British Journal of Neurosurgery, December 2014; 28(6): 771–775 © 2014 The Neurosurgical Foundation ISSN: 0268-8697 print / ISSN 1360-046X online DOI: 10.3109/02688697.2014.913780
ORIGINAL ARTICLE
Bilateral abducens nerve palsy associated with subarachnoid hemorrhage Kanwaljeet Garg, Pankaj Kumar Singh, Ashok Kumar Mahapatra & Bhawani Shankar Sharma Department of Neurosurgery, All India Institute of Medical Sciences, New Delhi, India
followed by abducens nerve, which accounts for about one-fifth of all cranial nerve lesions in patients with SAH. The fact that out of all abducens nerve lesions, 3.6% were due to intracranial aneurysms in a large study highlights the rarity of the situation.3 Bilateral abducens nerve involvement is even rarer and is seen in less than 10% of all patients with abducens nerve paresis.3 We describe our experience with SAH patients who developed bilateral abducens nerve palsy.
Abstract Objective. Isolated abducens nerve palsies associated with intracranial aneurysms have rarely been reported. The purpose of the study was to study the patients with bilateral abducens nerve palsy in association with subarachnoid hemorrhage (SAH). Methods. All patients admitted and managed at our center with a diagnosis of SAH and had bilateral abducens nerve palsy were included in the study. The demographic and clinical details, radiological findings, treatment data, and outcome of these patients were retrieved from the computerized database of our hospital. Results. Nine patients, with a mean age of 49.4 years, met the inclusion criteria. Male to female ratio of 1.25:1). Average duration of symptoms before presentation was 2.6 days (ranging from 1 to 4 days). Third nerve palsy in addition to bilateral abducens nerve palsy was present in 4 patients (44%). DSA demonstrated aneurysms in 7 patients; 4 had posterior circulation aneurysms and 3 had aneurysms of anterior circulation. Two patients had angionegative SAH. The abnormality resolved in all but one patient over a time period of 4–9 weeks, and one patient died due to unrelated cause. Conclusions. Bilateral abducens nerve palsy in association with SAH is rarely described. Proposed mechanisms include direct compression of the bilateral abducens nerves, vasospasm of the pontine branches of the basilar artery and hydrocephalous. Most of the patients in our series showed resolution of the symptoms over a period of 4–9 weeks.
Methods At our centre, 2433 patients with intracranial aneurysms were treated from January 2001 through March 2013. Patients who had bilateral abducens nerve palsy at the time of presentation were included in the study group. The data of these patients were retrospectively reviewed from the computerized database of our center. Demographic and clinical details, radiological findings, treatment data, and outcome were analyzed retrospectively. WFNS grade was used to grade the SAH. Computed tomogram followed by intra-arterial digital subtraction angiogram (IADSA) was done in all patients. Findings of IADSA were discussed among the neurosurgeons and neuroradiologists, and the treatment plan according to the aneurysm morphology and location was decided. In case both endovascular coiling and microsurgical clipping were feasible, patient’s attendants were given the option of both and depending on their decision, which is very much influenced by the financial constraints in India, further treatment was done. Once the aneurysm was secured by either means, the management of SAH was consistent with the standard guidelines. Patients were followed up in outpatient department at monthly intervals after intervention till 3 months, and 6 monthly thereafter. Glasgow outcome score (GOS) was used to assess the postoperative and follow-up outcome. A GOS of 4 and 5 was considered to be favorable outcome, whereas a GOS 1–3 was considered to be poor outcome.
Keywords: abducens nerve; aneurysms; bilateral; occulomotor, resolution; subarachnoid hemorrhage
Introduction Abducens nerve palsy is a common cause of diplopia in neurology clinics. It is involved in a number of disorders, may be due to its extremely long intracranial course1 and is the most frequently involved cranial nerve. Common presenting feature of subarachnoid hemorrhage (SAH) includes sudden onset severe headache, ictal loss of consciousness, seizures, and motor deficits. Cranial nerve involvement, especially those supplying extraocular muscles, is reported to occur in about 9% of patients with SAH.2 Third nerve is the most common nerve involved
Results Out of the 2433 patients treated for SAH at our center during the study period, 9 met the inclusion criteria of the study
Correspondence: Dr Pankaj Kumar Singh, Room No 720, Department of Neurosurgery, Cardio-Neuro Centre, All India Institute of Medical Sciences, New Delhi, India. Tel: ⫹ 919968398570. Fax: ⫹ 91-11-26589650. E-mail: [email protected] Received for publication 20 December 2013; accepted 6 April 2014
