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Retinal Breaks Secondary to Vascular Accidents
RETINAL BREAKS SECONDARY TO VASpULAR ACCIDENTS L. REGENBOGEN, M.D.,
V. GODEL, M.D., V. FEILER-OFRY, AND R. STEIN, M.D. Tel Hashomer,
M.D.,
Israel
AND G . COSCAS, M . D . Paris, France
Retinal breaks and detachments as complications of precedent occlusive vas cular retinal accidents seem to be rare events. 1-5 Two different mechanisms ac tive in the formation of retinal breaks secondary to major occlusive vascular ret inal accidents have been implicated up to now. One indicates a pathogenesis simi lar to the retinal breaks' of retinal detach ment.6 The other assumes that the ische mia provides a stimulus for the develop ment of neovascularization producing retinal breaks by vitreoretinal traction.7 In this report we present the histories, ophthalmoscopic and fluorescein-angiqgraphic findings of six patients in whom retinal holes were unequivocally'related to a precedent occlusion of a branch vein or an artery. We suggest a different patho genesis for some of the retinal holes. CASE REPORTS Case 1—In August 1969, a 60-year-old woman was referred for evaluation and treatment of an inferotemporal venous branch thrombosis of a few days' duration in her right eye. For many years she had been treated for essential arterial hypertension. Both eyes were slightly hyperopic. The visual acuity was 6/18 (20/60) in the right eye, and 6/6 (20/20) in the left. The. right eye presented the typical picture of a second branch thrombosis of the
From the Department of Ophthalmolpgy, Chaim Sheba Medical Center, Tel Aviv University Medical School, Tel Hashomer, Israel (Drs. Regenbogen, Godel, Feiler-Ofry, and Stein); and the Department of Ophthalmology, Creteil Medical Center, ParisVal de Marne Medical School, France (Dr. Coscas). Reprint requests to L. Regenbogen M.D., Depart ment of, Ophthalmology, Chaim Sheba Medical Center, Tel Hashomer, Israel.' ,
inferotemporal vein. In both eyes the posterior vitre ous appeared detached. After treatment with antico agulants for a period of five months, the vision in the affected eye improved to 6/12 (20/40), most of the retinal edema and the hemorrhages disappeared, and the patient was referred back to her attending physician. On re-examination three years later, two fullthickness retinal breaks were detected (Fig. 1). The occluded vein branch and all its tributaries appeared as whitish, slightly tortuous ghost vessels. Meander ing collaterals to the temporal upper vein were present. Fatty exudates were scattered within the affected area, especially at its' outer border. The adjacent temporal inferior artery was narrow and some of its branches invisible. The lower break at 8:30 o'clock was slightly oval, appearing as a punched out hole of approximately 0.5 disk diame ter and about 3 disk diameters from the fovea. Its operculum appeared a bit shrunken, and lay flatly and smoothly on the retina outside the hole, as if turned upon itself around its still-adherent narrow hinge. There were no adhesions between the oper culum and the flatly detached posterior hyaloid. The upper break at 10 o'clock was- a typical horseshoe tear, a bit larger and more distant from the fovea than the lower break. Its elevated flap, still broadly adherent to the retina, contained a patch of hard exudates and a tuft of neovascular tissue on its tip to which the detached pulling vitreous was attached. Fluorescein angiography (Fig. 2) revealed that the area around the lower hole was practically avascular. The ophthalmoscopically occluded venous branch appeared patent in its traject proximal to the disk. Its tributaries showed obstruction for some distance, with.only their distal parts filled by retrogade flow. The choroid of this region did not seem to be perfused. In contrast, the retina surrounding the upper tear was hyperfluorescent, showed leaking vessels, and the collaterals were luxuriant with their twisting course and bead-like ectasias. The tufts of neovascular tissue became more conspicuous after filling with fluorescein.. In January 1974, the upper tear was photocoagulated because its edges began to elevate. The lower hole was not treated. A£ the last re-examination in 1976 the tear was surrounded by a fine pigmented scar and the hole remained unchanged. Case 2—In 1969; a .59-year-old man started to complain of failing vision in both his eyes. Exami nation revealed a vision of 6/9 (20/30) in each eye.
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Fig. 1 (Regenbogen and associates). Case 1, right eye. The lower temporal vein with sheathing of its first branch (long arrow); the narrow adjacent artery (wide arrow); and the tortuosity of the branches of the upper temporal vein (thin arrow). At 10 o'clock is a horseshoe retinal tear (short arrow) with a tuft of neovascular tissue on its operculum. At 8:30 o'clock is an oval retinal hole with detached operculum (short arrow).
