Documenta Ophthalmologica 81: 197-208, 1992. (~) 1992 Kluwer Academic Publishers. Printed in the Netherlands.
Visual evoked potentials during the early phase of optic nerve compression in the orbital cavity MARTA JANAKY 1 & GYORGY BENEDEK 2 1Department of Ophthalmology and 2Department of Physiology, Albert Szent-Gy6rgyi Medical School, 6720, D6m tOr 10, Szeged, Hungary Accepted 24 January1992 Key words: Optic nerve, orbital cavity, vision, visual evoked potentials Abstract. We obtained case histories and electrophysiologicrecordings from four patients with transient vision impairment due to acute orbital compression. The visual evoked potentials (VEPs) displayed alterations that depended on the size and consistency of the compressing pathology and also on the duration of the compression. This study provides evidence of the utility of the VEP in the assessment of the severity and reversibility of optic nerve lesions. The case histories also emphasized the necessity to elucidate the pathologic process of compressive lesions of the optic nerve.
Introduction
The early diagnosis of chronic, slowly progressing intraorbital space-occupying processes is u n c o m m o n . Minor ptosis, proptosis, and other visual disturbances in the initial stages may not be detected by an ophthalmologist. Only the presence of steady visual impairment, exophthalmos, or diplopia yields a firm but late diagnosis; thus, treatment can only preserve residual optic nerve function. Several articles have recently been published on monitoring optic nerve function during surgery [1-5] or on optic nerve compression due to elevated intraocular pressure [6-9]. However, only a few reports have been published on optic nerve damage caused by acute compression in the orbital cavity [10-12]. The present report summarizes the case histories and electrophysiologic data on four patients with acute intraorbital optic nerve compression of various causes. The study provides evidence of the utility of the visual evoked potential ( V E P ) in the assessment of the severity and reversibility of optic nerve diseases.
Patients and m e t h o d s
All four patients underwent a battery of tests, including assessment of visual acuity, slit-lamp examination, ophthalmoscopy, perimetry, contrast sensitivi-
198 ty and color vision testing. Intraorbital space-occupying processes were localized with the help of an ultrasound scanner (Ultrascan Digital B/ System IV, 10 MHz) or by computed tomography. The VEPs were elicited by the reversal of a 20' or 40' checkerboard black-and-white high-contrast pattern on a 6~ • 8~ TV monitor. The stimulation frequency was 1.8 Hz. The VEPs were recorded via an electrode placed in the midline of the skull 2.5 cm above the inion, which was referred to a reference electrode clipped to the right earlobe. A ground electrode was placed on the forehead. The impedance of the electrodes was kept below 5 k i t The bandpass of the system was between 0.3 and 70 Hz. One hundred responses were averaged. Each eye was tested separately. VEPs were evaluated according to the latency and amplitude of the P100 component. Responses were regarded as pathologic when the N70-P100 amplitude was 50% of that of the contralateral eye or 50% of the original (precompression) value. Latency values were regarded as pathologic when lengthened beyond 120 ms.
Case reports Case 1. A 20-year-old man complained of a gradual impairment of vision in his right eye whenever he turned his gaze to the right and downward. The visual problem disappeared as soon as he looked forward again. The visual acuity in the primary position of gaze was 1.0 OU. The right upper eyelid was positioned slightly lower than the left, although this difference was so mild that the patient had been unaware of it (the interlid distance was 9 mm on the right eye and 11 mm on the left). The Hertel exophthalmometry value (the distance between the apex of the cornea and the lateral orbital rim) was 15 mm on the right side and 14 mm on the left side; the base value (the distance between the lateral rims of the two orbita) was 106 ram. No alterations were detected by slit-lamp examination or funduscopy. Visual fields, contrast sensitivity and color vision, which was tested with an anomaloscope (Nagel), were normal. Symptoms of diplopia were not detected. The Lancaster test indicated impaired function of the medial and superior rectus muscles and of the superior oblique muscle on the right side. Based on the mild ptosis, proptosis, and insufficient function of the extraocular muscles, an intraorbital space-occupying process was suspected. Computed tomography showed a slightly hyperdense area of 2 x 3 cm in the fight orbital cavity behind the bulbus, close to the upper medial wall (Fig. lb). The hyperdense area had a calcificated core. When the patient looked to the right and downward, the hyperdense area moved left and exerted an archlike bend on the optic nerve (Fig. lc). No fixed contact could be detected between the hyperdense alteration and the optic nerve. The bony
199
(a)
OD
OS
;1
lOOmser
(b)
(c)
Fig. 1. Patient/Case 1 (M, 20 years). (a) VEPs recorded when the patient was looking straight ahead (top), then to the right (middle), and straight ahead again (bottom). Left tracings: right eye stimulated; right tracings: left eye stimulated. Calibration: lOOms, 1 ixV; (b) computed tomography taken when the patient was looking straight ahead; (c) computed tomography taken when the patient was looking to the right and downward.
