DOI:10.2214/AJR.05.1588
AJR 2007; 188:W74-W81
© American Roentgen Ray Society
Neuroimaging Strategies for Three Types of Horner Syndrome with Emphasis on Anatomic Location
Jeong Hyun Lee1,
Ho Kyu Lee2,
Deok Hee Lee1,
Choong Gon Choi1,
Sang Joon Kim1 and
Dae Chul Suh1
1 Department of Radiology and Research Insitute of Radiology, University of
Ulsan College of Medicine, Asan Medical Center, 388-1 Poongnap-2dong,
Songpa-gu, 138-736, Seoul, South Korea.
2 Department of Radiology, University of Iowa Hospitals and Clinics, Iowa City,
IA 52242.
Received September 7, 2005;
accepted after revision November 3, 2005.
Presented at the 2004 Meeting of Radiological Society of North America.
138-736, Seoul, South Korea. Address correspondence to J. H. Lee
(jeonghlee{at}amc.seoul.kr).
WEB
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Abstract
OBJECTIVE. The purposes of this study were to review the anatomy of
the oculosympathetic pathway, to describe the clinical characteristics of the
three types of Horner syndrome, and to illustrate underlying pathologic
features with an emphasis on neuroimaging strategies based on three symptom
complexes.
CONCLUSION. Horner syndrome results from interruption of the
oculosympathetic pathway and is usually associated with unique clinical
features classified into central, preganglionic, and postganglionic types
according to the anatomic location of the underlying pathologic process.
Keywords: CT • Horner syndrome • MRI • neuroimaging
Introduction
Horner syndrome classically manifests as ipsilateral blepharoptosis,
pupillary miosis, and facial anhidrosis
[1,
2]. The syndrome results from
interruption of the oculosympathetic pathway, which follows a long, circuitous
route with central, preganglionic, and postganglionic neurons. Therefore,
depending on the anatomic location of the underlying pathologic process,
Horner syndrome usually is associated with unique clinical features classified
into central, preganglionic, and postganglionic types
[1]. We review the anatomy of
the oculosympathetic pathway and the clinical characteristics of the three
types of Horner syndrome. We also illustrate a variety of the underlying
pathologic processes involving the hypothalamus, brainstem, brachial plexus,
anterior aspect of the neck, skull base, internal carotid artery, and
cavernous sinus with an emphasis on neuroimaging strategies based on the three
symptom complexes.
Anatomy of the Oculosympathetic Pathway and Clinical Features of Horner Syndrome
Figure 1 shows the detailed
anatomy of the central, preganglionic, and postganglionic neurons of the
oculosympathetic pathway. Regardless of the location of the underlying
pathologic processes, interruption to the sympathetic innervation to the eye
causes ipsilateral blepharoptosis, pupillary miosis, and facial anhidrosis.
Müller's muscle receives sympathetic innervation and acts as an accessory
elevator of the upper eyelid. Because Müller's muscle is responsible for
approximately 2 mm of upper eyelid elevation, loss of sympathetic input
results in subtle ptosis
[1].
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Fig. 1 —Drawing shows normal anatomy of oculosympathetic pathway.
First-order neuron (dashed line) arises from posterolateral
hypothalamus, descends into brainstem and intermediolateral column of spinal
cord, and exits at cervical (C8) and thoracic (T1-T2) levels of spinal cord as
second-order neuron (dotted line). Second-order preganglionic neurons
exit ventral spinal roots (a) and arch over apex of lung to ascend in cervical
sympathetic chain, synapsing in superior cervical ganglion (b) and exiting as
third-order neuron (solid lines). Neural fibers for sweating of face,
except medial forehead, travel with external carotid artery. Third-order
postganglionic neuron travels with carotid artery (c) into cavernous sinus and
with ophthalmic branch (d) of fifth cranial nerve joins nasociliary branch of
fifth cranial nerve or passes through ciliary ganglion (e) directly, reaching
eye as long (f) and short (g) ciliary nerves
[7,
8]. Preganglionic
parasympathetic fibers (gray lines) arise from accessory oculomotor
nucleus (h), exit as oculomotor nerve (i), synapse at ciliary ganglion, and
reach eye as short ciliary nerves.
