Diabetic retinopathy (DR) progressively
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- Penelope Ford
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1 FOCUS ON DIABETIC MACULAR EDEMA * Frederick L. Ferris III, MD ABSTRACT The current state of treatment for diabetic macular edema (DME) is focused on slowing the rate of vision loss through assessment of retinal function and therapies that prevent DME progression. Recently developed pharmacologic agents have been shown to reduce the risk of vision loss as a result of DME and diabetic retinopathy. In clinical studies, the protein kinase C-β inhibitor ruboxistaurin reduced the risk of DME progression and moderate vision loss, and the vascular endothelial growth factor inhibitor pegaptanib also showed short-term early promise for DME. Bevacizumab is currently under investigation. Early Treatment Diabetic Retinopathy Study-type laser photocoagulation has been shown to improve long-term visual outcomes and is still the mainstay of therapy. Subsequent clinical trials are needed to determine the most effective role of pharmacologic agents and other interventions in preventing vision loss from DME. (Adv Stud Ophthalmol. 6;3(1):18-22) *Based on a presentation given by Dr Ferris at a satellite symposium held in conjunction with the AAO Annual Meeting in Chicago, Illinois, on October 15, 5. Director of Clinical Research and Epidemiology, National Eye Institute, National Institutes of Health, Bethesda, Maryland. Address correspondence to: Frederick L. Ferris III, MD, National Eye Institute, National Institutes of Health, Building 31, Room 6A52, 9 Rockville Pike, Bethesda, MD rickferris@nei.nih.gov. Diabetic retinopathy (DR) progressively damages retinal blood vessels, resulting in the breakdown of the blood-retina barrier and increased vascular permeability. Diabetic macular edema (DME) occurs when fluid and proteins leak from compromised vessels into the surrounding retinal tissue and collect within the macula. 1 In the United States, clinically significant DME develops in 6% of people with type 1 diabetes and 2% to 4% of people with type 2 diabetes. Ten-year incidence rates for clinically significant DME are.1% for people with type 1 diabetes and 13.9% for people with type 2 diabetes. 1 DR, a microvascular complication of diabetes, is the leading cause of blindness among US adults aged to 74 years, resulting in 12 to 24 new cases of blindness each year. 2 In addition to fluorescein angiography and funduscopy, ophthalmologists need reliable and reproducible methods for assessing DME. Although optical coherence tomography (OCT) is very good at measuring retinal thickness, questions remain as to whether it is an effective means of assessing visual function. Further studies on OCT as a tool for assessing DME are needed. When a patient develops DME, ophthalmologists typically intervene with photocoagulation to slow vision loss. New pharmacologic agents, such as protein kinase C-β (PKC-β) inhibitors and vascular endothelial growth factor (VEGF) inhibitors, are currently being studied in clinical trials and have shown evidence of benefit with regards to visual outcomes. These agents may in the future prove to be first-line therapies for the prevention of vision loss as a result of DME. Further study will determine their efficacy as monotherapy and their potential role in combined 18 Vol. 3, No. 1 March 6
2 therapies to prevent or slow vision loss. This article reviews novel therapeutic approaches to DME. ASSESSING DIABETIC MACULAR EDEMA OPTICAL COHERENCE TOMOGRAPHY Optical coherence tomography is a reproducible measurement of retinal thickness and is therefore valuable in the assessment of DME. Despite individual dayto-day and diurnal variations in retinal thickening, and some instrument-dependent variation, OCT is a reliable means of measuring retinal thickness, perhaps even better than photographic assessment. However, it remains unclear if diminished retinal thickness as determined by OCT will equate with functional improvement or improvement in visual acuity. The Diabetic Retinopathy Clinical Research Network (DRCR Network), a collaborative network that facilitates multicenter clinical research on DR, DME, and associated conditions, is conducting a 3-year pilot study which, among other outcomes, will examine the correlation between OCT measurements and visual acuity. 