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Show lournal of Clmrcal Neuro, of'hthalrnology 11( 4): 228- 232, 1991. Intraretinal Gray Lesions as a Sign of Reversible Visual Loss Following Prolonged Ophthalmic Artery Hypoperfusion Mark Cherny, M. B. B. S., Justin O'Day, F. R. A. CoP., FoR. A. C. So, and Jon Currie, F. R. A. C. P. © 1991 Raven Press, Ltd., New York A 49- year- old woman developed severe unilateral visual loss following carotid artery ligation for a carotidcavernous fistula. The pathophysiology was presumed to be an ophthalmic artery steal caused by the fistula. This was confirmed when visual acuity was restored by a subsequent ligation of the ophthalmic artery, despite 2 weeks of profound visual loss and ocular ischemia. Superficial cotton- wool spots and deep gray intraretinallesions developed in the retina during the period of ocular ischemia. We postulate that the deep intraretinallesions are clinical manifestations of a zone of retinal microvascular watershed ischemia, and that their presence may be an important diagnostic guide to the presence of reversible ocular ischemia. Key Words: Ophthalmic artery- Hypoperfusion- Gray intraretinal lesions- Cotton- wool spots- Reversible visualloss-- Carotid- cavernous fistula- Retrograde flow. From the Department of Neuro- ophthalmology, 5t. Vincent's Hospital. Fitzroy, 3065, Australia. Address correspondence and reprint requests to Dr. Justin ,--..". ,: nl'Jrtm'.' nt of Neuro- ophthalmology, 51. Vincent's - I, ~ 228 Visual loss can occur as a direct consequence of carotid- cavernous fistulae or can arise as a complication of surgical treatment of the fistula, particularly occlusion of the carotid artery. One postulated mechanism for ocular ischemia and visual loss occurring after internal carotid artery ligation is the development of an arterial" steal" created by retrograde flow in the ophthalmic artery toward the high- flow carotid- cavernous fistula. We describe a case which provides clinical confirmation of this hypothesis. In addition, the case described is remarkable for the unusual gray intraretinallesions that were observed at the time of ocular ischemia, and we postulate that these may be a sign of reversible ocular ischemia occurring at a watershed between the retinal and choroidal circulations. CASE REPORT A 49- year- old normotensive woman presented 2 weeks after minor head trauma, with symptoms of horizontal diplopia, frontal headaches, and a buzzing sound in the right ear. On examination, her visual acuities were 20/ 30 00 and 20/ 20 OS and she had 3 mm of pulsatile right proptosis, a partial right sixth- nerve paresis, and a right orbital bruito Intraocular pressures were 20 mm Hg 00 and 16 mm Hg OS. Conjunctival and retinal vessels were normal. There was a patch of myelinated nerve fibers inferior to the optic disc in the right eye. The clinical diagnosis of a carotid- cavernous fistula was confirmed by carotid angiography ( Fig. 1). Over the next 5 weeks she developed chemosis, increasing proptosis, and ophthalmoplegia ( Fig. 2); a balloon occlusion of the right internal carotid artery immediately above the bifurcation of the INTRARETINAL LESIONS IN REVERSIBLE ISCHEMIA 229 FIG. 1. Right internal carotid angiogram demonstrating the carotidcavernous fistula. common carotid artery was attempted. This failed to occlude the fistula, but caused thrombosis of the internal carotid artery between the balloon and the bifurcation of the common carotid artery. Within 24 hours there was a reduction in the right chemosis, and the orbital bruit disappeared. However, vision in the right eye deteriorated to " counting fingers." On examination of the right fundus, there were several white cotton- wool spots typical of ischemic axoplasmic stasis ( Fig. 3). However, in addition, there were many unusual grey intraretinallesions around the posterior pole lying deep to the retinal vessels and superficial to the retinal pigment epithelium. A fluorescein angiogram at that FIG. 2. Exophthalmos. chemosis, and dilation of conjunctival vessels 1 month following the injury ( prior to surgery). time showed delayed choroidal and retinal perfusion consistent with ophthalmic artery hypoperfusian ( Fig. 4). Her clinical condition deteriorated further, with right eye pain, increasing right proptosis, and right visual acuity reduced to perception of hand movements. Concurrently, the number of gray intraretinal lesions in the right eye increased. Carotid angiography confirmed that the right internal carotid