ARTIFICIAL RETINAL TEARS : Experimental Production of Tears in Hog Eyes with Particular References to Hook-shaped Tears

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ACTA OPHTHALMOLOGICA VOL. 4 1 1963 From the University Eye Clinic (Head: Professor H. Ehlers), Rigshospitalet, Copenhagen, Denmark ARTIFICIAL RETINAL TEARS*) Experimental Production o f Tears in Hog Eyes w i th Particular References to Hook-shaped Tears BY K . La11 and B . Backhaus Retinal tears, especially the significance of their localization to surgical treat- ment of retinal detachment, is of great topical interest. Indeed, the literature on retinal holes with or without detachment, their aetiology, morphology, and localization has increased immensely year by year since the studies of Go- nin (l), Arruga (3), and Vogt (2) appeared in the nineteen thirties. While it is agreed that round, oval, or more irregular holes are due to cystic, degenerative, inflammatory, or atrophic changes of the retina, choroid, or vitreous, possibly with pathological cord formation in the latter, the origin of the horseshoe-shaped tears has not been equally well elucidated. This type of tears occurs isolated or combined with other retinal defects in the named pathological changes of the eye or in the presence of abnormal static con- ditions in the eyeball, e. g. myopia, or following injury. However, these fish-hook-shaped or crescentic tears as well as the other types mentioned above may also be encountered in retinae which appear to be intact on ophthalmoscopy. But whether a pathological cause is visible or not, these tears are characterized almost without exception by the convexity being directed backward and the concavity or base peripherally. The opposite, i. e. the convexity facing the ora, has been described (Gonin, Vogt), but in extremely rare cases. This constant orientation of one type of tear in relation to the landmarks of the fundus is peculiar, and it might be imagined that this constancy could be elucidated if the same type could be induced experimentally. *) Received January 8th 1963. 176 Morphologically, it may be said to be shaped like the new moon with two horns envelopping the lid, operculum, whose base faces the periphery. Despite the decisive importance which must be attached to the retinal tears, our know- ledge is still very deficient. Experiments producing artificial retinal detach- ment have been reported, int. al. by Foulds and Tulloch (4). Studies on ex- perimental retinal tears have been reported by Minsky (5) . Through scleral windows in calf eyes he induced kidney-shaped retinal tears by a special technique. Our experiments comprised about 220 hog eyes. They were performed l/~-ll/t hours after slaughtering, and thereafter the eyes were immersed in a 10/o formalin solution for 24 hours. The eyeballs were cut by a longitudinal or equatorial section. The few microscopic examinations were carried out according to the current methods, using alcohol in increasing concentrations before staining. M E THO DS (1) Blunt injuries to the eyes. Muscles and fat were removed from the eyeball which was then placed, cornea up, on a cork plate and injured by dropping a weight of 300 g from a height of 30 cm. (2) The same procedure after injection of physiological saline into the vitreous until it was as hard as it could become so that maximum dilatation of the retina had been obtained. In order to prevent reflux of the injected solution, the injection was performed through the optic nerve. In these experiments no actual retinal tears were obtained. Only one eye showed, during Experiment 1, a retinal detachment in the form of a highly irregular tear, about 1 cm in length, along the equator. (3) Churning of the vitreous: This was done by insufflation of air, about 1 ml, into the eye. The air was placed centrally in the vitreous body. The idea was to test another elasticity of the ocular structures and to change the vitreous structure which might be imagined to possess special forces. (4) Sucking out a few drops of the vitreous humour through a needle inserted into the optic nerve in order to induce hypotonia and derangement of the vitreous. In these experimental series (3 + 4) we obtained in a few cases retinal detachment which subsided when the eyeball was cut, the retina either returning to its original position or becoming totally detached, but no characteristic tears were obtained. ( 5 ) Saline solution injected subretinally, '/4-'/2 ml. I t was only in a few cases that we could avoid perforating the retina with the needle. No