The changes of choriocapillaris blood flow in chronic central serous chorioretinopathy before and after photodynamic therapy_Chinese Journal of Ocular Fundus Diseases

Authors：

Liu Juejun ,  Chen Changzheng , Xu Yishuang , Zheng Hongmei , He Lu

Eye Center, People's Hospital of Wuhan University, Wuhan 430060, China;

Corresponding author：

Chen Changzheng, Email: whuchenchzh@163.com

Keywords：

Central serous chorioretinopathy; Tomography, optical coherence; Photochemotherapy; Choroidal capillaries

DOI：

10.3760/cma.j.issn.1005-1015.2019.04.009

Video：

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Objective To quantitatively analyze the changes of choroidal capillaries in chronic central serous chorioretinopathy (CCSC) before and after half-dose photodynamic therapy (PDT).Methods A retrospective cohort study. Nineteen patients (21 eyes) with CCSC were enrolled in this study from November 2017 to September 2018 in People’s Hospital of Wuhan University. Among them, there were 14 males (15 eyes) and 5 females (6 eyes), with diseases course over than 6 months. All patients underwent half-dose PDT. Twenty normal subjects (40 eyes) matched with age and sex in CCSC group were taken as controls. The subfoveal choroidal thickness (SFCT) was measured by Heidelberg depth enhanced imaging-OCT before and after PDT treatment in CCSC patients and in normal subjects. Spectral-domain OCT (Retina map) and Angio-OCT angiography (3 mm×3 mm) were arranged for all subjects at the same time. Macular fovea retinal thickness (CMT) was recorded under OCT-Retina map mode, and Angio-OCT 3 mm×3 mm choroidal capillary images were binarized using Image J software, and calculating the area ratio of low pixel area as flow signal void (FSV). BCVA, spectral-domain OCT and Angio-OCT were performed 1 week and 1, 3 months after PDT with the same equipment and methods before PDT. The changes of CMT, SFCT, FSV and BCVA in CCSC patients before and after PDT treatment were compared. Pearson correlation analysis was used to analyze the correlation between FSV and SFCT, age.Results The average CMT, SFCT and FSV in CCSC patients increased significantly compared with the controls (P＜0.05). The average SFCT and FSV in CCSC patients 3 months after treatment were higher and the average CMT decreased compared with the controls (P=0.000, 0.000, 0.000). Comparison before and after PDT in CCSC patients: there were significant differences in average CMT, SFCT and FSV before and after PDT (P=0.000, 0.000, 0.000). Post Hoc multiple comparisons showed that the average CMT (P=0.000, 0.000, 0.000, 0.000, 0.000) and FSV (P=0.010, 0.000, 0.000, 0.001, 0.000) decreased significantly in all time points except for 1 month and 3 months after treatment, so as the average FSV (P=0.788, 0.702). The average SFCT decreased 1 month and 3 months after treatment compared with the baseline (P=0.024, 0.008), and there was no significant difference between before treatment and 1 week after treatment (P=0.162), and between 1 month and 3 months after treatment (P=0.687). The correlation analysis showed that there was no correlation between FSV and age in CCSC patients (r=0.052, P=0.822), but there was a correlation between FSV and age in controls (r=0.716, P=0.000).Conclusion Quantitative analysis of OCTA showes the degree of choriocapillary ischemia in the form of FSV in CCSC patients decreased after PDT treatment, however, which is still higher than normal controls.

Citation： Liu Juejun, Chen Changzheng, Xu Yishuang, Zheng Hongmei, He Lu. The changes of choriocapillaris blood flow in chronic central serous chorioretinopathy before and after photodynamic therapy. Chinese Journal of Ocular Fundus Diseases, 2019, 35(4): 358-363. doi: 10.3760/cma.j.issn.1005-1015.2019.04.009 Copy

