Diagnostic imaging in neuro-ophthalmology

Radiología. 2018;60(3):190---207

www.elsevier.es/rx

UPDATE IN RADIOLOGY

Diagnostic imaging in neuro-ophthalmology�

A.C. Vela Marín ∗, P. Seral Moral, C. Bernal Lafuente, B. Izquierdo Hernández

Servicio de Radiodiagnóstico, Hospital Universitario Miguel Servet, Zaragoza, Spain

Received 2 January 2017; accepted 14 November 2017

KEYWORDSOrbit;Visual pathways;Ophthalmologicimaging techniques;Ocular diseases

Abstract Neuro-ophthalmology is a field combining neurology and ophthalmology that studiesdiseases that affect the visual system and the mechanisms that control eye movement andpupil function. Imaging tests make it possible to thoroughly assess the relevant anatomy anddisease of the structures that make up the visual pathway, the nerves that control eye and pupilmovement, and the orbital structures themselves. This article is divided into three sections(review of the anatomy, appropriate imaging techniques, and evaluation of disease accordingto clinical symptoms), with the aim of providing useful tools that will enable radiologists tochoose the best imaging technique for the differential diagnosis of patients’ problems to reachthe correct diagnosis of their disease.© 2018 SERAM. Published by Elsevier Espana, S.L.U. All rights reserved.

PALABRAS CLAVEÓrbita;Vías visuales;Técnicas de imagenoftalmológicas;Enfermedadesoculares

Diagnóstico por la imagen en neuroftalmología

Resumen La neuroftalmología es la parte de la neurología y la oftalmología que se encargadel estudio de las enfermedades que afectan al sistema visual y a los mecanismos que controlanla motilidad ocular y la función pupilar. Las pruebas de imagen permiten realizar una adecuadavaloración anatómica y patológica de las estructuras que conforman la vía visual, los nerviosque controlan la motilidad ocular y pupilar, y las propias estructuras orbitarias. Este artículose divide en tres apartados (recuerdo anatómico, técnicas de imagen apropiadas y valoraciónpatológica en función de la sintomatología clínica) con el propósito de proporcionar herramien-tas útiles que permitan al radiólogo elegir en cada momento la técnica de imagen más adecuadapara el correcto diagnóstico de las enfermedades y un ajustado diagnóstico diferencial.© 2018 SERAM. Publicado por Elsevier Espana, S.L.U. Todos los derechos reservados.

� Please cite this article as: Vela Marín AC, Seral Moral P, Bernal Lafuente C, Izquierdo Hernández B. Diagnóstico por la imagen enneuroftalmología. Radiología. 2018;60:190---207.

∗ Corresponding author.E-mail address: [email protected] (A.C. Vela Marín).

2173-5107/© 2018 SERAM. Published by Elsevier Espana, S.L.U. All rights reserved.

Document downloaded from http://www.elsevier.es/, day 08/05/2019. This copy is for personal use. Any transmission of this document by any media or format is strictly prohibited.Document downloaded from http://www.elsevier.es/, day 08/05/2019. This copy is for personal use. Any transmission of this document by any media or format is strictly prohibited.

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Diagnostic imaging in neuro-ophthalmology 191

a

III

III

II

IV

IV

VI

VI

V1V2

b

c

d

e

f

g

h

Figure 1 (a) Drawing representing the optic pathways. (b) Drawing showing the location of the nuclei of the oculomotor cranialpairs relative to the mesencephalon and the pons. (c) Schematic drawing of the correlations of the cranial pairs with the cavernoussinus and the intracavernous internal carotid artery. a: Retina; b: optic nerve; c: optic chiasm; d: optic tract; e: lateral geniculateganglion; f: inferior geniculocalcarine tracts or Meyer’s loop; g: superior geniculocalcarine tracts; h: occipital cortex; II: optic nerve;III: common oculomotor nerve; IV: trochlear nerve; VI: abducens nerve; V1: first branch of the trigeminal nerve; V2: second branchof the trigeminal nerve.

Introduction

The pathology of optic pathways and the orbital structuresvaries widely, but it has little global incidence, therefore itsstudy and assessment represent a small volume of cases ina radiologist’s standard practice, making it a not very well-known condition and, at times, difficult to manage. Thatis why it is useful to review the anatomy (Fig. 1), exposewhich are the imaging modalities suitable for its evalua-tion and make the right differential diagnosis based on thesymptoms.

Visual pathways

There are photoreceptors, cones and rods in the retinain charge of making the synapses with the first neuronsor bipolar cells, and in turn these make second synapseswith ganglion cells, whose axons make up the optic nervefibers.1 The nasal hemiretina receives information fromthe temporal visual field, and the temporal information isreceived from the nasal visual field. There also occurs asuperior---inferior crossing, so that the information from thesuperior visual field is collected by the inferior hemiretinas,and vice versa.1,2 The optical nerve runs through the orbitand into the skull via the optic foramen. It is surroundedby meningeal layers in continuity with the intracranialmeninges and by cerebrospinal fluid.

The intracranial segments of both optic nerves convergeforming the optic chiasm. The temporal fibers of each retina(nasal visual fields) remain on the same side (homolat-eral), and the medial ones (temporal visual fields) decussatetoward the contralateral side. Only one half the macu-lar fibers decussate; the rest remain on the homonymousside.1,3

The optic tracts start from the chiasm and, surroundingthe mesencephalon, reach the lateral geniculate body, thethalamic nucleus located behind the pulvinar nucleus.

