Accepted Manuscript Eye-Movement Abnormalities after a Ruptured Intracranial Aneurysm Elina Koskela, MD Aki Laakso, MD, PhD Riku Kivisaari, MD, PhD Kirsi Setälä, MD, PhD Ferzat Hijazy, MD Juha Hernesniemi, MD, PhD PII:
S1878-8750(14)00442-2
DOI:
10.1016/j.wneu.2014.04.059
Reference:
WNEU 2338
To appear in:
World Neurosurgery
Received Date: 11 November 2013 Accepted Date: 16 April 2014
Please cite this article as: Koskela E, Laakso A, Kivisaari R, Setälä K, Hijazy F, Hernesniemi J, EyeMovement Abnormalities after a Ruptured Intracranial Aneurysm, World Neurosurgery (2014), doi: 10.1016/j.wneu.2014.04.059. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Koskela
ACCEPTED MANUSCRIPT 1
Eye-Movement Abnormalities after a Ruptured Intracranial Aneurysm
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Elina Koskela MD,1 Aki Laakso MD, PhD,2 Riku Kivisaari MD, PhD,2 Kirsi
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Setälä MD, PhD,1 Ferzat Hijazy MD,2 Juha Hernesniemi MD, PhD2
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Division of Neuro-ophthalmology
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Helsinki University Central Hospital
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Helsinki Finland
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Helsinki University Central Hospital
Department of Neurosurgery
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Department of Ophthalmology
Helsinki Finland
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Corresponding author:
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Elina Koskela
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Department of Ophthalmology/ Division of Neuro-ophthalmology
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Helsinki University Central Hospital
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Haartmaninkatu 4 C
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00290 Helsinki Finland
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E-mail: [email protected]; Tel: +358 947173161, Fax: +358 947175919
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ACCEPTED MANUSCRIPT Abstract
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Objective The overlooking of eye-movement abnormalities associated with aneurysmal
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subarachnoid hemorrhage (aSAH) is common even though these may greatly affect survivors´
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quality of life; their prevalence remains undetermined. The aim of the study was to assess pre-
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and postoperative eye-movement abnormalities and their recovery in follow-up of patients
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with aSAH and their association with age, gender, and aSAH severity.
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Methods Patients admitted to Helsinki University Central Hospital who underwent surgery or
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endovascular treatment for a ruptured intracranial aneurysm during 2011 were participants in
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this prospective study. A neuro-ophthalmic examination was performed on admission, and 3
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days, 14 days, 2 to 4 months, and 6 months postoperatively; for those with third-, fourth- or
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sixth-nerve palsies or brainstem vascular syndromes, follow-up was 12 months. Associations
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between neuro-ophthalmic findings and relevant clinical, radiological, and demographic data
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were under study. Two intraoperative videos were selected to show rare cases of aneurysms
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causing cranial nerve palsies.
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Results Of 121 participants, 11 (9%) presented on admission, and 16 (13%) postoperatively
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with a third-, fourth-, or sixth-nerve palsy. Most of these palsies totally resolved leaving 2.5%
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of all patients presenting with a partial palsy at one year. We also evaluated the frequencies of
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horizontal gaze pareses (n=9) and Parinaud´s syndromes (n=3). No statistically significant
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associations emerged between neuro-ophthalmic findings and other clinical variables.
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Conclusion Eye-movement abnormalities are quite a common finding in the acute stage of
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aSAH. Within one year, however, marked improvement occurs. Identifying these neuro-
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ophthalmic findings can assist in localization of the underlying pathology.
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Key words: abducens nerve palsy; aneurysm; cranial nerve palsy; oculomotor nerve palsy;
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Parinaud´s syndrome; subarachnoid hemorrhage; trochlear nerve palsy
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Cranial nerve palsies and other eye-movement abnormalities can be an important element for
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any reduction in quality of life in adults; the resultant strabismus and diplopia can cause
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anxiety and interfere with daily activities, such as driving and reading (1, 16, 17).
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Abnormalities associated with aneurysmal subarachnoid hemorrhage (aSAH) may, however,
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easily be overlooked during medical concentration on motor- and speech- function
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impairment, even though they may obviously impact on the rehabilitation of aSAH.
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Prospective studies of the prevalence of ocular motor abnormalities and their recovery in
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patients with aSAH are missing. Retrospective analyses may miss transient palsies, and the
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rates of fourth-nerve palsies, in particular, may be underestimated, as they are the most
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difficult to diagnose (21). With regard to third-nerve palsies, both any standardized test
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method and a definition of complete recovery are lacking (36). Accordingly, most reports
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concentrate on third-nerve palsies and combine patients with ruptured and unruptured
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aneurysms, even though among them they may represent different mechanisms of nerve
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dysfunction.
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Eye-movement abnormalities can result from the aneurysm itself, causing compressive injury
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and damaging adjacent structures (35), and also from the pulsating effect of the aneurysm (2).
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Intracerebral and subarachnoid blood, associated edema, and intraneural hemorrhage can
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irritate tissues and cause direct damage (19). Finally, aneurysm treatment itself, increased
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intracranial pressure (ICP), or post-SAH vasospasm and other complications can also produce
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ocular movement disturbances.
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follow-up of patients treated for aSAH, we prospectively assessed these deficits and their
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association with age, gender, and aSAH severity.
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PATIENTS AND METHODS
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All consecutive patients with a ruptured intracranial aneurysm who were admitted for surgical
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clipping or endovascular treatment to the Department of Neurosurgery, Helsinki University
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Central Hospital, during 2011 were participants in this prospective study. All patients with
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aSAH within our catchment area in southern Finland (population 1.8 million) are treated in
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our department without selection bias. The diagnosis of aSAH was established by computed
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tomography (CT), magnetic resonance imaging (MRI), or lumbar puncture, or a combination
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of these, and associated aneurysms were imaged with CT angiography, MR angiography, or
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digital subtraction angiography, or a combination. The study protocol was approved by the
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local ethics committee.
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On admission, an experienced radiologist and neurosurgeon (R.K.) evaluated from
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radiological images the locations, dimensions, and projections of the aneurysms, presence of
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any hydrocephalus or intracerebral hemorrhage (ICH), and the severity of aSAH on the Fisher
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scale (9). The aneurysm was classified as partially occluded if any filling existed in
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postoperative angiograms. Clinical severity of aSAH on admission was evaluated based on
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the WFNS (World Federation of Neurosurgical Societies) (38) and Hunt and Hess scales (18).
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We also graded clinical outcomes at 6 months after the aSAH using the modified Rankin
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Scale (mRS) (7); scores prior to aSAH were evaluated based on medical records and clinical
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history obtained on admission from the patient or relatives or both. Follow-up time after
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surgery or endovascular treatment was at least 6 months. Clinical and radiological data were
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compared with eye-movement abnormalities.
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The on-admission examination included the function of cranial nerves III-VI for conscious
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patients, and squint, pupillary reactions, and anisocoria for unconscious patients. Bedside
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examination by a neuro-ophthalmologist took place within 3 days postoperatively. The next
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follow-up visit for patients cooperating adequately was at the Division of Neuro-
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ophthalmology at discharge.
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Neuro-ophthalmic follow-up assessments for all patients were 2 to 4 months and 6 months
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after the operation. For patients with a third-, fourth- or sixth-nerve palsy or any brainstem
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vascular syndrome with eye-movement abnormality, the follow-up lasted for 1 year.
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Examination included testing smooth pursuit eye-movements, the alternating cover test at
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distance and near, the Maddox rod and Hess screen tests, and evaluation of lids and pupils.