Perimetry showed irregular constriction of the visu al fields. Pressure in both eyes measured 16 mm Hg. On ophthalmoscopic examination slightly pale disks were discovered. In the right eye some segments of three arteries displayed pipestem sheathing. The medical history and various laboratory tests were noncontributory. Two years later, the vision in the right eye had decreased to 6/12 (20/40), the sheathing of the arter ies had progressed and involved the two arteries supplying the upper retina (Fig. 3). A large oval retinal hole about 3 disk diameters from the disk was found at a point where the nasal branch of the inferior artery was obstructed. There was a small hemorrhage at the first bifurcation of the artery (Fig. 4); on the nasal side of the hole an ill-defined cotton-wool exudate was present. The operculum, slightly elevated on its temporal margin, contained what looked like a cluster of newly formed vessels
adherent to a slightly detached vitreous. The atypi cal position of the operculum may have been due to the location of the hole in the lower part of the retina, even though the role played by the traction of the vitreous could not be ignored. Fluorescein angiography showed an ischemic area between the hole and the adjacent vein. This vein showed a delayed filling with fluorescein. Anastomosing vessels had developed centrally from the occlusion. No dye entered in the portion distal to the occlusion. Exten sive leakage took place in the later phase of the angiography. The hole and the cluster of new vessels were photocoagulated in October 1971. Ten days later, a massive vitreous hemorrhage occurred, which slow ly absorbed. In May 1975 the patient's vision re turned to 6/12 (20/40). Case 3—A 64-year-old woman with a past history of systemic hypertension was examined in January
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1969, because of a branch thrombosis of the left upper temporal vein. The corrected hypermetropic visual acuity was 6/6 (20/20) in the right eye and 6/18 (20/60) in the left. The thrombosis was located at the first upper temporal arteriovenous crossing. The obstructed vein had a hazy, veiled appearance and was dipping up and down in the still edematous retina. The accompanying artery was irregular and attenuated. In November 1970, an oval, 0.75 disk diameter large hole was detected, 1 disk diameter from the fovea. The free operculum tied to the detached vitreous was floating medially from the hole. The macula was still slightly edematous with scattered white dots and a few hemorrhages. In January 1971, the hole was sealed by photocoagulation. Figure 5 shows the photocoagulation scar, the ghost-like appearance of the occluded temporal upper vein, the obstructed part of the accompanying artery and the obstructed capillaries adjacent to the previous hole. Case 4—A 43-year-old man was examined in 1970
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because of a left retinal vascular accident. In he fundus a partial occlusion of both the superior temporal artery and vein at their first crossing was found. The onset of the patient's visual complaints had begun two weeks previously and his corrected visual acuity in this slightly hypermetropic eye was 6/60 (20/200). Hemorrhages and a few cotton-wool exudates were scattered over the entire superotemporal region involving the upper part of the macula. On fluorescein angiography some lumen patency of the involved vessels was present. In the following weeks the visual acuity improved to 6/15 (20/50), the macular edema regressed, and the hemorrhages dis appeared. About four years later the patient noted sudden blurring of vision. Visual acuity dropped to 6/60 (20/200). An oval retinal hole of about 0.75 disk diameter in size and about 4 disk diameters from the macula was detected. The hole was contiguous to a branch of the previously obstructed vein and the adjacent attenuated artery at the lower border of an avascular area. A slight hemorrhage into the vitreous
Fig 2 (Regenbogen and associates). Same area as in Figure 1. Arteriovenous phase of fluorescein angiography. The avascular area around the lower hole was caused by obstruction of the venous branch (long arrow) and by the irregular arterial perfusion (curved arrow). The retina is hyperfluorescent with persistent dye leakage (wide arrow) and meandering venous collaterals around the upper tear (short arrow).
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Fig. 3 (Regenbogen and associates). Case 2, right eye. A large oval retinal hole has neovascular tissue adherent to its operculum (thick arrow). The attenuated nasal branch of the inferior artery has hemorrhages at its first bifurcation (wide arrow); silver wire branch arteries (thin arrows).
originating from a vessel near the hole was the cause of the blurred vision. A narrow, apparently shrunk en operculum was still adherent to the upper edge of the hole and contained a tiny tuft of neovascular tissue to which a few strands of detached vitreous were adherent. (Fig. 6). Another cluster of flbrovascular tissue was present nasally and superiorly from the hole; a third cluster was present at 1 o'clock. Fluorescein angiography showed that the origi nally occluded vessels filled with some delay. The area around the hole was ischemic and the neovas cular formation leaked profusely in the late phase of angiography. At the site of the original obstruction the vein was deflected and its proximal part sinuous; the vein remained filled with dye in the late stage. The artery took a somewhat devious course after the crossing. Distally, collaterals and anastomosing ves sels were present which showed late fluorescein filling and leakage. The hole and the flbrovascular tissue were photocoagulated. The vision improved to 6/12 (20/40). No new occlusive episodes have occurred. Case 5—A 23-year-old man was referred to us with a history of sudden visual deterioration in his
left eye of two weeks' duration. The visual acuity in the left emetropic eye was 6/18 (20/60) and in the right eye 6/6 (20/20). Results of a complete physical examination and laboratory tests were normal. The left eye showed a subacute uveitis with mutton-fat precipitates on the posterior corneal surface, a flare in the anterior chamber, and a cloudy vitreous posteriorly detached. The retina was diffusely hazy. The retinal veins were slightly engorged and a small branch of the superior temporal vein just lateral to the macula appeared whitish and obstructed. In its immediate vicinity, 2 disk diameters laterally from the macula, a 1-disk diameter large oval hole was seen. Its margins were smooth and not elevated (Fig. 7). Its operculum was floating but remained tied to the detached vitreous body. Fluorescein angiography confirmed the avascularity of the in volved area. Within the hole persisting leakage of dye was seen coming from the choroid. The uveitis responded well to systemic corticosteroids. The hole was closed by photocoagulation. Case 6—A 72-year-old hypertensive woman was referred to our clinic because of a severe drop in visual acuity in her right eye. The ophthalmoscopic
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examination revealed a thrombosis of a branch of the inferotemporal vein with scattered flame-shape hemorrhages partially involving the macula. The visual acuity in the emetropic eye was 6/30 (20/100) without any correction. The acuity in the left eye was 6/6 (20/20). Four months later at her reexamination she complained of further deterioration of the visual acuity in her right eye. Ophthalmoscopic findings showed a central retinal detachment occupying the posterior pole around the macula. In the fovea a full-thickness atrophic hole was recog nized as being responsible for the detachment. Be cause of poor visual prognosis the patient refused surgery.
RESULTS
In a careful follow-up of 102 consecu tive patients suffering of an occlusive
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retinal accident during the past seven years, we found seven retinal breaks: five central nonmacular holes, one horseshoe tear (the second break in Case 1) and one macular hole. The occlusive vascular pro cess was venous in four eyes, arterial in two eyes, and combined in one. In each of our cases with primary venous or arterial occlusion, we found a secondary effect on the other portion of the retinal circula tion. The position and shape of all the retinal breaks in these six eyes are sche matically represented in Figure 8. The five central nonmacular retinal
Fig. 4 (Regenbogen and associates). The area surrounding the hole in Case 2. Top, The attenuated artery bridges the hole (arrow), continuing with a pipestem sheathing (arrowhead). Bottom left, Arterial-early venous phase of fluorescein angiography. The leakage is already present on the neovascular tissue of the operculum (curved arrow). Delayed fluorescence is present in the accompanying vein on the wall adjacent to the hole (wide arrow). The fluorescein outlines the opposite wall of this vein. Bottom right, Late venous phase of fluorescein angiography. Strong and persistent leakage is in the area of the retinal tear (thick arrow). Ischemic area is between the hole and adjacent vein (wide arrow); anastomosing vessels (thin arrow).
