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Fundus Appearance in Normal Eyes
FUNDUS APPEARANCE IN NORMAL EYES II. T H E STANDARD PERIPHERAL FUNDUS AND DEVELOPMENTAL VARIATIONS U T H A I R U T N I N , * M.D.,
AND CHARLES L. SCHEPENS,
M.D.
Boston, Massachusetts The peripheral fundus is defined as the area of the fundus anterior to the scierai en trances of the vortex veins. It is subdivided into an equatorial and an oral region. In this presentation, the oral region is studied with particular care as it is the least known clini cally and has the greatest tendency to ex hibit variations. Every visible detail of the peripheral fun dus in 102 subjects was recorded on a fun dus chart. Examination of the fundus pe riphery could not be completed in 59 other subjects because of hypersensitivity to the bright light of the ophthalmoscope, inade quate transparency of the ocular media or insufficient pupillary dilation. More than twice as many males as females were hyper sensitive to light, a statistically significant difference. The ophthalmoscopic study of 102 subjects was correlated with the dissec tion of 11 eyes supplied by the Boston EyeBank. In the study of 204 fundi, no significant difference was found between right and left eyes or between sexes except where specifically mentioned. Some of the subjects showed changes in the posterior fundus. For instance, sclerosis of the retinal vessels, diminished or absent foveal light reflex and macular mottling with normal visual acuity were seen in a few cases and interpreted as resulting from aging. Medullated nerve fibers were found near the optic disc in both eyes of one subject. Benign melanomas of the pigment epithelium noted in the posterior From the Department of Retina Research, Retina Foundation, and the Retina Service, Massachusetts Eye and Ear Infirmary. This work was supported by research grant B-3489 of the National Institute of Neurological Diseases and Blindness, United States Public Health Service. * Fellow of the Retina Foundation (1957-1963); Fellow in Ophthalmology, Massachusetts Eye and Ear Infirmary (1957-1961).
fundus will be discussed in a subsequent pub lication. These changes were considered de velopmental variations in normal subjects. Finally, the posterior fundus showed isolated drusen or groups of drusen in nine eyes of seven subjects; small intraretinal hemor rhages were observed in both eyes of two subjects; and a small area of superficial chorioretinal atrophy (less than 0.25 disc diameter) was found in one eye of four subjects. In this presentation, an attempt is made to describe the standard peripheral fundus and to relate observations about its develop mental variations. T H E STANDARD PERIPHERAL FUNDUS
The standard peripheral fundus is defined as one which shows no developmental varia tions, signs of aging or abnormalities. It differed from the posterior fundus in that the retina was thinner as estimated with the ophthalmoscope by the distance between the retinal vessels and the surface of the pig ment epithelium. In the periphery, it was impossible to differentiate between arterioles and venules on the basis of size, color or pattern. The only practical method of iden tification was to trace the vessels back to the posterior fundus. The retinal arterioles and venules did not course together but were evenly distributed through the fundus periphery. Most of them became very small and disappeared before reaching a distance of 0.5 disc diameter from the ora serrata. Arterioles disappeared first, while venules extended closer to the ora serrata. Occasionally, a large vein ex tended to 0.5 disc diameter from the ora serrata, then ran parallel to it for one to three disc diameters and finally turned back toward the posterior pole for 1.0 to 1.5 disc diameters before disappearing. The pigment
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epithelium generally appeared more granu lar in the periphery than in the posterior fundus. In the ora serrata region, mild degenera tive changes were frequent in a strip of ap proximately 0.25 to 0.5 disc diameter poste rior to the ora serrata. In this area, the ret ina became opalescent and marked by one to three rows of small cystoid cavities. The underlying pigment epithelium was defi nitely darker and more granular. At the ora serrata, the photosensitive retina stops abruptly and is continued by the ciliary epi thelium which appears considerably thinner than the retina. When the peripheral edge of the retina showed cystoid degeneration it was thickened. As the pars plana ciliaris was more deeply pigmented than the periph eral retina, the choroidal pattern was ob scured by that of the pigment epithelium. Occasionally, the pigment epithelium in the pars plana ciliaris showed discrete black spots of variable size and irregular con tours. In infants, the ora serrata was found to form a slightly wavy line which was symmet^ rical all around the fundus and lay close to the posterior border of the ciliary processes. During the early years of life, the pars plana ciliaris grows asymmetrically, becom ing wider temporally than nasally, and the nasal ora serrata forms scallops. The concave side of each scallop is nearly always turned anteriorly. Sometimes, how ever, the scallops appeared inverted with a slightly concave side turned posteriorly. The teeth and bays formed by scalloping of the ora serrata became obvious at about onehalf hour temporal to the 12-o'clock meridi an and extended nasally to one-half hour on the nasal side of the 6-o'clock meridian. The estimated length of the ora serrata teeth on the nasal side varied from 0.25 to 1.0 disc diameter, averaging 0.75 disc diameter and rarely exceeding 1.5 disc diameters. On the temporal side, bays were replaced by a wavy line and teeth were narrow and short or sometimes absent.
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In the posterior half of the pars plana ciliaris, the nonpigmented epithelium ap peared transparent, avascular and had a smooth glossy surface. It occupied a ringshaped area one and one-third disc diame ters wide. On dissection, it was adherent to the vitreous base which extended from the ora serrata anteriorly for approximately one disc diameter. With the ophthalmoscope, the vitreous base and its attachment to the ora serrata and ciliary epithelium were rarely visible. In seven eyes of six subjects, some sectors of the anterior limit of the vitreous base were visible as well as the adjacent hy aloid membrane (fig. 1). The latter ap peared as a thin membrane located in front of the surface of the pars plana ciliaris. It originated from the inner surface of the ciliary epithelium approximately one disc diameter anterior to the ora serrata and formed a faint ridge in the pars plana cilia ris over one and one-half hours to seven hours around the globe. Anteriorly, it disap peared beyond ophthalmoscopic view. The most frequent locations where it was visible were between the 11- and 1-o'clock and be tween the 5-and-7-o'clock positions. Findings by other authors. The develop ment of the ora serrata is incomplete at birth and continues to develop in early life. Its adult appearance is reached at the ap proximate age of seven years. 1 ' 2 Degenera tive changes begin near the ora serrata as early as the neonatal period. There are about 48 ora teeth per fundus and most of them correspond in position to the intervals between the ciliary processes.1 All the irreg ularities in the development of the corona ciliaris are reflected in the ora serrata. There seems to be no entirely satisfactory explanation for the development of serra tions at the ora serrata. In cross section, the teeth of the ora serrata form a spur of loose tissue which projects into the vitreous cavi ty. Its edges are undermined and are not ad herent to the ciliary epithelium. Adhesion to this epithelium exists only along the longitu dinal axis of the tooth. 1
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Fig. 1 (Rutnin and Schepens). Diagram representing the anterior limit of the vitreous base and the adjacent anterior hyaloid membrane sometimes visible in the extreme fundus periphery. (H) Anterior hyaloid attached to the middle of the pars plana ciliaris. (OS) Ora serrata. (R) Peripheral retina. (CP) Posterior extremities of the ciliary processes. OS
CP
bilateralism. In nearly all instances, varia DEVELOPMENTAL VARIATIONS A developmental variation of the periph tions in the teeth of the ora serrata ap eral fundus was assumed to be present when peared in association with deep ora bays. a structure in the retina or ciliary epitheli An overwhelming majority of these varia um appeared other than normal in size, tions were located nasally, near the horizon shape or texture and was found in a tal meridian (fig. 2 ) . Variations of bays. The usual contour of significant percentage of the subjects as sumed to be normal. Variations were so fre a bay was finely irregular and wavy but, in quent that at least one type was noted in a deep bay, the contour was perfectly 59.8% of 102 subjects (46.6% of the eyes). TABLE 1 The variations observed were divided into APPEARANCE OF THE PERIPHERAL FUNDUS IN three categories : ( 1 ) variations of the bays NORMAL EYES DEVELOPMENTAL VARIATIONS: 204 EYES IN 102 SUBJECTS and teeth of the ora serrata, (2) meridional retinal folds and (3) granular tissue. These N f Percentage of three categories of variations tended to £,£ Total No. Ey* of Eyes occur in the same eye with a significant fre quency (table 1). Occurred alone VARIATIONS OF BAYS AND TEETH OF THE ORA SERRATA
Variations of size and shape include: deep bays, giant teeth, forked teeth, ring teeth and bridging teeth (table 2 ) . Over 30% of the subjects examined showed at least one of these variations. When multiple, they tended to occur adjacent to each other. Deep ora bays were at least six times more frequent than any of the other ora serrata variations and had a significant tendency to
I. Variation of bay and tooth II. Fixed meridional fold III. Granular tissue
14 18 24
14.7 18.9 25.3
Occurred in combination I and II I and III II and III I and II and III
8 13 7 11
8.4 13.7 7.4 11.6
TOTAL
95
100.0
At least one developmental variation was present in 95 of 204 eyes (46.6%) and in 61 of 102 subjects (59.8%). The tendency for variations to occur in combination indicates that there exists a statistically significant relationship between them.
