Limited Macular Translocation for Atrophic Maculopathy

CLINICAL SCIENCES Limited Macular Translocation for Atrophic Maculopathy

Jeffrey D. Benner, MD; Janet S. Sunness, MD; Matthias D. Ziegler, BS; Jalal Soltanian, MSE

Objectives: To report visual improvement following bi- using scleral infolding in the right eye and scleral out- lateral limited macular translocation for a patient with atro- pouching in the left eye. Following translocation of her phic macular disease, and to discuss issues related to the maculae, her best-corrected visual acuity improved from selection of potential candidates for this technique. 20/200 to 20/30 OD and from 20/180 to 20/100 OS. She remained stable during 30 months of follow-up for the Design: Case report. right eye and 22 months of follow-up for the left eye.

Results: A 78-year-old woman with bilateral atrophic Conclusion: Macular translocation may allow visual re- maculopathy and no choroidal neovascularization had covery in selected patients with atrophic maculopathy, slowly progressive loss of visual acuity for at least 17 even after a prolonged period of poor vision. months in the right eye and 25 months in the left eye. She underwent bilateral limited macular translocation, Arch Ophthalmol. 2002;120:586-594

ACULAR translocation tomas.8-10 Theoretically, macular translo- was developed as a cation may be useful for treating atrophic technique for moving macular disease by placing the fovea over the fovea relative to un- healthier RPE, which could prevent the loss derlying choroidal neo- of photoreceptors and sustain foveal func- vascularization.M This allows both the pho- tion. This article presents the results of lim- tocoagulation of formerly subfoveal ited macular translocation in both eyes of choroidal neovascularization, while spar- a patient with atrophic macular disease, pre- ing the foveal center, and the reposition- sumed to be caused by pattern dystrophy, ing of the fovea over healthier retinal pig- who had poor visual acuity for a pro- ment epithelium (RPE). Machemer and longed period of time prior to the proce- Steinhorst1 first reported success with this dure. technique in 1993 by using a 360° retinotomy to translocate the macula. Later, de REPORT OF A CASE Juan et al2 and Pieramici et al3 used scleral shortening to perform limited macular A 78-year-old woman sought care from her translocation without the need for a 360° ophthalmologist in May 1996 because of retinotomy. Others have confirmed this ini- decreased vision in her left eye. At that tial success using both techniques.4-7 This time, her best-corrected visual acuity was procedure has preserved and even im- 20/50 OD with a refractive error of +1.00 From the Delmarva proved visual acuity. Although the empha- −2.00ϫ90° and 20/80 OS with a refrac- Vitreoretinal Center, Salisbury, sis, to date, has been on using macular tive correction of +2.75 −1.50ϫ70°. She Md, and the University of translocation to treat subfoveal choroidal had macular changes consistent with atro- Maryland, Baltimore neovascularization, this technique may pos- phic maculopathy. By May 1997, her best- (Dr Benner); and Wilmer Lions sibly be useful for patients with atrophic corrected visual acuity had declined to Vision Center, Johns Hopkins macular disease that involves the fovea and 20/80 OD and 20/100 OS. By March 1998, University School of Medicine, affects foveal function. Atrophic macular the visual acuity had further declined to Baltimore (Dr Sunness and Messrs Ziegler and Soltanian). disease is generally associated with under- 20/100 OD and 20/200 OS. By July 1998, The authors have no lying RPE atrophy, often with associated her visual acuity had declined further to commercial or proprietary loss of choriocapillaris, and the loss of RPE 20/200 OD and 20/400 OS. She was then interest in any device discussed is what often leads to the loss of photore- referred to one of us (J.D.B.) to see if any herein. ceptors and the development of central sco- treatment was available.