The geniculo-calcarine tracts (optic radiations) connectthe lateral geniculate nuclei with the visual cortex. Thesuperior axons relay information from the inferior visualfields, run lateral to the atrium and the posterior horn ofthe lateral ventricle, pass through the parietal white matterand reach the occipital cortex on the calcarine sulcus. Infe-rior fibers, with information from the superior visual fields,curve antero-laterally, pass through the caudal portion ofthe internal capsule, continue along the temporal whitematter (Meyer’s loop) surrounding the temporal horn of theventricle, and posteriorly aim at occipital cortex locatedunder the calcarine sulcus3,4 (Table 1).

Oculomotor nerves

The nuclei of the common oculomotor nerve or third cranialnerve (CN III) are located in the periaqueductal region of themesencephalon at the level of the superior quadrigeminal


192 A.C. Vela Marín et al.

Table 1 Scheme-summary of the direction of the visual pathways.

Visual field Hemiretina Chiasm Tract Geniculate ganglion Opticradiations

Occipital cortex

Temporal Nasal Cross Contralateral Contralateral Contralateral ContralateralDirect

Nasal Temporal Homolateral Homolateral Homolateral HomolateralSuperior Inferior Includes

Meyer’s loopInferior to the calcarine sulcus

Inferior Superior Superior to the calcarine sulcusMacula Cross Both sides of the calcarine sulcus

Direct

tubercles. A single central nucleus innervates both elevatingmuscles of the eyelid, the medial and inferior rectus mus-cles and the inferior oblique muscles are innervated fromthe homolateral nuclei, and the superior rectus muscles areinnervated from the contralateral ones. The nerve leavesthe mesencephalon via the interpeduncular cistern, runsthrough the superior cerebellar and posterior cerebral arter-ies running through the dural walls of the cavernous sinus,to reach its final destination on its superior edge.3---6

The nucleus of the CN IV (trochlear nerve) is in the mes-encephalon, of inferior location to the CN III nucleus, behindthe medial longitudinal fasciculus (MLF). Its fibers decussatein the mesencephalon and innervate the contralateral supe-rior oblique muscle. The nerve emerges to the subarachnoidspace at the level of the inferior quadrigeminal tubercles,running anteriorly through the ambient cistern between themesencephalon and the tentorium. It runs through the duralwalls of the cavernous sinus inferiorly to the CN III.3---6

The nucleus of the CN VI (abducens) is located in thedorsal region of the pons, in front of the floor of the fourthventricle, and adjacent to the MLF. The majority of its fibersinnervate the homolateral lateral rectus muscle, but a smallgroup of axons run, via the MLF, to the contralateral nucleus,providing innervation for the lateral rectus on the other sidetoo. The nerve emerges through the inferior side of the pons,ascends behind the clivus, enters the cavernous sinus, andruns inside the venous plexuses.3---6 After exiting the cav-ernous sinus, it reaches the orbit through the sphenoidalfissure. The first and the second branches of the trigeminalnerve also pierce the dural walls of the cavernous sinus.4

The MLF runs along the anterior side of the mesen-cephalic aqueduct up to the anterior cord of the spinal cord.It is made up of association fibers that connect the motornuclei of the homolateral CN III, IV, VI and XI, and each CNVI with the contralateral CN III. This structure is essential tocoordinate the horizontal conjugate gaze.3,6,7 The MLF, theinterstitial cells of Cajal and the CN III and IV participate inthe coordination of the vertical gaze.6,7

Sympathetic and parasympathetic pathways

The Edinger---Westphal parasympathetic nucleus is locatedposterior to the CN III nucleus. It is made up of pregan-glionic parasympathetic neurons whose axons join the CNIII fibers on their way toward the orbit. These fibers are in

the periphery of the nerve. Inside the orbit they run towardthe ciliary ganglion, from which the postganglionic fibersemerge to innervate the constricting muscles of the pupiland the muscle of the ciliary bodies.3,4,6,7

The sympathetic pathway is made up of three groups ofneurons. The first neuron is located in the hypothalamus andits axons descend to the levels of C8-D2 of the spinal cord,where they meet the second neuron. From that location, thesympathetic pathway ascends to the superior cervical gan-glion while running proximal to the carotid bifurcation. Thethird neuron is in this ganglion and its axons ascend, alongwith the adventitia of the internal carotid artery, toward thecavernous sinus, joining the first branch of the trigeminalnerve and aiming for the orbit.3,4,6---8

Imaging modalities

Simple skull X-ray

The only indication of skull X-rays today is to confirm thepresence of intraorbital or intracranial ferromagnetic for-eign bodies, whose presence can contraindicate performinga magnetic resonance imaging (MRI) due to risk of mobiliza-tion.

Orbital ultrasound

Ultrasound performed with high frequency transducers,7 mHz or more----it is the modality of choice to assess theocular globe.9---12 The globe is examined correctly throughophthalmoscopy, but in the presence of cataracts, vitreoushemorrhages, etc., which prevent seeing through, ultra-sound can be of great help.11,13 It is especially useful inpediatrics, since it does not require sedation and can be usedin the evolutionary control of the response to the treatmentof some tumors.11,13

Doppler is useful in the assessment of alterations in flowdynamics and it allows the characterization of some vascu-lar lesions. It can be used in the non-invasive assessment ofcarotid-cavernous fistulas, in which it is possible to observethickening of an ophthalmic vein with inversion of flow direc-tion and arterializations thereof (Fig. 2); it is useful forboth the diagnosis prior to arteriography and the follow-up



Figure 2 Carotid-cavernous fistula. Forty-eight-year-old woman who, after falling down the stairs, presents with progressive leftexophthalmos and palpebral swelling. The Color Doppler ultrasound (a and b) shows the thickening of the superior ophthalmic veinwith arterialized flow. Coronal (c) and axial (d) slices of orbital CT scan without contrast showing thickening of the left extraocularmuscles due to congestive edema and thickening of the superior ophthalmic vein (arrow); compare with the contralateral one.Arteriographic confirmation was made and treatment administered through embolization with no success, and later closure ofcarotid above and below the fistula.

of those with low flow in which a decision is made not tointervene.14

Computed tomography and magnetic resonanceimaging

They are the main imaging modalities for orbital andintracranial study.

