Introduction
C H A P T E R
88
Stroke and Eye Findings
V. Biousse, N.J. Newman
Emory University School of Medicine, Atlanta, GA, United States
INTRODUCTION
Stroke patients often have visual symptoms and signs,
the characteristics of which vary mostly depending on
the type of vessel involved (arteries versus veins), the
type of stroke (ischemic or hemorrhagic), and the size of
the arteries involved (large versus small artery disease).
Because the blood supply to the eye is mostly provided
by branches of the ophthalmic artery, the first intracra-
nial branch of the internal carotid artery (ICA), patients
with anterior circulation cerebral ischemia may present
with ipsilateral visual changes. Binocular visual loss or
abnormal extraocular movements are common with vas-
cular diseases affecting the posterior circulation, which
provides the blood supply to the occipital lobes and pos-
terior fossa. In addition, a number of ocular vascular dis-
orders are associated with numerous systemic diseases
affecting the eyes and the brain simultaneously [1,2].
Ocular Symptoms and Signs Associated With
Carotid Artery Disease and Anterior Circulation
Ischemia
Monocular (ipsilateral to the affected ICA) transient
and permanent visual symptoms and signs may develop
in patients with carotid artery disease or those with
emboli from the aortic arch or the heart. Contralateral
homonymous visual field defects, bitemporal visual
field defects, and bilateral simultaneous visual loss may
also result from anterior circulation ischemia, particu-
larly when the disease is bilateral [1,2].
Transient Monocular Visual Loss
Although transient monocular visual loss may
result from retinal transient ischemic attack (TIA),
it is important to emphasize that there are numerous
nonvascular causes of transient monocular visual loss,
Primer on Cerebrovascular Diseases, Second Edition
http://dx.doi.org/10.1016/B978-0-12-803058-5.00088-6 © 2017 Elsevier Inc. All rights reserved.
427
which require an emergent detailed ocular examina-
tion; therefore, an ophthalmic consultation should be
obtained before obtaining an extensive workup for
presumed vascular transient monocular visual loss
(so-called “amaurosis fugax”). Retinal TIAs classically
present as sudden, complete blackout of vision in one
eye, lasting few minutes without residual visual loss.
Ocular examination may show retinal emboli or may be
normal. The workup is similar to that of a cerebral TIA,
including stroke protocol brain imaging, since about
25% of patients with acute retinal ischemia have con-
comitant acute cerebral ischemia [3]. Multiple episodes
of transient visual loss or painful transient visual loss
in the elderly should raise the possibility of giant cell
arteritis [2].
Permanent Monocular Visual Loss
Partial or complete monocular loss of vision may
occur in patients with ipsilateral carotid artery disease,
or emboli in the anterior circulation. This results most
often from a central retinal artery occlusion (CRAO)
(Fig. 88.1) or from one or multiple branch retinal artery
occlusions (BRAOs) (Fig. 88.2). In such cases, emboli
may be seen in the affected vessels. The most com-
mon emboli that occlude retinal arterioles are made
of cholesterol, fibrin platelets, and calcium fragments
(Table 88.1). Acute retinal ischemia should be evaluated
emergently, in a similar manner as with acute cerebral
infarctions [2].
Venous stasis retinopathy and ocular ischemic syn-
drome are caused by severe carotid obstructive disease
and poor collateral circulation. The retinopathy is char-
acterized by insidious onset, dilated and tortuous retinal
veins, peripheral microaneurysms, and dot-blot hem-
orrhages in the mid-peripheral retina, associated with
neovascularization when ocular ischemic syndrome
develops (Fig. 88.3). Patients with this condition develop
progressive and often irreversible visual loss, sometimes
428 88.  Stroke and Eye Findings

FIGURE 88.1  Acute central retinal artery occlusion. Funduscopic photograph showing an acute central retinal artery occlusion in the left eye.
Note the attenuated central retinal artery with segmental arterial narrowing (yellow arrows). The ischemic retina is edematous and appears whitish,
and there is a cherry red spot (white arrow). Within few weeks, the retinal vessels often recanalize and the retina has an almost normal appearance;
however, the optic disk eventually becomes pale.