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Fig. 5 (Regenbogen and associates). Case 3, left eye. The upper temporal vein shows pipestem sheathing (thick arrow). A branch of the accompanying artery is occluded (thin arrow). Photocoagulated retinal hole (curved arrow) is 1 disk diameter temporally from the macula. Obstructed capillaries are adjacent to the hole (small arrow); hemorrhages and exudates around the macula.
holes found in our series had some com mon special features: 1. All were situated in the mid-retina, somewhere between macula and equator, not usually the site for the occurrence of retinal breaks. 2. All were topographically closely re lated to the precinct impaired by the preceding occlusive process of the vessels subserving this area. 3. All were round or oval, of a relative ly remarkable size ranging from 0.5 to 1 disk diameter. If they were oval, their longer diameter did not lie in the general direction of the major retinal vessels or of
the fibers of the nerve fiber layer but perpendicularly or obliquely to them. 4. Their edges were smooth. 5. The operculum was, if at all, only slightly elevated even when it was con nected to a detached vitreous. The oper culum, if not completely separated, was attached to the margin of the hole only by a narrow base and not in the way one usually sees in tears where the operculum is broad based. 6. The vitreous, even when detached, seemed to have played a secondary role in the formation of these holes. The only horseshoe tear was found in
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Fig. 6 (Regenbogen and associates). Case 4, left eye. Retinal vasculitis. An oval retinal hole (thick arrow) borders the narrow upper temporal vein. A tuft of neovascular tissue is adherent to the operculum (thin arrow); a big patch of neovascular tissue (curved arrow) is adherent to another vein branch.
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Fig. 7 (Regenbogen and associates). Case 5, left eye. Obstruction of a small branch of the superotemporal vein (short arrow). A large oval hole (long arrow) has floating operculum (curved arrow).
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Fig. 8 (Regenbogen and associates). The schemat ic representation of the position and shape of all the retinal breaks.
Case 1 as a second break. It was situated outside the retinal area affected by the vascular obstruction and appeared as a typical traction tear with a tuft of neovascular tissue pulled by the detached vitre ous. Although closely examined for, there were no changes such as the lattice, cystoid, or snail-track degenerations in the periphery of the affected eyes. None of the involved eyes were myopic. Five retinal breaks were closed by photocoagulation: the horseshoe tear in Case 1 because of the traction of the detached vitreous on its flap; another hole in Case 4 because of the presence of neovascular tissue in its operculum tied to some vitreous pulling. The remaining three holes were photocoagulated be cause of their size. DISCUSSION
Several hypotheses have been proposed to explain the etiology and pathogenesis of the peripheral retinal alterations that precede hole formation. In this process, peripheral degenerations in the retina,
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called detachment retinopathy, 8 are in volved and their course is related to the close proximity of the retinal periphery to the base of the vitreous. To explain this process, two views have been proposed. One stresses that the de tachment retinopathy is a primary process resulting from genetic causes in which senescence and myopia play their role, but in which occlusive vascular lesions in the smaller vessels of the retina and choroid are also involved. The other concept emphasizes the role of a pathological pulling vitreous, which may cause not only production of breaks and detach ments but also the detachment retinopa thy of the pre-hole stage. Today, it is generally accepted that trophic and tractional lesions are not mutually exclusive. Both processes may be active, though in different degrees, in the individual case. An altered vascular circulation pro duced by sclerotic narrowing of blood vessels and consequent obliteration of the lumen may be important factors in the formation of the detachment retinopathy. The typical picture of lattice degneration with the arborizing network of fine white lines in an area of retinal thinning sug gests an occlusive process of the periph eral retinal vessels. 9 The appearance of the cystoid degeneration in portions of the retina nourished by choriocapijlaris also indicates a vascular involvement. 10 A choroidretinopathy is sometimes associa ted with retinal hole formation and is characterized by pigment accumulation and sheathing of the retinal vessels. 11 Abnormalities in the overlying vitreous are present and probably represent a re sult of this choroidopathy. All these ob servations support the assumption that vascular deficiency plays a main role in the intimate mechanism of pre-hole de generation and consequent hole forma tion. Therefore, after occlusion of a major retinal vessel, artery, or vein, similar changes of detachment retinopathy may
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be found in the sector of the fundus served by the obstructed vessel. Retinal detachments after major vascu lar occlusion have been previously des cribed 6*7*12 and theories concerning their pathogenesis have been postulated. One hypothesis 6 was based on four cases of venous thrombosis where retinal holes appeared. Retinal detachments developed in three of these cases. The localization of all the retinal breaks were peripheral, situated in areas of typical retinal de generations. The following sequence of events was proposed: The vascular occlu sion causing microcystoid degeneration led to retinal cyst; the breakdown of its wall produced the retinal hole and finally retinal detachment appeared. The validity of such thinking was later questioned, 7 as the same sequence of Events occurs in peripheral retinal breaks without the presence of major vascular occlusion. It does not seem necessary to indict venous occlusion as a predisposing fac tor. An alternative explanation, 7 based on two cases in which a rhegmatogenous retinal detachment followed a retinal vein occlusion, suggested that after this occlu sion the retinal ischemia presumably served as a stimulus for the development of neovascularization. Because in both of these cases a tuft of neovascular tissue was adherent to the posterior hyaloid face, such a possibility warrants serious consideration. The sequence of events was thought to be identical to that oc curring in proliferative diabetic retinopathy, 1 3 in which neovascular fibrotic tissue produces tractional retinal detachment. The further contraction of these proliferative strands and the conse quent distension of the retina produce a retinal break, converting the tractional detachment to a rhegmatogenous one. The most prominent feature of the five round holes found in our cases was the location of the holes in a retinal region corresponding to the drainage area of the