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Recovery of a third-, fourth- or sixth-nerve palsy was classified as partial if any limited eye
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movement occurred on a detailed examination. Complete improvement of third-nerve palsy
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included a partial or a complete recovery of pupillary reaction.
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Intraoperative videos
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All operations performed by our senior author (J.H.) are routinely recorded. Intraoperative
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videos of patients with cranial nerve palsy on admission were reviewed, with 2 rare cases
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selected to show their microsurgical treatment (Videos 1-2). Patient consent was obtained for
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the videos.
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Statistical analysis
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The baseline characteristics, age, gender, the Fisher, WFNS, and Hunt and Hess grades, the
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presence of ICH or hydrocephalus, operation modality; and the mRS at 6 months were
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syndrome, by Pearson’s χ2 test or the Mann-Whitney U test, as appropriate. Statistical
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analysis was carried out with the SPSS for Windows 20.0 (IBM Corporation, Armonk, NY,
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USA). All tests were two-sided. The level of significance was set at P < 0.05.
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RESULTS
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Overall outcome
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Of the 125 patients with a ruptured intracranial aneurysm treated during 2011, 121 (97%)
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were participants in the study; 3 of the missing patients had Hunt and Hess grade V and died
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within 5 days of admission. No survivor was lost to follow-up at 3 months. One patient
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without cranial nerve palsy at 3 months did not come to the follow-up visit at 6 months.
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Patient characteristics are described in Table 1. Medial cerebral artery (MCA) aneurysms
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were the most common, occurring in 31% of the patients (Table 2). Aneurysm type was
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saccular in 90%, fusiform in 9%, and mycotic in 1%. One-third had 2 or more (up to 7)
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aneurysms. Among ruptured aneurysms, the mean size of the neck was 4 mm (range 2-19
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mm, median 4), width was 6 mm (range 2-20 mm, median 6), and length was 8 mm (range 2-
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29 mm, median 7).
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Complete aneurysm occlusion was achieved in 92%. Surgical technique comprised clipping
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(95%), reclipping (1%), proximal occlusion with bypass (1%), and in giant aneurysms
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resection (3%). Endovascular technique consisted of coiling in 10 patients and stenting in 1
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patient. Six patients underwent 2 operations for the ruptured aneurysm, and 9 underwent
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another operation for an unruptured aneurysm during 2011. During the follow-up, 10 deaths
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occurred as aSAH sequelae.
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Neuro-ophthalmic outcome
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statistical significance existed between eye-movement abnormalities and age, gender, the
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Fisher, WFNS, and Hunt and Hess grades, the presence of ICH or hydrocephalus, operation
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modality; or mRS at 6 months.
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Third-nerve palsies
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Preoperatively, 4 patients presented with pupil-involving third-nerve palsy due to direct
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aneurysm compression, and 3 of them had had onset of palsy over 10 days earlier. Seven
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other patients had a dilated pupil as a result of uncal herniation. Video 1 presents
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microsurgical clipping of a giant basilar artery (BA) bifurcation aneurysm of a patient with
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third-nerve palsy (Video 1, Figure 1).
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Total aneurysm occlusion was achieved in all those with third-nerve palsy by clipping; in one
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internal carotid - posterior communicating artery (ICA-PComA) aneurysm it was preceded by
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coiling and re-bleeding after that. All 3 new postoperative oculomotor nerve palsies
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(aneurysm locations ICA-PComA for 2 of them and BA bifurcation for 1) had totally
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recovered when examined 3 months after aSAH. Of 2 survivors with ICA-PComA aneurysm
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and oculomotor nerve palsy on admission, both showed only some limitation in upgaze at 1
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year. Neither aberrant regeneration nor Weber´s syndrome occurred in the series.
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Fourth- and sixth-nerve palsies
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One patient had fourth-nerve palsy as a presenting symptom (in addition to headache) of
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aSAH at childbirth. A thrombosed fusiform aneurysm of a distal branch of the anterior
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inferior cerebellar artery (AICA) was visible in the operation as adhered to the ipsilateral
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fourth nerve (Video 2, Figure 2). Another patient with a BA-AICA aneurysm underwent
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clipping surgery after failure of an attempt at coil embolization; postoperatively she
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Aneurysm occlusion without ischemic complications on head CT scan was complete. The
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sixth-nerve palsies completely recovered, but the fourth-nerve palsy was persisting at 1 year.
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Of 6 patients, 5 presented with bilateral sixth-nerve palsy on admission, and 4 also had
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hydrocephalus. All sixth-nerve palsies already showed total improvement when examined at 3
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months.
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Other eye-movement abnormalities
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One male patient with a left vertebral artery- posterior inferior cerebellar artery aneurysm
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(PICA) and infarction in the PICA territory experienced acute rotatory vertigo, and the
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aneurysm was clipped without additional ischemic changes on CT. This patient developed
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peripheral left facial nerve palsy, nystagmus when looking to the right, and moderate hearing
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loss in the left ear consistent with a lateral ponto-medullary syndrome. Facial nerve function
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partially recovered, but his hearing loss persisted at 1 year.
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Three patients had Parinaud´s syndrome appearing as a paralysis of upgaze and pupils
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constricting with near viewing but not to light. One of them also had a unilateral and another
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had bilateral sixth-nerve palsy. Aneurysm locations were anterior communicating artery in 2
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of them and ICA-PComA in 1, and they all had hydrocephalus and mild spasm. Two of these
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patients underwent clipping, and 1 needed a permanent shunt. One patient underwent
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endovascular coiling and became dependent on an external ventricular drainage device
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(EVD), since whenever the threshold for drainage was risen, headache, worsened diplopia,
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and supranuclear paralysis of upgaze occurred until we lowered the threshold again. No
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ischemic changes were visible in MRI in the mesencephalic tectum, but the ventricles were
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dilated. Since this patient also suffered from intraventricular hemorrhage, a Clostridium
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was preferred to a permanent shunt at 2 weeks. Parinaud´s syndrome greatly improved soon
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after the operation, and he never needed a permanent shunt.
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Seven patients presented on admission with gaze paresis. All of these had an ICH (5 temporal,
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2 frontal), and 6 of those with an MCA bifurcation aneurysm, contralateral hemiparesis, and
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gaze deviation. Each of these totally improved during the hospital stay. Additionally, a female
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patient with a left distal fusiform PICA aneurysm underwent PICA-PICA anastomosis, and
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the next day clipping proximal to the aneurysm. A head CT scan showed infarctions in both
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cerebellar hemispheres. She presented with a partial Wallenberg´s syndrome and an ipsilateral
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horizontal gaze paresis to the right accompanied by mild temporary contralateral motor
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hemiparesis. At 1 year, her gaze paresis still persisted.
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DISCUSSION
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This first prospective study of eye-movement abnormalities in an unselected series of
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consecutive patients with aSAH undergoing an operation showed that 9% of the patients had a
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third-, fourth- or sixth-nerve palsy on admission, and 13% immediately after operation.
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During a year, however, most of these patients experienced a total recovery, leaving only
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2.5% of all patients with a partial palsy. The results represent the entire scale of aSAH
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including vertebro-basilar aneurysms and all grades on the Hunt and Hess scale with a low
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drop-out rate.
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As to the limitations of the study, decreased level of consciousness may have masked eye-
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movement abnormalities in critically ill patients. We reported only those findings that were
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definite.
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(3.3%), and fourth-nerve palsies (0.8%). Laun et al., in their retrospective analysis among
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patients with sSAH, reported third-nerve palsies to be the most frequent finding (7.1%),
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followed by sixth- (3.0%) and fourth-nerve (0.2%) palsies (25). They had significantly more
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BA-superior cerebellar artery (SCA) aneurysms, which can explain their higher frequency of
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third-nerve palsies. Likewise, Tsementzis et al. revealed third-nerve palsies to be most
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common in their series of 28 patients with aSAH (39).
