Journal ofNeurology, Neurosurgery, and Psychiatry, 1977, 40, 1198-1202

Passive ocular proptosisBRIAN P. O'NEILL

From the Department of Neurology, University of Michigan Medical Center, and the NeurologyService, Veterans Administration Hospital, Ann Arbor, Michigan, USA

S UMM A R Y Two patients with oculomotor neuropathy demonstrated passive ocular proptosis.In both instances, there was no evidence of a pathological process exerting a vector of forcethrough the orbital opening. The proptosis is caused by a combination of the loss of the normalbackward force exerted by the ocular recti muscles and the presence of a small anteriorlydirected force exerted by the ocular obliques. Computerised tomography of the orbital andretro-orbital regions was of value in establishing the diagnosis and excluding orbital disease inone patient. The role of computerised tomography in the evaluation of the patient with ocularproptosis is discussed.

Unilateral orbital proptosis (exophthalmos) isusually associated with pathological conditions thatexert a vector of force directed externally throughthe orbital opening. Most commonly, unilateralexophthalmos results from a mass lesion at theorbital rim, such as a lacrimal gland tumour, amass behind the globe but within the orbit, suchas an optic nerve glioma, or a retro-orbital mass,such as a sphenoid wing meningioma. However,the proptosis may rarely be seen as a passivephenomenon secondary to impairment of the sup-porting tissues of the globe. The following patientsare examples of passive ocular proptosis due tooculomotor nerve palsy and illustrate the use ofcomputerised tomography (CT scan) in theevaluation of exophthalmos.

Case reports

CASE 1A 55 year old man, chronically ill from severediabetes mellitus, chronic renal failure, andcoronary atherosclerotic heart disease, experiencedsudden, throbbing, right sided supraorbital andretro-orbital head pain. This was followed within24 hours by total closure of the right eye and,when the eyelid was passively raised, diplopia.Although requiring, and taking, insulin, hisdiabetes was in poor control just before the onsetof symptoms. He was otherwise well without

Address for correspondence and reprint requests Dr O'Neill, Neur-ology Service (127), Veterans Administration Hospital, 2215 FullerRoad, Ann Arbor, Michigan 48105, USA.Accepted 16 July 1977

recent history of fever, nausea, vomiting, photo-phobia, trauma, or facial infections. He was ad-mitted to the Ann Arbor Veterans AdministrationHospital three days after the onset of hissymptoms.

Approximately 18 years earlier, the patient hada similar episode, marked by headache, ptosis,and diplopia which resolved after several weeks.His diabetes was first diagnosed at that time andhas since required insulin maintenance. Thepatient had no other eye complaints exceptgradually decreasing visual acuity, corrected byrefraction, and fluctuating worsening of his visualacuity when hyperglycaemia was pronounced.On neuro-ophthalmological examination, the

patient demonstrated 4 mm of proptosis, directedanterolaterally (Fig. 1) without tenderness tomovement or palpation, and there was normalretropulsion. No bruits, pulsations, or venousengorgement were noted. Complete ptosis waspresent at rest but 2 mm of levator function wasperformed. Central vision was without scotomaor visual field defect. Cataracts and a non-proliferative retinopathy were present bilaterally.No optic nerve changes were noted. Corneal andperiorbital sensation was normal. Tears andperiorbital sweating were symmetrically present.Pupillary reactions, both direct and consensual,were present equally well. Spontaneous ductionswere full in the left eye. The only spontaneousductions present in the right eye were those per-formed by the lateral rectus and the superioroblique muscles. All other motions of the righteye were absent. Forced ductions of the right eye

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Fig. 1 Case 1. Superior photograph showing anterior-lateral displacement of right eye.

were normal. An edrophonium test (10 mg edro-phonium chloride, intravenously) gave no changein the eye findings in the presence of systemicpharmocological responsiveness.Radiographs of the skull and sinuses were

normal. A lumbar puncture was performed toexclude subarachnoid bleeding and an acellularcerebrospinal fluid sample was obtained. Bloodsugar at admission was 18.26 mmol/l (329 mg/dl).Two consecutive sedimentation rates were elevated(55 and 56 mm/h, Wintrobe) and a biopsysample of the main temporal artery was normal.The clinical impression was diabetic cranialneuropathy of the right oculomotor nerve.

CASE 2A 75 year old man suddenly developed ptosis anddiplopia at age 72 years. The diplopia, however,was noted only when the ptosed lid was lifted;the patient's vision was otherwise essentiallymonocular. A vague headache accompanied theonset, but there was no eye pain or constitutionalsymptoms. Similarly, there were no identifiableprecipitants or paralleling systemic disease pro-cesses. Over the subsequent three years there hasbeen gradual anteromedial displacement of theglobe and persistent diplopia. The ptosis has partlyimproved thus allowing binocular vision. He wasreferred to the Ann Arbor VA Hospital at age74 years after symptoms of weakness, weight loss,and a change in the colour and texture of skin

and hair appeared. Skull radiographs and bilateralcarotid angiography were performed before re-ferral and were normal. Further radiographs ofthe skull, orbits, superior orbital fissures, andtomography of the sella turcica were normal, aswas a brain scan. Panhypopituitarism was sug-gested after endocrinological evaluation demon-strated subnormal values for thyroid, adrenal, andgonadal function tests. The probability ofpanhypopituitarism was affirmed by abnormalprovocative tests and near normal values forhypothalamic releasing hormones. Metyraponeadministration failed to elevate diagnosticallyabove baseline the plasma cortisol values or theurinary excretion of 17-ketosteroids and compoundS. Fasting blood sugar and a three hour glucosetolerance test were normal. Appropriate replace-ment therapy was begun.He was readmitted to the Ann Arbor VA

