Tomographic assessment of vitreous surgery for diabetic macular edema

Tomographic Assessment of Vitreous Surgery for Diabetic Macular Edema TOMOHIRO OTANI, MD, AND SHOJI KISHI, MD

● PURPOSE:

To evaluate the retinal structure before and after vitrectomy for diabetic macular edema and to assess the correlation between thickness of neurosensory retina and best-corrected visual acuity. ● METHODS: Tomographic features of 13 eyes (nine patients) with diabetic macular edema were prospectively evaluated with optical coherence tomography before and after vitrectomy. The foveal thickness (the distance between the inner retinal surface and the retinal pigment epithelium) and the retinal thickness (thickness of neurosensory retina) were measured by optical coherence tomography preoperatively and postoperatively. The correlation of the best-corrected visual acuity with foveal and retinal thickness was determined. ● RESULTS: All 13 eyes had retinal swelling with low intraretinal reflectivity. In addition to retinal swelling, there were cystoid spaces in five (38%) of 13 eyes, a serous retinal detachment in three (23%), and both cystoid spaces and serous detachment in three (23%). Six months postoperatively, the mean foveal thickness significantly decreased from 630 ⴞ 170 to 350 ⴞ 120 ␮m (P < .01, paired t test) and the mean thickness of neurosensory retina decreased from 540 ⴞ 160 to 320 ⴞ 140 ␮m (P < .01, paired t test). A serous retinal detachment occurred transiently in 3 eyes. Compared with the preoperative level, the postoperative best-corrected visual acuity level improved by more than 2 lines in five of the 13 eyes (38%), remained the same in seven eyes (54%), and decreased in one eye (8%). The postoperative thickness of neurosensory retina at the fovea and best-corrected visual acuity level at the sixth postoperative month had a strong negative correlation (correlation coefficient, ⴚ0.76; P < .01, Spearmans rank test). ● CONCLUSIONS: Vitrectomy was generally effective in treatment of diabetic macular edema. Optical coherence Accepted for publication Oct 15, 1999. From the Department of Ophthalmology, Gunma University School of Medicine, Maebashi, Gunma, Japan. This study was supported by grants from the Ministry of Education, Science and Culture of Japan, Tokyo, Japan. Reprint requests to Tomohiro Otani, MD, Department of Ophthalmology, Gunma University School of Medicine, 3 Showamachi, Maebashi, Gunma 371-8511, Japan; fax: 81-27-233-3841; e-mail: [email protected] 0002-9394/00/$20.00 PII S0002-9394(99)00409-2

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tomography demonstrated the intraretinal changes of macular edema and the process of edema absorption. During the process of macular edema absorption, intraretinal fluid appeared to move into the subretinal space in some cases. Best-corrected visual acuity improvement was greater in eyes with less preoperative increase in thickness of neurosensory retina. (Am J Ophthalmol 2000;129:487– 494. © 2000 by Elsevier Science Inc. All rights reserved.)

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ACULAR EDEMA IS A LEADING CAUSE OF VISUAL

loss in diabetic retinopathy. Grid-pattern laser photocoagulation is indicated for diffuse macular edema; however, it has limited efficacy.1 Lewis and associates2 reported the efficacy of vitrectomy for diabetic macular edema with a thickened and taut posterior hyaloid. Tachi and Ogino3 stated that vitrectomy is beneficial in eyes with diffuse macular edema without a thick posterior hyaloid. The posterior precortical vitreous pocket or premacular liquefied pocket is physiologically present anterior to the macular area in adult eyes.4 The posterior wall of the pocket is composed of a thin layer of vitreous cortex, which is in contact with the neurosensory retina in the macular area. The contraction of the premacular vitreous cortex generates anterior traction on the macula, which may lead to the development of an idiopathic macular hole.5 In diabetic retinopathy, contraction of the premacular cortex occasionally causes a trampoline-like shallow posterior vitreous detachment in the posterior fundus.6 This anterior traction produced by the premacular vitreous cortex may worsen macular edema.2 We performed vitrectomy to treat diabetic macular edema and eliminate the vitreous traction by detaching the premacular vitreous cortex from the retina. We prospectively evaluated the surgical outcomes using optical coherence tomography.

