The Visual Performance and Metamorphopsia of Patients with Macular Holes

CLINICAL SCIENCES The Visual Performance and Metamorphopsia of Patients With Macular Holes

Yoshihiro Saito, MD; Yoshiko Hirata, MD; Atsushi Hayashi, MD; Takashi Fujikado, MD; Masahito Ohji, MD; Yasuo Tano, MD

Background: Most patients attain better visual acuity divided the subjective changes into 2 types of metamor- with the elimination of metamorphopsia after success- phopsia; of the 54 eyes, pincushion distortion (bowed ful closure of a macular hole (MH) by vitrectomy. toward the center) was found in 33 (61%), and unpatterned distortion (no specific pattern) was found in 21 Objective: To determine the presurgical visual func- (39%). Pincushion distortion was significantly associ- tion of eyes with an MH. ated with an MH of shorter duration (Յ6 months) (P = .03) and an early stage (stage 2) of MH formation Methods: We examined 54 eyes of 51 patients with an (P = .02). A scotoma was hard to detect, and patients had idiopathic MH using the Amsler chart. We evaluated difficulty describing their scotomata and distortions. In the types of subjective metamorphopsia and compared the montage test, patients with early MHs chose por- them with the clinical factors associated with MHs. In a traits modified with a pincushion type of distortion. prospective study, we performed a montage test on a separate group of 16 patients with unilateral idiopathic Conclusions: We found concentric pincushion meta- MHs. The patients were asked to choose, while viewing morphopsia without subjective scotomata, which we sug- with their better eye, the computer-modified picture gest arises from an eccentric displacement of the photo- that best matched the unmodified image seen by the eye receptors. This accounts for the main characteristic of the with the MH. visual performance of patients with idiopathic MHs.

Results: From the results of the Amsler chart test, we Arch Ophthalmol. 2000;118:41-46

ELLY AND Wendel1 and the hole. The presence of these alter- others2-4 have reported on ations would be expected to produce a cen- the effect of the closure of tral absolute scotoma surrounded by an idiopathic macular holes area of metamorphopsia. When we exam- (MHs) on the recovery of ine the patients’ subjective symptoms, visualK function after pars plana vitrec- however, only a few patients have a sco- tomy and gas tamponade. After the suc- toma and the most consistent complaint cessful closure of the holes, many is that objects appeared distorted, frag- patients gain better visual acuity with the mented, or both (ie, metamorphopsia). disappearance of the presurgical meta- One of the methods used to detect morphopsia.5-7 However, relatively little functional visual changes is the Amsler attention has been paid to the quality of chart test.11,12 It is a rapid and sensitive visual function in the presence of MHs, technique for evaluating 10° of the cen- ie, the presurgical visual function. tral visual field in patients with macular The visual loss in eyes with a full- changes.13 Recently, it has been used to de- thickness MH is thought to be caused by tect the early signs of macular changes in the absence of the neurosensory retina in the fellow eye of patients with visual loss the area of the anatomical defect and by the from age-related macular degeneration. reduction of retinal function in the sur- Johnson and Gass14 conducted Amsler rounding area of retinal detachment.8 Pre- chart testing in patients with MHs and re- From the Departments of operative microperimetry with a scanning ported that metamorphopsia was the main Ophthalmology, Osaka laser ophthalmoscope has demonstrated an symptom. University Medical School, Osaka (Drs Saito, Hirata, absolute scotoma with a relative scotoma In this study, we studied in more de- Hayashi, Fujikado, Ohji, and in the surrounding concentric isopters that tail the visual performance of patients with 9,10 Tano), and Hyogo Prefectural corresponded to the anatomical defect. idiopathic MHs using the Amsler chart. We Nishinomiya Hospital, Histological studies have shown the found that the characteristic central meta- Nishinomiya (Dr Saito), Japan. absence of all retinal layers in the area of morphopsia was a pincushion distortion,

