Tractional Elevations of the Retina in Patients With Diabetes Harvey Lincoff, M.D., Yasser Serag, M.D., Stanley Chang, M.D., Ronald Silverman, P h . D . , Bothina Bondok, M.D., and M o h a m e d E l - A s w a d , M.D.
Tractional retinoschisis and tractional reti nal detachment are both complications of proliferative diabetic retinopathy. The two condi tions are frequently confused because they are similar in diagnostic features. We determined the respective incidence of tractional retinos chisis and tractional retinal detachment in 200 eyes with tractional elevations of the retina in patients with diabetes. In 39 eyes, the diagno sis was unequivocally tractional retinoschisis because the retinal elevation maintained its concave contour despite the development of retinal holes. In 65 eyes, tractional retinal detachment was diagnosed with equal cer tainty, either because pigment lines were present or because the elevation, after a reti nal hole developed, rapidly became convex and extended to the ora serrata. The remain ing 96 eyes, in which retinal holes or pigment lines were absent, were classified by other features that had been tested for significance in the already diagnosed eyes. On that basis, the diagnosis was retinoschisis in 46 eyes and retinal detachment in 50 eyes. I N I 974, two types of tractional elevation of the retina seen in the course of diabetic retinopathy were compared. 1 Concave borders and surfaces were initially present in both conditions. In one type of tractional elevation of the retina, the retina was translucent or opaque, and pigment
Accepted for publication Dec. 27, 1991. From the New York Hospital-Cornell University Medi cal Center, New York, New York (Drs. Lincoff, Chang, and Silverman); and Faculty of Medicine, Tanta Univer sity, Tanta, Egypt (Drs. Serag, Bondok, a n d El-Aswad). This study was supported by the Edward Grayson Fund, West Orange, New Jersey. Reprint requests to Harvey Lincoff, M.D., New York Hospital-Cornell Medical Center, 525 E. 68th St., New York, NY 10021.
lines developed at its borders. Additionally, if holes developed in the elevated retina, the elevation rapidly became convex and extended to the ora serrata. This condition was denned as tractional retinal detachment and its conver sion to rhegmatogenous retinal detachment if a hole occurred was noted. In the other type of tractional elevation of the retina, the elevated retina was transparent, pigment lines never developed, and the presence of holes in the elevated retina did not lead to a change in its contour. On that basis, the condition was de fined as tractional retinoschisis. 1 During the ensuing 16 years, we collected data on tractional retinal elevations among our patients with diabetes. We concluded that trac tional retinoschisis occurs frequently in pa tients with diabetes and proliferative retinopa thy, and may be subject to different treatment.
Material and Methods Two hundred eyes with concave elevations of the retina in 144 patients with diabetes were included in our study. Fifty-three patients were from the service of one of us (H.L.) and were monitored at intervals of three to four months for between one and ten years. The other 91 patients were referred to one of us (S.C.) for vitrectomy of presumed tractional retinal de tachment between July 1989 and March 1991. All patients were seen consecutively in each practice and were included in the study because a concave elevation of the retina was initially present in one or both eyes and the media over the elevation were clear. The patients were examined with indirect ophthalmoscopy and retinal drawings were made to outline the shape and extent of the retinal elevation. The drawings were augmented by slit-lamp biomicroscopic observations and stereophotography. The extent of the retinal elevation in each
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patient was graded with slight modification according to the scheme of McMeel.2 Eyes were initially classified into the follow ing three groups: (1) Group 1, fractional retinal detachment; (2) Group 2, tractional retinoschisis; and (3) Group 3, tractional retinal elevation of undetermined structure. Tractional retinal detachment was diagnosed because one or more pigment lines were seen within or at the borders of a concave elevation, or because the elevation that was concave when first seen became convex when a retinal break occurred. Tractional retinoschisis was diag nosed when the retinal elevation remained con cave despite the presence of retinal holes. The third classification, tractional retinal ele vation of undetermined structure, referred to eyes in which the retinal elevation was concave and free of pigment lines or holes. To classify eyes further in the group with tractional retinal elevation of undetermined structure, 17 other features that were recorded during the examination were tested for frequen cy in Groups 1 and 2. Potential criteria for diagnosis included general factors such as pa tient age and gender and type and duration of the diabetes, as well as the examination findings. The overall transparency of the elevat ed retina was examined and the extent of trans lucent areas was noted. Also recorded were the presence of vascular and avascular prolifera tion, sheathed blood vessels, vitreous hemor rhage, intraretinal or subretinal hemorrhage or exudate, subretinal bands, and intraretinal glial proliferation within the limits of the elevation. Another potential differentiating feature was the presence of pigment in the elevated retina over an area of previous photocoagulation. The extent of the elevation was measured. The visu al acuity before and after a vitrectomy to reattach an elevated macula was compared in those eyes in which the media had been clear preoperatively and remained clear postoperatively. The data were analyzed for statistical signifi cance by using Student's f-test and the chisquare test. Significant factors were used to distribute the tractional elevations that had neither retinal holes nor pigment lines into probable retinal detachment or probable reti noschisis. A stepwise discriminant analysis was performed with the criteria for variable entry of F = 4.0. The previous probabilities for group membership were equal. 3 Late in the study we explored the use of laser photocoagulation to differentiate retinoschisis from retinal detachment in 56 eyes. A laser
application of 500 |i.m at an energy level suffi cient to cause a white lesion in 0.2 second in the retina adjacent to the elevation was selected as the test standard. The laser beam was then applied to an area in the elevated retina that was remote from the edge, was maximally elevated, and was not obscured by a preretinal membrane. Formation of an equivalent white lesion deep beneath elevated retina was regarded as confirmation of the presence of outer retinal layers and was diagnostic for retinoschisis.