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occluded venous channel. The absence of any leakage of dye after fluorescein angiography indicated that the causal mecha nism seemed to be an ischemiccapillaropathy. One exception to such capillary loss appeared in Case 2, where, in the late phase, an extensive leakage of dye was seen. Another feature was the minor role played by the vitreous. Even in the three instances where the operculum appeared adherent to a detached posterior hyaloid membrane, the vitreous seemed to have a secondary role in the hole formation; in no case were the free borders of the holes rolled u p or elevated. The vitreal changes seemed fortuitous rather than causative. In Case 4 in which the posterior hyaloid adh'ered to a tuft of neovascular tissue the vitfeous, though contributing to the hole formation, did not seem to have a primary role. In a concept concerning the pathogene sis of retinal breaks following venous branch thrombosis the active role played by the choroid must also be emphasized. Histological data 1 4 demonstrate that choroidal edema, cell infiltration, and thickening of the choroid underlying the affected retinal quadrant are common changes in cases of vascular obstruction. Such existing histological support raises the question in our cases of the choroidal contribution to the formation of the reti nal breaks. Choriocapillary obstructions Were described histologically in cases of retinal vein thrombosis', 15 giving support to the claims that in retinal vascular dis eases a mutual tissue interrelationship is found. 1 6 Severe alteration of the inner retinal layer caused by the occlusion of the retinal vessel, may be followed by damage of the outer retinal layer altered by the choroid involvement. The more or less uniform shape and size of the retinal holes found in our cases resemble the configuration of the choriocapillary net work described anatomically as capillary
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lobules. Even though no histological proofs are available in our cases, such a possibility of choroidal participation in the retinal breaks formation cannot be excluded. It may be assumed that the five round holes in our patients were the re sult of a kind of sequestration of the retina in which the pattern of the seques ter was determined by the size and shape of the corresponding lobule of the choriocapillaris. As long as the sequester re mained in its bed it could not be dis cerned, but once removed, the hole be came visible. It could be lifted from its bed by an adherent detached vitreous, as in Cases 3 and 4, or by slipping out of its bed when a detached vitreous made room for this displacement, as in Case 1. The pathogenesis of the horseshoe tear that lay outside the area involved by the occlusion of venous branch in Case 1 was identical with that described previously. 7 The vitreous attached to a tuft of neovascular tissue tore a flap out of the retina during the process of detachment. The macular hole, developed by rup ture of the cystoid degeneration in the macula, probably caused by vascular in competence. SUMMARY
Seven retinal breaks occurring after oc clusion of a major retinal arterial or ve nous branch were found in the eyes of six patients. Five holes were in the midretina, in a nonperfused avascular area corresponding to the sector affected by the vascular accident. One was a macular hole, and one a horseshoe tear outside the area involved in the vascular occlusion caused by traction of vitreous on a tuft of neovascular tissue. Five of the holes may have been caused by a kind of sequestra
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tion of the retina secondary to vascular insufficiency. REFERENCES 1. Ricci, A., and Dernaz, J. P.: Pronostic et sequelles des thromboses veineuses retiniennes. Ophthalmologica 156:325, 1968. 2. Krill, A. E., Archer, D., and Newell, F . W.: Photocoagulation in complications secondary to branch vein occlusion. Arch. Ophthalmol. 85:48, 1971. 3. Hill, D. W.: FJuorescein studies in retinal vas cular occlusions. Br. J. Ophthalmol. 52:1, 1968. 4. Wise, G.: Macular changes after venous ob struction. Arch. Ophthalmol. 58:544, 1957. 5. Michels, R. G., and Gass, J. D. M.: The natural course of retinal branch vein occlusion. Trans. Am. Acad. Ophthalmol. Otolaryngol. 78:166, 1974. 6. Zauberman, H.: Retinopathy of retinal detach ment after major vascular occlusion. Br. J. Ophthal mol. 52:117, 1968. 7. Joondeph, H. C., and Goldberg, M. F.: Rhegmatogenous retinal detachment after tributary reti nal vein occlusion. Am. J. Ophthalmol. 80:253, 1975. '8. Ballantyne, A. J., and Michaelson, I. C.: Text book of the Fundus of the Eye. Edinburgh and London, E. S. Livingstone, 1970, p. 399. 9. Okun, E.: Gross and microscopic pathology in autopsy eyes. 3. Retinal breaks without detachment. Am. J. Ophthalmol. 51:369, 1961. 10. Teng, C. C., and Katzin, H. M.: An anatomic study of the peripheral retina. 2. Peripheral cystoid degeneration of the retina. Formation of cysts and holes. Am. J. Ophthalmol. 36:29, 1953. 11. Michaelson, I. C.: Role of distinctive choroido-retinal lesion in the pathogenesis of retinal hole. Br. J. Ophthalmol. 40:527, 1956. 12. Archer, D. B., Ernest, J. T„ and Newell, F. W.: Classification of branch retinal vein obstruction. Trans. Am. Acad. Ophthalmol. Otolaryngol. 78:148, 1974. 13. Davis, M. D.: Vitreous contraction in proliferative diabetic retinopathy. Arch. Ophthalmol. 74: 741, 1965. 14. Rabinowics, I., Litman, S., and Michaelson, I. C.: Branch venous thrombosis. A pathological re port. Trans. Ophthal. Soc. U. K. 88:191, 1968. 15. Neumann, E.: Histology of choroid and retina after multiple recent occlusions of the retinal arter ies as revealed by coronal serial sections of the globe. Br. J. Ophthalmol. 46:357, 1962. 16. Michaelson, I. C : Intertissue vascular rela tionships in the fundus of the eye. Invest. Ophthal mol. 4:1004, 1965.
