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      Melissa officinalis Extract Inhibits Laser-Induced Choroidal Neovascularization in a Rat Model

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          Abstract

          Purpose

          This study investigated the effect of Melissa officinalis extract on laser-induced choroidal neovascularization (CNV) in a rat model. The mechanism by which M. officinalis extract acted was also investigated.

          Methods

          Experimental CNV was induced by laser photocoagulation in Brown Norway rats. An active fraction of the Melissa leaf extract was orally administered (50 or 100 mg/kg/day) beginning 3 days before laser photocoagulation and ending 14 days after laser photocoagulation. Optical coherence tomography and fluorescein angiography were performed in vivo to evaluate the thickness and leakage of CNV. Choroidal flat mount and histological analysis were conducted to observe the CNV in vitro. Vascular endothelial growth factor (VEGF), matrix metalloproteinase (MMP)-2, and MMP-9 expression were measured in retinal and choroidal-scleral lysates 7 days after laser injury. Moreover, the effect of M. officinalis extract on tertiary-butylhydroperoxide (t-BH)-induced VEGF secretion and mRNA levels of VEGF, MMP-2, and MMP-9 were evaluated in human retinal epithelial cells (ARPE-19) as well as in human umbilical vein endothelial cells (HUVECs).

          Results

          The CNV thickness in M. officinalis-treated rats was significantly lower than in vehicle-treated rats by histological analysis. The CNV thickness was 33.93±7.64 µm in the high-dose group ( P<0.001), 44.09±12.01 µm in the low-dose group ( P = 0.016), and 51.00±12.37 µm in the control group. The proportion of CNV lesions with clinically significant fluorescein leakage was 9.2% in rats treated with high-dose M. officinalis, which was significantly lower than in control rats (53.4%, P<0.001). The levels of VEGF, MMP-2, and MMP-9 were significantly lower in the high-dose group than in the control group. Meanwhile, M. officinalis extract suppressed t-BH-induced transcription of VEGF and MMP-9 in ARPE-19 cells and HUVECs.

          Conclusions

          Systemic administration of M. officinalis extract suppressed laser-induced CNV formation in rats. Inhibition of VEGF and MMP-9 via anti-oxidative activity may underlie this effect.

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          Most cited references37

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          Ranibizumab and bevacizumab for neovascular age-related macular degeneration.

          Clinical trials have established the efficacy of ranibizumab for the treatment of neovascular age-related macular degeneration (AMD). In addition, bevacizumab is used off-label to treat AMD, despite the absence of similar supporting data. In a multicenter, single-blind, noninferiority trial, we randomly assigned 1208 patients with neovascular AMD to receive intravitreal injections of ranibizumab or bevacizumab on either a monthly schedule or as needed with monthly evaluation. The primary outcome was the mean change in visual acuity at 1 year, with a noninferiority limit of 5 letters on the eye chart. Bevacizumab administered monthly was equivalent to ranibizumab administered monthly, with 8.0 and 8.5 letters gained, respectively. Bevacizumab administered as needed was equivalent to ranibizumab as needed, with 5.9 and 6.8 letters gained, respectively. Ranibizumab as needed was equivalent to monthly ranibizumab, although the comparison between bevacizumab as needed and monthly bevacizumab was inconclusive. The mean decrease in central retinal thickness was greater in the ranibizumab-monthly group (196 μm) than in the other groups (152 to 168 μm, P=0.03 by analysis of variance). Rates of death, myocardial infarction, and stroke were similar for patients receiving either bevacizumab or ranibizumab (P>0.20). The proportion of patients with serious systemic adverse events (primarily hospitalizations) was higher with bevacizumab than with ranibizumab (24.1% vs. 19.0%; risk ratio, 1.29; 95% confidence interval, 1.01 to 1.66), with excess events broadly distributed in disease categories not identified in previous studies as areas of concern. At 1 year, bevacizumab and ranibizumab had equivalent effects on visual acuity when administered according to the same schedule. Ranibizumab given as needed with monthly evaluation had effects on vision that were equivalent to those of ranibizumab administered monthly. Differences in rates of serious adverse events require further study. (Funded by the National Eye Institute; ClinicalTrials.gov number, NCT00593450.).
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            Age-related macular degeneration