artery was occluded, with filling of the right ophthalmic artery from branches of the right external carotid artery. The carotid- cavernous fistula was still patent. A second procedure was undertaken 2 weeks after balloon occlusion had thrombosed the right internal carotid artery proximal to the carotidcavernous fistula. The right internal carotid artery was clipped immediately distal to the origin of the ophthalmic artery, occluding both the internal carotid artery and the origin of the ophthalmic artery. Within 24 hours, the patient's right visual acuity had begun to improve, and after 7 days was 20/ 40. The chemosis and proptosis resolved. A fluorescein angiogram 7 days postoperatively demonstrated a normal transit of dye through the retinal and choroidal circulations. The cotton- wool spots and gray intraretinallesions gradually disappeared over 6 weeks following the second procedure. DISCUSSION Although the retina can successfully tolerate longer periods of ischemia than the brain, the vi- I Clill Neuro- ophlhalmol, Vol. 11, No. 4, 1991 230 M. CHERNY ET AL. A B FIG. 3. Stereographic pair of fundus views demonstrating some superficial ( white arrows) and multiple deep ( black arrows) gray intraretinal cotton- wool spots. following occlusion of internal carotid artery proximal to the carotid- cavernous fistula. Note incidental findings of myelinated inferotemporal nerve fibers. sual loss that occurs following prolonged ocular ischemia is usually irreversible ( 1,2). There are, however, occasional reports of reversible visual loss following prolonged ocular ischemia ( 1,3), and in the case described above, vision recovered from counting fingers to 20/ 40 after a period of more than 2 weeks. Figure 5 summarizes the hemodynamic changes that we believe underlie the reversal of visual loss in this case. Following our patient's initial operation, the right internal carotid .• ' hrolllbosed in its proximal section. and vision in the right eye deteriorated to counting fingers. As demonstrated by carotid angiography, the right ophthalmic artery remained patent and was perfused by anastomotic branches from the right external carotid artery. However, despite the development of collateral perfusion to the ophthalmic artery, ocular ischemia supervened, evidenced by profound visual loss and fluorescein angiographic evidence of ocular hypoperfusion. We postulate that this was due to an arterial steal phenomenon with reversal of blood flow in the oph- INTRARETINAL LESIONS IN REVERSIBLE ISCHEMIA 231 FIG. 4. Fluorescein angiogram 22 seconds following intravenous fluorescein injection demonstrating slow choroidal and retinal flow. Complete choroidal filling took 14 seconds, and full filling of the retinal veins occurred after 16 seconds and before 25 seconds. thalmic artery toward the high- flow carotidcavernous fistula ( Fig. 5A). Following ligation of the origin of the ophthalmic artery at the second operation, vision " paradoxically" improved to 20/ 40, and fluorescein angiography showed more rapid filling of both the choroidal and retinal circulations. This suggests that following cessation of the arterial steal by occlusion of the origin of the ophthalmic artery, the anastomotic flow from the external carotid artery to the ophthalmic artery was redirected toward the eye, leading to improved retinal and choroidal perfusion and recovery of visual function despite prolonged ischemia ( Fig. 5B). Arterial steal, created by retrograde blood flow in the ophthalmic artery, is one of the putative pathophysiologic mechanisms invoked to explain the development of ocular hypoperfusion that sometimes occurs with carotid artery occlusion ( 4,5) or carotid- cavernous fistulae ( 6). To our knowledge this is the first report of direct clinical confirmation of such a mechanism terminating the arterial steal, and occlusion of the ophthalmic artery leading to increased ocular perfusion and reversal of visual loss. Together with the excellent visual recovery from prolonged ocular ischemia, another noteworthy feature in this case was the appearance of unusual gray intraretinal lesions at the time that the visual loss developed. We believe that these intraretinal VISION DECREASED E. C. A. OPHTHALMIC ARTERY BALLOON CATHETER 1st" OPERATION ~ THROMBUS .,,-----_--------,- - - -- t I. C. A. A B VISION IMPROVED FIG. 5. A: 1st operation- a balloon catheter fails to occlude the carotid- cavernous fistula. and the internal carotid artery ( ICA) is thrombosed proximal to the balloon. The collateral blood supply via the external carotid artery ( ECA) is shown. There is reduced ocular perfusion. B: 2nd operation- The internal carotid artery and the origin of the ophthalmic artery are occluded. There is improved ocular perfusion. The postulated changes in direction of maximum blood flow in the ophthalmic artery are indicated in the diagram. 