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PARS PLANA VITRECTOMY FOR DIABETIC MACULAR EDEMA: A Systematic Review, Meta-Analysis, and Synthesis of Safety Literature.

TL;DR: Vitrectomy produces structural and functional improvements in select eyes with diabetic macular edema, but the visual gains are not significantly better than with laser or observation.
Abstract: Purpose:To assess the risk and benefit of pars plana vitrectomy for diabetic macular edema.Methods:The authors conducted a systematic literature review using PubMed, EMBASE, Web of Science, and Cochrane Central Database of Controlled Trials until September 2014. The population was patients with diab

Summary (2 min read)

Introduction

  • Diabetic macular edema (DME) is a leading cause of visual loss in developed nations,1, 2 and as the population with diabetes expands,3 the burden of DME will increase.
  • There are a number of clinical studies suggesting that an attached vitreous may adversely affect the clinical course of DME, or possibly contribute to its pathogenesis.
  • Whilst PPV is well established for the treatment of persistent vitreous hemorrhage22 and tractional retinal detachment,23, 24 its use as a treatment for DME has not been supported by large randomized controlled trials (RCTs).
  • Laboratory studies provide a theoretical basis to support the use of PPV.
  • It has been estimated that vitreous viscosity is 300 to 2000 times greater than aqueous,29 and following vitrectomy diffusion coefficients of intravitreal molecules, including VEGF, should increase by a similar magnitude.

Methods

  • Study design, population, intervention, comparison and outcome.
  • The authors aimed to estimate the risk and benefit of PPV for DME.
  • The population was patients with DME, the intervention was PPV, and the comparison was traditional standard care,4 namely focal macular photocoagulation laser or observation.
  • Safety outcomes included all reported intra- or postoperative surgical complications, or other adverse events attributed to PPV or local or general anesthesia.
  • The study protocol was registered with the international prospective register of systematic reviews (registration number CRD42014013646, National Institute of Health Research Centre for Reviews and Dissemination, University of York, UK) and conducted in accordance with Preferred Reporting Items for Systematic reviews and Meta-Analyses guidance (http://www.prismastatement.org/, accessed 21 January 2015).

Eligibility

  • To be eligible for the meta-analysis RCTs had to recruit patients with DME, and compare PPV to traditional standard care (observation or macular photocoagulation laser), for the treatment of DME.
  • Outcome data had to include change in VA and change in CRT at least 6 months after enrolment, and safety at any time point.
  • The data had to be of sufficient quality, in terms of clear eligibility, defined efficacy and safety outcomes, and data completeness, and in particular studies had to report any complications that occurred, or state that there were none.
  • Only English, French and German language articles in peer-reviewed journals were eligible.
  • Studies that failed to provide pre- and post-operative VA were excluded, as were those appearing as abstract only, and studies where patients received adjunctive therapy such as intravitreal steroids and anti-VEGF drugs, as these could confound the analysis of vitrectomy versus laser/observation.

Literature review

  • An Ovid MEDLINE database search from 1946 to 23 September 2014 was undertaken using Boolean operators with the following keywords (and corresponding MESH headings if they were available): vitrectomy; diab*; macula*; oedema or edema; maculopathy; vitreomacular traction; vitreomacular adhesion; taut posterior hyaloid.
  • The search was not restricted by adding terms such as adverse events, complications, or safety, but rather each eligible article was reviewed for safety data.
  • The retrieved abstracts were then reviewed by two senior retinal experts (TJ, EP) who selected articles for full review if they appeared to meet the eligibility criteria.
  • Further articles were identified in the bibliographies of retrieved articles.
  • Where necessary, authors were contacted to obtain unpublished raw data from RCTs.

Data extraction

  • Three independent reviewers (FG, AA, EN) entered data from each article into an electronic data capture form.
  • Any discrepancy was resolved by consensus or, if necessary, by arbitration of a senior retinal specialist (TJ).
  • The risk of bias was assessed using the Cochrane Risk of Bias Assessment tool which grades risk of bias as low, unclear or high risk.
  • Seven domains of risk where assessed including assessments for selection bias, performance bias, detection bias, attrition bias and reporting bias.

Data analysis

  • The fixed effect method with inverse variance weighting was used.
  • Statistical analysis was performed using RevMan 5.2 available from the Cochrane Collaboration.41.
  • Safety data were pooled across all studies, including nonRCTs.

