Journal of Neuro-Ophthalmology, September 1990, Volume 10, Issue 3

Diabetic complete external ophthalmoplegia.

A 69-year-old diabetic patient taking oral hypoglycemic drugs and with no systemic complications presented a right peripheral facial palsy, and 2 months later a complete right external ophthalmoplegia with sparing of the pupillary function. Clinical, radiologic, and other laboratory investigation ruled out compressive, infectious, and inflammatory etiology. Four months later, after achieving good metabolic control, there was almost complete recovery of the ophthalmoplegia without signs of aberrant regeneration of the third nerve. Diabetes is proposed as the etiology of this case. A possible anatomic substrate is presented to explain the findings.

Journal of Clinical Neuro- ophthalmology 10( 3); 206- 209, 1990. © 1990 Raven Press, Ltd / ork Diabetic Complete External Ophthalmoplegia Cristian F. Luco, M. D., and Raul F. Valenzuela, M. D. A 69- year- old diabetic patient taking oral hypoglycemic drugs and with no systemic complications presented a right peripheral facial palsy, and 2 months later a com­plete right external ophthalmoplegia with sparing of the pupillary function. Clinical, radiologic, and other labo­ratory investigation ruled out compressive, infectious, and inflammatory etiology. Four months later, after achieving good metabolic control, there was almost com­plete recovery of the ophthalmoplegia without signs of aberrant regeneration of the third nerve. Diabetes is pro­posed as the etiology of this case. A possible anatomic substrate is presented to explain the findings. Key Words: Diabetes- Facial palsy- Ophthalmoplegia. From the Department of Neurology and Neurosurgery, Neu­rophthalmology Section, School of Medicine, Universidad Cat6lica de Chile, Instituto de Neurocirugfa, Universidad de Chile and Oftalm6logos Asociados; and Department of Neurol­ogy and Neurosurgery ( R. F. V.), School of Medicine, Univer­sidad Cat6lica de Chile, Santiago, Chile. Address correspondence and reprint requests to Dr. Chris­tian F. Luco at the Department of Neurology and Neurosur­gery, School of Medicine, Universidad Cat6lica de Chile, Santiago, Chile. 206 The oculomotor nerve nuclei are located in the brainstem, from which the nerve fibers emerge, and after travelling across the base of the cranial cavity, reach the ocular muscles in the orbit. Neu­rologic lesions involving the oculomotor nerve trunks or their nuclei produce paresis of the corre­sponding muscles which must be differentiated from mechanical or muscular disorders that might simulate a neurologic lesion ( 1- 3). Oculomotor nerve palsies may have numerous causes, and the most frequent ones are those that stretch or compress the nerve trunks, such as di­rect injury, aneurysm, or neoplasm. Less frequent causes are metabolic, ischemic, infiltrating, or de­myelinating lesions ( 4,5). In large series, diabetes mellitus is not an infrequent cause of oculomotor nerve palsies. The sixth nerve is the most fre­quently involved ( 6) cranial nerve in diabetic oph­thalmoplegia, although some have reported that the sixth and the third cranial nerves are equally affected ( 4,5,7). Diabetes rarely causes multiple si­multaneous oculomotor nerve palsies, and thus, these cases must be thoroughly investigated to ex­clude other causes ( 1,3). Ischemia as the mecha­nism of diabetic oculomotor nerve palsies was his­topathologically demonstrated by Dreyfus ( 8), As­bury ( 9), and Weber ( 10) by studying affected third nerves in diabetic patients. They demonstrated central core infarction of the nerve trunk with spar­ing of peripheral fibers. This mechanism also ex­plains why pupillary fibers, which run in the pe­riphery of the nerve, are spared; this is a charac­teristic sign of medical ( nonsurgical) palsy of the third nerve. In fact the finding of a spared pupil in a third nerve palsy of compressive etiology is ex­ceptional ( 11). We recently studied a diabetic patient who de­veloped a unilateral complete ophthalmoplegia without pupillary function involvement. DIABETIC OPHTHALMOPLEGIA 207 FIG. 1. Evolution of right peripheral facial palsy ( left side photograph was taken on November 28, 1988; right side photograph was taken on February 2, 1989). CASE REPORT A 69- year- old diabetic man who had no systemic complications had been treated with oral hypogly­cemic drugs ( glibenclamide) for 10 years. His com­plaints began with a right peripheral facial palsy, without hyperacusis or chorda tympani involve­ment, which recovered at a very slow rate. Fasting blood glucose was 276 mg % at that time. Two months later he suddenly developed severe diplo­pia and right supraciliary mild pain which disap­peared in about 1 week. Three weeks later he sought medical help. On examination his blood pressure was 145/ 80. General physical examina­tion, blood count, erythrocyte sedimentation rate, cholesterol, and chest x- ray were normal. Fasting blood glucose was 234 mg %. Neurological exam­ination disclosed a right peripheral facial palsy ( Fig. 1), diffuse deep tendon hyporeflexia, moder­ate distal unilateral hypoesthesia of the lower limb, and paresthesias of both lower limbs. Cerebrospi­nal fluid ( CSF) examination showed glucose 123 mg %, protein 86 mg %, cells 0.5 mm3 . Bacterio­logical studies and cytological examination for neo­plastic cells in CSF were all negative. Neurophthal­mological examination showed a corrected visual acuity of 20/ 25 in 00 and 20/ 20 in OS. Pupils were equal in size and both reacted briskly to light. Oc­ular motility tests demonstrated severe paresis of all extrinsic muscles and ptosis of the right eyelid ( Fig. 2). There was no exophthalmos. Fundoscopy showed normal papillae, a few microaneurysms, and small hemorrhages. Visual fields were normal. At the anterior pole there were no signs of