Journal of Neuro-Ophthalmology, September 1985, Volume 5, Issue 3

Reversible vertical ocular deviations associated with raised intracranial pressure.

Skew deviation is a common neuro-ophthalmologic finding, the presence of which is classically thought to signify a brainstem lesion. It is frequently seen in conjunction with other posterior fossa abnormalities. We report the cases of five patients having skew deviations with raised intracranial pressure without posterior fossa structural lesions. Whereas skew deviation almost always does indicate intrinsic posterior fossa disease, our experience demonstrates that increased intracranial pressure by itself can cause a skew deviation, probably by causing a secondary brainstem dysfunction.

J. Oil/. NCI//'{I-(II,lt!htllll/ol. S: 15H-lbJ, lYHS © 1985 Raven Press, New York Reversible Vertical Ocular Deviations Associated with Raised Intracranial Pressure LARRY P. FROHMAN, M.D. MARK J. KUPERSMlTH, M. D. Abstract Skew deviation is a common neuro-ophthalmologic finding, the presence of which is classically thought to signify a brainstem lesion. It is fre­quently seen in conjunction with other posterior fossa abnormalities. We report the cases of five pa­tients having skew deviations with raised intra­cranial pressure without posterior fossa structural lesions. Whereas skew deviation almost always does indicate intrinsic posterior fossa disease, our experience demonstrates that increased intracranial pressure by itself can cause a skew deviation, probably by causing a secondary brainstem dys­function. Skew deviation is classically defined as an ac­quired vertical divergence of the eyes that is sec­ondary to a supranuclear dysfunction and not secondary to a peripheral neuromuscular lesion or a mechanical process in the orbit. 1,2 When examining a patient with a suspected skew de­viation, the absence of a paretic muscle or lo­calizing noncomitance by version, saccades, and the prism cover test must be established. Prior vertical heterophoria that has decompen­sated because of systemic illness has to be elim­inated. Keane3 found skew deviations in 8% of in-hospital neuro-ophthalmologic consulta­tions. The entity's presence is thought to be a posterior fossa localizing sign. There are, how­ever, reports of a case of skew deviation in a patient with pseudotumor cerebri,4.5 a case of a patient with skew deviation secondary to he­patic coma,6 a case due to a supratentorial as­trocytoma, 2 and three cases with skew sec­ondary to a supratentorial bleed. 3 We describe From the Departments uf Ophthalmulugy (L.P.F., M.j.K.) and Neurolugy (M.j.K.), New York University School of Medicine, New Yurk, New York. Write for reprints to: M. j. Kupl'rsmith, M.D., 530 First Av­enue, New York, NY 10016, U.s.A. ISS our series of five patients (all examined by M.j.K.) who lacked posterior fossa structural le­sions, who had skew deviations, and none of whom had a prior history of strabismus. Case Studies Case 1 A 37-year-old woman had three or four epi­sodes of frontal headaches, confusion, and falling down over a 6-week period. Her appetite diminished and she was lethargic. The confu­sion would persist for several hours after she had fallen down. Two weeks prior to admis­sion, she had an episode during which her head jerked to the right, her arms twitched, and she fell down. She remained slight obtunded and had difficulty expressing herself. No further sei­zures occurred. On the day of admission, the patient noted the onset of intermittent vertical diplopia. The past medical history was noncon­tributory and she was taking no medications. The neurologic examination was remarkable only for difficulty with word finding and occa­sional inappropriate speech. Snellen acuity was 20/25 in each eye and the Ishihara pseudoiso­chromatic color plates were 7 of 10 correct in each eye. Visual fields were remarkable only for a large blind spot in each eye. The pupil was 3 mm in each eye, round and reactive to light without relative defect. The anterior examina­tion was unremarkable, the corneal reflexes were intact, and tensions were normal. Extra­ocular versions, pursuit, and saccades were in­tact. The prism cover test showed a left hyper­tropia of 2 prism diopters, present in all fields of gaze except left gaze, up and to the left, and up and to the right, when the deviation in­creased to 4 prism diopters. The hypertropia at ne~r measured 2 prism diopters in primary