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TABLE 2 APPEARANCE OF THE PERIPHERAL FUNDUS IN NORMAL EYES FREQUENCY OF VARIATIONS OF ORAL BAYS AND TEETH: 204 EYES IN 102 SUBJECTS
Deep bay Giant tooth Forked tooth Ring tooth Bridging tooth
No. of Eyes
Percent
No. of Subjects
Percent
45 7 S 4 2
22.1 3.4 2.5 2.0 1.0
30 5 4 3 2
29.4 4.9 3.9 2.9 2.0
smooth as if it had been pulled taut. A deep bay was two to four times wider and deeper than adjacent bays. As the size of regular bays varied in different individuals, the ac tual dimension of deep bays was also vari able. As a rule, the teeth bordering a deep bay were somewhat larger than adjacent teeth. One to five deep bays per eye, or a total of 58 deep bays, were found in 45 eyes of 30 subjects. The deep bays were found singly, in adjacent pairs or triplets. A single deep bay was located in the upper temporal quadrant of three eyes. The other 55 were near the horizontal meridian, 50 (91%) na sally and five (9%) temporally. They were located near the course of a visible long cili ary nerve and artery. In 11 of 45 eyes showing deep bays (24.4%), other changes such as pearls, retinal breaks or latticelike degeneration were present. Variations of teeth. Except for its size, a giant tooth appeared similar to a regular tooth (fig. 2-A). Its length extended beyond the middle of the pars plana ciliaris and al most touched the ciliary processes. Giant teeth were found exclusively in eyes with deep bays. One or two giant teeth per eye or a total of 13 giant teeth appeared in seven eyes of five subjects. Eleven of the 13 giant teeth were adjacent to horizontally located deep bays ; the other two were between reg ular bays in the upper nasal quadrant. A forked tooth had a bifurcated tip and was larger than average (fig. 2-B). Five forked teeth, all adjacent to horizontally lo cated deep bays, were found in five eyes of four subjects. Four of the teeth were so large that they were also classified as giant
teeth. One of the five forked teeth was so deeply bifurcated that the bottom of the fork reached almost as far as the base of the tooth. A ring tooth was formed by two adjacent teeth leaning toward each other so as to form a ring enclosing a bay. Ring teeth were larger than average. Six ring teeth were noted in four eyes of three subjects. All except one were in eyes with deep bays. The three stages of ring formation are: (1) open ring, (2) closed ring and (3) holein-the-tooth. An open ring was noted twice ; the tips of adjacent teeth did not quite touch each other (fig. 2-F). A closed ring was also noted twice; the tips of adjacent teeth had joined. Each tooth forming a closed ring was large (fig. 2-D). A hole-in-the-tooth was noted twice; two adjacent teeth were solidly merged together in a single wide tooth (fig. 2-E), and there was a small cir cular area of pars plana ciliaris forming an island in its base. This island, which was much smaller than one in a closed ring, superficially resembled a retinal hole. A bridging tooth was a cordlike structure extending from the peripheral retina to the anterior portion of the pars plana ciliaris (fig. 2-C). Except for its anterior extremi ty, it was detached from the ciliary epitheli um and appeared curved like a bow with its convexity toward the center of the globe. It seemed to be degenerated and cystic. A bridging tooth, not adjacent to other varia tions, was found in one eye of two subjects. All variations observed in teeth seemed to be interrelated except for bridging teeth. It is possible that the latter should be classified
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as a morphologic anomaly instead of a nor mal variation. MERIDIONAL RETINAL FOLDS
A meridional retinal fold is a permanent dry fold* of 0.5 to 1.5 disc diameters in length involving all retinal layers. As a rule, such a fold begins at the ora serrata and runs posteriorly and perpendicularly to it in a meridional direction. The surface of a me ridional retinal fold appeared irregular, lacked transparency and was finely wavy as though the fold were covered with microcysts. In most cases, the surrounding retinal area showed cystoid degeneration (figs. 2-B and D and 3-B, C and E ) . The adjacent vit reous and pigment epithelium appeared un changed. Meridional folds were found in 44 eyes of 28 subjects (27.5%) and were bilateral in a statistically significant number of in stances. Of 87 folds, 71 (82%) were poste rior extensions of ora serrata teeth (figs. 2-D and 3-A, C, D and F ) and 16 (18%) were posterior to ora serrata bays (figs. 2-B and 3-B and E ) . The number of folds per eye varied from one to 10, but 59% had only one fold. The posterior end of 10 folds was adjacent to granular globules (fig. 3-A C and F ) ; six other folds showed one of * The term "dry fold" is applied to a retinal fold which is not accompanied by retinal detach ment.
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the following changes: chorioretinal degen eration located either at the posterior ex tremity or on one side; incomplete or com plete retinal hole on the side and a granular patch at the posterior end; a globular mass on its course; a pearl on its side or on its anterior extremity. In one case (fig. 3-D), a piece of the meridional fold appeared to have broken off ; it was attached to the cor tex of the vitreous gel and cast a shadow on the fundus. Fixed meridional retinal folds were found significantly more often nasally than tempo rally and in the upper nasal quadrant more often than in the lower (table 3). Their fre quency near the nasal horizontal meridian was remarkable. Discussion and findings by other authors. The nature of meridional retinal folds is not clear. The folds located over the teeth of the ora serrata as well as the teeth themselves and the bays of the ora serrata are not visi ble in the newborn. Meridional folds, when present, become more conspicuous with age. The bays of the ora serrata may result from a pull exerted on the retina in a posterior direction. If such were the case during the postnatal development of the ora serrata re gion, the ora teeth would form because the retina is adherent to the pigment epithelium at the anterior extremity of the teeth. The meridional folds would then result from re dundant retinal tissue caused by stretching
Tfftl r
Fig. 2 (Rutnin and Schepens). Morphologic variations of the ora serrata region in normal fundi. (A) Nasal periphery with marked cystoid degeneration near horizontal meridian, giant tooth, and deep ora bay over long ciliary nerve. (B) Temporal periphery with marked cystoid degeneration near horizontal meridian, deep ora bay over long ciliary nerve, with forked tootn above, and below, a tooth with a pearl at its base. A second pearl is visible at the anterior end of the inferior tooth; above, small meridional fold on the side of an ora bay. (C) Upper temporal periphery with a bridging tooth covered with cystoid degeneration and almost in contact with a ciliary process; above, granular globule; below, white granular patch with large cystoid cavity on its anterior border. (D) Nasal periphery near horizontal meridian, with marked cystoid degeneration; ring tooth (closed ring) over long ciliary nerve; below, small meridional fold over ora tooth. (E) Temporal periphery near horizontal meridian; deep ora bay over long ciliary nerve; the tooth above the deep bay had part of its t i p broken off; ring tooth (hole-in-the-tooth) above. (F) Nasal periphery, near horizontal meridian, with ring tooth (open ring) and deep ora bay over long ciliary nerve. In the next bay, below, two tiny tags. A l l paintings are exact reproductions of individual fundi.