Results Sixty-five eyes had tractional retinal detach ments and 39 eyes had tractional retinoschisis. The remaining 96 eyes were initially labeled as having tractional retinal elevation of undeter mined structure. Of the 65 eyes in the tractional retinal detach ment group, the retinal elevations in 34 eyes had pigment demarcation lines. In 37 eyes (six with pigment lines), retinal breaks developed while the eyes were being observed; at that time the elevation rapidly became convex and spread to the ora serrata. The change was usual ly symptomatic, with the patient experiencing a rapid loss of vision. All 39 eyes in the tractional retinoschisis group met the definition of retinoschisis (the elevated surfaces remained concave despite the presence of retinal holes and pigment demarca tion lines were absent). In the 96 eyes classified as examples of trac tional retinal elevation of unknown structure, neither holes nor pigment lines were present. The populations of the three groups were similar. The mean age was 47 years (± 14.4 years) for the tractional retinal detachment group, 51.1 years (± 12.8 years) for the trac tional retinoschisis group, and 50.9 years (± 13.2 years) for the group with tractional retinal elevation of undetermined structure. Fifty-four of 65 eyes (83%) in the tractional retinal de tachment group, 34 of 39 eyes (87%) in the tractional retinoschisis group, and 77 of 96 eyes (80%) in the group with tractional retinal eleva tion of undetermined structure were from pa tients with insulin-dependent diabetes. The mean duration of the diabetes was 19.1 years (± 9.5 years) for the tractional retinal detachment group, 19.5 years (± 8.1 years) for the traction al retinoschisis group, and 17.5 years (± 7.3 years) for the group with tractional retinal
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tional retinal detachment group, but only the frequency of vascular proliferation had signifi cance. Vascular proliferation was present in 32 of 65 eyes (49.2%) with detachment and ten of 39 eyes (25.6%) with retinoschisis (P < .001). Conversely, avascular proliferation was associ ated with retinoschisis. Avascular proliferation was present in 22 of 39 eyes (56.4%) with retinoschisis and in 18 of 65 eyes (27.7%) with retinal detachments (P < .001). Sheathed reti nal vessels were also associated with retinos chisis. Sheathed retinal vessels were present in 22 of 39 eyes (56.5%) with retinoschisis and in four of 65 eyes (6.1%) with retinal detachments (P < .001). The intraretinal space was relatively clear in retinoschisis. Short string-shaped glial struc tures were Visible within the space in 17 of 39 eyes (43.6%; Fig. 1). Glial strings were never seen beneath the elevation in retinal detach ments and thus they were associated with the retinoschisis (P < .001). Intra- or subretinal hemorrhage and exudate in the area of the elevated retina were associated with retinal detachment. They were present in 35 of 65 eyes (53.8%) with retinal detachments and were not seen within the layers of retinoschisis (P < .001). Long, clothesline-shaped bands on the outer surface of elevated retina were associated with retinal detachment (Fig. 2). Bands were seen in nine of 65 eyes (13.8%) with retinal
elevation of undetermined structure. The mean duration of visual complaints was 42.4 weeks (± 37.8 weeks) for the tractional retinal detach ment group, 53.4 weeks (± 53.2 weeks) for the tractional retinoschisis group, and 46.8 weeks (± 49.9 weeks) for the group with tractional retinal elevation of undetermined structure. We observed no statistically significant difference between the groups regarding these criteria (P = .05). Statistical analysis of the frequency of other features in the 65 eyes classified as having retinal detachment and the 39 eyes classified as having retinoschisis identified eight clinical features with diagnostic significance (Table). A transparent retina was associated with retinos chisis (P < .001). The retinas were transparent in 34 of the 39 eyes (87%) designated as having retinoschisis. In the other five of the 39 eyes, some areas were transparent and some were translucent. In contrast, the entire retina was translucent in 35 of the 65 eyes (53.8%) that had retinal detachments and most of the elevat ed retina was translucent in 18 eyes (27.7%). In the remaining 12 eyes (18.5%), all of the elevat ed retina was transparent. The duration of the detachment in these 12 eyes was between six and 36 months, and all had pigment demarca tion lines. Vascular proliferation and vitreous hemor rhage developed more frequently in the trac
TABLE SIGNIFICANT DIAGNOSTIC FEATURES FOR TRACTIONAL RETINOSCHISIS AND TRACTIONAL RETINAL DETACHMENT
RETINOSCHISIS
EYES WITH TRACTIONAL DETACHMENT
p
(N = 39)
(N = 65)
VALUE
34 0
12 35
5 10 22 22 17
18 32 18 4 0
.001 .001 .001 .001
0 0 0
35 9 14
.001 .015 .001
EYES WITH TRACTIONAL FEATURES
Retinal transparency Transparent Translucent Transparent and translucent Vascular proliferation Avascular proliferation Sheathed blood vessels Intraretinal strings Subretinal hemorrhage or exudate Subretinal bands Pigment in elevated retina
.001*
'Significance figure is a composite of the significance in the following three subgroups. P values were determined by the chi-square test.
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Fig. 1 (Lincoff and associates). String-shaped glial proliferation (arrow) in the intraretinal space of frac tional retinoschisis.
Fig. 2 (Lincoff and associates). Subretinal bands (arrows) beneath tractional retinal detachment.
detachments and were not seen in any eye with retinoschisis (P = .015). Pigment deposits in the elevated retina over areas of previous photocoagulation were asso ciated with retinal detachment (P < .001). Pig ment was seen in 14 eyes with retinal detach ments. The pigmented spots were smaller than the coagulation scars in the pigment epithelium and choroid, but the distribution corresponded to the pattern of photocoagulation. Pigment was not seen in the inner retinal layers in 28 eyes with retinoschisis in which the retinoschi sis had invaded an area of photocoagulation. When the fractional retinal elevations in the 96 eyes in the group with fractional retinal elevation of undetermined structure were reclassified according to the eight significant fac tors described previously, 46 eyes were consid ered to have probable retinoschisis and 50 eyes were considered to have probable retinal de tachments. A discriminant model using all the findings (17 features, excluding the laser effect) yielded a diagnosis of retinoschisis in 43 eyes and retinal detachment in 53 eyes. The discrim inant model had a canonic correlation of .86 (chi-square = 132.5 and P < .001). The response to laser application was tested in 21 eyes with retinoschisis and nine eyes were designated as having probable retinoschisis. All eyes had a white lesion in the outer retinal layers (Fig. 3). Eleven eyes with tractional reti nal detachments and 16 eyes designated as having probable retinal detachments were test ed with the laser and none showed a response.
Other features, although not diagnostic, had some clinical relevance. The extent of the reti nal elevation tended to be greater in eyes with tractional retinal detachments than in eyes
Fig. 3 (Lincoff and associates). Tractional retinal elevation diagnosed as retinoschisis by other factors was tested for intact outer retinal layers with applica tions of argon laser. The yellow lesion in the outer layers in response to test applications (2 and 3) was similar to the response to the control application (1) in retina outside of the schisis elevation and further confirmed the diagnosis. Note that the schisis has invaded an area of previous panretinal photocoagu lation (broken line marks lower border of schisis).
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O
o
Grade 1
Grade 2
Grade 3
Grade 4
Grade 1
Grade 2
Grade 3
Grade 4
EXTENT
EXTENT
Fig. 4 (Lincoff and associates). A comparison of the extent of the retinal elevation in 200 diabetic eyes with tractional retinoschisis (left) and tractional retinal detachment (right). Extent is graded 1 to 4 (according to McMeel2). Grade 1: less than four disk diameters across. Grade 2: greater than four disk diameters across, but occupying less than a 30-degree circumferential segment of the fundus. Grade 3: occupying a 30- to 90-degree circumferential segment. Grade 4: occupying greater than a 90-degree circumferential segment. with tractional retinoschisis (P < .001; Fig. 4). Consequently, the macula was less frequently detached in retinoschisis and the visual acuity in eyes with retinoschisis tended to be better (P = .02; Fig. 5). After successful vitrectomy, the recovery of central vision in eyes in which the macula had been elevated tended to be greater in eyes with retinal detachments than in eyes with retinoschisis (P = .03; Fig. 6).
