clinical Perspectives,
edited by Gary D. Miner, Ralph W. Richter, John P. Blass, Jimmie L. Valentine, and
Linda A. Winters-Miner
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Jeffrey L. Cummings and Bruce L. Miller
5. Therapy of Parkinson’s Disease, edited by William C. Koller and George Paulson
6. Handbook of Sleep Disorders, edited by Michael J. Thorpy
7. Epilepsy and Sudden Death, edited by Claire M. Lathers and Paul L. Schraeder
8. Handbook of Multiple Sclerosis, edited by Stuart D. Cook
9. Memory Disorders: Research and Clinical Practice, edited byTakehiko Yanagihara
and Ronald C. Petersen
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11. Cognitive Disorders: Pathophysiology and Treatment, edited by Leon J. Thal,
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12. Handbook of Amyotrophic Lateral Sclerosis, edited by Richard Alan Smith
13. Handbook of Parkinson’s Disease: Second Edition, Revised and Expanded,
edited by William C. Koller
14. Handbook of Pediatric Epilepsy, edited by Jerome V. Murphy and Fereydoun
Dehkharghani
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edited by Roger Kurlan
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17. Handbook of Cerebrovascular Diseases, edited by Harold P. Adams, Jr.
18. Parkinsonian Syndromes, edited by Matthew B. Stern and William C. Koller
19. Handbook of Head and Spine Trauma, edited by Jonathan Greenberg
20. Brain Tumors: A Comprehensive Text, edited by Robert A. Morantz and
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Lieberman, C. Warren Olanow, Moussa B. H. Youdim, and Keith Tipton
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23. Handbook of Myasthenia Gravis and Myasthenic Syndromes,
edited by Robert P. Lisak
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25. Therapy with Botulinum Toxin, edited by Joseph Jankovic and Mark Hallett
26. Principles of Neurotoxicology, edited by Louis W. Chang
27. Handbook of Neurovirology, edited by Robert R. McKendall and William G. Stroop
28. Handbook of Neuro-Urology, edited by David N. Rushton
29. Handbook of Neuroepidemiology, edited by Philip B. Gorelick and Milton Alter
30. Handbook of Tremor Disorders, edited by Leslie J. Findley and William C. Koller
31. Neuro-Ophthalmological Disorders: Diagnostic Work-Up and Management,
edited by Ronald J. Tusa and Steven A. Newman
32. Handbook of Olfaction and Gustation, edited by Richard L. Doty
33. Handbook of Neurological Speech and Language Disorders,
edited by Howard S. Kirshner
34. Therapy of Parkinson’s Disease: Second Edition, Revised and Expanded,
edited by William C. Koller and George Paulson
35. Evaluation and Management of Gait Disorders, edited by Barney S. Spivack
36. Handbook of Neurotoxicology, edited by Louis W. Chang and Robert S. Dyer
37. Neurological Complications of Cancer, edited by Ronald G. Wiley
38. Handbook of Autonomic Nervous System Dysfunction, edited by Amos D. Korczyn
39. Handbook of Dystonia, edited by Joseph King Ching Tsui and Donald B. Calne
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and J. William Langston
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43. Handbook of Multiple Sclerosis: Second Edition, Revised and Expanded,
edited by Stuart D. Cook
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David G. Piepgras, and John L. D. Atkinson
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47. Spinal Cord Diseases: Diagnosis and Treatment, edited by Gordon L. Engler,
Jonathan Cole, and W. Louis Merton
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49. Sleep Disorders and Neurological Disease, edited by Antonio Culebras
50. Handbook of Ataxia Disorders, edited by Thomas Klockgether
51. The Autonomic Nervous System in Health and Disease, David S. Goldstein
52. Axonal Regeneration in the Central Nervous System, edited by Nicholas A. Ingoglia
and Marion Murray
53. Handbook of Multiple Sclerosis: Third Edition, edited by Stuart D. Cook
54. Long-Term Effects of Stroke, edited by Julien Bogousslavsky
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edited by C. Liana Bolis, Julio Licinio, and Stefano Govoni
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Clinical Implication, Second Edition, edited by Anita Sidhu, Marc Laruelle,
and Philippe Vernier
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edited by Richard L. Doty
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59. Handbook of Parkinson’s Disease: Third Edition, edited by Rajesh Pahwa,
Kelly E. Lyons, and William C. Koller
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61. Neuromuscular Junction Disorders: Diagnosis and Treatment,
Matthew N. Meriggioli, James F. Howard, Jr., and C. Michel Harper
62. Drug-Induced Movement Disorders, edited by Kapil D. Sethi
63. Therapy of Parkinson’s Disease: Third Edition, Revised and Expanded,
edited by Rajesh Pahwa, Kelly E. Lyons, and William C. Koller
64. Epilepsy: Scientific Foundations of Clinical Practice, edited by Jong M. Rho,
Raman Sankar, and José E. Cavazos
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Second Edition, edited by Roger Kurlan
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edited by Harold P. Adams, Jr.
67. Emerging Neurological Infections, edited by Christopher Power and
Richard T. Johnson
68. Treatment of Pediatric Neurologic Disorders, edited by Harvey S. Singer,
Eric H. Kossoff, Adam L. Hartman, and Thomas O. Crawford
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edited by Michel Baudry, Xiaoning Bi, and Steven S. Schreiber
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edited by Kelly E. Lyons and Rajesh Pahwa
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A. Gordon Smith
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Chaturvedi and Peter M. Rothwell
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and Matthew B. Stern
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Daniel L. Silbergeld
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and Paul H. Gordon
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edited by Jeffrey S. Chamberlain and Thomas A. Rando
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92. Handbook of Parkinson’s Disease, Fourth Edition, edited by Rajesh Pahwa and
Kelly E. Lyons
93. The Ischemic Penumbra, edited by Geoffrey A. Donnan, Jean-Claude Baron,
Stephen M. Davis, and Frank R. Sharp
 The Ischemic
Penumbra
Pathophysiology, Imaging
and Therapy

