Magnetic Resonance Imaging in Ischemic Stroke, 1st Edition

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Contents VII

Foreword

When MR imaging was added to the noninvasive diagnostic tools of radiology some 20 years
ago, CT did not immediately lose its significance as the method for obtaining structural
information on the brain in stroke. In fact, although MR imaging was soon found to have
superior contrast resolution and to be essentially free of artifacts below the tentorium, the
first large-scale treatment studies of acute stroke – in some of which Rüdiger von Kummer,
one of the editors of this book, played a major role – were based on CT not MR. This was
largely because CT had already reached an advanced technical stage, while MR imaging
was more or less still in its infancy. With further improvement in hardware and software,
including the advent of clinical imagers with higher field strengths, MR imaging did gain
in importance, but its breakthrough in stroke imaging came only with the development of
functional methods that allowed the study of cerebral pathophysiology, including perfusion.
At the same time the technical evolution continued of several other non-structural MR meth-
ods considered in various ways useful in stroke: MR angiography, MR spectroscopy and
functional (BOLD) MR imaging. All of these methods were soon studied by researchers from
many countries as to their value for understanding, diagnosing, treating, and possibly pre-
venting stroke. One method in particular, diffusion-weighted MR imaging, became rapidly
accepted by (neuro)radiologists and neurologists alike, as it was soon recognized as being
highly sensitive in visualizing even tiny areas of severe ischemia almost immediately after
the offending event. Since then, the interest in fathoming the potential of functional MR
(imaging) methods in ischemic stroke in particular and in neurovascular diseases in general
has not waned.
Now, why this book? Because! Because it is not just a(nother) book on MR imaging in
stroke but a lucid as well as comprehensive treatise on a complicated topic that succeeds in
correlating major aspects of stroke – pathophysiology, clinical syndromes, structural and
functional diagnostic MR findings, treatment and monitoring of therapeutic effects. Both
editors have a long history of active, enthusiastic involvement in laboratory as well as clinical
research on stroke; both are neurologists by training, with many years of clinical experience;
and both have had additional training in neuroradiology, the field that one of them eventu-
ally chose for good.
The idea of “a book on stroke” was conceived at Heidelberg many years back. Fortunately,
this idea never led to anything: had the book been written then, it would have been obsolete
at the time of publication. The present book, which contains all the dramatic advances in
MR stroke imaging that have occurred in recent years plus pertinent information on spinal
stroke, is not likely to have this fate. Rather, it will soon be found on many desks and book-
shelves, because clinicians and scientists interested in stroke will quickly recognize its emi-
nent qualities: well designed, well written, and highly instructive.
Rüdiger von Kummer and Tobias Back, together with their 23 expert co-authors, have
done a marvelous job in creating a timely book on stroke of great substance.

Heidelberg Klaus Sartor

Contents IX

Preface

It is a part of the adventure of science

to try to find a limitation in all directions
and to stretch the human imagination
as far as possible everywhere.
Richard P. Feynman

Cerebrovascular diseases have an enormous and increasing impact on societies: they rank
among the leading causes of death, are often associated with chronic handicap, and cause
high costs for primary treatment, rehabilitation and chronic care. The advent of treatment
options such as reperfusion therapies and, to a lesser degree, neuroprotective strategies on
the one hand, and growing means to enhance rehabilitation and functional plasticity on the
other hand, urges physicians to diagnose stroke subtypes as early and precisely as possible.
The localization, extent and pathology of lesions should be recognized and followed up by
imaging methods in order to develop and direct therapeutic approaches, detect complica-
tions, and start prevention.
Modern MR imaging and spectroscopy has provided new insights into the pathophysi-
ology of stroke and offers a wide range of available technologies that have not by far been
explored to their limits. Animal experiments have contributed considerably to our current
understanding of the underlying mechanisms of cerebral ischemia. Diffusion-weighted MR
imaging provides the best sensitivity for detection of patterns of ischemic lesions in acute
stroke patients. Although it is still too early to assess the true potential of MR methods for
stroke, nevertheless an attempt has to be made to demonstrate the diagnostic and scientific
capabilities of MR imaging in ischemic stroke and related disorders. This is the purpose of
our book.
When starting this project, it became clear that close correlations should be drawn
between pathology, clinical picture and imaging findings. This book competes with a variety
of publications, but differs from all of them in that it brings together what modern medical
teaching offers to students: a comprehensive presentation of pathological features of cerebro-
vascular disease, an up-to-date clinical description of stroke syndromes, and the footprints
of clinically relevant stroke syndromes in MR imaging modalities. For example, the reader
who comes across a case of symptomatic carotid stenosis with ipsilateral MCA stroke can
choose to consult Chap. 15 on occlusive carotid disease, but alternatively may be interested
in reading about vascular pathology (Chap. 5) or disturbed brain perfusion (Chap. 6). Finally,
he/she may be inclined to find out more about the therapeutic impact of imaging findings
as presented in Chap. 3.
The dual concept of presenting MR imaging of stroke pathology and MR correlates of
stroke syndromes has led to the division of this volume into two parts (Parts 2 and 3), pre-
ceded by Part 1 with introductory chapters on clinically relevant syndromes and informa-
tion on the clinical and therapeutic efficacy of MR imaging. We hope that readers will find it
intriguing to use the book and will always feel free to inform us about ways to improve this
work