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Third-nerve palsies
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In the present study, for those with ICA-PComA aneurysms, third-nerve palsy occurred
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preoperatively in 12%. Some older series report rates as high as 34% to 56% (14, 35).
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Probable factors lowering the current percentage include our unselected series, improved
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imaging modalities enabling detection of smaller aneurysms causing the aSAH, and faster
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access to angiography. Our findings are more consistent with those of Leivo et al.: among a
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retrospective series of 1314 patients with cerebral aneurysms, they reported 35 (2.7%)
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unilateral third-nerve palsies, and their total of 183 patients with an ICA-PComA aneurysm
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included 29 oculomotor palsies (21 with aSAH), (15.8%) (26).
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Improvement of a third-nerve palsy due to direct ICA-PComA aneurysm compression after
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clipping surgery has been convincing (3, 11, 13, 24, 35). The effectiveness of endovascular
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coiling in oculomotor nerve recovery has been a matter of debate; suggested mechanisms in
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various reports include disappearance of aneurysmal pulsation and subsequent shrinking that
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relieves the compressive effect (2, 15, 20, 23, 27, 29). Statistical analysis in the current study
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showed no association between eye-movement abnormalities and endovascularly or
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microsurgically treated patients; the small sample size of endovascularly treated aneurysms,
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however, precludes drawing definite conclusions about the effect of treatment modality.
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at 1 year based on rather stringent criteria. One with a BA bifurcation giant aneurysm-related
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partial palsy showed a total recovery. They each had had a delay in admission of more than 10
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days. In addition to an initial partial palsy (3, 11, 24), recovery has been particularly favorable
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for those operated on early (8, 11, 13, 35), especially within 3 days after palsy onset (26). It is
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our policy to perform the operation as soon as possible when a patient harbors a third-nerve
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palsy caused by a ruptured aneurysm. All of our new postoperative oculomotor nerve palsies
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resolved completely within 3 months. Based on a series of oculomotor complications
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following surgical treatment of BA bifurcation aneurysms, Cruciger et al. reported recovery
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from isolated palsy to be excellent if it avoids injury to the brain stem (5).
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Fourth- and sixth-nerve palsies
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Trochlear nerve palsies associated with aSAH are rare, and the literature has few reports on
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this topic (25, 31, 34, 39). A thrombosed fusiform aneurysm of a distal branch of the AICA
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presenting with trochlear nerve palsy in our series was a very rare finding. Some reports on
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ruptured (31) and unruptured distal SCA aneurysms presenting with fourth-nerve palsy do
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exist (4, 6, 10, 33). As trochlear nerve palsies are the most challenging of the ocular motor
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nerve palsies to diagnose, they are probably underdiagnosed on hospital wards, which is also
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reflected in the number of published case reports.
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Sixth-nerve palsies in the acute stage were bilateral in 5 of our 6 cases, and all showed rapid
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improvement, which is a similar finding to that of Laun et al. who saw a rapid regression in
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89% (25). The most likely explanation for these palsies in our series was increased ICP due to
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aSAH; the abducens nerves are anchored in Dorello´s canal, making it prone to pressure and
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stretching. No direct compression of the aneurysm was evident. Other suggested mechanisms
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cerebrospinal fluid compressing the abducens nerves (12, 40).
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Other eye-movement abnormalities
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Horizontal gaze paresis may follow pontine or large hemispheric damage. In the acute phase
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of a frontal lobe lesion, the eyes will deviate toward the side of the lesion, and the ability to
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generate saccades in the opposite direction may be impaired. Damage in the paramedian
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pontine reticular formation (PPRF), in turn, results in complete horizontal gaze paresis on the
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affected side (32). All 7 patients in the current study with gaze deviation with cerebral
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hemispheric basis improved soon after aSAH. Findings in our patient with an ipsilateral
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horizontal gaze paresis accompanied by contralateral hemiparesis are consistent with an
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infarction in the midpontine tegmentum involving part of the pyramidal tract and the PPRF.
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Her gaze paresis persisted, since dysfunction of the PPRF does not recover well (22).
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Parinaud´s syndrome has been reported to exist in the setting of SAH (28). Three of our
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patients presented with reversible Parinaud´s syndrome: of these, one apparently being EVD-
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dependent. Mechanisms behind Parinaud´s syndrome in hydrocephalus include dilatation of
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the posterior part of the third ventricle and of the rostral aqueduct with axial displacement of
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these structures and stretching of the posterior commissure (30, 37). Identifying this syndrome
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as causing visual complaints can assist and expedite treatment decisions.
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CONCLUSIONS
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In conclusion, eye-movement abnormalities are quite a common finding in the acute stage of
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aSAH. Within one year, however, marked improvement occurs, and the prognosis of surgery-
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related third-nerve palsy is usually excellent. Identifying these abnormalities can assist in
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localization and treatment decisions regarding the underlying pathology.
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Acknowledgement: This study was supported by grants from the Finnish Eye Foundation,
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the Finnish Eye and Tissue Bank Foundation, the Evald and Hilda Nissi Foundation, and the
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Maire Taponen Foundation.
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21. Keane JR: Fourth nerve palsy: Historical review and study of 215 inpatients. Neurology
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22. Kelley RE, Kovacs AG: Horizontal gaze paresis in hemispheric stroke. Stroke 17:1030-
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23. Ko JH, Kim YJ: Oculomotor nerve palsy caused by posterior communicating artery
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24. Kyriakides T, Aziz TZ, Torrens MJ: Postoperative recovery of third nerve palsy due to
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25. Laun A, Tonn JC: Cranial nerve lesions following subarachnoid hemorrhage and
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26. Leivo S, Hernesniemi J, Luukkonen M, Vapalahti M: Early surgery improves the cure of
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Resolution of cranial nerve paresis after endovascular management of cerebral aneurysms.
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Surg Neurol 68:500-504, 2007.
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28. Maramattom BV, Wijdicks EF: Dorsal mesencephalic syndrome and acute hydrocephalus
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after subarachnoid hemorrhage. Neurocrit Care 3:57-58, 2005.
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29. Mavilio N, Pisani R, Rivano C, Testa V, Spaziante R, Rosa M: Recovery of third nerve
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aneurysms. Interv Neuroradiol 6:203-209, 2000.
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30. Osher RH, Corbett JJ, Schatz NJ, Savino PJ, Orr LS: Neuro-ophthalmological
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complications of enlargement of the third ventricle. Br J Ophthalmol 62:536-542, 1978.
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31. Papo I, Caruselli G, Salvolini U: Aneurysm of the superior cerebellar artery. Surg Neurol
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7:15-17, 1977.
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32. Pedersen RA, Troost BT: Abnormalities of gaze in cerebrovascular disease. Stroke
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12:251-254, 1981.
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33. Peluso JP, van Rooij WJ, Sluzewski M, Beute GN: Distal aneurysms of cerebellar
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arteries: Incidence, clinical presentation, and outcome of endovascular parent vessel
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occlusion. AJNR Am J Neuroradiol 28:1573-1578, 2007.
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34. Son S, Park CW, Yoo CJ, Kim EY, Kim JM: Isolated, contralateral trochlear nerve palsy
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associated with a ruptured right posterior communicating artery aneurysm. J Korean
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Neurosurg Soc 47:392-394, 2010.
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Neurol Neurosurg Psychiatry 37:475-484, 1974.