po­SItion. A skew deviation was diagnosed. . Papilledema, with hemorrhages and exudates m both papulomacular bundles, was noted in Journal of Clinical Neuro-opthalmology both fundi and was felt to be the cause of the slight decrement in visual performance. Labo­ratory studies included a normal electrolyte panel, coagulation studies, and thyroid fUI1C­tions, and a negative serology for svphilis. The hemogram was significant for a whitt' count of 19,300, with a normal differential, and a platelet count of 562,000. T1w electrocardiogr<lm and chest roentgenogram were normal. An electro­encephalogram showed a left cerebral dysfunc­tion. A computed tomographic scan of tlie head showed a necrotic left frontal glioma (Fig. 1) and angiographY was consistent with malignancy. The patient was k)st tl) folknv-up. Case .2 A 39-~'ear-old man was hospitalized for sei­zures, and a left frontal lobe mass found on computed tomographic scan (Fig. 2). He had a new complaint of blurred vision. Despite his complaint, Snellen acuity was 20/20 in each eye and color vision and the visual fields were normal. The pupils were -1 mm in the right eye and 5 mm in the left eve, and were round and reactive to light with hippus and without rela- Figure 1. Preoperative computed tomographic scan (cast' 1). after administration of contrast medium, demonstrating a mass of increased attenuation surrounded by an area of de­creased attenuation, which is probably edema in till' left frontal lobe. The left anterior cerebral artery is displaced medially (arrowhead) and the left middle cerebral artery (broken arrow) is displaced posteriorly. There is no evidt'nCl' of extension into the posterior fossa. September 1985 Frohman, Kupersmith Figure 2. Preoperative computed tomographic scan (case 2). after contrast medium administration, showing right fron­t() temporal mass (arrow) compressing the right lateral ven­tricle, with areas of increased and decreased attenuation. The mass extends to the thalamus, compressing the third ventricle. tive afferent defect. The external examination was normal. Extraocular versions, saccades, and pursuit were normal. In left lateral gaze there was conjugate jerk nystagmus, and op­tokinetic nystagmus was diminished to the left. Red glass and prism cover test at near showed a comitant exophoria and a left hypertropia comitant in all fields of gaze except downgaze, consistent with skew deviation. A head tilt tesf was negative. Previous ophthalmic records in­dicated no preexisting strabismus. The fundi were normal except for the absence of sponta­neous or elicitable venous pulsations. The neu­rologic examination was remarkable only for acalculia and an ataxic gait. The etiology of the blurred vision was felt to be the extraocular eye muscle deviation. After a left frontal crani­otomy for excision of a glioma, the patient's diplopia and visual complaints resolved. Case 3 A 44-year-old man presented with a I-year history of fatigue and difficulty seeing to his left and a new onset of vertical diplopia that was present only with both eyes uncovered. Left leg weakness began a few days prior to hospital­ization. There was no history of headaches. 159 ReVl'rsiblp Vl'rtic"llkul.u Deviations Seven years before pn:'sentation he sustained a loss of consciousness, and an evaluation re­vl'aled a right tl'mporal mass for which he was taking phenytoin (Fig. 3). The remainder of the medical history was noncontributory. The neu­rologic examination was remarkable for a left central facial palsy, left-sided weakness (worse in upper extremity than in lower extremity), left-sided hyperreflexia, and a left Babinski re­flex. There was some dysmetria on left finger­to- nose testing. Uncorrected Snellen acuity was 20/20 in each eye. Color vision testing with the Ishihara plates was normal in each eye, but the numbers in the left visual field showed a dense, left homonymous hemianopsia. Two millime­ters of ptosis of the right upper eyelid with good levator function was present. The pupils were 3 mm in the right eye and 4 mm in the left eye in room light, and 6 mm in the right eye and 8 mm in the left eye in the dark. Both were round and reactive to light and showed no relative af­ferent defect. Phenylephrine, 0.5%, instilled into the inferior fornices had no effect on the ptosis or the pupilS. Extraocular versions were full, pursuit was of a cogwheel nature in all fields, and saccades were broken into hypo­metric microsteps. Optokinetic nystagmus was markedly diminished in all directions. At near, he had an exophoria of 10 prism diopters and a Figure 3. Preoperative computed tomographic scan (case 3). following administration of contrast medium, shOWing a Il'ft frontal lobe lesion (arrow) of decreased attenuation com­pressing the lateral ventricle without evidence (If either pos­tenor or Infenor extension. 