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The size of the pupil results from the balance of dilation and constriction
forces from the sympathetically innervated iris dilator muscle and the
parasympathetically innervated iris constrictor muscle. With sympathetic
denervation, the force of the iris constrictor muscle being
parasympathetically innervated is unopposed, resulting in pupillary miosis and
subtle anisocoria [1,
2]. A schematic for the
pharmacologic diagnosis of anisocoria caused by Horner syndrome is presented
in Figure 2.
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Fig. 2 —Pharmacologic diagnosis and localization of Horner syndrome.
Instillation of one drop of 10% cocaine solution is used for pharmacologic
diagnosis. Cocaine inhibits reuptake of norepinephrine at synaptic junction of
postganglionic fibers and iris dilator muscle and results in pupillary
dilation, but in Horner syndrome pupil does not dilate. One percent
hydroxyamphetamine solution releases norepinephrine from sympathetic synaptic
terminal, which dilates pupil in Horner syndrome only if postganglionic neuron
is intact. So 1% hydroxyamphetamine solution can be used for differential
diagnosis of central and preganglionic from postganglionic lesions.
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The fibers traveling to the sweat glands of the medial forehead branch off
with the third-order sympathetic fibers, and the fibers supplying the rest of
the face branch off more proximally. For this reason, central and
preganglionic lesions cause anhidrosis of the entire side of the face, whereas
anhidrosis limited to the medial forehead suggests a third-order cause
[1].
Types of Horner Syndrome
Central Horner syndrome is relatively uncommon
[3]. Central Horner syndrome
can usually be identified on the basis of the presence of associated
hypothalamic, brainstem, or spinal cord signs and symptoms
[1], which make it easy to
localize the lesion (Figs. 3A
and 3B). In these cases,
selection of imaging technique is influenced not by the presence of Horner
syndrome drome but by associated neurologic findings. The most common
presentation of central Horner syndrome is part of the lateral medullary
syndrome from infarction of the posterior-inferior cerebellar artery or of the
distal vertebral artery territory
[4] (Figs.
4A and
4B). Other neurologic findings
include dysphagia, ipsilateral facial analgesia, contralateral analgesia of
the trunk and extremities, cerebellar ataxia, and rotary nystagmus. As many as
three fourths of patients with central Horner syndrome also have ipsilateral
oculosympathoparesis [4].
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Fig. 3A —68-year-old woman with sudden neurologic symptoms and signs
including disorientation, left miosis, ptosis, and anhidrosis. Axial
T2-weighted image of brain shows acute infarction in anteromedial
thalamus.
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Fig. 3B —68-year-old woman with sudden neurologic symptoms and signs
including disorientation, left miosis, ptosis, and anhidrosis. Axial
T2-weighted image of brain at lower level than A shows acute infarction
involving left posteromedial hypothalamus and left cerebral peduncle of
midbrain.
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Fig. 4A —46-year-old man with right hemiplegia of sudden onset after
swimming. Left miosis, ptosis, and hypohidrosis were found at neurologic
examination. Axial T2-weighted image of brainstem shows acute lateral
medullary infarct (arrow) on left side.
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Fig. 4B —46-year-old man with right hemiplegia of sudden onset after
swimming. Left miosis, ptosis, and hypohidrosis were found at neurologic
examination. Axial T1-weighted image shows hyperintense thrombus along left
distal vertebral artery (arrow).
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Preganglionic Horner syndrome is most often caused by trauma or tumor
[1,
3]. Direct spinal cord trauma
or traction on the brachial plexus can distort the ventral roots and interrupt
sympathetic innervation. The trauma responsible for the injury is often
iatrogenic, including birth trauma, epidural spinal anesthesia, and surgical
trauma (e.g., radical neck dissection) (Figs.
5,
6A, and
6B). Lung and mediastinal
tumors can impinge on the second-order sympathetic neurons (Figs.
7A,
7B, and
8). Tumor from the apex of the
lung can cause Horner syndrome accompanied by shoulder and arm pain, also
known as Pancoast syndrome. Therefore, the presence of occult malignancy
should be considered in any patient with shoulder or arm pain and new Horner
syndrome without a history of trauma
[1].
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Fig. 5 —43-year-old woman with known papillary thyroid carcinoma.