3 This randomized, multicenter clinical trial will compare standard laser photocoagulation therapy to the mild macular grid method for the treatment of DME. Patients enrolled in the study must be at least 18 years old, have clinically significant DME, visual acuity of /4 or better, and no prior laser therapy. Results are expected to be published in 6. TREATING DIABETIC MACULAR EDEMA NOVEL THERAPEUTIC APPROACHES There is a growing body of evidence to support several therapeutic approaches to DME, including PKCβ inhibitors, 4 anti-inflammatory approaches, 5,6 vitrectomy, 7,8 and growth hormone inhibition. 9 The use of these novel medical approaches in combination with standard photocoagulation is also under examination. The use of combination therapies may offer treatment advantages, particularly when the therapies approach the disease through different pathways. The Protein Kinase C-β Inhibitor Diabetic Macular Edema Study (PKC-DMES) demonstrated that ruboxistaurin, a selective PKC-β inhibitor, did not have a significant effect on the progression of DME. However, if patients with very poor glycemic control at baseline were excluded, the risk of DME progression was reduced by 31% (Figure 1). 4 In the Protein Kinase C-β Inhibitor Diabetic Retinopathy Study (PKC-DRS), treatment with ruboxistaurin did not slow the progression of DR, although some loss of treatment effect could be attributed to an abbreviated follow-up period. However, PKC-DRS showed a % or more reduced risk for the development of moderate vision loss in patients treated with ruboxistaurin compared to patients who received placebo (Figure 2). 4,11 The results of these studies suggest that ruboxistaurin Figure 1. Ruboxistaurin Treatment Reduced the Risk of DME Progression PKC-β Inhibitor Trials Ruboxistaurin Development of Central DME 5 4 Placebo 32 mg P =.19 1 DME = diabetic macular edema; PKC = protein kinase C. Reprinted with permission from Aiello et al. Diabetologia. 3;46(suppl 2):A42. 4 Figure 2. Ruboxistaurin Treatment Reduced the Risk of Moderate Vision Loss PKC-β Inhibitor Trials Ruboxistaurin Development of Moderate Vision Loss 5 4 Placebo 32 mg P =.19 1 PKC = protein kinase C. Reprinted with permission from Diabetes. 5;54: Copyright 5 American Diabetes Association. Advanced Studies in Ophthalmology 19
3 is an effective therapy for the prevention of vision loss in DME and DR. Intravitreal VEGF inhibitors are another novel therapeutic approach to DME. A recently published phase II study showed that patients treated with pegaptanib had better visual acuity, were more likely to show a reduction in central retinal thickness, and were less likely to need photocoagulation at follow-up compared to patients receiving placebo. 9 In another small unpublished series, patients injected with bevacizumab experienced decreased neovascularization of the iris, of the disc, and elsewhere, in addition to decreased DME. 12 Studies of ranibizumab for DME are ongoing. Although these preliminary results are promising, the long-term outcomes from treatment with these agents remain unknown. For instance, data have shown that neovascularization appears to recur when pegaptanib is no longer present in the eye, suggesting that there may be a role for concomitant therapy with other modalities. Early phase studies of novel pharmacologic agents for the treatment of DR and DME show that these therapies are effective. Ruboxistaurin has been shown to substantially reduce the risk of DME progression and moderate vision loss. Pegaptanib treatment has been associated with improved visual acuity, lower rates of retinal thickening, and reduced need for further treatment at followup. Bevacizumab and ranibizumab injections also have shown promising early results. Further study will determine the long-term effects of pharmacologic therapies for DME and their potential utility as preventive treatments for this condition. STEROIDS Intravitreal steroid use is widely gaining acceptance as a treatment for DME. In animal studies, corticosteroids have been shown to reduce the breakdown of the blood-retinal barrier that occurs as a result of retinal photocoagulation. 