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Show Jounud of Cliniad Neuro-ophtluzlmology 7(2): 69-73, 1987. Bilateral Internuclear Ophthalmoplegia in Systemic Lupus Erythematosus Martin S. Cogen, M.D., Lanning B. Kline, M.D., and Ernest R. Duvall, M.D. © 1987 Raven Press, New York Internuclear ophthalmoplegia has been infrequently described in patients with systemic lupus erythematosus. We report a 23-year-old woman with lupus who presented with bilateral internuclear ophthalmoplegia and skew deviation. Additional neurologic findings included dysarthria, hemifacial weakness, hemiparesis, and dysmetria. Computed tomography of the patient's brainstem was unremarkable while magnetic resonance scanning demonstrated two areas of infarction. Magnetic resonance imaging is superior to computed tomography in both neuroradiographic study of the brainstem as well as evaluation of patients with neurologic complications of lupus. Key Words: Internuclear ophthalmoplegia-Magnetic resonance imaging-Medial longitudinal fasciculusSystemic lUpus erythematosus. From the Departments of Ophthalmology (M.S.C., L.B.K.) and Radiology (E.R.D.), University of Alabama School of Medicine, Birmingham, Alabama. Address correspondence and reprint requests to L. B. Kline, M.D., Suite 555, 1600 7th Avenue South, Birmingham, AL 35233, U.S.A. 69 Internuclear ophthalmoplegia is characterized by isolated paresis of the medial rectus muscle on conjugate lateral gaze due to a lesion of the ipsilateral medial longitudinal fasciculus in the brainstem (1-3). Frequently, there is disassociated horizontal jerk nystagmus in the abducting eye. Cogan (4) has divided internuclear ophthalmoplegia into a posterior type, in which medial rectus function during convergence is spared, and an anterior type, in which convergence is abolished. Unilateral internuclear ophthalmoplegia is caused primarily by vascular lesions of the medial longitudinal fasiculus (1,3,5). The bilateral form is usually due to multiple sclerosis (1,3,5-7), although other causes include ischemia from basilar artery disease (3,6-10), syphilis (6,11,12), tuberculous granuloma (13), brainstem and fourth ventricular brain tumors (11,12), Chiari malformation (14), cryptococcal meningitis (15), meningeal carcinomatosis (16), drugs (17,18), and trauma (19-21). We describe a patient with systemic lupus erythematosus who developed wall-eyed bilateral internuclear ophthalmoplegia (22,23) and skew deviation, and emphasize the value of magnetic resonance imaging in evaluating patients with brainstem dysfunction. CASE REPORT A 23-year-old woman with a 7-year history of systemic lupus erythematosus was admitted to the University of Alabama Hospital with an exacerbation of her disease. Systemic involvement had previously been limited to an erythematous rash of the face and trunk and arthralgias of varying severity. At the time of admission, the patient was taking 20 mg of prednisone daily and related a 2week history of increased joint pain and severe right-sided headaches associated with diplopia. 70 M. S. COGEN ET AL. General physical examination revealed a maculopapular rash in the characteristic butterfly distribution over the malar region and involving most of the upper extremities and trunk. Neurologic findings included a labile affect, dysarthria, left facial weakness, left hemiparesis, decreased sensation to a pin-prick on the left side, and dysmetria greater on the left side. Neuro-ophthalmologic testing revealed 45 prism diopters of exotropia and 10 prism diopters of right hypertropia in the primary position. Extraocular movements demonstrated bilateral adduction weakness with horizontal jerk nystagmus in the abducting eye (Fig. 1). In addition, there was upbeat nystagmus in upgaze. Downgaze was normal and convergence was intact. Visual acuity, pupillary reactions, visual fields, and fundi were normal. Laboratory data included an anti-nuclear antibody titer of 1:160 in a homogeneous pattern (normal < 1:20) and an anti-deoxyribonucleic acid titer of 1:40 (normal < 1:10). Cerebrospinal fluid analysis revealed normal glucose and protein levels, elevated IgG of 8.9 mgJdl (normal, 0.5-6.1 mgJdl), and no oligoclonal