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36. Stiebel-Kalish H, Maimon S, Amsalem J, Erlich R, Kalish Y, Rappaport HZ: Evolution of
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oculomotor nerve paresis after endovascular coiling of posterior communicating artery
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aneurysms: A neuro-ophthalmological perspective. Neurosurgery 53:1268-1273, 2003.
361
37. Swash M: Periaqueductal dysfunction (the Sylvian aqueduct syndrome): A sign of
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hydrocephalus? J Neurol Neurosurg Psychiatry 37:21-26, 1974.
363
38. Teasdale GM, Drake CG, Hunt W, Kassell N, Sano K, Pertuiset B, De Villers JC: A
364
universal subarachnoid hemorrhage scale: Report of a committee of the World Federation of
365
Neurosurgical Societies. J Neurol Neurosurg Psychiatry 51:1457, 1988.
366
39. Tsementzis SA, Williams A: Ophthalmological signs and prognosis in patients with a
367
subarachnoid haemorrhage. Neurochirurgia (Stuttg) 27:133-135, 1984.
368
40. Ziyal IM, Ozcan OE, Deniz E, Bozkurt G, Ismailoglu O: Early improvement of bilateral
369
abducens nerve palsies following surgery of an anterior communicating artery aneurysm. Acta
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Neurochir (Wien) 145:159-161, 2003.
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Figure 1. A 54-year-old man presenting with left third-nerve palsy. The patient had had
374
vertical diplopia corrected with prism lenses 1 month before aSAH. Computed tomography
375
angiogram reveals a ruptured giant basilar bifurcation aneurysm. The patient made an
376
excellent overall outcome and total recovery from the palsy after aneurysm clipping.
377
Figure 2. A 41-year-old woman presenting with fourth-nerve palsy. Magnetic resonance
378
imaging demonstrates a thrombosed fusiform aneurysm of a distal branch of the anterior
379
inferior cerebellar artery. The patient made an excellent recovery after resection of the
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aneurysm; the fourth-nerve palsy completely recovered at 6 months.
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ACCEPTED MANUSCRIPT Table 1. Characteristics of 121 patients with ruptured aneurysm treated during 2011. Sex 55 (45%)
Female
66 (55%)
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Male
Pre-SAH modified Rankin Scale
101 (84%)
Modified Rankin Scale 1
15 (12%)
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Modified Rankin Scale 0
Modified Rankin Scale 2
3 (2%) 2 (2%)
Modified Rankin Scale 4-5
Clinical condition on admission
30 (25%)
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Hunt and Hess Grade I Hunt and Hess Grade II Hunt and Hess Grade III
WFNS III WFNS IV
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WFNS II
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Hunt and Hess Grade IV
WFNS I
admission
31 (26%) 19 (16%) 21 (17%) 20 (16%) 49 (40%) 24 (20%) 8 (7%) 10 (8%)
WFNS V Radiological
0
55 (20-84)
Mean age at diagnosis (range)
Hunt and Hess Grade V
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30 (25%) findings
on
ACCEPTED MANUSCRIPT Hydrocephalus
63 (52%) 9 (7%)
Fisher scale II
13 (11%)
Fisher scale III
35 (29%)
Fisher scale IV
64 (53%)
Intracerebral hemorrhage
42 (35%)
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Fisher scale I
Treatment
110 (91%)
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Surgical Endovascular
11 (9%)
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Clinical outcome at six months Modified Rankin Scale 0
30 (25%)
Modified Rankin Scale 1
34 (28%)
Modified Rankin Scale 3 Modified Rankin Scale 4 Modified Rankin Scale 5
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Modified Rankin Scale 2
17 (14%) 12 (10%) 4 (3%) 10 (8%)
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Table 2. Locations of 121 ruptured aneurysms and frequencies associated with third-, fourth-, or sixth-nerve palsies on admission. No, n (%)
III, n (%)
IV, n (%)
14 (11.6)
2 (1.7)
0
True PCom
0
1 (0.8)
0
ICA, other
9 (7.4)
0
0
MCA
36 (29.8)
0
ACA
6 (4.9)
PICA
6 (4.9)
PCA
1 (0.8)
ACom
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Posterior circulation, other Total
0
0
0
0
0
0
0
0
0
0
2 (1.7)
2 (1.7)
0
0
0
1 (0.8)
0
0
0
4 (3.3)
1 (0.8)
0
0
1 (0.8)
0
1 (0.8)
0
110 (90.9)
4 (3.3)
1 (0.8)
6 (5.0)
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2 (1.6)
0
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0
1 (0.8)
30 (24.8)
BA trunk
1 (0.8)
0
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Aneurysm location
VI, n (%)
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Cranial nerve palsy
ICA, internal carotid artery; PComA, posterior communicating artery; MCA, medial cerebral artery; ACA, anterior cerebral artery; PICA, posterior inferior cerebellar artery; PCA, posterior cerebral artery; ACom, anterior communicating artery; BA, basilar artery; SCA, superior cerebellar artery
ACCEPTED MANUSCRIPT
Table 3. Eye-movement disorders in 121 patients with ruptured aneurysm treated during 2011. On admission, n
Immediately
At 1 year, n (%)
disorder
(%)
postoperatively, n (%)
Unilateral 2 (1.7)
Complete
2 (1.7)
2 (1.7)
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Partial
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Third-nerve palsy
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Eye-movement
2 (1.7)
5 (4.1)
0
0
0
5 (4.1)
1 (0.8)
0
1 (0.8)
1 (0.8)
1 (0.8)
1 (0.8)
0
0
0
0
1 (0.8)
2 (1.7)
0
0
0
0
Partial
3 (2.5)
3 (2.5)
0
Partial+complete
1 (0.8)
1 (0.8)
0
Bilateral
0
Dilated pupil
4 (3.3)
Fourth-nerve palsy
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Bilateral
Unilateral Partial Complete
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Sixth-nerve palsy
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Complete
Bilateral
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1 (0.8)
2 (1.7)
0
Parinaud´s
0
3 (2.5)
0
7 (5.8)
5 (4.1)
1 (0.8)
0
1 (0.8)
0
1 (0.8)
1 (0.8)
1 (0.8)
syndrome Horizontal gaze
Wallenberg´s
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paresis
1 (0.8)
medullary syndrome
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Skew deviation
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Lateral ponto-
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syndrome
1 (0.8)
1 (0.8)
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ACCEPTED MANUSCRIPT Abbreviations:
AICA: Anterior inferior cerebellar artery, ASAH: Aneurysmal subarachnoid hemorrhage, BA: Basilar artery, CT: Computed tomography, EVD: External ventricular drainage device, ICA:
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Internal carotid artery, ICH: Intracerebral hemorrhage, ICP: Intracranial pressure, MCA: Medial cerebral artery, MRI: Magnetic resonance imaging, mRS: Modified Rankin Scale, PICA: Posterior inferior cerebellar artery, PComA: Posterior communicating artery, PPRF: Paramedian pontine
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reticular formation, SCA: Superior cerebellar artery, WFNS: World Federation of Neurosurgical
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Societies
ACCEPTED MANUSCRIPT Disclosure – Conflict of Interest
Acknowledgement: Elina Koskela has received grants from the Finnish Eye Foundation, the Finnish Eye and Tissue Bank Foundation, the Evald and Hilda Nissi Foundation and the Maire Taponen Foundation.
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related to this study. The other authors report no conflicts of interest.
