Andrew J. Barkmeier, MD; Benjamin P. Nicholson, MA; Levent Akduman, MD

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1 c l i n i c a l s c i e n c e Effectiveness of Laser Photocoagulation in Clinically Significant Macular Edema With Focal Versus Diffuse Parafoveal Thickening on Optical Coherence Tomography Andrew J. Barkmeier, MD; Benjamin P. Nicholson, MA; Levent Akduman, MD n BACKGROUND AND OBJECTIVE: To evaluate whether increased foveal thickness in clinically significant diabetic macular edema responds differently to modified focal/grid laser photocoagulation in the setting of focal versus diffuse parafoveal thickening as defined by optical coherence tomography (OCT) criteria. n PATIENTS AND METHODS: The medical records of patients undergoing macular laser procedures for clinically significant diabetic macular edema were retrospectively reviewed. OCT, demographic, and clinical data were recorded for 62 consecutive eyes with clinically significant diabetic macular edema and foveal thickening (> 230 microns). Diffuse parafoveal thickening was defined as having all four parafoveal OCT quadrants greater than 300 microns, whereas focal thickening was defined as having fewer than four quadrants greater than 300 microns. n RESULTS: Mean foveal thickness decreased from 331 to 311 microns with relatively stable visual acuity INTRODUCTION Macular edema is a common cause of visual loss that occurs in up to one-third of patients with diabetes (20/54 vs 20/51) after a single laser treatment session. The diffuse parafoveal edema subgroup (24 eyes) had a mean foveal thickness change from 383 to 366 microns (P =.47) and mildly decreased visual acuity (20/62 vs 20/69). The focal parafoveal edema subgroup (38 eyes) experienced statistically significant foveal thinning from 299 to 276 microns (P =.018) and mildly improved visual acuity (20/48 to 20/43). n CONCLUSION: Increased foveal thickening associated with clinically significant diabetic macular edema responds more favorably to modified focal/grid laser photocoagulation in the setting of focal parafoveal edema by OCT criteria. Statistically significant foveal thinning occurred following treatment in the focal group (P =.018) but not the diffuse group (P =.47). Furthermore, eyes with focal parafoveal edema experienced a more beneficial visual acuity response than those with diffuse edema (P =.049). [Ophthalmic Surg Lasers Imaging 2009;40: ] mellitus. 1 Early Treatment Diabetic Retinopathy Study (ETDRS) reports have defined clinically significant diabetic macular edema as either retinal thickening or hard exudates associated with thickening within 500 From Saint Louis University, Saint Louis, Missouri. Accepted for publication April 30, Presented in part at the Association for Research in Vision and Ophthalmology Annual Meeting, Fort Lauderdale, Florida, May 10, Supported in part by a grant from Research to Prevent Blindness, Inc., New York, New York. The authors have no financial or proprietary interest in the materials presented herein. Address correspondence to Levent Akduman, MD, 1755 S. Grand Avenue, Saint Louis, MO doi: / Ophthalmic Surgery, Lasers & Imaging September/October 2009 Vol 40, No 5