Edited By
Geoffrey A. Donnan
National Stroke Research Institute, Austin Health
University of Melbourne, Victoria, Australia

Jean-Claude Baron
Addenbrooke’s Hospital and University of Cambridge, UK

Stephen M. Davis
Royal Melbourne Hospital and University of Melbourne, Victoria, Australia

Frank R. Sharp
University of California, Davis, USA
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Library of Congress Cataloging‑in‑Publication Data

The ischemic penumbra / [edited by] Geoffrey A. Donnan ... [et al.].
p. ; cm. ‑‑ (Neurological disease and therapy ; v. 93)
Includes bibliographical references and index.
ISBN‑13: 978‑0‑8493‑3990‑5 (hb : alk. paper)
ISBN‑10: 0‑8493‑3990‑1 (hb : alk. paper)
1. Cerebral ischemia‑‑Pathophysiology. 2. Cerebrovascular disease. I. Donnan, G. A. (Geoffrey A.)
II. Series.
[DNLM: 1. Cerebrovascular Accident‑‑diagnosis. 2. Cerebrovascular Accident‑‑therapy. 3.
Diagnostic Imaging‑‑methods. W1 NE33LD v.93 2007 / WL 355 I7675 2007]

RC388.5.I825 2007
616.8’106‑‑dc22 2007000619

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This book is dedicated to our parents,
who made it all possible.
 Foreword

Time is brain–penumbra is brain–brain is life.