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Disclosure: Aki Laakso has received consulting fees from Orion Pharma Ltd, Espoo, Finland, not
S1878-8750(14)00442-2
DOI:
10.1016/j.wneu.2014.04.059
Reference:
WNEU 2338
To appear in:
World Neurosurgery
Received Date: 11 November 2013 Accepted Date: 16 April 2014
Please cite this article as: Koskela E, Laakso A, Kivisaari R, Setälä K, Hijazy F, Hernesniemi J, EyeMovement Abnormalities after a Ruptured Intracranial Aneurysm, World Neurosurgery (2014), doi: 10.1016/j.wneu.2014.04.059. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Koskela
ACCEPTED MANUSCRIPT 1
Eye-Movement Abnormalities after a Ruptured Intracranial Aneurysm
2
Elina Koskela MD,1 Aki Laakso MD, PhD,2 Riku Kivisaari MD, PhD,2 Kirsi
3
Setälä MD, PhD,1 Ferzat Hijazy MD,2 Juha Hernesniemi MD, PhD2
4
1
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Division of Neuro-ophthalmology
6
Helsinki University Central Hospital
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Helsinki Finland
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2
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Helsinki University Central Hospital
Department of Neurosurgery
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Department of Ophthalmology
Helsinki Finland
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Corresponding author:
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Elina Koskela
13
Department of Ophthalmology/ Division of Neuro-ophthalmology
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Helsinki University Central Hospital
15
Haartmaninkatu 4 C
16
00290 Helsinki Finland
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E-mail: [email protected]; Tel: +358 947173161, Fax: +358 947175919
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ACCEPTED MANUSCRIPT Abstract
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Objective The overlooking of eye-movement abnormalities associated with aneurysmal
20
subarachnoid hemorrhage (aSAH) is common even though these may greatly affect survivors´
21
quality of life; their prevalence remains undetermined. The aim of the study was to assess pre-
22
and postoperative eye-movement abnormalities and their recovery in follow-up of patients
23
with aSAH and their association with age, gender, and aSAH severity.
24
Methods Patients admitted to Helsinki University Central Hospital who underwent surgery or
25
endovascular treatment for a ruptured intracranial aneurysm during 2011 were participants in
26
this prospective study. A neuro-ophthalmic examination was performed on admission, and 3
27
days, 14 days, 2 to 4 months, and 6 months postoperatively; for those with third-, fourth- or
28
sixth-nerve palsies or brainstem vascular syndromes, follow-up was 12 months. Associations
29
between neuro-ophthalmic findings and relevant clinical, radiological, and demographic data
30
were under study. Two intraoperative videos were selected to show rare cases of aneurysms
31
causing cranial nerve palsies.
32
Results Of 121 participants, 11 (9%) presented on admission, and 16 (13%) postoperatively
33
with a third-, fourth-, or sixth-nerve palsy. Most of these palsies totally resolved leaving 2.5%
34
of all patients presenting with a partial palsy at one year. We also evaluated the frequencies of
35
horizontal gaze pareses (n=9) and Parinaud´s syndromes (n=3). No statistically significant
36
associations emerged between neuro-ophthalmic findings and other clinical variables.
37
Conclusion Eye-movement abnormalities are quite a common finding in the acute stage of
38
aSAH. Within one year, however, marked improvement occurs. Identifying these neuro-
39
ophthalmic findings can assist in localization of the underlying pathology.
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Key words: abducens nerve palsy; aneurysm; cranial nerve palsy; oculomotor nerve palsy;
41
Parinaud´s syndrome; subarachnoid hemorrhage; trochlear nerve palsy
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44
Cranial nerve palsies and other eye-movement abnormalities can be an important element for
45
any reduction in quality of life in adults; the resultant strabismus and diplopia can cause
46
anxiety and interfere with daily activities, such as driving and reading (1, 16, 17).
47
Abnormalities associated with aneurysmal subarachnoid hemorrhage (aSAH) may, however,
48
easily be overlooked during medical concentration on motor- and speech- function
49
impairment, even though they may obviously impact on the rehabilitation of aSAH.
50
Prospective studies of the prevalence of ocular motor abnormalities and their recovery in
51
patients with aSAH are missing. Retrospective analyses may miss transient palsies, and the
52
rates of fourth-nerve palsies, in particular, may be underestimated, as they are the most
53
difficult to diagnose (21). With regard to third-nerve palsies, both any standardized test
54
method and a definition of complete recovery are lacking (36). Accordingly, most reports
55
concentrate on third-nerve palsies and combine patients with ruptured and unruptured
56
aneurysms, even though among them they may represent different mechanisms of nerve
57
dysfunction.
58
Eye-movement abnormalities can result from the aneurysm itself, causing compressive injury
59
and damaging adjacent structures (35), and also from the pulsating effect of the aneurysm (2).
60
Intracerebral and subarachnoid blood, associated edema, and intraneural hemorrhage can
61
irritate tissues and cause direct damage (19). Finally, aneurysm treatment itself, increased
62
intracranial pressure (ICP), or post-SAH vasospasm and other complications can also produce
63
ocular movement disturbances.
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ACCEPTED MANUSCRIPT In order to discover the true prevalence of eye-movement abnormalities and their recovery in
65
follow-up of patients treated for aSAH, we prospectively assessed these deficits and their
66
association with age, gender, and aSAH severity.
67
PATIENTS AND METHODS
68
All consecutive patients with a ruptured intracranial aneurysm who were admitted for surgical
69
clipping or endovascular treatment to the Department of Neurosurgery, Helsinki University
70
Central Hospital, during 2011 were participants in this prospective study. All patients with
71
aSAH within our catchment area in southern Finland (population 1.8 million) are treated in
72
our department without selection bias. The diagnosis of aSAH was established by computed
73
tomography (CT), magnetic resonance imaging (MRI), or lumbar puncture, or a combination
74
of these, and associated aneurysms were imaged with CT angiography, MR angiography, or
75
digital subtraction angiography, or a combination. The study protocol was approved by the
76
local ethics committee.
77
On admission, an experienced radiologist and neurosurgeon (R.K.) evaluated from
78
radiological images the locations, dimensions, and projections of the aneurysms, presence of
79
any hydrocephalus or intracerebral hemorrhage (ICH), and the severity of aSAH on the Fisher
80
scale (9). The aneurysm was classified as partially occluded if any filling existed in
81
postoperative angiograms. Clinical severity of aSAH on admission was evaluated based on
82
the WFNS (World Federation of Neurosurgical Societies) (38) and Hunt and Hess scales (18).
83
We also graded clinical outcomes at 6 months after the aSAH using the modified Rankin
84
Scale (mRS) (7); scores prior to aSAH were evaluated based on medical records and clinical
85
history obtained on admission from the patient or relatives or both. Follow-up time after
86
surgery or endovascular treatment was at least 6 months. Clinical and radiological data were
87
compared with eye-movement abnormalities.
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The on-admission examination included the function of cranial nerves III-VI for conscious
90
patients, and squint, pupillary reactions, and anisocoria for unconscious patients. Bedside
91
examination by a neuro-ophthalmologist took place within 3 days postoperatively. The next
92
follow-up visit for patients cooperating adequately was at the Division of Neuro-
93
ophthalmology at discharge.
94
Neuro-ophthalmic follow-up assessments for all patients were 2 to 4 months and 6 months
95
after the operation. For patients with a third-, fourth- or sixth-nerve palsy or any brainstem
96
vascular syndrome with eye-movement abnormality, the follow-up lasted for 1 year.
97
Examination included testing smooth pursuit eye-movements, the alternating cover test at
98
distance and near, the Maddox rod and Hess screen tests, and evaluation of lids and pupils.
99
Recovery of a third-, fourth- or sixth-nerve palsy was classified as partial if any limited eye
100
movement occurred on a detailed examination. Complete improvement of third-nerve palsy
101
included a partial or a complete recovery of pupillary reaction.