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Figure 1. Right eye: A preoperative fundus photograph (A) shows atrophic macular changes. On the color photograph, xanthophyll was apparent within the atrophic lesion. A preoperative fluorescein angiogram frame (B) shows areas of blockage and hyperfluorescence. No evidence of choroidal neovascularization is present, and the fluorescein pattern is not characteristic of geographic atrophy or Stargardt disease. An 8-month postoperative argon blue scanning laser ophthalmoscope (SLO) image (C) shows the xanthophyll entirely outside the atrophic lesion. An infrared SLO image (D) from 8 months after macular translocation shows the retina shifted inferiorly relative to the retinal pigment epithelium (RPE) lesion. Fixation is inferior to the atrophic lesion. The retina now overlying the atrophic lesion has a dense scotoma. The cross indicates fixation; shaded circles, stimulus that has been seen; and open triangles, stimulus that has not been seen (scotoma). Several stimulus intensities were employed, with the brighter symbols indicating a dimmer stimulus. An 8-month postoperative SLO autofluorescence image (E) shows a patchy loss of autofluorescence in the region of the atrophic RPE. A 22-month postoperative argon blue SLO image (F) shows that the RPE atrophy has become more pronounced and has an overlying dense scotoma. The xanthophyll appearance is unchanged.

On the initial evaluation in August 1998, the pa- giogram showed central blocked hypofluorescence sur- tient’s best-corrected visual acuity was 20/200 OD and rounded by a rim of transmission hyperfluorescence 20/400 OS. She had bilateral posterior chamber intra- within the macula in the right eye, with more promi- ocular lenses and a circular area of RPE atrophy and pig- nent transmission hyperfluorescence in the left eye (Fig- mentary change beneath the fovea, with the left eye worse ure 1B and Figure 2B). There was no evidence of occult than the right eye (Figure 1A and Figure 2A). In both or classic choroidal neovascularization. The patient asked eyes, she was able to accurately fixate foveally and fol- if any treatment would be available to either improve her low a 200-µm diameter spot projected from the slitlamp vision or slow the progression of the macular degenera- (Haag-Streit AG, Ko¨niz, Switzerland). A fluorescein an- tion she had experienced during the last 4 years. Macu-

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Figure 2. Left eye: A preoperative fundus photograph (A) shows a central atrophic lesion, within which xanthophyll is visible in the color photograph. A preoperative fluorescein angiogram frame (B) shows patchy transmission hyperfluorescence, consistent with atrophic maculopathy. A preoperative infrared scanning laser ophthalmoscope (SLO) image (C) shows fixation within the atrophic lesion. The cross indicates fixation; shaded circles, stimulus that has been seen; and open triangles, stimulus that has not been seen (scotoma). A number of stimulus intensities were employed, with the brighter symbols indicating a dimmer stimulus. When the cross was fixated within the atrophic lesion, few stimuli were detected near it. When the cross was moved out of the field, the area had a significant relative scotoma (but not a full dense scotoma). A preoperative argon blue SLO image (D) shows the presence of xanthophyll (dark area) within the atrophic lesion. A preoperative autofluorescence SLO image (E) shows a mottled, but not complete, loss of autofluorescence in the atrophic region. An argon blue SLO image (F) from 14 months after macular translocation shows that some of the xanthophyll is still overlying the atrophic lesion. A 14-month postoperative infrared SLO image (G) shows that fixation is inferior to the atrophic region, in the area of xanthophyll seen in F. There is a dense scotoma in the retinal area now overlying the atrophic region. lar translocation was discussed because it offered the pos- and potential benefits, she elected to undergo macular sibility of relocating the fovea over healthy and viable RPE. translocation in her right eye. In October 1998, one of After carefully considering all the known associated risks us (J.D.B.) performed a limited macular translocation us-