PATIENTS AND METHODS NINE PATIENTS WITH DIABETES (SEVEN MEN AND TWO

women; 13 eyes) ages 46 to 68 years (average, 58 years)

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FIGURE 1. Case 1. Fundus photograph of a 47-year-old man with diabetic macular edema. The vertical arrow indicates the line and the direction of scanning of the optical coherence tomograph. (Top left) Preoperative photograph. The best-corrected visual acuity is 20/500. (Top right) Two months after vitrectomy, the best-corrected visual acuity is 20/300. (Bottom left) Four months after vitrectomy, hard exudates are seen; the best-corrected visual acuity is 20/200. (Bottom right) Ten months after vitrectomy, the hard exudates have been absorbed; the best-corrected visual acuity is 20/70.

made up the study population. The inclusion criteria for this study were as follows: clinically detectable diffuse or cystoid macular edema for more than 3 months; bestcorrected visual acuity worse than 20/40 before vitrectomy; follow-up period of more than 6 months after surgery; no dense media opacity before and after surgery, such as cataract, vitreous hemorrhage, and so on; neither tractional retinal detachment nor active neovascularization. After informed consent was obtained, all patients underwent vitrectomy at Gunma University Hospital from May 1997 to April 1998 and were followed for 6 to 18 months (average, 10 months) postoperatively. Before surgery, panretinal photocoagulation had been performed in nine eyes and focal photocoagulation in four eyes. Intraoperatively, the posterior vitreous cortex was detached from the retina by suction after core vitrectomy in all 13 eyes with no posterior vitreous detachment. 488

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In addition to a comprehensive ophthalmic examination including best-corrected visual acuity, optical coherence tomography (Humphrey model 2000; Humphrey Instruments, San Leandro, California) was performed and best-corrected visual acuity was obtained at the same time in all eyes within 2 weeks before vitrectomy. After vitrectomy, optical coherence tomography was performed within 1 month and repeated once during the ensuing 2 or 3 months. The fundi were scanned with a measurement beam focused on the horizontal and vertical planes crossing the central fovea, which was determined by the fundus photograph. All eyes were examined at scan lengths of 2.8 and 5.0 mm. We defined the foveal thickness at the central fovea as the distance between the inner retinal surface and the retinal pigment epithelium, which included the serous retinal detachment. The measurement was automatically OF

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FIGURE 2. Case 2. Fundus photograph of a 70-year-old woman with diabetic macular edema. The vertical arrow indicates the line and the direction of scanning of the optical coherence tomograph. (Top left) Before vitrectomy, cystoid macular edema is seen; the best-corrected visual acuity is 20/70. (Top right) Two months after vitrectomy, the best-corrected visual acuity is 20/30. (Bottom left) Four months after vitrectomy, the cystoid macular edema disappeared; the best-corrected visual acuity is 20/30. (Bottom right) Nine months after vitrectomy, the best-corrected visual acuity is 20/25.

determined by computer. The thickness of neurosensory retina was defined as the distance between the inner and outer neurosensory retinal surfaces. We analyzed the correlation between the best-corrected visual acuity and the foveal and thickness of neurosensory retina. The correlation coefficient was calculated by Spearmans rank test. Best-corrected visual acuity was converted to the logarithm of the minimum angle of resolution (logMAR) and averaged.

observed in all 13 eyes, moreover cystoid macular edema in eight eyes (Figures 1 through 3). No serous retinal detachment could be detected (Figures 1 through 3). Optical coherence tomography showed retinal swelling in all 13

eyes. An area of low reflectivity was mainly located in the outer retina. In addition to retinal swelling, there were cystoid spaces in five (38%) of 13 eyes, a serous retinal detachment in three eyes (23%), and both cystoid spaces and serous retinal detachment in three eyes (23%). The foveal thickness ranged from 390 to 840 ␮m (average, 630 ⫾ 170 ␮m). A serous retinal detachment was seen in six of 13 eyes. The height of the subretinal space was greatest at the central fovea (average, 250 ⫾ 180 ␮m). The thickness of neurosensory retina at the central fovea ranged from 310 to 840 ␮m (average, 540 ⫾ 160 ␮m). The preoperative best-corrected visual acuity levels ranged from 20/40 to 20/500 (average, 20/100). Macular edema was gradually absorbed (Figures 1 through 3). Hard exudate increased on the process (Figures 1 and 3). The area of low reflectivity in the outer retina gradually diminished, and tissue reflectivity increased (Figure 4). The cystoid spaces flattened and disappeared in five

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FIGURE 3. Case 3. Fundus photograph of a 53-year-old man with diabetic macular edema. The vertical arrow indicates the line and the direction of scanning of the optical coherence tomograph. (Top left) Before vitrectomy, the best-corrected visual acuity is 20/70. (Top right) One month after vitrectomy, the best-corrected visual acuity is 20/70. (Bottom left) Three months after vitrectomy, the best-corrected visual acuity is 20/70. (Bottom right) Five months after vitrectomy, hard exudates have emerged during absorption of macular edema; the best-corrected visual acuity is 20/25.