1.	Daruich A, Matet A, Dirani A, et al. Central serous chorioretinopathy: recent findings and new physiopathology hypothesis[J]. Prog Retin Eye Res, 2015, 48: 82-118. DOI: 10.1016/j.preteyeres.2015.05.003.
2.	Lauermann JL, Eter N, Alten F. Optical coherence tomography angiography offers new insights into choriocapillaris perfusion[J]. Ophthalmologica, 2018, 239(2-3): 74-84. DOI: 10.1159/000485261.
3.	Branchini LA, Adhi M, Regatieri CV, et al. Analysis of choroidal morphologic features and vasculat ure in healthy eyes using spectral-domain optical coherence tomography[J]. Ophthalmology, 2013, 120(9): 1901-1908. DOI: 10.1016/j.ophtha.2013.01.066.
4.	Nassisi M, Lavia C, Alovisi C, et al. Short-term choriocapillaris changes in patients with central serous chorioretinopathy after half-dose photodynamic therapy[J/OL]. Int J Mol Sci, 2017, 18(11): 2468[2017-11-20]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5713434/. DOI: 10.3390/ijms18112468.
5.	Xu Y, Su Y, Li L, et al. Effect of photodynamic therapy on optical coherence tomography angiograp hy in eyes with chronic central serous chorioretinopathy[J]. Ophthalmologica, 2017, 237(3): 167-172. DOI: 10.1159/000456676.
6.	Demircan A, Yesilkaya C, Alkin Z. Early choriocapillaris changes after half-fluence photodynamic therapy in chronic central serous chorioretinopathy evaluated by optical coherence tomography angiography: preliminary results[J]. Photodiagnosis Photodyn Ther, 2018, 21: 375-378. DOI: 10.1016/j.pdpdt.2018.01.015.
7.	中华医学会眼科分会眼底病学组, 中国医师协会眼科医师分会眼底病专业委员会. 我国眼底相干光层析血管成像术的操作和阅片规范(2017年)[J]. 中华眼科杂志, 2017, 53(10): 729-734. DOI: 10.3760/cma.j.issn0412.4081.2017.10.003.Chinese Ocular Fundus Diseases Society, Chinese Ophthalmological Society, Chinese Medical Association;Professional Committee of Fundus Diseases, Ophthalmologist Branch of Chinese Doctors Association. Standards for operations and reading of coherent optical tomography angiography in China (2017)[J]. Chin J Ophthalmol, 2017, 53(10): 729-734. DOI: 10.3760/cma.j.issn0412.4081.2017.10.003.
8.	王倩, 魏文斌. 分频幅去相干血管成像[J]. 国际眼科纵览, 2016, 40(2): 112-116. DOI: 10.3760/cma.j.issn.1673-5803.2016.02.009.Wang Q, Wei WB. Optical coherence tomography angiography with split-spectrum amplitude decorrelation angiography[J]. Int Rev Ophthalmol, 2016, 40(2): 112-116. DOI: 10.3760/cma.j.issn.1673-5803.2016.02.009.
9.	Rochepeau C, Kodjikian L, Garcia MA, et al. Optical coherence tomography angiography quantitative assessment of choriocapillaris blood flow in central serous chorioretinopathy[J]. Am J Ophthalmol, 2018, 194: 26-34. DOI: 10.1016/j.ajo.2018.07.004.
10.	王镇, 谭晓俊, 陈翠, 等. 急性中心性浆液性脉络膜视网膜病变渗漏点的频域光相干断层扫描影像特征[J]. 中华眼底病杂志, 2017, 33(6): 577-579. DOI: 10.3760/cma.j.issn.1005-1015.2017.06.005.Wang Z, Tan XJ, Chen C, et al. Spectral-domain optical coherence tomography characteristics of acute central serous chorioretinopathy[J]. Chin J Ocul Fundus Dis, 2017, 33(6): 577-579. DOI: 10.3760/cma.j.issn.1005-1015.2017.06.005.
11.	Shiragami C, Takasago Y, Osaka R, et al. Clinical features of central serous chorioretinopathy with type 1 choroidal neovascularization[J]. Am J Ophthalmol, 2018, 193: 80-86. DOI: 10.1016/j.ajo.2018.06.009.
12.	莫宾, 周海英, 焦璇, 等. 中心性浆液性脉络膜视网膜病变的OCTA特点及与ICGA的比较分析[J]. 国际眼科杂志, 2017, 17(7): 1351-1354. DOI: 10.3980/j.issn.1672-5123.2017.7.40.Mo B, Zhou HY, Jiao X, et al. Comparative study of optical coherence tomography angiography and ICGA in central serous chorioretinopathy[J]. Int Eye Sci, 2017, 17(7): 1351-1354. DOI: 10.3980/j.issn.1672-5123.2017.7.40.