tears of horseshoe shape were obtained. Injury by the needle was avoided in only 5 out of 20 eyes which showed no detachment after the eyeball had been cut. Consequently, the subretinal fluid must have escaped at the edge of the incision. (6) Traction methods. Traction on the fixed eyeball. The traction was exerted at the site of the muscle insertions, either by sutures in the sclera or by placing a needle- holder in a fold of the sclera, one on each side corresponding to the muscle insertions and then exerting maximum traction until one or both holders slipped off. This method appears to be a simple way of obtaining uniform traction, comparable from one eye 177 12' Fig. 1. Total retinal detachment after traction by a suture in the sclera. The retina is attached only at the optic disc. to another. The eyeball had been fastened to a cork plate by needles applied in diametrical sites from the limbus into the plate and by a needle through the posterior pole of the sclera, also into the plate. Suture traction was used in the case of 10 eyes, the needle holder method in the other 10. Total retinal detachment occurred in 2 eyes where the pull was exerted by sutures in 2 diametrical areas of muscle insertion. In one of these eyes the retina remained attached only to the optic nerve (cf. Fig. 1). while in the other it showed a large defect at the site of one suture. It was impossible to demonstrate grossly visible tears in those retinae which were otherwise intact, i. e. 8 eyes. The tears were searched only by gross inspection. To this end we placed the detached retina in physiological saline solution where it was left to spread out and then inspected against a dark background, in some cases with a hand lens. With the needle holder method (10 eyes) we saw in one eye, about 1 mm behind the ora, 2 or 3 very small, transverse, i.e. equatorial defects visible only through the hand lens (after opening the eyeball by a longitudinal section). A photograph of this preparation did not visualize the tears. but on serial section with the microtome one of the tears was hit. It may be seen to represent simple tearing of all the retinal layers (cf. Fig. 2). In this case the edges are regular, not rolled up, perhaps fixed by the surroundings due to their small size. It seems unlikely that the tear could have been caused by the microtome, as the edges. and the surroundings on the whole, were not lacerated. (7) Suction on the vitrous by a suction cup, either after: The suction cup was then placed so as to suck in the backward direction or in the (a) equatorial scleral incision: equatorial plane (10 eyes in each experiment under a). 178 Fig. 2. Photomicrograph of a tear a few mm behind the ora resulting from traction on the sclera by the needle-holder method. All retinal layers are torn. The edges are regular. Fig . 3. Irregular, but arcuate tear resulting from suction on the vitreous. 179 Fig. 4. Tear in the ora caused by suction with a suction cup on the vitreous. In these experiments the inner structure of the vitreous must be partially crushed before a traction by suction can be established. By this procedure we produced 2 tears. one of which was greatly irregular and torn, but arcuate (cf. Fig. 3). The other eye. in which the suction cup was placed in the centre of the vitreous with the suctorial disc forward, i. e. a traction on the vitreous in the backward direction, showed a tear in the retina at the ora serrata, l'ir mm in length and 1 mm wide (cf. Fig. 4). It may be seen that behind the equator the retina was torn all the way. This happened upon longitudinal cutting of the eyeball. Microscopic examination showed the retina to be of normal appearance. In par- ticular, there were no lesions anteriorly. A photomicrograph of the edge (Fig. 5 ) is being included in order to illustrate the inversion of the retina. (b) after a frontal section 2-3 mm behind the limbus: In cases where the lens was preserved, suction was applied to it. In the other eyes the suction cup was applied to the anterior surface of the vitreous and suction was exerted in a forward direction. By this procedure we did not succeed in demonstrating retinal tears after longitudinal cutting of the eyeball. ( 8 ) ExPosure of the retina from the outside. The sclera and choroid were resected, making a window of a suitable extent. This preserves the connection between the retina and vitreous body. The resections were transverse anterior to the equator (where the connection is firmest) and longitudinal from the limbus to a site behind the equator. Thereupon, a suction cup was applied to each corner of the exposed retinal area. By suction using both suction cups at the same time, traction was exerted on the retina in the transverse as well as longitudinal direction. These procedures gave only a few retinal tears, and if so of a highly irregular appearance. 