of eight eyes within 6 months postoperatively (Figure 5). The height of the subretinal space decreased in all six eyes with a serous retinal detachment and resolved completely in two eyes within 6 months postoperatively (Figure 6). During absorption of the intraretinal macular edema, the serous retinal detachment enlarged temporarily in three eyes (Figures 4 and 5), and developed temporarily in three eyes. Six months postoperatively, the foveal thickness ranged from 120 to 500 ␮m (average, 350 ⫾ 120 ␮m). The thickness of neurosensory retina at the central fovea ranged from 120 to 500 ␮m (average, 320 ⫾ 140 ␮m). Both foveal and retinal thickness significantly decreased (P ⬍ .01, paired t test). Within 6 months postoperatively, the foveal thickness decreased to less than 50% of the preoperative foveal thickness in six of 13 eyes (46%), 50% to 80% in two eyes (15%), and 80% to 100% in four eyes (31%). In one eye, the foveal thickness increased because 490

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of retinal swelling at 6 months postoperatively compared with the preoperative level. The best-corrected visual acuity levels ranged from 20/25 to 20/400 (average, 20/70) at the sixth month postoperatively. Compared with the preoperative level, the postoperative vision improved by more than 2 lines in five (38%) of 13 eyes, remained the same in seven eyes (54%), and worsened in one eye (8%) (Figure 7). Four of the six eyes in which the foveal thickness decreased by more than 50% of the preoperative measurement gained more than 2 lines of best-corrected visual acuity (Figure 8). The remaining two eyes had an accumulation of hard exudates after resolution of the macular edema; the best-corrected visual acuity remained the same in one eye and worsened in another eye. The eyes with better preoperative best-corrected visual acuity tended to have better postoperative best-corrected visual acuity levels. The preoperative and the postoperaOF

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FIGURE 4. Case 1. Optical coherence tomographic findings. (Top left) Before vitrectomy, the retina is thickened with an area of low intraretinal reflectivity (yellow arrows) and cystoid cavities are seen in the retina. The fovea protrudes. A serous retinal detachment is seen at the fovea (white arrows); the foveal thickness is 780 ␮m. (Top right) Two months after vitrectomy, a serous retinal detachment (white arrows) is enlarged in diameter. (Bottom left) Four months after vitrectomy, an intraretinal area of low reflectivity is diminished and the serous retinal detachment has resolved; the foveal thickness decreased to 400 ␮m. (Bottom right) Ten months after vitrectomy, the foveal pit is restored.

tive best-corrected visual acuity levels at 6 months (Figure 7) showed an intermediate correlation (correlation coefficient, ⫺0.58; P ⬍ .05). The preoperative foveal thickness and best-corrected visual acuity at the sixth postoperative month had no significant correlation (correlation coefficient, ⫺0.27; P ⬍ .82). The preoperative thickness of neurosensory retina at the fovea and the best-corrected visual acuity at the sixth postoperative month (Figure 9) had a strong negative correlation (correlation coefficient, ⫺0.76; P ⬍ .01).

tional images of macular edema and the pattern of its absorption. All 13 study eyes had retinal thickening and

decreased intraretinal reflectivity. An area of low reflectivity was mainly located in the outer retina. The outer plexiform layer is known to be the preferential site for retinal edema.7 Low reflectivity of the outer retina seems to reflect the swelling of this layer.8,9 In addition to retinal swelling, cystoid cavities, which were located in the middle retinal layer, were seen in eight eyes (62%). The optical coherence tomography findings are consistent with histologic reports of cystoid macular edema, which is mainly located in the outer plexiform layer. Optical coherence tomography revealed a serous retinal detachment in six eyes (46%) with macular edema. Serous retinal detachment was distinguished from the outer retinal fluid accumulation by the highly reflective line that represented the outer surface of the detached retina.10 During absorption of the macular edema, retinal reflectivity increased and the area of low reflectivity of the outer

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FIGURE 5. Case 2. Optical coherence tomographic findings. (Top left) Before vitrectomy, cystoid cavities and slight serous retinal detachment (white arrows) are seen at the macula; the foveal thickness is 580 ␮m. (Top right) Two months after vitrectomy, the cystoid cavities are flat, but the serous retinal detachment has enlarged (white arrows); the foveal thickness is 410 ␮m. (Bottom left) Four months after vitrectomy, the cystoid cavities are smaller; the serous retinal detachment remains unchanged. (Bottom right) Nine months after vitrectomy, the cystoid spaces have disappeared and the foveal pit is restored; the serous retina detachment is still present. Foveal thickness is 230 ␮m.