13.	Teussink MM, Breukink MB, van Grinsven MJ, et al. OCT angiography compared to fluorescein and indocyanine green angiography in chronic central serous chorioretinopathy[J]. Invest Ophthalmol Vis Sci, 2015, 56(9): 5229-5237. DOI: 10.1167/iovs.15-17140.
14.	杨智, 王海林. 不同病灶活动程度的中心性浆液性脉络膜视网膜病变患眼脉络膜毛细血管扩张程度、中心凹下脉络膜厚度及其相关性分析[J]. 中华眼底病杂志, 2016, 32(3): 261-265. DOI: 10.3760/cma.j.issn.1005-1015.2016.03.008.Yang Z, Wang HL. The degree of choriocapillary ectasia and sub-foveal choroidal thickness in central serous chorioretinopathy with different activity and the correlation analysis among them[J]. Chin J Ocul Fundus Dis, 2016, 32(3): 261-265. DOI: 10.3760/cma.j.issn.1005-1015.2016.03.008.
15.	Nicolò M, Rosa R, Musetti D, et al. Choroidal vascular flow area in central serous chorioretinopathy using swept-source optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2017, 58(4): 2002-2010. DOI: 10.1167/iovs.17-21417.
16.	Gal-Or O, Dansingani KK, Sebrow D, et al. Inner choroidal flow signal attenuation in pachychoroid disease: optical coherence tomography angiography[J]. Retina, 2018, 38(10): 1984-1992. DOI: 10.1097/IAE.0000000000002051.
17.	Ma DJ, Park UC, Kim ET, et al.Choroidal vascularity changes in idiopathic central serous chorioretinopathy after half-fluence photodynamic therapy[J/OL]. PLoS One, 2018, 13(8): 0202930[2018-08-27]. https://doi.org/10.1371/journal.pone.0202930. DOI: 10.1371/journal.pone.0202930.
18.	Schmidt-Erfurth U, Laqua H, Schlötzer-Schrehard U, et al. Histopathological changes following photodynamic therapy in human eyes[J]. Arch Ophthalmol, 2002, 120(6): 835-844.
19.	Quaranta-El Maftouhi M, El Maftouhi A, Eandi CM. Chronic central serous chorioretinopathy imaged by optical coherence tomographic angiography[J]. Am J Ophthalmol, 2015, 160(3): 581-587. DOI: 10.1016/j.ajo.2015.06.016.
20.	Schmidt-Erfurth U, Kiss C, Sacu S. The role of choroidal hypoperfusion associated with photodynamic therapy in neovascular age-related macular degeneration and the consequences for combination strategies[J]. Prog Retin Eye Res, 2009, 28(2): 145-154. DOI: 10.1016/j.preteyeres.2009.01.001.
21.	Ozkaya A, Alkin Z, Ozveren M, et al. The time of resolution and the rate of recurrence in acute central serous chorioretinopathy following spontaneous resolution and low-fluence photodynamic therapy: a case-control study[J]. Eye (Lond), 2016, 30(7): 1005-1010. DOI: 10.1038/eye.2016.79.
22.	Erikitola OC, Crosby-Nwaobi R, Lotery AJ, et al. Photodynamic therapy for central serous choriore tinopathy[J]. Eye, 2014, 28(8): 944-957. DOI: 10.1038/eye.2014.134.
23.	Seo EJ, Um T, Yoon YH. Abnormal choroidal flow on optical coherence tomography angiography in central serous chorioretinopathy[J]. Clin Exp Ophthalmol, 2019, 47(4): 505-512. DOI: 10.1111/ceo.13454.
24.	Wu JS, Chen SN. Optical coherence tomography angiography for diagnosis of choroidal neovascu larization in chronic central serous chorioretinopathy after photodynamic therapy[J/OL]. Sci Rep, 2019, 9(1): 9040[2019-06-21]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6588615/. DOI: 10.1038/s41598-019-45080-8.
25.	Fung A, Yannuzzi L, Freund KB. Type 1(sub-retinal pigment epithelial) neovascularization in central serous chorioretinopathy masquerading as neovascular age-related macular degeneration[J]. Retina, 2012, 32(9): 1829-1837. DOI: 10.1097/IAE.0b013e3182680a66.
26.	Spaide RF. Choriocapillaris flow features follow a power law distribution: implications for characterization and mechanisms of disease progression[J]. Am J Ophthalmol, 2016, 170: 58-67. DOI: 10.1016/j.ajo.2016.07.023.