160 right hypertropia of 6 prism diopters comitant in all fields. At distance he had a comitant exophoria of 4 prism diopters and a comitant hypertropia, consistent with a skew deviation. A head tilt test was negative. Funduscopy was normal. After excision of a right temporal lobe glioma, the diplopia resolved. Case 4 A 37-year-old obese woman was admitted to University Hospital with a I-day history of throbbing occipital headache that woke her from sleep several times. She noticed the onset of vertical binocular diplopia and vertigo. Her past medical history was remarkable only for depression, for which she occasionally took tri­fluoperazine. There was no prior history of stra­bismus. She also took mineral and multivitamin supplements. The neurologic examination was unremarkable. Corrected Snellen acuity was 20/ 20 in both eyes and color vision was normal. The visual fields revealed enlarged blind spots in both eyes. The pupils were 4 mm in both eyes, round and reactive to light without rela­tive afferent defect. The external examination was normal. The extraocular versions, saccades, and pursuit were intact. Optokinetic nystagmus was intact, as were the corneal reflexes. A left hypertropia of 2 prism diopters in primary gaze, which increased to 6 prism diopters in left gaze, 4 prism diopters in downgaze, and 6 prism diop­ters down and to the left, was noted. A left hy­perphoria was present in all other fields of gaze. A head tilt test was negative. Funduscopy dem­onstrated early superior and inferior nerve fiber layer edema in both eyes. A computed tomo­graphic scan of the head was normal except for small ventricles. A lumbar puncture was normal except for an opening pressure of 290 mm of water. A diagnosis of skew deviation secondary to increased intracranial pressure from pseu­dotumor cerebri was made. Following the lumbar 'pun~ture, she was treated with a pro­gram ot weIght reduction and salt restriction, a~d, b.y 1 week later, there was no subjective dIplopIa. The prism cover test revealed her to have orthophoria in all fields of gaze even with the red glass test. Case 5 A 24-year-old woman presented with a retro­bulbar pressure headache and horizontal bin­ocular diplopia. No history of extraocular ab­no. rmalitie~ w~s noted by her ophthalmologist pnor to thIS tIme. Her regimen of chronic ste­rOIds had been tapered off following a colec­tomy for Crohn's disease 1 week before. The Journal of Clinical Neuro-ophthalmology neurologic examination was within normal limits. Uncorrected Snellen acuity was 20/20 and color vision was normal in both eyes. The pupils were round and reactive to light without af­ferent defect. Extraocular versions, pursuit, sac­cades, and optokinetic nystagmus were intact. A comitant esotropia of 10 prism diopters at near and 20 at distance was noted. No vertical deviation was present. The discs showed blur­ring of the nerve fiber layer in both eyes. When the patient was examined 3 weeks later, she still had headaches and diplopia. The examination was unchanged except that she now had an eso­tropia of 12 prism diopters and a comitant left hypertropia of 8 prism diopters at near, and both optic discs were edematous with splinter hemorrhages. Visual fields showed enlarged blind spots in both eyes. A computed tomo­graphic scan of the head was normal. A lumbar puncture was normal except for an opening pressure of 250 mm of water. Following the lumbar puncture, the diplopia markedly di­minished. A diagnosis of skew deviation and divergence insufficiency due to raised intra­cranial pressure from pseudotumor cerebri was made. She was placed on a regimen of oral ste­roids, and her papilledema and strabismus rap­idly resolved. When the patient was seen in follow-up 2 weeks later, an alternate cover test at distance revealed neither an esophoria nor a hyperphoria. Discussion Smith et aJ.2 in presenting their criteria for diagnosing skew deviation, suggested-de­spite the fact that they had one case of a supra­tentorial astrocytoma-that the presence of