771
Good (5) Good (5) Good (4) Clipping Coiling Coiling Yes No No B/L VI nerve palsy B/L VI nerve palsy B/L VI nerve palsy 1 3 4 48/F 45/M 55/F 7 8 9
Right PICA AComA aneurysm Right superior hypophyseal
Good (4) Clipping Yes B/L VI nerve palsy 3 45/M 6
Right PICA
4 2 2 45/M 58/F 59/M 3 4 5
VI nerve palsy at final follow up
Resolved in 8 weeks Resolved in 7 weeks Died 12 weeks after surgery due to cardiac illness No improvement at 24 months follow up Resolved in 6 weeks Resolved in 6 weeks Resolved in 4 weeks Good (5) Good (5) Good (4) Conservative Conservative Clipping and V-P shunt Yes Yes No
Good (5) Good (5) Clipping Clipping No Yes
B/L VI nerve palsy Right III nerve palsy B/L VI nerve palsy B/L VI nerve palsy B/L VI nerve palsy B/L VI nerve palsy 1 3
AComA aneurysm Left superior cerebellar aneurysm Angionegative SAH Angionegative SAH Right PICA 57/F 33/M 1 2
Outcome (GOS at discharge) Treatment Duration of symptoms before the Neurological deficits at diagnosis was made (in days) the time of presentation Ventriculomegaly Diagnosis S No Age/Sex
(Table I). The mean age of patients of our study group was 49.4 years (ranging from 43 to 61 years). There were five males and four females in our study group (male to female ratio of 1.25:1). All patients presented with sudden onset severe headache, classical presentation of SAH. Average duration of symptoms before presentation was 2.6 days (ranging from 1 to 4 days). Three patients in our study group were known hypertensive, while 2 (22%) were known diabetic. Examination revealed bilateral abducens nerve palsy in all the 9 patients at the time of presentation to our hospital. Third nerve palsy in addition to bilateral abducens nerve palsy was present in 4 patients (44%). Out of these 4 patients, 3 had unilateral third nerve involvement and one had bilateral involvement of third nerve. All the patients had good grade SAH (WFNS grade II). Computed tomography (CT) revealed subarachnoid blood in all patients. Ventriculomegaly was seen in 5 (56%) patients; however, no patient required external ventricular drainage (hence intracranial pressure [ICP] was not measured in any of the patients). All patients underwent diagnostic four-vessel IADSA. IADSA demonstrated aneurysms in 7 patients; 4 had posterior circulation aneurysms and 3 had aneurysms of anterior circulation. IADSA did not reveal any vascular abnormality in 2 patients (that is angionegative SAH). These patients had diffuse SAH on CT (and not only in the perimesencephalic region). Patients with aneurysms underwent either microscopic clipping (in 5 patients) or endovascular coiling with or without stent assistance (in 2 patients). Three patients (out of 4 with posterior circulation aneurysms) had posterior inferior cerebellar artery (PICA) aneurysm. The fourth patient had left superior cerebellar artery aneurysm. All these patients underwent surgical clipping of aneurysm. One patient required CSF diversion in the form of ventriculoperitoneal shunt, but there was no improvement in the symptoms following shunt till the patient died of some cardiac cause (12 weeks after surgery for aneurysm). In the anterior circulation aneurysm group, two patients had aneurysm of anterior communicating artery (AComA) and the third had right superior hypophyseal artery aneurysm. While one patient with AcomA aneurysm underwent microsurgical clipping, the other two in the anterior circulation aneurysms underwent endovascular procedure. The patients with angionegative SAH did not have any additional neurological deficits other than paresis of bilateral abducens nerve. Both the patients did not require any treatment for ventriculomegaly and had uneventful course in the hospital. Two patients had vasospasm in form of demonstrable high blood velocity, as seen on Transcranial Doppler. These patients were administered Triple H therapy and intravenous nimodepine. None of the patients developed infarct. The mean duration of hospital stay was 8 days (range: 4–11 days). There was no mortality in our study group and all the patients had favorable outcome (GOS 4 or 5) at the time of discharge. Seven patients had resolution of abducens nerve palsy over a period ranging from 4 to 9 weeks following ictus, while one patient did not have any improvement even at the end of 2 years following ictus. One patient died due to some cardiac cause 12 weeks after the ictus, but there
Resolved in 9 weeks Resolved in 9 weeks
K. Garg et al.
Table I. Description of patients in our study.
772
Bilateral abducens palsy associated with SAH 773 was no improvement till that time. There was no difference among patients managed by microsurgical clipping or endovascular procedures.
