Direct carotid-cavernous fistulas (CCFs) may occur after acceleration/deceleration head trauma and result in a high-flow connection between the cavernous segment of the internal carotid artery and the adjacent cavernous sinus. Symptoms may occur immediately or days later. Patients with direct CCF are typically young (younger than 50 years) and male, and they do not have vasculopathic risk factors that are often present in patients with indirect, low-flow dural arteriovenous fistulas (AVFs) (1). Clinical signs of direct CCF include proptosis, lid swelling, diplopia, conjunctival injection and chemosis, orbital bruit, increased intraocular pressure, and possible vision loss (2,3). Diplopia may result from the mechanical effects of extraocular muscle venous congestion, compression of the ocular motor cranial nerves by the arterialized venous channels, or a combination of both.
Treatment of direct CCF is endovascular embolization with platinum coils, detachable balloons, glue, or other substances and carries a high success rate, has a durable effect and a very low rate of recurrence (4).
Late recurrence of CCF-associated visual symptoms, including diplopia, is uncommon and raises concern for new or recurrent fistula formation. We describe 2 patients with traumatic CCF in whom ocular motility abnormalities with diplopia occurred years after endovascular CCF treatment.
A 31-year-old previously healthy man was involved in an accident while riding his motorcycle without a helmet. Approximately 1 week after the accident, the patient awoke with decreased vision in his right eye and diplopia that gradually worsened. At the time of referral to our neuro-ophthalmology service 2 months after the accident, visual acuity was 20/20 bilaterally, with 7.5-mm right eye proptosis with mild resistance to retropulsion and a right orbital bruit. There were arterialized and dilated right conjunctival vessels and a right sixth nerve palsy. The right optic nerve was mildly hyperemic. The left eye was normal.
Cerebral angiography confirmed the presence of a right CCF (Fig. 1A), and transarterial embolization with platinum coil obliteration of the fistula at the medial and posterior right cavernous sinus was performed the next day (Fig. 1B). Over the next several weeks, right proptosis and diplopia resolved.
Five years later, the patient returned with a 2–3 month history of recurrent diplopia. He was found to have a right eye abduction deficit and a mild limitation of elevation that worsened with attempted abduction. Motility in the left eye was normal. Afferent visual function and intraocular pressures were normal, and exophthalmometry showed 2 mm of right proptosis.
MRI of brain and orbits, computed tomography angiogram, and digital subtraction angiography all revealed no recurrence of the fistula and no intracranial pathology. The original coil pack was judged to be stable (Fig. 1C). No signs or symptoms of alternative causes of strabismus such as thyroid eye disease or myasthenia gravis were noted. Over the course of 8 months, the patient underwent 2 strabismus operations with resolution of his diplopia. He remained asymptomatic at 3-month follow-up.
A 20-year-old man in good health was thrown from a work vehicle and suffered closed head trauma. Several weeks later, he developed left eye swelling, redness, and proptosis and was found to have a left CCF (Fig. 2A). This was treated successfully with an ultrasound-guided transcutaneous puncture of the left super ophthalmic vein and placement of 16 platinum coils (Fig. 2B). He reported no diplopia either before or immediately after the procedure.
Four years later, the patient developed diplopia. Examination showed reduced motility of the left eye, consistent with left sixth nerve palsy and partial left third nerve palsy, with intact visual acuity and normal intraocular pressure (15 mm Hg in both eyes). There was 2 mm of left proptosis without periocular swelling or conjunctival injection. Postcontrast brain MRI and digital subtraction angiography revealed no recurrence of the left CCF with a stable coil pack (Fig. 2C) and no intracranial abnormalities.
Examination at our institution several months later showed limited left eye movements in all directions with 3 mm of left ptosis, and motility of the right eye was full. There were no signs suggestive of an underlying cause of his diplopia such as thyroid eye disease or myasthenia gravis. When his symptoms and clinical examination were unchanged 3 months later, eye muscle surgery was performed. Postoperatively, the patient had single binocular vision in primary position and experienced diplopia only with extremes of gaze. His eye position remained unchanged over the ensuing 6 months.
Approximately 20% of CCF patients have signs of isolated third nerve palsy, and an additional 32% have both third nerve involvement and findings consistent with dysfunction fourth and/or sixth nerves. Isolated sixth nerve involvement occurs in approximately 10% of patients, and isolated fourth nerve palsy is extremely rare (5–7).
Two possible neuropathic causes of diplopia with CCF have been proposed. The most widely accepted theory implicates venous congestion (8). Increased venous pressure may cause compression of cranial nerves; the third nerve can be compressed against the roof of the cavernous sinus (9), the fourth nerve can be compressed against the tentorial edge (10), and the sixth nerve can be compressed against the petroclinoid ligament (6). Other theories suggest that ophthalmoplegia is the result of cranial nerve paresis caused by thrombosis or a steal phenomenon. In reality, a combination of the processes likely exists in most cases (5,8).
Based on our review of the literature, we believe that our patients represent the first 2 cases of delayed mixed third and sixth nerve palsies appearing 5 years after complete resolution of direct CCF. Late onset of strabismus from isolated sixth nerve palsy has been reported after embolization of indirect (low flow) CCF. However, patients with indirect CCF often have other vasculopathic risk factors such as hypertension and/or hyperlipidemia, and multiple cranial nerve paresis has not been described (11). The cause of the multiple cranial nerve palsies in the otherwise healthy patients reported here may be multifactorial. Coil mass compression of the cranial nerves may result in immediate posttreatment symptoms, but coil compaction with time tends to reduce this untoward effect. Furthermore, the third and sixth nerves are believed to be vulnerable to injury in distinct and anatomically separate areas of the cavernous sinus (12,13) and the lack of apparent damage to other cranial nerves (fourth, ophthalmic, or maxillary) traveling in the same anatomic spaces does make chronic coil compression a less plausible explanation.
Another possibility is that the coils form a thrombophilic nidus for clot formation that does not resolve with fistula closure (11,12,14); it has been shown that the levels of d-dimer are higher in patients with AVF, and that the level will remain high even after treatment (15). Finally, it must be considered that the patients may have had permanent cranial nerve injury from the CCF, and that the diplopia occurred years later from decompensated strabismus. However, early diplopia resolution in Case 1 and lack of initial diplopia in Case 2 makes this possibility unlikely.
In conclusion, patients may be at long-term risk of diplopia after coil embolization of direct CCF. Delayed onset cranial nerve palsies are extremely rare in patients with completely treated fistulas. Our small case series does not permit us to identify specific risk factors for this late occurrence. We suggest 3 mechanisms that can partially explain the symptoms; however, we cannot determine with certainty which process(es) was/were present in our cases. Patients should be made aware of the potential for late-onset double vision even after successful treatment of direct CCF treatment.
STATEMENT OF AUTHORSHIP
Category 1: a. Conception and design: Subramanian; b. Acquisition of data: Bou Ghannam and Subramanian; c. Analysis and interpretation of data: Bou Ghannam and Subramanian. Category 2: a. Drafting the manuscript: Bou Ghannam and Subramanian; b. Revising it for intellectual content: Subramanian. Category 3: a. Final approval of the completed manuscript: Bou Ghannam and Subramanian.
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