200 wall of the orbital cavity was thinned in the upper part. No intracranial alteration was detected. The patient underwent surgery to remove the tumor (believed to be a sclerotizing granuloma or fibroma). His visual acuity was 1 . 0 0 U at the time of admission. The ptosis of the right eye had slightly progressed (interlid distance was 7 mm at discharge). The patient did not return for follow-up. Case 2. A 4.5-year-old boy had influenza and was brought to our outpatient department because of conjunctivitis with chemosis in the left eye. Two days later a dislocation of the left ocular bulb was detected, and he was admitted to our children's department because of the suspicion of orbital invasion by a purulent sinusoidal process. The visual acuity of the left eye was 1.0. The left bulb was dislocated upward and medially. The Hertel exophthalmometry value was 10 mm on the right side and 14ram on the left side (base value, 82mm). Eye movements were limited downward and laterally. Diplopia could not be tested because of the patient's lack of cooperation. No visual defects were found on confrontational testing. A slit-lamp examination showed no pathologic alterations. The ophthalmoscopic examination found fine horizontal folds in the lower temporal part of the fundus. No pathologic alterations were found on ophthalmologic examination of the right eye. Ultrasound scanning showed a mass of sharp borders 15 to 17 mm in diameter in the lower temporal part of the orbital cavity. It bulged into the bulb, reaching the optic nerve and compressing it considerably when the patient looked medially (Fig. 2b and 2c). Because of the rapidly progressing exophthalmos, an emergency orbitomy was performed. After penetration of the orbital cavity at its temporalinferior aspect, the tumor was removed together with its capsule. Histologic findings showed that the mass was a rhabdomyosarcoma. Postoperatively, visual acuity was 1.0OS and the exophthalmos disappeared. The Hertel exophthalmometry value was 10 mm on both sides (base value, 82 ram). The patient was devoid of any signs of a recurrence 2 years after surgery. Case 3. A 61-year-old man had been undergoing intermittent cytostatic treatment in the hematologic ward of our university for the last 4 yeas because of multiple myeloma. He was referred for an ophthalmologic examination because of diplopia and the appearance of exophthalmos. The visual acuity was 1.0OU. Slit-lamp examination showed no pathologic alterations. Ophthalmoscopic examination of the left eye revealed fine retinal folds and scattered microaneurysms in the upper temporal segment of the retina. Contrast sensitivity and color vision were normal. The lower nasal quadrant of the visual field of the left eye was constricted. The Hertel exophthalmometry value was 11 mm on the right side and 15 mm on the left (base value, 105 ram). The movements of the left ocular bulb
201 (a)
0609 89
29 II 89
I00 m S e c
(b)
(c)
Fig. 2. Patient/Case 2 (M, 4.5 years). (a) VEPs recorded after stimulation of the left eye when the patient was looking straight ahead (top left), to the fight (middle left), and straight ahead again (bottom left). On the fight side of the figure the same type of recordings made after the operation are displayed. Calibration: 100 ms, 1 p,V; (b) ultrasound scan while the patient was looking ahead; (c) ultrasound scan while the patient was looking medially.
202 (a)
OD
OS
I00 mSec
(b)
(c)
Fig. 3. Patier~t/Case 3 (M, 61 years). (a) VEPs recorded when the patient was looking straight ahead (top), to the right (middle), and straight ahead again (bottom). Left tracings: right eye stimulated; right tracings: left eye stimulated. Calibration: 100 ms, 1 IxV; (b) ultrasound scan when the patient was looking ahead; (c) ultrasound scan when the patient was looking medially.
203 were limited upward. The patient's sight was blurred when he looked to the right. The Lancaster test showed an improved function of the superior rectus muscle on the left side. Ultrasound scanning demonstrated a mass 30 m m in diameter with sharp lateral borders lateral to and above the optic
(a) 11.13.89.
1220.89.
3 3
11. 100 m s e c
(b)
(c)
Fig. 4. Patient/Case 4 (F, 25 years). (a) VEPs recorded on stimulating the left eye during the 1-year observation period. Time of recording is shown below each curve; (b) ultrasound scan of the dural diameter of the left optic nerve at admission; (c) ultrasound scan of the dural diameter of the left eye 2 days after admission.
204 nerve (Fig. 3b). It bulged into the optic bulb and compressed the optic nerve when the patient was looking to the right (Fig. 3c). Cytostatic t r e a t m e n t alleviated the exophthalmos rapidly. The visual acuity r e m a i n e d 1.0. The Hertel e x o p h t h a l m o m e t r y value on the left side decreased to 13 m m in 1 month. The patient died of renal insufficiency after 4 months. The autopsy revealed a p l a s m a c y t o m a in the orbital cavity. Case 4. A 24-year-old w o m a n suffered an accidental contusive t r a u m a to her left eye. H e r sight was blurred overnight, and even her light perception was affected. She was referred to our d e p a r t m e n t 5 days later for evaluation of a suspected functional disturbance in the absence of any intraocular alterations. Ophthalmologic examination showed that the visual acuity of the left eye was greatly impaired. Only vision of finger counting from a distance of 1 m was retained. Eye m o v e m e n t s were not limited. Visual field and color vision tests gave no objective data because of the greatly impaired visual acuity. U l t r a s o u n d scanning demonstrated a thickened optic nerve shadow on the left side. The dural diameter according to Schroeder [8] of the right and left optic nerves was 4.3 m m and 5.1 m m , respectively (Fig. 4b and 4c). T w o days later the diameter of the left optic nerve decreased to 4.4 m m , and the patient's vision improved to 0.1. In 10 days the visual field was Table 1. Clinical data of patients with intraorbital compression
Patient/Case
Eye Signsand symptoms
Sex/Age (years)
Vision Hertel exophthalmometry (mm) OD
OS Base
Fundus
1. M/20
OD
Blurred vision when looking to the right and downward
1.0
15
14
106
2. M/4.5
OS
Progressiveproptosis for 2 days; blurred vision when looking medially
1.0
10
14
82
3. M/61
OS
Progressivediplopia for 2 days; exophthalmos for 2 weeks
1.0
11
15
105
Normal optic disc; hypertonic blood vessels; retinal folds; microaneurysms
4. F/25
OS
Loss of vision for 5 days because of bulbar contusion
0.01
11
I1
104
Normal
M = male; F = female.