Discussion Duke-Elder and Dobree 4 described tractional retinoschisis in two patients with diabetes in 1968. They did not disclose their reasons for concluding that the elevations were examples of retinoschisis rather than of retinal detach ment, but presumably it was because the elevat
ed retina appeared transparent. A retinal hole was present in one retinal elevation. Also in 1969, Dobree 6 described the changes that devel oped in proliferative diabetic retinopathy in 112 eyes that were monitored from nine months to 8.5 years. Dobree 6 concluded that seven eyes had retinoschisis and 12 eyes had retinal de tachments. He also noted that the condition progressed slowly in eyes with retinoschisis. In 1971, McMeel2 described six of 279 eyes with diabetic retinopathy as having tractional reti nal detachments that developed retinal holes without other changes. These eyes were ob served for six months to eight years. McMeel2 concluded that possibly an internal separation of the retina similar to retinoschisis had oc curred. The presence of a retinal hole in a concave retinal elevation provides an unequivocal diag nosis of tractional retinoschisis. In our experi-
PROBABLE RETINOSCHISIS RETINOSCHISIS
VISUAL ACUITY
VISUAL ACUITY
Fig. 5 (Lincoff and associates). Comparisons of visual acuity in 200 diabetic eyes with tractional retinoschisis (left) and tractional retinal detachment (right).
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^
^S^
PREOPERATIVE VISUAL ACUITY
Fig. 6 (Lincoff and associates). Scattergram show ing the recovery of visual acuity of 50 eyes in which the maculas were reattached after vitrectomy. The media were clear pre- and postoperatively in all patients. ence a n d in t h a t of o t h e r s , 6 8 if a r e t i n a l h o l e d e v e l o p s in a t r a c t i o n a l d e t a c h m e n t , t h e eleva tion r a p i d l y b e c o m e s convex. We believe t h a t pillars of M u e l l e r ' s fibers w i t h o t h e r clinging n e u r a l e l e m e n t s c o m p a r t m e n t a l i z e the schisis cavity a n d m a i n t a i n the concave s h a p e in t r a c tional r e t i n o s c h i s i s (Fig. 7). N o r k a n d associ ates, 9 in a h i s t o p a t h o l o g i c s t u d y of proliferative diabetic r e t i n o p a t h y , d e m o n s t r a t e d i n t r a r e t i n a l b r i d g e s across cystic s p a c e s c o m p o s e d of cells t h a t t h e y identified as of Mueller-cell origin. In a n e l e c t r o n - m i c r o s c o p i c scan of senile r e t i n o s chisis, similar pillars of M u e l l e r ' s fibers w i t h a t t a c h e d n e u r a l e l e m e n t s t h a t b r i d g e d the schisis cavity w e r e d e m o n s t r a t e d . It is t h e n e u r -
NLP
LP
HM
CF
20/40020/30020/20020/100
VISUAL ACUITY
20/70
Fig. 7 (Lincoff and associates). Pathologic section of an eye with tractional retinoschisis from a patient with diabetes. The internal layers of the retina have been elevated by contraction of the posterior hyaloidal membrane (ph), which is attached to the apex of the schisis separation (arrow). The walls of intra retinal cysts form pillars that connect the inner and outer layers of the retina (arrowheads). The retina is artifactually detached (Mallory's connective tissue stain, x 4 ) .
al e l e m e n t s on the scaffold of M u e l l e r ' s fibers t h a t m a i n t a i n s o m e t r a n s m i s s i o n across all b u t the m o s t elevated a r e a s of t h e r e t i n o s c h i s i s cavity. In the m a c u l a r area, r e t i n o s c h i s i s t e n d e d to be s h a l l o w a n d c e n t r a l visual field t e s t i n g always p r o v i d e d e v i d e n c e of t r a n s m i s s i o n , vari ably r e d u c e d , across the s e p a r a t e d layers. C a p illary i s c h e m i a in p a t i e n t s w i t h d i a b e t e s is a n i n d e p e n d e n t factor t h a t c o n t r i b u t e s t o t h e r e d u c t i o n in function. The d i s t r i b u t i o n of m a c u lar vision in r e t i n o s c h i s i s did n o t differ signifi cantly from t h a t of r e t i n a l d e t a c h m e n t w h e n the m a c u l a s w e r e elevated (Fig. 8).
NLp
Lp
H
„
„
2 0/40020/30020/20020/10020/70 VISUAL ACUITY
Fig. 8 (Lincoff and associates). The similar distribution of the visual acuity in 42 eyes with tractional retinoschisis through the macula (left) and that in 95 eyes with tractional retinal detachment through the macula (right).
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The retinas of patients with diabetes may be susceptible to lamellar separation (retinoschisis) when under traction, because retinal capil lary ischemia has weakened the intraretinal connections. In the experimentally induced ischemic retina of miniature pigs, 11 neural cell loss in the inner layers at the retina was ob served and the outer plexiform layer became markedly thin or disappeared. The separation in the diabetic retina appears to be at the level of the outer plexiform layer. Sections of trac tional retinoschisis associated with diabetes have been examined and supported this opin ion (H. Beuttner, M.D., written communication, Jan. 21, 1991). Parenthetically, peripheral trac tional schisis develops in patients with sicklecell disease, a disorder characterized by periph eral retinal ischemia. In one of our patients with sickle-cell disease, we confirmed the diag nosis of peripheral tractional retinoschisis when the contour of the retinal elevation re mained concave after a retinal hole developed in the internal layers. The presence of a pigment demarcation line was pathognomonic of retinal detachment. Dobbie, 12 Okun and Cibis, 13 and DiScalafani and associates 14 agreed that a pigment line is a reliable differential point between stationary retinal detachment and retinoschisis. The lack of pigment lines in eyes in which retinoschisis
was diagnosed in our study after having been observed for six months to ten years is good evidence that tractional retinoschisis does not cause pigment lines. Pigment lines may infre quently occur within retinoschisis around outer layer breaks or at the edge of an outer-layer retinal detachment. 14 The two-layer configura tion can usually be discerned (Fig. 9). The lack of a pigment line at initial examina tion does not preclude tractional retinal de tachment; most clinicians agree that it takes at least three months for pigment lines to form.1516 Despite all the diagnostic features described previously, there will still be patients in whom the nature of the tractional elevation will be in doubt at initial examination. Barring a rapid and symptomatic extension of the elevation, which would indicate retinal detachment (and require intervention), observing the patient for three to six months will usually be rewarded with a diagnostic feature. Either a pigment line will develop, indicating retinal detachment; or will not develop, indicating retinoschisis. Eventually the inner layers of retinoschisis will develop retinal holes and fragment (Fig. 10). Diagnostic laser photocoagulation, which was begun late in our study, may prove to be a more immediate differential tool for uncertain diag noses. Except for testing visual acuity and some
Fig. 9 (Lincoff and associates). Tractional retinos chisis with two large retinal holes at the upper edge of an external layer detachment (arrows). A preretinal membrane that obscures retinal vessels in the internal layers (arrowheads) is also present.