Meta-analysis of efficacy:

  • Six RCTs were identified that provided mean change in LogMAR VA and mean change in retinal thickness, comparing patients having undergone PPV with controls.
  • 42-47 One study was excluded, as it was not possible to obtain raw data or summary statistics for the outcomes in question, despite contacting the author .
  • The review is based on the authors' judgements about each risk of bias item for each included study.
  • Figure 2 shows a meta-analysis of vision outcome (change in mean logarithm of the minimum angle of visual acuity), comparing pars plana vitrectomy to standard care (observation or macular laser).
  • Fixed effect model used; SD = standard deviation.

Safety:

  • Of these 106 potentially eligible articles were reviewed in full, of which 40 were eligible for the safety analysis.
  • The rate of post-vitrectomy cataract was not reliably reported and many reports did not detail the proportion of phakic eyes.
  • The only other complication reported was rhegmantogenous retinal detachment in one patient (2.1%).42-44, 46.

Discussion

  • The authors meta-analysis of RCTs suggests that the visual benefits following vitrectomy for DME were not significantly better than those achieved using conventional management with laser and observation.
  • Like previous reviews,21 the authors identified a lack of high quality evidence, and the need for large RCTs comparing PPV to the latest gold standard, in particular intravitreal anti-VEGF drugs.
  • Kuppermann BD, Blumenkranz MS, Haller JA, et al.
  • Otani T and Kishi S. A controlled study of vitrectomy for diabetic macular edema.

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T. L. Jackson, E. Nicod, A. Angelis, F. Grimaccia,
E. Pringle, P. Kanavos
Pars plana vitrectomy for diabetic macular
edema: a systematic review, meta-analysis,
and synthesis of safety literature
Article (Accepted version)
(Refereed)
Original citation:
Jackson, Timothy L., Nicod, Elena, Angelis, Aris, Grimaccia, Federico, Pringle,
Edward and Kanavos, Panos (2016) Pars plana vitrectomy for diabetic macular edema: a
systematic review, meta-analysis, and synthesis of safety literature. Retina. ISSN 1539-2864
DOI: 10.1097/IAE.0000000000001280
© 2016 Ophthalmic Communications Society, Inc.
This version available at: http://eprints.lse.ac.uk/66975/
Available in LSE Research Online: September 2016
LSE has developed LSE Research Online so that users may access research output of the
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This document is the author’s final accepted version of the journal article. There may be
differences between this version and the published version. You are advised to consult the
publisher’s version if you wish to cite from it.

From *School of Medicine, King’s College London; LSE Health, London School of Economics and
Political Science
Meetings: The paper has not been presented at any meetings.
Acknowledgments: We thank Dr Dhanes Thomas who provided anonymized participant-level data for
meta-analysis.
1
Pars plana vitrectomy for diabetic macular edema: a systematic review,
meta-analysis, and synthesis of safety literature
Timothy L Jackson PhD, FRCOphth*, Elena Nicod
MSc, Aris Angelis MSc,
Federico Grimaccia MD, Edward Pringle FRCOphth, MRCOphth*, and Panos
Kanavos PhD
Correspondence:
Tim Jackson PhD, FRCOphth
School of M edicine, King’s College London
Department of Ophthalmology
King’s College Hospital
London SE5 9RS
Tel: 020 3299 3385
Fax: 020 3299 3738
Email: t.jackson1@nhs.net
Abbreviated title: Vitrectomy for diabetic macular edema
Financial support: T. Jackson is an advisor to Bausch & Lomb, and DORC, and consultant to ThromboGenics,
and his employer received research grant from Novartis and Ophthotech for unrelated projects. E. Nicod, A.
Angelis, F. Grimaccia and P. Kanavos received an unrestricted educational grant from ThromboGenics for an
unrelated project.