V. GODEL, M.D., V. FEILER-OFRY, AND R. STEIN, M.D. Tel Hashomer,
M.D.,
Israel
AND G . COSCAS, M . D . Paris, France
Retinal breaks and detachments as complications of precedent occlusive vas cular retinal accidents seem to be rare events. 1-5 Two different mechanisms ac tive in the formation of retinal breaks secondary to major occlusive vascular ret inal accidents have been implicated up to now. One indicates a pathogenesis simi lar to the retinal breaks' of retinal detach ment.6 The other assumes that the ische mia provides a stimulus for the develop ment of neovascularization producing retinal breaks by vitreoretinal traction.7 In this report we present the histories, ophthalmoscopic and fluorescein-angiqgraphic findings of six patients in whom retinal holes were unequivocally'related to a precedent occlusion of a branch vein or an artery. We suggest a different patho genesis for some of the retinal holes. CASE REPORTS Case 1—In August 1969, a 60-year-old woman was referred for evaluation and treatment of an inferotemporal venous branch thrombosis of a few days' duration in her right eye. For many years she had been treated for essential arterial hypertension. Both eyes were slightly hyperopic. The visual acuity was 6/18 (20/60) in the right eye, and 6/6 (20/20) in the left. The. right eye presented the typical picture of a second branch thrombosis of the
From the Department of Ophthalmolpgy, Chaim Sheba Medical Center, Tel Aviv University Medical School, Tel Hashomer, Israel (Drs. Regenbogen, Godel, Feiler-Ofry, and Stein); and the Department of Ophthalmology, Creteil Medical Center, ParisVal de Marne Medical School, France (Dr. Coscas). Reprint requests to L. Regenbogen M.D., Depart ment of, Ophthalmology, Chaim Sheba Medical Center, Tel Hashomer, Israel.' ,
inferotemporal vein. In both eyes the posterior vitre ous appeared detached. After treatment with antico agulants for a period of five months, the vision in the affected eye improved to 6/12 (20/40), most of the retinal edema and the hemorrhages disappeared, and the patient was referred back to her attending physician. On re-examination three years later, two fullthickness retinal breaks were detected (Fig. 1). The occluded vein branch and all its tributaries appeared as whitish, slightly tortuous ghost vessels. Meander ing collaterals to the temporal upper vein were present. Fatty exudates were scattered within the affected area, especially at its' outer border. The adjacent temporal inferior artery was narrow and some of its branches invisible. The lower break at 8:30 o'clock was slightly oval, appearing as a punched out hole of approximately 0.5 disk diame ter and about 3 disk diameters from the fovea. Its operculum appeared a bit shrunken, and lay flatly and smoothly on the retina outside the hole, as if turned upon itself around its still-adherent narrow hinge. There were no adhesions between the oper culum and the flatly detached posterior hyaloid. The upper break at 10 o'clock was- a typical horseshoe tear, a bit larger and more distant from the fovea than the lower break. Its elevated flap, still broadly adherent to the retina, contained a patch of hard exudates and a tuft of neovascular tissue on its tip to which the detached pulling vitreous was attached. Fluorescein angiography (Fig. 2) revealed that the area around the lower hole was practically avascular. The ophthalmoscopically occluded venous branch appeared patent in its traject proximal to the disk. Its tributaries showed obstruction for some distance, with.only their distal parts filled by retrogade flow. The choroid of this region did not seem to be perfused. In contrast, the retina surrounding the upper tear was hyperfluorescent, showed leaking vessels, and the collaterals were luxuriant with their twisting course and bead-like ectasias. The tufts of neovascular tissue became more conspicuous after filling with fluorescein.. In January 1974, the upper tear was photocoagulated because its edges began to elevate. The lower hole was not treated. A£ the last re-examination in 1976 the tear was surrounded by a fine pigmented scar and the hole remained unchanged. Case 2—In 1969; a .59-year-old man started to complain of failing vision in both his eyes. Exami nation revealed a vision of 6/9 (20/30) in each eye.
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Fig. 1 (Regenbogen and associates). Case 1, right eye. The lower temporal vein with sheathing of its first branch (long arrow); the narrow adjacent artery (wide arrow); and the tortuosity of the branches of the upper temporal vein (thin arrow). At 10 o'clock is a horseshoe retinal tear (short arrow) with a tuft of neovascular tissue on its operculum. At 8:30 o'clock is an oval retinal hole with detached operculum (short arrow).