            Wanjiku Mathenge What is AMD? Age-related macular degeneration (AMD) is a disease of the retina that usually develops in people aged 60 years and older. It affects about 8.7% of the world's population and is the leading cause of blindness among people aged 50 and older in industrialised countries. 1 AMD affects the macula. When it becomes advanced, it destroys the central vision we use to look straight ahead. This is necessary for recognising faces, reading books or using mobile phone screens, watching television, sewing, preparing food, driving, safely navigating stairs and performing other daily tasks we take for granted. If the macula is damaged, the picture is there but the fine points are not clear. Fortunately, the peripheral vision remains intact. This means that some patients with AMD will retain some independence, and eye workers should reassure them that peripheral vision will not be lost, even if no treatment is possible. Is it increasing in low- and middle-income countries? A recent review of the global prevalence of AMD shows that the number of people with AMD in 2020 is projected to be 196 million, which will increase to 288 million in 2040. 1 Studies of AMD in low- and middle-income countries have shown that, in contrast to what was originally thought, AMD is not rare in Asian and African populations but is instead a significant contributor to blindness. Table 1 shows the prevalence from some recent studies involving different ethnic groups. Classification AMD can be classified as either early-stage or late-stage. In the early stage, AMD is characterised by atrophy or hypertrophy of the retinal pigment epithelium (RPE) underlying the central macula, as well as drusen deposition. (Drusen are deposits of extracellular material lying between the basement membrane of the RPE and the inner collagen layer of Bruch's membrane beneath the RPE.) Early AMD. There are irregular pale dots at the macula, which are called drusen. They are caused by a build-up of waste products from photoreceptor metabolism. Although drusen are associated with AMD, most patients with drusen will not develop severe AMD The early stages of AMD may progress to either atrophic (‘dry’) or exudative (‘wet’) AMD. It is these advanced stages that are associated with vision impairment. In atrophic AMD there is atrophy of the central macula, with gradual destruction of the RPE and the photoreceptors. In exudative AMD, abnormal choroidal vessels/capillaries (pathologic choroidal neovascular membranes) develop under the macula, leak fluid and blood, and, ultimately, cause a central fibrous sub-retinal scar, with destruction of the photoreceptors and retinal pigment epithelium. Approximately 10–20% of patients with atrophic AMD can progress to the exudative form. Risk factors Susceptibility to AMD is influenced by increasing age, smoking and family history. Smoking is the most consistent risk factor associated with advanced AMD in the majority of the prevalence studies. Several genetic variants that influence susceptibility to AMD have recently been identified. People who have one or more of these genetic variations are at particularly high risk of developing AMD if they also smoke. Three types of nutritional factors have been investigated for their potential protection against eye ageing: antioxidants (mainly zinc and vitamins C and E), the carotenoids lutein and xeanthine and omega-3 polyunsaturated fatty acids. Unfortunately, the results of supplementation have been disappointing, as large doses must be taken daily for the remainder of the patient's life and the benefit, if any, is small. Table 1. Prevalence of AMD in recent studies Author; Study Dates and country Number of subjects (N); age Prevalence of late AMD (%) La; Korean National Health and Nutrition Survey 2008–2011, Korea N = 14,352; ≥ 50 years 0.6 Mathenge; Nakuru Posterior Segment Eye Study 2007–2008, Kenya N = 3,304; ≥ 50 years 1.2 Kawasaki; Funagata Study 2000–2002, Japan N = 1,037; ≥ 55 years 0.8 Krishnan; INDEYE 2005–2007, India N = 4,266; ≥ 60 years 1.2 Korb; European cohort: Gutenberg Health Study 2007–2012, Germany N = 4,340; 35–74 years 0.2 How it presents AMD occurs in both eyes, but it is often asymmetric. In the early stage, patients are often without symptoms, or sometimes they notice mild symptoms such as minimally blurred central visual acuity, reduced contrast, changes in the way colour is seen, and mild metamorphopsia (distortion of visual images). Patients who develop atrophic AMD may notice a scotoma (blind spot), which slowly enlarges over months or years before becoming stable. This particularly affects reading. Patients with exudative AMD typically describe painless progressive blurring of their central visual acuity, which usually occurs quite rapidly, over a few weeks. Patients also report relative or absolute central scotomas, metamorphopsia and difficulty with reading. Using the Amsler grid for self-testing The Amsler grid can be given to patients with early AMD (and any other patients over 60 years of age) for self-testing. The Amsler grid can help the person spot macular defects early and tell their eye care worker about any increase in the distortion they see (which indicates increasing damage). Those reporting distortion should visit an ophthalmologist for further tests. If someone has a normal test, they should continue testing at regular intervals. If an Amsler grid is unavailable, people can test themselves for distortion by looking at a straight edge or a right angle, such as a door frame or window, with one eye at a time. If they notice any distortion, they should contact their nearest eye care or health care worker and request referral to an ophthalmologist. Early detection of wet AMD is critical because treatment, when indicated, is most successful when performed before damage occurs. The natural history of exudative AMD or occasionally atrophic AMD results in a stable central scotoma in which the visual acuity falls below the reading level and the legal driving level. With exudative AMD, the visual outcome can be much worse. However, peripheral vision is usually retained. At the district level With the advent of effective therapy for the neovascular form of AMD, early diagnosis and treatment is recommended and there is increased emphasis on patient self-screening for the early symptoms of disease. The most important preventive measure is to stop smoking. If a patient over the age of 60 years presents with any symptoms of AMD, visual acuity should be tested and recorded. At the primary level, all patients with reduced vision should be referred to the eye clinic for further assessment. At the district hospital, the macula can be examined for the presence of drusen (see image on page 49) or pigment changes at the macula. Drusen can be seen as pale yellow deposits. If these are present then an Amsler grid test may be carried out. The Amsler grid is a test that can be used in clinics to screen people over 60 years of age. It can also be taught to patients with early AMD for self-testing. An Amsler grid consists of straight lines, with a reference dot in the centre. Each eye is tested separately. The patient is advised to hold the chart at the normal reading distance and to cover one eye. While focusing only on the central dot, the patient describes whether she or he sees any distortions in the grid pattern. Someone with macular degeneration may see some or all of the following: Straight lines that appear wavy or bent Boxes that differ in size or shape from the others Lines that are missing, blurry or discoloured Dark areas at the centre of the grid. Patients with an abnormal Amsler grid test should be referred to an ophthalmologist. Investigations The ophthalmologist's initial examination of patients with signs and symptoms of AMD should include visual acuity testing and a thorough stereo examination of the macula using a biomicroscopy lens (60–90D). This is often followed by imaging studies such as: Stereo colour photography of the fundus: for establishing, documenting, and tracking the exact size of the lesion. Fundus fluorescein angiography (FFA): the gold standard for diagnosing choroidal new vessels (CNV) due to AMD. Facilities performing FFA must have an emergency care plan and a protocol to minimise the risk and to manage any complications. Optical coherence tomography (OCT): excellent at detecting increased retinal thickness due to leakage from the abnormal vessels. This is a simpler, faster and safer investigation than FFA, but OCT machines are still very expensive. Management Until recently, ophthalmologists used laser destruction of abnormal vessels/capillaries as the primary treatment for exudative AMD. 2 These procedures included thermal laser photocoagulation and later the inclusion of intravascular photosensitisers such as verteporfin used in photodynamic therapy. However, at best these treatments slowed progression of the condition. They were not expected to lead to any improvement in vision. The treatment of exudative AMD changed dramatically with the advent of vascular endothelial growth factor (VEGF) inhibitors (see articles on pages 44–48). Pharmaceutical drugs have been developed to block or neutralise VEGF in patients with AMD. These include pegaptanib (Macugen), ranibizumab (Lucentis), bevacizumab (Avastin), and aflibercept (Eylea). These are given as intravitreal injections and several doses are needed. They have been shown to stabilise vision in most patients with exudative AMD, and many patients will experience a significant improvement in visual acuity. 3 There are no effective treatments for atrophic AMD at present. Patients should be reassured that progression is usually slow and they are likely to retain their independence even if reading vision is compromised. Other useful interventions may include smoking cessation, rehabilitation and low vision aids. The latter two are important in improving patients' quality of life, and health workers should make patients aware of these options and how to access them.
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              2002 global update of available data on visual impairment: a compilation of population-based prevalence studies.