Fig. 10 (Lincoff and associates). Disintegration of the internal layers of tractional retinoschisis of two years' duration.
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c e n t r a l visual fields, we did n o t u s e f u n c t i o n a l tests to differentiate b e t w e e n fractional r e t i n o s chisis a n d fractional r e t i n a l d e t a c h m e n t . We w a n t e d to obtain criteria for a n a n a t o m i c differ ential. Present-day sophisticated functional a n d electrophysiologic t e s t i n g m a y a u g m e n t t h e a n a t o m i c differential. Testing will b e c o m plicated by the d y s f u n c t i o n c a u s e d b y t h e d i s ease itself. Trick, Trick, a n d Kilo 17 f o u n d t h a t color vision, contrast s e n s i t i v i t y , a n d v i s u a l evoked r e s p o n s e m a y b e a b n o r m a l in t h e d i a betic r e t i n a before r e t i n o p a t h y a p p e a r s . Retinoschisis was t h e a n a t o m i c s t r u c t u r e of at least 39 (19.5%) a n d p r o b a b l y as m a n y as 85 (42.5%) of the e l e v a t i o n s in 200 eyes. O b s e r v a t i o n s of v i t r e o u s s u r g e o n s c o u l d a u g m e n t t h e percentage. During vitrectomy, an iatrogenic b r e a k in a n area of e l e v a t e d r e t i n a w i t h o u t a c h a n g e in the c o n t o u r from concave to convex is a g o o d i n d i c a t i o n t h a t t h e b r e a k h a s o c c u r r e d in a n area of r e t i n o s c h i s i s ( a n d n e e d n o t b e t r e a t ed). In this respect, surgical p r o c e d u r e s for correction of fractional r e t i n o s c h i s i s are less risky t h a n t h o s e for c o r r e c t i o n of fractional retinal detachment. O t h e r factors may influence t h e t r e a t m e n t of p a t i e n t s w i t h d i a b e t e s a n d r e t i n a l e l e v a t i o n s in w h o m r e t i n o s c h i s i s h a s b e e n d i a g n o s e d . Tract i o n a l r e t i n o s c h i s i s p r o g r e s s e d slowly in o u r p a t i e n t s . Eventually, the i n n e r layers d i s i n t e g r a t e d a n d p r o g r e s s i o n ceased. P h o t o c o a g u l a tion to the b o r d e r s of the schisis did n o t i m p e d e its p r o g r e s s . If it i n v a d e d t h e m a c u l a , t h e visual loss was n o greater t h a n t h a t o c c u r r i n g w i t h fractional r e t i n a l d e t a c h m e n t , b u t r e a p p o s i t i o n of the m a c u l a w a s less likely to yield i m p r o v e m e n t in c e n t r a l vision. ACKNOWLEDGMENT
H e l m u t Buettner, M.D., p r o v i d e d Figure 7.
References 1. Lincoff, H., and Kreissig, I.: Patterns of nonrhegmatogenous elevations of the retina. Br. J. Ophthalmol. 58:899, 1974. 2. McMeel, J. W.: Diabetic retinopathy. Fibrotic proliferation and retinal detachment. Trans. Am. Ophthalmol. Soc. 69:440, 1971.
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3. Gnanadesikan, R.: Methods for Statistical Data Analysis of Multivariate Observations. New York, John Wiley and Sons, 1977, p. 82. 4. Duke-Elder, S., and Dobree, J. H.: The forma tion of avascular connective tissue bands in proliferative diabetic retinopathy. Ophthalmology 76:133, 1968. 5. Dobree, J. H.: Evolution of lesions in proliferative diabetic retinopathy. An 8-year photographic survey. In Goldberg, M. F., and Fine, S. L. (eds.): Symposium on the Treatment of Diabetic Retinopa thy, Public Health Service Publication No. 1890. Washington, D.C., Public Health Service, 1969, p. 55. 6. O'Connor, P. R.: Diabetic retinal detachment. Int. Ophthalmol. Clin. 16:157, 1976. 7. Boniuk, I., Okun, E., and Johnston, G. P.: Scleral buckling in diabetic retinal detachment. Mod. Probl. Ophthalmol. 10:341, 1972. 8. Kreissig, I., and Lincoff, H.: Die Ablatio bei diabetischer Retinopathie. Ihre Differentialdiagnose und Therapie. Sitzungsber. 129. Versammlung des Vereins Rhein.-Westf. Augenarzte, 1975, pp. 22-27. 9. Nork, T. M., Wallow, I. H. L, Samek, S. J., and Anderson, G.: Muller's cell involvement in proliferative diabetic retinopathy. Arch. Ophthalmol. 105:1424, 1987. 10. Marshall, J.: The effects of ultraviolet radiation on the eye. In Marshall, J. M. (ed.): Vision and Visual Dysfunction, vol. 16. London, Macmillan Press, Ltd., 1991, pp. 54-56. 11. Pournaras, C. J., Tsacopoulos, M., Strommer, K., Gilodi, N., and Leuenberger, P. M.: Experimental retinal branch vein occlusion in miniature pigs in duces local tissue hypoxia and vasoproliferative microangiopathy. Ophthalmology 97:1321, 1990. 12. Dobbie, G. J.: Cryotherapy in the management of senile retinoschisis. Trans. Am. Acad. Ophthal mol. Otolaryngol. 73:1047, 1969. 13. Okun, E., and Cibis, P. A.: The role of photocoagulation in the management of retinoschisis. Arch. Ophthalmol. 72:309, 1964. 14. DiScalafani, M., Wagner, A., Humphrey, W., and Valone, J., Jr.: Pigmentary changes in acquired retinoschisis. Am. J. Ophthalmol. 105:291, 1988. 15. Yanoff, M., and Fine, B. S.: Ocular Pathology. Philadelphia, Harper and Row Publishers, 1982, p. 570. 16. Schepens, C. L.: Retinal Detachment and Al lied Diseases. Philadelphia, W. B. Saunders Compa ny, 1983, p. 182. 17. Trick, G. L., Trick, L. R., and Kilo, C : Visual field defects in patients with insulin-dependent and non-insulin-dependent diabetics. Ophthalmology 97:475, 1990.