Dresden Rüdiger von Kummer

Mannheim Tobias Back
Contents XI

Contents

Part 1: Clinical Presentation and Impact of Imaging . . . . . . . . . . . . . . . . . . . . . . . . . . . 1

1 Stroke Syndromes
Georg Gahn . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

2 Clinical Efficacy of MR Imaging in Stroke

Rüdiger von Kummer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17

3 Therapeutic Impact of MR Imaging in Acute Stroke

Mark W. Parsons and Stephen M. Davis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23

4 Insights from Experimental Studies

Tobias Back. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41

Part 2: MR Imaging of Stroke Pathology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75

5 Vascular Anatomy and Pathology

Dirk Petersen and Stephan Gottschalk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77

6 Disturbed Brain Perfusion

Sabine Heiland . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103

7 Disturbed Proton Diffusion

Tobias Neumann-Haefelin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117

8 Ischemic Edema and Necrosis

Susanne Wegener, Mathias Hoehn, and Tobias Back. . . . . . . . . . . . . . . . . . . . . . 133

9 MR Imaging of White Matter Changes

Johanna Helenius and Turgut Tatlisumak . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 149

10 MR Detection of Intracranial Hemorrhage

Thamburaj Krishnamoorthy and Marco Fiorelli . . . . . . . . . . . . . . . . . . . . . . . . 159

11 MR Spectroscopy in Stroke
Heinrich Lanfermann and Ulrich Pilatus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171

Part 3: MR Correlates of Stroke Syndromes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183

12 Transient Ischemic Attacks

Hakan Ay and Achim Gass . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185
XII Contents

13 Microangiopathic Disease and Lacunar Stroke

Achim Gass and Hakan Ay . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193

14 Territorial and Embolic Infarcts

José M. Ferro . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 209

15 Hemodynamic Infarcts and Occlusive Carotid Disease

Kristina Szabo and Michael G. Hennerici . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 225