Perimetry showed irregular constriction of the visu al fields. Pressure in both eyes measured 16 mm Hg. On ophthalmoscopic examination slightly pale disks were discovered. In the right eye some segments of three arteries displayed pipestem sheathing. The medical history and various laboratory tests were noncontributory. Two years later, the vision in the right eye had decreased to 6/12 (20/40), the sheathing of the arter ies had progressed and involved the two arteries supplying the upper retina (Fig. 3). A large oval retinal hole about 3 disk diameters from the disk was found at a point where the nasal branch of the inferior artery was obstructed. There was a small hemorrhage at the first bifurcation of the artery (Fig. 4); on the nasal side of the hole an ill-defined cotton-wool exudate was present. The operculum, slightly elevated on its temporal margin, contained what looked like a cluster of newly formed vessels
adherent to a slightly detached vitreous. The atypi cal position of the operculum may have been due to the location of the hole in the lower part of the retina, even though the role played by the traction of the vitreous could not be ignored. Fluorescein angiography showed an ischemic area between the hole and the adjacent vein. This vein showed a delayed filling with fluorescein. Anastomosing vessels had developed centrally from the occlusion. No dye entered in the portion distal to the occlusion. Exten sive leakage took place in the later phase of the angiography. The hole and the cluster of new vessels were photocoagulated in October 1971. Ten days later, a massive vitreous hemorrhage occurred, which slow ly absorbed. In May 1975 the patient's vision re turned to 6/12 (20/40). Case 3—A 64-year-old woman with a past history of systemic hypertension was examined in January
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1969, because of a branch thrombosis of the left upper temporal vein. The corrected hypermetropic visual acuity was 6/6 (20/20) in the right eye and 6/18 (20/60) in the left. The thrombosis was located at the first upper temporal arteriovenous crossing. The obstructed vein had a hazy, veiled appearance and was dipping up and down in the still edematous retina. The accompanying artery was irregular and attenuated. In November 1970, an oval, 0.75 disk diameter large hole was detected, 1 disk diameter from the fovea. The free operculum tied to the detached vitreous was floating medially from the hole. The macula was still slightly edematous with scattered white dots and a few hemorrhages. In January 1971, the hole was sealed by photocoagulation. Figure 5 shows the photocoagulation scar, the ghost-like appearance of the occluded temporal upper vein, the obstructed part of the accompanying artery and the obstructed capillaries adjacent to the previous hole. Case 4—A 43-year-old man was examined in 1970
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because of a left retinal vascular accident. In he fundus a partial occlusion of both the superior temporal artery and vein at their first crossing was found. The onset of the patient's visual complaints had begun two weeks previously and his corrected visual acuity in this slightly hypermetropic eye was 6/60 (20/200). Hemorrhages and a few cotton-wool exudates were scattered over the entire superotemporal region involving the upper part of the macula. On fluorescein angiography some lumen patency of the involved vessels was present. In the following weeks the visual acuity improved to 6/15 (20/50), the macular edema regressed, and the hemorrhages dis appeared. About four years later the patient noted sudden blurring of vision. Visual acuity dropped to 6/60 (20/200). An oval retinal hole of about 0.75 disk diameter in size and about 4 disk diameters from the macula was detected. The hole was contiguous to a branch of the previously obstructed vein and the adjacent attenuated artery at the lower border of an avascular area. A slight hemorrhage into the vitreous
Fig 2 (Regenbogen and associates). Same area as in Figure 1. Arteriovenous phase of fluorescein angiography. The avascular area around the lower hole was caused by obstruction of the venous branch (long arrow) and by the irregular arterial perfusion (curved arrow). The retina is hyperfluorescent with persistent dye leakage (wide arrow) and meandering venous collaterals around the upper tear (short arrow).
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Fig. 3 (Regenbogen and associates). Case 2, right eye. A large oval retinal hole has neovascular tissue adherent to its operculum (thick arrow). The attenuated nasal branch of the inferior artery has hemorrhages at its first bifurcation (wide arrow); silver wire branch arteries (thin arrows).
originating from a vessel near the hole was the cause of the blurred vision. A narrow, apparently shrunk en operculum was still adherent to the upper edge of the hole and contained a tiny tuft of neovascular tissue to which a few strands of detached vitreous were adherent. (Fig. 6). Another cluster of flbrovascular tissue was present nasally and superiorly from the hole; a third cluster was present at 1 o'clock. Fluorescein angiography showed that the origi nally occluded vessels filled with some delay. The area around the hole was ischemic and the neovas cular formation leaked profusely in the late phase of angiography. At the site of the original obstruction the vein was deflected and its proximal part sinuous; the vein remained filled with dye in the late stage. The artery took a somewhat devious course after the crossing. Distally, collaterals and anastomosing ves sels were present which showed late fluorescein filling and leakage. The hole and the flbrovascular tissue were photocoagulated. The vision improved to 6/12 (20/40). No new occlusive episodes have occurred. Case 5—A 23-year-old man was referred to us with a history of sudden visual deterioration in his
left eye of two weeks' duration. The visual acuity in the left emetropic eye was 6/18 (20/60) and in the right eye 6/6 (20/20). Results of a complete physical examination and laboratory tests were normal. The left eye showed a subacute uveitis with mutton-fat precipitates on the posterior corneal surface, a flare in the anterior chamber, and a cloudy vitreous posteriorly detached. The retina was diffusely hazy. The retinal veins were slightly engorged and a small branch of the superior temporal vein just lateral to the macula appeared whitish and obstructed. In its immediate vicinity, 2 disk diameters laterally from the macula, a 1-disk diameter large oval hole was seen. Its margins were smooth and not elevated (Fig. 7). Its operculum was floating but remained tied to the detached vitreous body. Fluorescein angiography confirmed the avascularity of the in volved area. Within the hole persisting leakage of dye was seen coming from the choroid. The uveitis responded well to systemic corticosteroids. The hole was closed by photocoagulation. Case 6—A 72-year-old hypertensive woman was referred to our clinic because of a severe drop in visual acuity in her right eye. The ophthalmoscopic
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examination revealed a thrombosis of a branch of the inferotemporal vein with scattered flame-shape hemorrhages partially involving the macula. The visual acuity in the emetropic eye was 6/30 (20/100) without any correction. The acuity in the left eye was 6/6 (20/20). Four months later at her reexamination she complained of further deterioration of the visual acuity in her right eye. Ophthalmoscopic findings showed a central retinal detachment occupying the posterior pole around the macula. In the fovea a full-thickness atrophic hole was recog nized as being responsible for the detachment. Be cause of poor visual prognosis the patient refused surgery.
RESULTS
In a careful follow-up of 102 consecu tive patients suffering of an occlusive
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retinal accident during the past seven years, we found seven retinal breaks: five central nonmacular holes, one horseshoe tear (the second break in Case 1) and one macular hole. The occlusive vascular pro cess was venous in four eyes, arterial in two eyes, and combined in one. In each of our cases with primary venous or arterial occlusion, we found a secondary effect on the other portion of the retinal circula tion. The position and shape of all the retinal breaks in these six eyes are sche matically represented in Figure 8. The five central nonmacular retinal
Fig. 4 (Regenbogen and associates). The area surrounding the hole in Case 2. Top, The attenuated artery bridges the hole (arrow), continuing with a pipestem sheathing (arrowhead). Bottom left, Arterial-early venous phase of fluorescein angiography. The leakage is already present on the neovascular tissue of the operculum (curved arrow). Delayed fluorescence is present in the accompanying vein on the wall adjacent to the hole (wide arrow). The fluorescein outlines the opposite wall of this vein. Bottom right, Late venous phase of fluorescein angiography. Strong and persistent leakage is in the area of the retinal tear (thick arrow). Ischemic area is between the hole and adjacent vein (wide arrow); anastomosing vessels (thin arrow).
