Journal of Neuro-Ophthalmology:
Visual Sequelae After Consensus-Based Treatment of Ophthalmic Artery Segment Aneurysms: The Johns Hopkins Experience
Kanagalingam, Sivashakthi MD; Gailloud, Philippe MD; Tamargo, Rafael J. MD; Subramanian, Prem S. MD, PhD; Miller, Neil R. MD
Departments of Ophthalmology (SK, PSS, NRM), Radiology (PG), and Neurosurgery (RJT, PSS, NRM), The Johns Hopkins Hospital, Baltimore, Maryland.
Address correspondence to Neil R. Miller, MD, Wilmer Eye Institute, The Johns Hopkins Hospital, Maumenee 127, 600 N Wolfe Street, Baltimore, MD; E-mail: firstname.lastname@example.org
The authors report no conflicts of interest.
Background: To determine the anatomic and visual outcomes of patients with ophthalmic artery segment aneurysms treated at The Johns Hopkins Hospital using a consensus-based treatment algorithm.
Methods: Retrospective record review of a prospectively accrued case series of 88 patients (101 aneurysms) treated between January 2004 and July 2009. Presenting symptoms and aneurysm parameters were recorded for all subjects. Treatment strategy for all patients was determined by consensus among neurosurgeons, neurointerventionalists, neurologists, and neuroophthalmologists meeting to review the clinical cases on a weekly basis. Final clinical outcomes (aneurysm control, functional status, and vision) were ascertained from in-house examinations, medical records, telephone interviews, or a combination of these methods. Risk factors for visual or other complications were evaluated.
Results: An optic neuropathy was present in at least 30 (34%) of 88 patients after treatment. Presumed new visual loss occurred in 24 (27%) of these patients. The remaining 6 patients had preexisting optic neuropathy–related visual loss that worsened after treatment. No patient with a preexisting optic neuropathy improved following treatment.
Conclusion: Ophthalmic artery segment aneurysms present a treatment challenge because of their anatomic complexity and relationship to critical neural structures, particularly the visual sensory pathway. We have adopted a consensus-based treatment approach in an effort to optimize patient outcomes and aneurysm control. Although our approach resulted in durable treatment of the aneurysm, a sizable proportion of patients experienced new vision loss after treatment, and no patient with preexisting visual loss related to their aneurysm experienced visual improvement after treatment. We recommend that all patients with ophthalmic artery aneurysms receive careful and thorough preprocedural counseling to ensure they are aware of the risks and benefits of treatment regardless of the method used.
Aneurysms arising from the internal carotid artery (ICA) at the origin of or just distal to the ophthalmic artery are termed “ophthalmic artery segment aneurysms” (1). These aneurysms project dorsally or dorsomedially from the surface of the ICA toward the temporal aspect of the ipsilateral optic nerve (1,2).
The surgical treatment of ophthalmic artery segment aneurysms is both challenging and complex because of their close proximity to the anterior clinoid process and the optic nerves as well as the need to exclude the lesion from the intracranial circulation while maintaining patency of the parent vessel (1–6). Fortunately, refinements in microsurgical techniques and greater understanding of regional anatomy have made surgery of these aneurysms less formidable (7–9). In addition, endovascular therapy has evolved in the last decade to become an effective alternative to microsurgical clipping in the management of these lesions (10–13). Nevertheless, the inherent risk of vision loss remains a significant issue for patients with these aneurysms regardless of the modality of treatment (14,15).
In this report, we present the visual, neurologic, and neuroimaging results in treating patients with ophthalmic artery segment aneurysms treated using our consensus-based strategy at The Johns Hopkins Hospital from January 2004 to July 2009.
PATIENTS AND METHODS
All patients with ophthalmic artery segment aneurysms treated at The Johns Hopkins Hospital between January 2004 and July 2009 were identified using a database prospectively accrued and maintained by one of the authors (R.J.T.). Further details of the clinical course of the patients were then obtained from the Johns Hopkins electronic patient record and the digital picture archiving and communication system. A total of 88 patients with 101 unruptured and ruptured ophthalmic artery segment aneurysms were identified. We then reviewed the medical records, including operative and procedure notes, as well as all neuroimaging studies on the patients. Age, gender, clinical presentation, and aneurysm characteristics were documented. Aneurysm fundus sizes were taken at the point of maximum width or length. Ophthalmic artery segment aneurysms that measured 1–9 mm in greatest dimension were considered “small”; those measuring 10–24 mm were considered “large,” and aneurysms greater than 25 mm were termed “giant.” The neck size was regarded as narrow when it was 4 mm or less in largest diameter and wide when it was greater than 4 mm. For patients who presented with ruptured aneurysms, their clinical grade on admission was determined using the Glasgow Coma Scale, and the severity of subarachnoid hemorrhage (SAH) was graded using the Fisher CT Scale. The latter classifies SAH on the basis of the appearance on CT, with no hemorrhage defined as Grade 1, 1 mm thick as Grade 2, more than 1 mm thick as Grade 3, and any thickness associated with intraventricular or parenchymal hemorrhage as Grade 4 (16).
