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Animal Models of Retinal Vein Occlusion Reviews Animal Models of Retinal Vein Occlusion Meiaad Khayat,1,2 Noemi Lois,1 Michael Williams,3 and Alan W. Stitt1 1Wellcome-Wolfson Centre for Experimental Medicine, School of Medicine, Dentistry and Biomedical Sciences, Queen’s University, Belfast, United Kingdom 2Department of Anatomy, College of Medicine–Rabigh Branch, King Abdulaziz University, Jeddah, Saudi Arabia 3Centre for Medical Education, School of Medicine, Dentistry and Biomedical Sciences, Queen’s University, Belfast, United Kingdom Correspondence: Noemi Lois, Well- PURPOSE. To provide a comprehensive and current review on the available experimental come-Wolfson Centre for Experi- animal models of retinal vein occlusion (RVO) and to identify their strengths and limitations mental Medicine, School of with the purpose of helping researchers to plan preclinical studies on RVO. Medicine, Dentistry and Biomedical Sciences, Queen’s University Belfast, METHODS. A systematic review of the literature on experimental animal models of RVO was 97 Lisburn Road, BT9 7AE, Belfast, undertaken. Medline, SCOPUS, and Web of Science databases were searched. Studies United Kingdom; published between January 1, 1965, and March 31, 2017, and that met the inclusion criteria [email protected]. were reviewed. The data extracted included animal species used, methods of inducing RVO, Submitted: August 10, 2017 and the clinical and histopathologic features of the models, especially in relation to strengths, Accepted: October 16, 2017 limitations, and faithfulness to clinical sequelae. Citation: Khayat M, Lois N, Williams RESULTS. A total of 128 articles fulfilling the inclusion criteria were included. Several species M, Stitt AW. Animal models of retinal were used to model human branch and central RVO (BRVO; CRVO) with nonhuman primates vein occlusion. Invest Ophthalmol Vis being the most common, followed by rodents and pigs. BRVO and CRVO were most Sci. 2017;58:6175–6192. DOI: commonly induced by laser photocoagulation and all models showed early features of clinical 10.1167/iovs.17-22788 disease, including retinal hemorrhages and retinal edema. These features made many of the models adequate for studying the acute phase of BRVO and CRVO, although macular edema, retinal ischemia, and neovascular complications were observed in only a few experimental animal models (laser-induced model in rodents, pigs, and nonhuman primates, diathermy- induced model in pigs, and following intravitreal injection of PD0325901 in rabbits for BRVO; and in the laser-induced model in rodents, rabbits, and nonhuman primates, diathermy- induced model in nonhuman primates, following permanent ligation of the central retinal vein in nonhuman primates, and with intravitreal injection of thrombin in rabbits for CRVO). CONCLUSIONS. Experimental animal models of RVO are available to study the pathogenesis of this disease and to evaluate diagnostic/prognostic biomarkers and to develop new therapeutics. Data available suggest laser-induced RVO in pigs and rodents to be overall the best models of BRVO and the laser-induced RVO rodents the best model for CRVO. Keywords: retinal vein occlusion, retinal vein thrombosis, ischemia, experimental models, animal models, in vivo models etinal vein occlusion (RVO) is the second most common structural damage result of the disease.10,25–59 Furthermore, R vascular cause of visual loss, surpassed only by diabetic each of these treatments carries a risk to patients, such as retinopathy.1–5 Obstruction of the retinal venous system is destruction of the retina following laser photocoagulation, commonly caused by thrombus formation, which may result in endophthalmitis following intravitreal injections, and cataract devastating consequences, including macular edema and and glaucoma as a result of steroid administration. Treatments neovascular complications, leading to visual impairment and for macular edema that are a result of RVO have been blindness.1,6–14 RVO has been typically classified into central predominantly investigated for the nonischemic form, with (CRVO), branch (BRVO), hemicentral and hemispheric types most randomized clinical trials excluding or including only few based on the site of the occlusion.1,2,4,5,15–17 Each of these RVO with the iRVO.35,39,40,45,47,52–55,60 In trials in which they have types has been further subclassified into ischemic and been included, only approximately 50% or less of patients with nonischemic forms based on the severity of the disease and iRVO show a meaningful improvement in visual acuity the likelihood of developing neovascular complications. Ische- following these therapies,34,37,38,45,48–51,57 with often poor mic RVO (iRVO) is the most severe form, associated with higher final visual acuity ( 20/100) despite treatment.10,34,36–38,41,43, risk of complications and having a poorer prognosis than non- 51,57 iRVO.1,2,4,15,17,18 Further research is still needed to improve current Current treatments of RVO, including laser photocoagula- understanding of