Total thyroidectomy with bilateral modified radical neck dissection was
performed. In operative field, right sympathetic chain had thyroid adhesions
and was difficult to dissect. Right ptosis developed on first postoperative
day. Preoperative CT image of neck depicts heterogeneous masses in both lobes
of thyroid and metastasis in both level IV lymph nodes (long arrows).
Mass in right lobe shows exophytic growth and disruption of fat plane
(short arrows) between mass and prevertebral muscle.
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Fig. 6B —22-year-old man with palpable neck mass. Axial
contrast-enhanced T1-weighted image depicts heterogeneously enhanced ovoid
mass (arrow) between left carotid and prevertebral spaces. Surgical
excision confirmed mass as schwannoma arising from left cervical sympathetic
trunk. Two days after surgery, patient reported left ptosis and visual
dimness, findings suggestive of left preganglionic Horner syndrome resulting
from surgical trauma to cervical sympathetic trunk.
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Fig. 7A —64-year-old woman with paresthesia of left arm and left
ptosis with hypohidrosis and no clinical history of recent trauma. Axial
contrast-enhanced CT image at level of thoracic inlet depicts infiltrative
enhancing mass (asterisk).
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Fig. 7B —64-year-old woman with paresthesia of left arm and left
ptosis with hypohidrosis and no clinical history of recent trauma. CT image
shows mass partly encasing left subclavian artery (arrow) at level of
apex of left lung. Mass was confirmed to be squamous cell carcinoma of lung
causing clinical symptoms of Pancoast syndrome.
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Fig. 8 —41-year-old man who reported left anhidrosis and ptosis.
Patient also had left miosis but no associated symptom or sign except left
Horner syndrome of central or preganglionic type. Contrast-enhanced CT image
of thoracic inlet shows relatively well-defined homogeneous mass
(arrow) without encapsulation in left side of superior mediastinum.
Mass was attached to anterolateral aspect of T1 and T2 vertebral bodies.
Surgical excision confirmed mass as fibromatosis closely attached to
sympathetic trunk.
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Fig. 9A —53-year-old woman with right shoulder and hand pain, right
miosis, ptosis, and hypohidrosis of entire right side of face. Clinical
findings suggest tumor possibly involving brachial plexus with preganglionic
Horner syndrome. Sagittal T2-weighted MR image of brachial plexus shows
hypointense mass (asterisk) between anterior (ASM) and middle (MSM)
scalene muscles.
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Fig. 9B —53-year-old woman with right shoulder and hand pain, right
miosis, ptosis, and hypohidrosis of entire right side of face. Clinical
findings suggest tumor possibly involving brachial plexus with preganglionic
Horner syndrome. Sagittal T1-weighted image shows isointense mass
(asterisk) not clearly separated from adjacent muscles.
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Fig. 9C —53-year-old woman with right shoulder and hand pain, right
miosis, ptosis, and hypohidrosis of entire right side of face. Clinical
findings suggest tumor possibly involving brachial plexus with preganglionic
Horner syndrome. Coronal contrast-enhanced T1-weighted MR image depicts
homogeneous enhancement of mass (asterisk) infiltrating roots of
brachial plexus. Surgical finding was neurofibroma.
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On the basis of the etiologic background, there are two ways of imaging
patients with preganglionic Horner syndrome. When the presumed lesion is in
the lung, mediastinum, or anterior aspect of the neck, contrast-enhanced axial
CT is sufficient for localization of the lesion. However, when neurologic
symptoms or signs corresponding to a lesion in the cervical spinal cord or
brachial plexus are present, MRI of the cervical spinal or brachial plexus
should be considered (Figs.
9A,
9B, and
9C).
Postganglionic Horner syndrome can have causes ranging from benign to
life-threatening conditions
[1]. The lesions causing
postganglionic Horner syndrome are categorized in three ways: those in the
internal carotid artery (Figs.
10A,
10B,
10C, and
10D), those at the skull base,
and those at the cavernous sinus and orbital apex (Figs.
11A,
11B,
11C,
12A, and
12B). Carotid artery
dissection may be the most important cause of postganglionic Horner syndrome
to consider. Dissection can result from minor trauma or occur spontaneously in
patients with connective tissue disease
[5,
6]. In rare instances, carotid
artery stenting causes Horner syndrome, possibly because of arterial wall
stretch from the inserted stent
[7]. Horner syndrome
accompanied by third, fifth, or sixth cranial nerve palsy suggests the
presence of a lesion in the cavernous sinus, superior orbital fissure, or
orbital apex. Lesions of the superior orbital fissure are more likely than
cavernous sinus lesions to spare the secondary visual area. Orbital apex
lesions can be differentiated on the basis of visual loss secondary to
compromise of the optic nerve
[8].