16 Hypoxic-Ischemic Lesions
Karl Olof Lövblad . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 239

17 Spinal Infarcts
Michael Mull and Armin Thron . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 251

18 Veno-Occlusive Disorders
Armin Thron and Michael Mull . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 269

19 Stroke Mimicking Conditions

Joachim Röther. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 285

Subject Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293

List of Contributors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303

Stroke Syndromes 1

Part 1:
Clinical Presentation and Impact of Imaging
Stroke Syndromes 3

1 Stroke Syndromes
Georg Gahn

CONTENTS tion and size of the ischemia or the hemorrhage, but

may very well be due to an intracranial mass effect, a
1.1 Introduction 3 residuum after an epileptic seizure, a migraine attack,
1.2 Mechanisms of Ischemia 3
1.2.1 Territorial Infarcts 4
or an encephalitis. Combinations of neurological defi-
1.2.1.1 Large Vessel Occlusive Disease of the Anterior cits are numerous, both in the hemispheres and in the
Circulation 4 brainstem (see as well chapter 14).
1.2.1.2 Large Vessel Occlusive Disease of the Posterior
Circulation 6
1.2.2 Lacunar Infarction 8
1.2.3 Borderzone Infarction 9
1.3 Particular Etiological Stroke Syndromes 9 1.2
1.3.1 Cardioembolic Stroke 9 Mechanisms of Ischemia
1.3.2 Dissection 10
1.3.3 Cerebral Venous Thrombosis 11 Focal cerebral ischemia differs from global isch-
1.3.4 Migraine 11
1.3.5 Coma 12
emia. In global ischemia irreversible neuronal
1.3.6 Eye Movement Abnormalities 13 damage occurs after 4–8 min at normal body tem-
1.4 Summary 13 perature (Hochachka et al. 1996). In focal cerebral
References 13 ischemia collateral vessels almost always provide
some degree of residual blood flow, which may be in-
sufficient to preserve neuronal survival (Coyle and
1.1 Heistad 1991). Location of arterial occlusion affects
Introduction the impairment of cerebral function: Obstruction
below the circle of Willis often permits collateral
The major focus of this book is the evolving new flow through the anterior or the posterior commu-
technologies that help understand the underlying nicating arteries. Vertebral artery obstruction can
pathophysiological mechanisms of cerebral ischemia. be bypassed through small deep cervical arteries
Nevertheless, the anatomically based classification which are residuals from the embryonic rete mirabi-
of stroke syndromes originally elaborated by C.M. lis in the posterior circulation. In obstructions of the
Fisher still has a huge impact on the care of stroke cervical internal carotid artery, which derives from
patients. This chapter will give the reader a short a branchial arch and not from a rete mirabilis, lim-
overview of the most important stroke syndromes in ited collateral flow can be provided through exter-
the clinical setting. “Stroke” is defined as a sudden, nal carotid artery branches such as the periorbital
non-convulsive focal neurological deficit. The terms or the ethmoidal arteries. Collateral flow mainly
apoplexy originating from the Greek “αποπλεξ´ια” derives from the arteries of the circle of Willis.
and “insult” from the Latin “insultus” describe the Additional factors influence the extent of the
same phenomenon and can be used synonymously. final infarction. The speed of obstruction may allow
The term “neurovascular syndrome” may be a better collateral arteries to develop, if it occurs gradu-
term since a stroke is not unusually a slow progressing ally (Busch et al. 2003), whereas complete sudden
process rather than a “stroke” (Kennedy and Buchan blockade of a major artery by an embolus leaves only
2004). The neurological deficit reflects both the loca- some minutes to activate sufficient collateral flow.
Hypoxia, hyperglycemia, acidosis, fever, hypoto-
G. Gahn, MD nia, and normal or abnormal variants in vascular
Department of Neurology, University of Technology Dresden, anatomy my contribute to the resulting infarction
Fetscherstrasse 74, 01307 Dresden, Germany (Hossmann 1999). Basically, the loss of oxygen and
4 G. Gahn

glucose supply results in the collapse of cellular caused by a decrease in blood flow through the oph-
energy production with subsequent changes in cel- thalmic artery, distally to a hemodynamically rel-
lular metabolism, degradation of cell membranes, evant ICA obstruction. Alternatively small emboli,