Normal
Normal optic disc; fine, horizontal folds
205 Table 2. Latency (lat, msec) and amplitude (ampl, txV) values of VEPs in patients with intraorbital compression
Patient/Case 1 Lat
Patient/Case 2 Ampl
Lat
Ampl
Exp.
OD
OS
OD
OS
Exp.
OD
OS
OD
OS
(1) (2) (3)
107 114 110
107 110 108
4.14 1.42 4.14
4.71 4.14 4.28
(1) (2) (3)
107 110 110
128 151 130
4.71 4.57 4.57
4.00 2.57 4.14
Patient/Case 3 Lat
Patient/Case 4 Ampl
Lat
Ampl
Exp.
OD
OS
OD
OS
Exp.
OD
OS
OD
OS
(1) (2) (3)
114 107 107
128 150 128
4.28 4.00 4.58
2.57 1.57 2.85
(4) (5) (6)
114 110 107
nr 150 107
4.00 4.14 4.00
nr 1.14 4.14
Explanation: (1) Primary gaze. (2) Looking toward challenge direction. (3) Return to primary gaze. (4) At admission. (5) Two months after admission. (6) One year after admission. nr = nonrecordable. n o r m a l . I n 21 days the color vision had r e c o v e r e d to almost n o r m a l (objects still a p p e a r e d d a r k e r with the left eye). T h e contrast sensitivity r e m a i n e d i m p a i r e d for a longer time. T h e patient was free of s y m p t o m s in 3 m o n t h s . T h e clinical data on the four patients are given in Tables 1 and 2.
VEP results Case 1. A n o r m a l V E P was o b t a i n e d w h e n the patient fixated the center of the p a t t e r n screen. W h e n he positioned his h e a d to the left and backwards while looking at the T V m o n i t o r , turning his eyes d o w n w a r d s and to the right, the amplitude of the P100 c o m p o n e n t of the V E P abruptly decreased by half. N o appreciable latency difference was seen (1.07 m m w h e n looking a h e a d , a n d 114 ms w h e n looking d o w n w a r d s and to the left). O n repositioning o f the gaze, the n o r m a l V E P r e c o v e r e d immediately. A n identical 'mirror-like' p r o c e d u r e with the left eye failed to elicit similar changes in the V E P . T h e p h e n o m e n o n was easy to repeat (Fig. la). Case 2. Stimulation of the right eye e v o k e d n o r m a l V E P s . Stimulation of the left eye elicited a V E P with decreased amplitude and slightly increased
206 latency. We were able to elicit a compression of the optic nerve by making the patient look in the appropriate direction (to the right). This promptly decreased the amplitude and increased the latency (from 128 ms to 151 ms) of the P100 component. A similar procedure had no effect on the VEP of the right eye. Postoperative VEPs were normal on both eyes (Fig. 2a). Case 3. Pattern-reversal stimulation of the left eye elicited an evoked response with decreased amplitude and increased latency (128 ms). Increasing the compression of the optic nerve on voluntary fixation considerably decreased the amplitude of the VEP (Fig. 3a). The latency was increased to 150 ms. A similar procedure on the other eye had no effect on the VEP. Cytostatic treatment of the patient's multiple myeloma reduced the amplitude and latency differences between the two eyes. Case 4. During the first examination, stimulation of the right eye elicited normal VEPs, while no evoked response could be obtained on stimulation of the left eye. VEPs recorded 2 months later still showed greatly decreased P100 amplitude and increased latency values (150 ms) on stimulation of the left eye. The diminished amplitude values recovered in 4 months (the latency at that time was 128 ms). Normal VEPs were recorded 1 year after the trauma (Fig. 4a).