The ischemic penumbra is an enigma and is the key to stroke pathophysiology and treatment.
The term is used exhaustively and has become the major rationale for the early delivery of
stroke care. Knowledge about the penumbra, its variability, and its ever-changing extension
and individuality has dramatically changed stroke treatment. Paradoxically, it is still poorly
understood. Animal experiments contributed to the early concepts and allowed investigators to
establish blood flow thresholds. Information gained from these studies and those with multi-
tracer positron emission tomography defining the penumbra in humans for the first time have
been in existence for more than 20 years; it was the translation into the management of stroke
and the design of clinical trials that took longer than expected. The ultra-early treatment con-
cept of the early intravenous tissue plasminogen activator studies, specifically the National
Institute of Neurological Disorders and Stroke trial, opened the eyes of most stroke physicians.
Finally, it became clear that time was the most important variable in stroke treatment and that
this translated into the presence of penumbral tissue. Hence, the “time is brain” concept arose.
The next logical step was to look for mechanisms and tools that would allow the replace-
ment of a time-based therapy by a pathophysiologically based treatment window. It led to the
introduction of perfusion–diffusion mismatch magnetic resonance imaging and computer-
ized tomography angiography–computed tomography perfusion. These techniques offered
information about pathophysiological variables that would correspond to penumbral tissue,
never forgetting that it always would be just a snapshot of something penumbra-like at the
time of assessment.
This volume, edited by eminent scientists and clinicians who are experts in the field of
stroke pathophysiology and treatment, together with contributions by a prestigious list of
scientists involved in penumbral research, provides the first comprehensive book on one of the
most important concepts in acute stroke research and management. There is a comprehensive
review of the history, background, pathophysiology, and application of the penumbra, from con-
cept to stroke management. There is no doubt that the reader of this volume will gain a deeper
understanding of the penumbra, given that there is a consolidation of about half a century of
research that finally led to the first approved treatment of acute ischemic stroke. The book will
be judged a success if, as it will undoubtedly do, it stimulates readers to explore the penumbra
further and advance knowledge in the area. The most important outcome is recanalization and
reperfusion or, better, saving penumbral tissues and saving brain.

Werner Hacke, MD, PhD

Department of Neurology
University of Heidelberg
Heidelberg, Germany
 Preface

In the world of acute ischemic stroke, nothing is more important than an understanding of the
ischemic penumbra. The whole concept of the existence of salvageable tissue, that is, the penum-
bra, is based on the daily clinical observation of almost immediate and early recovery from an
episode of hemiparesis or other clinical expression of occlusion of a blood vessel within any
of the arterial territories of the brain. Indeed, even before there was an appreciation of the
complexities of the ischemic cascade, many clinicians dealing with stroke understood that
something akin to the ischemic penumbra was likely to exist. These ideas, which fueled pivotal
experimental studies to document the penumbra, clashed with the then prevailing dogma that
the ischemic brain was doomed to die within minutes of onset of the clinical event. It is because
of this central positioning of the penumbra in stroke outcome and therapy that we felt that a
volume dedicated to its existence was timely.
The editors are all clinical scientists working in the field of stroke, but coming from
different perspectives. In particular, we have backgrounds in imaging and therapies for stroke,
as well as its pathophysiology and neurochemistry. Hence, we have tried to draw together an
overview of the ischemic penumbra viewed predominantly from the clinical perspective, but
providing the reader with a solid component of the more basic experimental and neurochemi-
cal aspects. Also, we are of an opinion that this should also be put in historical context. Here we
have been particularly fortunate in having an enthusiastic contribution from Professor Lindsay
Symon, who had such a pivotal role in defining the ischemic penumbra during the 1970s by
means of a series of rigorous animal experiments. We have also included chapters that summa-
rize aspects of the penumbra in a way that has not been done before, such as providing an overall
view of species differences in thresholds for the penumbra and its duration. The duration of the
penumbra is particularly relevant if we are to extend the time window for treatment so more
patients can benefit from modern therapies.
In bringing together ideas about the definition, criteria, and the various penumbral imag-
ing modalities now available, one message becomes quite clear. Although already clearly useful
in the clinical setting, the concept of the ischemic penumbra is still evolving as there is still no
entirely satisfactory definition, and the operational criteria for its existence need refining.
Perhaps even more obviously, there is no ideal imaging technique to confirm its presence. Each
of the penumbral imaging techniques described in this volume have their advantages and
disadvantages, and none really directly and precisely images the penumbra as originally
defined. One conclusion that can be drawn from this is that the penumbra is still a fertile area
of research with many new discoveries of importance still to be made.
Hence, we hope that this volume is a useful resource for clinicians, researchers, and students
alike who have an interest in the ischemic penumbra. While we have attempted to include a
broad range of elements of the penumbra together, there are, of course, always areas that could
have been strengthened and others that may have been overemphasized. As the first major
attempt to paint a scientific picture of the penumbra on one canvas, we hope that this has been
a reasonable start. If the benefit achieved is to enhance penumbral research even to a small
extent, we will have realized our aim of helping those who, unfortunately, have been the victims
of stroke.

Geoffrey A. Donnan
Jean-Claude Baron
Stephen M. Davis
Frank R. Sharp
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