a brachium pontis or mesencephalic lesion strongly supported the diagnosis of skew de­viation. In our series of five patients, none of whom had a prior history of strabismus, all had a skew deviation without a posterior fossa le­sion. In case 4, although the prism cover test left a question of left inferior rectus palsy, ex­traocular versions and saccades were normal and there were no other findings to indicate the pr~sence of a paretic muscle. None of our pa­tients had clinical or laboratory evidence of phe­nytoin toxicity. Besides the case described by Smith et ai., we found five other cases in the literature of skew deviation without a definite posterior fossa le­sion. Whereas Keane3 arrived at conclusions similar to those of Smith et ai., he had three cases of "supratentorial hemorrhages with mid­brain dysfunction" that had skew deviations. Inasmuch as this was before the advent of com­puted tomographic scanning, there is no way to September 1985 Frohman, Kupersmith know if Keillw's cases were due to direct com­pression of the upper brainstem by extension of the hemorrhage. Merikangas4 described a 35­year- old woman who had headaches and epi­sodic vertical diplopia with papilledema and skew deviation. A negative computed tomo­graphic scan of the head and an opening pres­sure on lumbar puncture of 550 mm of water, with no other findings, confirmed the diagnosis of pseudotumor cerebri. As in our two patients with pseudotumor, the skew deviation resolved as the intracranial pressure was lowered. Fisher!> reported the case of a patient with skew deviation due to hepatic coma. That skew deviation could be a false localizing sign due to raised intracranial pressure is not surprising. Duke-Elder and WybarH state that heterophorias may become symptomatic from any form of disability including lack of sleep or exercise, and pregnancy and lactation. Al­though our patients had no prior history of stra­bismus, illness unmasking a latent vertical het­erophoria cannot absolutely be ruled out as the cause of a transient skew deviation in cases 1­4. A more likely possibility is that increased in­tracranial pressure, of any cause, may affect the vestibular system or brainstern to induce a true skew. In either instance, it is likely that the same mechanism (that is, raised intracranial pressure) induces either the skew or the un­masking of a latent heterophoria. The rapid re­covery of two of our patients after lumbar punc­ture supports this. Patients with raised intra­cranial pressure often complain of visual blurring. It is possible that small vertical devia­tions are a common cause of visual complaints in cases of elevated increased intracranial pres­sure, but they are overlooked because exam­iners focus on the obvious papilledema and in­creased intracranial pressure as the cause of the visual complaint. Increased intracranial pressure is known to cause a variety of false localizing brainstem signs. Devereaux et al. 4 reported the cases of two patients who developed internuclear oph­thalmoplegia secondary to subdural hematoma, which resolved after evacuation of the clot. Baker and BunciclO reported on a series of 60 pseudotumor cerebri patients, two of whom had a vertical deviation associated with an ab­ducens nerve paresis. Kirkham et al. 11 reported on a series of patients with divergence paralysis due to pseudotumor cerebri. These patients' symptoms all disappeared as intracranial pres­sure was lowered. Cranial nerve paresis can also occur as a false localizing sign in cases of increased intracranial pressure. McCammon et al. 12 stated that, in reviewing the literature on pseudotumor cerebri, 10-40% of patients de- 161 veloped sixth nerve palsies. They found facial weakness to be a not uncommon finding, and reported one case of oculomotor paralysis. Hal­pern and Gordon 11 reported the case of a patient with pSl'udotumor cerebri who developed twchll'ar nerve palsy, which resolved with ste­wid therapy. Snyder and FrenkeIl'] reported the case of one patient with bilateral total ophthal­moplegia and a facial nerve palsy secondary to pseudotumor cerebri, all of which responded to therapy. Hart and Carter!'; described one pa­tient with facial pain and a diminished corneal ret1ex due to pseudotumor cerebri. The symp­toms all resolved with the lowering of intra­cranial pressure. Increased intracranial pressure, therefore, has widespread effects on the cranial nerves and the brainstem. Just