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 ing circumferential scleral infolding, as described by de (Figure 1D). There was a mild reduction in general reti- Juan et al.2 The technique included a pars plana vitrec- nal sensitivity outside the area of her lesion. With argon tomy and creation of a temporal retinal detachment by blue imaging, the area of xanthophyll was prominent and infusing fluid into the subretinal space through a 39- outside the atrophic lesion (Figure 1C). Autofluores- gauge subretinal needle. Scleral infolding was per- cence imaging showed patchy black areas within the atro- formed by tying preplaced 5-0 Mersilene (Ethicon Inc, phic lesion rather than the solid black appearance seen Somerville, NJ) sutures in the superior temporal quad- in geographic atrophy with loss of RPE (Figure 1E). In rant. A gas bubble using sulfur hexafluoride gas was placed the left eye, the patient fixated within the area of the in the vitreous cavity, and the patient was positioned na- central atrophic lesion (Figure 2C). In this lesion, only sal side up for 5 minutes. She was then positioned up- the brightest SLO stimulus (0 dB with a Goldmann III– right to allow the gas bubble to translocate the macula sized target) could be seen. Peripherally, there was nor- inferiorly and reattach the retina. Postoperatively, her mal sensitivity, except for a mild relative scotoma in- course was uncomplicated, with spontaneous reattach- feronasally. Argon blue imaging showed xanthophyll ment of the retina and good translocation of the macula present within the atrophic lesion (Figure 2D), and au- (1191 µm). tofluorescence imaging showed patchy black areas Two months after surgery, her visual acuity had im- within the region of this lesion (Figure 2E). proved to 20/70-1 OD, but her refractive error had in- To better define the cause of her macular lesions, elec- creased dramatically, with a significant amount of in- trophysiological and visual function testing was per- duced astigmatism. Her new refractive error in the right formed. Electro-oculography was performed to evaluate eye had changed from her baseline of +1.00 −2.00ϫ90° any evidence of Best disease. The Arden ratio was normal (which had been confirmed on several occasions preop- in both eyes (2.64 OD and 2.84 OS; normal, Ն1.80). Elec- eratively by refraction, keratometry, low vision evalua- troretinography was performed to assess the presence of tion, and automated refraction) to +5.00 −6.75ϫ80°. Four diffuse retinal disease as a cause of the macular lesions. months after surgery, her visual acuity had improved to The scotopic responses were normal. The flicker re- 20/50+2 OD with the same refractive error. To help elimi- sponses were reduced to approximately 50% of normal in nate the anisometropia caused by the induced astigma- the right eye and 80% of normal in the left eye, and the tism, she underwent an astigmatic keratotomy in the right photopic flash response was reduced to about 80% of nor- eye. Eleven months after translocation surgery, her vi- mal in the right eye and was normal in amplitude in the sual acuity had improved to 20/40+2 OD with a refrac- left eye, but these responses were somewhat delayed. The tive error of +2.00 −0.75ϫ60°. Her acuity had generally Farnsworth D15 panel color vision was normal in the right been in the 20/40 to 20/50 range, but at her most recent eye and showed 1 minor error in