Discussion
VEP changes on compression of the intraorbital part of the optic nerve were first described by Halliday and coworkers [10, 11]. They found both a decreased amplitude and an increased latency of VEPs elicited by patternreversal stimulation. The alterations in the optic nerve function and consequently in the VEPs on intraorbital compression are of particular interest because of the appearance of visual field defects and optic nerve changes during glaucoma, and additionally because of the recent necessity to monitor optic nerve function during orbital surgical interventions. Accordingly, several animal models have been used to study both the pathologic processes underlying the functional and anatomical damage during acute and chronic optic nerve compression and the ensuing recovery. The relationship between orbital optic nerve compression and VEP alteration has been discussed in the literature [10, 13]. It seems that the decreased amplitude and increased latency in the VEP on intraorbital compression are based on separate pathologic mechanisms. Studies on experimental animals have yielded various explanations concerning the pathologic processes, including a mechanical [6, 8, 14] and a vascular [9, 15] theory. No analytical or follow-up study has appeared, however, on the effects of an elevated intraorbital pressure on optic nerve function and VEPs in
207 humans. Our study seems to provide evidence to the existence of several factors acting relatively separately on the VEP changes in patients with intraorbital diseases. The observations suggest that the relationship between VEP alterations and orbital compressions is influenced both by the intensity of the pressure and by its duration. In our Case 1 the optic nerve was compressed by an abruptly acting powerful effect. It elicited a prompt, separate decrease in the amplitude of the VEP. The recording of the VEP took approximately 3 minutes in our studies. This time was enough to induce considerable alterations in the evoked response, without any persisting damage. The recovery of the VEP amplitude after elimination of the compression was complete. The reversibility of this type of effect is in line with the data of Siliprandi et al. on cats (14). He found that an elevation of the intraocular pressure shorter than 5 minutes is not followed by irreversible impairment. It seems that an acute blockage of the blood supply is involved, which terminates both the vision and the bioelectric response over the visual cortex. The compression was mild but persistent in our Case 2, although the patient was able to increase the strength of the compression by looking in a particular direction. This again elicited an immediate visual disturbance and VEP changes characterized by both a decrease in the amplitude and an increased latency. Although the visual impairment and the VEP alterations seemed to be completely reversible, we may presume the interplay of several pathomechanical components in the background of these changes. Both a reduced blood supply and a decreased axoplasmic flow or some metabolic disturbance could play a role in this type of VEP alteration. Although the malignant tumor in our Case 3 progressed slowly into the orbital space and did not directly compress the optic nerve, both the latency and the amplitude of the VEP were pathologic. When the patient looked in the appropriate direction, the tumor immediately compressed the optic nerve, which exaggerated the VEP alterations. Cytostatic treatment was accompanied by a reduction of the compression and recovery of the function. This included complete normalization of the VEP. Of the four cases presented here, Case 4 had the most severe functional damage. The reduction of the VEP and the total loss of visual acuity could be caused by edema along the entire (or almost the entire) length of the optic nerve. It is interesting, however, that, although the dural diameter of the optic nerve and the visual acuity improved in a few days, the VEP remained abnormal for a considerable time. This observation seems to contradict the notion of an overlapping effect of pathologic processes on VEP and vision. However, the complete reversibility of the electrophysiological changes suggests that the impairment of VEP and vision in the early phase of optic nerve compression cannot be a consequence of degenerative processes (demyelinization). We must note, however, that some latency reduction during the course of an optic neuritis cannot be excluded either [7].
2O8 This study provides evidence on the utility of the VEP in the assessment of the severity and reversibility of optic nerve diseases.
References 1. Costa E Silva I, Wang A, Symon L. The application of flash evoked potentials during operations on anterior visual pathway. Neurol Res 1985; 7: 11-16. 2. Czedzich G, Schramm J, Mangedoth CF, Fahlbusch R. Factors that limit the use of flash visual evoked potentials for surgical monitoring. Electroencephalogr Clin Neurophysiol 1988; 71: 142-145. 3. Harding GFA, Smith UH, Yorke HC. Visual evoked potential monitoring of orbital surgery using a contact lens stimulator. In: Barber C, Blum T, eds. Evoked potentials. Boston: Butterworth, 1988: 240-244. 4. Harding GFA, Bland JD, Smith UH. Visual evoked potential monitoring of optic nerve function during surgery. J Neurol Neurosurg Psychiatry 1990; 53: 890-895. 5. Wright JE, Arden G, Jones BR. Continuous monitoring of the visual evoked response during intraorbital surgery. Trans Ophthalmol Soc UK 1973; 93: 311-314. 6. Gaasterland D, Tanishima T, Kuwabara T. Axoplasmic flow during chronic experimental glaucoma. Invest Ophthalmol Vis Sci 1978; 17: 838-846. 7. Harding GFA, Wright CE. Visual evoked potentials in acute optic neuritis. In: Hess RF, Plant GT, eds. Optic Neuritis. New York: Cambridge University Press, 1986: 230-254. 8. Quigley HA, Addicks EM. Chronic experimental glaucoma in primates, II: Effect of extended intraocular pressure elevation on optic nerve head and axonal transport. Invest Ophthalmol Visual Sci 1980; 19: 137-152. 9. Siliprandi R, Bucci MG, Canella R, Camignoto G. Flash and pattern electroretinograms during and after acute intraocular pressure elevation in cats. Invest Ophthalmol Vis Sci 1988; 29: 558-565. 10. Halliday AM, Halliday E, Kriss A, McDonald WI, Mushin J. The pattern-evoked potential in compression of the anterior visual pathways. Brain 1976; 99: 357-374. 11. Halliday AM, Halliday E, Kriss A, McDonald WI, Mushin J. Changes in the pattern evoked response in compressive lesions of the anterior visual pathways. Electroencephalogr Clin Neurophysiol 1976; 40: 541. 12. Simpson DE, Moser LA. Compressive optic neuropathy secondary to chronic sinusitis. Am J Optom Physiol Opt 1988; 65: 757-762. 13. McDonald WI. Pathophysiology of conduction in central nerve fibres. In: Desmedt JF, ed. New developments in visual evoked potentials in the human brain. London: Oxford University Press. 1976: 427-437. 14. Minckler DS, Bunt A, Kloc IB. Radioautographic and cytochemical ultrastrnctural studies of axoplasmic transport in the monkey optic nerve head. Invest Ophthalmol Vis Sci 1978; 17: 33-50. 15. Hayreh SS, Revie IHS, Edwards J. Vasogenic origin of visual field defects and optic nerve changes in glaucoma. Br J Ophthalmol 1970; 54: 461-472.
Address for correspondence: Prof. Gyrrgy Benedek, Department of Physiology, D6m t6r 10, H-6720 Szeged, Hungary. Tel: 36/62/12049; Fax: 36/62/12529.