Fig. 3 (Rutnin and Schepens). Morphologie variations of the ora serrata region in normal fundi. (A) Upper nasal periphery with meridional fold over ora tooth and granular globule on its posterior border. (B) Upper nasal periphery with marked cystoid degeneration and meridional fold in the middle of an ora bay. (C) Upper nasal periphery with marked cystoid degeneration and meridional fold over a giant tooth which is connected with a ciliary process; three granular globules on the disc side of the meridional f o l d . (D) Nasal periphery with meridional fold over ora tooth; a piece of the tooth was torn and is attached to the vitreous cortex; tiny tag in the middle of an ora bay, above the meridional fold. (E) Nasal periphery near the horizontal meridian; deep ora bay over long ciliary nerve; a meridional fold, in the middle of the deep bay, is surrounded by cystoid degeneration. (F) Nasal periphery with small meridional fold over ora tooth and three granular globules. A l l paintings are exact reproductions of individual fundi.
Fig. 4 (Rutnin and Schepens). Granular tissue in the periphery of normal fundi. (A) Three granular patches in the inferior periphery. (B) Five granular patches in the nasal periphery. (C) Granular patch, in the inferior fundus periphery, was torn off the retina causing an incomplete retinal tear; a tiny tag was partially torn from the retina, causing a small in complete tear. (D) Nasal periphery with granular globule, near the long ciliary nerve, in an area of white with pressure. (E) Nasal periphery with marked cystoid degeneration; granular globule was partly torn from retina, causing two incomplete retinal tears. (F) Temporal periphery wih granular globule surrounded by fine line of pigment. All paintings are exact reproductions of individual fundi.
B
H
Fig. 5 (Rutnin and Schepens). Shapes of granular globules found in the periphery of normal fundi. ( A and B) Pyramidal shapes. (C and D ) Columnar shapes. ( E ) Club shape. ( F ) Cystic globule. (G and H ) Irregular shapes.
Fig. 6 (Rutnin and Schepens). Granular tags in the periphery of normal fundi. (A) Upper nasal periphery with marked cystoid degeneration on the disc side of which early retinoscnisis is visible; vascularized granular tag with tiny pigment ring. (B) Nasal periphery with two white granular tags. (C) Inferior periphery with cystic granular globule and granular tag to which a visible vitreous band is attached; smaller granular tag at the base of ora tooth, with incomplete retinal break. (D) Inferior periphery with peel-shaped granular tag surrounded with incomplete retinal break. All paintings are exact reproductions of individual fundi.
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TABLE 3 APPEARANCE OF THE PERIPHERAL FUNDUS IN NORMAL EYES LOCATION AND NUMBER OF MERIDIONAL FOLDS: 204 EYES
Nasal Side
Temporal Side
Upper
Horizontal
Lower
Upper
51
IS
14
4
of the retina in an anteroposterior direction. In cases of subclinical retinal detachment, Schepens3 noted that retinal breaks tended to occur adjacent to the posterior extremity of meridional folds. The frequency of me ridional folds (26%) in his series of 102 eyes with subclinical retinal detachment4 was similar to that in this series of normal sub jects (27.5%). This may indicate that the existence of meridional folds does not in crease the risk of a subclinical retinal de tachment; however, if this condition de velops in an eye with meridional folds, the retinal breaks tend to be located near the folds. Teng and Katzin 5-0 have described me ridional folds located at the ora serrata, most often on the nasal side, in the eyes of babies. They consider them as developmen tal anomalies, and their pictures show that these meridional folds are associated with variations in the ora bays. In all their pic tures the folds were in the middle of an ora bay, a type of fold representing 18% of the folds we have observed. Teng and Katzin show no meridional fold over an ora tooth. It is probable, therefore, that meridional folds seen in adults are of two different kinds : those coinciding with ora teeth are acquired after birth and those in the middle of the ora bays develop before birth. In our findings, the rate of occurrence of meridio nal retinal folds was about evenly distributed among subjects whose ages ranged from 12 to 81 years. Meridional folds, therefore, must develop at an early age and no new folds seem to appear thereafter. GRANULAR TISSUE
The ophthalmoscopic appearance of this
Horizontal —
Lower 3
Total 87
tissue was that of an opaque whitish gray spot with a dull granular surface which pro truded slightly at the inner surface of the retina (figs. 2-C and 3-A, C and F and 4 ) . One to nine areas were noted per eye in 55 eyes of 41 subjects indicating a significant tendency to bilateralism. As the affected subjects were evenly distributed among the age groups, the granular areas must have been present early in life without multiply ing during later years. Areas of granular tissue were divided into morphologic types : patch, globule and tag or floater. The last category was divided in two groups: tags and floaters whose structure could be distinguished by indirect ophthalmoscopy, and those which were so tiny that their structure could not be made out. All types of granular tissue had common characteristics. They were found signifi cantly more often in the posterior oral region than in other areas of the fundus periph ery and were never seen in the posterior portion of the equatorial region (table 4 ) . A significant preference for the nasal half of the globe was evident. Within the nasal half, the upper nasal quadrant was affected significantly more often, except for regular and tiny tags or floaters (table 5). Granular tissue was often associated with a meridio nal retinal fold or a retinal vessel. Granular patch. The granular patch ap peared as a slightly raised plaque on the inner surface of the retina. Its border was irregular but well outlined. It had a more or less round shape and its diameter varied from about one-eighth to one-third disc di ameter; sometimes the patch was elongated. It resembled an isolated area of cystoid de-
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TABLE 4 APPEARANCE OF THE PERIPHERAL FUNDUS IN NORMAL EVES CIRCUMFERENTIAL LOCATION OF GRANULAR TISSUE: 204 EYES
Type of Granular Tissue Patch Globule Tag or floater Tiny tag or floater TOTAL
Anterior Oral Region*
Posterior Oral Regionf
Anterior Equatorial Region Î
Posterior Equatorial Region §
—
66 17 14 96 193
12 7 7 7 33
— — — — —
2 2 13 17
Total 78 26 23 116 243
* Anterior to ora serrata line. t Posterior to ora serrata line. j Anterior to equator. § Between equator and scierai entrances of vortex veins.
generation except for its opaqueness (figs. 2-C and 4-A and B). One to eight granular patches per eye were noted in 28 fundi of 19 subjects—a significant tendency to bi lateralism. Of 78 granular patches, 27 (34.6%) were either close to a meridional retinal fold or along a retinal vessel ; in one instance, a granular patch appeared to have shrunk causing the formation of an incom plete retinal break (fig. 2-C). Granular globule. This was an irregular mass of one-twelfth to one-fifth disc diame ter protruding at the inner surface of the retina (figs. 3-A, C and F and 4-D, E and F ) . Some globules were elongated like a col umn or club (fig. 4-D). The retina and pig ment epithelium under and around the mass appeared degenerated and hyperpigmented (fig. 4-F). A few coarse and taut vitreous strands were seen attached to the top of club-shaped globules. In one instance, a glo bule seemed to have shrunk causing the for mation of two incomplete retinal holes (fig.
