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CLINICAL STUDIES
EVOLUTION OF OCULOMOTOR NERVE PARESIS AFTER
ENDOVASCULAR COILING OF POSTERIOR
COMMUNICATING ARTERY ANEURYSMS: A NEURO-OPHTHALMOLOGICAL PERSPECTIVE
Hadas Stiebel-Kalish, M.D.Department of Ophthalmology,Rabin Medical Center, PetahTikva, Israel
Shimon Maimon, M.D.Division of InterventionalNeuroradiology, Department ofRadiology, Rabin Medical Center,Petah Tikva, Israel
Jacob Amsalem, M.D.Division of InterventionalNeuroradiology, Department ofRadiology, Rabin Medical Center,Petah Tikva, Israel
Rita Erlich, M.D.Department of Ophthalmology,Rabin Medical Center, PetahTikva, Israel
Yuval Kalish, Ph.D.Department of Psychology,University of Melbourne,Melbourne, Australia
Z. Harry Rappaport, M.D.Department of Neurosurgery,Rabin Medical Center, PetahTikva, Israel
Reprint requests:Hadas Stiebel-Kalish, M.D.,Division of Neuro-ophthalmology,Department of Ophthalmology,Rabin Medical Center, Petah Tikva49100, Israel.Email: [email protected]
Received, February 28, 2003.
Accepted, August 14, 2003.
OBJECTIVE: Guglielmi detachable coil treatment is becoming an accepted alternative tomicrosurgical clipping for select intracerebral aneurysms. Resolution of oculomotor nerveparesis (ONP) after endovascular packing was claimed to be complete in two prior series,with three and six cases. We describe the evolution of ONP after Guglielmi detachablecoil treatment of posterior communicating artery aneurysms, and we search for endovas-cular and patient factors correlated with the degree of functional nerve recovery.METHODS: Twelve cases of ONP attributable to posterior communicating artery aneu-rysms were treated with Guglielmi detachable coils between 1999 and 2002. Elevenpatients were available for follow-up monitoring. The degree of ONP was recorded atadmission, at discharge, after 3 months, and at yearly intervals thereafter. The size of theaneurysm, the duration of ONP before coiling, the degree of coiling, age, and the presenceof other microvascular risk factors were correlated with the degree of nerve recovery.RESULTS: Complete resolution of ONP did not occur in any of the 11 cases in thisseries. However, residual oculomotor nerve deficits did not cause diplopia withprimary gaze for 10 of 11 patients. Clinically significant ptosis did not persist for anyof the patients. The pupil remained minimally affected in all cases.CONCLUSION: Although mass effect remains after endovascular packing, oculomotornerve dysfunction improves comparably to the recovery observed after surgical clipping.Contrary to previous reports, typical residual oculomotor nerve deficits persist. Older ageand the presence of microvascular risk factors seem to be detrimental to ONP recovery.
Endovascular Guglielmi detachable coil(GDC) therapy has an increasingly impor-tant role as an alternative to microsurgical
clipping for treatment of select intracerebral an-eurysms (8). Although it is more comfortable forthe patient and is often associated with lowercomplication rates, coiling is not thought to re-solve all of the mass effect caused by aneurysms.The proposed mechanism by which coiling re-lieves adjacent-structure pressure is the lessen-ing of pulsations after aneurysm thrombosis.Resolution of oculomotor nerve paresis (ONP)after endovascular packing was claimed to becomplete in two prior series, describing a com-bined total of nine cases (1, 7). We describe aseries of 11 patients who were treated with en-
dovascular packing for posterior communicat-ing artery (PComA) aneurysms, with closeneuro-ophthalmological follow-up monitoring.
PATIENTS AND METHODS
Two hundred thirty small or large aneu-rysms among 185 patients were treated withendovascular coiling at our institution be-tween 1999 and 2001. A total of 12 patientsexperienced ONP resulting from PComA an-eurysms treated with GDCs. One patient diedshortly after the procedure, as a result of com-plications of cardiovascular disease. The re-maining 11 patients were prospectively exam-
ined by a neuro-ophthalmologist (HS-K) and by aninterventional neuroradiologist (SM).