Treatment recommendations for all 88 patients were determined by consensus during a conference held weekly and attended by a consistent group of interventional neuroradiologists, neurosurgeons, neurologists, and neuroophthalmologists. All recommendations were based on patient characteristics and a review of all imaging studies, including MRI and angiography, CT and angiography, and catheter angiography. The recommendations were then communicated to the patient. In some cases, the recommendation was for surgical clipping; in others, endovascular treatment was recommended; in still others, the consensus was that both treatment options had equal risks and benefits. In addition, it was assumed that in some patients for whom surgical clipping was recommended, anatomic features of the aneurysm would require wrapping in addition to or instead of clipping.
Direct surgery was performed via ipsilateral pterional/frontosphenotemporal craniotomy and often involved an anterior clinoidectomy. The carotid artery in the neck was dissected and the ICA exposed for proximal control. The anterior fossa floor, middle fossa floor, and greater and lesser wings of sphenoid were extensively drilled. After the aneurysm was exposed using the surgical microscope, the dural fold overlying the optic nerve was divided, the relationship of the optic nerve to the aneurysm assessed, and the optic nerve mobilized. This often was followed by drilling of the optic canal and anterior clinoid, followed by clipping of the aneurysm neck once it was free of the dura. In cases in which clipping was deemed inappropriate (9%), the aneurysm dome was contracted by coagulation with a bipolar cautery at a low setting (4–6) and then wrapped with coarse or fine cotton (muslin was not used in any case) and reinforced with fibrin sealant (fibrinogen, factor XIII, thrombin, and calcium). Patency of the ophthalmic artery was confirmed via intraoperative micro-Doppler sensors, and an intraoperative angiogram was performed routinely to confirm correct clip placement, obliteration of the aneurysm, and preservation of flow in both the ipsilateral ICA and the ophthalmic artery.
All interventional procedures were performed under general anesthesia. Following femoral arterial access, a 6-French guide catheter was advanced over a 0.035 guidewire into a stable position in the ICA. In 1 case, arterial access had to be obtained from a brachial approach. Preembolization digital subtraction angiography, including 3-dimensional imaging, was then performed. Patients with an unfavorable sac–neck ratio in whom placement of a stent (Enterprise; Cordis Neurovascular, Bridgewater, NJ, or Neuroform; Boston Scientific, Natick, MA) was anticipated were placed on a combined regimen of aspirin and clopidogrel at least 3 days before the procedure. Under road map guidance, a microcatheter was placed within the aneurysmal sac. Aneurysm coiling was performed using various brands of detachable microcoils. All patients were heparinized during treatment and monitored by assessing activated clotting time. Control angiography was obtained at the end of the procedure to ensure obliteration of the aneurysm as well as patency of the parent vessel and the rest of the intracranial circulation. Patients were admitted to the intensive care unit for overnight observation; heparinization was continued for 24 hours.
Patients in this series who received endovascular treatment of their aneurysms subsequently underwent cerebral angiography at least 6 months later, with the results being categorized using the classification proposed by Roy et al (17): complete occlusion of the aneurysm without any opacification of the neck or sac of the aneurysm (Class 1), near-complete occlusion with minimal neck remnant in aneurysms (Class 2), and incomplete occlusion with contrast-enhanced opacification in part of the sac (Class 3). Patients who underwent stent-assisted coiling were assessed for presence or absence of stenosis of the parent vessel, stent migration, and coil impaction.
All patients with visual complaints before or after treatment of their aneurysms were assessed by a complete examination, including best-corrected or pinhole visual acuity, color vision, visual field testing, pupillary examination, ocular motor assessment, intraocular pressure measurement, and ophthalmoscopy. Other patients were contacted by telephone and asked if they had experienced any visual changes postprocedure. If so, they were asked to return for an ophthalmologic examination, or if they were under the care of an ophthalmologist or optometrist, their records were obtained and reviewed.