13 Corticosteroids also downregulate the production of VEGF. 14 Case series of intravitreal triamcinolone acetonide use in patients with DME by Martidis et al, Jonas et al, and Massin et al (4 mg, 25 mg, and 4 mg, respectively) each reported improvement in mean visual acuity at endpoint The safety and efficacy of intravitreal triamcinolone acetonide in the treatment of diffuse DME has been retrospectively studied in a clinical case series by Chieh et al. 18 The study involved 2 eyes of 174 patients who received an intravitreal injection of 1 mg or 4 mg of triamcinolone acetonide, and found a significant improvement in visual acuity (P <.1) in the study group at 6 months. Cardillo et al compared the safety and efficacy of intravitreal versus posterior sub-tenon s capsule injection of triamcinolone acetonide for diffuse DME in a prospective, double-masked, randomized controlled trial involving 12 patients (24 eyes). 19 This study randomized 1 eye of each patient to receive 4-mg triamcinolone acetonide intravitreal injection and the fellow eye to receive a 4-mg triamcinolone acetonide posterior sub-tenon s capsule injection. Both intravitreal and sub-tenon s capsule injections resulted in significant but transient improvements in central macular thickness, with the intravitreal injection demonstrating significantly thinner central macular thickness than that obtained with the sub-tenon s capsule injection. The mean visual acuity was significantly better than in the sub-tenon s capsule-injected eyes at 3 months after injection. Studies delineating the possible role of steroids in DR are ongoing. A DRCR Network randomized multicenter trial that began enrolling patients in 5 seeks to compare intravitreal triamcinolone acetonide injections at doses of 1 mg or 4 mg to macular laser photocoagulation for DME. Another DRCR Network-sponsored phase II randomized clinical trial of peribulbar triamcinolone acetonide to treat DME is currently recruiting patients. 21 PHOTOCOAGULATION TREATMENT Studies published before the development of photocoagulation showed that approximately 5% of patients with proliferative diabetic retinopathy (PDR) were blind within 5 years of onset. 22,23 With intensive treatment and careful follow-up, as demonstrated by the Early Treatment Diabetic Retinopathy Study (ETDRS) Report 9, only 4% of patients with PDR who received active treatment progressed to severe vision loss within 5 years. 24 The long-term effectiveness of pan-retinal photocoagulation in DR also has been demonstrated. In one series, 15-year repeat procedure rates for argon laser and xenon photocoagulation were not significantly higher than 5-year rates. Of the patients randomized to photocoagulation, 5% of the argon-treated patients and 3% of the xenon-treated patients had received additional laser treatment, 58% of the argon-treated patients and 41% of the xenontreated patients had /4 or better visual acuity, and 95% of argon-treated patients and 82% of xenontreated patients had / or better visual acuity. 25 Photocoagulation also remains the principal treatment for DME. ETDRS Report 1 showed that focal Vol. 3, No. 1 March 6
4 photocoagulation for clinically significant DME substantially reduced the risk of vision loss, increased the chance of visual improvement, and decreased the frequency of persistent macular edema. However, approximately 12% of eyes lost lines of vision even with treatment (Figure 3). 26,27 Findings from the ETDRS Report 19 support photocoagulation for patients with clinically significant DME, particularly when the center of the macula is involved. 