All endovascular procedures were performed by one inter-ventional neuroradiologist (SM), using general anesthesia, livesimultaneous road-mapping (mainly via biplane imaging),and systemic heparinization (adjusted to an activated clottingtime of 250–300 s). All treatments were performed via thetransfemoral route; 6-French guiding catheters were posi-tioned in the internal carotid artery. Tracker-10, Tracker-18, orExcel-14 microcatheters (Boston Scientific/Target, Fremont,CA) were used to treat the aneurysms with GDC-10 orGDC-18 coils (Boston Scientific/Target). At the end of theprocedure, all patients were transferred to the neurosurgicalintensive care unit for observation. Heparin was administeredfor 24 hours after the procedure. The duration of hospitaliza-tion depended on the course and severity of the disease. Onepatient with an unruptured aneurysm was discharged within3 days. The patients with subarachnoid hemorrhage weremonitored for the presence of vasospasm with transcranialDoppler ultrasonography and were treated prophylacticallywith nimodipine. Digital subtraction angiography was sched-uled at 3 and 15 months, and magnetic resonance imagingassessments were scheduled at yearly intervals thereafter. Thecompleteness of aneurysm closure was noted. One patientdemonstrated coil compaction (from 100% to 90% occlusion)at the 3-month follow-up angiographic examination and wasretreated with GDCs.
The interventional radiologist prospectively recorded infor-mation on the clinical Hunt and Hess grade and the aneurysmsize. The neuro-ophthalmologist prospectively recorded theduration of ONP before treatment for each patient and thedegree of ONP at admission before treatment, at discharge,after 3 months, and at yearly intervals thereafter. Patient ageand the presence of other microvascular risk factors (smoking,diabetes mellitus, and hypertension) were noted. Aneurysmand patient risk factors were correlated with the degree ofONP recovery by using two different analyses, i.e., effect sizeanalysis (Cohen’s D test) (2) and Fisher’s exact test. An effectsize (Cohen’s D value) of more than 0.3 was considered toindicate a small meaningful effect. An effect size of 0.5 or moresignified a medium-size effect. The degree of ONP was clas-sified into three categories, as follows: 1) minimal residualONP, defined as an upgaze deficit (trace underaction of thesuperior rectus muscle) with mild diplopia present only dur-ing looking up; 2) moderate residual ONP, with diplopiapresent with upgaze (superior rectus muscle) or downgaze(inferior rectus muscle) but not primary gaze, or 3) significantresidual diplopia with primary gaze, with a slight adductiondeficit (medial rectus muscle) in addition to a mild upgazedeficit.
RESULTS
Follow-up data were available for all 11 patients, for peri-ods ranging from 8 months to 3 years. The ages of the patientsranged from 30 to 77 years. A history of smoking was noted
for seven patients. Hypertension was present for seven pa-tients, two of whom were also being treated for diabetesmellitus. Five patients had a large PComA aneurysm as thecause of their ONP, whereas six had a small aneurysm of lessthan 1 cm in its largest diameter. Three patients were admittedin Hunt and Hess Grade III, seven were admitted in Grade I orII, and one patient was admitted without aneurysm rupture.All patients exhibited complete pupil-involving ONP, begin-ning 3 to 23 days before treatment (mean, 9 d). The duration ofONP before coiling for each patient is presented in Table 1.Severe ipsilateral retro-orbital pain and headache was a prom-inent feature for five of the patients (45%), beginning days tomonths before ONP.
Complete recovery of oculomotor nerve function was not ob-served for any of the 11 patients in this series. The ONP recoveryresults are detailed in Table 1. Residual oculomotor nerve motordeficits did not cause diplopia with primary gaze (lookingstraight ahead) for 10 of 11 patients. Four patients exhibitedminimal residual ONP. Six patients exhibited moderate residualONP, and one patient complained of significant residual diplopiawith primary gaze as well as upgaze and downgaze.
Mild ptosis of 1 to 2 mm, compared with the contralateraleye, persisted for all patients, but this did not cause anyclinical disability because the pupil was not covered. Thepupil remained minimally affected for all patients. All patientsexhibited a residual sluggish direct reaction to light in theaffected pupil. The 11 patients exhibited mild anisocoria, withthe affected pupil being persistently 1.5 to 5 mm larger thanthe contralateral pupil. Aberrant regeneration, in the form of alid lag with downgaze (pseudo-von Graefe’s sign), was ob-served for 3 of 11 patients (27%).
Endovascular features of the 11 PComA aneurysms aredetailed in Table 2. There were five patients with large aneu-rysms (�10 mm), three of whom were left with moderate ONPdefects. Of the six patients with small aneurysms, three wereleft with moderate ONP (P � 0.65, Cohen’s D � 0.46). Two ofthe four patients with aneurysms coiled more than 10 daysafter the onset of symptoms and five of the seven patients withaneurysms treated within 10 days after ONP onset demon-strated residual moderate or significant ONP at the 1-yearfollow-up assessments (P � 0.470, Cohen’s D � 0.26). Of thesix patients whose aneurysms were completely closed duringthe initial treatment, three exhibited minimal ONP at 1 year.Of the four patients with nearly complete initial occlusion(95–99%), two exhibited minimal residual ONP. One patientexperienced a cerebral stroke resulting from vasospasm dur-ing her initial coiling procedure. The procedure was stopped,and the patient was left with 50% occlusion of her aneurysm.Ten days later, a second endovascular treatment was per-formed, with nearly complete occlusion.