and finally necrosis. the so-called Hollenhorst plaques, may occlude reti-
The margins of the infarction are usually hyper- nal branches (Hollenhorst 1958).
emic due to activated meningeal collaterals. The Hemispheric TIAs display a variety of transient
ischemic tissue swells rapidly because of increased focal neurological deficits (Ferro 2004). Stereo-
intracellular and intercellular water content. During typed TIAs point either to a hemodynamic rather
ischemia, the arteries first dilate to increase blood than an embolic mechanism of cerebral ischemia
supply to the oligemic tissue, but will subsequently or to an imminent lacunar infarction, the so-called
constrict due to ischemic damage. Reperfusion may capsular warning syndrome (see Sect. 1.2.2). Per-
then lead to hyperemia due to impaired autoregula- manent ischemia with infarction within the MCA
tive capacity of the damaged arteries. In prolonged territory usually leads to weakness of the contralat-
ischemia sludging and endothelial damage will pre- eral limbs more pronounced in the face and the arm
vent reperfusion (Markus 2004). than in the leg (Ferro 2004). Concomitant or iso-
lated sensory symptoms are usually loss of position
and pinprick sense and stereoagnosis. Neglect of the
1.2.1 contralateral space and an attentional hemianopia
Territorial Infarcts are often prominent in larger hemispheric strokes
which are then also accompanied by conjugate eye
1.2.1.1 deviation towards the side of the brain lesion. Weak-
Large Vessel Occlusive Disease of the Anterior ness mainly affecting the leg often occurs in ante-
Circulation rior cerebral artery (ACA) territory stroke because
of the representative area of the “homunculus” at
In 1951 C. Miller Fisher described the clinical find- the vertex (Bogousslavsky and Regli 1990). Left
ings associated with occlusion of the internal carotid sided lesions are often accompanied by an aphasia
artery (ICA) (Fisher 1951). In his report he first (Kertesz 1993). Depending on the lesion location a
called attention to warning episodes preceding cere- more motor (frontal) or sensory (posterior) type of
bral ischemia and called them “transient ischemic aphasia will occur (Pedersen et al. 2004).
attack” (TIA). The major cause for occlusive disease
of the ICA is atherosclerotic narrowing at the bifur- 1.2.1.1.1
cation of the common carotid artery (CCA) extend- Middle Cerebral Artery Occlusion
ing into the external and internal carotid arteries.
Often atherosclerotic disease of the ICA is accom- In Caucasians, the vast majority of MCA occlu-
panied by atherosclerotic disease of the coronary sions are of embolic origin with emboli arising
and peripheral arteries (de Groot et al. 2004). Ath- from a carotid stenosis, the aortic arch or the heart
erosclerotic plaques gradually narrow the vascular (Heinsius et al. 1998) or from the venous side in case
lumen. Ulceration of the plaque and hemorrhage of a patent foramen ovale. In black or Asian patients
into the plaque cause clotting of thrombocytes to the a higher prevalence of intracranial occlusive disease
vessel wall and finally embolization to more distal is found with subsequent thrombotic arterial occlu-
arteries in the brain (Hennerici 2004). Progres- sion or stenosis (Feldmann et al. 1990).
sive narrowing of the arterial lumen may also cause Acute occlusion of the upper MCA trunk may
hemodynamic impairment of the cerebral territory lead to infarction in the frontal and superior pari-
supplied by the diseased artery if collateral flow etal lobes. Hemiplegia, more pronounced in the face
through the arteries of the circle of Willis is not and arm, hemisensory loss, conjugate eye deviation
sufficient. and neglect to the contralateral side of space, espe-
An important warning sign for occlusive ICA dis- cially to visual stimuli, will be the symptoms (Ferro
ease is an episode of transient monocular visual dis- 2004). Right sided lesions usually cause more severe
turbance also called “amaurosis fugax” or “ocular visual neglect than left sided lesions (Karnath et
TIA” (Wray 1993). Patients often describe this phe- al. 2002). Left sided lesions will also cause a motor
nomenon as a dimming, darkening, obscuration or a aphasia in right handed patients (Kertesz 1993).
curtain from above or from the side, which resolves Right sided lesions will also cause anosognosia more
after seconds or a few minutes. These attacks are often than left sided lesions (Beis et al. 2004).
Stroke Syndromes 5