1. Daruich A, Matet A, Dirani A, et al. Central serous chorioretinopathy: recent findings and new physiopathology hypothesis[J]. Prog Retin Eye Res, 2015, 48: 82-118. DOI: 10.1016/j.preteyeres.2015.05.003.
2. Lauermann JL, Eter N, Alten F. Optical coherence tomography angiography offers new insights into choriocapillaris perfusion[J]. Ophthalmologica, 2018, 239(2-3): 74-84. DOI: 10.1159/000485261.
3. Branchini LA, Adhi M, Regatieri CV, et al. Analysis of choroidal morphologic features and vasculat ure in healthy eyes using spectral-domain optical coherence tomography[J]. Ophthalmology, 2013, 120(9): 1901-1908. DOI: 10.1016/j.ophtha.2013.01.066.
4. Nassisi M, Lavia C, Alovisi C, et al. Short-term choriocapillaris changes in patients with central serous chorioretinopathy after half-dose photodynamic therapy[J/OL]. Int J Mol Sci, 2017, 18(11): 2468[2017-11-20]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5713434/. DOI: 10.3390/ijms18112468.
5. Xu Y, Su Y, Li L, et al. Effect of photodynamic therapy on optical coherence tomography angiograp hy in eyes with chronic central serous chorioretinopathy[J]. Ophthalmologica, 2017, 237(3): 167-172. DOI: 10.1159/000456676.
6. Demircan A, Yesilkaya C, Alkin Z. Early choriocapillaris changes after half-fluence photodynamic therapy in chronic central serous chorioretinopathy evaluated by optical coherence tomography angiography: preliminary results[J]. Photodiagnosis Photodyn Ther, 2018, 21: 375-378. DOI: 10.1016/j.pdpdt.2018.01.015.
7. 中华医学会眼科分会眼底病学组, 中国医师协会眼科医师分会眼底病专业委员会. 我国眼底相干光层析血管成像术的操作和阅片规范(2017年)[J]. 中华眼科杂志, 2017, 53(10): 729-734. DOI: 10.3760/cma.j.issn0412.4081.2017.10.003.Chinese Ocular Fundus Diseases Society, Chinese Ophthalmological Society, Chinese Medical Association;Professional Committee of Fundus Diseases, Ophthalmologist Branch of Chinese Doctors Association. Standards for operations and reading of coherent optical tomography angiography in China (2017)[J]. Chin J Ophthalmol, 2017, 53(10): 729-734. DOI: 10.3760/cma.j.issn0412.4081.2017.10.003.
8. 王倩, 魏文斌. 分频幅去相干血管成像[J]. 国际眼科纵览, 2016, 40(2): 112-116. DOI: 10.3760/cma.j.issn.1673-5803.2016.02.009.Wang Q, Wei WB. Optical coherence tomography angiography with split-spectrum amplitude decorrelation angiography[J]. Int Rev Ophthalmol, 2016, 40(2): 112-116. DOI: 10.3760/cma.j.issn.1673-5803.2016.02.009.
9. Rochepeau C, Kodjikian L, Garcia MA, et al. Optical coherence tomography angiography quantitative assessment of choriocapillaris blood flow in central serous chorioretinopathy[J]. Am J Ophthalmol, 2018, 194: 26-34. DOI: 10.1016/j.ajo.2018.07.004.
10. 王镇, 谭晓俊, 陈翠, 等. 急性中心性浆液性脉络膜视网膜病变渗漏点的频域光相干断层扫描影像特征[J]. 中华眼底病杂志, 2017, 33(6): 577-579. DOI: 10.3760/cma.j.issn.1005-1015.2017.06.005.Wang Z, Tan XJ, Chen C, et al. Spectral-domain optical coherence tomography characteristics of acute central serous chorioretinopathy[J]. Chin J Ocul Fundus Dis, 2017, 33(6): 577-579. DOI: 10.3760/cma.j.issn.1005-1015.2017.06.005.