On repeat angiograms obtained at 3 months, 9 of 11 patientsdemonstrated complete or nearly complete closure of their an-eurysms. Coil compaction, leading to 90% occlusion or less,occurred for two patients. One of those two patients (Patient 8)was left with significant ONP, which did not improve afterrecoiling (Table 2). The other patient was the aforementioned
NEUROSURGERY VOLUME 53 | NUMBER 6 | DECEMBER 2003 | 3
patient with vasospasm and stroke (Patient 6); she elected not tobe retreated (Table 2). On 3-month angiograms, two aneurysmsexhibited slight coil compaction, from complete to nearly com-plete occlusion. One of those two patients remained with un-changed minimal ONP, whereas the other was left with a stablemoderate oculomotor nerve deficit. We did not observe a corre-lation between the Hunt and Hess grade at the time of presen-tation and the degree of eventual ONP recovery.
Five of six patients older than 60 years were left with resid-ual moderate or significant ONP. Two of the five youngerpatients demonstrated persistent moderate ONP (P � 0.197).When age was analyzed as a continuous variable with respectto the degree of ONP recovery, it seemed that older patientsrecovered less than did their younger counterparts (Cohen’s D� 0.50). Four of the seven smokers were left with moderateoculomotor nerve deficits, whereas three of the four nonsmok-ers exhibited similar residual deficits (P � 0.53). Of the sevenpatients left with more than minimal oculomotor nerve defi-cits, six had either hypertension or hypertension and diabetesmellitus; minimal ONP occurred for one of the hypertensivepatients (P � 0.088). Cohen’s D value correlating the presenceof microvascular risk factors (0, no microvascular risk factors;1–3, presence of smoking, hypertension, and/or diabetes mel-litus) with the degree of ONP recovery was 0.58. Table 3presents patient risk factors and the degree of ONP recovery.
DISCUSSION
The resolution of ONP after endovascular packing ofPComA aneurysms was reported to be complete by Mavilio et
al. (7) and Birchall et al. (1), who reported six and three cases,respectively. Those nine patients did not undergo full record-ings of motor defects in all cardinal fields of gaze or assess-ments of levator palpebrae muscle and pupil function. Thepatients in those two series were reported to have experiencedresolution of diplopia with primary gaze, as did most (91%) ofthe patients in this series. Incomplete resolution of ONP aftersurgical clipping has been well documented (3–6, 9). Thetypical pattern of recovery observed in our series, in which thelevator palpebrae and medial rectus muscles demonstratedrapid recovery and the parasympathetic fibers of the pupiland the superior and inferior rectus muscles lagged behind,was previously described by Hamer (4). In a recent report byYanaka et al. (10), describing 15 patients who were treated forsmall unruptured aneurysms (14 after microsurgical clippingand 1 after intravascular embolization), 6 patients (37.5%)were noted to exhibit incomplete ONP recovery, whereas 2(12.5%) exhibited no change. The fact that Yanaka et al. (10)reported 43.8% complete ONP recovery might be attributableto the fact that only small unruptured aneurysms were in-cluded. Those authors also observed that a shorter intervalbetween the onset of ONP and treatment was beneficial forONP recovery. It is possible that time was not demonstrated tobe an important factor in our series because the mean intervalbetween the onset of treatment and ONP was 9 days, com-pared with a mean of 17 days in the series reported by Yanakaet al. (10).
Careful neuro-ophthalmological follow-up monitoring inour series revealed that true complete cure of ONP did not
TABLE 2. Angiographic features of the 11 posterior communicating artery aneurysms causing oculomotor nerve paresisa
4 | VOLUME 53 | NUMBER 6 | DECEMBER 2003 www.neurosurgery-online.com
T3
occur often. We hope that recognition of the typical residualdeficits and monitoring of those deficits after endovascularcoiling can assist endovascular surgeons in the early recogni-tion of coil compaction and aneurysm reopening. Withoutregular neuro-ophthalmological follow-up monitoring, it maybe difficult to recognize subtle signs of worsening or a lack ofexpected improvement.