Computed tomography (CT) provides more informationon the bony walls of the orbit, it visualizes calcificationsclearly and it is the imaging modality of choice in thepresence of ferromagnetic intraorbital foreign bodies thatcontraindicate the use of MRI.15 Since it is fast and iswidely available, it is the modality indicated in emergencycontexts. The sequential study of the skull provides thenecessary information in cases of urgent vascular and trau-matic encephalic pathology.16 Acquisition on multi-slice CTmachines with reformatting on the coronal and sagittalplanes allows a comprehensive assessment of facial andorbital traumatic lesions.

MRI provides greater anatomic resolution and better tis-sue characterization, and good assessment of the signaldifferences among the different tissues; therefore, it is ofchoice in orbital studies.17 If it cannot be conducted, it canbe replaced by the CT scan with sufficient diagnostic guar-antees on most occasions. It can be conducted with skull orsurface antennas17; the latter provide better signal/noise

relation, providing excellent anatomic details of the ocularglobe during the examination, yet they are not enough toassess the orbital apex and the intracranial spread of thelesions.

The correct assessment of the hypothalamus-hypophyseal region as well as the study of brain structuresshould be conducted through an MRI. The protocols willdepend on the anatomical area studied.18

Cranial CT-angiography or MRI are indicated in cases ofsuspicion of aneurysms or vascular malformations.

Table 2 shows the CT and MRI study protocols used in ourcenter.

Arteriography

Arteriography maintains its indication in selected casesof aneurysms, carotid-cavernous fistulas, varices or vascu-lar malformations that require diagnostic confirmation andtherapeutic procedures.19 In highly vascularized orbital andintracranial tumors its partial embolization can prove ben-eficial prior to surgery.

Clinical indications of imaging modalities

The first neurophthalmological goal is the clinical locationof the lesion. The different symptomatology allows locat-ing the origin of the pathology in each anatomic region and



Table 2 CT scan and MRI protocols in the neuro-ophtalmology unit at the Hospital Universitario Miguel Servet, Zaragoza, Spain.

CT-scan protocol

Sequential CT-scan Helical CT-scan Angio-CT-scan

Brain structures Orbit and facial structures Cerebral and supra-aortic trunksReconstruction Reconstruction:

Slice thickness: 5---8 mm Slice thickness: 0.5---1 mm Slice thickness: 0.5---1 mmAdvance: 5 mm Interspace: 0.3---0.8 mm Interspace: 0.3---0.8 mmAlgorithm: brain and bone Algorithm: soft tissues and bone Algorithm: soft tissues and bone

Reformatting: axial, sagittal and coronalMPR

Reformatting: axial, sagittal andcoronal MIP

(1---2 mm every 2 mm) (7---10 mm every 5---8 mm)Administration of contrast: Administration of contrast: Administration of contrast:Tumor, infectious or

vascular pathologyTumor, infectious or vascular pathology 50 cc high concentration at 5 ml/s

50 cc physiological saline solution

MRI protocol

Cranial MRI Orbital MRI Hypophyseal MRI

Skull (orbit) or surface (balloon) antennaT1 Axial T1 Sagittal and coronal T1FLAIR T2 Axial T2FS Sagittal and coronal T1 with gadoliniumDiffusion (factor B: 1000) Coronal STIR Coronal T2Gradient Echo: T2*, SWI T1FS with gadolinium (axial, coronal, sagittal)

Slice thickness: 2---3 mm Slice thickness: 2---3 mmMatrix: 256 × 256; 512 × 512 Matrix: 256 × 256

Complementary sequences: Complementary sequences: Complementary sequences:3D SS Coherent: cranial pairs Dynamic fast SPGR FS: 3DT1 with gadoliniumAngio-MRI 3D TOF: aneurysms Tumors vascular lesions T2 sagittal3DT1 with gadolinium Diffusion SE, EPI, T2* calcifications

CT machine: Toshiba Aquilion 64. Toshiba Medical Systems.MRI machine: Signa Excite 1.5. General Electric Healthcare. Milwakee. Wisconsin, USA.EPI: echo-planar imaging; Fast SPGR: fast spoiled gradient; FS: fat sat (fat saturation); MIP: maximum intensity projection; MPR: multi-plane reformatting; SE: spin echo; SS coherent: steady state coherent; STIR: short tau inversion recovery; SWI: susceptibility-weightedimaging; T2*: weighted gradient echo in T2; TOF: time of flight.

Table 3 Indications of the imaging modalities in neuro-ophthalmology based on anatomical areas and pathology.