Visual evoked potentials during the early phase of optic nerve compression in the orbital cavity MARTA JANAKY 1 & GYORGY BENEDEK 2 1Department of Ophthalmology and 2Department of Physiology, Albert Szent-Gy6rgyi Medical School, 6720, D6m tOr 10, Szeged, Hungary Accepted 24 January1992 Key words: Optic nerve, orbital cavity, vision, visual evoked potentials Abstract. We obtained case histories and electrophysiologicrecordings from four patients with transient vision impairment due to acute orbital compression. The visual evoked potentials (VEPs) displayed alterations that depended on the size and consistency of the compressing pathology and also on the duration of the compression. This study provides evidence of the utility of the VEP in the assessment of the severity and reversibility of optic nerve lesions. The case histories also emphasized the necessity to elucidate the pathologic process of compressive lesions of the optic nerve.
Introduction
The early diagnosis of chronic, slowly progressing intraorbital space-occupying processes is u n c o m m o n . Minor ptosis, proptosis, and other visual disturbances in the initial stages may not be detected by an ophthalmologist. Only the presence of steady visual impairment, exophthalmos, or diplopia yields a firm but late diagnosis; thus, treatment can only preserve residual optic nerve function. Several articles have recently been published on monitoring optic nerve function during surgery [1-5] or on optic nerve compression due to elevated intraocular pressure [6-9]. However, only a few reports have been published on optic nerve damage caused by acute compression in the orbital cavity [10-12]. The present report summarizes the case histories and electrophysiologic data on four patients with acute intraorbital optic nerve compression of various causes. The study provides evidence of the utility of the visual evoked potential ( V E P ) in the assessment of the severity and reversibility of optic nerve diseases.
Patients and m e t h o d s
All four patients underwent a battery of tests, including assessment of visual acuity, slit-lamp examination, ophthalmoscopy, perimetry, contrast sensitivi-
198 ty and color vision testing. Intraorbital space-occupying processes were localized with the help of an ultrasound scanner (Ultrascan Digital B/ System IV, 10 MHz) or by computed tomography. The VEPs were elicited by the reversal of a 20' or 40' checkerboard black-and-white high-contrast pattern on a 6~ • 8~ TV monitor. The stimulation frequency was 1.8 Hz. The VEPs were recorded via an electrode placed in the midline of the skull 2.5 cm above the inion, which was referred to a reference electrode clipped to the right earlobe. A ground electrode was placed on the forehead. The impedance of the electrodes was kept below 5 k i t The bandpass of the system was between 0.3 and 70 Hz. One hundred responses were averaged. Each eye was tested separately. VEPs were evaluated according to the latency and amplitude of the P100 component. Responses were regarded as pathologic when the N70-P100 amplitude was 50% of that of the contralateral eye or 50% of the original (precompression) value. Latency values were regarded as pathologic when lengthened beyond 120 ms.
Case reports Case 1. A 20-year-old man complained of a gradual impairment of vision in his right eye whenever he turned his gaze to the right and downward. The visual problem disappeared as soon as he looked forward again. The visual acuity in the primary position of gaze was 1.0 OU. The right upper eyelid was positioned slightly lower than the left, although this difference was so mild that the patient had been unaware of it (the interlid distance was 9 mm on the right eye and 11 mm on the left). The Hertel exophthalmometry value (the distance between the apex of the cornea and the lateral orbital rim) was 15 mm on the right side and 14 mm on the left side; the base value (the distance between the lateral rims of the two orbita) was 106 ram. No alterations were detected by slit-lamp examination or funduscopy. Visual fields, contrast sensitivity and color vision, which was tested with an anomaloscope (Nagel), were normal. Symptoms of diplopia were not detected. The Lancaster test indicated impaired function of the medial and superior rectus muscles and of the superior oblique muscle on the right side. Based on the mild ptosis, proptosis, and insufficient function of the extraocular muscles, an intraorbital space-occupying process was suspected. Computed tomography showed a slightly hyperdense area of 2 x 3 cm in the fight orbital cavity behind the bulbus, close to the upper medial wall (Fig. lb). The hyperdense area had a calcificated core. When the patient looked to the right and downward, the hyperdense area moved left and exerted an archlike bend on the optic nerve (Fig. lc). No fixed contact could be detected between the hyperdense alteration and the optic nerve. The bony
199
(a)
OD
OS
;1
lOOmser
(b)
(c)
Fig. 1. Patient/Case 1 (M, 20 years). (a) VEPs recorded when the patient was looking straight ahead (top), then to the right (middle), and straight ahead again (bottom). Left tracings: right eye stimulated; right tracings: left eye stimulated. Calibration: lOOms, 1 ixV; (b) computed tomography taken when the patient was looking straight ahead; (c) computed tomography taken when the patient was looking to the right and downward.
