Establishment and research progress of retina ischemic animal model_Chinese Journal of Ocular Fundus Diseases

Authors：

Zhang Yongjie ¹ , Xu Hong ² ,  Tian Xuesong ¹

1. Innovation Research Institute of Traditional Chinese Medicine, Center for Drug Safety Evaluation and Research, Shanghai University of Traditional Chinese Medicine, Shanghai 201203, China;
2. Department of Acupuncture-Moxibustion, Longhua Hospital, Shanghai University of Traditional Chinese Medicine, Shanghai 200031, China;
Zhang Yongjie and Xu Hong are contributed equally to the article;

Corresponding author：

Tian Xuesong, Email: xuesong.tian@shutcm.edu.cn

Keywords：

Retina; Ischemia; Models, animal; Review

DOI：

10.3760/cma.j.cn511434-20200716-00342

Video：

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Retinal ischemia is the common pathologic process in many ophthalmic diseases, including ischemic optic neuropathy, retinal artery and vein occlusion, carotid artery obstructive disease, retinopathy of prematurity, chronic diabetic retinopathy and glaucoma. It is very important to establish animal models to investigate pathology mechanism and explore the treatment of retinal ischemia disease. At present, the commonly used methods for establishing retinal ischemia animal models include increasing intraocular pressure, ligating of blood vessels, suture method, photochemical method, and drug injection etc. This article summarizes the methods to establish the animal models and analyzes the indication for each animal model. It is expected that the method of establishing a retinal ischemic animal model will be helpful to the experimental design of follow-up retinal ischemia studies.

Citation： Zhang Yongjie, Xu Hong, Tian Xuesong. Establishment and research progress of retina ischemic animal model. Chinese Journal of Ocular Fundus Diseases, 2021, 37(5): 408-413. doi: 10.3760/cma.j.cn511434-20200716-00342 Copy