In inferior MCA trunk occlusion infarctions of the ischemic stroke has been called “malignant” MCA
lateral surface of the temporal lobe and the inferior infarction (Fig. 1.1). The diagnosis of complete MCA
parietal lobe may occur (Olsen 1991; Ringelstein territory infarction based on clinical judgment is
et al. 1992). Motor or sensory deficits may not be unspecific and often requires neuroimaging studies
severe, but visual field deficit and sensory aphasia (Berrouschot et al. 1998).
in left sided infarctions and constructional apraxia
in right sided lesions occur (Geschwind 1975; 1.2.1.1.2
Spinazzola et al. 2003). Right temporal lesions Anterior Cerebral Artery
cause agitation and confusion resembling an organic
psychosis (Ferro 2001). The ACA supplies the head of the caudate nucleus,
Deep infarctions in the MCA territory result from the anterior part of the internal capsule, the anterior
proximal MCA occlusion with blockage or hypoper- perforated substance and the paramedian frontal
fusion of the lenticulostriate arteries causing striato- lobe above the corpus callosum through the recur-
capsular infarcts (Russmann et al. 2003). The basal rent artery of Heubner (Ghika et al. 1990). Infarc-
ganglia have poor collateral supply, but leptomenin- tion of the paramedian frontal lobe causes weakness
geal collaterals may prevent extension of infarction of foot, leg and shoulder and represents a typical
to the cortex (Ringelstein et al. 1992). Striatocap- pattern of neurological symptoms (Bogousslavsky
sular infarcts cause dense hemiplegia and less pro- and Regli 1990). Also apraxia of the left arm (“ante-
nounced sensory deficits if the posterior capsule is rior disconnection syndrome”) may be a typical
spared (Donnan et al. 1991). Left sided infarcts may sign (Geschwind 1965). Transcortical motor and
cause a temporary mutism or dysarthria (Urban sensory aphasia, urinary incontinence in bilateral
et al. 2001). Right sided lesions cause neglect to the lesions occur. Abulia is seen in both unilateral and
contralateral side (Karnath et al. 2002). bilateral frontal lobe infarctions, sometimes of fluc-
Complete occlusion of the MCA trunk with infarc- tuating intensity. The “alien hand sign” is also found
tion of the entire MCA territory is a potentially dev- in frontal lobe infarctions and may be another form
astating situation with severe paralysis, hemisensory of disconnection syndrome (Geschwind et al. 1995).
loss, attentional hemianopia, conjugate eye devia- Occasionally both ACA territories are supplied by
tion, and global aphasia in left sided lesions (Hacke only one ACA in a unilateral hypoplastic or aplastic
et al. 1996). Because of its high mortality this type of A1 segment. Infarction of both ACA territories will