4-E). In another case, a relatively large, clear, fluid-containing cyst was seen to be partially embedded in a globule (fig. 5-F). The various shapes of globules encountered are schematically represented in Figure 5. One to three globules per eye were noted in 19 fundi of 18 subjects. Of 26 globules, 11 (42.3%) were found along retinal ves sels. Granular tag or floater. This type of granular tissue appeared to belong to one of the first two types but was modified by vit reous traction (fig. 6 ) . It seemed shrunken or curled and, in some cases, was so markedly distorted that it was impossible to be sure of its original shape. In one in stance, a granular tag showed signs of orga nization with new-formed blood vessels in it. All tags and floaters had the common characteristic of being a definite piece of de generated tissue which was pulled into the vitreous cavity. The granular tag was an elongated strand
TABLE S APPEARANCE OF THE PERIPHERAL FUNDUS IN NORMAL EYES QUADRANTIC LOCATION OF GRANULAR TISSUE: 2 0 4 EYES
Type of Granular Tissue Patch Globule Tag or floater Tiny tag or floater TOTAL
Nasal
Temporal
Upper
Lower
Upper
Lower
43 16 8 69 136
18 6 9 73 106
S 3 4 13 25
12 1 2 26 41
78 26 23 181 308
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of tissue about 0.25 disc diameter in length which protruded from the inner surface of the retina (fig. 6-A and B ) . It was distin guished from even smaller tags whose tex ture could not be identified with the indirect ophthalmoscope. The granular tag was gen erally attached to an area of degenerated retina. Fifteen granular tags were noted in 12 fundi or 12 subjects ; four were located along retinal vessels (fig. 6-A, B) ; none ap peared related to meridional folds. The granular floater generally retained its original character of patch or globule. It was either partially or completely torn off the retina. Torn tissue formed either a sin gle piece (fig. 6-C), or it was fragmented; sometimes it looked like a peel (fig. 6-D). Its area of origin always showed a coarse degenerated retina which, in certain cases, appeared as an incomplete or complete reti nal break (fig. 6-C). One granular floater was noted in eight fundi of eight subjects. Tiny tag or floater. A large number of tags and floaters observed were so small that their structure could not be distin guished by indirect ophthalmoscopy (figs. 2-F, 3-D and 4-C). They did not appear to be related to granular tissue and, in most eyes, were multiple with an average of nine per eye. Ninety-eight eyes of 64 subjects were affected—a significant tendency to bi lateralism. Affected individuals were of all ages, but when they were divided by age groups, those above 40 years of age showed about three times more tiny tags and float ers than the younger subjects. Therefore, it is probable that many of these tiny struc tures are degenerative and differ from the larger tags and floaters of granular nature. The tiny tags and floaters were over four times more frequent in the posterior oral region than in any other area of the globe ; they were not seen in the posterior equatori al region. In many cases, they were located along the ora line itself. The nasal side was over four times more often affected than the temporal side without preference for a
851
quadrant. About one half were tags with one end attached to the internal layers of the retina and the other end protruding into the vitreous cavity. Tiny tags were always elongated in a meridional direction. The other half were floaters lying in the vitreous cavity close to the inner layer of the retina. Most of them looked gray-white but a few were pigmented. In the majority of the eyes affected, tiny tags and floaters did not appear to be re lated to any other visible fundus anomaly. In five of 98 eyes, a tiny tag had been pulled from an area of chorioretinal degeneration causing a minute incomplete retinal tear without detachment (fig. 4-C). In six eyes, tiny floaters were seen over areas of lattice like retinal degeneration. The surface of the underlying retina looked fluffy but no defect was found in the retina to account for the floaters. In seven eyes, tiny tags and floaters were seen over the surface of cystoid retinal de generation. There were 12 floaters overlying broken inner walls of cystoid cavities, and in three instances, the broken wall showed a tiny tag attached to its anterior border (fig. 4-C). It is probable that in all of these cases, the resulting retinal tears were incom plete. In seven eyes, small tags and floaters were overlying areas of retinoschisis but no defect could be seen in the inner layer of the retina. In 11 eyes, pigmented tiny tags were seen at the ora serrata; they were clubshaped and protruded into the vitreous cavi ty. Generally, a group of them lay anterior to an area of chorioretinal degeneration. Discussion and findings by other authors. Granular tissue and rosette formation have been described in microphthalmic and in colobomatous eyes ; they have also been repro duced experimentally,8 "Microanomalies" which have been described histologically in apparently normal eyes7 may well represent granular tissue. In autopsy eyes5"a,b,c'8 granular patches
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were observed in the inner layer of the pe ripheral retina, mostly on the nasal side, and within five mm of the ora serrata. The inci dence at autopsy was quite similar to that of our clinical findings. The size of the lesions varied from a few micra to 0.5 mm by 2.5 mm; they were elongated in a meridional direction. Histologically, this tissue showed prolif eration and degeneration of the nonpigment ed epithelium of the pars plana ciliaris, gliosis and pigment proliferation with degenera tion of the normal retinal elements. Epithelioid cells found in this tissue were thought to be either metaplastic neuroepithelium re sulting from irregularity in the development of the retina or cells from degenerated glial tissue in the retina. Granular tissue was found to be firmly adherent to the vitreous, which may account for its being pulled into the vitreous cavity in some cases. This process may lead to complete or incomplete retinal tears with operculum located near the ora serrata. Local ized and slightly raised areas of chorioretinal pigmentation located near the equator have been reported as causing retinal tears rather frequently.9 It is possible that they also are areas of granular tissue. Tiny tags and floaters may be of diverse origin, some resulting from a developmental variation and others being the result of lo calized vitreoretinal degeneration. SUMMARY
The standard peripheral fundus located anterior to the scierai entrance of the vortex veins is described. Changes with age in the shape of the ora serrata are noted. The an terior limit of the vitreous base is sometimes visible ophthalmoscopically. Developmental variations are of three types : A. Variations in size and shape of the bays and teeth of the ora serrata are most frequent nasally, especially near the hori zontal meridian. Giant bays are often multi ple and seem to be caused by traction. Giant
NOVEMBER, 1967
teeth are often associated with giant bays. Unusually shaped teeth include forked teeth, ring teeth and bridging teeth. B. Meridional retinal folds are more fre quent as extensions of oral teeth than over oral bays. They are most often seen nasally, especially near the horizontal meridian. C. Granular tissue seems to represent embryonic remnants most often located na sally. The only exceptions are tiny tags and floaters which appear to be of degenerative origin. The shape of these embryonic rem nants varies and may be modified by vitre ous traction. Accordingly, granular tissue has been divided into granular patches, globules, tags or floaters and tiny tags or floaters. 99 West Cedar Street (02114) ACKNOWLEDGMENT
We are grateful to O. Pomerantzeff, Dipl. Eng., and I. Shefler, M.A, for their assistance in statis tical evaluation. REFERENCES
1. Salzmann, M. : The Anatomy and Histology of the Human Eyeball in the Normal State: Its Development and Senescence. (Authorized transla tion by E. V. L. Brown.) Chicago, Univ. Chicago Press, 1912. 2. Maggiore, L. : L'ora serrata nell'occhio umano, Ann. Ottal. 52:62S, 1924. 3. Schepens, C. L. and Bahn, G. C. : Examina tion of the ora serrata: Its importance in retinal detachment, Arch. Ophth. 44:677, 1950. 4. Schepens, C. L. : Subclinical retinal detach ments. Arch. Ophth. 47:593, 1952. 5. Teng, C. C. and Katzin, H. M. : An anatomic study of the periphery of the retina (a) Part I : Nonpigmented epithelial cell proliferation and hole formation. Am. J. Ophth. 34:1237, 1951; (b) Part I I : Peripheral cystoid degeneration of the retina; formation of cysts and holes. Am. J. Ophth. 36 :29, 1953; (c) Part I I I : Congenital retinal rosettes. Am. J. Ophth. 36:169, 1953. 6. Duke Elder, W. S. : Textbook of Ophthalmol ogy. St. Louis, Mosby, 1938, v. 2, p. 1336. 7 Hagedoorn, A. and Sieger, D. H. : Idiopathic retinal detachment. Am. J. Ophth. 41:660, 1956. 8. Okun, E. : Gross and microscopic pathology in autopsy eyes : Part III. Retinal breaks without de tachment. Am. J. Ophth. 51:369, 1961. 9. Dumas, J. and Schepens, C. L. : Chorioretinal lesions predisposing to retinal breaks. Am. J. Ophth. 61:620, 1966.