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6.	Osborne NN, Larsen AK. Antigens associated with specific retinal cells are affected by ischaemia caused by raised intraocular pressure: effect of glutamate antagonists[J]. Neurochem Int, 1996, 29(3): 263-270. DOI: 10.1016/0197-0186(96)00005-8.
7.	Gurdita A, Tan B, Joos KM, et al. Pigmented and albino rats differ in their responses to moderate, acute and reversible intraocular pressure elevation[J]. Doc Ophthalmol, 2017, 134(3): 205-219. DOI: 10.1007/s10633-017-9586-x.
8.	Osborne NN, Casson RJ, Wood JP, et al. Retinal ischemia: mechanisms of damage and potential therapeutic strategies[J]. Prog Retin Eye Res, 2004, 23(1): 91-147. DOI: 10.1016/j.preteyeres.2003.12.001.
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26.	Wang W, Liu X, Lu H, et al. A method for predicting the success of Pulsinell's four-vessel occlusion rat model by LDF monitoring of cerebral blood flow decline[J/OL]. J Neurosci Methods, 2019, 328: 108439[2019-12-01]. https://pubmed.ncbi.nlm.nih.gov/31545958/. DOI: 10.1016/j.jneumeth.2019.108439.
27.	Ozden S, Müftüoğlu S, Tatlipinar S, et al. Protective effects of antithrombin Ⅲ on retinal ischemia/reperfusion injury in rats: a histopathologic study[J]. Eur J Ophthalmol, 2005, 15(3): 367-373. DOI: 10.1177/112067210501500309.
28.	Gallyas F, Hsu M, Buzsaki G. Delayed degeneration of the optic tract and neurons in the superior colliculus after forebrain ischemia[J]. Neurosci Lett, 1992, 144(1-2): 177-179. DOI: 10.1016/0304-3940(92)90744-r.
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1. Country MW. Retinal metabolism: a comparative look at energetics in the retina[J]. Brain Res, 2017, 1672: 50-57. DOI: 10.1016/j.brainres.2017.07.025.
2. Smith GG, Baird CD. Survival time of retinal cells when deprived of their blood supply by increased intraocular pressure[J]. Am J Ophthalmol, 1952, 35(5): 133-136. DOI: 10.1016/0002-9394(52)90266-3.
3. Büchi ER, Suivaizdis I, Fu J. Pressure-induced retinal ischemia in rats: an experimental model for quantitative study[J]. Ophthalmologica, 1991, 203(3): 138-147. DOI: 10.1159/000310240.
4. Ettaiche M, Heurteaux C, Blondeau N, et al. ATP-sensitive potassium channels (K(ATP)) in retina: a key role for delayed ischemic tolerance[J]. Brain Res, 2001, 890(1): 118-129. DOI: 10.1016/s0006-8993(00)03152-8.
5. Safa R, Osborne NN. Retinas from albino rats are more susceptible to ischaemic damage than age-matched pigmented animals[J]. Brain Res, 2000, 862(1-2): 36-42. DOI: 10.1016/s0006-8993(00)02090-4.
6. Osborne NN, Larsen AK. Antigens associated with specific retinal cells are affected by ischaemia caused by raised intraocular pressure: effect of glutamate antagonists[J]. Neurochem Int, 1996, 29(3): 263-270. DOI: 10.1016/0197-0186(96)00005-8.
7. Gurdita A, Tan B, Joos KM, et al. Pigmented and albino rats differ in their responses to moderate, acute and reversible intraocular pressure elevation[J]. Doc Ophthalmol, 2017, 134(3): 205-219. DOI: 10.1007/s10633-017-9586-x.
8. Osborne NN, Casson RJ, Wood JP, et al. Retinal ischemia: mechanisms of damage and potential therapeutic strategies[J]. Prog Retin Eye Res, 2004, 23(1): 91-147. DOI: 10.1016/j.preteyeres.2003.12.001.
9. Gehlbach P, Purple RL. Enhancement of retinal recovery by conjugated deferoxamine after ischemia-reperfusion[J]. Invest Ophthalmol Vis Sci, 1994, 35(2): 669-676. DOI: 10.1007/BF00171675.
10. Shabanzadeh AP, D'Onofrio PM, Monnier PP, et al. Neurosurgical modeling of retinal ischemia-reperfusion injury[J]. J Stroke Cerebrovasc Dis, 2018, 27(4): 845-856. DOI: 10.1016/j.jstrokecerebrovasdis.2017.10.019.
11. Sugiyama K, Gu ZB, Kawase C, et al. Optic nerve and peripapillary choroidal microvasculature of the rat eye[J]. Invest Ophthalmol Vis Sci, 1999, 40(13): 3084-3090.
12. Allen RS, Sayeed I, Cale HA, et al. Severity of middle cerebral artery occlusion determines retinal deficits in rats[J]. Exp Neurol, 2014, 254: 206-215. DOI: 10.1016/j.expneurol.2014.02.005.
13. Scremin, Oscar U. Cerebral vascular system[M]//Paxinos G. The rat nervous system. 4th ed. Amsterdam: Elsevier Inc., 2015: 985-1011.
14. Block F, Schwarz M, Sontag KH. Retinal ischemia induced by occlusion of both common carotid arteries in rats as demonstrated by electroretinography[J]. Neurosci Lett, 1992, 144(1-2): 124-126. DOI: 10.1016/0304-3940(92)90731-l.
15. Qin Y, Ji M, Deng T, et al. Functional and morphologic study of retinal hypoperfusion injury induced by bilateral common carotid artery occlusion in rats[J/OL]. Sci Rep, 2019, 9(1): 80[2019-01-14]. https://pubmed.ncbi.nlm.nih.gov/30643163/. DOI: 10.1038/s41598-018-36400-5.
16. Karamian P, Burford J, Farzad S, et al. Alterations in retinal oxygen delivery, metabolism, and extraction fraction during bilateral common carotid artery occlusion in rats[J]. Invest Ophthalmol Vis Sci, 2019, 60(8): 3247-3253. DOI: 10.1167/iovs.19-27227.
17. Blair NP, Felder AE, Tan MR, et al. A model for graded retinal ischemia in rats[J/OL]. Transl Vis Sci Technol, 2018, 7(3): 10[2018-06-04]. https://pubmed.ncbi.nlm.nih.gov/29881647/. DOI: 10.1167/tvst.7.3.10.
18. Guo XJ, Tian XS, Ruan Z, et al. Dysregulation of neurotrophic and inflammatory systems accompanied by decreased CREB signaling in ischemic rat retina[J]. Exp Eye Res, 2014, 125: 156-163. DOI: 10.1016/j.exer.2014.06.003.
