Acta Neurochir (2015) 157:1103–1111 DOI 10.1007/s00701-015-2440-6
CLINICAL ARTICLE - VASCULAR
Oculomotor nerve palsy induced by internal carotid artery aneurysm: prognostic factors for recovery Julien Engelhardt 1 & Jérôme Berge 2 & Emmanuel Cuny 1,3 & Guillaume Penchet 1
Received: 18 December 2014 / Accepted: 28 April 2015 / Published online: 9 May 2015 # Springer-Verlag Wien 2015
Abstract Background Aneurysms at the posterior face of the internal carotid artery can lead to oculomotor nerve palsy (ONP) with an uncertain prognosis of recovery post-treatment. The aim of this study was to define the prognostic factors for ONP recovery, with particular interest in treatment modality (surgery or endovascular techniques). Method A literature review was performed to select the most pertinent prognostic factors. A retrospective study was then performed to determine whether these factors had significantly modified the prognosis of ONP recovery in our series of patients. Results In the literature, factors linked to poorer outcome were age, vascular risk factors, initial ONP severity and delay before treatment; better recovery was associated with surgical treatment. Between 2000 and 2013, 23 consecutive patients were treated in our department for ONP-inducing aneurysms: 14 by endovascular embolization and 9 by surgical clipping and aneurysm puncture. Mean follow-up was 48.8 months. After treatment, overall recovery occurred in 87 % of cases, always within 6 months. Apart from treatment modality, no Portions of this work were presented in abstract form at the National Congress of The French Neurosurgical Society, Dijon, France, 6 April 2011. * Julien Engelhardt [email protected] 1
CHU Pellegrin, Service de Neurochirurgie B, Hôpital Pellegrin-Tripode, Place Amélie Raba-Léon, 33 076 Bordeaux Cedex, France
2
CHU Pellegrin, Service de Neuroimagerie Diagnostique et Thérapeutique, Bordeaux, France
3
Université de Bordeaux, Bordeaux, France
selected prognostic factor significantly modified the quality or timing of ONP recovery. In the endovascular group, four patients recovered completely, seven partially and three did not recover. In the surgical group, seven patients recovered completely and two partially. Surgery was significantly associated with a more complete and earlier ONP recovery (p3 or 5 days depending on the series) [1, 8, 15, 17, 24]. Equally, the positive prognostic value of subarachnoid hemorrhage (SAH) [15] and surgical treatment versus endovascular management of ONP-inducing aneurysm [1, 3, 7, 9, 14, 19, 21, 24] remains uncertain. Thus, considering that the debate over endovascular and surgical treatment of ONP-inducing aneurysms remains unresolved, and that any prognostic factors reportedly active in ONP recovery remain controversial, we aimed to ascertain whether the treatment modality and such prognostic factors had affected recovery in our own series of patients. In our literature review, the six factors most commonly reported to affect ONP prognosis were age, vascular risk factors, degree of initial ONP, delay before treatment, SAH and, of particular interest to our study, treatment modality.
Acta Neurochir (2015) 157:1103–1111
Endpoints The primary endpoint was the quality of ONP recovery after treatment, evaluated by the degree of ONP recovery after at least 1 year of routine postoperative follow-up. The secondary endpoint was the timing of recovery, approximated by an evaluation of the ONP recovery at regular intervals (1 week after treatment, 2 months, 6 months, 1 year and once a year).
Oculomotor nerve palsy definition The preoperative ONP degree was defined as follows: –
–
total if all signs of extrinsic (i.e., ptosis, palsy of the superior, inferior and medial rectus muscles and inferior oblique muscle) and intrinsic (areactive mydriasis) impairment were shown; partial if only some of these signs were present.
Degree of ONP recovery (total vs. partial) was defined by ophthalmologic examination: – –
total if all of the signs had disappeared; partial if signs of extrinsic or intrinsic impairment persisted.
Patients and methods
Data collection
Informed patient consent
ONP recovery was retrospectively analyzed. We reviewed all records of routine follow-up consultations for the first year after treatment conducted by the neurosurgeon and/or the neuroradiologist (depending on the treatment chosen), during which a simple ophthalmologic examination including interrogation (to evaluate functional signs such as diplopia, blurred vision, eyestrain) and physical examination (looking for ptosis, mydriasis and ophtalmoplegia) was performed and noted. All operative or endovascular intervention reports were reviewed to confirm, in the case of surgery, the exclusion by clipping followed by systematic puncture of the aneurysm or, in the case of endovascular intervention, a pure coiling embolization without the use of additional devices (such as stents or flow diverters) as a first treatment (i.e., emergency treatment and not second-step embolization for recanalization). Finally, all postoperative digital subtracted angiography (DSA) or angioCT scans were reviewed in order to confirm the total and definitive exclusion of aneurysms without signs of recanalization. Long-term follow-up was conducted by phone interview in which an independent investigator, unaware of precedent medical data, employed a standardized questionnaire (Fig. 1).