200 wall of the orbital cavity was thinned in the upper part. No intracranial alteration was detected. The patient underwent surgery to remove the tumor (believed to be a sclerotizing granuloma or fibroma). His visual acuity was 1 . 0 0 U at the time of admission. The ptosis of the right eye had slightly progressed (interlid distance was 7 mm at discharge). The patient did not return for follow-up. Case 2. A 4.5-year-old boy had influenza and was brought to our outpatient department because of conjunctivitis with chemosis in the left eye. Two days later a dislocation of the left ocular bulb was detected, and he was admitted to our children's department because of the suspicion of orbital invasion by a purulent sinusoidal process. The visual acuity of the left eye was 1.0. The left bulb was dislocated upward and medially. The Hertel exophthalmometry value was 10 mm on the right side and 14ram on the left side (base value, 82mm). Eye movements were limited downward and laterally. Diplopia could not be tested because of the patient's lack of cooperation. No visual defects were found on confrontational testing. A slit-lamp examination showed no pathologic alterations. The ophthalmoscopic examination found fine horizontal folds in the lower temporal part of the fundus. No pathologic alterations were found on ophthalmologic examination of the right eye. Ultrasound scanning showed a mass of sharp borders 15 to 17 mm in diameter in the lower temporal part of the orbital cavity. It bulged into the bulb, reaching the optic nerve and compressing it considerably when the patient looked medially (Fig. 2b and 2c). Because of the rapidly progressing exophthalmos, an emergency orbitomy was performed. After penetration of the orbital cavity at its temporalinferior aspect, the tumor was removed together with its capsule. Histologic findings showed that the mass was a rhabdomyosarcoma. Postoperatively, visual acuity was 1.0OS and the exophthalmos disappeared. The Hertel exophthalmometry value was 10 mm on both sides (base value, 82 ram). The patient was devoid of any signs of a recurrence 2 years after surgery. Case 3. A 61-year-old man had been undergoing intermittent cytostatic treatment in the hematologic ward of our university for the last 4 yeas because of multiple myeloma. He was referred for an ophthalmologic examination because of diplopia and the appearance of exophthalmos. The visual acuity was 1.0OU. Slit-lamp examination showed no pathologic alterations. Ophthalmoscopic examination of the left eye revealed fine retinal folds and scattered microaneurysms in the upper temporal segment of the retina. Contrast sensitivity and color vision were normal. The lower nasal quadrant of the visual field of the left eye was constricted. The Hertel exophthalmometry value was 11 mm on the right side and 15 mm on the left (base value, 105 ram). The movements of the left ocular bulb
201 (a)
0609 89
29 II 89
I00 m S e c
(b)
(c)
Fig. 2. Patient/Case 2 (M, 4.5 years). (a) VEPs recorded after stimulation of the left eye when the patient was looking straight ahead (top left), to the fight (middle left), and straight ahead again (bottom left). On the fight side of the figure the same type of recordings made after the operation are displayed. Calibration: 100 ms, 1 p,V; (b) ultrasound scan while the patient was looking ahead; (c) ultrasound scan while the patient was looking medially.
202 (a)
OD
OS
I00 mSec
(b)
(c)
Fig. 3. Patier~t/Case 3 (M, 61 years). (a) VEPs recorded when the patient was looking straight ahead (top), to the right (middle), and straight ahead again (bottom). Left tracings: right eye stimulated; right tracings: left eye stimulated. Calibration: 100 ms, 1 IxV; (b) ultrasound scan when the patient was looking ahead; (c) ultrasound scan when the patient was looking medially.
203 were limited upward. The patient's sight was blurred when he looked to the right. The Lancaster test showed an improved function of the superior rectus muscle on the left side. Ultrasound scanning demonstrated a mass 30 m m in diameter with sharp lateral borders lateral to and above the optic
(a) 11.13.89.
1220.89.
3 3
11. 100 m s e c
(b)
(c)
Fig. 4. Patient/Case 4 (F, 25 years). (a) VEPs recorded on stimulating the left eye during the 1-year observation period. Time of recording is shown below each curve; (b) ultrasound scan of the dural diameter of the left optic nerve at admission; (c) ultrasound scan of the dural diameter of the left eye 2 days after admission.
204 nerve (Fig. 3b). It bulged into the optic bulb and compressed the optic nerve when the patient was looking to the right (Fig. 3c). Cytostatic t r e a t m e n t alleviated the exophthalmos rapidly. The visual acuity r e m a i n e d 1.0. The Hertel e x o p h t h a l m o m e t r y value on the left side decreased to 13 m m in 1 month. The patient died of renal insufficiency after 4 months. The autopsy revealed a p l a s m a c y t o m a in the orbital cavity. Case 4. A 24-year-old w o m a n suffered an accidental contusive t r a u m a to her left eye. H e r sight was blurred overnight, and even her light perception was affected. She was referred to our d e p a r t m e n t 5 days later for evaluation of a suspected functional disturbance in the absence of any intraocular alterations. Ophthalmologic examination showed that the visual acuity of the left eye was greatly impaired. Only vision of finger counting from a distance of 1 m was retained. Eye m o v e m e n t s were not limited. Visual field and color vision tests gave no objective data because of the greatly impaired visual acuity. U l t r a s o u n d scanning demonstrated a thickened optic nerve shadow on the left side. The dural diameter according to Schroeder [8] of the right and left optic nerves was 4.3 m m and 5.1 m m , respectively (Fig. 4b and 4c). T w o days later the diameter of the left optic nerve decreased to 4.4 m m , and the patient's vision improved to 0.1. In 10 days the visual field was Table 1. Clinical data of patients with intraorbital compression
Patient/Case
Eye Signsand symptoms
Sex/Age (years)
Vision Hertel exophthalmometry (mm) OD
OS Base
Fundus
1. M/20
OD
Blurred vision when looking to the right and downward
1.0
15
14
106
2. M/4.5
OS
Progressiveproptosis for 2 days; blurred vision when looking medially
1.0
10
14
82
3. M/61
OS
Progressivediplopia for 2 days; exophthalmos for 2 weeks
1.0
11
15
105
Normal optic disc; hypertonic blood vessels; retinal folds; microaneurysms
4. F/25
OS
Loss of vision for 5 days because of bulbar contusion
0.01
11
I1
104
Normal
M = male; F = female.
