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Interventional Neuro-Ophthalmology: Not an Oxymoron

Newman, Steven A. MD

Journal of Neuro-Ophthalmology: June 2012 - Volume 32 - Issue 2 - p 177–184
doi: 10.1097/WNO.0b013e318256638e
The Tenth Annual Hoyt Lecture
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Department of Ophthalmology, University of Virginia, Charlottesville, Virginia.

Address correspondence to Steven A. Newman, MD, Department of Ophthalmology, University of Virginia, Charlottesville, VA 22908; E-mail: san7a@virginia.edu

The author declares no conflicts of interest.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the full text and PDF versions of this article on the journal's Web site (www.jneuro-ophthalmology.com).

I am deeply honored to present the Tenth Annual Hoyt Lecture. No one has had more influence on modern neuro-ophthalmology than William Hoyt, MD. The list of students, residents, and fellows who he directly mentored, or who were indirectly touched by his trainees, is too long to enumerate. In particular, Bill's contributions, including the clinical vignettes in the third edition of Clinical Neuro-Ophthalmology, his meticulous approach to patients, and his ability to adapt to new technology, have served as a model and inspiration for all of us.

In ophthalmology, as in other areas of medicine, some people fix things, and others teach those individuals what to fix. Neuro-ophthalmology has as its primary goal the diagnosis of visual system pathology. As such, this “cognitive” branch of ophthalmology has largely been separated from therapeutics. Cogan (1) stated that “Neuro-ophthalmology shares with neurology in general, limited therapeutic successes. Its strength is largely diagnostic, rather than therapeutic.” Yet, this has changed dramatically with advances in neuroimaging and neurotherapeutics. As neuro-ophthalmologists, we are going to be asked increasingly, if not to play a primary interventional role, then to be involved in making decisions about when and how intervention takes place.

In the last 3 to 4 decades, there has been a paradigm shift to quantification of the 3 diagnostic pillars of our specialty: anatomy, physiology, and psychophysics. The study of clinical neuroanatomy has been revolutionized with the introduction of neuroimaging techniques such as computed tomography (CT) and magnetic resonance imaging (MRI). Optical coherence tomography (OCT) is a revolutionary technology for examining various parts of the eye including the nerve fiber layer and optic disc. Physiology can now be quantitated through a variety of electrophysiologic tests, including electroretinography (ERG) and visual evoked potentials (VEP). In recent years, these technologies have been improved to the point that we can now examine specific areas of the retina or the visual field with the advent of multifocal ERG and VEP. Other examples of quantifying physiologic function are the use of neutral density filters in the assessment of a relative afferent pupillary defect (2), and the quantification of relative movement of the 2 eyes as described by Hess (3), 1 of the 3 ophthalmologists to win the Nobel Prize. Finally, the development of automated perimetry has allowed standardization and greater reproducibility of visual field testing. In addition, new psychophysical techniques have been devised to study the visual field in a more rapid and specific fashion, including frequency doubling technique and short wavelength automated perimetry.

The combination of the neuro-ophthalmologist becoming more involved in therapeutics, and the advent of more accurate and reproducible techniques to quantify our clinical findings, form the basis of my lecture. I will approach this in 4 major categories: (1) what the neuro-ophthalmologist can treat; (2) how the neuro-ophthalmologist can assist in diagnosis; (3) how the neuro-ophthalmologist can assist with treatment; (4) how the neuro-ophthalmologist can provide advice for a variety of treatment decisions. In the tradition of Walsh & Hoyt's Clinical Neuro-Ophthalmology, 3rd edition, I will illustrate my presentation with a series of clinical case studies.

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WHAT THE NEURO-OPHTHALMOLOGIST CAN TREAT

Eye muscle surgery often plays a critical role in rehabilitation of many of our patients who present with strabismus of restrictive or paretic cause. The goal of any strabismus surgery is not only to give the patient single binocular vision in primary position and down reading gaze but also to maximize the area of binocularity (4,5). At times, it may be impossible to improve the overall excursion of an eye with limited eye movements. This may necessitate surgery on the contralateral eye, limiting its range, but allowing the patient to achieve maximum binocularity (6).

A 69-year-old man was evaluated for a 3-month history of vertical diplopia. He was found to have 2 mm of right proptosis and marked limitation of elevation of the right eye (Fig. 1). His only area of single binocular vision was in extreme downgaze. Orbital CT demonstrated enlargement of the inferior rectus muscles, compatible with thyroid eye disease. Recession of the right inferior rectus muscle might have provided single vision in primary gaze, but probably would have led to diplopia in downgaze. Instead, inferior oblique surgery on the left eye was performed (Fig. 2), which dramatically improved the patient's area of single binocular vision (Fig. 3).