28 The group of ETDRS patients at the highest risk for vision loss from DME had definite involvement of the macula center at baseline. Nevertheless, patients receiving immediate focal photocoagulation had improved visual outcomes compared to patients who were assigned to deferred photocoagulation treatment. These studies suggest that focal photocoagulation was effective in slowing the vision loss associated with DME. The results from scatter photocoagulation studies suggest that more intense scatter photocoagulation may have detrimental effects on the macula. The ETDRS Report 3 showed that full scatter treatment increased the risk of losing 3 full lines of vision compared to no treatment, and the incidence of vision loss was twice as high within the first 4 months of treatment. Patients in the mild scatter group had a high initial event rate that decreased over time (Figure 4). The high initial rates could be partially attributed to the mild scatter photocoagulation being administered in 2 treatments (6 8 burns at baseline followed by another 6 8 burns). The difference between full scatter and mild scatter was highly statistically significant, whereas there was no difference between vision loss rates for patients receiving full scatter photocoagulation compared to those not receiving treatment. 29 Focal photocoagulation also has been shown to be effective treatment for PDR and DME, although further studies are needed to determine optimal photocoagulation strategies and the role of photocoagulation in combination therapy. CONCLUSIONS Diabetic retinopathy is a common microvascular complication, which is a factor in the development of DME, that contributes to blindness in patients with DR. Photocoagulation is currently the primary intervention to slow vision loss in DME. Clinical trials of pharmacologic agents also have shown benefit for visual outcomes. Patients treated with ruboxistaurin had reduced risk for DME progression and reduced risk for moderate vision loss, and preliminary studies and case reports of pegaptanib, ranibizumab, and bevacizumab treatment have shown improved visual outcomes. Areas of current and future investigation include photocoagulation, intravitreal steroid injection, vitrectomy, peribulbar and retrobulbar steroids, combination therapies, and medical and surgical procedures. Further study will determine the role of structural assessments, photocoagulation techniques, and pharmacologic agents in an optimized treatment strategy for patients with DME. Figure 3. Focal Photocoagulation Treatment Reduced the Risk of Moderate Vision Loss Early Treatment Diabetic Retinopathy Study Development of Moderate Vision Loss Control group Focal argon P <.1 1 Data from Arch Ophthalmol. 1985;3: ; and Early Treatment Diabetic Retinopathy Study Group. 27 Figure 4. Mild Scatter Photocoagulation Treatment Reduced the Long-Term Risk of Moderate Vision Loss 4 Scatter Treatment and Macular Edema Moderate Visual Acuity Loss Eyes with Central Macular Edema at Baseline* Control group Full scatter delayed focal Mild scatter delayed focal P < *Mild to moderate nonproliferative DR. DR = diabetic retinopathy. Reprinted with permission from Int Ophthalmol Clin. 1987;27: Advanced Studies in Ophthalmology 21
5 REFERENCES 1. Williams R, Airey M, Baxter H, et al. Epidemiology of diabetic retinopathy and macular edema: a systematic review. Eye. 4;18: National Diabetes Statistics Fact Sheet: General Information and National Estimates on Diabetes in the United States, 3. Bethesda, Md: National Institute of Diabetes and Digestive and Kidney Diseases; US Department of Health and Human Services, National Institute of Health. 3. A pilot study of laser photocoagulation for diabetic macular edema. Diabetic Retinopathy Clinical Research Network. Available at: ProtocolA_laser/ProtAInfo.html. Accessed November 15, Aiello LP, Davis M, Milton R, et al. Initial results of the protein kinase C β inhibitor diabetic macular edema study (PKC-DMES) [abstract]. Diabetologia. 3;46(suppl 2):A Jonas JB, Kreissig I, Sofker A, Degenring RF. Intravitreal injection of triamcinolone for diffuse diabetic macular edema. Arch Ophthalmol. 3;121: Spandau UH, Derse M, Schmitz-Valckenberg P, et al. Dosage dependency of intravitreal triamcinolone acetonide as treatment for diabetic macular edema. Br J Ophthalmol. 5;89: Stolba U, Binder S, Gruber D, et al. Vitrectomy for persistent diffuse diabetic macular edema. Am J Ophthalmol. 