the left eye. visit, 30 months postoperatively, her best-corrected vi- The macular lesion in the left eye showed evidence sual acuity was 20/30 OD. of preserved photoreceptor function within the lesion. Given her success with surgery in the right eye, the This conclusion was based on the patient’s ability to fix- patient inquired about surgery on the left eye. The pa- ate centrally in the left eye, the ability to see bright stimuli tient was assessed at the Wilmer Eye Institute, Balti- within the lesion, the presence of xanthophyll within the more, Md, in June 1999. The patient reported that her lesion, as demonstrated by argon blue imaging, and the left eye had always been her weaker eye. She also re- absence of a completely black appearance on autofluo- ported that she was occasionally aware of a blind spot in rescence imaging. Although her vision had been de- her left eye and that she had been aware of a blind spot creased to 20/100 or worse in this eye for 25 months, the in the right eye, but that this had resolved following the results of all her measurements suggested that there was translocation surgery. The patient reported some diffi- a reasonable chance for improvement in foveal function culty with night vision but normal color vision and pe- if macular translocation were performed. ripheral vision. Her best-corrected visual acuity, mea- The patient therefore underwent limited macular sured with an ETDRS (Early Treatment of Diabetic translocation in the left eye by one of us (J.D.B.) in June Retinopathy Study) chart, was 20/50 OD and 20/180 OS. 1999. This time, a different technique was performed, us- The patient missed the middle letters of some lines with ing radial scleral outpouching.7 The technique was oth- her left eye. Her Pelli-Robson contrast sensitivity was re- erwise identical to that performed in the right eye, ex- duced to 1.35 OD and 1.20 OS (normal, Ն1.65). No rela- cept that scleral shortening was performed by creating a tive afferent pupillary defect was present. A dilated ex- radial scleral outfold. A scleral folding clamp was used amination of the right fundus (Figure 1C) revealed an to create a radial scleral outfold, followed by placement atrophic lesion located superior to the fovea that was not of a full-thickness 6-0 Prolene (Ethicon Inc) horizontal as discrete and “punched out” as advanced geographic mattress suture to secure the radial fold. Postopera- RPE atrophy generally appears. In the left eye, there was tively, her course was uncomplicated, with macular trans- an atrophic lesion of similar character involving the fo- location of 832 µm and prompt retinal reattachment. Post- veal center (Figure 2A). The patient did not have high- operatively, her visual acuity remained in the 20/200 to risk drusen or the pigmentary alterations typically asso- 20/400 OS range, although at the Wilmer Eye Institute, ciated with a pattern dystrophy in either eye. she attained 20/100-2 with an ETDRS chart (improved Scanning laser ophthalmoscope (SLO) macular pe- from 20/180 preoperatively at the Wilmer Eye Institute) rimetry showed that fixation was inferior (on the retina) and 20/100 (Snellen) at 1 other visit. Her refractive er- to the atrophic RPE lesion in the right eye and that the ror was essentially unchanged from the preoperative level, area over the atrophic RPE lesion had a dense scotoma with no induced astigmatism in the left eye. At a fol-