Tractional retinoschisis and tractional reti nal detachment are both complications of proliferative diabetic retinopathy. The two condi tions are frequently confused because they are similar in diagnostic features. We determined the respective incidence of tractional retinos chisis and tractional retinal detachment in 200 eyes with tractional elevations of the retina in patients with diabetes. In 39 eyes, the diagno sis was unequivocally tractional retinoschisis because the retinal elevation maintained its concave contour despite the development of retinal holes. In 65 eyes, tractional retinal detachment was diagnosed with equal cer tainty, either because pigment lines were present or because the elevation, after a reti nal hole developed, rapidly became convex and extended to the ora serrata. The remain ing 96 eyes, in which retinal holes or pigment lines were absent, were classified by other features that had been tested for significance in the already diagnosed eyes. On that basis, the diagnosis was retinoschisis in 46 eyes and retinal detachment in 50 eyes. I N I 974, two types of tractional elevation of the retina seen in the course of diabetic retinopathy were compared. 1 Concave borders and surfaces were initially present in both conditions. In one type of tractional elevation of the retina, the retina was translucent or opaque, and pigment
Accepted for publication Dec. 27, 1991. From the New York Hospital-Cornell University Medi cal Center, New York, New York (Drs. Lincoff, Chang, and Silverman); and Faculty of Medicine, Tanta Univer sity, Tanta, Egypt (Drs. Serag, Bondok, a n d El-Aswad). This study was supported by the Edward Grayson Fund, West Orange, New Jersey. Reprint requests to Harvey Lincoff, M.D., New York Hospital-Cornell Medical Center, 525 E. 68th St., New York, NY 10021.
lines developed at its borders. Additionally, if holes developed in the elevated retina, the elevation rapidly became convex and extended to the ora serrata. This condition was denned as tractional retinal detachment and its conver sion to rhegmatogenous retinal detachment if a hole occurred was noted. In the other type of tractional elevation of the retina, the elevated retina was transparent, pigment lines never developed, and the presence of holes in the elevated retina did not lead to a change in its contour. On that basis, the condition was de fined as tractional retinoschisis. 1 During the ensuing 16 years, we collected data on tractional retinal elevations among our patients with diabetes. We concluded that trac tional retinoschisis occurs frequently in pa tients with diabetes and proliferative retinopa thy, and may be subject to different treatment.
Material and Methods Two hundred eyes with concave elevations of the retina in 144 patients with diabetes were included in our study. Fifty-three patients were from the service of one of us (H.L.) and were monitored at intervals of three to four months for between one and ten years. The other 91 patients were referred to one of us (S.C.) for vitrectomy of presumed tractional retinal de tachment between July 1989 and March 1991. All patients were seen consecutively in each practice and were included in the study because a concave elevation of the retina was initially present in one or both eyes and the media over the elevation were clear. The patients were examined with indirect ophthalmoscopy and retinal drawings were made to outline the shape and extent of the retinal elevation. The drawings were augmented by slit-lamp biomicroscopic observations and stereophotography. The extent of the retinal elevation in each
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patient was graded with slight modification according to the scheme of McMeel.2 Eyes were initially classified into the follow ing three groups: (1) Group 1, fractional retinal detachment; (2) Group 2, tractional retinoschisis; and (3) Group 3, tractional retinal elevation of undetermined structure. Tractional retinal detachment was diagnosed because one or more pigment lines were seen within or at the borders of a concave elevation, or because the elevation that was concave when first seen became convex when a retinal break occurred. Tractional retinoschisis was diag nosed when the retinal elevation remained con cave despite the presence of retinal holes. The third classification, tractional retinal ele vation of undetermined structure, referred to eyes in which the retinal elevation was concave and free of pigment lines or holes. To classify eyes further in the group with tractional retinal elevation of undetermined structure, 17 other features that were recorded during the examination were tested for frequen cy in Groups 1 and 2. Potential criteria for diagnosis included general factors such as pa tient age and gender and type and duration of the diabetes, as well as the examination findings. The overall transparency of the elevat ed retina was examined and the extent of trans lucent areas was noted. Also recorded were the presence of vascular and avascular prolifera tion, sheathed blood vessels, vitreous hemor rhage, intraretinal or subretinal hemorrhage or exudate, subretinal bands, and intraretinal glial proliferation within the limits of the elevation. Another potential differentiating feature was the presence of pigment in the elevated retina over an area of previous photocoagulation. The extent of the elevation was measured. The visu al acuity before and after a vitrectomy to reattach an elevated macula was compared in those eyes in which the media had been clear preoperatively and remained clear postoperatively. The data were analyzed for statistical signifi cance by using Student's f-test and the chisquare test. Significant factors were used to distribute the tractional elevations that had neither retinal holes nor pigment lines into probable retinal detachment or probable reti noschisis. A stepwise discriminant analysis was performed with the criteria for variable entry of F = 4.0. The previous probabilities for group membership were equal. 3 Late in the study we explored the use of laser photocoagulation to differentiate retinoschisis from retinal detachment in 56 eyes. A laser
application of 500 |i.m at an energy level suffi cient to cause a white lesion in 0.2 second in the retina adjacent to the elevation was selected as the test standard. The laser beam was then applied to an area in the elevated retina that was remote from the edge, was maximally elevated, and was not obscured by a preretinal membrane. Formation of an equivalent white lesion deep beneath elevated retina was regarded as confirmation of the presence of outer retinal layers and was diagnostic for retinoschisis.