The regional ethics committee (Comité de Protection des Personnes, Sud-Ouest et Outre-Mer) was informed about this retrospective study and did not deem it necessary to compile an official report because of the study’s retrospective character as well as the fact that it did not modify current patient care or require the use of further radiological examination. Consent was, however, obtained from patients (or their family) for the examination of their medical records as well as for their participation in a phone interview. All patients were over 18 years old. Patient selection Hospital records of patients treated in our unit between January 2000 and June 2013 for aneurysm in the supraclinoid segment of the internal carotid artery (ICA) leading to III cranial nerve palsy were systematically reviewed. All consecutive patients who underwent surgical clipping or endovascular coiling of any aneurysm inducing ONP were included.
Acta Neurochir (2015) 157:1103–1111
1105
Treatment modality Fourteen patients were treated by embolization and nine by surgery. All surgically treated aneurysms were excluded by clipping and then punctured. The third cranial nerve was systematically checked and found to be free of all vascular and clip conflict at the end of the surgery in all cases. In the endovascular group, no devices other than coils were used in the first intervention. After initial embolization, occlusion of the aneurysm was complete in 12 patients (class I of the Raymond-Roy Occlusion Classification) and incomplete, with a residual neck, in 2 patients (class II). These two aneurysms went on to develop secondary recanalization. Fig. 1 Standardized questionnaire
Statistical analysis We tested the relationship between major prognostic factors of ONP recovery (i.e., those that were statistically significant in previous studies: age, initial degree of ONP, delay before treatment, SAH, vascular risk factors and treatment modality) and our two endpoints (quality and speed of recovery) in univariate and multivariate analysis. Student's test was used to compare quantitative variables between two groups (e.g., endovascular vs. surgical treatment), an ANOVA test (variance analysis) to compare quantitative variables among more than two groups (e.g., total, partial and no recovery) and a Fisher's exact test for the qualitative variables because the sample size was too small for χ2 testing. Timing of recovery was described by Kaplan-Meier curves and compared using the log-rank test. Differences were considered significant at the level of p
CLINICAL ARTICLE - VASCULAR
Oculomotor nerve palsy induced by internal carotid artery aneurysm: prognostic factors for recovery Julien Engelhardt 1 & Jérôme Berge 2 & Emmanuel Cuny 1,3 & Guillaume Penchet 1
Received: 18 December 2014 / Accepted: 28 April 2015 / Published online: 9 May 2015 # Springer-Verlag Wien 2015
Abstract Background Aneurysms at the posterior face of the internal carotid artery can lead to oculomotor nerve palsy (ONP) with an uncertain prognosis of recovery post-treatment. The aim of this study was to define the prognostic factors for ONP recovery, with particular interest in treatment modality (surgery or endovascular techniques). Method A literature review was performed to select the most pertinent prognostic factors. A retrospective study was then performed to determine whether these factors had significantly modified the prognosis of ONP recovery in our series of patients. Results In the literature, factors linked to poorer outcome were age, vascular risk factors, initial ONP severity and delay before treatment; better recovery was associated with surgical treatment. Between 2000 and 2013, 23 consecutive patients were treated in our department for ONP-inducing aneurysms: 14 by endovascular embolization and 9 by surgical clipping and aneurysm puncture. Mean follow-up was 48.8 months. After treatment, overall recovery occurred in 87 % of cases, always within 6 months. Apart from treatment modality, no Portions of this work were presented in abstract form at the National Congress of The French Neurosurgical Society, Dijon, France, 6 April 2011. * Julien Engelhardt [email protected] 1
CHU Pellegrin, Service de Neurochirurgie B, Hôpital Pellegrin-Tripode, Place Amélie Raba-Léon, 33 076 Bordeaux Cedex, France
2
CHU Pellegrin, Service de Neuroimagerie Diagnostique et Thérapeutique, Bordeaux, France
3
Université de Bordeaux, Bordeaux, France
selected prognostic factor significantly modified the quality or timing of ONP recovery. In the endovascular group, four patients recovered completely, seven partially and three did not recover. In the surgical group, seven patients recovered completely and two partially. Surgery was significantly associated with a more complete and earlier ONP recovery (p3 or 5 days depending on the series) [1, 8, 15, 17, 24]. Equally, the positive prognostic value of subarachnoid hemorrhage (SAH) [15] and surgical treatment versus endovascular management of ONP-inducing aneurysm [1, 3, 7, 9, 14, 19, 21, 24] remains uncertain. Thus, considering that the debate over endovascular and surgical treatment of ONP-inducing aneurysms remains unresolved, and that any prognostic factors reportedly active in ONP recovery remain controversial, we aimed to ascertain whether the treatment modality and such prognostic factors had affected recovery in our own series of patients. In our literature review, the six factors most commonly reported to affect ONP prognosis were age, vascular risk factors, degree of initial ONP, delay before treatment, SAH and, of particular interest to our study, treatment modality.