2
Key words: complications; diabetic macular edema; efficacy; meta-analysis; optical coherence tomography
central retinal thickness; pars plana vitrectomy; safety; systematic review; visual acuity.
Summary statement: A meta-analysis of vitrectomy for diabetic macular edema found no significant difference in
visual outcome compared to laser or observation. Retinal thickness was better than with laser/observation at 6
months, but this benefit had reversed by 12 months. Intraoperative retinal breaks occurred in 7.1%, and
postoperative retinal detachment in 1.2%

3
Abstract
Purpose. To assess the risk and benefit of pars plana vitrectomy for diabetic macular
edema (DME).
Methods. We conducted a systematic literature review using PubMed, EMBASE,
Web of Science, and Cochrane Central Database of Controlled Trials until September
2014. The population was patients with DME, intervention vitrectomy, comparator
macular laser or observation, and efficacy outcome visual acuity and central retinal
thickness (CRT). Safety outcomes were intra- and postoperative surgical
complications. The efficacy meta-analysis included only randomized controlled trials.
The safety analysis included prospective, retrospective, controlled and uncontrolled
studies.
Results. Five studies were eligible for the efficacy meta-analysis (n = 127 eyes) and
40 for the safety analysis (n = 1,562 eyes). Combining follow up intervals from 6 to
12 months, the meta-analysis found a non-significant 2 letter visual acuity difference
favoring vitrectomy, and a significant 102 micron greater reduction in CRT favoring
vitrectomy, but a post-hoc subgroup analysis found that a 6 month CRT benefit
reversed by 12 months. The most frequent complications were retinal break (7.1%),
elevated intraocular pressure (5.2%), epiretinal membrane (3.3%), and vitreous
hemorrhage (2.4%). Cataract developed in 68.6% of 121 phakic eyes.
Conclusions. Vitrectomy produces structural and functional improvements in select
eyes with DME, but the visual gains are not significantly better than with laser or
observation. No major safety concerns were identified.

4
Introduction
Diabetic macular edema (DME) is a leading cause of visual loss in developed
nations,
1, 2
and as the population with diabetes expands,
3
the burden of DME will
increase. For many years the standard therapy for DME has been focal macular
photocoagulation laser. The Early Treatment of Diabetic Retinopathy Study (ETDRS)
established that laser approximately halves the risk of moderate vision loss in patients
with clinically significant macular edema.
4
More recently, several randomized
controlled trials (RCTs) have demonstrated the safety and efficacy of intravitreal
steroid injections and implants.
5-9
Vascular endothelial growth factor (VEGF), by
increasing vascular permeability, plays an important role in the pathogenesis of
DME.
10, 11
Studies investigating the intravitreal use of the anti-VEGF agents
ranibizumab,
12-16
aflibercept,
2, 17
and bevacizumab
18
have also shown favorable
results.
19
There are a number of clinical studies suggesting that an attached vitreous may
adversely affect the clinical course of DME, or possibly contribute to its pathogenesis.
Sivaprasad et al found that posterior vitreous detachment (PVD) was less common in
eyes with DME, and that vitreous attachment appeared to reduce the benefit of
intravitreal steroid therapy.
20
A synthesis of the literature by Jackson et al found that
some degree of vitreomacular traction (VMT) was present in 12% of eyes with DME,
and up to 24% in surgical series.
21
Vitreomacular traction may aggravate any
underlying tendency for DME, and if severe, VMT can cause macular edema in its
own right. It therefore seems reasonable to assume that relief of VMT would be
beneficial.