Discussion Abducens nerve emerges from pontomedullary junction and enters the prepontine cistern. It then runs vertically along the dorsal surface of the clivus beside the petrous apex and then it enters the medial cavernous sinus via Dorello’s canal to leave the skull via the superior orbital fissure. It supplies the lateral rectus, the primary abductor muscle of eyeball. Along its course it is anatomically related to major vessels like anterior inferior cerebellar artery and labyrinthine artery, dorsal surface of the clivus, Dorello’s canal and cavernous sinus.4 It is susceptible to injury as a result of diverse compressive pathologies due to its long cisternal course over the clivus and sharp ridges of the petrous temporal bone.4 Abducens nerve palsy is seen as false localizing sign in patients with raised ICP of any reason. The vulnerability of the abducens nerve to raised ICP is usually attributed to its long intracranial course. This concept was challenged by Hanson et al.1 They performed a two-part anatomic study and concluded that it is not the length of the intracranial portion of the abducens that is critical to its vulnerability to increased ICP but rather its local anatomic relationships that are brought into play as the basis pontis slips caudally during transtentorial herniation. In a population-based study from United States, the age and gender adjusted annual incidence rate for abducens nerve palsy was 11.3/100000.5 In this study, five cases were related to aneurysms (pre- or post-surgery) out of the total 137 cases and none of the patients had bilateral affliction. These figures emphasize the rarity of bilateral abducens nerve palsy associated with aneurysms. Laun and Tonn2 studied 570 patients with an aneurysm and/or SAH and found that cranial nerve deficits were the first manifestations of SAH in 9% (n ⫽ 48) of patients. However, the rate of cranial nerve involvement in unruptured aneurysms was very high (about 27.8%). The third nerve was the most frequently involved nerve (involved in 38 patients), followed by abducens nerve (involved in 18 cases) but none of them was bilateral. The highest rate of cranial nerve symptoms occurred in cases of ophthalmic carotid aneurysms (83.3%). Damage to the abducens nerve had a high tendency to regress (89%) and it regressed very rapidly (within a month in 75% of patients). They speculated that indirect, temporary pressure damage to the nerve might be responsible for high recovery rates. They found no difference in clinical results of SAH patients with or without cranial nerve deficits, in contrary to what is described in the literature. There are other various isolated reports of bilateral abducens nerve palsy, some associated with aneurysms,6–10 trauma11,12 and some idiopathic.13 Various authors have studied patients of abducens nerve lesions of all etiologies combined.3,14,15 The reports of bilateral abducens nerve palsy are summarized in Table II. Rush and Younge studied 419 cases of abducens nerve palsy, out of which only 33 (7.9%) were bilateral.3 Only 3.6%
of abducens nerve palsies were related to an intracranial aneurysm in their study, as compared 13.8% of third nerve palsies.3 It was not mentioned that how many of the bilateral nerve palsies were related to aneurysms. Keane studied 125 cases of bilateral abducens nerve palsy.15 Tumors were the most common causative factor. Other implicated factors included demyelinating diseases, SAH, infection, trauma, and Guillain–Barre syndrome in that order. Subarachnoid hemorrhage was responsible for 12.8% of all cases of bilateral abducens nerve palsy as compared 7% of unilateral abducens nerve palsy cases. Durkin et al. studied 69 cases of bilateral abducens nerve palsy.14 The mean age of patients in this study was 34.9 years (range, 1–79). Children constituted 23% of the patients and 62% of the patients were male. The most common etiology was trauma affecting 42% of patients in their series, followed by vascular lesions (23.2%). The latter category included aneurysms, cerebrovascular accident, and arteriovenous malformations. In a study to determine the association of preexisting diabetes mellitus and systemic hypertension with isolated abducens nerve palsy, the authors concluded that cases of abducens nerve palsy are six times more likely to have diabetes than controls whereas there is no increased prevalence in patients with systemic hypertension alone.16 Two out of nine patients in the present series were known diabetics. All the patients in the present series had WFNS grade 2 SAH. It might be possible that the finding of bilateral abducens palsy was missed in the higher grade SAH patients. In the literature many studies have not described the location of aneurysm in relation to bilateral abducens nerve palsy and the reports that have described it, have described it in association with AComA aneurysm. However, in our study patients suffered from AcomA, PICA, and ICA superior hypophyseal artery aneurysms. Two patients also had angionegative SAH. Several mechanisms have been proposed to explain the bilateral abducens nerve involvement in SAH. These include direct compression by the aneurysm, elevated ICP, vasospasm of the pontine branches of the basilar artery affecting the abducens nuclei, and direct compression of the clot on the nerve in the prepontine cistern.6 Direct compression of the bilateral abducens nerves by the aneurysm can occur in region of cavernous sinus by cavernous ICA aneurysm but it is not always possible.7 Vasospasm of the pontine branches of the basilar artery will lead to abducens nerve palsy of the nuclear type. It will be associated with gaze paresis and/or facial paresis due to the close anatomical relationship between the abducens nuclei, the medial longitudinal fasciculus, and the facial nuclei. SAH leading to hydrocephalus can produce abducens nerve palsy due to raised ICP. Ventriculomegaly was seen in 5 patients in our series and can be the contributing factor. Nathal et al. described a case of bilateral abducens nerve palsy with AComA aneurysm.6 They proposed that the symmetrical filling of the basal cisterns with blood and/or the direct shock to the brainstem caused by aneurysmal rupture, followed by stretching of the structures lying between the brain and the skull in the subarachnoid space could be
53 yr/F
32 yr/M
Headache, nausea and loss of consciousness
51 yr/F
Goksu et al.10, 2007
Jeon et al.9, 2013
Headache, vomiting and diplopia
43 yr/M
Ziyal et al.7, 2007
Diplopia, dizziness, headache and seizure
Headache, nausea and vomiting
Headache and drowsiness
Age/Sex
56 yr/F
Author, year
Nathal et al.6, 1992
Presenting complaints
Neurological examination findings
Nuchal rigidity and bilateral VI nerve palsy
Bilateral VI nerve palsy
Bilateral VI nerve palsy
Bilateral VI nerve palsy
Bilateral VI nerve palsy
Table II. Summary of cases described in the literature.