Ocular globe Choice Ultrasounda

Foreign body/calcifications CT-scana

Soft tissues MRIa

Trauma, foreign body, CT-scana

bony lesions, calcifications MRIGraves’ disease

Orbit (optic nerve) Exophthalmos, suspicion of tumors MRIa

CT-scanAlteration of flow dynamics Dopplera

ArteriographyCT-scan/MRI

Sellar and parasellar region MRIa

Chiasm (hypothalamus-hypophyseal region) Base of skull CT-scana

Vascular pathology Angio-CT scan/MRIa

Retrochiasmatic pathways MRIa

Posterior fossa Emergency CT-scana

a Modality of choice.



choosing the right imaging modality; it is possible to make ageneric division of the ocular globe, orbit, parasellar region,middle cranial fossa and posterior cranial fossa. Table 3 indi-cates the most appropriate imaging modalities to be used ineach region. On many occasions, the use of one modalitydoes not exclude the others, and findings often complementone another to be able to reach diagnosis.

Pathology of the ocular globe

Doppler ultrasound is the best screening technique of ocularglobe pathology, indicated to differentiate retinal detach-ment from vitreous hemorrhages, which are sometimes hardto assess through ophthalmoscopy.11,20 It is simple and easyto manage when trying to find foreign bodies, althoughextreme caution should be exercised if ocular globe rup-ture is suspected, since pressure on the ocular globe withthe transducer could cause the extrusion of its content. Inthese cases, it is better to perform a CT-scan,10,12,20 that alsoallows us to assess, with high sensitivity, foreign bodies ofdifferent materials as well as the condition of the remainingorbital structures.20

Ultrasound provides higher spatial resolution than MRIwhen looking for small ocular tumors, but the MRI is moreprecise for the assessment of sclerotic infiltration andretrobulbar tumor spread.12,21

The most common intraocular tumor in pediatric age isretinoblastoma (Fig. 3), whose characteristic clinical signis leukocoria. Calcifications are present in up to 90---95 percent of retinoblastomas,13,22,23 in general in the posteriorportion of the globe. Both the ultrasound and the CT scanare highly sensitive to detect them, identifying calcifica-tions of 2 or more mm in thickness. However, the MRI showsbetter the tumor characteristics, the retrobulbar infiltra-tion and the spread of the disease to the central nervoussystem, as well as the presence of associated pineal orsuprasellar retinoblastomas.22,24 Today, despite its high sen-sitivity, the orbital CT scan is not adviseable considering thehigh radiation that it would mean for the orbit of pediatricpatients.24 There are studies that show that the combinationof ophthalmoscopy, ultrasound and MRI manages to detectcalcifications with the same percentage as CT-scan.23 Themost sensitive MRI sequence for the detection of calcifi-cations is the T2-weighted sequence*.23 Recent researchsupports the utility of diffusion sequences in the diagno-sis of retinoblastomas, since they show greater restriction

Figure 3 Retinoblastoma. Ocular ultrasound (a) and T2 axial slice with fat saturation (b) in a two-month-old infant with leukocoria.The ultrasound shows one lobulated, heterogeneous mass, with hyper-refringent images indicative of calcifications. The T2 the imageis highly hypointense. Both modalities rule out retrobulbar invasion. Bilateral retinoblastoma. T2 axial slices with fat saturation (c)and T1 with fat saturation with gadolinium (d) in a nine-month-old infant with right leukocoria. Right intraocular lesion hypointensein T2 with homogeneous enhancement after the administration of gadolinium, that produces retinal detachment without invasionof retrobulbar structures. It is possible to observe a small image in the left ocular globe with similar characteristics in the nasalregion (arrow).



Figure 4 Melanoma. Ocular ultrasound (a) and T2 axial slice with fat saturation (b) in a 58-year-old male who presented to theER with blurry vision. Ophthalmoscopy revealed one slightly pigmented, elevated peripapillary mass. The ultrasound reveals onesmall lenticular mass with the choroidal excavation sign (arrows), and the T2 MRI slice shows the hypointense lesion adjacent to thepapilla. Melanoma. T1 (c) and T2 axial slices with fat saturation (d) of a 73-year-old patient with one prominent mass in the lowerquadrants revealed by the ophthalmoscopy. On the MRI, the lesion shows the characteristics typical of melanomas, hyperintense inT1 and hypointense in T2.

to diffusion than other ocular lesions, and also allow us tomonitor the response to treatment by differentiating viabletumor tissue from necrotic tissue.25,26

Choroidal melanoma as primary tumor (Fig. 4) and metas-tasis (breast and lung, mainly) are the most common oculartumors in the adult population,10,11,27,28 but other lesionscan appear, such as hemangiomas, hemangioblastomas orgranulomatous lesions. The ultrasound is very sensitive forthe detection of small tumors, but the MRI is the modalityof choice for its study, since it contributes some characteris-tic details and allows assessing whether there is extraocularspread.

On the ultrasounds, melanomas look hypoechogenic withthe sign of choroidal excavation, characteristic (though notalways present) and indicative of local invasion. By applyingDoppler, they show high vascularization.10,27 Metastases arehyperechogenic, with greater vascularization in the Dopplerstudy, and they can be multiple. The most significant char-acteristic of melanomas on the MRI is hyperintensity on T1and hypointensity on T2, due to its melanin content: themore melanin content, the higher the signal intensity is onthe T1-weighted image, and according to some authors, thisleads to worse prognosis.17 Amelanotic melanomas do notshow hyperintensity on T1, which makes it hard to make adifferential diagnosis with other tumors.29 Metastases arenot visualized as hyperintense on T1 unless there is a hem-orrhagic component or high mucoid content inside them.27

Research conducted with diffusion shows great diffusion

restriction, with a reduced apparent diffusion coefficient inmelanomas with respect to other lesions. Since today thetreatment of choice is radiosurgery, monitoring the appar-ent diffusion coefficient in serial studies allows us to assesshow the response to treatment really is.30