Citations
More filters
Journal ArticleDOI
TL;DR: There remains no one single strategy for the management of the particular stages of DR and DME as there are many options that have not been rigorously tested through large, randomized, controlled clinical trials.
Abstract: Purpose To review the current therapeutic options for the management of diabetic retinopathy (DR) and diabetic macular edema (DME) and examine the evidence for integration of laser and pharmacotherapy. Methods A review of the PubMed database was performed using the search terms diabetic retinopathy, diabetic macular edema, neovascularization, laser photocoagulation, intravitreal injection, vascular endothelial growth factor (VEGF), vitrectomy, pars plana vitreous surgery, antiangiogenic therapy. With additional cross-referencing, this yielded 835 publications of which 301 were selected based on content and relevance. Results Many recent studies have evaluated the pharmacological, laser and surgical therapeutic strategies for the treatment and prevention of DR and DME. Several newer diagnostic systems such as optical coherence tomography (OCT), microperimetry, and multifocal electroretinography (mfERG) are also assisting in further refinements in the staging and classification of DR and DME. Pharmacological therapies for both DR and DME include both systemic and ocular agents. Systemic agents that promote intensive glycemic control, control of dyslipidemia and antagonists of the renin-angiotensin system demonstrate beneficial effects for both DR and DME. Ocular therapies include anti-VEGF agents, corticosteroids and nonsteroidal anti-inflammatory drugs. Laser therapy, both as panretinal and focal or grid applications continue to be employed in management of DR and DME. Refinements in laser devices have yielded more tissue-sparing (subthreshold) modes in which many of the benefits of conventional continuous wave (CW) lasers can be obtained without the adverse side effects. Recent attempts to lessen the burden of anti-VEGF injections by integrating laser therapy have met with mixed results. Increasingly, vitreoretinal surgical techniques are employed for less advanced stages of DR and DME. The development and use of smaller gauge instrumentation and advanced anesthesia agents have been associated with a trend toward earlier surgical intervention for diabetic retinopathy. Several novel drug delivery strategies are currently being examined with the goal of decreasing the therapeutic burden of monthly intravitreal injections. These fall into one of the five categories: non-biodegradable polymeric drug delivery systems, biodegradable polymeric drug delivery systems, nanoparticle-based drug delivery systems, ocular injection devices and with sustained release refillable devices. At present, there remains no one single strategy for the management of the particular stages of DR and DME as there are many options that have not been rigorously tested through large, randomized, controlled clinical trials. Conclusion Pharmacotherapy, both ocular and systemic, will be the primary mode of intervention in the management of DR and DME in many cases when cost and treatment burden are less constrained. Conventional laser therapy has become a secondary intervention in these instances, but remains a first-line option when cost and treatment burden are more constrained. Results with subthreshold laser appear promising but will require more rigorous study to establish its role as adjunctive therapy. Evidence to support an optimal integration of the various treatment options is lacking. Central to the widespread adoption of any therapeutic regimen for DR and DME is substantiation of safety, efficacy, and cost-effectiveness by a body of sound clinical trials.

111 citations

Journal Article
TL;DR: Pars plana vitrectomy with ILM peeling was associated with a reduction in DME when measured by OCT in the majority of eyes, but visual acuity outcomes showed minimal improvement compared to baseline.
Abstract: Purpose: To evaluate anatomic and visual acuity (VA) results of pars plana vitrectomy (PPV) with internal limiting membrane (ILM) peeling for diffuse diabetic macular edema (DME), and to review the literature on the topic. Methods: Retrospective noncomparative case series of patients who underwent PPV with ILM peeling for diffuse DME between January 1, 2000, and December 1, 2005, performed by three surgeons at Bascom Palmer Eye Institute. Main outcome measures included pre- and postoperative optical coherence tomography (OCT) and visual acuity. Mean follow-up period was 8 months (range, 43 days–2 years). Results: Twenty-four eyes of 23 patients meeting the criteria were evaluated. Duration of DME ranged from 1 to 93 months. Mean preoperative logMAR vision was 0.782 (range, 0.30–1.82). Mean logMAR visual acuity at final follow-up was 0.771 (range, 0.10–2.00). At last follow-up, 25% of eyes had ≥2 line increase in VA from baseline, 54% of eyes had no improvement in VA, and 21% of eyes had ≥2 line decrease in VA. Of 9 eyes with pre- and postoperative OCT, there was an overall reduction in central macular thickness of 141 &mgr;m at postoperative month 3 and 120 &mgr;m at last follow-up. Postoperative complications included progression of cataract in 6 (60%) of 10 phakic eyes, postoperative intraocular pressure ≥30 mmHg in 6 (24%) eyes, and postoperative vitreous hemorrhage in 2 (8%) eyes. Conclusions: Pars plana vitrectomy with ILM peeling was associated with a reduction in DME when measured by OCT in the majority of eyes, but visual acuity outcomes showed minimal improvement compared to baseline. These results suggest the efficacy of PPV with ILM peeling for eyes with DME has not been well established and should be reserved for therapy with selected cases.

80 citations

Journal ArticleDOI
TL;DR: Once considered the gold standard in treatment of DME, focal/grid laser is now reserved mostly for non-center-involving DME while anti-vascular endothelial growth factor (anti-VEGF) therapy has become the first-line treatment.
Abstract: Diabetes mellitus is a global epidemic which is growing in prevalence, and diabetic macular edema (DME) is a leading cause of visual impairment among patients affected by this disease. Our objective is to review current and upcoming therapeutic approaches to DME. Once considered the gold standard in treatment of DME, focal/grid laser is now reserved mostly for non-center-involving DME, while anti-vascular endothelial growth factor (anti-VEGF) therapy has become the first-line treatment. However, suboptimal responders to anti-VEGF and the burden of frequent injections have stimulated the development of novel approaches. Corticosteroids can be effective in treating DME, but adverse effects such as intraocular pressure elevation and cataract formation must be considered. Emerging therapeutics and drug delivery systems in the pipeline offer exciting potential solutions to this vision-threatening disease. Multiple types of therapeutics targeting various pathways implicated in the pathogenesis of DME may help lessen the global burden of vision loss from diabetes.