CT findings
CT - Normal MRI - hemorrhage in the occipital horn
Fischer grade 4 SAH
Fischer grade 2 SAH
SAH in anterior supratentorial, prepontine and perimesencephalic cisterns
SAH in interhemispheric and left Sylvian fissures Moderate ventricular enlargement
Anterior communicating artery aneurysm
Anterior communicating artery aneurysm
Anterior communicating artery aneurysm
Saccular aneurysm in the anterior communicating artery
Anterior communicating artery aneurysm projecting anteroinferiorly
Angiographic findings Treatment
Coil embolization
Clipping
Clipping
Clipping
Clipping
Symmetrical filling of the basal cisterns with blood leads to stretching of the structures lying between the brain and the skull in the subarachnoid space Clot was extensively The extensive clot in removed and the the basal cisterns subarachnoid caused direct space was compression of irrigated with both abducens saline solution nerves. Liliequist’s Compression of nerve membrane and by the entrapped prepontine cistern CSF in cisterns were opened Liliequist’s Intracisternal clot membrane and formation or prepontine cistern raised intracranial were opened pressure due to frontal hematoma and SAH Lumbar drainage for Local CSF entrapment 6 days
Special measures Not described
Proposed mechanism of VI nerve palsy
9 weeks
1 month
1 month
3rd postoperative day
3 months
Time taken before resolution of VI nerve palsy
774 K. Garg et al.
Bilateral abducens palsy associated with SAH 775 responsible for bilateral abducens nerve palsy. They added that a ruptured AComA, especially an inferiorly pointing aneurysm, might lead to filling of the basal cisterns. Goksu et al. described two cases of AComA aneurysm with bilateral abducens nerve palsy.10 They proposed that Liliequist’s membrane may become thickened following SAH and create a loculation of CSF in the interpeduncular and prepontine area. This entrapped CSF in the interpeduncular cistern may compress both abducens nerves. They opened the Liliequist’s membrane during surgery in both their patients, and CSF under raised pressure was seen in one of the patients. Ziyal et al. described a 43-year-old patient with AComA aneurysm who developed bilateral abducens nerve palsy.7 They contemplated that the extensive clot in the basal cisterns caused direct compression of both abducens nerves. Further support to this hypothesis is provided by the early recovery following opening of basal cisterns with drainage of blood clots.7 They recommended the use of thrombolytic agents in addition to drainage of cerebrospinal fluid and irrigation with saline solution. Similar mechanism may be responsible for the bilateral abducens nerve palsy in our patients with angionegative SAH. Appearance of blood in basal cisterns and its thickness (Fischer’s grade) could help in predicting abducens nerve palsy. Jeon et al. reported bilateral abducens nerve palsy in a 32-year-old man with AComA aneurysm.9 The patient underwent endovascular coil embolization followed by lumbar CSF drainage for 6 days. Bilateral paresis of abducens nerve recovered completely within 9 weeks after ictus. They concluded that draining of arachnoid CSF via lumbar puncture might help in resolving the blood clot in cisterns. The recovery time period in our study varied from 4 to 9 weeks. The recovery period varied from 3 days to 3 months in the various described cases in the literature.6,7,9 The difference may be due to different pathophysiology of the nerve palsy and different treatment modalities used.
Conclusion Abducens nerve palsy is seen as false localizing sign in patients with raised ICP of any reason but isolated abducens nerve palsies associated with intracranial aneurysms have rarely been reported. We describe nine such patients. Proposed mechanisms for bilateral abducens nerve palsy
associated with subarachnoid hemorrhage include direct compression of the bilateral abducens nerves, vasospasm of the pontine branches of the basilar artery, and hydrocephalous. Most of the patients showed resolution of the symptoms over a period of 4–9 weeks. Declaration of interest: The authors report no declaration of interest. The authors alone are responsible for the content and writing of the paper.