FIGURE 88.2  Retinal emboli. Funduscopic photograph showing refractile cholesterol retinal emboli (yellow arrows) associated with inferior
retinal ischemia (whitish discoloration of the retina; white arrow) in a patient with aortic arch atheroma (A). One week later, repeat funduscopic
photographs showed new emboli superiorly (yellow arrows) (B).

associated with cerebral hypoperfusion, and the progno-
sis is poor [1,4].
Ischemic optic neuropathy, anterior or posterior,
results from small vessel disease and is usually not asso-
ciated with large artery disease, explaining why carotid
artery evaluation is not usually indicated in patients
with classic anterior ischemic optic neuropathy [5].
Permanent Binocular Visual Loss
Partial or complete contralateral homonymous hemi-
anopic visual field defects may result from cerebral
ischemia in the anterior circulation. This is most often
caused by occlusion of branches of the middle cerebral
artery, but it may result from occlusion of the anterior
choroidal artery or some of its branches to the optic tract
and lateral geniculate body [1,6].
Horner Syndrome
Horner syndrome is a classic sign of carotid dissec-
tion and may also occur in patients with atherosclerotic
carotid artery disease. The Horner syndrome may be iso-
lated (often with ipsilateral facial pain) or may be asso-
ciated with other neurological symptoms and signs of
carotid artery disease [1].

VI.  CLINICAL ASPECTS: MEDICAL AND SURGICAL

 Introduction 429
TABLE 88.1  Most Common Types of Retinal Emboli
Type of Retinal Emboli Source of Emboli Funduscopic Appearance

Cholesterol (Hollenhorst Ipsilateral internal carotid artery Yellow, refractile

plaque) Aortic arch
Multiple in 70% of cases

Appear wider than the arteriole

Often at an arteriole bifurcation

Platelet fibrin Carotid thrombus White–gray, pale, not refractile

Aortic arch thrombus
Cardiac thrombus Often multiple
Cardiac prosthesis Within small retinal arterioles

Calcium Calcified atheromatous plaque White and large

Calcified cardiac valve
Usually isolated

In the proximal segment of the central retinal artery or its branches

Infectious Infective endocarditis White spots (Roth’s spots)

Candidemia Multiple

Talc Intravenous drugs Yellow, refractile

Multiple

Neoplasm Cardiac myxoma White, gray

Often multiple

Fat Fat emboli in the setting of leg facture Whitish spots with hemorrhages and cotton wool spots

Multiple

compression of the trigeminal branches. It may also be

part of the ocular ischemic syndrome [1].
Ocular Motor Nerve Paresis
Exceptionally, patients with acute occlusion or severe
ICA stenosis may develop one or more ocular motor
nerve pareses on the side of the occlusion, either in isola-
tion or with signs of ocular ischemia [1].

Visual Symptoms and Signs Associated With

FIGURE 88.3  Chronic ocular ischemia. Funduscopic photograph
showing multiple dot-blot retinal hemorrhages (yellow arrows) in the
right eye of a patient with right internal carotid occlusion.
Referred Pain
Isolated facial pain (often periocular) may be a
symptom of carotid occlusive disease, even without
other symptoms and signs of vascular disease. It is
usually a referred pain resulting from ischemia or
Posterior Circulation Disease
The vertebrobasilar system supplies the entire brain
stem ocular motor system as well as the posterior visual
sensory pathways and visual cortex. For this reason, ocu-
lar motor and visual symptoms and signs play a major
role in the diagnosis of vascular disease in the vertebro-
basilar system [1,7].
Transient Binocular Visual Loss
Episodes of transient binocular visual loss are common
in vertebrobasilar ischemia (Table 88.2). The visual loss
is always bilateral, with both eyes being affected simul-
taneously and symmetrically. The change in vision may
be described as a sudden “gray-out of vision,” “a sensa-
tion of looking through fog or smoke,” or “the feeling
that someone has turned down the lights,” classically