The presence of drusen in the optic nerve head can causeelevation of the papilla and blurring of its edges, and onthe ophthalmoscopy it can be mistaken for papillary edema.Both on the ultrasound and the CT scan, asymmetrical bilat-eral or unilateral calcified nodules can be observed.11,12,20

Optic neuritis

Optic neuritis is a clinical diagnosis that leads to the uni-lateral loss of vision, pain, afferent pupillary defect andcampimetric defect.7 Imaging tests of the optic nerve shouldbe conducted whenever there is indication of optic neuritisthat cannot be explained by glaucoma, ischemia or toxic,metabolic, infectious or hereditary causes.31

Since optic neuritis can be the initial manifestation in15---25 per cent of the patients with multiple sclerosis, andup to 75 per cent of these patients will have at least oneepisode of optic neuritis, the cranial MRI is recommendedin young patients with acute retrobulbar optic neuritis whodo not show the above mentioned etiologic factors, seekinglesions typical of demyelinating disease.31 Brain MRI is thebest isolated test to assess risk of future multiple sclerosis



Table 4 Causes for compressive optic neuropathy (orbit).

Thyroid orbitopathy

Tumor/infiltration of nerve

Tumor: Optic nerve glioma Inflammatory: SarcoidosisOptic nerve sheath meningioma Inflammatory pseudotumorLymphoproliferative syndromes

Intraconal masses

Vascular: Cavernous vascular malformationa Inflammation/infectionVenolymphatic malformationb Inflammatory pseudotumorOrbital varicose vein Granulomatous polyangiitisc

High flow arteriovenous malformation Orbital cellulitisTumors: Leukemia/lymphoma Orbital abscess

Cranial spread of meningiomaIntracranial hypertension

Traumas Direct Optic nerve avulsion and lacerationd

Indirect Perineural hematomaa Also known as cavernous hemangioma.b Also known as cystic lymphangioma.c Formerly known as Wegener’s granulomatosis.d It is not cause for compressive optic neuropathy as such, but the lesion includes nervous fiber tears.

a

I.VP:120

FOV 13.0 cm

70s

mA:200

mAs:100Thk:0.5 mmAquilion P

2

R

2

msec:500

d e

b

c

Figure 5 Orbital trauma. Axial slice with bone window (a) and sagittal reformatting with soft tissue algorithm (b and c) in a26-year-old woman with facial trauma after a recent traffic accident. She had multiple fractures in her left maxillary sinus andorbit, with multi-fragmented fracture in her orbital roof, revealing one fragment (arrow) in the optic foramen that caused anirreversible lesion of the optic nerve despite urgent treatment. Orbital trauma. Axial slice (d) and sagittal reformatting (e) of CTscan performed on an 80-year-old woman after falling down the stairs, with periorbital hematoma and limitation of ocular motility.Thickening and fraying of retrobulbar and perineural fat compatible with hematoma, which was immediately drained.



and help in the decision of prescribing immunomodulatorytherapy.32,33

The risk of developing the disease is up to 38 per centat 10 years and 50 per cent at 15 years in patients withhyperintense lesions on the MRI.31,33,34 The risk of developingthe disease with a normal MRI is much less, 22 per cent at10 years.32,34

Compressive optic neuropathy

It usually starts with slow and progressive loss of vision. Itcan be due to thyroid ophthalmopathy due to intraorbitalspace involvement, to the compression of the optic nervefibers due to tumor or infiltrative causes of the nerve itself,or to lesions occupying the intraconal space4,7,35,36 (Table 4).

Increase of intracranial pressure, whether tumor or idio-pathic, causes an increase of the cerebrospinal fluid in theoptic nerve sheath and the compression of its fibers withvision alterations.37,38

Damage is generally unilateral, with loss of the monoc-ular visual field, except in the thyroid ophthalmopathy andcranial hypertension, where it is usually bilateral.35

Traumas can cause acute decrease of vision due to anoptic nerve lesion of a direct cause, avulsion of the opticnerve itself, laceration by bony fragments, compression, orintraorbital hematomas in the nerve sheath39 (Fig. 5). Braincontusions in the frontal lobes can also damage the opticnerves in their intracranial trajectory.35

The MRI is the modality of choice for the assessment ofthe orbit, due to its greater capacity to discriminate softtissues.17,40 The T1-weighted sequence is essential, sincemost orbital lesions are hypointense with respect to fat,which allows the adequate assessment of their edges. T2and T1 sequences with gadolinium, with or without fat sup-pression, provide differentiating data about some tumors(Fig. 6).

Diffusion sequences can help differentiate some orbitaltumors. Some studies have proven that optic nervegliomas show apparent diffusion coefficient values that

Figure 6 Optic nerve glioma. T2 axial slices with fat saturation (a) and T1 with fat saturation with gadolinium (b) in a patient withreduced visual acuity and papillary edema. Fusiform thickening of the right optic nerve that impacts on the papilla, hyperintense inT2 with homogeneous enhancement after contrast administration. Optic nerve sheath meningioma. T1 axial slice with fat saturation(c) with gadolinium and T1 sagittal slice with fat saturation (d) in a young man with slow, progressive loss of vision and signs ofsevere left neuropathy in evoked potentials. Tubular thickening of the left optic nerve sheath that surrounds and constricts the nerveand enhances intensely with gadolinium, spreading through the orbital foramen to the middle cranial fossa (arrow). Venolymphaticmalformation. T2 axial slices with fat saturation (e) and T1 (f) in a 2-year-old girl with right ocular proptosis. Right orbital masswith intraconal and extraconal component, with cystic images and fluid/fluid levels due to the hemorrhagic component of the cysts.Cavernous vascular malformation. T2 axial slice with fat saturation (g) and T1 sagittal slice with fat saturation with gadolinium (h)in a 60-year-old patient with reduced visual acuity in his left eye. Rounded, well-established mass in the orbital apex, hyperintensein T2 and intensely enhanced in the slice with contrast that compresses the optic nerve.