2 microns of the foveal avascular zone center or the presence of one disc area of retinal thickening within one disc diameter of the foveal avascular zone center. Focal/ grid laser photocoagulation reduces the risk of moderate vision loss in patients with clinically significant diabetic macular edema by approximately 50%. 2,3 Although ETDRS-based biomicroscopic criteria remain the gold standard for diagnosis of clinically significant diabetic macular edema, optical coherence tomography (OCT) is proving to be an important adjunctive technology for macular edema management. OCT has proven to be more sensitive in identifying subclinical macular thickening, which helps clinicians identify patients for whom closer follow-up may be advisable. 4,5 OCT is also used to objectively track longitudinal changes in retinal thickening and to provide an objective basis for evaluating clinical responsiveness to different treatment modalities and techniques Increasingly, OCT data are being used to attempt to classify patterns of macular edema with the ultimate goal of directing therapy and predicting outcomes. 9,10,12,14-16 Although local pharmacologic (eg, intravitreal triamcinolone) and incisional surgical (eg, pars plana vitrectomy with internal limiting membrane peeling) modalities have been shown to effectively treat diabetic macular edema, proper patient selection is critical because both carry an increased risk of complications compared to focal macular laser treatment. OCT has been shown to help identify those patients with taut posterior hyaloid membranes for whom vitrectomy surgery is likely to be the most beneficial treatment. In this study, we wanted to identify the group of patients most likely to benefit from laser treatment. We retrospectively analyzed the predictive value of parafoveal OCT criteria (number of parafoveal quadrants > 300 microns) with respect to response following modified ETDRS focal/grid laser photocoagulation. These criteria are straightforward and readily available from the standard Stratus OCT3 (Carl Zeiss Meditec, Dublin, CA) 6.0-mm macular map. PATIENTS AND METHODS A retrospective review was conducted on patient medical records identified by coding for focal macular laser procedures performed between January 2004 and May Procedures were performed at the Saint Louis University Eye Institute, an urban academic university setting, and the O Donnell Eye Institute, a suburban multispecialty ophthalmology practice. OCT, demographic, and clinical data were recorded for 62 consecutive eyes of 37 patients with diabetes mellitus who had clinically significant diabetic macular edema, had at least borderline foveal thickening (central 1.0- mm diameter area > 230 microns), and for whom baseline and 3- to 5-month follow-up OCT data were available (Table 1). Exclusion criteria included any retinal laser procedure, ocular surgery, or intraocular injection within the past 6 months or presence of a thickened, taut posterior hyaloid membrane on OCT. Foveal thickening (central 1.0-mm diameter area) was defined as greater than 230 microns and thickening of the parafoveal quadrants (inner 1.0-mm width quadrants on the 6.0-mm OCT3 display) was defined as greater than 300 microns based on OCT3 normative data from two recent reports (212 ± 20 microns 6 and 197 ± 31 microns 14 in the foveal region; 251 to 267 ± 13 to 17 microns 6 in the parafoveal quadrants). Focal parafoveal thickening was defined for study purposes as having fewer than four parafoveal OCT quadrants greater than 300 microns and diffuse parafoveal thickening was defined as having all four parafoveal quadrants greater than 300 microns in thickness (Fig. 1). All patients had pre-treatment OCT, stereo-color fundus photography, and fluorescein angiography and were diagnosed as having clinically significant diabetic macular edema based on ETDRS biomicroscopic criteria by the same retina specialist. Argon green laser was applied in a modified ETDRS focal/grid pattern with a spot size of 50 to 200 microns, with areas closer to the foveal center receiving smaller spots. Light burns were placed in the clinically thickened areas 1 to 2 spot sizes apart, sparing the foveal avascular zone. All microaneurysms and points of discrete fluorescein angiography leakage within the edematous region were treated focally. The typical follow-up schedule consisted of a complete ophthalmologic examination at 1 month post-treatment followed by examination plus OCT at 3 to 5 months. OCT data were obtained through a dilated pupil by an experienced technician using the Stratus OCT (OCT3). Decentered OCTs and those with fewer than three data points were excluded. Seventy-two percent of all values were based on six data points. The primary outcome measures were OCT foveal OCT & Laser Photocoagulation Barkmeier et al. 473

3 Table 1 Baseline Demographics and Characteristics Parafoveal Edema Classification Characteristic Overall (N = 62) Focal (n = 38) Diffuse (n = 24) No. of parafoveal zones > 300 µm < 4 all 4 Age (y) 64.7 ± ± ± 11.2 Female Race African American White Previous focal/grid photocoagulation Previous panretinal photocoagulation Visual acuity Snellen 20/54 20/48 20/62 LogMAR ± ± ± 0.31 Foveal thickness (µm) (central 3.0 mm) 331 ± ± ± 105 Inner macular volume (mm 3 ) (central 3.0 mm) 2.35 ± ± ± 0.41 Macular volume (mm 3 ) (central 6.0 mm) 8.19 ± ± ± 1.03 LogMAR = logarithm of the minimum angle of resolution. Figure 1. Focal parafoveal edema (left) with fewer than four quadrants greater than 300 microns thick and diffuse parafoveal edema (right) having all four quadrants greater than 300 microns. thickness and visual acuity comparisons between the pretreatment and 3- to 5-month follow-up visits. In addition to the OCT parafoveal edema criteria, treatment response was also analyzed for subgroupings based on 474 Ophthalmic Surgery, Lasers & Imaging September/October 2009 Vol 40, No 5