Results Sixty-five eyes had tractional retinal detach ments and 39 eyes had tractional retinoschisis. The remaining 96 eyes were initially labeled as having tractional retinal elevation of undeter mined structure. Of the 65 eyes in the tractional retinal detach ment group, the retinal elevations in 34 eyes had pigment demarcation lines. In 37 eyes (six with pigment lines), retinal breaks developed while the eyes were being observed; at that time the elevation rapidly became convex and spread to the ora serrata. The change was usual ly symptomatic, with the patient experiencing a rapid loss of vision. All 39 eyes in the tractional retinoschisis group met the definition of retinoschisis (the elevated surfaces remained concave despite the presence of retinal holes and pigment demarca tion lines were absent). In the 96 eyes classified as examples of trac tional retinal elevation of unknown structure, neither holes nor pigment lines were present. The populations of the three groups were similar. The mean age was 47 years (± 14.4 years) for the tractional retinal detachment group, 51.1 years (± 12.8 years) for the trac tional retinoschisis group, and 50.9 years (± 13.2 years) for the group with tractional retinal elevation of undetermined structure. Fifty-four of 65 eyes (83%) in the tractional retinal de tachment group, 34 of 39 eyes (87%) in the tractional retinoschisis group, and 77 of 96 eyes (80%) in the group with tractional retinal eleva tion of undetermined structure were from pa tients with insulin-dependent diabetes. The mean duration of the diabetes was 19.1 years (± 9.5 years) for the tractional retinal detachment group, 19.5 years (± 8.1 years) for the traction al retinoschisis group, and 17.5 years (± 7.3 years) for the group with tractional retinal
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tional retinal detachment group, but only the frequency of vascular proliferation had signifi cance. Vascular proliferation was present in 32 of 65 eyes (49.2%) with detachment and ten of 39 eyes (25.6%) with retinoschisis (P < .001). Conversely, avascular proliferation was associ ated with retinoschisis. Avascular proliferation was present in 22 of 39 eyes (56.4%) with retinoschisis and in 18 of 65 eyes (27.7%) with retinal detachments (P < .001). Sheathed reti nal vessels were also associated with retinos chisis. Sheathed retinal vessels were present in 22 of 39 eyes (56.5%) with retinoschisis and in four of 65 eyes (6.1%) with retinal detachments (P < .001). The intraretinal space was relatively clear in retinoschisis. Short string-shaped glial struc tures were Visible within the space in 17 of 39 eyes (43.6%; Fig. 1). Glial strings were never seen beneath the elevation in retinal detach ments and thus they were associated with the retinoschisis (P < .001). Intra- or subretinal hemorrhage and exudate in the area of the elevated retina were associated with retinal detachment. They were present in 35 of 65 eyes (53.8%) with retinal detachments and were not seen within the layers of retinoschisis (P < .001). Long, clothesline-shaped bands on the outer surface of elevated retina were associated with retinal detachment (Fig. 2). Bands were seen in nine of 65 eyes (13.8%) with retinal
elevation of undetermined structure. The mean duration of visual complaints was 42.4 weeks (± 37.8 weeks) for the tractional retinal detach ment group, 53.4 weeks (± 53.2 weeks) for the tractional retinoschisis group, and 46.8 weeks (± 49.9 weeks) for the group with tractional retinal elevation of undetermined structure. We observed no statistically significant difference between the groups regarding these criteria (P = .05). Statistical analysis of the frequency of other features in the 65 eyes classified as having retinal detachment and the 39 eyes classified as having retinoschisis identified eight clinical features with diagnostic significance (Table). A transparent retina was associated with retinos chisis (P < .001). The retinas were transparent in 34 of the 39 eyes (87%) designated as having retinoschisis. In the other five of the 39 eyes, some areas were transparent and some were translucent. In contrast, the entire retina was translucent in 35 of the 65 eyes (53.8%) that had retinal detachments and most of the elevat ed retina was translucent in 18 eyes (27.7%). In the remaining 12 eyes (18.5%), all of the elevat ed retina was transparent. The duration of the detachment in these 12 eyes was between six and 36 months, and all had pigment demarca tion lines. Vascular proliferation and vitreous hemor rhage developed more frequently in the trac
TABLE SIGNIFICANT DIAGNOSTIC FEATURES FOR TRACTIONAL RETINOSCHISIS AND TRACTIONAL RETINAL DETACHMENT
RETINOSCHISIS
EYES WITH TRACTIONAL DETACHMENT
p
(N = 39)
(N = 65)
VALUE
34 0
12 35
5 10 22 22 17
18 32 18 4 0
.001 .001 .001 .001
0 0 0
35 9 14
.001 .015 .001
EYES WITH TRACTIONAL FEATURES
Retinal transparency Transparent Translucent Transparent and translucent Vascular proliferation Avascular proliferation Sheathed blood vessels Intraretinal strings Subretinal hemorrhage or exudate Subretinal bands Pigment in elevated retina
.001*
'Significance figure is a composite of the significance in the following three subgroups. P values were determined by the chi-square test.
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Fig. 1 (Lincoff and associates). String-shaped glial proliferation (arrow) in the intraretinal space of frac tional retinoschisis.
Fig. 2 (Lincoff and associates). Subretinal bands (arrows) beneath tractional retinal detachment.
detachments and were not seen in any eye with retinoschisis (P = .015). Pigment deposits in the elevated retina over areas of previous photocoagulation were asso ciated with retinal detachment (P < .001). Pig ment was seen in 14 eyes with retinal detach ments. The pigmented spots were smaller than the coagulation scars in the pigment epithelium and choroid, but the distribution corresponded to the pattern of photocoagulation. Pigment was not seen in the inner retinal layers in 28 eyes with retinoschisis in which the retinoschi sis had invaded an area of photocoagulation. When the fractional retinal elevations in the 96 eyes in the group with fractional retinal elevation of undetermined structure were reclassified according to the eight significant fac tors described previously, 46 eyes were consid ered to have probable retinoschisis and 50 eyes were considered to have probable retinal de tachments. A discriminant model using all the findings (17 features, excluding the laser effect) yielded a diagnosis of retinoschisis in 43 eyes and retinal detachment in 53 eyes. The discrim inant model had a canonic correlation of .86 (chi-square = 132.5 and P < .001). The response to laser application was tested in 21 eyes with retinoschisis and nine eyes were designated as having probable retinoschisis. All eyes had a white lesion in the outer retinal layers (Fig. 3). Eleven eyes with tractional reti nal detachments and 16 eyes designated as having probable retinal detachments were test ed with the laser and none showed a response.
Other features, although not diagnostic, had some clinical relevance. The extent of the reti nal elevation tended to be greater in eyes with tractional retinal detachments than in eyes
Fig. 3 (Lincoff and associates). Tractional retinal elevation diagnosed as retinoschisis by other factors was tested for intact outer retinal layers with applica tions of argon laser. The yellow lesion in the outer layers in response to test applications (2 and 3) was similar to the response to the control application (1) in retina outside of the schisis elevation and further confirmed the diagnosis. Note that the schisis has invaded an area of previous panretinal photocoagu lation (broken line marks lower border of schisis).
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O
o
Grade 1
Grade 2
Grade 3
Grade 4
Grade 1
Grade 2
Grade 3
Grade 4
EXTENT
EXTENT
Fig. 4 (Lincoff and associates). A comparison of the extent of the retinal elevation in 200 diabetic eyes with tractional retinoschisis (left) and tractional retinal detachment (right). Extent is graded 1 to 4 (according to McMeel2). Grade 1: less than four disk diameters across. Grade 2: greater than four disk diameters across, but occupying less than a 30-degree circumferential segment of the fundus. Grade 3: occupying a 30- to 90-degree circumferential segment. Grade 4: occupying greater than a 90-degree circumferential segment. with tractional retinoschisis (P < .001; Fig. 4). Consequently, the macula was less frequently detached in retinoschisis and the visual acuity in eyes with retinoschisis tended to be better (P = .02; Fig. 5). After successful vitrectomy, the recovery of central vision in eyes in which the macula had been elevated tended to be greater in eyes with retinal detachments than in eyes with retinoschisis (P = .03; Fig. 6).