VI.  CLINICAL ASPECTS: MEDICAL AND SURGICAL

430 88.  Stroke and Eye Findings

TABLE 88.2  Differential Diagnosis of Cerebral Visual Loss acuity. When both occipital lobes are infarcted, visual
Classified by Mechanism acuity is usually severely impaired, but the amount of
Mechanism Cause of Vision Loss visual loss is symmetric in both eyes. In some cases of
occipital lobe infarction, the anterior portion of the lobe
Vascular Vertebrobasilar ischemia (posterior cerebral is unaffected, resulting in sparing of part or all of the
artery territory)
peripheral 30  degree of the contralateral, monocular
Cerebral anoxia temporal field—the temporal crescent. Some patients
Cerebral venous thrombosis (superior sagittal initially experience complete blindness, with vision
sinus) returning in the ipsilateral homonymous visual field
Hypertensive encephalopathy (posterior
within minutes. Pain in the ipsilateral eye or over the
reversible encephalopathy syndrome) ipsilateral brow (contralateral to the hemianopia) is a
classic symptom in such patients. This pain is referred
Eclampsia
from the tentorial branches of the trigeminal nerve [6].
Head trauma Occipital lobe injury
Disorders of Higher Cortical Function
Occipital mass Tumor
A number of syndromes described by patients as
Abscess
“difficulty seeing” or “difficulty reading” may result from
Vascular (aneurysm, arteriovenous posterior circulation cerebral ischemia, including alexia
malformation) without agraphia, Gerstmann syndrome, ­associative visual
Hemorrhage agnosia, prosopagnosia, visual neglect, cerebral blindness,
Balint’s syndrome, simultagnosia, and achromatopsia [1,6].
Demyelinating Multiple sclerosis
disease
Visual Hallucinations
Infection Occipital abscess
Formed visual hallucinations may be caused by ver-
Meningitis tebrobasilar ischemia. These hallucinations, which may
Progressive multifocal leukoencephalopathy last 30 min or more, may be associated with decreased
consciousness, but they usually occur in an otherwise
Creutzfeld–Jacob disease
alert patient who is aware that the visual images are
Toxic Cyclosporine not real. The hallucinations are generally restricted to a
Tacrolimus hemianopic field, and they are often complex [1,6].
Metabolic Hypoglycemia Diplopia
Porphyria Transient binocular horizontal or vertical diplopia is a
Hepatic encephalopathy
common manifestation of vertebrobasilar ischemia. The
diplopia may result from transient ischemia of the ocular
Migraine Migrainous visual aura motor nerves or their nuclei (ocular motor nerve paresis)
Seizure Occipital lobe seizures or from transient ischemia to supranuclear or internuclear
Degenerative Alzheimer disease/posterior cortical atrophy
ocular motor pathways (skew deviation, internuclear
ophthalmoplegia, gaze paresis). In most cases, the diplo-
pia is not isolated, and the patient has other neurological
lasting no more than few minutes. Transient, complete symptoms suggesting vertebrobasilar ischemia [1,6,7].
90–180 degree inversion of the visual image may rarely Persistent disturbances of eye movements are
occur [7]. extremely common in patients with vertebrobasilar isch-
emia. Ocular motor nerve paresis, internuclear ophthal-
Homonymous Visual Field Defects moplegia, supranuclear deficits, and nystagmus develop
An isolated homonymous visual field defect of sud- based on the anatomical location of the lesion. Nystag-
den onset is the hallmark of a vascular lesion in the mus produces oscillopsia, which is often described by
occipital lobe in the territory supplied by the posterior the patients as “jumping of vision” [1,6,7].
cerebral artery (PCA). The visual field defect may be
complete or incomplete, but when it is incomplete or
Ocular Symptoms and Signs Associated With
scotomatous, it is usually congruous. When there is a
complete homonymous hemianopia, macular sparing
Cerebral Vasculitis
is common, and the occipital pole is usually spared. Both infectious and noninfectious inflammation
Patients with a homonymous visual field defect caused affecting the central nervous system can produce visual
by ischemia in the PCA territory have normal visual symptoms. In some vasculitides with a predilection for