4 Parafoveal Edema Classification Focal (n = 38) Table 2 Results Following Modified ETDRS Focal/Grid Photocoagulation Initial Foveal Thickness (µm) Final Foveal Thickness (µm) Final Foveal Thickness Change (µm) SCMT (%) Initial Acuity (LogMAR) Final Acuity (LogMAR) Acuity Change (LogMAR) Mean SD Diffuse (n = 24) Mean SD Total (N = 62) Mean SD ETDRS = Early Treatment Diabetic Retinopathy Study; SCMT = standardized change in macular thickening; LogMAR = logarithm of the minimum angle of resolution; SD = standard deviation. initial foveal thickness, visual acuity, and macular volume. Inner macular volume calculations for the central 3.0-mm diameter area were made using weighted values for the central foveal area and the four inner quadrants. Snellen visual acuity data from patient records were converted to logarithm of the minimum angle of resolution (LogMAR) equivalents for analysis. A commercially available software program was used for statistical analysis (SPSS version 14.0; SPSS, Inc., Chicago, IL). Statistical significance of differences between pretreatment and post-treatment foveal thickness was assessed by paired t tests and visual acuity changes were compared using independent samples t tests. Graph whiskers represent the 95% confidence interval, whereas the circles and stars represent near and far outliers, respectively. Saint Louis University Institutional Review Board approval was obtained prior to study commencement. RESULTS Forty-one eyes of 25 females and 21 eyes of 12 males were studied. The patient population consisted of 19 African Americans and 18 whites. The overall mean patient age was 65.0 ± 11.1 years with a mean of 67.6 years (range: 41 to 87 years) in the focal group and 61.0 years (range: 42 to 83 years) in the diffuse group. The significance of the baseline age difference between the groups (P =.012) is unknown. Focal laser photocoagulation had previously been performed on 32 eyes (19 in the focal group, 13 in the diffuse group) with a mean interval of 8.5 months since the previous treatment (6 unknown intervals). Sixteen eyes had previously been treated with panretinal photocoagulation (6 in the focal group, 10 in the diffuse group). Follow-up was 3.9 ± 0.9 months (Table 2). Two patients were excluded from analysis due to pretreatment OCT diagnoses of taut, thickened posterior hyaloid membranes (one in each group). Both eyes had modest foveal thinning, but the patient with diffuse parafoveal edema had significant worsening of visual acuity from 20/80 to 20/200 and the focally involved eye remained stable. Another study eye in the focal parafoveal edema group was diagnosed as having moderate to severe foveal capillary dropout based on the baseline fluorescein angiography. This eye experienced moderate foveal thickening and doubling of the visual angle following treatment. Due to ETDRS Report No. 19 findings that such eyes may still be candidates for photocoagulation, the eye was included in the analysis. Change in Foveal Thickness The overall mean foveal thickness decreased from 331 to 311 microns (P =.053). There was a statistically significant thinning of the central 1.0-mm foveal zone in the subgroup with clinically significant diabetic macular edema and focal edema by OCT criteria (299 to 276 microns, P =.018), but not in the diffuse group (383 to 366 microns, P =.47). This effect was seen despite the larger mean initial foveal thickness in the OCT & Laser Photocoagulation Barkmeier et al. 475

5 Figure 2. Baseline foveal thickness correlates weakly with foveal thinning following laser photocoagulation. diffuse group. Initial foveal thickness correlates weakly with the degree of foveal thinning following photocoagulation (Fig. 2). However, grouping patients based merely on whether the initial foveal thickness is greater or less than 300 microns is only minimally useful because neither group achieved statistically significant thinning. Those initially greater than 300 microns decreased from 406 to 368 microns (n = 30; P =.063; standard deviation = 107), whereas those less than 300 microns showed minimal thinning from 261 to 257 microns (n = 32; P =.58; standard deviation = 47). The standardized change in macular thickening, defined by Chan and Duker as the change in foveal OCT thickness divided by the potential change (initial thickness minus normative thickness) was 24% in the focal group and 5% in the diffuse group 8 (P =.33) (Fig. 3). No subgroups were identified based on initial inner macular volume criteria (central 3.0-mm diameter) that achieved statistically significant foveal thinning. The subgroup of patients with smaller initial total macular volumes (< 8.0 mm 3 ) experienced a significant foveal thinning following treatment from 288 to 261 microns (n = 32; P =.009; standard deviation = 57), whereas those with larger macular volumes (> 8.0 mm 3 ) responded less predictably (377 to 364 microns; n = 30; P =.50; standard deviation = 122). Patients with a history of focal/grid laser showed similar responsiveness to repeat laser photocoagulation in both groups (301 to 270 microns in the focal group [P =.065]; 416 to 382 microns in the diffuse group [P =.38]) compared to those who had not previously been treated. Figure 3. Slightly increased standardized change in macular thinning (SCMT) (%) in focal versus diffuse parafoveal edema. OCT = optical coherence tomography. Change in Visual Acuity Overall, visual acuity remained relatively stable (20/54 baseline vs 20/51 final). Subgroup analysis of patients with clinically significant diabetic macular edema and diffuse edema by OCT criteria experienced mildly decreased visual acuity (20/62 baseline vs 20/69 final), whereas those with focal parafoveal edema experienced mildly improved visual acuity (20/48 to 20/43). The intergroup difference in visual acuity change was statistically significant (P =.049) (Fig. 4). This effect was seen despite the better initial visual acuity in the focal group. Better initial visual acuity is inversely related to visual improvement following treatment. The subgroup of patients with an initial visual acuity of 20/30 or better actually experienced a statistically significant worsening of vision following treatment (20/26 to 20/30; n = 23; P =.046), whereas those with visual acuity that was initially 20/40 or worse experienced visual improvement (20/82 to 20/70; n = 39; P =.25). No subgroups were identified based on initial inner macular volume or total macular volume criteria that achieved statistically significant visual improvement, nor were there any significant volume-based intergroup differences in acuity change. Patients with a history of focal/grid laser photocoagulation showed similar visual 476 Ophthalmic Surgery, Lasers & Imaging September/October 2009 Vol 40, No 5