General clinical outcomes were reported using the Glasgow Outcome Score (GOS) (18): a score of 5 indicating a neurologically normal result, 4 with disability but independent, 3 with disability, 2 with vegetative survival, and 1 representing death. Clinical outcomes were recorded at the time of discharge and at follow-up.
There were 68 women and 20 men ranging in age from 21 to 76 years (mean ± SD, 52.3 ± 12.4 years). Forty-nine patients were white, 30 African American, 5 Hispanic, and 4 of Asian origin. Among the 88 patients, 31 (35.2%) had multiple intracranial aneurysms. Thirteen patients (14.8%) had 2 ophthalmic artery segment aneurysms.
Nine patients presented with SAH from a ruptured ophthalmic artery segment aneurysm. These patients were treated during the acute phase after rupture. Of the 79 patients with unruptured aneurysms, the patient presentations were as follows: 50 (57%) had an incidental finding detected when neuroimaging was performed for an unrelated reason, 17 (19%) experienced headaches, 6 (7%) presented with visual changes, 3 (3.5%) complained of dizziness, and 3 (3.5%) had experienced at least 1 transient ischemic attack.
Of the patients with incidental ophthalmic artery segment aneurysm findings, 8 had experienced previous rupture of another intracranial aneurysm and 7 had visual symptoms unrelated to the aneurysm, including cataract, glaucoma, and a contralateral aneurysm causing optic neuropathy.
Of the 101 aneurysms, 63 were on the left and 38 were on the right. Seventy-seven (76.2%) were small aneurysms, 22 (21.8%) were large, and 2 (2%) were giant.
Aneurysm Treatment and Outcomes
Sixty-nine aneurysms (68.3%) were clipped, 10 (10%) could not be clipped and were wrapped, and 22 (21.7%) were coiled. Seventeen (77%) of the 22 coiled aneurysms also were stented. Three of the 69 aneurysms that were clipped had undergone prior unsuccessful endovascular embolization elsewhere. Of the 22 aneurysms that were coiled, 2 previously had been coiled incompletely and 3 previously wrapped.
Of the 79 aneurysms for which clipping was attempted, 69 (87%) were clipped successfully as confirmed by intraoperative angiography, 3 (4%) were clipped and wrapped, and 7 (9%) could not be clipped but were wrapped. Subsequent imaging was performed in the 8 of the 9 patients with aneurysms that were wrapped (with and without clipping), and none of their aneurysms was determined to require retreatment. In addition, none of the patients whose aneurysms were wrapped experienced an SAH during the follow-up period, which ranged from 6 months to 5 years (mean, 2 years). Of the 22 aneurysms that were coiled or stent coiled, immediate postprocedural angiography demonstrated complete occlusion (Class 1) in 5 (23%), near-complete occlusion with minimal neck remnant (Class 2) in 7 (32%), and incomplete occlusion with opacification of the aneurysmal sac in 10 (45%). At follow-up, complete occlusion (Class 1) was seen in 9 aneurysms (41%), near-complete occlusion (Class 2) in 3 (14%), and incomplete occlusion in 2 (9%). Seven patients with 8 aneurysms (36%) were lost to angiographic follow-up. During the follow-up period, 4 aneurysms initially demonstrating incomplete occlusion (Class 3) spontaneously progressed to complete occlusion (Class 1), 1 aneurysm progressed from incomplete occlusion (Class 3) to near-complete occlusion (Class 2), and 1 aneurysm, initially classified as near-complete occlusion (Class 2), improved to complete occlusion (Class 1). Mild-to-moderate coil compaction (i.e., contraction of the coils within the aneurysm sac) was noted in 5 aneurysms (23%). Recanalization of the aneurysm and subsequent recurrence at the neck were observed in 2 aneurysms (9%). Neither stent migration nor parent artery stenosis was detected in our series.
Prior to treatment, 13 of the 88 patients had visual complaints. All of these patients were examined before treatment by a member of the Neuro-Ophthalmology Division of the Wilmer Eye Institute. Six of these patients (6.9%) were found to have visual deficits from an optic neuropathy related to their aneurysm. The remaining 7 patients had unrelated causes for their visual complaints (e.g., cataract, glaucoma). An additional 5 patients (5.7%) with no visual complaints were evaluated preoperatively and found to have no visual deficits. Posttreatment, 37 (42%) of 88 patients were examined in our institute. Of the remaining 51 patients, we reviewed records of 34 patients (38.6% of total) from outside ophthalmologists, neuroophthalmologists, or optometrists. Seventeen patients (19.3%) for whom we were unable to obtain records were contacted by telephone and asked if they had any visual symptoms that had occurred after their surgery. Based on the above assessments, we determined that at least 30 patients (34.1%) had posttreatment visual dysfunction. Twenty-four of these individuals (80%) definitely or possibly had developed a new visual deficit. Among the 6 patients with preexisting optic neuropathy–related visual loss, 5 (16.6%) experienced further visual loss and 1 (3.4%) maintained stable decreased vision. Thus, none of the patients with preexisting aneurysm-related visual loss experienced improvement in vision posttreatment. In addition, 2 patients developed visual loss in the eye contralateral to the aneurysm following treatment (see below).