VI.  CLINICAL ASPECTS: MEDICAL AND SURGICAL

 Introduction 431
TABLE 88.3  Characteristics of the Three Autosomal Dominant Cerebro-Ocular Vasculopathies Mapped to Chromosome 3
Name Ocular Findings Neurological Findings Other Findings

Hereditary Vascular Microangiopathy Multiple small lesions in Raynaud phenomenon

Retinopathy (HVR) Retinal periphery and gray and white matter
posterior pole
Headaches

Cerebro-Retinal Microangiopathy Cerebral pseudotumors

Vasculopathy (CRV) Posterior pole
Extensive white matter lesions

Dementia

Headaches

Death <55 years

Hereditary Endotheliopathy, Microangiopathy Cerebral pseudotumors Renal involvement

Retinopathy, Nephropathy, Posterior pole
and Stroke (HERNS) Extensive white matter lesions

Dementia

Headaches

Stroke

Death <55 years

large arteries, such as Takayasu’s arteritis, ocular isch-
emia is common. Most often, vasculitis produces retinal
vasculitis with retinal vascular occlusions and visual
loss, often associated with ocular inflammation (uveitis).
Giant cell arteritis should be considered in all patients
over 50 years presenting with acute optic nerve or retinal
ischemia. Permanent visual loss is common in giant cell
arteritis, and is often preceded by transient monocular
visual loss [1].
Ocular Symptoms and Signs Associated With
Noninflammatory Cerebral Vasculopathies
Susac Syndrome
Susac syndrome describes young patients with
multiple bilateral branch retinal arterial occlusions,
hearing loss, and neurological symptoms suggestive
of a brain microangiopathy. It classically occurs in
young women but can affect men. Affected patients
have recurrent multiple BRAOs that are most often
bilateral, progressive hearing loss (low and medium
frequencies, and best demonstrated by audiogram),
and various neurological presentations including psy-
chiatric changes and encephalopathy (which varies
in severity from mild memory loss and personality
changes to severe cognitive dysfunction, confusion,
psychiatric disorders, seizures, and focal neurologi-
cal symptoms and signs). The disease usually has a
chronic relapsing course punctuated by frequent
remissions and exacerbations.
Retinal fluorescein angiography classically shows reti-
nal arterial wall hyperfluorescence, which is indicative
of disease activity. Brain MRI typically shows multiple
enhancing small lesions in both the white and gray mat-
ter, with classic involvement of the corpus callosum. The
MRA is normal, but catheter angiography has shown
evidence of vasculopathy in some patients. In few cases,
brain biopsy was performed and showed microinfarcts
with some minimal perivascular lymphocytic infiltration,
but no true vasculitis [8].
Hereditary Retinopathies
A number of rare hereditary retinopathies are asso-
ciated with central nervous system abnormalities.
Genetic characterization of three of these syndromes
has shown that there is an overlap among these entities
(Table 88.3) [9].
Aneurysms, Fistulas, and Vascular
Malformations
Aneurysms
The most common neuro-ophthalmic manifesta-
tions of intracranial aneurysms are secondary to local
mass effect on adjacent cranial nerves. The pulsatile
process of the aneurysm may be as important as the
direct mass effect. Aneurysms arising from the oph-
thalmic artery, the cavernous carotid artery, the ante-
rior communicating artery, or the ICA can result in
unilateral optic neuropathy or chiasmal visual field
defects. Rarely, a homonymous hemianopia can
result from compression of the optic tract. Multiple
ocular motor nerve palsies can result from an aneu-
rysm involving the cavernous carotid artery. Posterior