As Cohen (2) noted, statistical significance (P values) isstrongly influenced by sample size and may thus confoundany interpretation. A more appropriate approach for smallsamples is the use of effect size (Cohen’s D value), whichrepresents the standardized mean difference between groups.Effect size is not influenced by sample size and thus providesvalid reliable estimates of effects. An effect size of 0.3 or moreis considered to indicate a small meaningful effect, whichshould become statistically significant with a larger samplesize. In addition to this analysis, we performed the morewidely known Fisher’s exact test. Each analysis confirmed theresults of the other. It seems that a pattern of patient factorspredicting poor recovery can be recognized. Eighty-three per-cent of patients older than 60 years were left with moderate orsignificant oculomotor nerve deficits, compared with 40% ofyounger patients (P � 0.197). Cohen’s D test confirmed theimportance of age as a poor prognosticator of nearly completerecovery. Microvascular risk factors other than age (hyperten-sion, diabetes mellitus, and a history of smoking) were alsoobserved more often among patients with moderate or severeresidual ONP. Twenty-five percent of patients without hyper-tension or diabetes mellitus remained with moderate ONP,compared with 86% of patients with those risk factors (P �0.088). Cohen’s D test demonstrated that patients with more
microvascular risk factors had lesser chances of nearly com-plete recovery (Cohen’s D � 0.67). Fisher’s exact test did notdemonstrate effects of aneurysm size or duration of ONPbefore coiling on the degree of ONP recovery in this smallseries, which might preclude the recognition of significantstatistical trends. However, Cohen’s D test demonstrated analmost medium-size effect of size on ONP recovery (Cohen’sD � 0.46). Coil compaction to nearly complete occlusion after3 months could not be demonstrated to affect outcomes. De-spite the small number of such cases, it should be noted thattwo patients whose coils compacted to partial (50%) or 90%occlusion did experience worse outcomes. We hope that fu-ture reports will indicate whether poor ONP recovery mightsuggest significant coil compaction among patients who areexpected to fare better.
CONCLUSIONS
Small residual oculomotor nerve deficits, mainly diplopiawith upward or downward gaze, are often observed afterendovascular coiling. This finding is contrary to the results ofprevious small studies of outcomes after coiling and is similarto the results observed after surgical clipping. Older age andthe presence of microvascular risk factors might decrease thechances of ONP recovery.
REFERENCES
1. Birchall D, Khangure MS, McAuliffe W: Resolution of third nerve paresisafter endovascular management of aneurysms of the posterior communicat-ing artery. AJNR Am J Neuroradiol 20:411–413, 1999.
TABLE 3. Correlation of endovascular and patient risk factors with the degree of oculomotor nerve paresis recoverya
4. Hamer J: Prognosis of oculomotor palsy in patients with aneurysms ofthe posterior communicating artery. Acta Neurochir (Wien) 66:173–185,1982.
5. Kyriakides T, Aziz TZ, Torrens MJ: Postoperative recovery of third nervepalsy due to posterior communicating aneurysms. Br J Neurosurg 3:109–111, 1989.
6. Leivo S, Hernesniemi JA, Luukkonen M, Vapalahti MP: Early surgeryimproves the cure of aneurysm-induced oculomotor palsy. Surg Neurol45:430–434, 1996.
7. Mavilio N, Pisani R, Rivano C, Testa V, Spaziante R, Rosa M: Recovery ofthird nerve paresis after endovascular management of aneurysms of theposterior communicating artery. 6:203–209, 2000.
8. Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J,Holman R: International Subarachnoid Aneurysm Trial (ISAT) of neurosur-gical clipping versus endovascular coiling in 2143 patients with rupturedintracranial aneurysms: A randomised trial. Lancet 360:1267–1274, 2002.
9. Perneczky A, Czech T: Prognosis of oculomotor palsy following subarach-noid hemorrhage due to aneurysms of the posterior communicating artery.Zentralbl Neurochir 45:189–195, 1984.
10. Yanaka K, Matsumaru Y, Mashiko R, Hyodo A, Sugimoto K, Nose T: Smallunruptured cerebral aneurysms presenting with oculomotor nerve palsy.Neurosurgery 52:553–557, 2003.
AQ1—‘Please confirm that this is the correct/desired email address for correspondence concerningyour article. Publication of email address is optional.‘
AQ2—‘Please confirm changes in Table 1 or clarify descriptions and values. Also, define values/provide units for diplopia measurements.‘
AQ3—‘Please confirm changes of “motility” to “motor” or clarify term meant.‘
AQ4—‘Please provide the name of the journal in Reference 7. Unable to locate on Medline.‘