AND CHARLES L. SCHEPENS,
M.D.
Boston, Massachusetts The peripheral fundus is defined as the area of the fundus anterior to the scierai en trances of the vortex veins. It is subdivided into an equatorial and an oral region. In this presentation, the oral region is studied with particular care as it is the least known clini cally and has the greatest tendency to ex hibit variations. Every visible detail of the peripheral fun dus in 102 subjects was recorded on a fun dus chart. Examination of the fundus pe riphery could not be completed in 59 other subjects because of hypersensitivity to the bright light of the ophthalmoscope, inade quate transparency of the ocular media or insufficient pupillary dilation. More than twice as many males as females were hyper sensitive to light, a statistically significant difference. The ophthalmoscopic study of 102 subjects was correlated with the dissec tion of 11 eyes supplied by the Boston EyeBank. In the study of 204 fundi, no significant difference was found between right and left eyes or between sexes except where specifically mentioned. Some of the subjects showed changes in the posterior fundus. For instance, sclerosis of the retinal vessels, diminished or absent foveal light reflex and macular mottling with normal visual acuity were seen in a few cases and interpreted as resulting from aging. Medullated nerve fibers were found near the optic disc in both eyes of one subject. Benign melanomas of the pigment epithelium noted in the posterior From the Department of Retina Research, Retina Foundation, and the Retina Service, Massachusetts Eye and Ear Infirmary. This work was supported by research grant B-3489 of the National Institute of Neurological Diseases and Blindness, United States Public Health Service. * Fellow of the Retina Foundation (1957-1963); Fellow in Ophthalmology, Massachusetts Eye and Ear Infirmary (1957-1961).
fundus will be discussed in a subsequent pub lication. These changes were considered de velopmental variations in normal subjects. Finally, the posterior fundus showed isolated drusen or groups of drusen in nine eyes of seven subjects; small intraretinal hemor rhages were observed in both eyes of two subjects; and a small area of superficial chorioretinal atrophy (less than 0.25 disc diameter) was found in one eye of four subjects. In this presentation, an attempt is made to describe the standard peripheral fundus and to relate observations about its develop mental variations. T H E STANDARD PERIPHERAL FUNDUS
The standard peripheral fundus is defined as one which shows no developmental varia tions, signs of aging or abnormalities. It differed from the posterior fundus in that the retina was thinner as estimated with the ophthalmoscope by the distance between the retinal vessels and the surface of the pig ment epithelium. In the periphery, it was impossible to differentiate between arterioles and venules on the basis of size, color or pattern. The only practical method of iden tification was to trace the vessels back to the posterior fundus. The retinal arterioles and venules did not course together but were evenly distributed through the fundus periphery. Most of them became very small and disappeared before reaching a distance of 0.5 disc diameter from the ora serrata. Arterioles disappeared first, while venules extended closer to the ora serrata. Occasionally, a large vein ex tended to 0.5 disc diameter from the ora serrata, then ran parallel to it for one to three disc diameters and finally turned back toward the posterior pole for 1.0 to 1.5 disc diameters before disappearing. The pigment
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epithelium generally appeared more granu lar in the periphery than in the posterior fundus. In the ora serrata region, mild degenera tive changes were frequent in a strip of ap proximately 0.25 to 0.5 disc diameter poste rior to the ora serrata. In this area, the ret ina became opalescent and marked by one to three rows of small cystoid cavities. The underlying pigment epithelium was defi nitely darker and more granular. At the ora serrata, the photosensitive retina stops abruptly and is continued by the ciliary epi thelium which appears considerably thinner than the retina. When the peripheral edge of the retina showed cystoid degeneration it was thickened. As the pars plana ciliaris was more deeply pigmented than the periph eral retina, the choroidal pattern was ob scured by that of the pigment epithelium. Occasionally, the pigment epithelium in the pars plana ciliaris showed discrete black spots of variable size and irregular con tours. In infants, the ora serrata was found to form a slightly wavy line which was symmet^ rical all around the fundus and lay close to the posterior border of the ciliary processes. During the early years of life, the pars plana ciliaris grows asymmetrically, becom ing wider temporally than nasally, and the nasal ora serrata forms scallops. The concave side of each scallop is nearly always turned anteriorly. Sometimes, how ever, the scallops appeared inverted with a slightly concave side turned posteriorly. The teeth and bays formed by scalloping of the ora serrata became obvious at about onehalf hour temporal to the 12-o'clock meridi an and extended nasally to one-half hour on the nasal side of the 6-o'clock meridian. The estimated length of the ora serrata teeth on the nasal side varied from 0.25 to 1.0 disc diameter, averaging 0.75 disc diameter and rarely exceeding 1.5 disc diameters. On the temporal side, bays were replaced by a wavy line and teeth were narrow and short or sometimes absent.
841
In the posterior half of the pars plana ciliaris, the nonpigmented epithelium ap peared transparent, avascular and had a smooth glossy surface. It occupied a ringshaped area one and one-third disc diame ters wide. On dissection, it was adherent to the vitreous base which extended from the ora serrata anteriorly for approximately one disc diameter. With the ophthalmoscope, the vitreous base and its attachment to the ora serrata and ciliary epithelium were rarely visible. In seven eyes of six subjects, some sectors of the anterior limit of the vitreous base were visible as well as the adjacent hy aloid membrane (fig. 1). The latter ap peared as a thin membrane located in front of the surface of the pars plana ciliaris. It originated from the inner surface of the ciliary epithelium approximately one disc diameter anterior to the ora serrata and formed a faint ridge in the pars plana cilia ris over one and one-half hours to seven hours around the globe. Anteriorly, it disap peared beyond ophthalmoscopic view. The most frequent locations where it was visible were between the 11- and 1-o'clock and be tween the 5-and-7-o'clock positions. Findings by other authors. The develop ment of the ora serrata is incomplete at birth and continues to develop in early life. Its adult appearance is reached at the ap proximate age of seven years. 1 ' 2 Degenera tive changes begin near the ora serrata as early as the neonatal period. There are about 48 ora teeth per fundus and most of them correspond in position to the intervals between the ciliary processes.1 All the irreg ularities in the development of the corona ciliaris are reflected in the ora serrata. There seems to be no entirely satisfactory explanation for the development of serra tions at the ora serrata. In cross section, the teeth of the ora serrata form a spur of loose tissue which projects into the vitreous cavi ty. Its edges are undermined and are not ad herent to the ciliary epithelium. Adhesion to this epithelium exists only along the longitu dinal axis of the tooth. 1
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Fig. 1 (Rutnin and Schepens). Diagram representing the anterior limit of the vitreous base and the adjacent anterior hyaloid membrane sometimes visible in the extreme fundus periphery. (H) Anterior hyaloid attached to the middle of the pars plana ciliaris. (OS) Ora serrata. (R) Peripheral retina. (CP) Posterior extremities of the ciliary processes. OS
CP
bilateralism. In nearly all instances, varia DEVELOPMENTAL VARIATIONS A developmental variation of the periph tions in the teeth of the ora serrata ap eral fundus was assumed to be present when peared in association with deep ora bays. a structure in the retina or ciliary epitheli An overwhelming majority of these varia um appeared other than normal in size, tions were located nasally, near the horizon shape or texture and was found in a tal meridian (fig. 2 ) . Variations of bays. The usual contour of significant percentage of the subjects as sumed to be normal. Variations were so fre a bay was finely irregular and wavy but, in quent that at least one type was noted in a deep bay, the contour was perfectly 59.8% of 102 subjects (46.6% of the eyes). TABLE 1 The variations observed were divided into APPEARANCE OF THE PERIPHERAL FUNDUS IN three categories : ( 1 ) variations of the bays NORMAL EYES DEVELOPMENTAL VARIATIONS: 204 EYES IN 102 SUBJECTS and teeth of the ora serrata, (2) meridional retinal folds and (3) granular tissue. These N f Percentage of three categories of variations tended to £,£ Total No. Ey* of Eyes occur in the same eye with a significant fre quency (table 1). Occurred alone VARIATIONS OF BAYS AND TEETH OF THE ORA SERRATA
Variations of size and shape include: deep bays, giant teeth, forked teeth, ring teeth and bridging teeth (table 2 ) . Over 30% of the subjects examined showed at least one of these variations. When multiple, they tended to occur adjacent to each other. Deep ora bays were at least six times more frequent than any of the other ora serrata variations and had a significant tendency to
I. Variation of bay and tooth II. Fixed meridional fold III. Granular tissue
14 18 24
14.7 18.9 25.3
Occurred in combination I and II I and III II and III I and II and III
8 13 7 11
8.4 13.7 7.4 11.6
TOTAL
95
100.0
At least one developmental variation was present in 95 of 204 eyes (46.6%) and in 61 of 102 subjects (59.8%). The tendency for variations to occur in combination indicates that there exists a statistically significant relationship between them.
