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Show Journal of Cli" ical Neuro- ophthalmology 12( 1), 21- 25, 1992, Evolution of Oculomotor Nerve Palsies Hilda Capo, M. D., Floyd Warren, M. D., and Mark J. Kupersmith, M. D. I[) 1992 Raven Press, Ltd" New York The management of patients with isolated oculomotor nerve palsies ( OMPs) who have normal pupils and no other signs of neurological disease is a controversial issue. A more precise delineation of the clinical course of isolated OMPs may help to determine whether neuroradiologic evaluation is indicated in these cases, We studied 41 patients with isolated third cranial nerve palsies, emphasizing the times of progression and resolution of the oculomotor nerve dysfunction. The average interval from onset to development of maximal ophthalmoplegia failed to differentiate between a microvascular etiology ( 3.3 days) or posterior communicating artery aneurysm ( 3 days). Of the 28 patients with diabetic or idiopathic palsies, regardless of pupillary involvement, 68% had improvement of the oculomotor paresis within 4 weeks, 96% within 8 weeks, and 100% within 12 weeks of the onset of symptoms, Our study suggests that patients with pupil- sparing OMPs should be considered for extensive neuroradiologic evaluation only if there is deterioration or failure to improve within 4 to 8 weeks. Key Words: Intracranial aneurysm- Oculomotor palsy- Third cranial nerve, From the Bascom Palmer Eye Institute ( H, C) University of Miami, Miami Florida, and the Departments of Ophthalmology ( F. W" M.], K.) and Neurology ( M,]. K.) New York University Medical Center, New York, New York, U, S, A, This work was supported in part by an unrestricted grant from Research to Prevent Blindness to the Department of Oph-thalmology, New York University. . This paper was presented at the 42nd Annual Meehn, g of the American Academy of Neurology, May 3, 1990, Miami Beach, Florida. Address correspondence and reprint requests to Dr. Hilda Capo, 900 N. W. 17th Street, Miami, FL 33136, U. S. A, 21 The management of patients with isolated third cranial nerve palsies is a controversial issue. It is generally accepted that computed tomography ( CT) or magnetic resonance imaging ( MRI), followed by cerebral angiography, should be performed to rule out the presence of an aneurysm in patients with oculomotor nerve palsy ( OMP) and pupillary paresis, but the proper approach in cases with pupillary sparing is unclear. An isolated, pupil- sparing OMP usually occurs with microvascular infarction of the nerve ( 1,2); there is general agreement that a normal pupil practically excludes an aneurysm as the cause of the OMP ( 2,3). Kissel ( 4), however, reported four patients with a posterior communicating artery ( PCoA) aneurysm who presented with pupil- sparing OMP and no signs of subarachnoid hemorrhage ( SAH). Progression to pupillary involvement occurred in three of the patients ( 4). Recently, complete external ophthalmoplegia with pupillary sparing was reported in a patient with a basilar artery aneurysm ( 5). The occurrence of pupil- sparing OMPs with intracranial aneurysms has led some authors to recommend neuroimaging studies ( 5) and many neurosurgeons to perform cerebral angiography ( 6) in all patients with OMP regardless of the state of the pupil. A more precise definition of the time course of evolution of acute, isolated OMPs may be useful in determining the need for neuroradiographic studies in these cases. We studied 41 cases of isolated third cranial nerve palsy, with special attention to the course of progression and resolution of the oculomotor nerve dysfunction. SUBJECTS AND METHODS We reviewed the medical records of patients evaluated between 1982 and 1989 by the New York University Medical Center Neuro- Ophthalmology Service for acute isolated third nerve palsies. Only 22 H. CAP6 ET AL. patients with adequate history and follow- up were included. In order to assess only patients wtth an isolated OMP, patients with additional cranial neuropathies or systemic or neurologic symptoms at presentation were not included. Traumatic cases and those with evidence of SAH were also excluded. Particular attention was given to the pupillary status, presence of pain, the degree of involvement of the extraocular muscles ( EOM), and the time course of evolution of the OMP. Patients were grouped according to the degree of pupillary and EOM involvement ( Table 1). Partial pupillary dysfunction was defined as ipsilateral pupil dilation of more than 1 mm or decreased reactivity in cases of equal pupillary size. External ophthalmoplegia was considered partial when the appropriate muscles were underacting but not fully paralyzed, or when some of the