Fig. 1.1. Upper row, computed tomography of a patient with malignant right middle cerebral artery infarction on day one after
onset of symptoms. Lower row, on day two massive edema with midline shift in spite of hemicraniectomy
6 G. Gahn

cause a sudden onset of abulia, paraparesis, apathy, when the emboli travel through the basilar artery
and incontinence, which may be misinterpreted as into the posterior cerebral arteries (PCA). The
sudden onset of dementia (Ferro 2001). Infarction pathophysiology of proximal VA obstruction is not
of the head of the caudate and the anterior inter- well understood, since the VA is rarely operated
nal capsule by occlusion of the Heubner artery will on and therefore specimens as in carotid endarter-
cause slight motor weakness, dysarthria, behavioral ectomy are rare (Caplan 1993). The mechanical
changes such as abulia or restlessness and hyper- situation in VA is very different form the ICA since
activity. Cognitive and behavioral changes in these it leaves the SCA at a 90° angle, whereas the ICA
patients resemble the clinical signs found in patients takes off the CCA at an almost 180° angle (Brandt
with medial thalamic lesions (Bogousslavsky et al. 2000).
1994). VA obstruction causes hemodynamic problems
in approximately one third of patients with pos-
1.2.1.1.3 terior circulation ischemia (Caplan et al. 2004).
Anterior Choroidal Artery Asymmetrical caliber of the two VAs is normal. In
the neck multiple nuchal and muscular branches
Blockade of the anterior choroidal artery may cause provide a network for potential collateral pathways,
infarction of the lateral geniculate body causing that can be activated in VA obstruction.
hemianopia with preserved central vision and a Intracranial atherosclerotic VA obstruction is
prominent sensory loss with hemiparesis (Bruno mainly located at the origin of the posterior inferior
et al. 1989). cerebellar artery (PICA) and less frequent at the site
of dura penetration. Consequently the most frequent
clinical syndrome in VA occlusive disease is the dor-
1.2.1.2 solateral medullary syndrome (“Wallenberg’s” syn-
Large Vessel Occlusive Disease of the Posterior drome) consisting of dizziness, retroorbital pain,
Circulation facial numbness, dissociated sensory deficit, weak-
ness, hoarseness, dysphagia and vomiting, nystag-
1.2.1.2.1 mus, Horner’s syndrome and failure of autonomic
Obstruction of the Subclavian Artery respiration (Vuilleumier et al. 1995).
With involvement of the cerebellar hemisphere
In severe occlusive disease of the subclavian artery supplied by the PICA, subsequent edema may cause
(SCA) blood supply of the arm is mainly provided obstruction of the 4th ventricle, hydrocephalus or
by reversed flow through the vertebral artery (VA) compression of the medulla oblongata. Clinically,
arising behind the obstruction. The so-called sub- involvement of the entire cerebellar hemisphere
clavian-steal syndrome consists of ischemic symp- can not be distinguished from partial cerebellar
toms in the arm, especially after exercise, such as infarction (Amarenco and Hauw 1990). Therefore
pain or numbness or coolness (Reivich et al. 1961). patients with neurological symptoms suggesting
Consequently a diminished or delayed pulse in the infarction within the PICA territory require neuro-
radial artery or decreased blood pressure on the imaging studies and close clinical monitoring.
side of SCA stenosis can be palpated. Rarely neuro- In blockade of the anterior spinal artery, isch-
logical symptoms such as spells of dizziness may be emia of the medial medulla may occur with contra-
brought about by exercise of the arm. Even more rare lateral hemiparesis, ipsilateral tongue weakness and
are ischemic brainstem strokes in subclavian-steal contralateral loss of posterior column sensation (Ho
syndrome (Bornstein and Norris 1986). and Meyer 1981).
Isolated cerebellar infarction without involvement
1.2.1.2.2 of the medulla is often difficult to identify, since gait
Obstruction of the Vertebral Arteries ataxia, vomiting and dizziness may not be accompa-
nied by typical brainstem symptoms (Barth et al.
The origin of the VA at the SCA is the most common 1994). Cerebellar edema may compress the medulla
location of atherosclerotic VA disease. Dizziness, and the pons leading to conjugate eye deviation to
accompanied by other brainstem symptoms, such the side opposite the lesion without contralateral
as diplopia, dysarthria, motor or sensory symp- hemiparesis. This sign is probably pathognomonic
toms, suggest embolism towards the brainstem. for severe cerebellar mass effect and requires imme-
Also hemianopia may occur due to VA embolism diate intervention.
Stroke Syndromes 7

1.2.1.2.3 the diencephalon by small perforating arteries.