VI.  CLINICAL ASPECTS: MEDICAL AND SURGICAL

432 88.  Stroke and Eye Findings
FIGURE 88.4  Right Terson syndrome. Funduscopic photograph
showing multiple intraocular hemorrhages in a patient with acute
aneurysmal subarchnoid hemorrhage. Note the intraretinal hemor-
rhages (white arrow), preretinal hemorrhages (yellow arrow), and disk
edema (blue arrow). There was a dense vitreous hemorrhage in the left
eye and the funduscopy could not be visualized.
communicating artery aneurysms classically produce
an isolated third nerve palsy, whereas isolated troch-
lear or abducens nerve palsies only rarely result from
aneurysmal compression.
Aneurysmal rupture producing a subarachnoid hem-
orrhage may be associated with intraocular hemor-
rhages (so-called “Terson syndrome”) (Fig. 88.4). The
presumed mechanism is that of acute raised intracranial
pressure with sudden elevation of ocular central venous
pressure. When an aneurysm arises from the cavern-
ous carotid artery or from its branches in the cavernous
sinus, rupture results in carotid–cavernous fistula, not
subarachnoid hemorrhage [1,10].
Carotid–Cavernous Sinus Fistula
Direct carotid–cavernous fistula resulting from
direct communication of the cavernous carotid artery
and the cavernous sinus with resultant high velocity
of blood flow most often results from trauma or from
rupture of a preexisting aneurysm of the cavernous
carotid artery. Ocular manifestations are usually obvi-
ous and include proptosis, periorbital swelling, che-
mosis, dilation of the episcleral vessels, orbital bruit,
ophthalmoplegia, elevated intraocular pressure, dila-
tion or occlusion of the retinal veins, and optic disc
edema.
Dural carotid–cavernous sinus fistulas result from
indirect communications between branches of the inter-
nal and external carotid arteries and the cavernous sinus.
They are more common in middle-aged and elderly
women. Neuro-ophthalmic manifestations depend on
the blood flow velocity and vary from the full classical
VI.  CLINICAL ASPECTS: MEDICAL AND SURGICAL
appearance of direct fistulas to isolated bruit, cranial
nerve palsies, or simply a “red eye.”
Orbital imaging with CT or MRI classically shows
dilation of the superior ophthalmic veins, enlargement
of the extra-ocular muscles, or enlargement of the cav-
ernous sinus. Catheter angiography is still the best way
to confirm a carotid–cavernous fistula which can often
be treated with an endovascular approach at the same
time [1,10].
Arteriovenous Malformations
Intracranial arteriovenous malformations may result
in intraparenchymal hemorrhage, subarachnoid hemor-
rhage, seizures, or mass effect. Occipital arteriovenous
malformations can cause episodic visual symptoms
mimicking the visual aura of migraine. Homonymous
hemianopia is common in occipital lesions, most often
as the result of bleeding or as a complication of treat-
ment. Posterior fossa arteriovenous malformations
usually cause intermittent or permanent diplopia,
often associated with other neurological signs. Orbital
arteriovenous malformations produce an acute or sub-
acute orbital syndrome, including proptosis, chemo-
sis, ophthalmoplegia, visual loss, and elevation of the
intraocular pressure.
Retinal arteriovenous malformations are rare. They
are sometimes isolated or are associated with intracra-
nial or facial arteriovenous malformations [1,10].
Cavernous Hemangioma
Cavernous hemangiomas are most common in the
posterior fossa and usually produce diplopia when
they bleed. Familial cavernous hemangiomas are
often multiple and may be associated with grape-like
appearing small retinal hemangiomas that are usually
asymptomatic [1,10].
Venous Disease
Central and Branch Retinal Vein Occlusions
Central retinal vein occlusion (CRVO) and branch
retinal vein occlusions (BRVO) are common ocular dis-
orders in elderly patients often associated with athero-
matous vascular risk factors. Occlusion of the central
retinal vein is presumed to result from compression by
the central retinal artery within the optic nerve. Patients
with CRVO complain of blurry vision, the severity of
which depends on the severity of the CRVO and associ-
ated retinal ischemia. Funduscopic examination reveals
diffuse retinal hemorrhages, retinal and macular edema,
dilated and tortuous veins, and optic disk edema. This
disorder is primarily managed by the ophthalmolo-
gist, and the goals of the treatment are to treat macular
edema and prevent or treat neovascularization and its
complications.
 REFERENCES
Cerebral Venous Thrombosis
Cerebral infarction related to cerebral venous throm-
bosis may present with acute focal neurological signs,
including homonymous hemianopia or cranial nerve
palsies, usually in the setting of headaches or altered
mental status. Most neuro-ophthalmic manifestations
of cerebral venous thrombosis, however, are related to
increased intracranial pressure, and include papilledema
and diplopia from uni- or bilateral sixth nerve palsies.
Cavernous sinus thrombosis is extremely rare and
produces acute painful proptosis with chemosis, oph-
thalmoplegia, venous stasis retinopathy, and visual loss.
CONCLUSION
Cerebrovascular diseases are commonly associated
with neuro-ophthalmological symptoms and signs,
which mostly depend on the type, the size and the loca-
tion of the vessels involved, and the mechanism of the
vascular lesion.
433
References
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838–56.
[3] Biousse V. Acute retinal arterial ischemia: an emergency often
ignored. Am J Ophthalmol 2014;157:1119–21.
[4] Mendrinos E, Machinis TG, Pournaras CJ. Ocular ischemic syn-
drome. Surv Ophthalmol 2010;55:2–34.
[5] Biousse V, Newman NJ. Ischemic optic neuropathies. N Engl J
Med 2015;372:2428–36.
[6] Caplan L. Posterior circulation ischemia: then, now, and tomor-
row. The Thomas Willis Lecture-2000. Stroke 2000;31:2011–23.
[7] Moncayo J, Bogousslavsky J. Vertebro-basilar syndromes causing
oculo-motor disorders. Curr Opin Neurol 2003;16:45–50.
[8] Rennebohm R, Susac JO, Egan RA, Daroff RB. Susac’s syndrome–
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C H A P T E R