Of the 24 patients who apparently or definitely had normal vision preoperatively and who experienced new visual deficits following treatment, 21 had undergone clipping of their aneurysms, 2 had had their aneurysms wrapped, and 1 had had the aneurysm coiled. In 5 of these patients, the aneurysm had ruptured prior to treatment, whereas 19 patients had unruptured aneurysms. Fifteen of the patients (62.5%) had small aneurysms, 7 (29.2%) had large aneurysms, and 2 (8.3%) had giant-sized aneurysms. In 13 patients (54.2%), the new visual deficit consisted of decreased visual acuity, reduced color vision, and a visual field defect. In 12 of these patients, the visual deficit was related to a new optic neuropathy, whereas in 1 patient, pretreatment rupture of the aneurysm produced Terson syndrome with persistent visual loss despite clearing of the intraocular hemorrhage. The degree of visual loss ranged from 20/25 in 1 patient to no perception of light in 2 patients, and 7 of the 13 patients had visual acuity of 2/100 or worse in their affected eye. Of the 11 remaining patients, 3 had normal acuity but reduced color vision and a visual field defect in the affected eye, and 8 patients had only a visual field defect associated with normal acuity and color vision.
Of the 5 patients who experienced progression of their optic neuropathy posttreatment (Table 1), all had unruptured aneurysms: 1 was giant sized, 3 were large, and 1 was small. All patients in this group experienced progressive decreased visual acuity, color vision, and worsening visual field defects. Two of the 5 patients had undergone surgical clipping and 3 had undergone coiling (Table 2). Two of the patients, 1 who underwent clipping and 1 who underwent coiling, had had unsuccessful or incomplete treatment elsewhere before undergoing definitive treatment at our institution. Both experienced both ipsilateral and contralateral visual loss following treatment.
Among the 31 eyes with visual field loss, the defects were purely or primarily inferior in 19 (61.3%). Among the remaining 12 eyes, the defect was nasal in 5 (41.7%), superior in 2 (16.7%), and complete in 2 (16.7%). The remainder of the eyes had mixed defects. The only 2 eyes with purely temporal visual field defects were those contralateral to the aneurysm.
Complications following clipping or wrapping occurred in 19 (27%) of 69 patients, of whom 3 had ruptured aneurysms and 16 had unruptured aneurysms. These complications included stroke (9%), cranial nerve palsies (6%), epidural or subdural hemorrhage (4%), hydrocephalus (1%), myocardial infarction (1%), pulmonary emboli (1%), heparin-induced thrombocytopenia (1%), seizure (1%), cerebral salt wasting (i.e., hyponatremia and dehydration from centrally mediated excessive renal sodium excretion) (1%), vision loss from clipping of contralateral intracranial aneurysm (1%), and diabetes insipidus (1%). Complications following coiling occurred in 4 patients (21%), of whom 1 had a ruptured aneurysm and 3 had unruptured aneurysms. The complications in this group of patients included SAH (5.2%), deep vein thrombosis (5.2%), contralateral occipital hemorrhage and associated vision loss (5.2%), right arm compartment syndrome (5.2%), and transient paresthesias (5.2%).
At discharge, the overall clinical outcomes were excellent (GOS, 5) in 58 patients (65.9%), good (GOS, 4) in 16 (18.2%), and fair (GOS, 3) in 14 (15.9%). At follow-up at least 6 months posttreatment, clinical outcomes were excellent in 66 (75%), good in 13 (14.8%), and fair in 9 (10.2%). As might be expected, patients with unruptured aneurysms were more likely to have an excellent outcome than those with ruptured aneurysms. There were no patient deaths.
The paraclinoid segment of the ICA is known to be a particularly challenging region to access due to several anatomic complexities, including the adjacent anterior clinoid process and optic nerves, as well as the potential for aneurysms in this location to be partly extradural (1,3,18).