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TABLE 2 APPEARANCE OF THE PERIPHERAL FUNDUS IN NORMAL EYES FREQUENCY OF VARIATIONS OF ORAL BAYS AND TEETH: 204 EYES IN 102 SUBJECTS
Deep bay Giant tooth Forked tooth Ring tooth Bridging tooth
No. of Eyes
Percent
No. of Subjects
Percent
45 7 S 4 2
22.1 3.4 2.5 2.0 1.0
30 5 4 3 2
29.4 4.9 3.9 2.9 2.0
smooth as if it had been pulled taut. A deep bay was two to four times wider and deeper than adjacent bays. As the size of regular bays varied in different individuals, the ac tual dimension of deep bays was also vari able. As a rule, the teeth bordering a deep bay were somewhat larger than adjacent teeth. One to five deep bays per eye, or a total of 58 deep bays, were found in 45 eyes of 30 subjects. The deep bays were found singly, in adjacent pairs or triplets. A single deep bay was located in the upper temporal quadrant of three eyes. The other 55 were near the horizontal meridian, 50 (91%) na sally and five (9%) temporally. They were located near the course of a visible long cili ary nerve and artery. In 11 of 45 eyes showing deep bays (24.4%), other changes such as pearls, retinal breaks or latticelike degeneration were present. Variations of teeth. Except for its size, a giant tooth appeared similar to a regular tooth (fig. 2-A). Its length extended beyond the middle of the pars plana ciliaris and al most touched the ciliary processes. Giant teeth were found exclusively in eyes with deep bays. One or two giant teeth per eye or a total of 13 giant teeth appeared in seven eyes of five subjects. Eleven of the 13 giant teeth were adjacent to horizontally located deep bays ; the other two were between reg ular bays in the upper nasal quadrant. A forked tooth had a bifurcated tip and was larger than average (fig. 2-B). Five forked teeth, all adjacent to horizontally lo cated deep bays, were found in five eyes of four subjects. Four of the teeth were so large that they were also classified as giant
teeth. One of the five forked teeth was so deeply bifurcated that the bottom of the fork reached almost as far as the base of the tooth. A ring tooth was formed by two adjacent teeth leaning toward each other so as to form a ring enclosing a bay. Ring teeth were larger than average. Six ring teeth were noted in four eyes of three subjects. All except one were in eyes with deep bays. The three stages of ring formation are: (1) open ring, (2) closed ring and (3) holein-the-tooth. An open ring was noted twice ; the tips of adjacent teeth did not quite touch each other (fig. 2-F). A closed ring was also noted twice; the tips of adjacent teeth had joined. Each tooth forming a closed ring was large (fig. 2-D). A hole-in-the-tooth was noted twice; two adjacent teeth were solidly merged together in a single wide tooth (fig. 2-E), and there was a small cir cular area of pars plana ciliaris forming an island in its base. This island, which was much smaller than one in a closed ring, superficially resembled a retinal hole. A bridging tooth was a cordlike structure extending from the peripheral retina to the anterior portion of the pars plana ciliaris (fig. 2-C). Except for its anterior extremi ty, it was detached from the ciliary epitheli um and appeared curved like a bow with its convexity toward the center of the globe. It seemed to be degenerated and cystic. A bridging tooth, not adjacent to other varia tions, was found in one eye of two subjects. All variations observed in teeth seemed to be interrelated except for bridging teeth. It is possible that the latter should be classified
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as a morphologic anomaly instead of a nor mal variation. MERIDIONAL RETINAL FOLDS
A meridional retinal fold is a permanent dry fold* of 0.5 to 1.5 disc diameters in length involving all retinal layers. As a rule, such a fold begins at the ora serrata and runs posteriorly and perpendicularly to it in a meridional direction. The surface of a me ridional retinal fold appeared irregular, lacked transparency and was finely wavy as though the fold were covered with microcysts. In most cases, the surrounding retinal area showed cystoid degeneration (figs. 2-B and D and 3-B, C and E ) . The adjacent vit reous and pigment epithelium appeared un changed. Meridional folds were found in 44 eyes of 28 subjects (27.5%) and were bilateral in a statistically significant number of in stances. Of 87 folds, 71 (82%) were poste rior extensions of ora serrata teeth (figs. 2-D and 3-A, C, D and F ) and 16 (18%) were posterior to ora serrata bays (figs. 2-B and 3-B and E ) . The number of folds per eye varied from one to 10, but 59% had only one fold. The posterior end of 10 folds was adjacent to granular globules (fig. 3-A C and F ) ; six other folds showed one of * The term "dry fold" is applied to a retinal fold which is not accompanied by retinal detach ment.
NOVEMBER, 1967
the following changes: chorioretinal degen eration located either at the posterior ex tremity or on one side; incomplete or com plete retinal hole on the side and a granular patch at the posterior end; a globular mass on its course; a pearl on its side or on its anterior extremity. In one case (fig. 3-D), a piece of the meridional fold appeared to have broken off ; it was attached to the cor tex of the vitreous gel and cast a shadow on the fundus. Fixed meridional retinal folds were found significantly more often nasally than tempo rally and in the upper nasal quadrant more often than in the lower (table 3). Their fre quency near the nasal horizontal meridian was remarkable. Discussion and findings by other authors. The nature of meridional retinal folds is not clear. The folds located over the teeth of the ora serrata as well as the teeth themselves and the bays of the ora serrata are not visi ble in the newborn. Meridional folds, when present, become more conspicuous with age. The bays of the ora serrata may result from a pull exerted on the retina in a posterior direction. If such were the case during the postnatal development of the ora serrata re gion, the ora teeth would form because the retina is adherent to the pigment epithelium at the anterior extremity of the teeth. The meridional folds would then result from re dundant retinal tissue caused by stretching
Tfftl r
Fig. 2 (Rutnin and Schepens). Morphologic variations of the ora serrata region in normal fundi. (A) Nasal periphery with marked cystoid degeneration near horizontal meridian, giant tooth, and deep ora bay over long ciliary nerve. (B) Temporal periphery with marked cystoid degeneration near horizontal meridian, deep ora bay over long ciliary nerve, with forked tootn above, and below, a tooth with a pearl at its base. A second pearl is visible at the anterior end of the inferior tooth; above, small meridional fold on the side of an ora bay. (C) Upper temporal periphery with a bridging tooth covered with cystoid degeneration and almost in contact with a ciliary process; above, granular globule; below, white granular patch with large cystoid cavity on its anterior border. (D) Nasal periphery near horizontal meridian, with marked cystoid degeneration; ring tooth (closed ring) over long ciliary nerve; below, small meridional fold over ora tooth. (E) Temporal periphery near horizontal meridian; deep ora bay over long ciliary nerve; the tooth above the deep bay had part of its t i p broken off; ring tooth (hole-in-the-tooth) above. (F) Nasal periphery, near horizontal meridian, with ring tooth (open ring) and deep ora bay over long ciliary nerve. In the next bay, below, two tiny tags. A l l paintings are exact reproductions of individual fundi.