how it causes skew deviation is not known. There is much literature relating the vestibular apparatus to maintenance of eye po­sition. Cogan] mentioned that "the fact that a vertical divergence occurs on stimulating the labyrinth or with unilateral labyrinth disease suggests that the pathogenesis of skew devia­tion is linked with the vestibulo-ocular path­ways." Brain16 reported in 1926 on a patient with chronic nonsuppurative otitis interna, with no neurologic disease, and a skew deviation. Cairns and Brain 17 reported on four patien ts with intractable dizziness who underwent ther­apeutic eighth cranial nerve transection. One patient developed a transient postoperative skew deviation. From the description of the other three cases, it seems likely that all had a skew deviation, since no single paretic muscle could explain the vertical strabismus the pa­tients developed. The authors stated that "there is ample physiological evidence that skew de­via~ ion of the eyes is an abnormal ocular posture whICh may be produced by a defect in tonic im­pulses from the labyrinth on the side of the di­vided nerve." Halmagyi et al.l~ reported on a patient who had his left vestibular labyrinth in­advertantly destroyed. The patient~ demon­strated postural changes, left ocular counter­rolling, a left head tilt, and a skew deviation. The Tullio phenomenon, as reported by Deecke et al.,]Y demonstrates the capacity or semicir­cular canal stimulation to produce a skew de­viation. Experimental stimulation of an ampul­lary nerve of the semicircular canal in cats can cause a skew deviation. 20 KeaneJ pointed out that skew deviation secondary to a brainstem l~sio~ often has an accompanying medial lon­gItudInal fasciculus lesion. None of our patients had this. . Whereas most cases of acquired skew devia­tIon are indicative of brainstem pathology, we postulate a second, less trequently encountered 162 Reversible Vertical Ocular Deviations presentation of skew deviation due to increased intracranial pressure of any cause. It is likely that the raised intracranial pressure somehow affects the labyrinth or its projections through the brainstem, perhaps similar to unequal stim­ulation of the ampullary nerves, producing a skew. In fact, Kaaber and Zilstorfpl reviewed vestibular symptoms and other inner ear com­plaints with increased intracranial pressure and showed that, in patients with benign intra­cranial hypertension, 56% demonstrate ab­normal vestibular function. In follow-up, 92% of patients had the vestibular function return to normal with normalization of the intracranial pressure. In addition, McPherson et a!. 22 dem­onstrated that, in rabbits, increased intracranial pressure prolonged latency of the auditory evoked potential, which reversed with the low­ering of the increased intracranial pressure. The effect was felt to be due to some neuropraxic conduction defect from increased intracranial pressure on the brainstern pathways involved with the auditory evoked potential response. A similar mechanism in humans could cause the unequal stimulation of the ampullary nerves. A study of the auditory evoked potentials of pa­tients with increased intracranial pressure of re­versible causes would be useful in determining if this is true. References 1. Cogan, D. G.: ,\'eurolog!! 0; the Ocular Muscles. Charles C Thomas, Springfield, 1956, pp. 134­135,219. 2. Smith, J. L., David, :\'. J., and Clintworth, G.: Skew deviations . .\'eurology14: 96-105, 1964. 3. Keane, J. R.: Ocular skew deviation. Arch. Neurol. 32: 185-190, 1975. -1. Merikangas, J. R.: Skew deviation in pseudo­tumor cerebri. .'11111. SCI/rol. 4: 583, 1978. 5. Baker, R. S., and Buncic, J. R.: Vertical ocular motility disturbance in pseudotumor cerebri. J. Clill. Ncuro-l'l'hthalllll11. 5: -11-.f.l, 1985. b. Fisher, M.: Ocular skew deviation in hepatic coma. ,. Ncurt'l . .\icurosurg. PSl/chiatrl/ 44: 458, 1981. . . 7. Burian, H. M., and \'lm Noorden, G. K.: Binoc­ular \ 'isio~ alld Ocular A10tililtr C. V. Mosby, St. LOUIS, 19/-1, p. 3-15. 8. Duke-Elder, S., and Wvbar, K,: Ocular Motility alld Stral1isllluS. \'lll. 6, In SystclII of Ophthalmology, Duke-Elder,S., Ed. C. V. Mosby, 51. Louis, 1973, pp, 527, 538. . 9. Devereaux, M. W., Brust, J. C. M., and Keane, J. R.: Internuclear ophthalmoplegia caused by subdural hematoma. Ncurology 29: 251-255, 1979. . 10. Baker, R, 5" and Bunde, J. 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