102
Intraoperative videos
103
All operations performed by our senior author (J.H.) are routinely recorded. Intraoperative
104
videos of patients with cranial nerve palsy on admission were reviewed, with 2 rare cases
105
selected to show their microsurgical treatment (Videos 1-2). Patient consent was obtained for
106
the videos.
107
Statistical analysis
108
The baseline characteristics, age, gender, the Fisher, WFNS, and Hunt and Hess grades, the
109
presence of ICH or hydrocephalus, operation modality; and the mRS at 6 months were
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ACCEPTED MANUSCRIPT compared statistically with the presence of third-, fourth- or sixth-nerve palsies or Parinaud´s
111
syndrome, by Pearson’s χ2 test or the Mann-Whitney U test, as appropriate. Statistical
112
analysis was carried out with the SPSS for Windows 20.0 (IBM Corporation, Armonk, NY,
113
USA). All tests were two-sided. The level of significance was set at P < 0.05.
114
RESULTS
115
Overall outcome
116
Of the 125 patients with a ruptured intracranial aneurysm treated during 2011, 121 (97%)
117
were participants in the study; 3 of the missing patients had Hunt and Hess grade V and died
118
within 5 days of admission. No survivor was lost to follow-up at 3 months. One patient
119
without cranial nerve palsy at 3 months did not come to the follow-up visit at 6 months.
120
Patient characteristics are described in Table 1. Medial cerebral artery (MCA) aneurysms
121
were the most common, occurring in 31% of the patients (Table 2). Aneurysm type was
122
saccular in 90%, fusiform in 9%, and mycotic in 1%. One-third had 2 or more (up to 7)
123
aneurysms. Among ruptured aneurysms, the mean size of the neck was 4 mm (range 2-19
124
mm, median 4), width was 6 mm (range 2-20 mm, median 6), and length was 8 mm (range 2-
125
29 mm, median 7).
126
Complete aneurysm occlusion was achieved in 92%. Surgical technique comprised clipping
127
(95%), reclipping (1%), proximal occlusion with bypass (1%), and in giant aneurysms
128
resection (3%). Endovascular technique consisted of coiling in 10 patients and stenting in 1
129
patient. Six patients underwent 2 operations for the ruptured aneurysm, and 9 underwent
130
another operation for an unruptured aneurysm during 2011. During the follow-up, 10 deaths
131
occurred as aSAH sequelae.
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Neuro-ophthalmic outcome
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134
statistical significance existed between eye-movement abnormalities and age, gender, the
135
Fisher, WFNS, and Hunt and Hess grades, the presence of ICH or hydrocephalus, operation
136
modality; or mRS at 6 months.
137
Third-nerve palsies
138
Preoperatively, 4 patients presented with pupil-involving third-nerve palsy due to direct
139
aneurysm compression, and 3 of them had had onset of palsy over 10 days earlier. Seven
140
other patients had a dilated pupil as a result of uncal herniation. Video 1 presents
141
microsurgical clipping of a giant basilar artery (BA) bifurcation aneurysm of a patient with
142
third-nerve palsy (Video 1, Figure 1).
143
Total aneurysm occlusion was achieved in all those with third-nerve palsy by clipping; in one
144
internal carotid - posterior communicating artery (ICA-PComA) aneurysm it was preceded by
145
coiling and re-bleeding after that. All 3 new postoperative oculomotor nerve palsies
146
(aneurysm locations ICA-PComA for 2 of them and BA bifurcation for 1) had totally
147
recovered when examined 3 months after aSAH. Of 2 survivors with ICA-PComA aneurysm
148
and oculomotor nerve palsy on admission, both showed only some limitation in upgaze at 1
149
year. Neither aberrant regeneration nor Weber´s syndrome occurred in the series.
150
Fourth- and sixth-nerve palsies
151
One patient had fourth-nerve palsy as a presenting symptom (in addition to headache) of
152
aSAH at childbirth. A thrombosed fusiform aneurysm of a distal branch of the anterior
153
inferior cerebellar artery (AICA) was visible in the operation as adhered to the ipsilateral
154
fourth nerve (Video 2, Figure 2). Another patient with a BA-AICA aneurysm underwent
155
clipping surgery after failure of an attempt at coil embolization; postoperatively she
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157
Aneurysm occlusion without ischemic complications on head CT scan was complete. The
158
sixth-nerve palsies completely recovered, but the fourth-nerve palsy was persisting at 1 year.
159
Of 6 patients, 5 presented with bilateral sixth-nerve palsy on admission, and 4 also had
160
hydrocephalus. All sixth-nerve palsies already showed total improvement when examined at 3
161
months.
162
Other eye-movement abnormalities
163
One male patient with a left vertebral artery- posterior inferior cerebellar artery aneurysm
164
(PICA) and infarction in the PICA territory experienced acute rotatory vertigo, and the
165
aneurysm was clipped without additional ischemic changes on CT. This patient developed
166
peripheral left facial nerve palsy, nystagmus when looking to the right, and moderate hearing
167
loss in the left ear consistent with a lateral ponto-medullary syndrome. Facial nerve function
168
partially recovered, but his hearing loss persisted at 1 year.
169
Three patients had Parinaud´s syndrome appearing as a paralysis of upgaze and pupils
170
constricting with near viewing but not to light. One of them also had a unilateral and another
171
had bilateral sixth-nerve palsy. Aneurysm locations were anterior communicating artery in 2
172
of them and ICA-PComA in 1, and they all had hydrocephalus and mild spasm. Two of these
173
patients underwent clipping, and 1 needed a permanent shunt. One patient underwent
174
endovascular coiling and became dependent on an external ventricular drainage device
175
(EVD), since whenever the threshold for drainage was risen, headache, worsened diplopia,
176
and supranuclear paralysis of upgaze occurred until we lowered the threshold again. No
177
ischemic changes were visible in MRI in the mesencephalic tectum, but the ventricles were
178
dilated. Since this patient also suffered from intraventricular hemorrhage, a Clostridium
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180
was preferred to a permanent shunt at 2 weeks. Parinaud´s syndrome greatly improved soon
181
after the operation, and he never needed a permanent shunt.
182
Seven patients presented on admission with gaze paresis. All of these had an ICH (5 temporal,
183
2 frontal), and 6 of those with an MCA bifurcation aneurysm, contralateral hemiparesis, and
184
gaze deviation. Each of these totally improved during the hospital stay. Additionally, a female
185
patient with a left distal fusiform PICA aneurysm underwent PICA-PICA anastomosis, and
186
the next day clipping proximal to the aneurysm. A head CT scan showed infarctions in both
187
cerebellar hemispheres. She presented with a partial Wallenberg´s syndrome and an ipsilateral
188
horizontal gaze paresis to the right accompanied by mild temporary contralateral motor
189
hemiparesis. At 1 year, her gaze paresis still persisted.
190
DISCUSSION
191
This first prospective study of eye-movement abnormalities in an unselected series of
192
consecutive patients with aSAH undergoing an operation showed that 9% of the patients had a
193
third-, fourth- or sixth-nerve palsy on admission, and 13% immediately after operation.
194
During a year, however, most of these patients experienced a total recovery, leaving only
195
2.5% of all patients with a partial palsy. The results represent the entire scale of aSAH
196
including vertebro-basilar aneurysms and all grades on the Hunt and Hess scale with a low
197
drop-out rate.
198
As to the limitations of the study, decreased level of consciousness may have masked eye-
199
movement abnormalities in critically ill patients. We reported only those findings that were
200
definite.