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Fig. 5 (Regenbogen and associates). Case 3, left eye. The upper temporal vein shows pipestem sheathing (thick arrow). A branch of the accompanying artery is occluded (thin arrow). Photocoagulated retinal hole (curved arrow) is 1 disk diameter temporally from the macula. Obstructed capillaries are adjacent to the hole (small arrow); hemorrhages and exudates around the macula.
holes found in our series had some com mon special features: 1. All were situated in the mid-retina, somewhere between macula and equator, not usually the site for the occurrence of retinal breaks. 2. All were topographically closely re lated to the precinct impaired by the preceding occlusive process of the vessels subserving this area. 3. All were round or oval, of a relative ly remarkable size ranging from 0.5 to 1 disk diameter. If they were oval, their longer diameter did not lie in the general direction of the major retinal vessels or of
the fibers of the nerve fiber layer but perpendicularly or obliquely to them. 4. Their edges were smooth. 5. The operculum was, if at all, only slightly elevated even when it was con nected to a detached vitreous. The oper culum, if not completely separated, was attached to the margin of the hole only by a narrow base and not in the way one usually sees in tears where the operculum is broad based. 6. The vitreous, even when detached, seemed to have played a secondary role in the formation of these holes. The only horseshoe tear was found in
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\ \
Fig. 6 (Regenbogen and associates). Case 4, left eye. Retinal vasculitis. An oval retinal hole (thick arrow) borders the narrow upper temporal vein. A tuft of neovascular tissue is adherent to the operculum (thin arrow); a big patch of neovascular tissue (curved arrow) is adherent to another vein branch.
z*
Fig. 7 (Regenbogen and associates). Case 5, left eye. Obstruction of a small branch of the superotemporal vein (short arrow). A large oval hole (long arrow) has floating operculum (curved arrow).
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Fig. 8 (Regenbogen and associates). The schemat ic representation of the position and shape of all the retinal breaks.
Case 1 as a second break. It was situated outside the retinal area affected by the vascular obstruction and appeared as a typical traction tear with a tuft of neovascular tissue pulled by the detached vitre ous. Although closely examined for, there were no changes such as the lattice, cystoid, or snail-track degenerations in the periphery of the affected eyes. None of the involved eyes were myopic. Five retinal breaks were closed by photocoagulation: the horseshoe tear in Case 1 because of the traction of the detached vitreous on its flap; another hole in Case 4 because of the presence of neovascular tissue in its operculum tied to some vitreous pulling. The remaining three holes were photocoagulated be cause of their size. DISCUSSION
Several hypotheses have been proposed to explain the etiology and pathogenesis of the peripheral retinal alterations that precede hole formation. In this process, peripheral degenerations in the retina,
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called detachment retinopathy, 8 are in volved and their course is related to the close proximity of the retinal periphery to the base of the vitreous. To explain this process, two views have been proposed. One stresses that the de tachment retinopathy is a primary process resulting from genetic causes in which senescence and myopia play their role, but in which occlusive vascular lesions in the smaller vessels of the retina and choroid are also involved. The other concept emphasizes the role of a pathological pulling vitreous, which may cause not only production of breaks and detach ments but also the detachment retinopa thy of the pre-hole stage. Today, it is generally accepted that trophic and tractional lesions are not mutually exclusive. Both processes may be active, though in different degrees, in the individual case. An altered vascular circulation pro duced by sclerotic narrowing of blood vessels and consequent obliteration of the lumen may be important factors in the formation of the detachment retinopathy. The typical picture of lattice degneration with the arborizing network of fine white lines in an area of retinal thinning sug gests an occlusive process of the periph eral retinal vessels. 9 The appearance of the cystoid degeneration in portions of the retina nourished by choriocapijlaris also indicates a vascular involvement. 10 A choroidretinopathy is sometimes associa ted with retinal hole formation and is characterized by pigment accumulation and sheathing of the retinal vessels. 11 Abnormalities in the overlying vitreous are present and probably represent a re sult of this choroidopathy. All these ob servations support the assumption that vascular deficiency plays a main role in the intimate mechanism of pre-hole de generation and consequent hole forma tion. Therefore, after occlusion of a major retinal vessel, artery, or vein, similar changes of detachment retinopathy may
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be found in the sector of the fundus served by the obstructed vessel. Retinal detachments after major vascu lar occlusion have been previously des cribed 6*7*12 and theories concerning their pathogenesis have been postulated. One hypothesis 6 was based on four cases of venous thrombosis where retinal holes appeared. Retinal detachments developed in three of these cases. The localization of all the retinal breaks were peripheral, situated in areas of typical retinal de generations. The following sequence of events was proposed: The vascular occlu sion causing microcystoid degeneration led to retinal cyst; the breakdown of its wall produced the retinal hole and finally retinal detachment appeared. The validity of such thinking was later questioned, 7 as the same sequence of Events occurs in peripheral retinal breaks without the presence of major vascular occlusion. It does not seem necessary to indict venous occlusion as a predisposing fac tor. An alternative explanation, 7 based on two cases in which a rhegmatogenous retinal detachment followed a retinal vein occlusion, suggested that after this occlu sion the retinal ischemia presumably served as a stimulus for the development of neovascularization. Because in both of these cases a tuft of neovascular tissue was adherent to the posterior hyaloid face, such a possibility warrants serious consideration. The sequence of events was thought to be identical to that oc curring in proliferative diabetic retinopathy, 1 3 in which neovascular fibrotic tissue produces tractional retinal detachment. The further contraction of these proliferative strands and the conse quent distension of the retina produce a retinal break, converting the tractional detachment to a rhegmatogenous one. The most prominent feature of the five round holes found in our cases was the location of the holes in a retinal region corresponding to the drainage area of the