              For the past 25 years, the WHO Programme for the Prevention of Blindness and Deafness has maintained a Global Data Bank on visual impairment with the purpose of storing the available epidemiological data on blindness and low vision. The Data Bank has now been updated to include studies conducted since the last update in 1994. An extensive literature search was conducted in international and national scientific and medical journals to identify epidemiological studies that fulfilled basic criteria for inclusion in the Data Bank, namely a clearly stated definition of blindness and low vision, and prevalence rates derived from population-based surveys. Sources such as National Prevention of Blindness Programmes, academic institutions or WHO country or regional reports were also investigated. Two-hundred-and-eight population-based studies on visual impairment for 68 countries are reported in detail, providing an up-to-date, comprehensive compilation of the available information on visual impairment and its causes globally.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                14 October 2014
                : 9
                : 10
                : e110109
                Affiliations
                [1 ]Department of Ophthalmology, Seoul National University College of Medicine, Seoul National University Hospital, Seoul, Korea
                [2 ]Department of Ophthalmology, Seoul National University Hospital Biomedical Research Institute, Seoul, Korea
                [3 ]Department of Biomedical Sciences, Seoul National University Graduate School, Seoul, Korea
                Medical University of South Carolina, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: EKL YJK HGY. Performed the experiments: EKL YJK JYK HBS HGY. Analyzed the data: EKL YJK HGY. Contributed reagents/materials/analysis tools: EKL HGY. Contributed to the writing of the manuscript: EKL HGY.

                Article
                PONE-D-14-18992
                10.1371/journal.pone.0110109
                4197006
                25314292
                ceefa8f1-1022-4496-803c-7b28fadf4e83
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 28 April 2014
                : 15 September 2014
                Page count
                Pages: 11
                Funding
                This research was supported by a grant of the Korea Health technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (Grant Number: A121835-1201-0000103). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Agronomy
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                Medicine and Health Sciences
                Oncology
                Cancer Treatment
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                Retinal Degeneration
                Macular Degeneration
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                The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.

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