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ACCEPTED MANUSCRIPT On admission, the prevalence of sixth-nerve palsies was highest (5.0%), followed by third
202
(3.3%), and fourth-nerve palsies (0.8%). Laun et al., in their retrospective analysis among
203
patients with sSAH, reported third-nerve palsies to be the most frequent finding (7.1%),
204
followed by sixth- (3.0%) and fourth-nerve (0.2%) palsies (25). They had significantly more
205
BA-superior cerebellar artery (SCA) aneurysms, which can explain their higher frequency of
206
third-nerve palsies. Likewise, Tsementzis et al. revealed third-nerve palsies to be most
207
common in their series of 28 patients with aSAH (39).
208
Third-nerve palsies
209
In the present study, for those with ICA-PComA aneurysms, third-nerve palsy occurred
210
preoperatively in 12%. Some older series report rates as high as 34% to 56% (14, 35).
211
Probable factors lowering the current percentage include our unselected series, improved
212
imaging modalities enabling detection of smaller aneurysms causing the aSAH, and faster
213
access to angiography. Our findings are more consistent with those of Leivo et al.: among a
214
retrospective series of 1314 patients with cerebral aneurysms, they reported 35 (2.7%)
215
unilateral third-nerve palsies, and their total of 183 patients with an ICA-PComA aneurysm
216
included 29 oculomotor palsies (21 with aSAH), (15.8%) (26).
217
Improvement of a third-nerve palsy due to direct ICA-PComA aneurysm compression after
218
clipping surgery has been convincing (3, 11, 13, 24, 35). The effectiveness of endovascular
219
coiling in oculomotor nerve recovery has been a matter of debate; suggested mechanisms in
220
various reports include disappearance of aneurysmal pulsation and subsequent shrinking that
221
relieves the compressive effect (2, 15, 20, 23, 27, 29). Statistical analysis in the current study
222
showed no association between eye-movement abnormalities and endovascularly or
223
microsurgically treated patients; the small sample size of endovascularly treated aneurysms,
224
however, precludes drawing definite conclusions about the effect of treatment modality.
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ACCEPTED MANUSCRIPT In the present study, 2 survivors with an ICA-PComA aneurysm had a partial palsy remaining
226
at 1 year based on rather stringent criteria. One with a BA bifurcation giant aneurysm-related
227
partial palsy showed a total recovery. They each had had a delay in admission of more than 10
228
days. In addition to an initial partial palsy (3, 11, 24), recovery has been particularly favorable
229
for those operated on early (8, 11, 13, 35), especially within 3 days after palsy onset (26). It is
230
our policy to perform the operation as soon as possible when a patient harbors a third-nerve
231
palsy caused by a ruptured aneurysm. All of our new postoperative oculomotor nerve palsies
232
resolved completely within 3 months. Based on a series of oculomotor complications
233
following surgical treatment of BA bifurcation aneurysms, Cruciger et al. reported recovery
234
from isolated palsy to be excellent if it avoids injury to the brain stem (5).
235
Fourth- and sixth-nerve palsies
236
Trochlear nerve palsies associated with aSAH are rare, and the literature has few reports on
237
this topic (25, 31, 34, 39). A thrombosed fusiform aneurysm of a distal branch of the AICA
238
presenting with trochlear nerve palsy in our series was a very rare finding. Some reports on
239
ruptured (31) and unruptured distal SCA aneurysms presenting with fourth-nerve palsy do
240
exist (4, 6, 10, 33). As trochlear nerve palsies are the most challenging of the ocular motor
241
nerve palsies to diagnose, they are probably underdiagnosed on hospital wards, which is also
242
reflected in the number of published case reports.
243
Sixth-nerve palsies in the acute stage were bilateral in 5 of our 6 cases, and all showed rapid
244
improvement, which is a similar finding to that of Laun et al. who saw a rapid regression in
245
89% (25). The most likely explanation for these palsies in our series was increased ICP due to
246
aSAH; the abducens nerves are anchored in Dorello´s canal, making it prone to pressure and
247
stretching. No direct compression of the aneurysm was evident. Other suggested mechanisms
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ACCEPTED MANUSCRIPT for sixth-nerve palsies include a clot in the basal cisterns or intracisternal entrapment of
249
cerebrospinal fluid compressing the abducens nerves (12, 40).
250
Other eye-movement abnormalities
251
Horizontal gaze paresis may follow pontine or large hemispheric damage. In the acute phase
252
of a frontal lobe lesion, the eyes will deviate toward the side of the lesion, and the ability to
253
generate saccades in the opposite direction may be impaired. Damage in the paramedian
254
pontine reticular formation (PPRF), in turn, results in complete horizontal gaze paresis on the
255
affected side (32). All 7 patients in the current study with gaze deviation with cerebral
256
hemispheric basis improved soon after aSAH. Findings in our patient with an ipsilateral
257
horizontal gaze paresis accompanied by contralateral hemiparesis are consistent with an
258
infarction in the midpontine tegmentum involving part of the pyramidal tract and the PPRF.
259
Her gaze paresis persisted, since dysfunction of the PPRF does not recover well (22).
260
Parinaud´s syndrome has been reported to exist in the setting of SAH (28). Three of our
261
patients presented with reversible Parinaud´s syndrome: of these, one apparently being EVD-
262
dependent. Mechanisms behind Parinaud´s syndrome in hydrocephalus include dilatation of
263
the posterior part of the third ventricle and of the rostral aqueduct with axial displacement of
264
these structures and stretching of the posterior commissure (30, 37). Identifying this syndrome
265
as causing visual complaints can assist and expedite treatment decisions.
266
CONCLUSIONS
267
In conclusion, eye-movement abnormalities are quite a common finding in the acute stage of
268
aSAH. Within one year, however, marked improvement occurs, and the prognosis of surgery-
269
related third-nerve palsy is usually excellent. Identifying these abnormalities can assist in
270
localization and treatment decisions regarding the underlying pathology.
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ACCEPTED MANUSCRIPT 271
Acknowledgement: This study was supported by grants from the Finnish Eye Foundation,
272
the Finnish Eye and Tissue Bank Foundation, the Evald and Hilda Nissi Foundation, and the
273
Maire Taponen Foundation.
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21. Keane JR: Fourth nerve palsy: Historical review and study of 215 inpatients. Neurology
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22. Kelley RE, Kovacs AG: Horizontal gaze paresis in hemispheric stroke. Stroke 17:1030-
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24. Kyriakides T, Aziz TZ, Torrens MJ: Postoperative recovery of third nerve palsy due to
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25. Laun A, Tonn JC: Cranial nerve lesions following subarachnoid hemorrhage and
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26. Leivo S, Hernesniemi J, Luukkonen M, Vapalahti M: Early surgery improves the cure of
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Resolution of cranial nerve paresis after endovascular management of cerebral aneurysms.
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28. Maramattom BV, Wijdicks EF: Dorsal mesencephalic syndrome and acute hydrocephalus
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29. Mavilio N, Pisani R, Rivano C, Testa V, Spaziante R, Rosa M: Recovery of third nerve
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30. Osher RH, Corbett JJ, Schatz NJ, Savino PJ, Orr LS: Neuro-ophthalmological
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31. Papo I, Caruselli G, Salvolini U: Aneurysm of the superior cerebellar artery. Surg Neurol
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32. Pedersen RA, Troost BT: Abnormalities of gaze in cerebrovascular disease. Stroke
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33. Peluso JP, van Rooij WJ, Sluzewski M, Beute GN: Distal aneurysms of cerebellar
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occlusion. AJNR Am J Neuroradiol 28:1573-1578, 2007.