References 1. Hanson RA , Ghosh S, Gonzalez-Gomez I, Levy ML, Gilles FH. Abducens length and vulnerability? Neurology 2004;62:33–6. 2. Laun A , Tonn JC. Cranial nerve lesions following subarachnoid hemorrhage and aneurysm of the circle of Willis. Neurosurg Rev 1988;11:137–41. 3. Rush JA , Younge BR. Paralysis of cranial nerves III, IV, and VI. Cause and prognosis in 1,000 cases. Arch Ophthalmol 1981;99:76–9. 4. Jha RM, Klein JP. Clinical anatomy and imaging of the cranial nerves and skull base. Semin Neurol 2012;32:332–46. 5. Patel SV, Mutyala S, Leske DA , Hodge DO, Holmes JM. Incidence, associations, and evaluation of sixth nerve palsy using a population-based method. Ophthalmology 2004;111:369–75. 6. Nathal E, Yasui N, Suzuki A , Hadeishi H. Ruptured anterior communicating artery aneurysm causing bilateral abducens nerve paralyses–case report. Neurol Med Chir (Tokyo) 1992;32:17–20. 7. Ziyal IM, Ozcan OE, Deniz E, Bozkurt G, Ismailoglu O. Early improvement of bilateral abducens nerve palsies following surgery of an anterior communicating artery aneurysm. Acta Neurochir 2003;145:159–61; discussion 61. 8. Da Silva IR. ‘Man-in-the-barrel’ syndrome with bilateral 6th cranial nerve palsy. Eur Neurol 2012;68:367. 9. Jeon JS, Lee SH, Son YJ, Chung YS. Slowly recovering isolated bilateral abducens nerve palsy after embolization of ruptured anterior communicating artery aneurysm. J Korean Neurosurg Soc 2013;53:112–4. 10. Goksu E, Akyuz M, Gurkanlar D, Tuncer R. Bilateral abducens nerve palsy following ruptured anterior communicating artery aneurysm: report of 2 cases. Neurocirugia (Astur) 2007; 18:420–2. 11. Salunke P, Savardekar A , Sura S. Delayed-onset bilateral abducens paresis after head trauma. Indian J Ophthalmol 2012;60:149–50. 12. Schneider RC, Johnson FD. Bilateral traumatic abducens palsy. A mechanism of injury suggested by the study of associated cervical spine fractures. J Neurosurg 1971;34:33–7. 13. Gupta PK, Bhatti MT, Rucker JC. A sweet case of bilateral sixth nerve palsies. Surv Ophthalmol 2009;54:305–10. 14. Durkin SR, Tennekoon S, Kleinschmidt A , et al. Bilateral sixth nerve palsy. Ophthalmology 2006;113:2108–9. 15. Keane JR. Bilateral sixth nerve palsy. Analysis of 125 cases. Arch Neurol 1976;33:681–3. 16. Patel SV, Holmes JM, Hodge DO, Burke JP. Diabetes and hypertension in isolated sixth nerve palsy: a population-based study. Ophthalmology 2005;112:760–3.
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ORIGINAL ARTICLE
Bilateral abducens nerve palsy associated with subarachnoid hemorrhage Kanwaljeet Garg, Pankaj Kumar Singh, Ashok Kumar Mahapatra & Bhawani Shankar Sharma Department of Neurosurgery, All India Institute of Medical Sciences, New Delhi, India
followed by abducens nerve, which accounts for about one-fifth of all cranial nerve lesions in patients with SAH. The fact that out of all abducens nerve lesions, 3.6% were due to intracranial aneurysms in a large study highlights the rarity of the situation.3 Bilateral abducens nerve involvement is even rarer and is seen in less than 10% of all patients with abducens nerve paresis.3 We describe our experience with SAH patients who developed bilateral abducens nerve palsy.
Abstract Objective. Isolated abducens nerve palsies associated with intracranial aneurysms have rarely been reported. The purpose of the study was to study the patients with bilateral abducens nerve palsy in association with subarachnoid hemorrhage (SAH). Methods. All patients admitted and managed at our center with a diagnosis of SAH and had bilateral abducens nerve palsy were included in the study. The demographic and clinical details, radiological findings, treatment data, and outcome of these patients were retrieved from the computerized database of our hospital. Results. Nine patients, with a mean age of 49.4 years, met the inclusion criteria. Male to female ratio of 1.25:1). Average duration of symptoms before presentation was 2.6 days (ranging from 1 to 4 days). Third nerve palsy in addition to bilateral abducens nerve palsy was present in 4 patients (44%). DSA demonstrated aneurysms in 7 patients; 4 had posterior circulation aneurysms and 3 had aneurysms of anterior circulation. Two patients had angionegative SAH. The abnormality resolved in all but one patient over a time period of 4–9 weeks, and one patient died due to unrelated cause. Conclusions. Bilateral abducens nerve palsy in association with SAH is rarely described. Proposed mechanisms include direct compression of the bilateral abducens nerves, vasospasm of the pontine branches of the basilar artery and hydrocephalous. Most of the patients in our series showed resolution of the symptoms over a period of 4–9 weeks.
Methods At our centre, 2433 patients with intracranial aneurysms were treated from January 2001 through March 2013. Patients who had bilateral abducens nerve palsy at the time of presentation were included in the study group. The data of these patients were retrospectively reviewed from the computerized database of our center. Demographic and clinical details, radiological findings, treatment data, and outcome were analyzed retrospectively. WFNS grade was used to grade the SAH. Computed tomogram followed by intra-arterial digital subtraction angiogram (IADSA) was done in all patients. Findings of IADSA were discussed among the neurosurgeons and neuroradiologists, and the treatment plan according to the aneurysm morphology and location was decided. In case both endovascular coiling and microsurgical clipping were feasible, patient’s attendants were given the option of both and depending on their decision, which is very much influenced by the financial constraints in India, further treatment was done. Once the aneurysm was secured by either means, the management of SAH was consistent with the standard guidelines. Patients were followed up in outpatient department at monthly intervals after intervention till 3 months, and 6 monthly thereafter. Glasgow outcome score (GOS) was used to assess the postoperative and follow-up outcome. A GOS of 4 and 5 was considered to be favorable outcome, whereas a GOS 1–3 was considered to be poor outcome.
