Time Course of Collateral Vessel Formation After Retinal Vein Occlusion Visualized by OCTA and Elucidation of Factors in Their Formation

Overview

Journal Heliyon

Specialty Social Sciences

Date 2021 Jan 21

PMID 33474512

Citations 3

Authors

Hajime Takahashi

Kazuki Nakagawa

Haruhiko Yamada

Hidetsugu Mori

Shimpei Oba

Keiko Toyama

Kanji Takahashi

Affiliations

Soon will be listed here.

Abstract

Background: It is clinically recognized that collateral vessels can form after retinal vein occlusion (RVO) in some cases and these vessels can lead to spontaneous recovery of the pathological condition. In recent years, optical coherence tomography angiography (OCTA) has become a decisive clinical instrument. Unlike previous angiography tests, OCTA enables the non-invasive visualization of fundus vasculature without the need for administration of a contrast agent. However, it remains to be determined if OCTA depicts the 'true' histological status as several studies have reported artifacts in OCTA imaging.

Methods: We generated a laser-induced mouse RVO model, and evaluated the subsequent formation of collateral vessels in order to understand the mechanisms by which collateral vessels form using OCTA imaging, as well as molecular and histological assessments.

Results: We succeeded in visualizing the time course of collateral vessel formation in a mouse RVO model and confirmed the similarity in formation of collateral vessels only within the deep layer of the retina in both human and mouse. We hypothesized that sphingosine 1-phosphate receptor-1 (S1PR1) may play important roles via vascular shear stress linking vein occlusion and collateral vessel formation. Results from OCTA revealed that collateral vessels are increased in response to administration of a S1PR1 agonist in a mouse RVO model. Based on quantitative reverse transcription polymerase chain reaction (qRT-PCR), S1PR1 messenger ribonucleic acid (mRNA) levels in the whole retina peaked 6 h after photocoagulation in this model. Immunohistochemical staining of retinal flat mounts revealed that S1PR1 staining occurred along the laser-occluded blood vessels.

Conclusion: We observed the temporal process of collateral vessel formation in a mouse RVO model and identified the relationship between S1PR1 and shear stress as one of the factors in collateral vessel formation in RVO.

Citing Articles

Exploring laser-induced acute and chronic retinal vein occlusion mouse models: Development, temporal in vivo imaging, and application perspectives.

Xu X, Li X, Tang Q, Zhang Y, Zhang L, Zhang M PLoS One. 2024; 19(6):e0305741.

PMID: 38885229 PMC: 11182531. DOI: 10.1371/journal.pone.0305741.

Differences in collateral vessel formation after experimental retinal vein occlusion in spontaneously hypertensive rats and wild-type rats.

Omi M, Yamada H, Takahashi H, Mori H, Oba S, Hattori Y Heliyon. 2024; 10(6):e27160.

PMID: 38509953 PMC: 10950832. DOI: 10.1016/j.heliyon.2024.e27160.

In vivo Vascular Injury Readouts in Mouse Retina to Promote Reproducibility.

Chen C, Potenski A, Colon Ortiz C, Avrutsky M, Troy C J Vis Exp. 2022; (182).

PMID: 35532239 PMC: 9233924. DOI: 10.3791/63782.

References

Zhang H, Sonoda K, Qiao H, Oshima T, Hisatomi T, Ishibashi T . Development of a new mouse model of branch retinal vein occlusion and retinal neovascularization. Jpn J Ophthalmol. 2007; 51(4):251-7. DOI: 10.1007/s10384-007-0445-2. View

Tomiyasu T, Hirano Y, Yoshida M, Suzuki N, Nishiyama T, Uemura A . Microaneurysms cause refractory macular edema in branch retinal vein occlusion. Sci Rep. 2016; 6:29445. PMC: 4937381. DOI: 10.1038/srep29445. View

Suzuki N, Hirano Y, Tomiyasu T, Kurobe R, Yasuda Y, Esaki Y . Collateral vessels on optical coherence tomography angiography in eyes with branch retinal vein occlusion. Br J Ophthalmol. 2018; 103(10):1373-1379. DOI: 10.1136/bjophthalmol-2018-313322. View

Klein R, Klein B, Henkind P, Bellhorn R . Retinal collateral vessel formation. Invest Ophthalmol. 1971; 10(7):471-80. View

Iwasawa E, Ichijo M, Ishibashi S, Yokota T . Acute development of collateral circulation and therapeutic prospects in ischemic stroke. Neural Regen Res. 2016; 11(3):368-71. PMC: 4828985. DOI: 10.4103/1673-5374.179033. View