A 36-year-old woman was referred for evaluation of double vision. She was known to have fibrous dysplasia of the left orbital roof. Previous cranial reconstructive surgery had left her with restriction of the left superior rectus muscle, making it difficult for her to look down (Fig. 4). Because I realized that it would not be possible to make her left eye move better, I performed a right inferior rectus recession with posterior fixation suture (Faden procedure). This, combined with a left superior rectus recession, reduced her diplopia while reading and achieved single binocular vision in primary gaze as well (Fig. 5).

Although many of us spend little time in the operating room, there are some procedures that traditionally have fallen within the purview of neuro-ophthalmology. One such example is optic nerve sheath fenestration. A 34-year-old woman reported that things “look dark.” Her visual acuity was 20/30 in the right eye and 20/50 in the left eye, with bilateral papilledema. She was found to have a tuberculum sellae meningioma, but 10 days after neurosurgical resection, her papilledema persisted and her visual fields became more constricted (Fig. 6). She underwent right optic nerve sheath fenestration, and within 1 week, she noted improvement in her visual function. At 2-year follow-up, her bilateral optic disc edema had resolved, and while she was left with optic atrophy and arcuate nerve fiber bundle defects in her visual fields, central acuity was preserved at 20/25 in each eye (Fig. 7).

The mechanism of action and indications for optic nerve sheath fenestration remain unclear. Noncontrolled studies suggest that it can protect the optic nerve from progressive damage related to intracranial hypertension (7,8). Although generally accepted as a treatment for chronic papilledema secondary to idiopathic intracranial hypertension, there are no controlled, prospective studies evaluating appropriate surgical indication and timing, and progressive visual loss may occur even after optic nerve sheath fenestration surgery (9–11).

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HOW THE NEURO-OPHTHALMOLOGIST CAN ASSIST IN DIAGNOSES

Although the advent of high-resolution neuroimaging techniques has improved anatomic localization of a disease process, these studies are not specific and obtaining tissue for pathologic examination is often required. A 57-year-old man presented with a 3-week history of periocular pain and horizontal diplopia. He was found to have limited abduction of the right eye, which was presumed due to a right sixth nerve palsy. Quantitative measurement of intraocular pressure in abduction revealed a 10 mm Hg rise suggestive of medial rectus restriction and an orbital CT confirmed a mass involving the right medial rectus muscle. Fine needle aspiration biopsy (FNAB) of the mass was diagnostic of metastatic carcinoid tumor (Fig. 8). The patient was treated with endocrine suppression and radiation therapy.

Modifications of the FNAB technique introduced by Kennerdell et al (12–14) permit biopsy of skull base lesions. A 68-year-old woman was referred with a 6-week history of diplopia and was found to have a right sixth nerve palsy. Her MRI demonstrated a suspicious area in the region of the right cavernous sinus (Fig. 9). To reach this area of the skull base, I adapted the technique used in neurosurgery for percutaneous trigeminal rhizotomy. Using the Stealth neuronavigation system to access the posterior cavernous sinus through the foramen ovale (Fig. 10), cellular elements were obtained, revealing B cells, which stained for CD10 and CD19. The patient was spared a craniotomy, and her lymphoma was treated with radiation therapy.

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HOW THE NEURO-OPHTHALMOLOGIST CAN ASSIST WITH TREATMENT

The past 30 years have seen a revolution in the endovascular approach (transarterial, transvenous) to a variety of intracranial lesions, including aneurysms, arteriovenous malformations, and carotid–cavernous sinus fistulae (15). The neuro-ophthalmologist can play a critical role in providing neurovascular access. A 61-year-old woman reported the acute onset of blurred vision in each eye, and an eye examination was unremarkable. While her symptoms resolved, 1 month later, she complained of double vision. A CT and MRI of the brain were reported as normal. The following month, she noted pulsatile tinnitus and over the next 3 months, her diplopia worsened, and she developed bilateral conjunctival injection and chemosis. The patient was started on systemic antibiotics, but when her vision deteriorated, she was referred for neuro-ophthalmic evaluation.

At the time of examination, her visual acuity was 20/25 in the right eye and 20/400 in the left eye. There was a 1.2 log unit left relative afferent pupillary defect, with bilateral abduction deficits, 2 mm of left proptosis with marked chemosis of the left eye. Visual fields showed a pattern of nerve fiber layer field loss greater in the left eye. The right fundus was normal, whereas the left showed prominent retinal veins.