1 CIin Neuro- iJphthalmol. Vol. 11, No. 4, 1991 232 M. CHERNY ET AL. gray lesions may represent a clinically distinctive sign that provides an important diagnostic guide to the presence of reversible ocular ischemia. These lesions were different from the occasional typical white cotton- wool spots that were also present in the fundus. Cotton- wool spots are located superficially in the retina and are caused by axoplasmic stasis often due to ischemia at the level of the retinal capillaries or precapillary arterioles ( 7,8). They occur in association with conditions such as hypertension, retinal vasculitis, papilledema, or ischemic optic neuropathy, none of which was present in our patient. They may also occur in the presence of retinal artery hypoperfusion which was present in this patient ( retinal filling time of 25 seconds). However, the numerous deeper gray intraretinallesions that also developed in this patient at the time of severe visual loss, following carotid artery ligation, do not occur when retinal artery hypoperfusion is present in isolation. These gray lesions were diffusely scattered around the macula, rather than oriented around the optic nerve head. On stereoscopic fundus examination, they were situated deep within the retina and not in the superficial nerve fiber layer. These clinical features also distinguish the lesions from other " atypical" cotton- wool spots that have previously been described ( 5,9- 11). Schenk ( 12), however, in 1955 described a patient with a traumatic carotid- cavernous fistula whose vision in one eye deteriorated to counting fingers follOWing ligation of the carotid artery. This patient developed numerous discrete gray retinal lesions similar to those described above. After a 3- week period of visual loss, this patient had a sudden and dramatic improvement in visual acuity with resolution of the gray retinal lesions. This may represent a similar reversible ischemic process to that in our case. We believe that these gray intraretinal lesions may be situated at a microvascular watershed zone in the retina. The vascular supply of outer retina is provided by the choriocapiIlaris, while the inner layers of the retina are supplied by retinal vessels that lie in the superficial nerve- fiber layer and in the plane betweeT' the inner nuclear layer and outer plexiform layer ( 13,14). A potential vascular I Clin Neuro- ophtllalmol, \ ", .' watershed zone exists at the junction between these two blood supplies, in the region of the outer nuclear and outer plexiform layers of the retina. The presence of many gray intraretinallesions, but few superficial white cotton- wool spots suggests that our patient may have had retinal ischemia in this deeper watershed zone. We suggest that these gray intraretinallesions are a clinical manifestation of ischemia occurring at a microvascular watershed, and may therefore be an important clinical indicator of potentially reversible ocular ischemia and visual loss. In the setting of ocular ischemia from complex vascular lesions such as carotidcavernous fistulae, such gray intraretinal lesions may actually be more frequent than previously recognized, and their presence may help both in determining the pathophysiology of visual loss and in planning further management. REFERENCES 1. Hayreh 55, Weingast TA, Experimental occlusion of the central retinal artery of the retina, IV, Retinal tolerance time to acute ischemia, Br I Ophthalmol 1980; 64: 818- 25, 2, Brown GC, Magargal LE, 5ergott R. Acute obstruction of the retinal and choroidal circulations, Ophthalmology 1986; 93: 1373- 82, 3, Edwards 5E, Chater LN, Stanley JA. Reversal of chronic ocular ischemia by extracranial- intracranial arterial bypass: case report, Neurosurgery 1980; 7: 480- 3, 4, Huckman MS, Haas J. 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Uber das Aufrtreten einer Retinopathia traumatIca Pyrtscher nach Unterbindung der Arteria carotis commumums. Kim Monatsbl Augenheilkd 1955; 127: 669- 76. 13. Hogan MJ, Alvarado JA, Weddell JE. Histology of the human eye. Philadelphia: WB Saunders, 1971: 403. 14. Warwick R. Eugene Wolff's Anatomy of the Eye and Orbit. London: Lewis, 1976: 151. |