6 Figure 5. Visual acuity change in focal versus diffuse parafoveal edema within each baseline inner macular volume range (central 3.0 mm). logmar = logarithm of the minimum angle of resolution; OCT = optical coherence tomography. Figure 4. Eyes with clinically significant diabetic macular edema and focal parafoveal edema experienced a more favorable visual acuity response following laser photocoagulation than those with diffuse edema (P =.049). logmar = logarithm of the minimum angle of resolution; OCT = optical coherence tomography. Figure 6. Visual acuity change in focal versus diffuse parafoveal edema within each baseline total macular volume range. logmar = logarithm of the minimum angle of resolution; OCT = optical coherence tomography. acuity changes following repeat laser photocoagulation in the focal group (20/63 to 20/55) and a slightly better response in the diffuse group (20/77 to 20/76) compared to those who had not previously been treated. DISCUSSION OCT provides objective data that may assist in predicting clinical response to clinically significant diabetic macular edema treatment. Foveal thickening associated with clinically significant diabetic macular edema appeared to respond more favorably to modified ETDRS focal/grid laser photocoagulation in the setting of focal (fewer than four parafoveal quadrants > 300 microns) rather than diffuse (all four parafoveal quadrants > 300 microns) thickening, as defined by OCT criteria. Statistically significant central thinning occurred following treatment in the focal group (P =.018) but not the diffuse group (P =.47). Furthermore, visual acuity was more likely to improve in those with focal rather than diffuse edema (P =.049). These results may be even more significant considering that the baseline intergroup differences in foveal thickness and visual acuity would predict the opposite. There is clearly a direct relationship between the number of parafoveal zones being greater than 300 microns in thickness and other OCT data including the inner macular volume (central 3.0-mm diameter) and the total macular volume (central 6.0-mm diameter). For example, 22 of the 23 eyes with both the smallest inner macular volumes and total macular volumes are classified as having focal parafoveal edema. However, the focal versus diffuse classification system continues OCT & Laser Photocoagulation Barkmeier et al. 477

7 Figure 7. Foveal thinning in focal versus diffuse parafoveal edema within each baseline inner macular volume range (central 3.0 mm). OCT = optical coherence tomography. Figure 8. Foveal thinning in focal versus diffuse parafoveal edema within each baseline total macular volume range. OCT = optical coherence tomography. Figure 9. Standardized change in macular thinning (SCMT) (%) within each range of initial foveal thickness. OCT = optical coherence tomography. to be predictive of more favorable visual acuity change within the intermediate ranges of inner macular and total macular volumes (Figs. 5 and 6). Those with focal parafoveal edema also experienced more significant foveal thinning within each range of baseline inner macular volumes (Fig. 7) and each range of baseline total macular volume, with the exception of eyes between 8.0 and 9.0 mm 3 (Fig. 8). Although there are a limited number of eyes in these volume-based subgroups, study results suggest the proposed parafoveal OCT criteria are not merely a surrogate marker for increased retinal volume. Although the standardized change in macular thinning method of analyzing the effect of treatments for macular edema is an important tool, it may not be the best method of assessing statistically significant thinning in this study population due to its propensity to create extreme outliers when the initial foveal thickening is minimal. For example, one eye that improved from 235 to 192 microns was calculated to have a standardized change in macular thinning of 187% and another eye that worsened from 236 to 299 microns had a standardized change in macular thinning of -263%. The standardized change in macular thinning standard deviation for the 10 eyes with initial foveal thickness values less than 250 microns was 144% (Fig. 9). Previous studies using this tool to analyze changes in diffuse diabetic macular edema had significantly larger mean foveal thickness values. We believe absolute changes in macular thickness are more reliable than standardized change in macular thinning in the setting of modest foveal thickening. Despite the lack of intergroup standardized change in macular thinning statistical significance (P =.33), Figure 9 demonstrates a favorable standardized change in macular thinning in the focal parafoveal edema group for each of the baseline foveal thickness ranges. 478 Ophthalmic Surgery, Lasers & Imaging September/October 2009 Vol 40, No 5