19. Tian XS, Guo XJ, Ruan Z, et al. Long-term vision and non-vision dominant behavioral deficits in the 2-VO rats are accompanied by time and regional glial activation in the white matter[J/OL]. Plos One, 2014, 9(6): e101120[2014-06-26]. https://pubmed.ncbi.nlm.nih.gov/24968196/. DOI: 10.1371/journal.pone.0101120.
20. 孙伟, 耿悦, 陈叶婷, 等. Sprague-Dawley与Wistar大鼠双侧颈总动脉结扎后大脑病理变化和认知功能的差异[J]. 生理学报, 2019, 1(5): 705-716. DOI: 10.13294/j.aps.2019.0065.Sun W, Geng Y, Chen YT, et al. Differences of brain pathological changes and cognitive function after bilateral common carotid artery occlusion between Sprague-Dawley and Wistar rats[J]. Sheng Li Xue Bao, 2019, 1(5): 705-716. DOI: 10.13294/j.aps.2019.0065.
21. Minhas G, Morishita R, Anand A. Preclinical models to investigate retinal ischemia: advances and drawbacks[J/OL]. Front Neurol, 2012, 3: 75[2012-05-11]. https://pubmed.ncbi.nlm.nih.gov/22593752/. DOI: 10.3389/fneur.2012.00075.
22. Minhas G, Morishita R, Shimamura M, et al. Modeling transient retinal ischemia in mouse by ligation of pterygopalatine artery[J]. Ann Neurosci, 2015, 22(4): 222-225. DOI: 10.5214/ans.0972.7531.220406.
23. Ogishima H, Nakamura S, Nakanishi T, et al. Ligation of the pterygopalatine and external carotid arteries induces ischemic damage in the murine retina[J]. Invest Ophthalmol Vis Sci, 2011, 52(13): 9710-9720. DOI: 10.1167/iovs.11-8160.
24. Ohta H, Nishikawa H, Kimura H, et al. Chronic cerebral hypoperfusion by permanent internal carotid ligation produces learning impairment without brain damage in rats[J]. Neuroscience, 1997, 79(4): 1039-1050. DOI: 10.1016/s0306-4522(97)00037-7.
25. Pulsinelli WA, Brierley JB, Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia[J]. Ann Neurol, 1982, 11(5): 491-498. DOI: 10.1002/ana.410110509.
26. Wang W, Liu X, Lu H, et al. A method for predicting the success of Pulsinell's four-vessel occlusion rat model by LDF monitoring of cerebral blood flow decline[J/OL]. J Neurosci Methods, 2019, 328: 108439[2019-12-01]. https://pubmed.ncbi.nlm.nih.gov/31545958/. DOI: 10.1016/j.jneumeth.2019.108439.
27. Ozden S, Müftüoğlu S, Tatlipinar S, et al. Protective effects of antithrombin Ⅲ on retinal ischemia/reperfusion injury in rats: a histopathologic study[J]. Eur J Ophthalmol, 2005, 15(3): 367-373. DOI: 10.1177/112067210501500309.
28. Gallyas F, Hsu M, Buzsaki G. Delayed degeneration of the optic tract and neurons in the superior colliculus after forebrain ischemia[J]. Neurosci Lett, 1992, 144(1-2): 177-179. DOI: 10.1016/0304-3940(92)90744-r.
29. Longa EZ, Weinstein PR, Carlson S, et al. Reversible middle cerebral artery occlusion without craniectomy in rats[J]. Stroke, 1989, 20(1): 84-91. DOI: 10.1161/01.str.20.1.84.
30. Block F, Grommes C, Kosinski C, et al. Retinal ischemia induced by the intraluminal suture method in rats[J]. Neurosci Lett, 1997, 232(1): 45-48. DOI: 10.1016/s0304-3940(97)00575-2.
31. Steele EC, Guo Q, Namura S. Filamentous middle cerebral artery occlusion causes ischemic damage to the retina in mice[J]. Stroke, 2008, 39(7): 2099-2104. DOI: 10.1161/STROKEAHA.107.504357.
32. Lee JY, Castelli V, Bonsack B, et al. Eyeballing stroke: Blood flow alterations in the eye and visual impairments following transient middle cerebral artery occlusion in adult rats[J/OL]. Cell Transplant, 2020, 29: 963689720905805[2020-01-29]. https://pubmed.ncbi.nlm.nih.gov/32098493/. DOI: 10.1177/0963689720905805.
33. Tian X, Guo J, Zhu M, et al. δ-Opioid receptor activation rescues the functional TrkB receptor and protects the brain from ischemia-reperfusion injury in the rat[J/OL]. PLoS One, 2013, 8(7): e69252[2013-07-02]. https://pubmed.ncbi.nlm.nih.gov/23844255/. DOI: 10.1371/journal.pone.0069252.
34. Geng Y, Chen Y, Sun W, et al. Electroacupuncture ameliorates cerebral I/R-induced inflammation through DOR-BDNF/TrkB Pathway[J/OL]. Evid Based Complement Alternat Med, 2020, 2020: 3495836[2020-03-16]. https://pubmed.ncbi.nlm.nih.gov/32256638/. DOI: 10.1155/2020/3495836.
35. Wilson CA, Hatchell DL. Photodynamic retinal vascular thrombosis. Rate and duration of vascular occlusion[J]. Invest Ophthalmol Vis Sci, 1991, 32(8): 2357-2365.
36. Nanda SK, Hatchell DL, Tiedeman JS, et al. A new method for vascular occlusion. Photochemical initiation of thrombosis[J]. Arch Ophthalmol, 1987, 105(8): 1121-1124. DOI: 10.1001/archopht.1987.01060080123041.
37. Watson BD, Dietrich WD, Busto R, et al. Induction of reproducible brain infarction by photochemically initiated thrombosis[J]. Ann Neurol, 1985, 17(5): 497-504. DOI: 10.1002/ana.410170513.
38. Nguyen VP, Li Y, Zhang W, et al. High-resolution multimodal photoacoustic microscopy and optical coherence tomography image-guided laser induced branch retinal vein occlusion in living rabbits[J/OL]. Sci Rep, 2019, 9(1): 10560[2019-07-22]. https://pubmed.ncbi.nlm.nih.gov/31332266/. DOI: 10.1038/s41598-019-47062-2.
39. 温鑫, 袁敏而, 李成, 等. 新型视网膜缺血-再灌注损伤模型的建立及评价[J]. 中华实验眼科杂志, 2020, 38(7): 566-572. DOI: 10.3760/cma.j.cn115989-20190404-00162.Wei X, Yuan ME, Li C, et al. Establishment and evaluation of a novel retinal ischemia-reperfusion injury model[J]. Chin J Exp Ophthalmol, 2020, 38(7): 566-572. DOI: 10.3760/cma.j.cn115989-20190404-00162.
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