Hospital one year later at age 75 years wherestability of his endocrinological status on replace-ment therapy was documented. The precedingradiological studies were repeated and were againnormal. Computerised axial tomography of thehead was performed with particular emphasis onthe orbital and retro-orbital areas (Fig. 2). Noperiorbital, intraorbital, or retro-orbital abnor-malities were noted either before or after infusionof contrast medium. Several 4 mm sections weremade at the level of the orbits to define carefullythe appearance of the optic nerves and extra-

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Brian P. O'Neill

Fig. 2 Case 2. CT scan (non-enhanced) of the orbits at level of optic nerves. Periorbital,orbital, and retro-orbital areas are normal. A very slight asymmetry of globe positions isnoted. The dissimilar lens images suggest dysconjugance.

Fig. 3 Case 2. Superior photograph showing slight anterior displacement of left eye.

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ocular muscles. Only a small degree of anteriordisplacement of the left globe, and dissimilar lensimages, suggesting dysconjugance, were seen.The neuro-ophthalmological examination

showed the same abnormalities on his two AnnArbor VA hospitalisations, and are summarisedas follows. The general appearance of the patientwas marked by 2 mm of proptosis (Hertelexophthalmometer) of the left eye with normalretropulsion (Fig. 3). There was no pulsation,bruit, or venous engorgement present. Fourmillimetres of ptosis were present at rest, as wellas 4 mm of levator function. Visual acuity (withrefraction), one metre tangent screen examin-ation, and funduscopic evaluation were normal.The corneal and periorbital sensation was normal.A dilated, fixed pupil was present on the left.Normal pupillary responses and spontaneousductions were present on the right. Spontaneousductions of the left eye showed the functions ofthe lateral rectus and superior oblique to be nor-mal, whereas the other recti and the inferioroblique were moderately restricted in movement.Forced ductions of the left eye were normal, andan edrophonium test (10 mg edrophoniumchloride, intravenously) gave no change in the eyefindings. The clinical diagnosis was pituitaryapoplexy with oculomotor nerve infarction.

Comment

Both these patients clinically had oculomotornerve infarction as evidenced by the suddennessof onset, totality of the ptosis, the paresis ofoculomotor nerve innervated extraocularmusculature, and the normality of both fourthand sixth nerve function. The sparing of pupillaryfunction and the peri- and retro-orbital pain inthe first patient, a severe diabetic, is typical ofdiabetic oculomotor neuropathy (Dreyfus et al.,1957). Angiography to exclude the rare posteriorcommunicating artery aneurysm that spares thepupil (Kasoff and Kelly, 1975) was not thought tobe indicated clinically without evidence of sub-arachnoid haemorrhage and because of thepatient's general state of health. Temporalarteritis, although a consideration and probablymediated by a microvascular infarction of theoculomotor nerve (Walsh and Hoyt, 1969b) similarto that of diabetes, was probably excluded by thebiopsy of the trunk of the main temporal artery(Meadows, 1966). Therefore, high dose corti-costeroids in spite of the negative biopsy wasjudged particularly hazardous because of his pre-carious diabetic control, even though someinvestigators recommend therapy in the face of a

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negative temporal artery biopsy (Hunder et al.,1969).The second patient's total ophthalmoplegia and

panhypopituitarism were temporally related andprobably represent the form of adenoma describedby Symonds where a tongue of the adenomaescapes from the sella turcica and compresses thethird nerve against the dura mater near its en-trance into the cavernous sinus (Symonds, 1962).According to Symonds, this tongue of theadenoma may become strangulated and produceinfarction, thus resulting in a sudden third nervepalsy or total ophthalmoplegia and hypo-pituitarism. Both patients, therefore, representforms of oculomotor neuropathy, one manifesta-tion of which was passive proptosis.The four rectus muscles normally exert a re-

traction effect on the globe. Their long coursesfrom the posterior pole of the orbit mediate aforce directed backward that is normallycountered by the anterior displacement effect ofthe oblique muscles. In oculomotor nerve lesions,three of the four recti may be involved to produceup to 3 to 4 mm of proptosis (Walsh, 1957). Thiseffect is presumably a combination of the loss ofthe normal retraction effect of the three recti andthe active anterior and inferior displacing effectof the superior oblique. Similarly, in the neuro-muscular paresis of myasthenia gravis, ocularproptosis may occur (Walsh and Hoyt, 1969a)which has been observed to disappear after neo-stigmine administration (Hatch, 1952). In thislatter instance, the degree of proptosis and theaxis of deviation will depend on the profile ofindividual musculature impaired by the defectiveneuromuscular transmission.The separation of disorders that produce prop-