bands. Cranial computed tomography showed only mild cortical atrophy. Magnetic resonance scan of the head revealed a 7 x 10 mm lesion in the right side of the pons near the fourth ventricle and a 9 x 10 mm lesion in the mesencephalon just anterior to the periaqueductal gray matter, which appeared to represent separate infarcts (Fig. 2). The patient was given intravenous methylpred- FIG. 1. Extraocular movements. Top: primary posi' ion: middle: ettempted right gaze; bottom: attempted nisolone (400 mg daily) and oral Plaquenil (400 mg daily). Over the course of a week, there was improvement in adduction of the left eye, and resolution of left-sided weakness. She was subsequently switched to a gradually tapering dose of oral prednisone and continued on PlaquE'!1'lU. However, the dysarthria and dysmetria persiste-d, as did total inability to adduct the right eye on left gaze. The patient was transferred to a rehabilitation center for further care. DISCUSSION Systemic lupus erythematosus is an aut-oimmune, inflammatory, collagen vascular disorder characterized by multiorgan involvement. Ne~ logic manifestations have been reported with ~. quencies ranging from 14-75% (24-26). How~ abnormalities in regional distribution of oxygj(* utilization and blood flow to the brain have beq,. documented in patients with systemic lupus ~ ythematosus who have no neurologic signs .~ symptoms (27). This suggests that many patien.:~ with systemic lUpus erythematosus have su~ ical involvement of the nervous system. Seizures and psychoses are the most coInm.OJn neurologic manifestations of lupus, but the .de-. ease can affect virtually all portions of the Iierv(:jij$ system (Table 1) (23-25). Neurologic mani.fe~~ tions, as demonstrated in our case, tend to be mUltiple and occur when the disease is active (25,26). Pathologically, the characteristic lesion is microl&farction, related to changes in capillaries and smaIl. arterioles, and possibly to alterations in platelets (28-30). Other abnormalities include vasculitis, hemorrhages, and occlusion of the large blood vessels (24,29,30). Although arteritis of cerebral vessels has been a rare finding, perivascular infiltrates of lymphocytes have been noted frequently (30). The pathophysiology of central nevous system involvement in lupus remains incompletely understood, although several me~hanisms have been proposed. These include deposition of circulating immune complexes in the choroid plexus and cerebral vessels (24,26,29,30), direct neuronal binding of cross-reactive neurotoxic antibodies (24,26), and fluctuations in serotonin metabolism stemming from abnormal platelet activity (24,26). There are only six reports in the literature of internuclear ophthalmoplegia occurring in association with systemic lupus erythematosus. In 1950~ Cogan and associates (I) reported the first case of unilateral internuclear ophthalmoplegia in a pa.tient who died of systemic lupus erythematosus. BILATERAL INTERNUCLEAR OPHTHALMOPLEGIA 71 At autopsy, gross inspection of the blood vessels, meninges, and outer surfaces of the brain and brainstem appeared normal. Sections through the middle portion of the pons disclosed an area of infarction on the left side involving the mediallongitudinal fasciculus. At the inner margin of the lesion, there was a small artery filled with organized thrombus. Vascular changes of the small blood vessels elsewhere in the brainstern and cerebellum consisted of adventitial infiltration by lymphocytes and plasma cells with degeneration of the vessel wall, as well as intimal proliferation and thrombosis. In 1956, Bailey et al. (31) reported a case of intermittent diplopia with nystagmus on lateral gaze in a patient with lupus who subsequently died. Pathologic examination revealed vascular degeneration and vacuolization of the left medial longitudinal fasciculus. In 1959, Smith and Cogan (5) included a patient with systemic lupus erythe- FIG. 2. Magnetic resonance images of brainstem (T2 weighted, SE 2,000/100). (A) coronal section shows a focal pathologic signal in the mesencephalon (arrow). A second lesion (arrowhead) is seen in the pons. (B) axial image of mesencephalon shows a pathologic bright