Normal
Normal optic disc; fine, horizontal folds
205 Table 2. Latency (lat, msec) and amplitude (ampl, txV) values of VEPs in patients with intraorbital compression
Patient/Case 1 Lat
Patient/Case 2 Ampl
Lat
Ampl
Exp.
OD
OS
OD
OS
Exp.
OD
OS
OD
OS
(1) (2) (3)
107 114 110
107 110 108
4.14 1.42 4.14
4.71 4.14 4.28
(1) (2) (3)
107 110 110
128 151 130
4.71 4.57 4.57
4.00 2.57 4.14
Patient/Case 3 Lat
Patient/Case 4 Ampl
Lat
Ampl
Exp.
OD
OS
OD
OS
Exp.
OD
OS
OD
OS
(1) (2) (3)
114 107 107
128 150 128
4.28 4.00 4.58
2.57 1.57 2.85
(4) (5) (6)
114 110 107
nr 150 107
4.00 4.14 4.00
nr 1.14 4.14
Explanation: (1) Primary gaze. (2) Looking toward challenge direction. (3) Return to primary gaze. (4) At admission. (5) Two months after admission. (6) One year after admission. nr = nonrecordable. n o r m a l . I n 21 days the color vision had r e c o v e r e d to almost n o r m a l (objects still a p p e a r e d d a r k e r with the left eye). T h e contrast sensitivity r e m a i n e d i m p a i r e d for a longer time. T h e patient was free of s y m p t o m s in 3 m o n t h s . T h e clinical data on the four patients are given in Tables 1 and 2.
VEP results Case 1. A n o r m a l V E P was o b t a i n e d w h e n the patient fixated the center of the p a t t e r n screen. W h e n he positioned his h e a d to the left and backwards while looking at the T V m o n i t o r , turning his eyes d o w n w a r d s and to the right, the amplitude of the P100 c o m p o n e n t of the V E P abruptly decreased by half. N o appreciable latency difference was seen (1.07 m m w h e n looking a h e a d , a n d 114 ms w h e n looking d o w n w a r d s and to the left). O n repositioning o f the gaze, the n o r m a l V E P r e c o v e r e d immediately. A n identical 'mirror-like' p r o c e d u r e with the left eye failed to elicit similar changes in the V E P . T h e p h e n o m e n o n was easy to repeat (Fig. la). Case 2. Stimulation of the right eye e v o k e d n o r m a l V E P s . Stimulation of the left eye elicited a V E P with decreased amplitude and slightly increased
206 latency. We were able to elicit a compression of the optic nerve by making the patient look in the appropriate direction (to the right). This promptly decreased the amplitude and increased the latency (from 128 ms to 151 ms) of the P100 component. A similar procedure had no effect on the VEP of the right eye. Postoperative VEPs were normal on both eyes (Fig. 2a). Case 3. Pattern-reversal stimulation of the left eye elicited an evoked response with decreased amplitude and increased latency (128 ms). Increasing the compression of the optic nerve on voluntary fixation considerably decreased the amplitude of the VEP (Fig. 3a). The latency was increased to 150 ms. A similar procedure on the other eye had no effect on the VEP. Cytostatic treatment of the patient's multiple myeloma reduced the amplitude and latency differences between the two eyes. Case 4. During the first examination, stimulation of the right eye elicited normal VEPs, while no evoked response could be obtained on stimulation of the left eye. VEPs recorded 2 months later still showed greatly decreased P100 amplitude and increased latency values (150 ms) on stimulation of the left eye. The diminished amplitude values recovered in 4 months (the latency at that time was 128 ms). Normal VEPs were recorded 1 year after the trauma (Fig. 4a).