Keywords: abducens nerve; aneurysms; bilateral; occulomotor, resolution; subarachnoid hemorrhage
Introduction Abducens nerve palsy is a common cause of diplopia in neurology clinics. It is involved in a number of disorders, may be due to its extremely long intracranial course1 and is the most frequently involved cranial nerve. Common presenting feature of subarachnoid hemorrhage (SAH) includes sudden onset severe headache, ictal loss of consciousness, seizures, and motor deficits. Cranial nerve involvement, especially those supplying extraocular muscles, is reported to occur in about 9% of patients with SAH.2 Third nerve is the most common nerve involved
Results Out of the 2433 patients treated for SAH at our center during the study period, 9 met the inclusion criteria of the study
Correspondence: Dr Pankaj Kumar Singh, Room No 720, Department of Neurosurgery, Cardio-Neuro Centre, All India Institute of Medical Sciences, New Delhi, India. Tel: ⫹ 919968398570. Fax: ⫹ 91-11-26589650. E-mail: [email protected] Received for publication 20 December 2013; accepted 6 April 2014
771
Good (5) Good (5) Good (4) Clipping Coiling Coiling Yes No No B/L VI nerve palsy B/L VI nerve palsy B/L VI nerve palsy 1 3 4 48/F 45/M 55/F 7 8 9
Right PICA AComA aneurysm Right superior hypophyseal
Good (4) Clipping Yes B/L VI nerve palsy 3 45/M 6
Right PICA
4 2 2 45/M 58/F 59/M 3 4 5
VI nerve palsy at final follow up
Resolved in 8 weeks Resolved in 7 weeks Died 12 weeks after surgery due to cardiac illness No improvement at 24 months follow up Resolved in 6 weeks Resolved in 6 weeks Resolved in 4 weeks Good (5) Good (5) Good (4) Conservative Conservative Clipping and V-P shunt Yes Yes No
Good (5) Good (5) Clipping Clipping No Yes
B/L VI nerve palsy Right III nerve palsy B/L VI nerve palsy B/L VI nerve palsy B/L VI nerve palsy B/L VI nerve palsy 1 3
AComA aneurysm Left superior cerebellar aneurysm Angionegative SAH Angionegative SAH Right PICA 57/F 33/M 1 2
Outcome (GOS at discharge) Treatment Duration of symptoms before the Neurological deficits at diagnosis was made (in days) the time of presentation Ventriculomegaly Diagnosis S No Age/Sex
(Table I). The mean age of patients of our study group was 49.4 years (ranging from 43 to 61 years). There were five males and four females in our study group (male to female ratio of 1.25:1). All patients presented with sudden onset severe headache, classical presentation of SAH. Average duration of symptoms before presentation was 2.6 days (ranging from 1 to 4 days). Three patients in our study group were known hypertensive, while 2 (22%) were known diabetic. Examination revealed bilateral abducens nerve palsy in all the 9 patients at the time of presentation to our hospital. Third nerve palsy in addition to bilateral abducens nerve palsy was present in 4 patients (44%). Out of these 4 patients, 3 had unilateral third nerve involvement and one had bilateral involvement of third nerve. All the patients had good grade SAH (WFNS grade II). Computed tomography (CT) revealed subarachnoid blood in all patients. Ventriculomegaly was seen in 5 (56%) patients; however, no patient required external ventricular drainage (hence intracranial pressure [ICP] was not measured in any of the patients). All patients underwent diagnostic four-vessel IADSA. IADSA demonstrated aneurysms in 7 patients; 4 had posterior circulation aneurysms and 3 had aneurysms of anterior circulation. IADSA did not reveal any vascular abnormality in 2 patients (that is angionegative SAH). These patients had diffuse SAH on CT (and not only in the perimesencephalic region). Patients with aneurysms underwent either microscopic clipping (in 5 patients) or endovascular coiling with or without stent assistance (in 2 patients). Three patients (out of 4 with posterior circulation aneurysms) had posterior inferior cerebellar artery (PICA) aneurysm. The fourth patient had left superior cerebellar artery aneurysm. All these patients underwent surgical clipping of aneurysm. One patient required CSF diversion in the form of ventriculoperitoneal shunt, but there was no improvement in the symptoms following shunt till the patient died of some cardiac cause (12 weeks after surgery for aneurysm). In the anterior circulation aneurysm group, two patients had aneurysm of anterior communicating artery (AComA) and the third had right superior hypophyseal artery aneurysm. While one patient with AcomA aneurysm underwent microsurgical clipping, the other two in the anterior circulation aneurysms underwent endovascular procedure. The patients with angionegative SAH did not have any additional neurological deficits other than paresis of bilateral abducens nerve. Both the patients did not require any treatment for ventriculomegaly and had uneventful course in the hospital. Two patients had vasospasm in form of demonstrable high blood velocity, as seen on Transcranial Doppler. These patients were administered Triple H therapy and intravenous nimodepine. None of the patients developed infarct. The mean duration of hospital stay was 8 days (range: 4–11 days). There was no mortality in our study group and all the patients had favorable outcome (GOS 4 or 5) at the time of discharge. Seven patients had resolution of abducens nerve palsy over a period ranging from 4 to 9 weeks following ictus, while one patient did not have any improvement even at the end of 2 years following ictus. One patient died due to some cardiac cause 12 weeks after the ictus, but there
Resolved in 9 weeks Resolved in 9 weeks
K. Garg et al.
Table I. Description of patients in our study.