retina diminished. This represents the increased tissue density along with absorption of the retinal edema. Six months after vitrectomy, the thickness of neurosensory retina decreased to less than 50% of the preoperative level in six of 13 eyes. The cystoid spaces flattened and disappeared in five of eight eyes within 6 months postoperatively. In the six eyes with a serous retinal detachment, the height of the subretinal space decreased in all six eyes and disappeared completely in two eyes. During macular edema absorption, serous retinal detachment transiently enlarged in three eyes and developed temporarily in three eyes. According to histopathologic reports, retinal edema starts as intracytoplasmic swelling of the Mu¨ller cells.7 Intracytoplasmic fluid seems to exude into the extracellular spaces, which may result in cystoid macular edema or subretinal fluid accumulation. Transient serous retinal detachment may represent fluid movement 492

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from the retina to the subretinal space during the process of macular edema absorption. The postoperative best-corrected visual acuity was affected by the preoperative thickness of neurosensory retina and not by the preoperative foveal thickness. Best-corrected visual acuity did not improve in two eyes with severe retinal swelling in which the thickness of neurosensory retina was more than 800 ␮m, despite the fact that the postoperative thickness of neurosensory retina decreased to less than half of the preoperative level. In these two eyes, hard exudates aggregated at the fovea along with macular edema resolution. The thickened retina appeared to be severely damaged. Optical coherence tomography enabled histologic assessment of the surgical outcome of macular edema. Vitrectomy was effective in decreasing foveal thickness in most eyes (92%). Postoperative visual outcome was more OF

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FIGURE 6. Case 3. Optical coherence tomographic findings. (Top left) Preoperative optical coherence tomography shows an intraretinal area of low reflectivity (yellow arrows) and a serous retinal detachment (white arrows) at the fovea; the foveal thickness is 810 ␮m and the height of the subretinal space is 470 ␮m. (Top right) One month after vitrectomy, the height of the serous retinal detachment has decreased slightly. (Bottom left) Three months after vitrectomy, the serous retinal detachment has decreased and highly reflective dots are seen in the subretinal space. (Bottom right) Five months after vitrectomy, the cystoid space and the serous retinal detachment have disappeared. The foveal pit is restored.

FIGURE 7. Preoperative and postoperative best-corrected visual acuity levels. The best-corrected visual acuity improved by more than 2 lines in five (38%) of 13 eyes, remained the same in seven eyes (54%), and worsened in one eye (8%).

FIGURE 8. Preoperative and postoperative foveal thicknesses. ■ indicates that best-corrected visual acuity increased more than 2 lines. The gray area indicates that the foveal thickness decreased by more than 50% of the preoperative measurement. Four of the six eyes in this area gained more than 2 lines of best-corrected visual acuity.

tion, intraretinal fluid appeared to move into the subretinal space in some cases.

REFERENCES 1. Bresnick GH. Diabetic macular edema. A review. Ophthalmology 1986;93:989 –997. 2. Lewis H, Abrams GW, Blumenkranz MS, et al. Vitrectomy for diabetic macular traction and edema associated with posterior hyaloidal traction. Ophthalmology 1992;99:753– 759. 3. Tachi N, Ogino N. Vitrectomy for diffuse macular edema in cases of diabetic retinopathy. Am J Ophthalmol 1996;122: 258 –260. 4. Kishi S, Shimizu K. Posterior precortical vitreous pocket. Arch Ophthalmol 1990;108:979 –982. 5. Kishi S, Hagimura N, Shimizu K. The role of the premacular liquefied pocket and premacular vitreous cortex in idiopathic macular hole development. Am J Ophthalmol 1996;122: 622– 628. 6. Kishi S, Shimizu K. Clinical manifestations of posterior precortical vitreous pocket in proliferative diabetic retinopathy. Ophthalmology 1993;100:225–229. 7. Yanoff M, Fine BS, Brucker AJ, et al. Pathology of human cystoid macular edema. Surv Ophthalmol 1984;28:505–511. 8. Puliafito CA, Hee MR, Lin CP, et al. Imaging of macular diseases with optical coherence tomography. Ophthalmology 1995;102:217–229. 9. Hee MR, Puliafito CA, Wong C, et al. Quantitative assessment of macular edema with optical coherence tomography. Arch Ophthalmol 1995;113:1019 –1029. 10. Otani T, Kishi S, Maruyama Y. Patterns of diabetic macular edema with optical coherence tomography. Am J Ophthalmol 1999;127:688 – 693.

FIGURE 9. Preoperative thickness of neurosensory retina versus postoperative best-corrected visual acuity. A strong negative correlation (correlation coefficient, ⴚ0.76; P < .01) is seen between the preoperative thickness of neurosensory retina at the fovea and the best-corrected visual acuity 6 months postoperatively.

related to preoperative thickness of neurosensory retina rather than foveal thickness. Visual improvement was limited in eyes with a very thick retina. Macular edema consisted of retinal thickening with decreased reflectivity in the presence of cystoid macular edema or serous retinal detachment. During the process of macular edema absorp-

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