180 Fig. 5. Inversion of the retina, the so-called retinal proversion, from an arcuate ora tear caused by section on the vitreous. If, before the named traction procedure, a small incision of 1 mrn is made at right angles to the direction of the pull, the edges will bc seen in a few cases to be bent forward at one or both corners of the incision. This was observed in 2 out of 10 eyes in which the section had been made slightly in front of the equator during simultane- ous antero-posterior traction. The suction exerted by the suction cup was continued until1 it slipped off (cf. Figs. G and Ga). In the other eyes of this series, treated by traction from side to side, i. e. equatorial traction, and incision at right angles to the pull, the corners of the edges did not in any case bend up to any of the sides, but in one case the retina rolled up to one side. It is difficult to assess the microscopic appearances of these tears at the sites of the bent-up corners, partly because, unlike premortal retinal tears, these lesions cannot be distinguished from artefacts and partly because it was a question of isolated retinae. (9) On vertically or frontally cut eyeballs, in which the vitreous was removed without destroying the retina, the same attempts were made to tear the retina between 2 suction cups. 181 Fig. 6. Fig. 6a. One corner of an equatorially cut tear in the retina - exposed from the outside - bending forward on antero-posterior traction. Fig. 7 . Retinal tear produced by a knife. The sclera may be seen at the bottom of the tear. In other words, the choroid has been included in the incision. The choroid + sclera were used as a foundation. It was found that the retina was very easily torn where the suction cup was applied, although crushing by pressure against the firmer foundation was carefully avoided. In these experiments we found no characteristic tears. On the whole, only a few tears were found, because the retina burst a t the sites of suction before an actual traction could be established. In the experiments from the outside, through a window in the sclera, where the choroid is easily separated from the retina, few lesions were found at the sites of suction. This is no doubt because the connection with the vitreous was preserved, the retina being supported by the soft, partially adherent vitreous during the local out- ward suction. Incidentally, the retinal area between the two suction cups is stronger than might be assumed. Especially with traction on the outside several attempts had to be made before the pull was sufficient, because the suction cup slipped off before a tear was induced. (1 0) Cutt ing methods: These consisted in equatorial and meridional retinal incision by a cataract knife into the unopened eyeball. To this end. the knife was introduced through the sclera and a tear was made into the retina on the opposite side. Incisions were made anterior and posterior to the equator. 183 It was imagined that the incisions might assume various shapes in different meri- dians because of inherent anatomical tensions. Of course, this invariably resulted in a tear, usually of a linear course, but at times gaping more or less. In one case we obtained a tear of a beautiful arc-shape (cf. Fig. 7). On the photograph the white sclera may be seen at the bottom of the tear, i. e. the incision has included the choroid. In the other 19 eyes where the choroid was included in the incision there was no case of such a shape, all the tears being linear. As may be seen from the above referred experiments no reliable method for producing artificial tears by blunt methods could be indicated. Even by cutting methods the clinically known shapes of retinal tears were rarely obtained. Before we had practised the technique of exposing the retina from the out- side, we tried to make an incision through the choroid + retina from the outside, i. e. after having resected only the sclera. Traction in various directions in relation to the small incision in the choroid + retina nearly al- ways resulted in circular holes, the retina being rolled up along a major or minor part of the circumference of this choroid hole (cf. Fig. 8). I t must be assumed that a defect in the choroid, perhaps due to the arcuate vortex