68 citations

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TL;DR: Ranibizumab treatment resulted in DR improvements in all 3 baseline DR severity subsets examined, and the greatest benefits in DR improvement occurred in patients with baseline moderately severe to severe NPDR (DR levels 47/53).

61 citations

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TL;DR: Exudative and tractional intraretinal cystoid spaces displayed characteristic multimodal imaging features and they may represent two different pathologic conditions with equally different clinical implications.

39 citations

References
More filters
Journal ArticleDOI
TL;DR: The data suggest that VEGF plays a major part in mediating active intraocular neovascularization in patients with ischemic retinal diseases, such as diabetic retinopathy and retinal-vein occlusion.
Abstract: Background Retinal ischemia induces intraocular neovascularization, which often leads to glaucoma, vitreous hemorrhage, and retinal detachment, presumably by stimulating the release of angiogenic molecules. Vascular endothelial growth factor (VEGF) is an endothelial-cell-specific angiogenic factor whose production is increased by hypoxia. Methods We measured the concentration of VEGF in 210 specimens of ocular fluid obtained from 164 patients undergoing intraocular surgery, using both radioimmunoassays and radioreceptor assays. Vitreous proliferative potential was measured with in vitro assays of the growth of retinal endothelial cells and with VEGF-neutralizing antibody. Results VEGF was detected in 69 of 136 ocular-fluid samples from patients with diabetic retinopathy, 29 of 38 samples from patients with neovascularization of the iris, and 3 of 4 samples from patients with ischemic occlusion of the central retinal vein, as compared with 2 of 31 samples from patients with no neovascular disorders (P<0.00...

3,714 citations


"PARS PLANA VITRECTOMY FOR DIABETIC ..." refers background in this paper

  • ...Vascular endothelial growth factor (VEGF), by increasing vascular permeability, plays an important role in the pathogenesis of DME.(10,11) Studies investigating the intravitreal use of the anti-VEGF agents ranibizumab, aflibercept,(2,17) and bevacizumab(18) have also shown favorable results....

    [...]

  • ...Several authors have advocated the use of pars plana vitrectomy (PPV) to treat DME....

    [...]

  • ...The Early Treatment of Diabetic Retinopathy Study established that laser approximately halves the risk of moderate vision loss in patients with clinically significant macular edema.4 More recently, several randomized controlled trials (RCTs) have demonstrated the safety and efficacy of intravitreal steroid injections and implants.5–9 Vascular endothelial growth factor (VEGF), by increasing vascular permeability, plays an important role in the pathogenesis of DME.10,11 Studies investigating the intravitreal use of the anti-VEGF agents ranibizumab,12–16 aflibercept,2,17 and bevacizumab18 have also shown favorable results.19 There are a number of clinical studies suggesting that an attached vitreous may adversely affect the clinical course of DME, or possibly contribute to its pathogenesis....

    [...]

  • ...Although the safety of PPV for DME seems comparable to other studies of PPV, the complication rates are higher than those seen after intravitreal anti-VEGF injections for DME.13,15,16 The main strength of the present meta-analysis is that it provides a pooled estimate of treatment effect across several RCTs, and the safety analysis considers an even larger pool of patients that may be better able to detect rare events....

    [...]

  • ...To be eligible for the meta-analysis, RCTs had to recruit patients with DME, and compare PPV to traditional standard care (observation or macular photocoagulation laser) for the treatment of DME....

    [...]