the pathogenesis of RVO as well as to identify tion, intravitreal anti-VEGF therapies, intravitreal steroids, and more clinically effective and cost-effective therapeutic options. pars plana vitrectomy, target the complications of RVO, namely This is especially true for patients with iRVO. macular edema and neovascularization and its consequences,1, Experimental animal models often can be useful to study 5,7,16,17,19–24 and may not fully reverse the functional and disease mechanisms and to test the efficacy and potential Copyright 2017 The Authors iovs.arvojournals.org j ISSN: 1552-5783 6175 This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License. Downloaded from iovs.arvojournals.org on 09/25/2021 Animal Models of RVO IOVS j December 2017 j Vol. 58 j No. 14 j 6176 toxicity of new treatments. Such animal approaches have been successful in ophthalmic research, allowing advancement in our understanding of pathogenesis and development of improved novel therapies.61–66 Experimental animal models of RVO also are available, which variably develop functional and structural features resembling those present in people with this disorder. Herein, we aim at providing a comprehen- sive up-to-date review on experimental animal models of RVO References including species, methods of vessel occlusion, their clinico- histopathologic features, and the limits of their translational , number of articles. n value. Taken together, this focused and in-depth review ought 190, 192, 193 to help researchers design future studies and appreciate the strengths and weaknesses of the animal models they use. 13) 175, 176, 178–181, 184, 187– 6) 130–134, 154 8) 80,1) 83, 85, 89, 90, 92, 96, 97 114 n ¼ ¼ ¼ ¼ METHODS ent of neovascularization, extensive areas of 4) 180, 186, 190, 193 ¼ A systematic review of the literature was conducted, and data Total, sources were Medline, SCOPUS, and Web of Science databases. (ischemia (MO (ischemia Keywords including ‘‘retinal vein occlusion,’’ ‘‘retinal vein (ischemia thrombosis,’’ and ‘‘retinal vein obstruction’’ were combined n with ‘‘experimental models’’ or ‘‘animal models.’’ The search 1) (ischemia covered published articles from January 1, 1965, to March 31, ¼ 2017, and was filtered to include articles in English only. The included articles of studies describing methods of creating outer retinal layers). MO, macular edema; animal models of RVO and their findings were analyzed, and Intravitreal PD0325901, 6 data contained in these articles were used to inform species- (ischemia specific model systems, the range of methods for inducing vein occlusion, pathologic and clinical features developed in these models, and strengths and limitations of available models. The n information extracted was used to populate Tables 1 through 8 of this review. In addition, their clinical value and potential translational implications for the management of patients with this disorder was considered. Changes on levels of cytokines/ chemokines/growth factors and other biochemical and molec- Diathermy, ular events occurring as a result of the induction or RVO in these models, as well as effects of treatments tested in these animal models are beyond the scope of this review and, thus, are not summarized herein. þ n RESULTS Studies Included After removal of duplicates, a total of 320 titles were identified and their abstracts obtained and evaluated for potential Photosensitizer, inclusion in the review. Of the 320 abstracts, 193 were found to relate to studies outside the scope of this review and, thus, Photodynamic Therapy were excluded. Full articles of the remaining 128 studies were obtained, found to be directly related to the topic of this 6 review, and used to extract pertinent data. n 13) 6) Species 8) ¼ ¼ ¼ Several animal species have been used to study RVO, including 4) rodents,67–100 rabbits,101–114 cats,115–124 dogs,125–127 pigs,128– ¼ 156 and nonhuman primates82,111,129,157–196 (Tables 1, 2). Each (MO 21(ischemia 0 0 0 21 129, 175–181, 183–194, 196 64320(ischemia 1 1 0 2 0 5 0 4 1 0 0 0 9 10 3 26 104–107, 109, 110, 112, 114 115–124 125–127 129–134, 136–142, 144–156 17(ischemia 3 0 0 20 70, 74, 80, 83–86, 88–100, 220 71 7 9 1 89 of these species has its own size and anatomic advantages, but Photosensitizer, also ethical challenges and cost implications; these have been summarized in Table 3. Although the retina and retinal vessels Laser Photocoagulation of these animals share many anatomic features with humans, differences still exist and are more pronounced in some n species (Table 4). None of the animal models, with the exception of the nonhuman primate, have an anatomic macula or fovea centralis.197 Pigs,198–202 cats,201,203 and dogs198,204 Animal Species and Techniques Used to Induce BRVO n have a central retinal area with high density of ganglion cells n Species n n 1. n and cone photoreceptors known as area centralis, which n would correspond to the fovea centralis in humans but is less Bolded values represent models that addressed macular edema or ischemic features.
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