Basilar Artery Obstruction Signs of dysfunction in the rostral brainstem are
a variety of pupillary abnormalities (e.g. anisoco-
Basilar artery (BA) occlusive disease is a highly life- ria, afferent pupillary deficit) (Martin et al. 1998;
threatening condition first described by Kubik and Mehler 1989). Vertical gaze palsy or skew devia-
Adams (1946). Atherosclerotic changes are mostly tion also point to the midbrain causing the “Top
located at the origin of the BA, sometimes extend- of the basilar” syndrome (Caplan 1980). Memory
ing from the VAs. Often these patients experience loss may occur in thalamic infarction as well as
brainstem TIAs such as diplopia, dizziness, weak- agitation, hallucinations mimicking frontal lobe
ness of both legs, or occipital headaches (von Campe disorders (Biller et al. 1985; Ghika-Schmid and
et al. 2003). Obstruction of the BA often interrupts Bogousslavsky 2000). The triad of hypersomnia,
blood supply of the basis of the pons by the superior supranuclear vertical-gaze defect, and amnesia (the
cerebellar arteries (SCA). Pseudobulbar paralysis so-called “paramedian diencephalic syndrome”)
by interruption of descending tracts to the bulbar is typically due to bilateral paramedian thalamic
nuclei is often seen. The spinothalamic tract and strokes in the territory of the anterior thalamic/sub-
the cerebellar hemispheres are often spared from thalamic (or thalamoperforating) arteries (“en ailes
infarction. Disturbance of eye movements occur de papillon”) (Meissner et al. 1987).
because of infarction of the lateral gaze centers in
the paramedian pontine tegmentum, e.g. the medial 1.2.1.2.4
longitudinal fasciculus (internuclear ophthalmople- Posterior Cerebral Artery (PCA)
gia), the parapontine reticular formation (PPRF),
which generates lateral gazes, or the combination Historically, the French neurologist Charles Foix
of both, resulting in the so called “one and a half- in 1923 first described the syndrome of infarction in
syndrome” (Mehler 1989; Voetsch et al. 2004). the PCA territory as a thalamocapsular deficit (Foix
Infarction of the medial pontine tegmentum will and Masson 1923). The PCAs arise from the BA, but
cause coma and is a poor prognostic sign (Fisher about 30% of patients have a hypo- or aplastic P1
1977; Kataoka et al. 1997). segment with the PCA nourished by the ICA through
In most patients with BA thrombosis, obstruc- the posterior communicating artery (Margolis et
tion is limited to the mid portion of the basilar al. 1971).
artery (Fig. 1.2) (Voetsch et al. 2004). Embolic Headache in patients with PCA disease is often
occlusion rather than thrombotic occlusion mainly retro-orbital or above the eye reflecting innerva-
blocks the distal part of the BA when it divides into tion of the upper surface of the tentorium by the
the PCAs. The distal BA supplies the midbrain and first division of the trigeminal nerve (Brandt et

Fig. 1.2. Digital subtraction angiography of a patient with basilar artery thrombosis before (left) and after (right) thrombolytic
therapy. (Courtesy of Prof. von Kummer)
8 G. Gahn

al. 2000; Ferro et al. 1995). Infarction in the PCA may contribute to the blockade of the artery at this
territory usually causes visual symptoms such as point. Finally a small infarction, called a “lacune”,
homonymous hemianopia or quadrantanopia and will occur. Especially in the basilar artery atheroma-
sensory deficits but seldom paralysis. Patients with tous changes in the arterial wall may occlude the ori-
hemianopia due to infarction of the striate cortex gins of the small penetrating arteries or be the origin
are fully aware of their deficit. In contrast patients of an expanding thrombosis adherent to the arterial
with infarction in the parietal lobe within the MCA wall (“microatheroma”) (Fisher and Caplan 1971).
territory have visual neglect and are unaware of Usually this will cause blockade of several perfo-
their deficit (Ferber and Karnath 2001). Proxi- rating arteries and subsequent small deep infarcts
mal PCA-occlusion may simulate MCA-infarction in contrast to lacunar infarcts which result from
because of thalamic involvement (Chambers et al. single perforating artery disease. An animal model
1991). Optokinetic nystagmus is normal in patients to study cerebral microangiopathy in a standardized
with hemianopia but reduced towards the side of the matter is presently not available (Caplan 1993).
visual defect in those with visual neglect (Morrow Conversely we rely on clinical and imaging data in
and Sharpe 1993). humans to understand this disease.
Some neuropsychological syndromes can be pres- Lacunar infarcts are typically located in the basal
ent in PCA infarction (Ferro 2001): ganglia, the deep white matter and in the brainstem
Alexia without agraphia in left occipital lobe (Fisher 1965a, 1998). Depending on their location
infarction and the splenium of the corpus callo- and their size circumscribed neurological symp-
sum. Transfer of read words from the functional toms will occur. C. Miller Fisher described the
right visual cortex to the left sided language center four classical lacunar syndromes:
is impossible due to interruption of the splenium.
Transfer of primary language information for writ- • Pure motor stroke (Fisher and Curry 1964)
ing or speech is not impaired. • Pure sensory stroke (Fisher 1965b)
Transcortical sensory aphasia appears in patients • Ataxic hemiparesis (Fisher 1978)
with left PCA infarctions and displays difficulties in • Dysarthria-clumsy-hand-syndrome
naming objects but no problems in repeating without (Fisher 1967; Fisher and Curry 1964)
understanding. Gerstmann’s syndrome with infarc-
tion of the angular gyrus consists of inability for All these syndromes are a consequence of small
right-left differentiation, finger anomia, construc- lacunes interrupting pathways in the white matter.
tional apraxia, agraphia and acalculia. In associa- Lacunar strokes almost never cause cortical symp-
tive visual agnosia after left PCA infarctions visual toms such as aphasia or apraxia. Depending again
but not tactile recognition of objects is impaired. on the location of the infarctions, patients may
Prosopagnosia is a problem with recognizing faces present with combined symptoms sometimes with
and occurs in right PCA infarctions. Cortical blind- preceding stereotyped TIAs. Lacunes within the
ness occurs in bilateral PCA infarctions; however, internal capsule may cause dense hemiplegia, but
pupillary reflexes are preserved (also see Chap. 14). never combined with impaired consciousness or
conjugate eye deviation as in territorial infarcts
with mass effect. At presentation, symptoms may be
1.2.2 subtle or mild and may fluctuate or progress. This is
Lacunar Infarction probably related to the hemodynamic aspect in the
pathogenesis of the disease. Many patients experi-
Cerebral microangiopathy accounts for 20%–30 % ence progression of the neurological deficits during
of all ischemic strokes and is mainly due to long the first 24 h after onset of ischemic symptoms, the
lasting arterial hypertension. Narrowing of arteri- so-called capsular warning syndrome (Donnan
oles is caused by so called lipohyalinosis, a process et al. 1993; Staaf et al. 2004). Often these patients
collecting hyaline substances in the media of the wake up in the morning with neurological deficits
small cerebral arteries (Fisher 1965c). These small which occurred sometimes during sleep and with
arteries typically supply exclusively small territories comparatively low blood pressure (Chaturvedi et
of less than 1 or 2 cm in diameter. With progres- al. 1999). In contrast embolic strokes tend to occur
sion of arterial narrowing blood flow towards the after getting up, when activation of the cardiovascu-
nourished territory diminishes until oligemia or lar system provokes plaque disruption or increased
ischemia occur. Eventually thrombotic mechanisms cardiac contractility. Notably, recent MRI studies
Stroke Syndromes 9