89
Spinal Cord Strokes
R. Bhole1, L.R. Caplan2
1University of Tennessee Health Science Center, Memphis, TN, United States; 2Harvard University, Beth Israel
Deaconess Medical Center, Boston, MA, United States

Spinal cord strokes are a rare but important differen-
tial consideration in central nervous system vascular dis-
ease. As in the brain, spinal cord strokes can be divided
into two large groups—ischemic and hemorrhagic. They
account for about 1% of all strokes and about 5–8% of
acute myelopathies [1,2].
SPINAL CORD VASCULAR SUPPLY
The arterial supply of the spinal cord is unique.
A large single anterior spinal artery runs in the ven-
tral midline from the spinomedullary junction at the
foramen magnum to the filum terminale. In contrast
paired smaller posterior spinal arteries are located on the
dorsal surface, which often form a rich plexus of small
vessels (Fig. 89.1) [3]. The central portion between the
two zones of supply has often been called the border
zone or watershed region of the spinal cord.
The anterior spinal artery originates from the two ver-
tebral arteries at the base of the skull, feeds the medulla,
and descends in the midline through the foramen mag-
num to supply the cervical spinal cord. The artery is fed by
a series of 5–10 unpaired radicular arteries that originate
from the vertebral arteries and the aorta and its branches.
The blood supply is most marginal in the upper thoracic

Primer on Cerebrovascular Diseases, Second Edition

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