772
Bilateral abducens palsy associated with SAH 773 was no improvement till that time. There was no difference among patients managed by microsurgical clipping or endovascular procedures.
Discussion Abducens nerve emerges from pontomedullary junction and enters the prepontine cistern. It then runs vertically along the dorsal surface of the clivus beside the petrous apex and then it enters the medial cavernous sinus via Dorello’s canal to leave the skull via the superior orbital fissure. It supplies the lateral rectus, the primary abductor muscle of eyeball. Along its course it is anatomically related to major vessels like anterior inferior cerebellar artery and labyrinthine artery, dorsal surface of the clivus, Dorello’s canal and cavernous sinus.4 It is susceptible to injury as a result of diverse compressive pathologies due to its long cisternal course over the clivus and sharp ridges of the petrous temporal bone.4 Abducens nerve palsy is seen as false localizing sign in patients with raised ICP of any reason. The vulnerability of the abducens nerve to raised ICP is usually attributed to its long intracranial course. This concept was challenged by Hanson et al.1 They performed a two-part anatomic study and concluded that it is not the length of the intracranial portion of the abducens that is critical to its vulnerability to increased ICP but rather its local anatomic relationships that are brought into play as the basis pontis slips caudally during transtentorial herniation. In a population-based study from United States, the age and gender adjusted annual incidence rate for abducens nerve palsy was 11.3/100000.5 In this study, five cases were related to aneurysms (pre- or post-surgery) out of the total 137 cases and none of the patients had bilateral affliction. These figures emphasize the rarity of bilateral abducens nerve palsy associated with aneurysms. Laun and Tonn2 studied 570 patients with an aneurysm and/or SAH and found that cranial nerve deficits were the first manifestations of SAH in 9% (n ⫽ 48) of patients. However, the rate of cranial nerve involvement in unruptured aneurysms was very high (about 27.8%). The third nerve was the most frequently involved nerve (involved in 38 patients), followed by abducens nerve (involved in 18 cases) but none of them was bilateral. The highest rate of cranial nerve symptoms occurred in cases of ophthalmic carotid aneurysms (83.3%). Damage to the abducens nerve had a high tendency to regress (89%) and it regressed very rapidly (within a month in 75% of patients). They speculated that indirect, temporary pressure damage to the nerve might be responsible for high recovery rates. They found no difference in clinical results of SAH patients with or without cranial nerve deficits, in contrary to what is described in the literature. There are other various isolated reports of bilateral abducens nerve palsy, some associated with aneurysms,6–10 trauma11,12 and some idiopathic.13 Various authors have studied patients of abducens nerve lesions of all etiologies combined.3,14,15 The reports of bilateral abducens nerve palsy are summarized in Table II. Rush and Younge studied 419 cases of abducens nerve palsy, out of which only 33 (7.9%) were bilateral.3 Only 3.6%
of abducens nerve palsies were related to an intracranial aneurysm in their study, as compared 13.8% of third nerve palsies.3 It was not mentioned that how many of the bilateral nerve palsies were related to aneurysms. Keane studied 125 cases of bilateral abducens nerve palsy.15 Tumors were the most common causative factor. Other implicated factors included demyelinating diseases, SAH, infection, trauma, and Guillain–Barre syndrome in that order. Subarachnoid hemorrhage was responsible for 12.8% of all cases of bilateral abducens nerve palsy as compared 7% of unilateral abducens nerve palsy cases. Durkin et al. studied 69 cases of bilateral abducens nerve palsy.14 The mean age of patients in this study was 34.9 years (range, 1–79). Children constituted 23% of the patients and 62% of the patients were male. The most common etiology was trauma affecting 42% of patients in their series, followed by vascular lesions (23.2%). The latter category included aneurysms, cerebrovascular accident, and arteriovenous malformations. In a study to determine the association of preexisting diabetes mellitus and systemic hypertension with isolated abducens nerve palsy, the authors concluded that cases of abducens nerve palsy are six times more likely to have diabetes than controls whereas there is no increased prevalence in patients with systemic hypertension alone.16 Two out of nine patients in the present series were known diabetics. All the patients in the present series had WFNS grade 2 SAH. It might be possible that the finding of bilateral abducens palsy was missed in the higher grade SAH patients. In the literature many studies have not described the location of aneurysm in relation to bilateral abducens nerve palsy and the reports that have described it, have described it in association with AComA aneurysm. However, in our study patients suffered from AcomA, PICA, and ICA superior hypophyseal artery aneurysms. Two patients also had angionegative SAH. Several mechanisms have been proposed to explain the bilateral abducens nerve involvement in SAH. These include direct compression by the aneurysm, elevated ICP, vasospasm of the pontine branches of the basilar artery affecting the abducens nuclei, and direct compression of the clot on the nerve in the prepontine cistern.6 Direct compression of the bilateral abducens nerves by the aneurysm can occur in region of cavernous sinus by cavernous ICA aneurysm but it is not always possible.7 Vasospasm of the pontine branches of the basilar artery will lead to abducens nerve palsy of the nuclear type. It will be associated with gaze paresis and/or facial paresis due to the close anatomical relationship between the abducens nuclei, the medial longitudinal fasciculus, and the facial nuclei. SAH leading to hydrocephalus can produce abducens nerve palsy due to raised ICP. Ventriculomegaly was seen in 5 patients in our series and can be the contributing factor. Nathal et al. described a case of bilateral abducens nerve palsy with AComA aneurysm.6 They proposed that the symmetrical filling of the basal cisterns with blood and/or the direct shock to the brainstem caused by aneurysmal rupture, followed by stretching of the structures lying between the brain and the skull in the subarachnoid space could be
53 yr/F
32 yr/M
Headache, nausea and loss of consciousness
51 yr/F
Goksu et al.10, 2007
Jeon et al.9, 2013
Headache, vomiting and diplopia
43 yr/M
Ziyal et al.7, 2007
Diplopia, dizziness, headache and seizure
Headache, nausea and vomiting
Headache and drowsiness
Age/Sex
56 yr/F
Author, year
Nathal et al.6, 1992
Presenting complaints
Neurological examination findings
Nuchal rigidity and bilateral VI nerve palsy
Bilateral VI nerve palsy
Bilateral VI nerve palsy
Bilateral VI nerve palsy
Bilateral VI nerve palsy
Table II. Summary of cases described in the literature.