vascular congestion, nor orbital or periorbital bruits. A high resolution computed tomography ( CT) scan did not show lesions in the orbit, cavernous sinus, cra­nial base, or brainstem. In the follOWing weeks, good metabolic control was achieved with diet and drug adjustment. Eleven weeks later, he began to recover motility of all right eye extrinsic muscles, but he still had im­portant residual paresis with diplopia. At that time the ptosis had diminished, but the facial palsy re­mained. A 4- month follow- up examination showed sig­nificant recovery of facial palsy ( Fig. 1), and no changes in neurologic signs of the limbs. Neuro­ophthalmologic examination demonstrated a very important recovery of ocular motility, with slight limitation of lateral rectus and superior oblique muscles of the right eye ( Fig. 3), and absence of any sign of aberrant regeneration of the third nerve. At follow- up late in 1989, serum VORL and se­rum Lyme enzyme- linked immunosorbent assay ( ELISA) tests were negative in our laboratory and checked ( also negative) in the Louis Pasteur Insti­tute in France. Figs. 4 and 5 show the patient's current appearance, with notable clearing of the right facial paresis, but subtle aberrant regenera­tion of the right facial nerve is now evident. DISCUSSION Each ocular motor nerve has its own separate pathway and they approach each other at the cav­ernous sinus. A multiple ocular motor nerve dys­function tends to localize the lesion in the cavern­ous sinus or distally. An isolated nerve dysfunc­tion does not allow a precise topographic localization since the lesion could be at any place FIG. 2. Ocular movements during acute phase of right ophthalmoplegia ( picture taken on November 28, 1988). JClin Neuro- ophthalmol. Vol. 10, No. 3. 1990 208 C. F. LueD AND R. F. VALENZUELA FIG. 3. Photograph taken on February 2, 1989 demon­strates very important recovery of ocular motility; a slight limitation of superior oblique and lateral rectus muscles still remains. from the nucleus to the orbit. Our patient had mul­tiple nerve involvement which led us to clinically localize the lesion in the cavernous sinus. Causes of cavernous sinus syndrome are numerous: in­fraclinoidal aneurysms, primary or metastatic tu- FIG. 4. Taken late 1989; shows improvement of right facial paresis. I Gin Nnlro- ophthalmol, Vol. 10. No. 3. 1990 mors, inflammatory and vascular provo.:'; es, etc. ( 1,4,5). A high resolution CT scan excluded a struc­tural lesion of the orbit, the cavernous sinus and the brainstem. The only associated illness this pa­tient had was a decompensated diabetes, therefore a diabetic ophthalmoplegia was diagnosed. The evolution of the ophthalmoplegia into spontane­ous resolution ( by achieving metabolic control) and the absence of aberrant regeneration signs in the third nerve, made compression a highly im­probable cause of the ophthalmoplegia. Meningeal carcinomatosis, mucormycosis, or an intracranial neoplasia were ruled out with the clinical evolu­tion; CT scan and normal CSF [ the increased level of CSF protein is in the range of values frequently encountered in diabetic neuropathy ( 12,13)]. In To­losa- Hunt syndrome severe periorbital pain is a very important sign ( 14- 16) which was almost ab­sent in this patient who had only a slight and tran­sient supraciliary pain with the severe ophthal­moplegia. The singularity of this case is the simultaneous multiple paralysis of the three ocular motor nerves which has been reported in the literature as very infrequent in diabetes ( 2,3,6,7,17) and is not even mentioned in some large series ( 4,5). Weber ( 10) demonstrated a central core infarction at the sub­arachnoidal portion of the third nerve in a diabetic FIG. 5. Same date as Fig. 4, showing aberrant regen­eration of right VII ( arrow). DIABETIC OPHTHALMOPLEGIA 209 patient with a oculomotor palsy. In our patients, we believe, as in the cases of Dreyfus and Asbury ( 8,9), that the ocular motor nerves were damaged at the cavernous sinus where they have common nutrient vessels ( 18-- 20). The internal carotid artery at its intracavernous portion gives off three branches: the meningohypophysial trunk, the in­ferior artery of the cavernous sinus and the capsu­lar artery. The meningohypophysial trunk gives off three smaller branches: the tentorial artery which irrigates the third and fourth cranial nerves, the dorsomeningeal artery that irrigates the sixth nerve and the inferior hypophysial artery. The in­ferior artery of the cavernous sinus irrigates the third, fourth and sixth cranial nerves in almost all their intracavernous portion ( 18). In this patient probably one of these small arteries was occluded, perhaps the inferior cavernous sinus artery which could have suffered a diabetic angiopathy leading to ischemia of all three ocular motor nerves. Without histopathology we cannot be certain of the exact etiology of the ophthalmoplegia in our patient, but clinically the patient had an evolution consistent with a diabetic neuropathy, recovering when good metabolic control was achieved and having excluded all other common causes. REFERENCES 1. Bosley T, Schatz N. Clinical diagnosis of cavernous syn­dromes. In: Neurologic clinics 1983; 4: 929- 49. 2. Ross, A. Recurrent cranial nerve palsies in diabetes melli­tus. Neurology 1962; 12: 180- 5. 3. Sergott R, Glaser J, Berger L. Simultaneous bilateral dia-betic ophthalmoplegia. Report of two cases and discussion of differential diagnosis. Ophthalmology 1984; 91: 18- 22. 4. Rucker CWo The causes of paralysis of the third, fourth and sixth cranial nerves. Am JOphthalmol 1966; 61: 1293-- 8. 5. Rucker CWo Paralysis of the third, fourth and sixth cranial nerves. Am JOphthalmoI1958; 46: 787- 94. 6. Collier J. Paralysis of the oculomotor nerve trunks in dia­betes. 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