Fig. 3 (Rutnin and Schepens). Morphologie variations of the ora serrata region in normal fundi. (A) Upper nasal periphery with meridional fold over ora tooth and granular globule on its posterior border. (B) Upper nasal periphery with marked cystoid degeneration and meridional fold in the middle of an ora bay. (C) Upper nasal periphery with marked cystoid degeneration and meridional fold over a giant tooth which is connected with a ciliary process; three granular globules on the disc side of the meridional f o l d . (D) Nasal periphery with meridional fold over ora tooth; a piece of the tooth was torn and is attached to the vitreous cortex; tiny tag in the middle of an ora bay, above the meridional fold. (E) Nasal periphery near the horizontal meridian; deep ora bay over long ciliary nerve; a meridional fold, in the middle of the deep bay, is surrounded by cystoid degeneration. (F) Nasal periphery with small meridional fold over ora tooth and three granular globules. A l l paintings are exact reproductions of individual fundi.
Fig. 4 (Rutnin and Schepens). Granular tissue in the periphery of normal fundi. (A) Three granular patches in the inferior periphery. (B) Five granular patches in the nasal periphery. (C) Granular patch, in the inferior fundus periphery, was torn off the retina causing an incomplete retinal tear; a tiny tag was partially torn from the retina, causing a small in complete tear. (D) Nasal periphery with granular globule, near the long ciliary nerve, in an area of white with pressure. (E) Nasal periphery with marked cystoid degeneration; granular globule was partly torn from retina, causing two incomplete retinal tears. (F) Temporal periphery wih granular globule surrounded by fine line of pigment. All paintings are exact reproductions of individual fundi.
B
H
Fig. 5 (Rutnin and Schepens). Shapes of granular globules found in the periphery of normal fundi. ( A and B) Pyramidal shapes. (C and D ) Columnar shapes. ( E ) Club shape. ( F ) Cystic globule. (G and H ) Irregular shapes.
Fig. 6 (Rutnin and Schepens). Granular tags in the periphery of normal fundi. (A) Upper nasal periphery with marked cystoid degeneration on the disc side of which early retinoscnisis is visible; vascularized granular tag with tiny pigment ring. (B) Nasal periphery with two white granular tags. (C) Inferior periphery with cystic granular globule and granular tag to which a visible vitreous band is attached; smaller granular tag at the base of ora tooth, with incomplete retinal break. (D) Inferior periphery with peel-shaped granular tag surrounded with incomplete retinal break. All paintings are exact reproductions of individual fundi.
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TABLE 3 APPEARANCE OF THE PERIPHERAL FUNDUS IN NORMAL EYES LOCATION AND NUMBER OF MERIDIONAL FOLDS: 204 EYES
Nasal Side
Temporal Side
Upper
Horizontal
Lower
Upper
51
IS
14
4
of the retina in an anteroposterior direction. In cases of subclinical retinal detachment, Schepens3 noted that retinal breaks tended to occur adjacent to the posterior extremity of meridional folds. The frequency of me ridional folds (26%) in his series of 102 eyes with subclinical retinal detachment4 was similar to that in this series of normal sub jects (27.5%). This may indicate that the existence of meridional folds does not in crease the risk of a subclinical retinal de tachment; however, if this condition de velops in an eye with meridional folds, the retinal breaks tend to be located near the folds. Teng and Katzin 5-0 have described me ridional folds located at the ora serrata, most often on the nasal side, in the eyes of babies. They consider them as developmen tal anomalies, and their pictures show that these meridional folds are associated with variations in the ora bays. In all their pic tures the folds were in the middle of an ora bay, a type of fold representing 18% of the folds we have observed. Teng and Katzin show no meridional fold over an ora tooth. It is probable, therefore, that meridional folds seen in adults are of two different kinds : those coinciding with ora teeth are acquired after birth and those in the middle of the ora bays develop before birth. In our findings, the rate of occurrence of meridio nal retinal folds was about evenly distributed among subjects whose ages ranged from 12 to 81 years. Meridional folds, therefore, must develop at an early age and no new folds seem to appear thereafter. GRANULAR TISSUE
The ophthalmoscopic appearance of this
Horizontal —
Lower 3
Total 87
tissue was that of an opaque whitish gray spot with a dull granular surface which pro truded slightly at the inner surface of the retina (figs. 2-C and 3-A, C and F and 4 ) . One to nine areas were noted per eye in 55 eyes of 41 subjects indicating a significant tendency to bilateralism. As the affected subjects were evenly distributed among the age groups, the granular areas must have been present early in life without multiply ing during later years. Areas of granular tissue were divided into morphologic types : patch, globule and tag or floater. The last category was divided in two groups: tags and floaters whose structure could be distinguished by indirect ophthalmoscopy, and those which were so tiny that their structure could not be made out. All types of granular tissue had common characteristics. They were found signifi cantly more often in the posterior oral region than in other areas of the fundus periph ery and were never seen in the posterior portion of the equatorial region (table 4 ) . A significant preference for the nasal half of the globe was evident. Within the nasal half, the upper nasal quadrant was affected significantly more often, except for regular and tiny tags or floaters (table 5). Granular tissue was often associated with a meridio nal retinal fold or a retinal vessel. Granular patch. The granular patch ap peared as a slightly raised plaque on the inner surface of the retina. Its border was irregular but well outlined. It had a more or less round shape and its diameter varied from about one-eighth to one-third disc di ameter; sometimes the patch was elongated. It resembled an isolated area of cystoid de-
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TABLE 4 APPEARANCE OF THE PERIPHERAL FUNDUS IN NORMAL EVES CIRCUMFERENTIAL LOCATION OF GRANULAR TISSUE: 204 EYES
Type of Granular Tissue Patch Globule Tag or floater Tiny tag or floater TOTAL
Anterior Oral Region*
Posterior Oral Regionf
Anterior Equatorial Region Î
Posterior Equatorial Region §
—
66 17 14 96 193
12 7 7 7 33
— — — — —
2 2 13 17
Total 78 26 23 116 243
* Anterior to ora serrata line. t Posterior to ora serrata line. j Anterior to equator. § Between equator and scierai entrances of vortex veins.
generation except for its opaqueness (figs. 2-C and 4-A and B). One to eight granular patches per eye were noted in 28 fundi of 19 subjects—a significant tendency to bi lateralism. Of 78 granular patches, 27 (34.6%) were either close to a meridional retinal fold or along a retinal vessel ; in one instance, a granular patch appeared to have shrunk causing the formation of an incom plete retinal break (fig. 2-C). Granular globule. This was an irregular mass of one-twelfth to one-fifth disc diame ter protruding at the inner surface of the retina (figs. 3-A, C and F and 4-D, E and F ) . Some globules were elongated like a col umn or club (fig. 4-D). The retina and pig ment epithelium under and around the mass appeared degenerated and hyperpigmented (fig. 4-F). A few coarse and taut vitreous strands were seen attached to the top of club-shaped globules. In one instance, a glo bule seemed to have shrunk causing the for mation of two incomplete retinal holes (fig.