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©2000 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 pincushion distortion that made lines bowed toward the center (Figure 1, A), and the second was unpatterned PATIENTS AND METHODS metamorphopsia (Figure 1, B) that had no specific pattern. Of the 54 eyes, pincushion distortion was found in Between January 9, 1995, and December 19, 1997, 33 (61%) and unpatterned metamorphopsia was found in we examined 54 eyes of 51 patients with an idio- 21 (39%). The Table shows the clinical features associ- pathic MH using the Amsler chart. The research fol- ated with the metamorphopsia as determined by Amsler lowed the tenets of the Declaration of Helsinki, in- chart testing. A pincushion distortion was significantly as- formed consent was obtained from all participants, sociated with an MH of shorter duration (Յ6 months) and and the research was approved by the Departmental with an earlier stage of MH (stage 2). Review Board of Osaka University, Osaka, Japan. Because there was metamorphopsia in all of the pa- There were 16 men and 35 women whose mean ± SD tients, the central scotoma was usually difficult to delin- age was 64.3 ± 6.5 years (range, 45-77 years). Fun- eate. Although most of the patients complained of loss dus examinations were performed with a double of central vision, a scotoma or the disappearance of the aspheric indirect lens (Super Field; Volk Optical Inc, Mentor, Ohio) or a +78-diopter lens. When there was fixation dot was hard to detect. The patients stated that a question about the MH, microperimetry with a scan- when they gazed a little away from the central dot, it be- ning laser ophthalmoscope was used to separate a came easier to find the dot. pseudo-MH from a true full-thickness MH.10 For the montage test, we modified the classic Mona Using Gass classification,16 there were 16 eyes Lisa portrait as follows: unmodified (Figure 2, A), a sco- with stage 2, 32 eyes with stage 3, and 6 eyes with toma in the face (Figure 2, B), a pincushion distortion stage 4 MHs. The duration of the MH, based on the between the eyebrows (Figure 2, C), and a pincushion patient’s complaint, was 0.2 to 48 months (mean ± SD, distortion with a small central area removed from the left 5.0 ± 9.1 months). The preoperative visual acuities eye (Figure 2, D). When viewed, all of the patients ranged from 0.02 to 0.80. promptly denied seeing a central scotoma in Figure 2, We examined the results of the Amsler tests of the patients retrospectively, and evaluated the type B. The patients had difficulty describing their scoto- of metamorphopsia. The type of metamorphopsia was mata and distortions precisely; however, all patients se- compared with the duration of the MH, the stage of lected the pincushion photograph as their perception with the MH, and the preoperative visual acuity. The Am- the eye with the MH (Figure 2, C and D). The difference sler chart examinations were carried out by the in their description was in the location, size, or both of method recommended by Amsler,11 with a working the pincushion lesion in the photographs. Two patients distance of 0.3 m and the use of the same spectacle stated that the pincushion area appeared darker than other correction as used to test the reading acuity. Statis- parts of the photograph. tical analysis was performed using the ␹2 test or the Fisher exact test. Between January 12, 1998, and December 18, COMMENT 1998, a separate group of 16 patients with unilateral idiopathic MHs (stage 2, 4 patients; stage 3, 10 pa- Our results indicated that approximately 70% of the patients; and stage 4, 2 patients) was studied to deter- tients with a fresh MH (duration, Յ6 months) have meta- mine the visual perception of patients with an MH. morphopsia of the pincushion type. After a comprehen- The patients consisted of 4 men and 12 women (mean sive study of the development of an MH, Gass15,16 age, 66 years; range, 55-83 years). The duration of established a classification of MHs, including the en- the MH was less than 6 months. largement of retinal tissue resulting from a tangential trac- These patients were shown 4 photographs 17 ϫ tion of the vitreous. Smith and associates also implied (10 13 cm) of a painting (Leonardo da Vinci’s Mona that the enlargement of the MH occurs without tissue loss Lisa), an unmodified picture and 3 that had been modified using computer software (Adobe Photo- around the macula. We have obtained evidence support- shop; Adobe Systems Inc, San Jose, Calif). While viewing the hypothesis by Gass, namely, an enlargement of ing the pictures with their unaffected eye, they were the MH with displacement of the photoreceptors. asked to select the portrait that best resembled the Can these observations on patients with an MH tell unmodified photograph seen by the affected eye. us anything about the retinal pathological characteristics? Assume a vertical line is imaged on the retina a few degrees from the fovea (Figure 3, A). If the line is to be perceived as bowing inward at the center, ie, a pincush- ie, a distortion bowed toward the center of the hole. We ion type of distortion, the center of the line must be clos- suggest that this results from the displacement of the pho- est to the fovea and the eccentric points of the line must toreceptors due to the tangential traction by the poste- fall on retinal points of increasing distance from the ver- rior vitreous.15 We also allowed patients to view computer- tical meridian (Figure 3, B). For this to happen, the pho- modified pictures, and we hypothesized about how the toreceptors underlying the bowed line must be dis- MH affected the visual function of patients. placed (Figure 3, C) toward the vertical line shown in Figure 3, A, ie, from A through F to AЈ through FЈ. If this RESULTS movement of the photoreceptors occurs as by the traction of the retina, the image of the vertical line will fall From the results of the Amsler chart testing, the meta- on photoreceptors that will project the image as if it arose morphopsia was divided into 2 types. The first type was a from stimulation of A through F, ie, a curved line bow-

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Pincushion Unpatterned

Figure 1. Plots from the Amsler chart test. A, A pincushion distortion in a patient with an early macular hole. B, Unpatterned metamorphopsia in a patient with a long-standing macular hole.