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 low-up visit 22 months postoperatively, her best- determination in the left eye, and a 200-µm diameter slit- corrected visual acuity was 20/200. lamp spot was used to assess fixation in both eyes. An- She was reevaluated at Wilmer Eye Institute by one other indirect measure of viability and residual photore- of us (J.S.S.) in August 2000, which was 22 months post- ceptor function is the presence of xanthophyll within the operatively in the right eye (Figure 1F) and 14 months atrophic lesion.11 Xanthophyll may be visualized by oph- postoperatively in the left eye (Figure 2F). She reported thalmoscopic examination and standard fundus photog- that the vision in the right eye had gotten better and the raphy, but its visualization is enhanced using either argon vision in her left eye was better than it had been preop- blue SLO imaging or fundus photography with an appro- eratively. She reported that her night vision continued priate filter for detecting xanthophyll. Finally, the SLO can to be somewhat reduced, as it had been all her life. She be used to identify residual RPE within the atrophic area. denied having diplopia, except when looking at Christ- The SLO macular perimetry preoperatively showed fixa- mas lights. On this visit, her best-corrected visual acuity tion and residual function within the atrophic lesion (al- was 20/50-1 OD and 20/100-2 OS (ETDRS chart). She though postoperatively there was a dense scotoma of the was able to read 1 M print with the right eye and 2.5 M retina now overlying the atrophic lesion). Our patient had print with the left eye at 40 cm. The SLO macular pe- mottled, rather than totally black, autofluorescence in the rimetry showed a dense scotoma over the areas of RPE atrophic lesion. This provides further suggestive evidence atrophy in each eye (Figure 2G). Argon blue SLO imag- that the photoreceptors are viable and complements macu- ing of the left eye demonstrated that the xanthophyll area lar perimetry over the atrophic lesion.12 had been translocated inferior to the atrophic lesion, ex- The exact cause of this patient’s atrophic maculopa- cept for the superior-most portion, which remained par- thy is unclear. Her progressive visual loss in her late 70s tially over the atrophic RPE (Figure 2F). This was in con- and the well-circumscribed area of subfoveal RPE atrophy trast to the right eye, where the entire xanthophyll area are consistent with age-related macular degeneration. Yet, had completely cleared the atrophic lesion (Figure 1F). the absence of drusen, the blocked hypofluorescence on the fluorescein angiogram, and the retention of fixation COMMENT within the lesion are more consistent with a pattern dystrophy of the macula. Additionally, the pattern of a patchy VISUAL IMPROVEMENT decrease in autofluorescence seen with the SLO in this patient was different from the homogeneously black area (loss Several aspects of this case are remarkable. This patient of autofluorescence) seen in patients with geographic at- had a significant improvement in vision in her right eye rophy from age-related macular degeneration.12-15 The elec- after having had slowly progressive visual acuity loss, with tro-oculogram was normal, so Best disease was not the cause. acuity at 20/80 or worse for at least 17 months prior to The electroretinogram showed a mild reduction in cone the procedure in her right eye and for at least 37 months amplitudes and some delay in cone responses, suggesting prior to the procedure in her left eye. Her visual acuity a cone dystrophy, but the color vision was essentially nor- improved from 20/200 to 20/30 OD (best acuity, with acu- mal. The patient did not have a dark choroid or flecks that ities ranging from 20/30 to 20/50) and from 20/186 to would suggest Stargardt disease. The most likely diagno- 20/100 OS (best acuity, with acuities ranging from 20/ sis is RPE atrophy, resulting from pattern dystrophy. Early 100 to 20/200). The amount of foveal translocation was RPE changes and atrophy, from age-related macular de- greater in the right eye (1191 µm) than the left eye (832 generation and related conditions, may be associated with µm). As a result, the fovea (as delineated by the xantho- decreased retinal function even before frank geographic at- phyll) was relocated completely outside the atrophic RPE rophy occurs16,17; this decreased function may reverse with in the right eye and only partially outside the slightly larger translocation to a healthier area of RPE. atrophic area in the left eye. The more atrophic appear- Other forms of atrophic macular disease may not ben- ance of the lesion preoperatively and the longer dura- efit from translocation surgery, so careful consideration tion of visual loss may have accounted for the more lim- must be given to the likelihood of visual improvement. ited amount of improvement in the left eye. That her vision Geographic atrophy that already involves the fovea, with improved after having been decreased for so long sug- a dense central scotoma, will likely not benefit from trans- gests that her foveal photoreceptors had remained vi- location. Translocation that will move the fovea to an area able over the atrophic lesion during this time. After they that will likely develop frank RPE atrophy in the future were relocated to a new site over healthy RPE, the pho- is not likely to benefit the patient. For example, in a pa- toreceptors apparently were able to function more effec- tient with a bull’s-eye scotoma surrounding the foveal cen- tively, and her vision improved. ter, macular translocation might relocate the fovea to a site with a higher risk of becoming atrophic than the fo- PATIENT SELECTION veal center itself. Because geographic atrophy often de- velops in the parafoveal region first, thought must be given This case illustrates the use of macular translocation for to the health of the RPE in the area to which transloca- patients with atrophic macular disease. Preoperative evalu- tion is contemplated. The patient with geographic atro- ation of visual function may provide insight into which eyes phy from age-related macular degeneration most likely are likely to benefit from translocation. The most critical to benefit from macular translocation is one with recent element is residual photoreceptor function and foveal fixa- visual loss who has an isolated atrophic lesion just su- tion within the atrophic region prior to the procedure. In perior to the fovea that is threatening to spread into the this patient, the SLO evaluation was used to make this foveal center. In this case, macular translocation would