Table 5 Causes for diplopia.

Restrictive diplopia (orbit)Trauma Other muscular alterations:

Thyroid orbitopathy MyositisInflammatory pseudotumor Muscular tumors (metastasis)

Congenital (Brown’s syndrome)Inflammatory (secondary Brown’s syndrome)

Neurological diplopia (cranial pairs)CNS (Nuclei of CN and MLF)

IschemiaHemorrhageNeoplasmInflammatory (multiplesclerosis)

Nerve (trajectory):

CongenitalVascular Nerve microvascular ischemia

Compression (blood vessel,aneurysm, pathology ofcavernous sinus)

Tumor---

Trauma

Schwannoma (nerve)Bone tumors (chordoma)Intracranial tumors (meningioma)Intraorbital tumorsMost common cranial nerves VIand IV

Inflammatory Sarcoidosis Benign intracranial hypertensionOther granulomatousTolosa Hunt Syndrome

CNS: central nervous system. MLF: medial longitudinal fasciculus. MS: multiple sclerosis.

are significantly lower than meningiomas.17 Also, lympho-proliferative diseases (lymphoma) cause greater diffusionrestriction than inflammatory diseases (inflammatorypseudotumor).41,42

The CT scan is more useful for the assessment of bonyalterations, being the modality of choice in orbital traumasand for the detection of calcifications (present in up to 33per cent of nerve sheath meningiomas)17 or phleboliths incavernous hemangiomas and lymphangiomas.

The presence of bilateral papilledema requires an urgentCT scan in order to seek intracranial massess or hydro-cephaly as causes of the cranial hypertension. In the absenceof findings, the angio-CT can be indicated to rule out throm-bosis of the venous sinus.7,43

Diplopia

Binocular diplopia occurs as a result of misalignment of thevisual axes, resulting in the images coming from each eyenot fusing in the brain and thus originating double vision. Itcan have a restrictive cause and then the lesion is located inthe orbit, or a nervous cause with the lesion located in theCN nuclei or their trajectory, whether due to nerve intrinsicpathology or compression in its trajectory through the basalcisterns44,45 (Table 5).

Restrictive diplopia

Thyroid ophthalmopathy and traumas are the most commoncauses of restrictive diplopia.

Thyroid ophthalmopathy (Fig. 7) starts with extraocularmuscle enlargement, usually bilateral, but asymmetrical.The muscles most commonly affected are the internal andinferior rectus muscles, and more rarely the lateral rectusmuscle.36,45

The orbital CT scan is included in most thyroid oph-thalmopathy diagnostic protocols.36,46 Axial slices assessthe degree of exophthalmos and the increase of orbitalfat; coronal slices are essential to compare the volume ofhomonymous muscles in both eyes and their size variationsin serial controls, as well as to monitor the response totreatment. The CT scan makes adequate assessments of theorbital walls before planning decompressive surgery.36,40,46

The administration of iodinated contrast is not useful andshould be avoided.16,47

The MRI allows us to differentiate the acute from thechronic stages of the disease. In the acute stage, muscu-lar edema causes hypersignal on the T2-weighted sequenceswith fat suppression and STIR, and in the fibrosis stage, themuscles are hypointense in T1 and T2, with hyperintense fociin T1, representative of fat infiltration.40,46 A good correla-tion between the signal pattern in T2 and the reversibilityof diplopia has been described, when seeing how the caseswith homogeneous hypersignal show better responses totreatment than whenever the signal is hypointense andheterogeneous.48

Orbital wall fractures, especially those on the orbitalfloor or the lamina papyracea (blow-out), can cause ocu-lar movements restriction, and therefore diplopia due toedema or hemorrhages in the orbital fat that pulls from the



Figure 7 Thyroid orbitopathy. Coronal (a and b) and axial slices (c and d) of CT scan without contrast in a 43-year-old womanwith hyperthyroidism. Fusiform thickening of the bilateral and asymmetric extraocular muscles, especially of the inferior recti and,to a lesser extent, of the left medial and right lateral rectus. We can also see the inflammatory infiltration of intraconal fat. T1and T2 axial slices with fat saturation (e and f) and T1 orbital and coronal slices with gadolinium of hypophysis (g) in a patient withhyperthyroidism. Fusiform thickening of left internal rectus muscle with hypersignal in T2 sequence with fat saturation, hypersignalthat is also observed in the right medial rectus, indicative of the acute stage of the disease. As an incidental finding, there is onehypophyseal macroadenoma that superiorly displaces the chiasm.

muscle, also muscle swelling or herniation of the muscularcenter through the fracture (in general of the inferior rec-tus). This is why it is crucial to assess the condition of theextraocular muscles in the CT scans of patients with facialtraumas.49 The coronal plane provides more information forthe detection of muscle herniations (Fig. 8) and it is essentialwhen making the decision of conducting urgent or delayedsurgery.50,51

Other damage to the extraocular muscle can cause move-ment restriction and diplopia. The differentiation is basedmainly on the morphological assessment of the lesions.40