Suzuki N, Hirano Y, Yoshida M, Tomiyasu T, Uemura A, Yasukawa T . Microvascular Abnormalities on Optical Coherence Tomography Angiography in Macular Edema Associated With Branch Retinal Vein Occlusion. Am J Ophthalmol. 2015; 161:126-32.e1. DOI: 10.1016/j.ajo.2015.09.038. View

Tsuboi K, Sasajima H, Kamei M . Collateral Vessels in Branch Retinal Vein Occlusion: Anatomic and Functional Analyses by OCT Angiography. Ophthalmol Retina. 2019; 3(9):767-776. DOI: 10.1016/j.oret.2019.04.015. View

Hassani F, Ebrahimi B, Moini A, Ghiaseddin A, Bazrafkan M, Hassanzadeh G . Chitosan Hydrogel Supports Integrity of Ovarian Follicles during In Vitro Culture: A Preliminary of A Novel Biomaterial for Three Dimensional Culture of Ovarian Follicles. Cell J. 2019; 21(4):479-493. PMC: 6722450. DOI: 10.22074/cellj.2020.6393. View

Arderiu G, Pena E, Badimon L . Angiogenic microvascular endothelial cells release microparticles rich in tissue factor that promotes postischemic collateral vessel formation. Arterioscler Thromb Vasc Biol. 2014; 35(2):348-57. DOI: 10.1161/ATVBAHA.114.303927. View

10.

Christoffersen N, Larsen M . Pathophysiology and hemodynamics of branch retinal vein occlusion. Ophthalmology. 1999; 106(11):2054-62. DOI: 10.1016/S0161-6420(99)90483-9. View

11.

Ebneter A, Agca C, Dysli C, Zinkernagel M . Investigation of retinal morphology alterations using spectral domain optical coherence tomography in a mouse model of retinal branch and central retinal vein occlusion. PLoS One. 2015; 10(3):e0119046. PMC: 4361633. DOI: 10.1371/journal.pone.0119046. View

12.

Khayat M, Lois N, Williams M, Stitt A . Animal Models of Retinal Vein Occlusion. Invest Ophthalmol Vis Sci. 2017; 58(14):6175-6192. DOI: 10.1167/iovs.17-22788. View

13.

Belting M, Dorrell M, Sandgren S, Aguilar E, Ahamed J, Dorfleutner A . Regulation of angiogenesis by tissue factor cytoplasmic domain signaling. Nat Med. 2004; 10(5):502-9. DOI: 10.1038/nm1037. View

14.

Ghimire K, Zaric J, Alday-Parejo B, Seebach J, Bousquenaud M, Stalin J . MAGI1 Mediates eNOS Activation and NO Production in Endothelial Cells in Response to Fluid Shear Stress. Cells. 2019; 8(5). PMC: 6562810. DOI: 10.3390/cells8050388. View

15.

de Carlo T, Romano A, Waheed N, Duker J . A review of optical coherence tomography angiography (OCTA). Int J Retina Vitreous. 2016; 1:5. PMC: 5066513. DOI: 10.1186/s40942-015-0005-8. View

16.

Wada T, Song Y, Oomae T, Sogawa K, Yoshioka T, Nakabayashi S . Longitudinal Changes in Retinal Blood Flow in a Feline Retinal Vein Occlusion Model as Measured by Doppler Optical Coherence Tomography and Optical Coherence Tomography Angiography. Invest Ophthalmol Vis Sci. 2020; 61(2):34. PMC: 7326600. DOI: 10.1167/iovs.61.2.34. View

17.

Lee H, Wang Y, Fayed A, Fawzi A . Exploring the relationship between collaterals and vessel density in retinal vein occlusions using optical coherence tomography angiography. PLoS One. 2019; 14(7):e0215790. PMC: 6655539. DOI: 10.1371/journal.pone.0215790. View

18.

Klein L, Campos E . The Embryologic Origin of Vieussens' Ring. J Invasive Cardiol. 2019; 31(3):49-51. DOI: 10.25270/jic/19.3103.49. View

19.

Nakagawa K, Yamada H, Mori H, Toyama K, Takahashi K . Comparison between optical coherence tomography angiography and immunolabeling for evaluation of laser-induced choroidal neovascularization. PLoS One. 2018; 13(8):e0201958. PMC: 6084993. DOI: 10.1371/journal.pone.0201958. View

20.

Fuma S, Nishinaka A, Inoue Y, Tsuruma K, Shimazawa M, Kondo M . A pharmacological approach in newly established retinal vein occlusion model. Sci Rep. 2017; 7:43509. PMC: 5333144. DOI: 10.1038/srep43509. View