Discussion Duke-Elder and Dobree 4 described tractional retinoschisis in two patients with diabetes in 1968. They did not disclose their reasons for concluding that the elevations were examples of retinoschisis rather than of retinal detach ment, but presumably it was because the elevat
ed retina appeared transparent. A retinal hole was present in one retinal elevation. Also in 1969, Dobree 6 described the changes that devel oped in proliferative diabetic retinopathy in 112 eyes that were monitored from nine months to 8.5 years. Dobree 6 concluded that seven eyes had retinoschisis and 12 eyes had retinal de tachments. He also noted that the condition progressed slowly in eyes with retinoschisis. In 1971, McMeel2 described six of 279 eyes with diabetic retinopathy as having tractional reti nal detachments that developed retinal holes without other changes. These eyes were ob served for six months to eight years. McMeel2 concluded that possibly an internal separation of the retina similar to retinoschisis had oc curred. The presence of a retinal hole in a concave retinal elevation provides an unequivocal diag nosis of tractional retinoschisis. In our experi-
PROBABLE RETINOSCHISIS RETINOSCHISIS
VISUAL ACUITY
VISUAL ACUITY
Fig. 5 (Lincoff and associates). Comparisons of visual acuity in 200 diabetic eyes with tractional retinoschisis (left) and tractional retinal detachment (right).
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^
^S^
PREOPERATIVE VISUAL ACUITY
Fig. 6 (Lincoff and associates). Scattergram show ing the recovery of visual acuity of 50 eyes in which the maculas were reattached after vitrectomy. The media were clear pre- and postoperatively in all patients. ence a n d in t h a t of o t h e r s , 6 8 if a r e t i n a l h o l e d e v e l o p s in a t r a c t i o n a l d e t a c h m e n t , t h e eleva tion r a p i d l y b e c o m e s convex. We believe t h a t pillars of M u e l l e r ' s fibers w i t h o t h e r clinging n e u r a l e l e m e n t s c o m p a r t m e n t a l i z e the schisis cavity a n d m a i n t a i n the concave s h a p e in t r a c tional r e t i n o s c h i s i s (Fig. 7). N o r k a n d associ ates, 9 in a h i s t o p a t h o l o g i c s t u d y of proliferative diabetic r e t i n o p a t h y , d e m o n s t r a t e d i n t r a r e t i n a l b r i d g e s across cystic s p a c e s c o m p o s e d of cells t h a t t h e y identified as of Mueller-cell origin. In a n e l e c t r o n - m i c r o s c o p i c scan of senile r e t i n o s chisis, similar pillars of M u e l l e r ' s fibers w i t h a t t a c h e d n e u r a l e l e m e n t s t h a t b r i d g e d the schisis cavity w e r e d e m o n s t r a t e d . It is t h e n e u r -
NLP
LP
HM
CF
20/40020/30020/20020/100
VISUAL ACUITY
20/70
Fig. 7 (Lincoff and associates). Pathologic section of an eye with tractional retinoschisis from a patient with diabetes. The internal layers of the retina have been elevated by contraction of the posterior hyaloidal membrane (ph), which is attached to the apex of the schisis separation (arrow). The walls of intra retinal cysts form pillars that connect the inner and outer layers of the retina (arrowheads). The retina is artifactually detached (Mallory's connective tissue stain, x 4 ) .
al e l e m e n t s on the scaffold of M u e l l e r ' s fibers t h a t m a i n t a i n s o m e t r a n s m i s s i o n across all b u t the m o s t elevated a r e a s of t h e r e t i n o s c h i s i s cavity. In the m a c u l a r area, r e t i n o s c h i s i s t e n d e d to be s h a l l o w a n d c e n t r a l visual field t e s t i n g always p r o v i d e d e v i d e n c e of t r a n s m i s s i o n , vari ably r e d u c e d , across the s e p a r a t e d layers. C a p illary i s c h e m i a in p a t i e n t s w i t h d i a b e t e s is a n i n d e p e n d e n t factor t h a t c o n t r i b u t e s t o t h e r e d u c t i o n in function. The d i s t r i b u t i o n of m a c u lar vision in r e t i n o s c h i s i s did n o t differ signifi cantly from t h a t of r e t i n a l d e t a c h m e n t w h e n the m a c u l a s w e r e elevated (Fig. 8).
NLp
Lp
H
„
„
2 0/40020/30020/20020/10020/70 VISUAL ACUITY
Fig. 8 (Lincoff and associates). The similar distribution of the visual acuity in 42 eyes with tractional retinoschisis through the macula (left) and that in 95 eyes with tractional retinal detachment through the macula (right).
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The retinas of patients with diabetes may be susceptible to lamellar separation (retinoschisis) when under traction, because retinal capil lary ischemia has weakened the intraretinal connections. In the experimentally induced ischemic retina of miniature pigs, 11 neural cell loss in the inner layers at the retina was ob served and the outer plexiform layer became markedly thin or disappeared. The separation in the diabetic retina appears to be at the level of the outer plexiform layer. Sections of trac tional retinoschisis associated with diabetes have been examined and supported this opin ion (H. Beuttner, M.D., written communication, Jan. 21, 1991). Parenthetically, peripheral trac tional schisis develops in patients with sicklecell disease, a disorder characterized by periph eral retinal ischemia. In one of our patients with sickle-cell disease, we confirmed the diag nosis of peripheral tractional retinoschisis when the contour of the retinal elevation re mained concave after a retinal hole developed in the internal layers. The presence of a pigment demarcation line was pathognomonic of retinal detachment. Dobbie, 12 Okun and Cibis, 13 and DiScalafani and associates 14 agreed that a pigment line is a reliable differential point between stationary retinal detachment and retinoschisis. The lack of pigment lines in eyes in which retinoschisis
was diagnosed in our study after having been observed for six months to ten years is good evidence that tractional retinoschisis does not cause pigment lines. Pigment lines may infre quently occur within retinoschisis around outer layer breaks or at the edge of an outer-layer retinal detachment. 14 The two-layer configura tion can usually be discerned (Fig. 9). The lack of a pigment line at initial examina tion does not preclude tractional retinal de tachment; most clinicians agree that it takes at least three months for pigment lines to form.1516 Despite all the diagnostic features described previously, there will still be patients in whom the nature of the tractional elevation will be in doubt at initial examination. Barring a rapid and symptomatic extension of the elevation, which would indicate retinal detachment (and require intervention), observing the patient for three to six months will usually be rewarded with a diagnostic feature. Either a pigment line will develop, indicating retinal detachment; or will not develop, indicating retinoschisis. Eventually the inner layers of retinoschisis will develop retinal holes and fragment (Fig. 10). Diagnostic laser photocoagulation, which was begun late in our study, may prove to be a more immediate differential tool for uncertain diag noses. Except for testing visual acuity and some
Fig. 9 (Lincoff and associates). Tractional retinos chisis with two large retinal holes at the upper edge of an external layer detachment (arrows). A preretinal membrane that obscures retinal vessels in the internal layers (arrowheads) is also present.