tosis secondarily, from those groups of diseases thatproduce proptosis actively (anteriorly directedvector of force) is usually not difficult. By noting itsfrequent occurrence with oculomotor neuropathy,a puzzling finding may be explained and, whenthere is no other contrary evidence, may sparethe patient unnecessary diagnostic tests ordiagnostic exploration. However, the occurrenceof proptosis in a diabetic, for example, stillnecessitates a search for an active process suchas cavernous sinus thrombosis. The separation ofprocesses is made easier by the presence orabsence of certain clinical signs. In these twopatients, normal retropulsion and the absence ofeye tenderness, chemosis, dilated episcleral veins,pulsations, and bruits all indicated the absenceof a force generating lesion. The forced ductiontest (FDT) determined that the disturbance inocular motility was not due to a mechanical

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obstacle (Von Noorden and Maumenee, 1967). Inthyroid eye disease, for example, the FDT canestablish that the limitation of upgaze is due toa restricted inferior rectus and thus correlate withthe proptosis, and other physical signs of thyroideye disease. Similarly, limitation of the FDT willbe seen in processes involving the muscle conenear the superior orbital fissure, whereas oculo-motor neuropathies and myasthenia gravis areassociated with a normal FDT since there is noimpedence to muscle motion.

Computerised axial tomography (CT scanning)is now felt to be the diagnostic procedure ofchoice in evaluating exophthalmos. Particularlywith the use of contrast enhancing infusions, andthe capability of thin tomographic sections, anaccurate definition of the orbits and its contentscan be obtained (Lampert et al., 1974). Separationof the images produced by the inferior rectusmuscle and the optic nerve can now be mademore clearly with these refinements in CT scan-ning, and the difficulty in differentiating opticnerve tumours from thyroid eye disease is be-coming less common. Periorbital tumours such asa lacrimal gland tumour, and retro-orbitaltumours, such as sphenoid wing meningiomas, arealso easily detected by CT scanning. In the secondpatient, the normal CT scan, along with otherdata, corroborates the clinical impression ofpassive proptosis after oculomotor nerve in-farction.

In summary, not all protrusions of the globeare due to expansile disease within or near theorbit. Proptosis may occur passively and mayindicate a disease process far different from thoseusually considered in the differential diagnosis ofexophthalmos. Myasthenia gravis and oculomotornerve lesions are the most likely causes of thispassive proptosis.

The cooperation of Dr Joachim F. Seeger of theDepartment of Radiology, University of MichiganMedical Center, is gratefully noted. I am apprecia-

Brian P. O'Neill

tive of the photographic assistance of Robert J.McKnight, Chief, Medical Media Production Ser-vice, Ann Arbor Veterans AdministrationHospital. Dr Russell N. DeJong, ChairmanEmeritus, Department of Neurology, Universityof Michigan Medical Center, kindly read themanuscript and offered constructive comments.

References

Dreyfus, P. M., Hakim, S., and Adams, R. D. (1957).Diabetic ophthalmoplegia. Report of a ca.e, withpost-mortem study and comments on vascularsupply of human oculomotor nerve. Archives ofNeurology and Psychiatry (Chicago), 77, 337-349.

Hatch, H. A. (1952). Myasthenia gravis: Report of acase without hyperthyroidism relieved by neostig-mine. New England Journal of Medicine, 246, 856-858.

Hunder, G. G., Disney, T. F., and Ward, L. E. (1969).Polymyalgia rheumatica. Mayo Clinic Proceedings,44, 849-875.

Kasoff, I., and Kelly, D. L. (1975). Pupillary sparingin oculomotor palsy from internal carotid aneurysm.Journal of Neurosurgery, 42, 713-717.

Lampert, V. L., Felch, J. V., and Cohen, D. N. (1974).Computed tomography of the orbits. Radiology,113, 351-354.

Meadows, S. P. (1966). Temporal or giant cellarteritis. Proceedings of the Royal Society ofMedicine, 59, 329-333.

Symonds, C. P. (1962). Ocular palsy as the presentingsymptom of pituitary adenoma. Bulletin of theJohns Hopkins Hospital, 82, 72-82.

Von Noorden, G. K., and Maumenee, A. E. (1967).Atlas of Strabismus. C. V. Mosby: St Louis.

Walsh, F. B. (1957). Clinical Neuro-ophthalmology.Second edition, p. 221. Williams and Wilkins Co:Baltimore.

Walsh, F. B., and Hoyt, W. F. (1969a). ClinicalNeuro-ophthalmology. Third edition, p. 1284.Williams and Wilkins Co: Baltimore.

Walsh, F. B., and Hoyt, W. F. (1969b). Clinical Neuro-ophthalmology. Third edition, p. 1884. Williams andWilkins Co: Baltimore.

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