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occluded venous channel. The absence of any leakage of dye after fluorescein angiography indicated that the causal mecha nism seemed to be an ischemiccapillaropathy. One exception to such capillary loss appeared in Case 2, where, in the late phase, an extensive leakage of dye was seen. Another feature was the minor role played by the vitreous. Even in the three instances where the operculum appeared adherent to a detached posterior hyaloid membrane, the vitreous seemed to have a secondary role in the hole formation; in no case were the free borders of the holes rolled u p or elevated. The vitreal changes seemed fortuitous rather than causative. In Case 4 in which the posterior hyaloid adh'ered to a tuft of neovascular tissue the vitfeous, though contributing to the hole formation, did not seem to have a primary role. In a concept concerning the pathogene sis of retinal breaks following venous branch thrombosis the active role played by the choroid must also be emphasized. Histological data 1 4 demonstrate that choroidal edema, cell infiltration, and thickening of the choroid underlying the affected retinal quadrant are common changes in cases of vascular obstruction. Such existing histological support raises the question in our cases of the choroidal contribution to the formation of the reti nal breaks. Choriocapillary obstructions Were described histologically in cases of retinal vein thrombosis', 15 giving support to the claims that in retinal vascular dis eases a mutual tissue interrelationship is found. 1 6 Severe alteration of the inner retinal layer caused by the occlusion of the retinal vessel, may be followed by damage of the outer retinal layer altered by the choroid involvement. The more or less uniform shape and size of the retinal holes found in our cases resemble the configuration of the choriocapillary net work described anatomically as capillary
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lobules. Even though no histological proofs are available in our cases, such a possibility of choroidal participation in the retinal breaks formation cannot be excluded. It may be assumed that the five round holes in our patients were the re sult of a kind of sequestration of the retina in which the pattern of the seques ter was determined by the size and shape of the corresponding lobule of the choriocapillaris. As long as the sequester re mained in its bed it could not be dis cerned, but once removed, the hole be came visible. It could be lifted from its bed by an adherent detached vitreous, as in Cases 3 and 4, or by slipping out of its bed when a detached vitreous made room for this displacement, as in Case 1. The pathogenesis of the horseshoe tear that lay outside the area involved by the occlusion of venous branch in Case 1 was identical with that described previously. 7 The vitreous attached to a tuft of neovascular tissue tore a flap out of the retina during the process of detachment. The macular hole, developed by rup ture of the cystoid degeneration in the macula, probably caused by vascular in competence. SUMMARY
Seven retinal breaks occurring after oc clusion of a major retinal arterial or ve nous branch were found in the eyes of six patients. Five holes were in the midretina, in a nonperfused avascular area corresponding to the sector affected by the vascular accident. One was a macular hole, and one a horseshoe tear outside the area involved in the vascular occlusion caused by traction of vitreous on a tuft of neovascular tissue. Five of the holes may have been caused by a kind of sequestra
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tion of the retina secondary to vascular insufficiency. REFERENCES 1. Ricci, A., and Dernaz, J. P.: Pronostic et sequelles des thromboses veineuses retiniennes. Ophthalmologica 156:325, 1968. 2. Krill, A. E., Archer, D., and Newell, F . W.: Photocoagulation in complications secondary to branch vein occlusion. Arch. Ophthalmol. 85:48, 1971. 3. Hill, D. W.: FJuorescein studies in retinal vas cular occlusions. Br. J. Ophthalmol. 52:1, 1968. 4. Wise, G.: Macular changes after venous ob struction. Arch. Ophthalmol. 58:544, 1957. 5. Michels, R. G., and Gass, J. D. M.: The natural course of retinal branch vein occlusion. Trans. Am. Acad. Ophthalmol. Otolaryngol. 78:166, 1974. 6. Zauberman, H.: Retinopathy of retinal detach ment after major vascular occlusion. Br. J. Ophthal mol. 52:117, 1968. 7. Joondeph, H. C., and Goldberg, M. F.: Rhegmatogenous retinal detachment after tributary reti nal vein occlusion. Am. J. Ophthalmol. 80:253, 1975. '8. Ballantyne, A. J., and Michaelson, I. C.: Text book of the Fundus of the Eye. Edinburgh and London, E. S. Livingstone, 1970, p. 399. 9. Okun, E.: Gross and microscopic pathology in autopsy eyes. 3. Retinal breaks without detachment. Am. J. Ophthalmol. 51:369, 1961. 10. Teng, C. C., and Katzin, H. M.: An anatomic study of the peripheral retina. 2. Peripheral cystoid degeneration of the retina. Formation of cysts and holes. Am. J. Ophthalmol. 36:29, 1953. 11. Michaelson, I. C.: Role of distinctive choroido-retinal lesion in the pathogenesis of retinal hole. Br. J. Ophthalmol. 40:527, 1956. 12. Archer, D. B., Ernest, J. T„ and Newell, F. W.: Classification of branch retinal vein obstruction. Trans. Am. Acad. Ophthalmol. Otolaryngol. 78:148, 1974. 13. Davis, M. D.: Vitreous contraction in proliferative diabetic retinopathy. Arch. Ophthalmol. 74: 741, 1965. 14. Rabinowics, I., Litman, S., and Michaelson, I. C.: Branch venous thrombosis. A pathological re port. Trans. Ophthal. Soc. U. K. 88:191, 1968. 15. Neumann, E.: Histology of choroid and retina after multiple recent occlusions of the retinal arter ies as revealed by coronal serial sections of the globe. Br. J. Ophthalmol. 46:357, 1962. 16. Michaelson, I. C : Intertissue vascular rela tionships in the fundus of the eye. Invest. Ophthal mol. 4:1004, 1965.