Nervous diplopia

Diplopia due to paralysis of a CN can be due to ischemia inthe vasculature of the nerve itself or to small infarctions inthe mesencephalic nuclei, due to trauma, aneurysms in the

circle of Willis arteries or neoplasms that can compress thenerves along their trajectory.45,52---54

The isolated paralyzes of some CN in patients over 50years old with a history of diabetes, high blood pressureor vascular diseases are usually of microvascular origin andthere is no need to conduct imaging modalities.43,53,55---57

They are usually resolved completely in less than 3 months.If they are not resolved or if we are dealing with a youngpatient without vascular risk factors, neuroradiological testsare indicated, being the MRI the modality of choice58

(Fig. 9a---c). In such case, it would be good to administercontrast.43

CN IV, due to its length, and CN VI, due to its ascendingtrajectory posterior to the clivus, are vulnerable to cranialtraumas.43,45,54 Bilateral damage to the CN VI can be due tocranial hypertension or tumor-related compression.43,53 Theinitial imaging modality is the CT scan, since these patientsare usually under urgent examination.



Figure 8 Blow-out fracture of lamina papyracea with muscle herniation. Axial (a) and coronal (b) CT slices and T1coronal slices(c and d) in a 13-year-old girl who, after suffering a head trauma following run over accident, presents complete adduction andpartial abduction deficits in her left eye with diplopia. The CT slices show the fracture line in the lamina papyracea, occupation ofthe middle ethmoidal cell, and irregular morphology of the internal rectus muscle on her left side. The MRI slices show the changein shape and orientation of the internal rectus muscle with respect to the contralateral one, with ‘‘bow-tie’’ morphology due tomuscle herniation in the ethmoidal cell.

The complete paralysis of the CN III is associated to pupil-lary dysfunction or incomplete paralysis with or withoutpupillary damage, requires conducting an urgent angio-CTscan or angio-MRI to rule out aneurysm, usually located inthe junction between the posterior communicating arteryand the internal carotid artery.55,56,59 The angio-CT scan, dueto its greater availability in the ER context is the most com-monly used modality (Fig. 10). The intracavernous internalcarotid artery aneurysm commonly causes CN VI paralysisdue to its proximity within the cavernous sinus.60

Neoplasms, severe cranial traumas, or large aneurysmscan cause damage to several CNs.54 Conducting either a CTscan or an MRI will depend on their availability within thepatient’s clinical context.

The cavernous sinus diseases (carotid-cavernous fistula,dural fistula, thrombosis) can cause damage to several CNsor CN VI along with the sympathetic pathway, due to theirproximity to the internal carotid artery.3,5,45 The MRI is themost suitable modality for its study. The Tolosa---Hunt syn-drome (Fig. 9d---f) is a clinical diagnosis consisting of orbitalpain with homolateral ophthalmoplegia (more frequently CNIII, followed by CN IV and VI) that affects the cavernous sinusand can spread toward the orbital apex.60,61 On the MRI it

is possible to observe cavernous sinus thickening, bulging ofits lateral edge, and intense enhancement after the adminis-tration of gadolinium. Corticoid therapy leads to clinical andradiological improvement. There are times that the findingscan be subtle. To make sure that its diagnosis is accurate,other cavernous sinus damage causes should be ruled outhere.62

Internuclear ophthalmoplegia consists of the loss or lim-itation of adduction in one eye and horizontal nystagmusduring the abduction of the other eye.6 The MRI shows thelesions in MLF location, being the most common causesmultiple sclerosis in young people and ischemia in theelderly.4,6

Bitemporal campimetric defects

In the bitemporal campimetric defects, the pathology is inthe chiasmatic region, where the decussation of the nasalfibers is consistent with temporal hemiretinas.

Tumors in the sellar and parasellar region (Fig. 11), amongthem, the hypophyseal adenoma being the most commoncan compress the optic chiasm (Table 6). Chiasm gliomas



Figure 9 Patient with multiple sclerosis. DP (a), FLAIR (b) and FLAIR (c) axial slices in a 27-year-old woman with right cranial nerveVI palsy. The MRI slices show one hyperintense demyelinating plate adjacent to the floor of the fourth ventricle in the location of thecranial nerve VI nucleus. The complete study showed typical periventricular and juxtacortical demyelinating lesions. Tolosa---Huntsyndrome. Coronal T2 (d), axial (e) and coronal (f) slices with gadolinium of a patient with headache, left palpebral ptosis, and palsyof the left cranial nerves III and IV. Treatment with corticoids led to a rapid clinical improvement. The MRI slices show thickeningof left cavernous sinus, with intense enhancement, spreading toward the orbital apex.

Table 6 Causes for hemianopsia.