veins. acquires this circular shape because of considerable elasticity in the tissue. The fact is that a very small hole made by the tip of a cataract knife may be seen to dilate in a circular manner, when the choroid is pulled by two suction cups or when simple traction is applied to the sclera. Fig. 8. Section through choroid + retina. The retinal tear assumes its shape from the round choroid hole. Cf. text. 184 ' When the hole has attained a certain size and the traction is continued, the contours of the hole burst, but the edges remain arcuate, one-half or one- quarter of a circle. Even when the incision includes only the choroid there will be round holes having the retina as a *floor*. When concentric defects occur in the choroid and retina at the same time, the retinal hole - owing to the adhesion to the choroid - must assume a shape conditioned by the latter. The choroid may then, when detached from the sclera as in the present experiments, decide the shape of a defect in a concentrically corresponding site in the retina, presumably because of the greater strength of the tissue, its elasticity, and perhaps its more pronounced splitting pattern. Thus, the choroid may be among the factors which under certain circum- stances influence the splitting of the retina. However, retinal defects, in particular the horseshoe tears, occur in the living eye regardless of the venous pattern in the horoid, and incidentally the ophthalmoscope nearly always shows an intact choroid below a retinal tear. Presumably, the horseshoe tear is the result of several factors acting at the same time. It may be imagined that the retina possesses special properties which are in many cases influenced by the vitreous or changes in the vitreous. As far as the retina is concerned, the occurrence of the horseshoe tear might be explained as a result of peripheral divergence of the nerve fibres and vessels, the edge of the lid deviating towards the ora representing the site of least resistance (Vogt 2). Arruga (3) advanced a similar hypothesis, emphasiz- ing the relatively rare occurrence of a horseshoe tear closest to the ora where nerve fibres are few or absent. True, the radial course of the tear might be explained on the basis of the course of the nerve fibres, but the transverse tear at the site of the convexity must occur across the nerve fibres. This has been mentioned by Bartels (6) who emphasized the rare occurrence of torn vessels at the site of the tear. The vessels, on the other hand, are often seen to be intact in the periphery of a horseshoe tear. At times, the tear may be situated at the bifurcation of the vessel, or a vessel may run across the tear. Maybe the retina is in some areas dilated by the course of the vessels. And perhaps, such tensions manifest themselves rather in the periphery than to- wards the centre, where the layer of nerve fibres is denser and the vessels converge. In this connection Ehlers (7) reflections on the vascular pattern of the retina may be of interest. According to this author the blood current in the wall of a sphere may cause tractions on the retina. A t any rate, pathological vessels with perivascular degeneration or thinning of the retina are contributory causes in cases exhibiting holes crossed by a vessel or of holes along one or both sides of a vessel (Fuchs 8). 185 But vascular changes cannot be the sole cause of the hook-shaped retinal tear. That normal vessels may influence the retina was according to Bartels (6) apparent from the predilection of such tears for the upper and lower temporal quadrants, where the vesaels are larger than on the nasal aspect. However, the tears are far more common in the upper than in the lower half of the retina, so other factors must be at play. The vitreous is most movable superiorly, where it may, by reason of gravity, exert the greatest traction upon the retina (Duke Elder 9). Opercular formation and the relation of the operculum to the vitreous have been the subjects of much theoretical speculation. Leber (lo), Nordensson (12), and Gonin (1) have emphasized the inversion of the operculum towards the vitreous, attributing it to cord formation in the vitreous similar to the occurrence of the other types of retinal tear in the presence of proliferative or haemorrhagic changes in the vitreous or retina. Ophthalmoscopy and slit-lamp inspection, however, far from always reveal signs of cord formation. Frequently, the vitreous is even liquid to a greater or lesser extent, often detached from its connection with the retina posteriorly. According