appropriate muscles were spared. Cases were classified according to the etiology of the third nerve palsy. Idiopathic and diabetic palsies were grouped together on the presumption that both share an ischemic microvascular etiology and a benign course. Cases of intracavernous internal carotid artery ( lCA) aneurysms and meningiomas of the cavernous sinus region were combined as compressive lesions of the cranial nerves in the cavernous sinus. All patients with pupillary involvement, except one, underwent CT or MRI and cerebral angiography to confirm that there was no intracranial aneurysm. RESULTS Forty- one patients met our criteria for inclusion. Twenty- eight of them ( 6690) had an idiopathic or diabetic ( presumed microvascular) etiology, and 10 patients ( 26%) had angiogram- proven aneurysms ( 7 PCoA, 3 cavernous ICA). Two patients ( 5S7c) had a meningioma in the cavernous sinus area, and one ( 3%) had CNS lymphoma. TABLE 1. Degree of oculomotor nerve inVOlvement Idiopathic or Diabetic Etiology The group with idiopathic or diabetic etiologies included 12 women ( 43%) and 16 men ( 57%), with an average age of 67 years ( range 2~ 89 years). Five patients had diabetes mellitus, 7 had high blood pressure, and 2 had both diseases ( T~ ble. 2). The 14 patients without any known systemIC dIsease had a negative 4- or 5- hour glucose tolerance test. The pupil was spared in 21 patients ( 75%). and involved in 7 ( 2590). Two of the seven patIents with pupillary involvement initially presented with pupillary sparing, but developed pupil paresis at days 11 and 14. Of those with pupillary involvement, three had complete iridoplegia and four had partial pupillary dysfunction; EOM dysfunction was complete in four patients and partial in three ( Table 1). Six of the patients with pupillary involvement had a normal head CT or MRI and a normal cerebral angiogram of the ipsilateral ICA and vertebrobasilar artery, which confirmed the absence of an aneurysm, The only patient who refused cerebral angiography had a normal MRI and spontaneous improvement of the paresis. Of the 21 patients with pupillary sparing, 17 had partial and 4 had complete external ophthalmoplegia ( Table 1), In two of these patients, only the superior division was involved. Because third nerve ischemia rarely spares the inferior division, these patients had a head and orbit CT or MRI, the results of which were normal. Ipsilateral periorbital or retroorbital pain was present in 16 patients ( 610/ c) with a microvascular etiology, The pain preceded the onset of ophthalmoplegia in seven patients, was concurrent in eight, and appeared afterwards in two. The time from the first symptoms to the development of maximal internal and external ophthalmoplegia is shown in Fig. 1. The mean time of progression was 3.3 days ( SO ± 3.2). The improvement rate is shown in Fig. 2. Sixty- eight percent of the patients had improvement of the OMP within 4 weeks; 96S7c, within 8 weeks; and 100%, within 12 weeks of the onset of symptoms. CNS. central nervous system: NP. normal pupil; PP. partial pupil dysfunction: CP, complete pupil dysfunction: PO, partial external ophthalmoplegia: CO complete external ophthalmoplegia NP. PO NP. CO PP. PO PP. co CPo PO CP, CO Total Diabetic or idiopathic 17( 61%) 4 ( 14%) 2 ( 7%) 2 ( 7%) 2 ( 7%) 1 ( 4%) 28 ( 100%) Posterior communicating aneurysm oo2 ( 29%) , ( 14%) 1 ( 14%) 3 ( 43%) 7 ( 100%) Cavernous sinus lesion 2( 40%) o2 ( 40%) o o1 ( 20%) 5( 100%) eNS lymphoma o o1o o o TABLE 2. Distribution by etiology Diabetic Posterior Cavernous or communicating sinus CNS idiopathic aneurysm lesion lymphoma Total cases 28 7 5 1 Average age 67 years 57 years 58 years 56 years Women 12 ( 43%) 5 ( 71%) 3( 60%) 0 Men 16 ( 57%) 2 ( 29%) 2 ( 40%) 1 Pain 17 ( 61%) 5 ( 71%) 3 ( 60%) 0 OM 5( 18%) 0 0 1 HBP 7 ( 25%) 2 0 0 OM and HBP 2( 7%) 0 0 0 OM, diabetes mellitus; HBP. high blood pressure. OCULOMOTOR PALSIES 23 FIG. 1. Interval from first symptoms of oculomotor nerve palsy to maximal ophthalmoplegia. Posterior Communicating Artery Aneurysms Seven patients ( 18%), all with pupillary dysfunction at presentation, had angiogram- proven PCoA aneurysms ipsilateral to the OMP. There were five women and two men, with a mean age of 57 years ( range 37- 68 years). Two of the patients had high blood pressure, and none had diabetes mellitus ( Table 2). Pain was present in five patients ( 71 %) and preceded the onset of ophthalmoplegia in four. Pupil dysfunction was complete in four patients and partial in three. The external ophthalmoplegia was complete in four patients and partial in three ( Table 1). The course of progression is shown in Fig. 1. The difference in the mean time of progression between the microvascular ( 