Cerebral angiography confirmed a left carotid–cavernous sinus fistula, with cortical venous hypertension (Fig. 11A). A transvenous approach through the inferior petrosal sinus to embolize the fistula was unsuccessful. I was able to assist in accessing the fistula through the right superior ophthalmic vein (Fig. 12) (18). The neuroradiology team was able to use detachable coils to embolize the fistula (Fig. 11B), with resolution of chemosis, diplopia, and improvement in visual acuity. In this case, a transverse approach through the superior ophthalmic vein was successful (19). At times, such access is not available, requiring embolization through the superior orbital fissure via a direct percutaneous orbital puncture (15–17,19–21). Complications may arise in treating carotid–cavernous sinus fistula, many with ophthalmic manifestations (22,23). The neuro-ophthalmologist must remain involved in delivering care to the patients.

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HOW THE NEURO-OPHTHALMOLOGISTS CAN PROVIDE ADVICE FOR A VARIETY OF TREATMENT DECISIONS

Following the observation of Smith (24) , and confirmed by others (25–28), not only can radiation therapy slow progression, but it may also actually improve visual function, in patients with optic nerve sheath meningioma. A 39-year-old woman presented with a 3-year history of decreased vision at 2/200 in the right eye, while vision in the left eye remained at 20/20. She had a 2.1 log unit right afferent papillary defect. MRI confirmed the presence of a right optic nerve sheath meningioma (Fig. 13), and the patient who was treated with 50 Gy of fractionated external beam radiation within 3 months had right visual acuity improved to 20/200, she was able to “see colors.” Two years later, her visual acuity in the right eye further improved to 20/40. In a commensurate fashion, the patient's right relative afferent defect improved from 2.1 to 0.9 log units (3 months after radiotherapy) and to 0.3 log units (2 years after radiotherapy), as did her visual fields (Fig. 14). OCT demonstrated moderate bilateral retinal nerve fiber layer thinning (right eye: 75.22 μm; left eye: 82.92 μm). Savino (29) pointed out in the Seventh Annual Hoyt Lecture that OCT might help predict which patients may be expected to experience improved visual acuity following treatment. As our patient demonstrated, thinning of the nerve fiber layer does not preclude improvement in central acuity and visual fields (30,31).

In linking the neuro-ophthalmologists' increasing role in treatment with improved methods of quantifying our clinical findings, it will be essential that we obtain class 1 evidence with prospective, randomized double-blind clinical trials. To date, we have completed the Optic Neuritis Treatment Trial (ONTT) (32) and the Ischemic Optic Neuropathy Decompression Trial (IONDT) (33). Both studies provided useful information concerning therapy, but perhaps more importantly, they have delineated the natural history of these 2 optic nerve disorders. The ONTT proved that while intravenous corticosteroids might hasten visual recovery early in the clinical course, over a 15-year follow-up period, there was no difference in recovery of visual function between treated and untreated patients. In fact, oral corticosteroids predispose patients to recurrent attacks of optic neuritis. The ONTT also taught us a great deal about the likelihood of a patient developing multiple sclerosis after an episode of optic neuritis and demonstrated that MRI of the brain is a powerful predictor of the chances of developing demyelinating disease. The IONDT proved that optic nerve sheath fenestration was not only efficacious in the treatment of ischemic optic neuropathy but also found that approximately 40% of patients (with visual acuity <20/60) can experience spontaneous improvement.

A third prospective study, the Idiopathic Intracranial Hypertension Treatment Trial is currently underway. Hopefully, it will provide us with a better understanding of the natural history of idiopathic intracranial hypertension and the efficacy of medical therapy.

I see the neuro-ophthalmologists role evolving, not only in our ability to establish the correct diagnosis but also in becoming more involved in the treatment of our patients. But every treatment has a risk–benefit ratio or as I teach my residents: “There is no operation that can't make a patient worse.” We must always be mindful of the guiding principle in medicine: first do no harm.

In conclusion, it is essential that data regarding anatomy, physiology, and psychophysics be obtained in a standardized and quantifiable manner. It is these data that allow us to determine whether our patient's condition is changing and enables us to make better decisions regarding therapy. As neuro-ophthalmologists, we now stand ready to be more involved in patient evaluation, guiding intervention, and being there to assist when intervention is necessary.

For the full Hoyt Lecture and accompanying figures, please consult Supplemental Digital Content at the following links:

* Hoyt Lecture Report, http://links.lww.com/WNO/A39.

* Figures 1-10, http://links.lww.com/WNO/A40.

* Figures 11-20, http://links.lww.com/WNO/A41.

* Figures 21-30, http://links.lww.com/WNO/A42.

* Figures 31-40, http://links.lww.com/WNO/A43.

* Figures 41-49, http://links.lww.com/WNO/A44.

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