to Vogt (2, 11) this inversion of the operculum must be due to an elastic property in the retina proper. In isolated animal and human retinae, the same phenomenon could be reproduced by inducing tears. This so-called *retinal proversionu has been demonstrated by a number of other investigators, and it was observed by us in the present experiments. It tends to keep a retinal tear open and thereby to produce detachment, but it does not afford the sole explanation of the horseshoe shape. It might be imagined, that in analogy with skin, cartilages and other tissues. including the cornea (Ehlers 13), the retina may have an inherent charac- teristic tissue tension which causes a cleavage in certain directions and of various shapes. The possible lines of splitting then indicate the directions in which the tissue is strongest. Possibly, the internal limiting membrane is a factor in the named retinal proversion and might perhaps condition a characteristic cleavage pattern. This membrane is firmly adherent to the retina where it is formed and kept fixed by outriders from the Muller cells (Polyak 14, Hogan and Zimmermanii 15). It is loosely attached to the hyaloid membrane posteriorly, while ante- riorly towards the ora serrata there are firmer adhesions between the in- vesting membranes. This firmer adhesion increases with advancing age and in the event of inflammatory or degenerative changes. Another factor might be the rugged contour of the ora serrata. This festoon- like attachment of the retina anteriorly might cause a similar arrangement or configuration of fibers and cells in the posterior aspects of the retina. The attachment at the ora cannot be said to form an even transition to the 106 ciliary body, at any rate not as far as the movability against the underlying structures is concerned. Indeed, the retina may be torn to a major or minor extent, at the transition to the ora, as observed in one eye in our experi- ments (7 a). I n the approximately round vitreous - owing to its jelly-like nature - characteristic elastic forces of fluctuation may be elicited as demonstrated by Lindner (16) in experiments using flasks filled with gelatin. In a spherical jelly mass these forces may also act upon the retina. All considered, the crescent tear must arise through the collaboration of 3 number of different traction and pressure factors. CONCLUSION By various procedures we tried to injure the retina of hog eyes, and in some cases succeeded in inducing artificial tears. I t was not possible to find a reliable method for producing retinal holes by blunt measures, but within the individual experimental series a number of tears were produced. I n 2 out of 10 eyes with incised tears there was a tendency to a forward direction of an equatorial tear, indicating that in the vitreous or in the retina there may be forces or tensions tending to lend a retinal defect an arcuate course. The microscopic examination of the retinal tears is illustrated in the figures which, however, afford no explanation of the mechanism. A tear of the ora was induced in an eye where traction was exerted on the vitreous in the backward direction. REFERENCES 1. Gonin 1.: Le dccollement de la retine. Lausanne 1934. 2. Vogt A.: Die operative Therapie und die Pathogenese der Netzhautablosung. 1936 3. Arruga H.: Detachment of the retina. Barcelona 1936. 4. Foulds W . S. and Tulloch C . G.: Research on retinal detachment. (British Journal Preliminary report in Thirteenth Annual Report of the London Institute of Ophthal- 5. MinsRy H.: Experimental Holes in the retina. Journal of Mount Sinai Hospital 6. Bartels M.: Klin. Monbl. f. Augenheilkunde 1936, vol. 96, pag. 1-9. 7 . Ehlers H.: Acta Opht. Scand. 1954: Streamlines within a waterfilled globe. 8. Fuchs A.: Klin. Monbl. f . Augenheilkunde 1937, vol. 98, pag. 145-162. 9. Duke-Elder Stewart: Textbook of Ophthalmology, vol. 3, pag. 2881. of Ophthalmology 1961). mology ass. with Moorfields Eye Hospital. New York, 1942. 187 10. Leber Th.: Uber die Entstehung der Netzhautablosung. Bericht iiber die viei- zehnte Versammlung der Ophthalmologischen Gesellschaft, Heidelberg 1882. 11. Vogt A.: Klin. Monbl. f. Augenheilkunde, vol. 96, pag. 10-15, 1936. 12. Nordenson E.: Die Netzhautablosung, Wiesbaden 1885. 13. Ehlers H.: Corneas kar og struktur. With an English summary). Copenhagen 1929. 14. Polyak S. L.: The Anatomy and Histology of the retina in man, ape and monkey 15. Hogan and Zimmermann: Ophthalmic Pathology 1952. 16. Lindner K . : Klin. Monbl. f. Augenheilkunde 1933, vol. 90, pag. 289-307. 1941. 188