3.3 days) and the PCoA ( 3 days, SO ::!:: 2.7) OMPs was not statistically significant by the Mann- Whitney test. NUMBER OF CASES 25 1 21 20 j 15 ~ Lymphoma One patient who initially presented with a partial internal and external OMP worsened over 1 month and developed paresis of the ipsilateral fourth and sixth cranial nerves. Magnetic resonance imaging and cerebral angiography performed at the time of presentation were normal, but the glucose tolerance test demonstrated a diabetic curve. A lumbar puncture, performed at 1 month, revealed lymphoma cells in the spinal fluid. A systemic evaluation did not show lymphoma outside of the central nervous system. DISCUSSION men ( 55 and 70 years old). Three patients had periorbital pain ipsilateral to the lesion ( two ICA aneurysms, one meningioma). The external ophthalmoplegia was partial in four and complete in one patient; three patients had internal ophthalmoplegia ( Table 1). The two patients with pupillary sparing ( one meningioma, one ICA aneurysm) had no improvement of the OMP by eight and nine weeks, when neuroradiologic studies were performed. The time course of progression was variable, ranging from 1 day to 3 years. One patient with a cavernous ICA aneurysm had spontaneous thrombosis of the aneurysm, with improvement of the pupil- involving OMP within 1 month and complete resolution within 4 months. o 13- 15 ro •• o 10- 12 4 [- I . 0 c ---' 4- 6 2 .,,:=::~ [. 7- 9 TIME (~ YS) o mlcronIScular _ post comm lUIelllY5m 5 1- 3 o 10 j 5~ Cavernous Sinus Lesions Three patients ( 8%) had angiogram- proven aneurysms of the intracavernous portion of the ICA, and two ( 7%) had a meningioma in the cavernous sinus area. Both conditions were grouped together as compressive lesions of the cranial nerves in the cavernous sinus. The three patients with intracavernous ICA aneurysms were women ( 25, 67, and 74 years old), and the two with meningiomas were The recommendations for the evaluation of patients with a nontraumatic, isolated third cranial nerve palsy usually vary according to the degree of pupillary and EOM involvement. The question is: To what extent is a third nerve paresis a harbinger of a life- threatening condition, such as an intracranial aneurysm? lntracavernous ICA aneurysms can occasionally cause an isolated OMP, but these differ from the PCoA and basilar artery aneurysms in that they carry only a minimal risk of producing a significant neurological deficit or death. Rupture of intracavernous ICA aneurysms usually results in a carotidcavernous fistula without causing SAH. Only two cases of SAH caused by a ruptured intracavernous aneurysm have been reported ( 7,8). Consequently, emergency treatment in most cavernous carotid aneurysms is not recommended. Approximately 86- 100% of patients with OMPs caused by intradural aneurysms will have some degree of pupillary dysfunction at presentation ( 2,4,9- 11) making it necessary to exclude an aneurysm in cases where the pupil is involved. It is week 2 week 12 '! II OF CASF. S IMPROVED 96 1:: 68 r-'--~ ~+--",,"",_ 2~ 5~. L---. r r- t--,---~ week 4 week 8 TIME INTERVAL ( WEEKS) FIG. 2. Improvement rate of microvascular oculomotor nerve palsy. , CLi" Neuro- ophthalmol. Vol. 12, No. 1, 1992 24 H. CAPO ET AL. generally agreed that, because of the risk of a SAH from rupture of PCoA or basilar artery aneurysms, patients with partial or complete iridoplegia, irrespective of the degree of external ophthalmoplegia, should have neuroimaging studies including cerebral angiography for patients older than 20 years of age. If the results of these studies are normal, a lumbar puncture should be performed to rule out a low- grade meningitis or lymphoma. Patients with complete external ophthalmoplegia and sparing of the pupil are most likely to have suffered an ischemic event ( 3). A microvascular infarct of the extra- axial portion of the nerve with sparing of the peripheral pupilloconstrictor fibers has been identified in pathology specimens from diabetic OMPs, which explains the preservation of the pupillary function ( 12- 14). Therefore, cerebral angiography is usually not initially recommended when the pupil is spared and the patient is 50 years of age or older and without SAH ( 3). Recently, Lustbader and Miller ( 5) reported a complete external oph thalmoplegia with pupillary sparing in a patient with a basilar artery aneurysm. This is the only case in the literature of an intracranial aneurysm with this presentation. The clinical course of this patient differed from that of our patients with microvascular disease in that there was no improvement 8 weeks after the onset of symptoms, while 969< of our patients had already improved by this time. We agree with previous