Table 1 summarizes the
characteristics, diagnostic tests, anatomic sites, and differential diagnosis
for each type of Horner syndrome.
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Fig. 10A —48-year-old man with left occipital headache and left ptosis,
left miosis, hypohidrosis of left medial part of forehead, paresthesia of area
innervated by ophthalmic branch of left fifth cranial nerve, and decreasing
visual acuity. Neck CT angiography was performed to rule out carotid artery
dissection. Curved planar reformatted CT image shows dissection of cervical
carotid artery and hypoattenuating thrombus in false lumen
(arrows).
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Fig. 10B —48-year-old man with left occipital headache and left ptosis,
left miosis, hypohidrosis of left medial part of forehead, paresthesia of area
innervated by ophthalmic branch of left fifth cranial nerve, and decreasing
visual acuity. Neck CT angiography was performed to rule out carotid artery
dissection. Maximum-intensity-projection image of contrast-enhanced MR
angiogram on same day as A shows only mild luminal irregularity of
distal cervical internal carotid artery (arrow).
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Fig. 10C —48-year-old man with left occipital headache and left ptosis,
left miosis, hypohidrosis of left medial part of forehead, paresthesia of area
innervated by ophthalmic branch of left fifth cranial nerve, and decreasing
visual acuity. Neck CT angiography was performed to rule out carotid artery
dissection. Axial source image of neck CT angiogram shows low-attenuating
thrombus (arrow) in false lumen.
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Fig. 10D —48-year-old man with left occipital headache and left ptosis,
left miosis, hypohidrosis of left medial part of forehead, paresthesia of area
innervated by ophthalmic branch of left fifth cranial nerve, and decreasing
visual acuity. Neck CT angiography was performed to rule out carotid artery
dissection. Axial T2-weighted MR image shows hyperintense thrombus
(arrow) in false lumen.
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Fig. 11A —67-year-old woman with right ptosis, diplopia, and miosis.
(Reprinted from [9]) Axial
T2-weighted image shows large signal void (arrows) due to aneurysms
of internal carotid arteries in both cavernous sinuses.
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Fig. 11B —67-year-old woman with right ptosis, diplopia, and miosis.
(Reprinted from [9]) Coronal
contrast-enhanced T1-weighted image shows crescent isointense thrombus
(arrows) in right aneurysm and intense enhancement of left
aneurysm.
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Fig. 11C —67-year-old woman with right ptosis, diplopia, and miosis.
(Reprinted from [9]) Digital
subtraction angiogram of both internal carotid arteries shows partially
thrombosed aneurysms of internal carotid artery of right cavernous sinus
(long arrow) and another aneurysm of internal carotid artery of left
cavernous sinus (short arrows).
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Fig. 12A —50-year-old man with right facial pain. Neurologic
examination revealed right miosis, ptosis, and palsy of sixth and maxillary
branch of fifth cranial nerves. Coronal T2-weighted image shows homogeneous
infiltrating lesion (arrow) in right anterior cavernous sinus.
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Fig. 12B —50-year-old man with right facial pain. Neurologic
examination revealed right miosis, ptosis, and palsy of sixth and maxillary
branch of fifth cranial nerves. Contrast-enhanced axial T1-weighted image
shows homogeneous intense enhancement (arrow) of infiltrating lesion.
Tolosa-Hunt syndrome was confirmed.
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TABLE 1: Summary of Characteristics, Diagnostic Tests, Anatomic Sites, and
Differential Diagnosis of Types of Horner Syndrome
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Conclusions
Horner syndrome is usually associated with unique clinical features based
on the anatomic location of the underlying pathologic process. In most cases,
imaging of the sympathetic pathway according to the symptoms is warranted.
Understanding the clinical features of the three types of Horner syndrome and
their implications assists in localization of the underlying pathologic
process and choice of imaging technique for the differential diagnosis of this
complex entity.
Acknowledgments
We thank Eun Ja Yoon for help in preparing this article.
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Abstract
Introduction