Journal ArticleDOI
26 May 2004-JAMA
TL;DR: The reporting of trial outcomes is not only frequently incomplete but also biased and inconsistent with protocols and Published articles, as well as reviews that incorporate them, may therefore be unreliable and overestimate the benefits of an intervention.
Abstract: ContextSelective reporting of outcomes within published studies based on the nature or direction of their results has been widely suspected, but direct evidence of such bias is currently limited to case reports.ObjectiveTo study empirically the extent and nature of outcome reporting bias in a cohort of randomized trials.DesignCohort study using protocols and published reports of randomized trials approved by the Scientific-Ethical Committees for Copenhagen and Frederiksberg, Denmark, in 1994-1995. The number and characteristics of reported and unreported trial outcomes were recorded from protocols, journal articles, and a survey of trialists. An outcome was considered incompletely reported if insufficient data were presented in the published articles for meta-analysis. Odds ratios relating the completeness of outcome reporting to statistical significance were calculated for each trial and then pooled to provide an overall estimate of bias. Protocols and published articles were also compared to identify discrepancies in primary outcomes.Main Outcome MeasuresCompleteness of reporting of efficacy and harm outcomes and of statistically significant vs nonsignificant outcomes; consistency between primary outcomes defined in the most recent protocols and those defined in published articles.ResultsOne hundred two trials with 122 published journal articles and 3736 outcomes were identified. Overall, 50% of efficacy and 65% of harm outcomes per trial were incompletely reported. Statistically significant outcomes had a higher odds of being fully reported compared with nonsignificant outcomes for both efficacy (pooled odds ratio, 2.4; 95% confidence interval [CI], 1.4-4.0) and harm (pooled odds ratio, 4.7; 95% CI, 1.8-12.0) data. In comparing published articles with protocols, 62% of trials had at least 1 primary outcome that was changed, introduced, or omitted. Eighty-six percent of survey responders (42/49) denied the existence of unreported outcomes despite clear evidence to the contrary.ConclusionsThe reporting of trial outcomes is not only frequently incomplete but also biased and inconsistent with protocols. Published articles, as well as reviews that incorporate them, may therefore be unreliable and overestimate the benefits of an intervention. To ensure transparency, planned trials should be registered and protocols should be made publicly available prior to trial completion.

1,638 citations


"PARS PLANA VITRECTOMY FOR DIABETIC ..." refers background in this paper

  • ...There is a risk that publication or reporting bias may favor the selection of reports describing positive surgical outcomes.(84,85) Also, postvitrectomy lens changes may be a confounding variable....

    [...]

Journal ArticleDOI
TL;DR: Ranibizumab monotherapy and combined with laser provided superior visual acuity gain over standard laser in patients with visual impairment due to DME and had a safety profile in DME similar to that in age-related macular degeneration.

1,187 citations

Journal ArticleDOI
TL;DR: Intravitreous aflibercept, bevacizumAB, or ranibizumab improved vision in eyes with center-involved diabetic macular edema, but the relative effect depended on baseline visual acuity.
Abstract: Background The relative efficacy and safety of intravitreous aflibercept, bevacizumab, and ranibizumab in the treatment of diabetic macular edema are unknown. Methods At 89 clinical sites, we randomly assigned 660 adults (mean age, 61±10 years) with diabetic macular edema involving the macular center to receive intravitreous aflibercept at a dose of 2.0 mg (224 participants), bevacizumab at a dose of 1.25 mg (218 participants), or ranibizumab at a dose of 0.3 mg (218 participants). The study drugs were administered as often as every 4 weeks, according to a protocol-specified algorithm. The primary outcome was the mean change in visual acuity at 1 year. Results From baseline to 1 year, the mean visual-acuity letter score (range, 0 to 100, with higher scores indicating better visual acuity; a score of 85 is approximately 20/20) improved by 13.3 with aflibercept, by 9.7 with bevacizumab, and by 11.2 with ranibizumab. Although the improvement was greater with aflibercept than with the other two drugs (P 0.50 for each pairwise comparison). When the initial letter score was less than 69 (approximately 20/50 or worse), the mean improvement was 18.9 with aflibercept, 11.8 with bevacizumab, and 14.2 with ranibizumab (P Conclusions Intravitreous aflibercept, bevacizumab, or ranibizumab improved vision in eyes with center-involved diabetic macular edema, but the relative effect depended on baseline visual acuity. When the initial visual-acuity loss was mild, there were no apparent differences, on average, among study groups. At worse levels of initial visual acuity, aflibercept was more effective at improving vision. (Funded by the National Institutes of Health; ClinicalTrials.gov number, NCT01627249.).

1,174 citations

Journal ArticleDOI
TL;DR: The prevalence of macular edema and its relationship to a number of risk factors were examined in a population-based study in southern Wisconsin this paper, where the authors determined the presence of maculopathy from its presence on stereoscopic fundus photographs or from past history as recorded and documented in clinic records and photographs.

759 citations

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