recommendations ( 15) that patients with complete external third nerve palsies and sparing of the pupil do not require neuroradiologic studies except when the patient either deviates from the usual clinical course of an ischemic OMP or in younger patients in whom an ischemic process is therefore unlikely. Trobe ( 3) recommends cerebral angiography for adults with an incomplete OMP and a normal pupil, particularly if the inferior division is spared. Although diabetic isolated palsies of the superior division of the third cranial nerve have been reported ( 16), these palsies are most commonly caused by compressive lesions, such as neoplasms and aneurysms of the ICA in the anterior cavernous sinus, where the nerve bifurcates ( 17) or less frequently, by basilar artery aneurysms ( 17,18). In patients with a superior division paresis of the oculomotor nerve, a high- resolution contrast CT scan or MRI is usually adequate to visualize the cavernous sinus and basilar artery areas and should be initially obtained in these patients ( 17). There are very few cases in the literature of PCoA aneurysms causing incomplete OMPs with a normal pupil. Kassof et ,11 ( 19) and Oono et al. ( 20) have each reported one case of a PCoA aneurysm with a pupil- sparing partial third nerve palsy. Bartleson et al. ( 21) reported three patients who presented with an incomplete pupil- sparing OMP caused by unruptured intracranial aneurysms, one in the basilar artery and two in the ICA ( presumably PCoA junction). None of these patients had improved 6 weeks after the onset of symptoms. Kissel et al. ( 4) reported four patients with PCoA aneurysms without SAH, who presented initially with pupil- sparing partial OMPs. However, one had an ipsilateral abducens palsy; two developed a complete iridoplegia within 5 days; and one, by 4 months. Pupil- sparing, partial OMP appears to be a rare presentation of intracranial aneurysms, but is common in idiopathic or diabetic OMP as observed in 61 ( 7c of our patients with microvascular etiology ( Table 1). Since most of the patients with intracranial aneurysms initially have an abnormal pupiL or will develop pupillary involvement within several days of the ophthalmoparesis ( 4,6), and 68% of the patients with idiopathic or diabetic OMPs will improve by 1 month and 969< by 2 months, it seems prudent to closely observe the patient with a pupillary- sparing third nerve paresis for 4 to 8 weeks before performing neuroradiographic studies, particularly cerebral angiography. Previous reports suggest that a CT scan MRI scan should be performed earlier in adults younger than 50 years of age and in those with an isolated superior branch paresis. It may be argued that 4 weeks is a long period of time, since Okawara ( 22) found that in cases of PCoA aneurysms the EOM involvement preceded the rupture of the aneurysm by an average of 29.6 days. It should be noted, however, that this average was based on onlv 6 cases, and no information was provided on the ' pupillary status, so this information may not apply to cases of pupil- sparing OMP. It is unfortunate that the time of progression of the third nerve paresis is not helpful in distinguishing patients with an ischemic etiology from those with an aneurysm. We found that both groups worsened over an average of approximately 3 days. In conclusion, patients with OMPs that involve the pupil ( either initially or later) should have expedited noninvasive neuroimaging studies and cerebral angiography at the time of presentation. In patients with isolated complete or partial external ophthalmoplegia and normal pupils, the clinical course remains helpful in determining the extent of the neuroradiologic evaluation. Though one could argue that the miniscule risk of MR or CT OCULOMOTOR PALSIES 25 warrants that all patients be studied, our data suggests that only patients who fail to improve within 4 to 8 weeks must be scanned. According to previous reports, exceptions include patients with a superior division paresis in whom compressive lesions are common, and younger patients in whom an ischemic process is unlikely. REFERENCES 1 Nadeau SE. Trobe JD Pupil sparing in lKulomotor palsv: a brid re\' lew. AI111 Nellr,) 1 19i13; 13: I- IJ-- ll. ~ RULker CW The causes llf p, uail'si,; l'f the third. fourth and shth Lranial ner\' es. Alii Ill/' ilt/ IIl! IIII)! I% b; bl : 12Y3- il. 3. Trl) be JD. Isolated pupil- sparin~ third nerve palsv Uphtha! IIWlt',\ I/ 1985; 9258-- b1 - I. K. iss~ i. fT, Burde RM. Klin~ ele TG. Zei~ er NE. Pupil- sparin~ oLulomotor paresis with internal Larotid- posterior Lommunicating artery aneurysms. AIII1 NellroI1983; 13: 149- 54. ~. Lustbader JI\ I, Miller NR. 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