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34. Son S, Park CW, Yoo CJ, Kim EY, Kim JM: Isolated, contralateral trochlear nerve palsy
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Neurol Neurosurg Psychiatry 37:475-484, 1974.
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36. Stiebel-Kalish H, Maimon S, Amsalem J, Erlich R, Kalish Y, Rappaport HZ: Evolution of
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37. Swash M: Periaqueductal dysfunction (the Sylvian aqueduct syndrome): A sign of
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38. Teasdale GM, Drake CG, Hunt W, Kassell N, Sano K, Pertuiset B, De Villers JC: A
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39. Tsementzis SA, Williams A: Ophthalmological signs and prognosis in patients with a
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40. Ziyal IM, Ozcan OE, Deniz E, Bozkurt G, Ismailoglu O: Early improvement of bilateral
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abducens nerve palsies following surgery of an anterior communicating artery aneurysm. Acta
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Neurochir (Wien) 145:159-161, 2003.
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373
Figure 1. A 54-year-old man presenting with left third-nerve palsy. The patient had had
374
vertical diplopia corrected with prism lenses 1 month before aSAH. Computed tomography
375
angiogram reveals a ruptured giant basilar bifurcation aneurysm. The patient made an
376
excellent overall outcome and total recovery from the palsy after aneurysm clipping.
377
Figure 2. A 41-year-old woman presenting with fourth-nerve palsy. Magnetic resonance
378
imaging demonstrates a thrombosed fusiform aneurysm of a distal branch of the anterior
379
inferior cerebellar artery. The patient made an excellent recovery after resection of the
380
aneurysm; the fourth-nerve palsy completely recovered at 6 months.
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ACCEPTED MANUSCRIPT Table 1. Characteristics of 121 patients with ruptured aneurysm treated during 2011. Sex 55 (45%)
Female
66 (55%)
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Male
Pre-SAH modified Rankin Scale
101 (84%)
Modified Rankin Scale 1
15 (12%)
SC
Modified Rankin Scale 0
Modified Rankin Scale 2
3 (2%) 2 (2%)
Modified Rankin Scale 4-5
Clinical condition on admission
30 (25%)
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Hunt and Hess Grade I Hunt and Hess Grade II Hunt and Hess Grade III
WFNS III WFNS IV
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WFNS II
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Hunt and Hess Grade IV
WFNS I
admission
31 (26%) 19 (16%) 21 (17%) 20 (16%) 49 (40%) 24 (20%) 8 (7%) 10 (8%)
WFNS V Radiological
0
55 (20-84)
Mean age at diagnosis (range)
Hunt and Hess Grade V
M AN U
Modified Rankin Scale 3
30 (25%) findings
on
ACCEPTED MANUSCRIPT Hydrocephalus
63 (52%) 9 (7%)
Fisher scale II
13 (11%)
Fisher scale III
35 (29%)
Fisher scale IV
64 (53%)
Intracerebral hemorrhage
42 (35%)
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Fisher scale I
Treatment
110 (91%)
SC
Surgical Endovascular
11 (9%)
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Clinical outcome at six months Modified Rankin Scale 0
30 (25%)
Modified Rankin Scale 1
34 (28%)
Modified Rankin Scale 3 Modified Rankin Scale 4 Modified Rankin Scale 5
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Modified Rankin Scale 6 (Dead)
13 (11%)
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Modified Rankin Scale 2
17 (14%) 12 (10%) 4 (3%) 10 (8%)
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SAH, subarachnoid hemorrhage; WFNS, World Federation of Neurosurgeons Scale
ACCEPTED MANUSCRIPT
Table 2. Locations of 121 ruptured aneurysms and frequencies associated with third-, fourth-, or sixth-nerve palsies on admission. No, n (%)
III, n (%)
IV, n (%)
14 (11.6)
2 (1.7)
0
True PCom
0
1 (0.8)
0
ICA, other
9 (7.4)
0
0
MCA
36 (29.8)
0
ACA
6 (4.9)
PICA
6 (4.9)
PCA
1 (0.8)
ACom
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Posterior circulation, other Total
0
0
0
0
0
0
0
0
0
0
2 (1.7)
2 (1.7)
0
0
0
1 (0.8)
0
0
0
4 (3.3)
1 (0.8)
0
0
1 (0.8)
0
1 (0.8)
0
110 (90.9)
4 (3.3)
1 (0.8)
6 (5.0)
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BA bifurcation
2 (1.6)
0
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BA-SCA
0
1 (0.8)
30 (24.8)
BA trunk
1 (0.8)
0
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ICA-PComA
SC
Aneurysm location
VI, n (%)
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Cranial nerve palsy
ICA, internal carotid artery; PComA, posterior communicating artery; MCA, medial cerebral artery; ACA, anterior cerebral artery; PICA, posterior inferior cerebellar artery; PCA, posterior cerebral artery; ACom, anterior communicating artery; BA, basilar artery; SCA, superior cerebellar artery
ACCEPTED MANUSCRIPT
Table 3. Eye-movement disorders in 121 patients with ruptured aneurysm treated during 2011. On admission, n
Immediately
At 1 year, n (%)
disorder
(%)
postoperatively, n (%)
Unilateral 2 (1.7)
Complete
2 (1.7)
2 (1.7)
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Partial
SC
Third-nerve palsy
RI PT
Eye-movement
2 (1.7)
5 (4.1)
0
0
0
5 (4.1)
1 (0.8)
0
1 (0.8)
1 (0.8)
1 (0.8)
1 (0.8)
0
0
0
0
1 (0.8)
2 (1.7)
0
0
0
0
Partial
3 (2.5)
3 (2.5)
0
Partial+complete
1 (0.8)
1 (0.8)
0
Bilateral
0
Dilated pupil
4 (3.3)
Fourth-nerve palsy
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Unilateral Partial
Bilateral
Unilateral Partial Complete
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Sixth-nerve palsy
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Complete
Bilateral
ACCEPTED MANUSCRIPT Complete
1 (0.8)
2 (1.7)
0
Parinaud´s
0
3 (2.5)
0
7 (5.8)
5 (4.1)
1 (0.8)
0
1 (0.8)
0
1 (0.8)
1 (0.8)
1 (0.8)
syndrome Horizontal gaze
Wallenberg´s
RI PT
paresis
1 (0.8)
medullary syndrome
AC C
EP
TE D
Skew deviation
M AN U
Lateral ponto-
SC
syndrome
1 (0.8)
1 (0.8)
AC C
EP
TE D
M AN U
SC
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ACCEPTED MANUSCRIPT
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ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT Abbreviations:
AICA: Anterior inferior cerebellar artery, ASAH: Aneurysmal subarachnoid hemorrhage, BA: Basilar artery, CT: Computed tomography, EVD: External ventricular drainage device, ICA:
RI PT
Internal carotid artery, ICH: Intracerebral hemorrhage, ICP: Intracranial pressure, MCA: Medial cerebral artery, MRI: Magnetic resonance imaging, mRS: Modified Rankin Scale, PICA: Posterior inferior cerebellar artery, PComA: Posterior communicating artery, PPRF: Paramedian pontine
SC
reticular formation, SCA: Superior cerebellar artery, WFNS: World Federation of Neurosurgical
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Societies
ACCEPTED MANUSCRIPT Disclosure – Conflict of Interest
Acknowledgement: Elina Koskela has received grants from the Finnish Eye Foundation, the Finnish Eye and Tissue Bank Foundation, the Evald and Hilda Nissi Foundation and the Maire Taponen Foundation.
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related to this study. The other authors report no conflicts of interest.
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Disclosure: Aki Laakso has received consulting fees from Orion Pharma Ltd, Espoo, Finland, not