Bitemporal hemianopsia (chiasmatic region)

Hypophyseal adenoma MetastasisCraniopharyingioma PituicytomaMeningioma Clivus chordomaChiasm glioma LymphomaAneurysms Histiocytosis XDysgerminoma

Homonymous hemianopsia (retrochiasmatic pathways and occipital cortex)

Vascular InfarctionHematoma Optic tracts

Tumor Lateral geniculate nucleusInflammatory Demyelinating disease Occipital lobeTrauma Temporal lobe



Figure 10 Aneurysms. Axial (a), coronal (b) and 3D (c) reformatting of maximum intensity projection of an angio-CT scan con-ducted in a 50-year-old woman who, after suffering from progressive headache for several weeks, presents to the ER with completepalsy of the right cranial nerve III and mydriatic pupil. Small aneurysm in the junction between the right internal carotid arteryand the posterior communicating artery in contact with the cranial nerve III. Axial (d) and coronal (e) MIP reformatting of angio-CTscan and diagnostic arteriography images (f) and after treatment (g) of a 48-year-old patient who presented to the ER with intense,headache of two-day duration with vomits and left cranial nerve VI palsy. One aneurysm is identified in the intracavernous internalcarotid artery justifying the compression of the cranial nerve VI. It is confirmed through the arteriography, and the complete closureof the aneurysm is confirmed after the embolization.

themselves can cause asymmetric bitemporal campimet-ric defects depending on the fibers damaged. Intrasellarlesions affect the superior temporal fields, and hypothala-mic lesions or those of the third ventricle region damage theinferior ones.3

The modality of choice for its assessment is the MRIfocused on the hypothalamus-hypophysis region.18

Homonymous hemianopsia

The homonymous defects of the visual field involve lesions ofthe retrochiasmatic visual pathway3 (Table 6). If hemianop-sia is congruent, the lesion will be found in the occipitalcortex or close to it, if it is not, the lesion should be lookedfor in the optic tracts, the lateral geniculate ganglion orMeyer’s loop.7

Cerebral vascular accidents are the most common causeof isolated homonymous hemianopsias63 (Fig. 12). These

defects should always be studied radiologically, except whenthey are clearly associated with an old cerebral vascularaccident. Given that strokes have an acute clinical presen-tation, the cranial CT scan is the initial modality to assessthese cases, especially if hemorrhage is suspected. When thecause is thought not to be vascular (tumors, demyelinatingdisease, etc.), the cranial MRI provides more information tobe able to reach the correct diagnosis.

Horner’s syndrome

Damage to the sympathetic pathway occurs with mild ptosis,miosis and, at times, anhidrosis.3,4 On suspicion that the firstneuron is affected with cerebral symptoms, both an MRI anda brain angio-MRI should be conducted, and in the absenceof brain symptoms, a cervical MRI should the modality ofchoice. In the former case we could find ischemic, inflam-matory or tumor lesions in the hypothalamic region and, if



Figure 11 Hypophyseal macroadenoma. T1 coronal (a), and coronal (b) and T1 sagittal (c) slices with gadolinium, in a 59-year-oldpatient with bitemporal hemianopsia. Hypophyseal mass with intrasellar and suprasellar component, with ‘‘snowman’’ morphologycompressing the optic chiasm (arrows). The macroadenoma shows one hyperintense cystic component in T1 that does not enhance,unlike the rest of the lesion. Craniopharyingioma. T1 sagittal (d) and axial FLAIR (e) and SPGRT1 (T1 spoiled gradient) slices withgadolinium (f), in a 61-year-old patient with right and left temporal visual field damage. Suprasellar mass with cystic lesion and solidcomponent that enhances with gadolinium. Note that, unlike the macroadenoma, the lesion compresses the chiasm from above,and the hypophysis is compressed on the bottom of the sella turcica (arrow).

there is medullary damage, we can find syringohydromyeliaor medullary neoplasms. To study the pathology that affectsthe preganglionic neurons, one CT scan of the neck, includ-ing the cervicothoracic junction, is more suitable, since itis possible to find tumors of the pulmonary apex, endotho-racic goiter, schwannomas, or neuroblastic tumors, and incases where there is damage to the postganglionic neurons,the CT scan or the MRI should be conducted including vas-cular sequences in order to rule out arterial pathology, suchas carotid dissection or lesions in the sellar and parasellarregions.8,64

Conclusions

Knowledge of the optic pathway anatomy, the CNs and theautonomous pathways involved in the motility and correctclinical information are crucial to be able to select and planradiological examinations. The classification of the pathol-ogy based on the most relevant clinical sign or symptom in

each case will allow us to select the most suitable imag-ing modality, while taking into account the most commondifferential diagnoses in each group of patients.

Authors’ contributions

1. Manager of the integrity of the study: ACVM.2. Study Idea: ACVM.3. Study Design: ACVM.4. Data Mining: ACVM, PSM, CBL and BIH.5. Data Analysis and Interpretation: ACVM, PSM, CBL and

BIH.6. Statistical analyses N/A.7. Reference: ACVM, PSM, CBL and BIH.8. Writing: ACVM.9. Critical review of the manuscript with intellectually rel-

evant remarks: ACVM, PSM, CBL and BIH.10. Approval of final version: ACVM, PSM, CBL and BIH.



Figure 12 Acute occipital infarction. Axial FLAIR (a) and diffusion (b) slices in a patient with sudden alteration of vision, andconfirmation of right inferior homonymous quadrantanopia. Hyperintense lesion in the left occipital cortex shining in diffusion. Thelesion was located above the calcarine sulcus. Acute occipital hemorrhages. CT axial (c) slices in a 75-year-old patient that presentsto the ER with headache, vomits and left homonymous hemianopsia, and CT axial (d) slice of the same patient presenting one yearlater with total blindness. In the first study, the right occipital acute hematoma can be seen, which justifies the presence of lefthemianopsia. In the subsequent study, the right occipital encephalomalacia residual to the prior hematoma can be seen plus onenew left occipital hematoma that by causing the right hemianopsia is causing total blindness.

Conflicts of interest

The authors declare no conflict of interests associated withthis article whatsoever.

Acknowledgements

We wish to thank Ms. Elena Marín, and Ms. Ana Sarto for theirdrawings appearing in this article.

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Diagnostic imaging in neuro-ophthalmology

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