Fig. 10 (Lincoff and associates). Disintegration of the internal layers of tractional retinoschisis of two years' duration.
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c e n t r a l visual fields, we did n o t u s e f u n c t i o n a l tests to differentiate b e t w e e n fractional r e t i n o s chisis a n d fractional r e t i n a l d e t a c h m e n t . We w a n t e d to obtain criteria for a n a n a t o m i c differ ential. Present-day sophisticated functional a n d electrophysiologic t e s t i n g m a y a u g m e n t t h e a n a t o m i c differential. Testing will b e c o m plicated by the d y s f u n c t i o n c a u s e d b y t h e d i s ease itself. Trick, Trick, a n d Kilo 17 f o u n d t h a t color vision, contrast s e n s i t i v i t y , a n d v i s u a l evoked r e s p o n s e m a y b e a b n o r m a l in t h e d i a betic r e t i n a before r e t i n o p a t h y a p p e a r s . Retinoschisis was t h e a n a t o m i c s t r u c t u r e of at least 39 (19.5%) a n d p r o b a b l y as m a n y as 85 (42.5%) of the e l e v a t i o n s in 200 eyes. O b s e r v a t i o n s of v i t r e o u s s u r g e o n s c o u l d a u g m e n t t h e percentage. During vitrectomy, an iatrogenic b r e a k in a n area of e l e v a t e d r e t i n a w i t h o u t a c h a n g e in the c o n t o u r from concave to convex is a g o o d i n d i c a t i o n t h a t t h e b r e a k h a s o c c u r r e d in a n area of r e t i n o s c h i s i s ( a n d n e e d n o t b e t r e a t ed). In this respect, surgical p r o c e d u r e s for correction of fractional r e t i n o s c h i s i s are less risky t h a n t h o s e for c o r r e c t i o n of fractional retinal detachment. O t h e r factors may influence t h e t r e a t m e n t of p a t i e n t s w i t h d i a b e t e s a n d r e t i n a l e l e v a t i o n s in w h o m r e t i n o s c h i s i s h a s b e e n d i a g n o s e d . Tract i o n a l r e t i n o s c h i s i s p r o g r e s s e d slowly in o u r p a t i e n t s . Eventually, the i n n e r layers d i s i n t e g r a t e d a n d p r o g r e s s i o n ceased. P h o t o c o a g u l a tion to the b o r d e r s of the schisis did n o t i m p e d e its p r o g r e s s . If it i n v a d e d t h e m a c u l a , t h e visual loss was n o greater t h a n t h a t o c c u r r i n g w i t h fractional r e t i n a l d e t a c h m e n t , b u t r e a p p o s i t i o n of the m a c u l a w a s less likely to yield i m p r o v e m e n t in c e n t r a l vision. ACKNOWLEDGMENT
H e l m u t Buettner, M.D., p r o v i d e d Figure 7.
References 1. Lincoff, H., and Kreissig, I.: Patterns of nonrhegmatogenous elevations of the retina. Br. J. Ophthalmol. 58:899, 1974. 2. McMeel, J. W.: Diabetic retinopathy. Fibrotic proliferation and retinal detachment. Trans. Am. Ophthalmol. Soc. 69:440, 1971.
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3. Gnanadesikan, R.: Methods for Statistical Data Analysis of Multivariate Observations. New York, John Wiley and Sons, 1977, p. 82. 4. Duke-Elder, S., and Dobree, J. H.: The forma tion of avascular connective tissue bands in proliferative diabetic retinopathy. Ophthalmology 76:133, 1968. 5. Dobree, J. H.: Evolution of lesions in proliferative diabetic retinopathy. An 8-year photographic survey. In Goldberg, M. F., and Fine, S. L. (eds.): Symposium on the Treatment of Diabetic Retinopa thy, Public Health Service Publication No. 1890. Washington, D.C., Public Health Service, 1969, p. 55. 6. O'Connor, P. R.: Diabetic retinal detachment. Int. Ophthalmol. Clin. 16:157, 1976. 7. Boniuk, I., Okun, E., and Johnston, G. P.: Scleral buckling in diabetic retinal detachment. Mod. Probl. Ophthalmol. 10:341, 1972. 8. Kreissig, I., and Lincoff, H.: Die Ablatio bei diabetischer Retinopathie. Ihre Differentialdiagnose und Therapie. Sitzungsber. 129. Versammlung des Vereins Rhein.-Westf. Augenarzte, 1975, pp. 22-27. 9. Nork, T. M., Wallow, I. H. L, Samek, S. J., and Anderson, G.: Muller's cell involvement in proliferative diabetic retinopathy. Arch. Ophthalmol. 105:1424, 1987. 10. Marshall, J.: The effects of ultraviolet radiation on the eye. In Marshall, J. M. (ed.): Vision and Visual Dysfunction, vol. 16. London, Macmillan Press, Ltd., 1991, pp. 54-56. 11. Pournaras, C. J., Tsacopoulos, M., Strommer, K., Gilodi, N., and Leuenberger, P. M.: Experimental retinal branch vein occlusion in miniature pigs in duces local tissue hypoxia and vasoproliferative microangiopathy. Ophthalmology 97:1321, 1990. 12. Dobbie, G. J.: Cryotherapy in the management of senile retinoschisis. Trans. Am. Acad. Ophthal mol. Otolaryngol. 73:1047, 1969. 13. Okun, E., and Cibis, P. A.: The role of photocoagulation in the management of retinoschisis. Arch. Ophthalmol. 72:309, 1964. 14. DiScalafani, M., Wagner, A., Humphrey, W., and Valone, J., Jr.: Pigmentary changes in acquired retinoschisis. Am. J. Ophthalmol. 105:291, 1988. 15. Yanoff, M., and Fine, B. S.: Ocular Pathology. Philadelphia, Harper and Row Publishers, 1982, p. 570. 16. Schepens, C. L.: Retinal Detachment and Al lied Diseases. Philadelphia, W. B. Saunders Compa ny, 1983, p. 182. 17. Trick, G. L., Trick, L. R., and Kilo, C : Visual field defects in patients with insulin-dependent and non-insulin-dependent diabetics. Ophthalmology 97:475, 1990.