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©2002 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/29/2021 move the foveal center away from the atrophic RPE, This study was presented in part at the annual meet- reducing the likelihood that atrophy would spread to ing of the Association for Research in Vision and Ophthal- involve the new foveal center. mology, Ft Lauderdale, Fla, May 2, 2001, and at the an- This case suggests that limited macular transloca- nual meeting of the Macula Society, Scottsdale, Ariz, tion may be helpful for patients with certain other atro- February 28, 2001. phic maculopathies. However, the disease process caus- We thank Morton F. Goldberg, MD, for his critical re- ing the atrophy may well be a factor in determining view of the manuscript. whether surgery would be likely to be beneficial. If en- Corresponding author and reprints: Janet S. Sunness, largement of atrophy over time is anticipated, one might MD, 550 N Broadway, Sixth Floor, Baltimore, MD 21205 have to contemplate performing further translocation at (e-mail: [email protected]). a later time. In limited macular translocation, the fovea is generally translocated inferiorly because of anatomi- REFERENCES cal and surgical limitations. In terms of visual function, when the fovea is moved inferiorly, the atrophic lesion 1. Machemer R, Steinhorst UH. Retinal separation, retinotomy, and macular relo- is then positioned beneath a focal area of retina superior cation, II: a surgical approach for age-related macular degeneration? Graefes Arch to the fovea. The patient will then have a scotoma infe- Clin Exp Ophthalmol. 1993;231:635-641. rior to fixation (corresponding to the superior retina that 2. de Juan E, Loewenstein A, Bressler NM, Alexander J. 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Eckhardt C, Eckhardt U, Conrad HG. Macular rotation with and without counter- ranted remains to be seen. rotation of the globe in patients with age-related macular degeneration. Graefes Arch Clin Exp Ophthalmol. 1999;237:313-325. POSTOPERATIVE LOSS OF FUNCTION OF 6. Lewis H, Kaiser PK, Lewis S, Estafanous M. Macular translocation for subfoveal choroidal neovascularization in age-related macular degeneration: a prospec- RETINA OVERLYING THE ATROPHIC LESION tive study. Am J Ophthalmol. 1999;128:135-146. 7. Benner JD, Meyer CH, Shirkey BL, Toth CA. Macular translocation with radial An interesting observation was the loss of functioning retina scleral outfolding: experimental studies and initial human results. Graefes Arch in the region that came to reside over the RPE atrophy in Clin Exp Ophthalmol. 2001;239:815-823. 8. Green WR, Enger C. Age-related macular degeneration histopathologic stud- each eye after surgery. This was demonstrated at 8 months ies: the 1992 Lorenz E. 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Invest Ophthal- lowing the translocation surgery, the retina that was re- mol Vis Sci. 1999;40:1761-1769. 12. Sunness JS, Ziegler M, Fujii G, Tian Y, Bressler NM, Applegate CA. The use of located over the RPE atrophy, and had previously tested SLO autofluorescence imaging to define and quantify atrophy in macular dis- normal with the SLO, now had a dense scotoma. The fact ease [abstract]. Invest Ophthalmol Vis Sci. 2000;41(suppl 2):S959. that function remained in the foveal retinal area overly- 13. Holz FG, Bellmann C, Margaritidis M, Schutt F, Otto TP, Volcker HE. Patterns of ing the RPE prior to translocation could be due to spe- increased in vivo fundus autofluorescence in the junctional zone of geographic cific protection conferred on the foveal photoreceptors, atrophy of the retinal pigment epithelium associated with age-related macular degeneration. Graefes Arch Clin Exp Ophthalmol. 1999;237:145-152. or it may reflect additional damage to the RPE-pho- 14. Holz FG, Bellman C, Staudt S, Schutt F, Volcker HE. Fundus autofluorescence toreceptor interface following translocation. and development of geographic atrophy in age-related macular degeneration. In- vest Ophthalmol Vis Sci. 2001;42:1051-1056. Submitted for publication May 31, 2001; final revision re- 15. Von Ruckmann A, Fitzke FW, Bird AC. Fundus autofluorescence in age-related macular degeneration imaged with a laser scanning ophthalmoscope. Invest Oph- ceived December 28, 2001; accepted January 24, 2002. thalmol Vis Sci. 1997;38:478-486. This study was supported in part by grant NEI EY08552 16. Midena E, Angeli CD, Blarzino MC, Valenti M, Segato T. Macular function im- from the National Eye Institute, Bethesda, Md, and the James pairment in eyes with early age-related macular degeneration. Invest Ophthal- S. Adams Research to Prevent Blindness Special Scholar mol Vis Sci. 1997;38:469-477. Award, New York, NY (Dr Sunness); the John A. Hartford 17. Sunness JS, Massof RW, Johnson MA, Finkelstein D, Fine SL. Peripheral retinal function in age-related macular degeneration. Arch Ophthalmol. 1985;103:811- Foundation/American Federation of Aging Research Medi- 816. cal Student Geriatric Scholars Program, New York (Dr Sun- 18. Guez JE, Le Gargasson JF, Rigaudiere F, O’Regan JK. Is there a systematic lo- ness and Mr Soltanian); the Panitch Fund to Stop Age- cation for the pseudo-fovea in patients with central scotoma? Vision Res. 1993; Related Macular Degeneration, Baltimore; core grant NEI 9:1271-1279. 19. Sunness JS, Applegate CA, Haselwood D, Rubin GS. Fixation patterns and read- 2 P30 EY01765-24 from the National Eye Institute; and an ing rates in eyes with central scotomas from advanced atrophic age-related macu- unrestricted research grant from Research to Prevent Blind- lar degeneration and Stargardt’s disease. Ophthalmology. 1996;103:1458- ness to the Wilmer Eye Institute. 1466.

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