signal (curved arrow) in the center of the midbrain in the region of both medial longitudinal fasciculi. The cerebral aqueduct (straight arrow) appears as a low signal area due to cerebrospinal fluid pulsation. (C) axial image of pons shows a lesion (curved arrow) in the region of the right medial longitudinal fasciculus. Signal intensity of the lesion is similar to that of cerebrospinal fluid in the fourth ventricle (straight arrow). matosus in their series of 29 patients with unilateral internuclear ophthalmoplegia. Meyer and Wild (32) reported a case of unilateral internuclear ophthalmoplegia in which the patient had relatively mild systemic lupus erythematosus without other evidence of central nervous system involvement. Finally, Lessell (26) reported two cases of unilateral internuclear ophthalmoplegia resulting from brainstem involvement in patients with systemic lupus erythematosus. The predominance of unilateral medial longitudinal fasciculus involvement in vascular disorders is accounted for by anatomic features of the blood supply to the brainstem, with its strict lateralization (33). As a result, an infarction may be limited to one side. With demyelinating lesions such as those of multiple sclerosis, which are not related to the blood supply, both medial longitudinal fasciculi are usually involved (1). JClin Neuro-ophthalmol, Vol. 7, No.2, 1987 72 M. S. COGEN ET AL. TABLE 1. Neurologic manifestations of systemic lupus erythematosus Seizures Psychosis Organic brain syndrome Pseudotumor cerebri Focal encephalopathy Brainstem infarct Chorea Peripheral neuropathy Myopathy Parkinsonian syndrome Coma Myelopathy Cranial neuropathy Neuromyelitis optica Meniere's disease Aseptic meningitis Encephalomyelitis Guillain-Barre syndrome Vascular causes of bilateral internuclear opthalmoplegia have been reported in the setting of occlusive cerebrovascular disease (3,6-10), including basilar artery thrombosis due to severe atherosclerosis or hypercoagulable states and basilar artery emboli of cardiac origin. We believe that our patient represents the first reported case of bilateral internuclear ophthalmoplegia in association with systemic lupus erythematosus. Patients with bilateral internuclear ophthalmoplegia often have vertical gaze-evoked nystagmus as seen in our patient. This is due to disruption of medial longitudinal fasciculus pathways, which also transmit vertical eye movement information (34). Although skew deviation frequently occurs with unilateral internuclear ophthalmoplegia, it is rarely seen with bilateral internuclear ophthalmoplegia. The cause of skew deviation is unknown, but it may reflect imbalance of otolith inputs that cross in the medulla and ascend in the medial longitudinal fasciculi (34). Our case illustrates the value of magnetic resonance imaging in evaluating patients with suspected brainstem disease. It has been reported that even in the presence of florid symptoms of central nervous system lupus, computed tomography may show no abnormality (35-37). The most common finding on cranial computed tomography in lupus, as demonstrated in our patient, is nonspecific cerebral atrophy. Vermess et al. (35), in comparing magnetic resonance imaging to computed tomography, found brain lesions in patients with central nervous system lupus imaged only with magnetic resonance. In addition,. aH lesions demonstrated by computed to- J Clin Neuro-ophtlullmol,i(0l. 7, Nv. 2, 1987 mography were also seen on magnetic resonance imaging, often with greater clarity. Aisen et al. (36) and McCune et al. (37) made similar observations. Our case supports this view. REFERENCES 1. Cogan 0, Kubick C, Smith W. Unilateral internuclear ophthalmoplegia. Arch OphthalmoI1950;44:783-96. 2. Daroff RB, Troost BT. Supranuclear disorders of eye movements. In: Duane TO ed. Clinical ophthalmology. Hagerstown: Harper & Row, 1978;2:1-18. 3. Cogan DG. Internuclear ophthalmoplegia, typical and atypical. Arch OphthalmoI1970;84:583-9. 4. Cogan DG. Neurology of the ocular muscles, 2nd ed. Springfield: Charles C. Thomas, 1956:84-91. 5. Smith JL, Cogan DG. Internuclear ophthalmoplegia, a review of 58 cases. 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