ing toward the center. This would then imply that the retina would be displaced the most at the center and pro- Characteristics of Metamorphopsia by Amsler Chart Testing gressively less in the peripheral portion. This agrees well and Factors Associated With the MH* with the appearance of an MH as observed by indirect ophthalmoscopy. Type of Metamorphopsia The Amsler chart consists of a grid with vertical and Pincushion Unpatterned horizontal lines with a fixation dot in the center. If we MH Features (n = 33) (n = 21) P use a chart with only vertical lines and a fixation dot, we Duration, mo Figure 4 Յ63013 can represent the patient’s view ( ). With an MH .03 and the displacement of the retina, the brain’s image of Ͼ638 straight lines is bent toward the center (the pincushion Stage 2142 distortion) and the fixation dot is not seen by the pa- 3 17 15 .02 tient with an MH (the central scotoma). This agrees well 424 with the main characteristic of metamorphopsia in pa- Preoperative VA Ͻ20/100 19 8 tients with an MH as a pincushion distortion with a de- .20 fect of the central visual field. The central dot in the chart Ն20/100 14 13 cannot be recognized because of the MH, although most patients can point out the central dot by eccentric fixa- *MH indicates macular hole; VA, visual acuity. tion. An MH is usually accompanied by a fluid cuff around acteristics of metamorphopsia can be caused by these rea- the hole leading to functional damage to the retina sur- sons. Thus, patients with an MH of short duration who rounding the MH (Figure 5), and the patient’s percep- maintain good photoreceptor function with less adapta- tion will be more complicated than the anatomical al- tion or fill-in phenomenon in the brain are more sensi- terations. The reason why some patients with an MH have tive to the pincushion distortion as a defect of the cen- metamorphopsia without any specific pattern (unpat- tral visual field. terned) is probably due to the duration of the MH, namely, The enlargement of the hole without tissue loss there may be more damage to the surrounding macular around the macula, ie, retinal photoreceptor displace- region with an MH of longer duration. In addition, we ment, was also confirmed by Jensen and Larsen19 using must also be aware of suppression in the brain as an ad- differential perimetry. They reported a discrepancy in the aptation to the metamorphopsia. If one assumes that the size of the objective and subjective scotoma by differen- foveal cells can also become nonfunctioning in long- tial perimetry using red and green filter glasses. They standing cases, then there would be a true foveal sco- found that the subjective scotoma was concentric but con- toma, rather than a remapping. Schuchard18 illustrated siderably smaller than the objective scotoma in patients that scotomata frequently are “filled in” perceptually, and with symptoms for less than 6 months. In patients with patients often report the filling in as distortions similar a documented duration of symptoms for longer than 2 to the unpatterned distortions described herein. In this years, no discrepancy was found between the objective case, the distortion might be attributed to an active cor- and subjective scotomata. tical phenomenon rather than simply an extension of the We also investigated the theoretical basis of the abnormal retinotopic projection hypothesis. The signifi- Watzke-Allen sign (Figure 6). Patients with a full- cant (P = .03) correlation between MH duration and char- thickness MH can describe a complete break in a vertical

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C D

Figure 2. Photographs of a Mona Lisa portrait modified by computer software. A, Normal portrait. B, Scotoma in a part of the face. C, Pincushion modification between the eyebrows using a pinch filter. D, Pincushion modification with deletion of a small area of the left eye mainly by a pinch filter. The original picture size is 10 ϫ13 cm. For a viewing distance of 0.3 m, the scotoma and pinch-filtered area are approximately 2° and 4°, respectively.

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B B′

C C′ Fovea Fovea D D′ E E′ F F′

Figure 3. A, A straight line projected on the retina. B, A pincushion-type line imaged on the retina. C, Both lines on the retina. If a straight line is to be seen as a curved line, the retinal points A through F must move to AЈ through F Ј or the photoreceptors must be displaced so that they underlie AЈ through F Ј. When any of the primed letters are stimulated, they will be perceived as originating from A through F retinal points.

A B

Lines and a Dot Macular Normal Projected on Hole the Macular Photoreceptor

Lines and a Dot Recognized in the Brain

Normal Macular Hole

Figure 4. Theoretical background of Amsler chart testing for a macular hole. Figure 6. Theoretical basis of Watzke-Allen testing. Because of the eccentric Light dots represent photoreceptors of a normal retina (A) and a retina with a displacement of the macular photoreceptors, a slit of light oriented macular hole (B) that revealed eccentric displacement. The central dot of the perpendicularly and crossing the macular hole is usually reported as thinning chart cannot be recognized because of the macular hole, ie, absence of the of the beam by the brain. retina. other piece of evidence for the displacement of the pho- A B toreceptor. We found concentric pincushion metamorphopsia without a subjective scotoma, which we suggest arises from an eccentric displacement of the retina. This ac- Eccentric counts for the main characteristics of the visual perfor- Movement of the mance of patients with an idiopathic MH. Photoreceptor Accepted for publication July 13, 1999. Reprints: Yoshihiro Saito, MD, Department of Oph- thalmology, Hyogo Prefectural Nishinomiya Hospital, 13-9 Rokutanji, Nishinomiya 662-0918, Japan (e-mail:

A Straight Line Projected Brain Image of the Straight Line [email protected]). on the Macular Hole in the Patient

Figure 5. A straight line of the Amsler chart projected on the macular hole REFERENCES (A). Theoretically, the brain image of the straight line is bent toward the center (B). However, because the retina around the macular hole (black dots) 1. Kelly NE, Wendel RT. Vitreous surgery for idiopathic macular holes: results of a may be damaged functionally, the patient’s view will be more complicated. pilot study. Arch Ophthalmol. 1991;109:654-659. 2. Poliner LS, Tornambe PE. Retinal pigment epitheliopathy after macular hole sur- light beam,20 although this sign is not always reliable. Care- gery. Ophthalmology. 1992;99:1671-1677. 3. Glaser BM, Michels RG, Kuppermann BD, Sjaarda RN, Pena RA. Transforming ful questioning of the patient during the testing is im- growth factor-␤ 2 for the treatment of full-thickness macular holes: a prospec- portant to determine whether a complete break or a thin- tive randomized study. Ophthalmology. 1992;99:1162-1172. ning of the light beam is being perceived.21,22 Because of 4. Liggett PE, Skolik SA, Horio B, Saito Y, Alfaro DV, Mieler W. Human autologous the eccentric displacement of the macular retina, a slit serum for the treatment of full-thickness macular holes. Ophthalmology. 1995; 102:1071-1076. light beam oriented perpendicularly and centered on the 5. Maeno T, Hattori T, Ninomiya Y, et al. Visual functional changes in idiopathic macular lesion is usually perceived as a thinning of the macular holes treated by vitrectomy. Nippon Ganka Gakkai Zasshi. 1996;100: slit light beam by the brain. This phenomenon is an- 40-45.

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©2000 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 6. Liesenhoff O, Messmer EM, Pulur A, Kampik A. Surgical management of com- 14. Johnson RN, Gass JDM. Idiopathic macular holes: observations, stages of for- plete macular foramina. Ophthalmologe. 1996;93:655-659. mation, and implication for surgical intervention. Ophthalmology. 1988;95:917- 7. Matsumura M. Impressions: a patient’s view [letter]. Retina. 1998;18:489. 924. 8. Sjaarda RN, Frank DA, Glaser BM, Thompson JT, Murphy RP. Resolution of an 15. Gass JDM. Idiopathic senile macular hole: its early stages and pathogenesis. Arch absolute scotoma and improvement of relative scotomata after successful macu- Ophthalmol. 1988;106:629-639. lar hole surgery. Am J Ophthalmol. 1993;116:129-139. 16. Gass JDM. Reappraisal of biomicroscopic classification of stages of develop- 9. Acosta F, Lashkari K, Raynaud X, Jalkh AE, Van de Velde F, Chedid N. Charac- ment of a macular hole. Am J Ophthalmol. 1995;119:752-759. terization of functional changes in macular holes and cysts. Ophthalmology. 1991; 17. Smith RG, Hardmanlea SJ, Galloway NR. Visual performance in idiopathic macu- 98:1820-1823. lar holes. Eye. 1990;4:190-194. 10. Tsujikawa M, Ohji M, Fujikado T, et al. Differentiating full thickness macular holes 18. Schuchard RA. Validity and interpretation of Amsler grid reports. Arch Ophthal- from impending macular holes and macular pseudoholes. Br J Ophthalmol. 1997; mol. 1993;111:776-780. 81:117-122. 19. Jensen OM, Larsen M. Objective assessment of photoreceptor displacement and 11. Amsler M. Quantitative and qualitative vision. Trans Ophthalmol Soc U K. 1949; metamorphopsia. Arch Ophthalmol. 1998;116:1303-1306. 69:397-410. 20. Watzke RC, Allen L. Subjective slit beam sign for macular diseases. Am J Oph- 12. Amsler M. Earliest symptoms of disease of the macula. Br J Ophthalmol. 1953; thalmol. 1969;68:449-453. 37:521-537. 21. Martinez J, Smiddy WE, Kim J, Gass JDM. Differentiating macular holes from 13. Walsh AR, Magargal LM, Wright F, Donoso LA. The early natural history of sub- macular pseudoholes. Am J Ophthalmol. 1994;117:762-767. foveal neovascular membranes in eyes with age-related macular degeneration. 22. Smiddy WE, Gass JDM. Masquerades of macular holes. Ophthalmic Surg La- Ann Ophthalmol. 1989;21:348-350. sers. 1995;26:16-24.

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