CT findings
CT - Normal MRI - hemorrhage in the occipital horn
Fischer grade 4 SAH
Fischer grade 2 SAH
SAH in anterior supratentorial, prepontine and perimesencephalic cisterns
SAH in interhemispheric and left Sylvian fissures Moderate ventricular enlargement
Anterior communicating artery aneurysm
Anterior communicating artery aneurysm
Anterior communicating artery aneurysm
Saccular aneurysm in the anterior communicating artery
Anterior communicating artery aneurysm projecting anteroinferiorly
Angiographic findings Treatment
Coil embolization
Clipping
Clipping
Clipping
Clipping
Symmetrical filling of the basal cisterns with blood leads to stretching of the structures lying between the brain and the skull in the subarachnoid space Clot was extensively The extensive clot in removed and the the basal cisterns subarachnoid caused direct space was compression of irrigated with both abducens saline solution nerves. Liliequist’s Compression of nerve membrane and by the entrapped prepontine cistern CSF in cisterns were opened Liliequist’s Intracisternal clot membrane and formation or prepontine cistern raised intracranial were opened pressure due to frontal hematoma and SAH Lumbar drainage for Local CSF entrapment 6 days
Special measures Not described
Proposed mechanism of VI nerve palsy
9 weeks
1 month
1 month
3rd postoperative day
3 months
Time taken before resolution of VI nerve palsy
774 K. Garg et al.
Bilateral abducens palsy associated with SAH 775 responsible for bilateral abducens nerve palsy. They added that a ruptured AComA, especially an inferiorly pointing aneurysm, might lead to filling of the basal cisterns. Goksu et al. described two cases of AComA aneurysm with bilateral abducens nerve palsy.10 They proposed that Liliequist’s membrane may become thickened following SAH and create a loculation of CSF in the interpeduncular and prepontine area. This entrapped CSF in the interpeduncular cistern may compress both abducens nerves. They opened the Liliequist’s membrane during surgery in both their patients, and CSF under raised pressure was seen in one of the patients. Ziyal et al. described a 43-year-old patient with AComA aneurysm who developed bilateral abducens nerve palsy.7 They contemplated that the extensive clot in the basal cisterns caused direct compression of both abducens nerves. Further support to this hypothesis is provided by the early recovery following opening of basal cisterns with drainage of blood clots.7 They recommended the use of thrombolytic agents in addition to drainage of cerebrospinal fluid and irrigation with saline solution. Similar mechanism may be responsible for the bilateral abducens nerve palsy in our patients with angionegative SAH. Appearance of blood in basal cisterns and its thickness (Fischer’s grade) could help in predicting abducens nerve palsy. Jeon et al. reported bilateral abducens nerve palsy in a 32-year-old man with AComA aneurysm.9 The patient underwent endovascular coil embolization followed by lumbar CSF drainage for 6 days. Bilateral paresis of abducens nerve recovered completely within 9 weeks after ictus. They concluded that draining of arachnoid CSF via lumbar puncture might help in resolving the blood clot in cisterns. The recovery time period in our study varied from 4 to 9 weeks. The recovery period varied from 3 days to 3 months in the various described cases in the literature.6,7,9 The difference may be due to different pathophysiology of the nerve palsy and different treatment modalities used.
Conclusion Abducens nerve palsy is seen as false localizing sign in patients with raised ICP of any reason but isolated abducens nerve palsies associated with intracranial aneurysms have rarely been reported. We describe nine such patients. Proposed mechanisms for bilateral abducens nerve palsy
associated with subarachnoid hemorrhage include direct compression of the bilateral abducens nerves, vasospasm of the pontine branches of the basilar artery, and hydrocephalous. Most of the patients showed resolution of the symptoms over a period of 4–9 weeks. Declaration of interest: The authors report no declaration of interest. The authors alone are responsible for the content and writing of the paper.
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