5;14: Patel JI, Hykin PG, Schadt M, et al. Pars plana vitrectomy for diabetic macular edema: OCT and functional correlations. Eye. Oct 21, 5 [Epub ahead of print]. 9. Cunningham ET Jr., Adamis AP, Altaweel M, et al. A phase II randomized double-masked trial of pegaptanib, an antivascular endothelial growth factor aptamer, for diabetic macular edema. Ophthalmology. 5;112: Zacks DN, Johnson MW. Combined intravitreal injection of triamcinolone acetonide and pan-retinal photocoagulation for concomitant diabetic macular edema and proliferative diabetic retinopathy. Retina. 5;25: The effect of ruboxistaurin on visual loss in patients with moderately severe to very severe nonproliferative diabetic retinopathy: initial results of the Protein Kinase C beta Inhibitor Diabetic Retinopathy Study (PKC-DRS) multicenter randomized clinical trial. Diabetes. 5;54: Avery R. Intravitreal bevacizumab (Avastin) for retinal vascular diseases. Presented at: the American Academy of Ophthalmology 9th Annual Meeting; October 15-18, 5; Chicago, Illinois. 13. Wilson CA, Berkowitz BA, Sato Y, et al. Treatment with intravitreal steroid reduces blood-retinal barrier breakdown due to retinal photocoagulation. Arch Ophthalmol. 1992;1: Osaki NK, Behany KD, Nishihara KC, et al. Regulation of retinal vascular endothelial growth factor and receptors in rabbits exposed to hyperoxia. Invest Ophthalmol Vis Sci. 2;43: Martidis A, Duker J, Greenberg P, et al. Intravitreal triamcinolone for refractory diabetic macular edema. Ophthalmology. 2;9: Jonas J, Kreissig I, Sofker A, Degenring R. Intravitreal injection of triamcinolone for diffuse diabetic macular edema. Arch Ophthalmol. 3;121: Massin P, Audren F, Haouchine B, et al. Intravitreal triamcinolone acetonide for diabetic diffuse macular edema. Ophthalmology. 4;111: Chieh JJ, Roth DB, Liu M, et al. Intravitreal triamcinolone acetonide for diabetic macular edema. Retina. 5; 25: Cardillo JA, Melo LA Jr, Costa RA. Comparison of intravitreal versus posterior sub-tenon s capsule injection of triamcinolone acetonide for diffuse diabetic macular edema. Ophthalmology. 5;112: Diabetic Retinopathy Clinical Research Network Web site. A randomized trial comparing intravitreal triamcinolone acetonide and laser photocoagulation for diabetic macular edema. Available at: ProtocolB_steroid/ProtBInfo.html. Accessed January 31, Diabetic Retinopathy Clinical Research Network Web site. Triamcinolone acetonide injections to treat diabetic macular edema. Available at: gov/ct/gui/show/nct2323. Accessed January 31, Caird FI, Burditt AF, Draper GJ. Diabetic retinopathy. A further study of prognosis for vision. Diabetes. 1968;17: Deckert T, Simonsen SE, Poulsen JE. Prognosis of proliferative retinopathy in juvenile diabetics. Diabetes. 1967;16: Early photocoagulation for diabetic retinopathy. ETDRS report number 9. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology. 1991;98(5, suppl): Blankenship GW. Fifteen-year argon laser and xenon photocoagulation results of Bascom Palmer Eye Institute s patients participating in the diabetic retinopathy study. Ophthalmology. 1991;98: Photocoagulation for diabetic macular edema. Early Treatment Diabetic Retinopathy Study report number 1. Early Treatment Diabetic Retinopathy Study Research Group. Arch Ophthalmol. 1985;3: Early Treatment Diabetic Retinopathy Study Group. Treatment technique and clinical guidelines for photocoagulation of diabetic macular edema. Early Treatment Diabetic Retinopathy Study report number 2. Ophthalmology. 1987;94: Focal photocoagulation treatment of diabetic macular edema. Relationship of treatment effect to fluorescein angiographic and other retinal characteristics at baseline: ETDRS report no. 19. Early Treatment Diabetic Retinopathy Study Research Group. Arch Ophthalmol. 1995;113: Techniques for scatter and local photocoagulation treatment of diabetic retinopathy: Early Treatment Diabetic Retinopathy Study Report no. 3. The Early Treatment Diabetic Retinopathy Study Research Group. Int Ophthalmol Clin. 1987;27: Vol. 3, No. 1 March 6
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