8 This study has limitations, including the retrospective nature of the analysis, the number of subjects, and the use of standard Snellen charts rather than the ETDRS visual acuity system. Furthermore, the followup is limited to 5 months post-treatment and involves only one vitreoretinal surgeon. Despite these limitations, these data appear promising in that such straightforward criteria may offer predictive value regarding anticipated response to focal/grid laser photocoagulation. Photocoagulation has the longest lasting effect and most favorable side effect profile of diabetic macular edema treatments and would be recommended in nearly all situations of non-tractional clinically significant diabetic macular edema fitting the described OCT criteria for focal parafoveal edema. Positive results were seen regardless of previous photocoagulation history, which considerably expands the potential clinical value of the findings. Further validation of these criteria may be warranted either through a larger prospective trial or through their application to existing patient databases containing the necessary clinical information. Due to the relatively arbitrary nature of the 300-micron parafoveal thickness cutoff and the 6.0-mm OCT macular map organization, future methods of organizing and analyzing OCT data may further enhance the predictive utility of this imaging modality regarding clinically significant diabetic macular edema response to laser photocoagulation. REFERENCES 1. Klein R, Klein BEK, Moss SE, Davis MD, DeMets DL. The Wisconsin epidemiologic study of diabetic retinopathy: IV. Diabetic macular edema. Ophthalmology. 1984;91: Early Treatment Diabetic Retinopathy Study Research Group. Photocoagulation for diabetic macular edema. ETDRS Report No. 1. Arch Ophthalmol. 1985;103: Early Treatment Diabetic Retinopathy Study Research Group. Focal photocoagulation treatment of diabetic macular edema: relationship of treatment effect to fluorescein angiographic and other retinal characteristics at baseline. ETDRS Report No. 19. Arch Ophthalmol. 1995;113: Browning DJ, McOwen MD, Bowen RM Jr, O Marah TL. Comparison of the clinical diagnosis of diabetic macular edema with diagnosis by optical coherence tomography. Ophthalmology. 2004;111: Brown JC, Solomon SD, Bressler SB, Schachat AP, DiBernardo C, Bressler NM. Detection of diabetic foveal edema: contact lens biomicroscopy compared with optical coherence tomography. Arch Ophthalmol. 2004;122: Chan A, Duker JS, Ko TH, Fujimoto JG, Schuman JS. Normal macular thickness measurements in healthy eyes using Stratus optical coherence tomography. Arch Ophthalmol. 2006;124: Rivellese M, George A, Sulkes D, Reichel E, Puliafito C. Optical coherence tomography after laser photocoagulation for clinically significant macular edema. Ophthalmic Surg Lasers. 2000;31: Chan A, Duker JS. A standardized method for reporting changes in macular thickening using optical coherence tomography. Arch Ophthalmol. 2005;123: Lattanzio R, Brancato R, Pierro L, et al. Macular thickness measured by optical coherence tomography (OCT) in diabetic patients. Eur J Ophthalmol. 2002;12: Parolini B, Panozzo G, Gusson E, et al. Diode laser, vitrectomy and intravitreal triamcinolone: a comparative study for the treatment of diffuse non tractional diabetic macular edema. Semin Ophthalmol. 2004;19: Writing Committee for the Diabetic Retinopathy Clinical Research Network. Comparison of the modified Early Treatment Diabetic Retinopathy Study and mild macular grid laser photocoagulation strategies for diabetic macular edema. Arch Ophthalmol. 2007;125: Panozzo G, Gusson E, Parolini B, Mercanti A. Role of OCT in the diagnosis and follow up of diabetic macular edema. Semin Ophthalmol. 2003;18: Browning DJ, Fraser CM, Powers ME. Comparison of the magnitude and time course of macular thinning induced by different interventions for diabetic macular edema: implications for sequence of application. Ophthalmology. 2006;113: Browning DJ, Fraser CM. Regional patterns of sightthreatening diabetic macular edema. Am J Ophthalmol. 2005;140: Otani T, Kishi S, Maruyama Y. Patterns of diabetic macular edema with optical coherence tomography. Am J Ophthalmol. 1999;127: Hee MR, Puliafito CA, Duker JS, et al. Topography of diabetic macular edema with optical coherence tomography. Ophthalmology. 1998;105: OCT & Laser Photocoagulation Barkmeier et al. 479

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