Previous reports of aneurysms of the entire paraclinoid segment usually deal with a treatment modality: microsurgical clipping (3,5,14,19–24) or endovascular coiling (10,17,25,26). Few have addressed in detail the risks of visual loss since the availability of endovascular coiling compared to surgical clipping or wrapping (11,13,15,27). Furthermore, inclusion of other ICA aneurysms in some series makes accurate assessment of visual morbidity of ophthalmic artery segment aneurysms difficult (28).
In this series, we have used the classification of ophthalmic artery segment aneurysms proposed by Day (1), that is, those arising in clear relation to the ophthalmic artery. We chose this subset of aneurysms because of their proximity to the optic nerve and the potential for treatment to be associated with damage to the visual apparatus, resulting in visual loss. Using a consensus-based approach, our results demonstrate that regardless of the treatment modality, there is significant risk of vision loss. Twenty-nine patients (33%) had what appeared to be either a new visual deficit or a worse visual deficit after treatment, and no patient with preexisting visual loss experienced visual improvement postoperatively. Factors associated with postoperative vision loss were greater aneurysm size, pretreatment aneurysm rupture, preexisting visual loss, and aneurysm retreatment. Specifically, 2 giant aneurysms, 7 (32%) of 22 large aneurysms, and 15 (19.5%) of 77 small aneurysms occurred in the group of patients that experienced visual deficits. Five (56%) of 9 ruptured aneurysms were in this group vs 19 (21%) of 92 unruptured aneurysms. Five (83%) of 6 patients with preexisting visual symptoms experienced worsening of their vision posttreatment. In addition, 2 patients in this series, both with large aneurysms, had been treated previously at another institute: one patient had an aneurysm stented and coiled and the other patient had an aneurysm wrapped. Both these patients had bilateral postoperative vision loss.
The most common locations of the visual field defects in the 31 eyes in which defects were present were completely or partly inferior or nasal, presumably reflecting the location of the aneurysm superior and/or temporal to the optic nerve, the surgical approach to the aneurysm, or both. The only 2 eyes with purely temporal visual field defects were those contralateral to the aneurysm, reflecting damage to the nasal region of the contralateral optic nerve, the region most likely to be damaged by the aneurysm or the surgical approach.
Posttreatment optic nerve–related visual loss in patients with ophthalmic artery aneurysms may occur by several mechanisms regardless of the treatment modality used. Intraoperative injury of the optic nerve during clipping may occur from direct vascular compromise (4,29,30), excessive manipulation (6,31), or direct heat from the high-speed drill (12,24,32–34). Wrapping an unclippable or a partially clipped aneurysm may induce a significant inflammatory reaction (35). Suggested strategies to improve visual outcomes postoperatively include minimizing manipulation of the optic nerve during dissection of the surrounding tissue and placement of the clip, preservation of the blood supply to the nerve during these procedures, judicious use of irrigation during drilling of the anterior clinoid process, avoiding the use of muslin for wrapping an aneurysm, and using systemic corticosteroids to reduce the damage caused by muslin-related inflammation (1,3,35,36). Vision loss postcoiling may result from emboli to the optic nerve or retina, an increase in mass effect from coil packing, or coil-related perianeurysmal inflammation that may or may not respond to systemic corticosteroids (11,35,37).
A major limitation of this retrospective study is that not all patients underwent a preoperative or postoperative visual assessment. It is therefore possible that some patients who were visually asymptomatic before and after surgery nevertheless had an unappreciated preoperative deficit that worsened postoperatively and that some patients who had no visual deficit preoperatively had a subclinical postoperative deficit. Thus, the percentage of patients with new or worse visual deficits following treatment of their aneurysms is likely higher than 33%. Although we did not appreciate optic disc pallor in patients with new visual complaints and evidence of an optic neuropathy who were examined within a few days to a week after treatment, we did not perform optical coherence tomography of the peripapillary retinal nerve fiber layer in any of the patients to determine if any had a preexisting subclinical optic neuropathy.
Nevertheless, our findings indicate that regardless of the procedure used to treat an ophthalmic artery aneurysm and even when the treatment used is consensus based, there is a significant risk of visual loss following treatment. There appears to be little chance for improvement of vision in eyes that have already experienced visual loss from the aneurysm following treatment. Finally, patients with giant ophthalmic artery aneurysms may experience not only ipsilateral visual loss following treatment but also contralateral visual loss from damage to the contralateral optic nerve. We recommend that all patients with ophthalmic artery aneurysms be informed prior to endovascular or surgical treatments that there is a risk of permanent vision loss that may be severe and potentially bilateral and that the likelihood of visual recovery after treatment is low.
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