Acta Neurochir (2015) 157:1103–1111
Endpoints The primary endpoint was the quality of ONP recovery after treatment, evaluated by the degree of ONP recovery after at least 1 year of routine postoperative follow-up. The secondary endpoint was the timing of recovery, approximated by an evaluation of the ONP recovery at regular intervals (1 week after treatment, 2 months, 6 months, 1 year and once a year).
Oculomotor nerve palsy definition The preoperative ONP degree was defined as follows: –
–
total if all signs of extrinsic (i.e., ptosis, palsy of the superior, inferior and medial rectus muscles and inferior oblique muscle) and intrinsic (areactive mydriasis) impairment were shown; partial if only some of these signs were present.
Degree of ONP recovery (total vs. partial) was defined by ophthalmologic examination: – –
total if all of the signs had disappeared; partial if signs of extrinsic or intrinsic impairment persisted.
Patients and methods
Data collection
Informed patient consent
ONP recovery was retrospectively analyzed. We reviewed all records of routine follow-up consultations for the first year after treatment conducted by the neurosurgeon and/or the neuroradiologist (depending on the treatment chosen), during which a simple ophthalmologic examination including interrogation (to evaluate functional signs such as diplopia, blurred vision, eyestrain) and physical examination (looking for ptosis, mydriasis and ophtalmoplegia) was performed and noted. All operative or endovascular intervention reports were reviewed to confirm, in the case of surgery, the exclusion by clipping followed by systematic puncture of the aneurysm or, in the case of endovascular intervention, a pure coiling embolization without the use of additional devices (such as stents or flow diverters) as a first treatment (i.e., emergency treatment and not second-step embolization for recanalization). Finally, all postoperative digital subtracted angiography (DSA) or angioCT scans were reviewed in order to confirm the total and definitive exclusion of aneurysms without signs of recanalization. Long-term follow-up was conducted by phone interview in which an independent investigator, unaware of precedent medical data, employed a standardized questionnaire (Fig. 1).
The regional ethics committee (Comité de Protection des Personnes, Sud-Ouest et Outre-Mer) was informed about this retrospective study and did not deem it necessary to compile an official report because of the study’s retrospective character as well as the fact that it did not modify current patient care or require the use of further radiological examination. Consent was, however, obtained from patients (or their family) for the examination of their medical records as well as for their participation in a phone interview. All patients were over 18 years old. Patient selection Hospital records of patients treated in our unit between January 2000 and June 2013 for aneurysm in the supraclinoid segment of the internal carotid artery (ICA) leading to III cranial nerve palsy were systematically reviewed. All consecutive patients who underwent surgical clipping or endovascular coiling of any aneurysm inducing ONP were included.
Acta Neurochir (2015) 157:1103–1111
1105
Treatment modality Fourteen patients were treated by embolization and nine by surgery. All surgically treated aneurysms were excluded by clipping and then punctured. The third cranial nerve was systematically checked and found to be free of all vascular and clip conflict at the end of the surgery in all cases. In the endovascular group, no devices other than coils were used in the first intervention. After initial embolization, occlusion of the aneurysm was complete in 12 patients (class I of the Raymond-Roy Occlusion Classification) and incomplete, with a residual neck, in 2 patients (class II). These two aneurysms went on to develop secondary recanalization. Fig. 1 Standardized questionnaire
Statistical analysis We tested the relationship between major prognostic factors of ONP recovery (i.e., those that were statistically significant in previous studies: age, initial degree of ONP, delay before treatment, SAH, vascular risk factors and treatment modality) and our two endpoints (quality and speed of recovery) in univariate and multivariate analysis. Student's test was used to compare quantitative variables between two groups (e.g., endovascular vs. surgical treatment), an ANOVA test (variance analysis) to compare quantitative variables among more than two groups (e.g., total, partial and no recovery) and a Fisher's exact test for the qualitative variables because the sample size was too small for χ2 testing. Timing of recovery was described by Kaplan-Meier curves and compared using the log-rank test. Differences were considered significant at the level of p