4-E). In another case, a relatively large, clear, fluid-containing cyst was seen to be partially embedded in a globule (fig. 5-F). The various shapes of globules encountered are schematically represented in Figure 5. One to three globules per eye were noted in 19 fundi of 18 subjects. Of 26 globules, 11 (42.3%) were found along retinal ves sels. Granular tag or floater. This type of granular tissue appeared to belong to one of the first two types but was modified by vit reous traction (fig. 6 ) . It seemed shrunken or curled and, in some cases, was so markedly distorted that it was impossible to be sure of its original shape. In one in stance, a granular tag showed signs of orga nization with new-formed blood vessels in it. All tags and floaters had the common characteristic of being a definite piece of de generated tissue which was pulled into the vitreous cavity. The granular tag was an elongated strand
TABLE S APPEARANCE OF THE PERIPHERAL FUNDUS IN NORMAL EYES QUADRANTIC LOCATION OF GRANULAR TISSUE: 2 0 4 EYES
Type of Granular Tissue Patch Globule Tag or floater Tiny tag or floater TOTAL
Nasal
Temporal
Upper
Lower
Upper
Lower
43 16 8 69 136
18 6 9 73 106
S 3 4 13 25
12 1 2 26 41
78 26 23 181 308
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of tissue about 0.25 disc diameter in length which protruded from the inner surface of the retina (fig. 6-A and B ) . It was distin guished from even smaller tags whose tex ture could not be identified with the indirect ophthalmoscope. The granular tag was gen erally attached to an area of degenerated retina. Fifteen granular tags were noted in 12 fundi or 12 subjects ; four were located along retinal vessels (fig. 6-A, B) ; none ap peared related to meridional folds. The granular floater generally retained its original character of patch or globule. It was either partially or completely torn off the retina. Torn tissue formed either a sin gle piece (fig. 6-C), or it was fragmented; sometimes it looked like a peel (fig. 6-D). Its area of origin always showed a coarse degenerated retina which, in certain cases, appeared as an incomplete or complete reti nal break (fig. 6-C). One granular floater was noted in eight fundi of eight subjects. Tiny tag or floater. A large number of tags and floaters observed were so small that their structure could not be distin guished by indirect ophthalmoscopy (figs. 2-F, 3-D and 4-C). They did not appear to be related to granular tissue and, in most eyes, were multiple with an average of nine per eye. Ninety-eight eyes of 64 subjects were affected—a significant tendency to bi lateralism. Affected individuals were of all ages, but when they were divided by age groups, those above 40 years of age showed about three times more tiny tags and float ers than the younger subjects. Therefore, it is probable that many of these tiny struc tures are degenerative and differ from the larger tags and floaters of granular nature. The tiny tags and floaters were over four times more frequent in the posterior oral region than in any other area of the globe ; they were not seen in the posterior equatori al region. In many cases, they were located along the ora line itself. The nasal side was over four times more often affected than the temporal side without preference for a
851
quadrant. About one half were tags with one end attached to the internal layers of the retina and the other end protruding into the vitreous cavity. Tiny tags were always elongated in a meridional direction. The other half were floaters lying in the vitreous cavity close to the inner layer of the retina. Most of them looked gray-white but a few were pigmented. In the majority of the eyes affected, tiny tags and floaters did not appear to be re lated to any other visible fundus anomaly. In five of 98 eyes, a tiny tag had been pulled from an area of chorioretinal degeneration causing a minute incomplete retinal tear without detachment (fig. 4-C). In six eyes, tiny floaters were seen over areas of lattice like retinal degeneration. The surface of the underlying retina looked fluffy but no defect was found in the retina to account for the floaters. In seven eyes, tiny tags and floaters were seen over the surface of cystoid retinal de generation. There were 12 floaters overlying broken inner walls of cystoid cavities, and in three instances, the broken wall showed a tiny tag attached to its anterior border (fig. 4-C). It is probable that in all of these cases, the resulting retinal tears were incom plete. In seven eyes, small tags and floaters were overlying areas of retinoschisis but no defect could be seen in the inner layer of the retina. In 11 eyes, pigmented tiny tags were seen at the ora serrata; they were clubshaped and protruded into the vitreous cavi ty. Generally, a group of them lay anterior to an area of chorioretinal degeneration. Discussion and findings by other authors. Granular tissue and rosette formation have been described in microphthalmic and in colobomatous eyes ; they have also been repro duced experimentally,8 "Microanomalies" which have been described histologically in apparently normal eyes7 may well represent granular tissue. In autopsy eyes5"a,b,c'8 granular patches
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were observed in the inner layer of the pe ripheral retina, mostly on the nasal side, and within five mm of the ora serrata. The inci dence at autopsy was quite similar to that of our clinical findings. The size of the lesions varied from a few micra to 0.5 mm by 2.5 mm; they were elongated in a meridional direction. Histologically, this tissue showed prolif eration and degeneration of the nonpigment ed epithelium of the pars plana ciliaris, gliosis and pigment proliferation with degenera tion of the normal retinal elements. Epithelioid cells found in this tissue were thought to be either metaplastic neuroepithelium re sulting from irregularity in the development of the retina or cells from degenerated glial tissue in the retina. Granular tissue was found to be firmly adherent to the vitreous, which may account for its being pulled into the vitreous cavity in some cases. This process may lead to complete or incomplete retinal tears with operculum located near the ora serrata. Local ized and slightly raised areas of chorioretinal pigmentation located near the equator have been reported as causing retinal tears rather frequently.9 It is possible that they also are areas of granular tissue. Tiny tags and floaters may be of diverse origin, some resulting from a developmental variation and others being the result of lo calized vitreoretinal degeneration. SUMMARY
The standard peripheral fundus located anterior to the scierai entrance of the vortex veins is described. Changes with age in the shape of the ora serrata are noted. The an terior limit of the vitreous base is sometimes visible ophthalmoscopically. Developmental variations are of three types : A. Variations in size and shape of the bays and teeth of the ora serrata are most frequent nasally, especially near the hori zontal meridian. Giant bays are often multi ple and seem to be caused by traction. Giant
NOVEMBER, 1967
teeth are often associated with giant bays. Unusually shaped teeth include forked teeth, ring teeth and bridging teeth. B. Meridional retinal folds are more fre quent as extensions of oral teeth than over oral bays. They are most often seen nasally, especially near the horizontal meridian. C. Granular tissue seems to represent embryonic remnants most often located na sally. The only exceptions are tiny tags and floaters which appear to be of degenerative origin. The shape of these embryonic rem nants varies and may be modified by vitre ous traction. Accordingly, granular tissue has been divided into granular patches, globules, tags or floaters and tiny tags or floaters. 99 West Cedar Street (02114) ACKNOWLEDGMENT
We are grateful to O. Pomerantzeff, Dipl. Eng., and I. Shefler, M.A, for their assistance in statis tical evaluation. REFERENCES
1. Salzmann, M. : The Anatomy and Histology of the Human Eyeball in the Normal State: Its Development and Senescence. (Authorized transla tion by E. V. L. Brown.) Chicago, Univ. Chicago Press, 1912. 2. Maggiore, L. : L'ora serrata nell'occhio umano, Ann. Ottal. 52:62S, 1924. 3. Schepens, C. L. and Bahn, G. C. : Examina tion of the ora serrata: Its importance in retinal detachment, Arch. Ophth. 44:677, 1950. 4. Schepens, C. L. : Subclinical retinal detach ments. Arch. Ophth. 47:593, 1952. 5. Teng, C. C. and Katzin, H. M. : An anatomic study of the periphery of the retina (a) Part I : Nonpigmented epithelial cell proliferation and hole formation. Am. J. Ophth. 34:1237, 1951; (b) Part I I : Peripheral cystoid degeneration of the retina; formation of cysts and holes. Am. J. Ophth. 36 :29, 1953; (c) Part I I I : Congenital retinal rosettes. Am. J. Ophth. 36:169, 1953. 6. Duke Elder, W. S. : Textbook of Ophthalmol ogy. St. Louis, Mosby, 1938, v. 2, p. 1336. 7 Hagedoorn, A. and Sieger, D. H. : Idiopathic retinal detachment. Am. J. Ophth. 41:660, 1956. 8. Okun, E. : Gross and microscopic pathology in autopsy eyes : Part III. Retinal breaks without de tachment. Am. J. Ophth. 51:369, 1961. 9. Dumas, J. and Schepens, C. L. : Chorioretinal lesions predisposing to retinal breaks. Am. J. Ophth. 61:620, 1966.