Pictorial Essay
Neuroradiology
January 2007

Neuroimaging Strategies for Three Types of Horner Syndrome with Emphasis on Anatomic Location

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.

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].
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.
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].
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.
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.
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.
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.
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.
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).
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].
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.
Fig. 6A 22-year-old man with palpable neck mass. Coronal T2-weighted MR image of neck shows well-defined, ovoid hyperintense mass compressing medial aspect of prevertebral muscle.
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.
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).
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.
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.
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.
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.
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.
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.
TABLE 1: Summary of Characteristics, Diagnostic Tests, Anatomic Sites, and Differential Diagnosis of Types of Horner Syndrome
CharacteristicsDiagnostic TestsAnatomic SitesDifferential Diagnosis
Central subtype   
   Occurs uncommonly in isolation, usually one of a constellation of neurologic findingsCocaine test (+)Hypothalamus, thalamus, brainstemIschemia, tumor, hemorrhage, demyelination
 Hydroxyamphetamine test (+)Cervical spinal cord 
Preganglionic subtype   
   Most often caused by trauma or tumor, including malignant tumorsCocaine test (+)Cervicothoracic spinal cordTrauma
 Hydroxyamphetamine test (+)Brachial plexuslatrogenic injury (obstetric, surgical)
  Anterior aspect of neckTumor (apical lung cancer, thyroid and mediastinal tumor)
  Mediastinum 
Postganglionic subtype   
   Variable causes from benign to life-threateningCocaine test (+)Superior cervical ganglionTrauma including iatrogenic injury
 Hydroxyamphetamine test (–)Internal carotid arterySkull base tumor
  Cavernous sinusCarotid artery dissection
  Orbital apexCarotid aneurysm
   Carotid–cavernous fistula
   Inflammation (Tolosa-Hunt syndrome)



Cavernous sinus thrombophlebitis
Note—Plus sign (+) = positive result, minus sign (–) = negative result
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).
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).
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.
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.
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.
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.
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).
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.
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.

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.

Footnotes

Presented at the 2004 Meeting of Radiological Society of North America. 138-736, Seoul, South Korea. Address correspondence to J. H. Lee ([email protected]).
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References

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Information & Authors

Information

Published In

American Journal of Roentgenology
Pages: W74 - W81
PubMed: 17179330

History

Submitted: September 7, 2005
Accepted: November 3, 2005

Keywords

  1. CT
  2. Horner syndrome
  3. MRI
  4. neuroimaging

Authors

Affiliations

Jeong Hyun Lee
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.
Ho Kyu Lee
Department of Radiology, University of Iowa Hospitals and Clinics, Iowa City, IA 52242.
Deok Hee Lee
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.
Choong Gon Choi
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.
Sang Joon Kim
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.
Dae Chul Suh
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.

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