showed no differences in stroke subtypes between borderzone infarction in the case of poor collateral
waking strokes and strokes occurring during sleep supply through the circle of Willis (Powers 1991).
(Donnan et al. 1993; Fink et al. 2002). Lacunar Clinically stereotyped TIAs or the opticocerebral
syndromes do not specifically help to localize the symptom with simultaneous amaurosis and contra-
infarct to a certain territory in the brain and are lateral hemiparesis due to critically low blood supply
not highly specific for the diagnosis of a “lacune” through an occluded or almost occluded ICA herald
(Baumgartner et al. 2003; Gan et al. 1997). a pending borderzone ischemia (Tsiskaridze et al.
2001). Rarely so-called limb shaking TIAs may point
to a hemodynamic ischemia in ICA occlusive disease
1.2.3 (Baquis et al. 1985).
Borderzone Infarction

Borderzone infarcts develop at the junction between

different arterial territories (Adams et al. 1966). 1.3
Pathophysiologically two different classes of border- Particular Etiological Stroke Syndromes
zone infarcts can be identified: infarction between
two arterial territories with a connecting arterio- 1.3.1
lar collateral network, so-called watershed infarcts, Cardioembolic Stroke
and infarcts between two arterial territories without
arteriolar collaterals, so-called end-zone infarcts Thromboembolic stroke mainly derives from cardiac
(Bogousslavsky and Moulin 1995). This classifi- thrombus formation (Schneider et al. 2004). Less
cation is based on the anatomic distribution of the frequently the source is intra-arterial, from the distal
cerebral vascular supply consisting of two main sys- end of a thrombus within the lumen of an obstructed
tems: first, superficial arteries surround the brain carotid or vertebral artery or from an atheromatous
parenchyma with an anastomotic network and send plaque in the cervical arteries or in the aortic arch.
off perforating centripetal branches that do not anas- The cardiac embolus usually arises in the anterior
tomose (Moody et al. 1990). Second, deep branches circulation through the internal carotid artery up
originating from the major arterial branches pen- into the middle cerebral artery. At a site of sudden
etrating the brain without anastomoses. Clinically lumen reduction either at the origin of the middle
relevant borderzones are the anterior borderzone cerebral artery or more distally at the bifurcation
between the MCA and the ACA and the posterior into the middle cerebral artery branches, it gets
borderzone between the MCA and the PCA. They stuck and blocks the lumen of the artery (Caplan
represent watershed areas and cause mainly cortical 1993). Embolic infarction often turns into hemor-
infarction. The subcortical borderzones between the rhagic transformation. Most often the middle cere-
deep and the superficial perforators represent end- bral artery, especially its inferior branch, is the site
zone areas and cause subcortical infarctions (Read of embolic obstruction (Bogousslavsky et al. 1989).
et al. 1998). In the posterior circulation both water- The embolic material may remain arrested and plug
shed and end-zone areas exist between the PICA the artery solidly. It also may break into fragments
and the SCA territories. The penetrating branches of and spread into smaller branches more peripherally.
the basilar artery are a potential source of end-zone The phenomenon of a clot first lodging in the inter-
infarctions comparable to the lenticulostriate arter- nal carotid artery, producing profound symptoms of
ies (Bogousslavsky and Moulin 1995). hemispheric ischemia, and then migrating distally
The underlying mechanism of borderzone to a MCA pial branch has been called the “spectacu-
infarcts is the low flow situation (Ringelstein et lar shrinking deficit” (Minematsu et al. 1992). The
al. 1983) in the most distal fields supplied by the dramatic initial deficit diminishes to a minor deficit
cerebral circulation (“last meadows”) (also see corresponding to the terminal branch artery.
Chap. 15). Hemodynamic impairment will conse- At total of 75% of cardiac emboli reach the
quently first cause ischemia in these areas. Typical brain. Non-valvular atrial fibrillation with throm-
clinical situations are a prolonged drop in systemic bus formation within the left atrial appendix or
blood pressure, e.g. during cardiac surgery causing the left atrium is the most common reason for car-
bilateral borderzone infarcts or severe occlusive diac emboli (Ferro 2003). Cardio-embolic infarcts
disease of the internal carotid artery (Bladin and within the MCA territory carry a high risk for hem-
Chambers 1994). This may only lead to unilateral orrhagic transformation after reperfusion. Hemor-
10 G. Gahn

rhagic transformation is a natural consequence of after both major or trivial traumatic head or neck
cerebral infarction, occurring in up to 65% of stroke injury (Schievink 2001). Many patients have preced-
patients and in up to 90% of patients with cardio- ing warning symptoms: the typical patient with carotid
embolic stroke within the first week after symptom artery dissection presents with pain on one side of the
onset (Molina et al. 2001). Hemorrhagic transfor- head, face, or neck accompanied by a partial Horner’s
mation does not impair neurological outcome after syndrome and followed hours or days later by cerebral
embolic stroke (Fiorelli et al. 1999). It may even or retinal ischemia (Schievink 2001). Final infarction
suggest favorable outcome indicating early reperfu- may arise mostly due to embolic and seldom due to
sion of the blocked MCA (Molina et al. 2002). hemodynamic mechanism (Benninger et al. 2004).
Paradoxical embolism can occur in a patent fora- In carotid artery dissection, Horner’s syndrome
men ovale with a right to left shunt. Embolic material develops in less than half of patients as well as vagal,
arising from the pelvic or leg veins or elsewhere in hypoglossal or accessorial nerve palsy. The underly-
the venous system may bypass the pulmonary system ing mechanism could be nerve compression, stretch-
and reach the cerebral arteries (Braun et al. 2004). ing or occlusion of small nourishing branches within
an arterial wall by the intramural hematoma (Mokri
et al. 1996). The pathogenesis of dissection remains
1.3.2 obscure except in patients with obvious collagen tissue
Dissection disease such as fibromuscular dysplasia. Other types
of connective tissue alterations may also be associated
Spontaneous dissection of the internal carotid or with cervical artery dissections (Hausser et al. 2004).
the vertebral artery is an important cause of isch- The site of dissection in adults is mainly the internal
emic stroke in young adults (Fig. 1.3). In the late carotid artery at its distal extracranial course above
1970s Fisher et al. (1978) and Mokri et al. (1979) the carotid bulb. In children the site of dissection is
described dissections of carotid and vertebral arteries predominately intracranially (Fullerton et al. 2001).
as detected by modern diagnostic techniques rather The risk for recurrent dissections is very low (Touze
than by post-mortem examination. This may occur et al. 2003).

Fig. 1.3. Computed tomography (left), digital subtraction angiography (DSA, middle) and MRI (right) of a patient with internal
carotid artery dissection. Note diffuse swelling of the frontal-parietal cortex on CT on day three after onset of symptoms. At this
time point the patient suffered from a severe left hemiparesis. DSA shows classical “string sign” of cervical artery dissection
with continuous narrowing of arterial lumen. MRI: ADC map (upper images) on day three after onset of symptoms shows small
area of ischemia (dark). Time-to-peak parameter image (lower images) shows delayed contrast inflow to the entire right MCA
territory. The patient underwent stent protected dilatation of the arterial stenosis 6 days after symptom onset and recovered
almost completely from the severe hemiparesis. (Courtesy of Prof. von Kummer)