Discussion
VEP changes on compression of the intraorbital part of the optic nerve were first described by Halliday and coworkers [10, 11]. They found both a decreased amplitude and an increased latency of VEPs elicited by patternreversal stimulation. The alterations in the optic nerve function and consequently in the VEPs on intraorbital compression are of particular interest because of the appearance of visual field defects and optic nerve changes during glaucoma, and additionally because of the recent necessity to monitor optic nerve function during orbital surgical interventions. Accordingly, several animal models have been used to study both the pathologic processes underlying the functional and anatomical damage during acute and chronic optic nerve compression and the ensuing recovery. The relationship between orbital optic nerve compression and VEP alteration has been discussed in the literature [10, 13]. It seems that the decreased amplitude and increased latency in the VEP on intraorbital compression are based on separate pathologic mechanisms. Studies on experimental animals have yielded various explanations concerning the pathologic processes, including a mechanical [6, 8, 14] and a vascular [9, 15] theory. No analytical or follow-up study has appeared, however, on the effects of an elevated intraorbital pressure on optic nerve function and VEPs in
207 humans. Our study seems to provide evidence to the existence of several factors acting relatively separately on the VEP changes in patients with intraorbital diseases. The observations suggest that the relationship between VEP alterations and orbital compressions is influenced both by the intensity of the pressure and by its duration. In our Case 1 the optic nerve was compressed by an abruptly acting powerful effect. It elicited a prompt, separate decrease in the amplitude of the VEP. The recording of the VEP took approximately 3 minutes in our studies. This time was enough to induce considerable alterations in the evoked response, without any persisting damage. The recovery of the VEP amplitude after elimination of the compression was complete. The reversibility of this type of effect is in line with the data of Siliprandi et al. on cats (14). He found that an elevation of the intraocular pressure shorter than 5 minutes is not followed by irreversible impairment. It seems that an acute blockage of the blood supply is involved, which terminates both the vision and the bioelectric response over the visual cortex. The compression was mild but persistent in our Case 2, although the patient was able to increase the strength of the compression by looking in a particular direction. This again elicited an immediate visual disturbance and VEP changes characterized by both a decrease in the amplitude and an increased latency. Although the visual impairment and the VEP alterations seemed to be completely reversible, we may presume the interplay of several pathomechanical components in the background of these changes. Both a reduced blood supply and a decreased axoplasmic flow or some metabolic disturbance could play a role in this type of VEP alteration. Although the malignant tumor in our Case 3 progressed slowly into the orbital space and did not directly compress the optic nerve, both the latency and the amplitude of the VEP were pathologic. When the patient looked in the appropriate direction, the tumor immediately compressed the optic nerve, which exaggerated the VEP alterations. Cytostatic treatment was accompanied by a reduction of the compression and recovery of the function. This included complete normalization of the VEP. Of the four cases presented here, Case 4 had the most severe functional damage. The reduction of the VEP and the total loss of visual acuity could be caused by edema along the entire (or almost the entire) length of the optic nerve. It is interesting, however, that, although the dural diameter of the optic nerve and the visual acuity improved in a few days, the VEP remained abnormal for a considerable time. This observation seems to contradict the notion of an overlapping effect of pathologic processes on VEP and vision. However, the complete reversibility of the electrophysiological changes suggests that the impairment of VEP and vision in the early phase of optic nerve compression cannot be a consequence of degenerative processes (demyelinization). We must note, however, that some latency reduction during the course of an optic neuritis cannot be excluded either [7].
2O8 This study provides evidence on the utility of the VEP in the assessment of the severity and reversibility of optic nerve diseases.
References 1. Costa E Silva I, Wang A, Symon L. The application of flash evoked potentials during operations on anterior visual pathway. Neurol Res 1985; 7: 11-16. 2. Czedzich G, Schramm J, Mangedoth CF, Fahlbusch R. Factors that limit the use of flash visual evoked potentials for surgical monitoring. Electroencephalogr Clin Neurophysiol 1988; 71: 142-145. 3. Harding GFA, Smith UH, Yorke HC. Visual evoked potential monitoring of orbital surgery using a contact lens stimulator. In: Barber C, Blum T, eds. Evoked potentials. Boston: Butterworth, 1988: 240-244. 4. Harding GFA, Bland JD, Smith UH. Visual evoked potential monitoring of optic nerve function during surgery. J Neurol Neurosurg Psychiatry 1990; 53: 890-895. 5. Wright JE, Arden G, Jones BR. Continuous monitoring of the visual evoked response during intraorbital surgery. Trans Ophthalmol Soc UK 1973; 93: 311-314. 6. Gaasterland D, Tanishima T, Kuwabara T. Axoplasmic flow during chronic experimental glaucoma. Invest Ophthalmol Vis Sci 1978; 17: 838-846. 7. Harding GFA, Wright CE. Visual evoked potentials in acute optic neuritis. In: Hess RF, Plant GT, eds. Optic Neuritis. New York: Cambridge University Press, 1986: 230-254. 8. Quigley HA, Addicks EM. Chronic experimental glaucoma in primates, II: Effect of extended intraocular pressure elevation on optic nerve head and axonal transport. Invest Ophthalmol Visual Sci 1980; 19: 137-152. 9. Siliprandi R, Bucci MG, Canella R, Camignoto G. Flash and pattern electroretinograms during and after acute intraocular pressure elevation in cats. Invest Ophthalmol Vis Sci 1988; 29: 558-565. 10. Halliday AM, Halliday E, Kriss A, McDonald WI, Mushin J. The pattern-evoked potential in compression of the anterior visual pathways. Brain 1976; 99: 357-374. 11. Halliday AM, Halliday E, Kriss A, McDonald WI, Mushin J. Changes in the pattern evoked response in compressive lesions of the anterior visual pathways. Electroencephalogr Clin Neurophysiol 1976; 40: 541. 12. Simpson DE, Moser LA. Compressive optic neuropathy secondary to chronic sinusitis. Am J Optom Physiol Opt 1988; 65: 757-762. 13. McDonald WI. Pathophysiology of conduction in central nerve fibres. In: Desmedt JF, ed. New developments in visual evoked potentials in the human brain. London: Oxford University Press. 1976: 427-437. 14. Minckler DS, Bunt A, Kloc IB. Radioautographic and cytochemical ultrastrnctural studies of axoplasmic transport in the monkey optic nerve head. Invest Ophthalmol Vis Sci 1978; 17: 33-50. 15. Hayreh SS, Revie IHS, Edwards J. Vasogenic origin of visual field defects and optic nerve changes in glaucoma. Br J Ophthalmol 1970; 54: 461-472.
Address for correspondence: Prof. Gyrrgy Benedek, Department of Physiology, D6m t6r 10, H-6720 Szeged, Hungary. Tel: 36/62/12049; Fax: 36/62/12529.