11. Shiragami C, Takasago Y, Osaka R, et al. Clinical features of central serous chorioretinopathy with type 1 choroidal neovascularization[J]. Am J Ophthalmol, 2018, 193: 80-86. DOI: 10.1016/j.ajo.2018.06.009.
12. 莫宾, 周海英, 焦璇, 等. 中心性浆液性脉络膜视网膜病变的OCTA特点及与ICGA的比较分析[J]. 国际眼科杂志, 2017, 17(7): 1351-1354. DOI: 10.3980/j.issn.1672-5123.2017.7.40.Mo B, Zhou HY, Jiao X, et al. Comparative study of optical coherence tomography angiography and ICGA in central serous chorioretinopathy[J]. Int Eye Sci, 2017, 17(7): 1351-1354. DOI: 10.3980/j.issn.1672-5123.2017.7.40.
13. Teussink MM, Breukink MB, van Grinsven MJ, et al. OCT angiography compared to fluorescein and indocyanine green angiography in chronic central serous chorioretinopathy[J]. Invest Ophthalmol Vis Sci, 2015, 56(9): 5229-5237. DOI: 10.1167/iovs.15-17140.
14. 杨智, 王海林. 不同病灶活动程度的中心性浆液性脉络膜视网膜病变患眼脉络膜毛细血管扩张程度、中心凹下脉络膜厚度及其相关性分析[J]. 中华眼底病杂志, 2016, 32(3): 261-265. DOI: 10.3760/cma.j.issn.1005-1015.2016.03.008.Yang Z, Wang HL. The degree of choriocapillary ectasia and sub-foveal choroidal thickness in central serous chorioretinopathy with different activity and the correlation analysis among them[J]. Chin J Ocul Fundus Dis, 2016, 32(3): 261-265. DOI: 10.3760/cma.j.issn.1005-1015.2016.03.008.
15. Nicolò M, Rosa R, Musetti D, et al. Choroidal vascular flow area in central serous chorioretinopathy using swept-source optical coherence tomography angiography[J]. Invest Ophthalmol Vis Sci, 2017, 58(4): 2002-2010. DOI: 10.1167/iovs.17-21417.
16. Gal-Or O, Dansingani KK, Sebrow D, et al. Inner choroidal flow signal attenuation in pachychoroid disease: optical coherence tomography angiography[J]. Retina, 2018, 38(10): 1984-1992. DOI: 10.1097/IAE.0000000000002051.
17. Ma DJ, Park UC, Kim ET, et al.Choroidal vascularity changes in idiopathic central serous chorioretinopathy after half-fluence photodynamic therapy[J/OL]. PLoS One, 2018, 13(8): 0202930[2018-08-27]. https://doi.org/10.1371/journal.pone.0202930. DOI: 10.1371/journal.pone.0202930.
18. Schmidt-Erfurth U, Laqua H, Schlötzer-Schrehard U, et al. Histopathological changes following photodynamic therapy in human eyes[J]. Arch Ophthalmol, 2002, 120(6): 835-844.
19. Quaranta-El Maftouhi M, El Maftouhi A, Eandi CM. Chronic central serous chorioretinopathy imaged by optical coherence tomographic angiography[J]. Am J Ophthalmol, 2015, 160(3): 581-587. DOI: 10.1016/j.ajo.2015.06.016.
20. Schmidt-Erfurth U, Kiss C, Sacu S. The role of choroidal hypoperfusion associated with photodynamic therapy in neovascular age-related macular degeneration and the consequences for combination strategies[J]. Prog Retin Eye Res, 2009, 28(2): 145-154. DOI: 10.1016/j.preteyeres.2009.01.001.
21. Ozkaya A, Alkin Z, Ozveren M, et al. The time of resolution and the rate of recurrence in acute central serous chorioretinopathy following spontaneous resolution and low-fluence photodynamic therapy: a case-control study[J]. Eye (Lond), 2016, 30(7): 1005-1010. DOI: 10.1038/eye.2016.79.
22. Erikitola OC, Crosby-Nwaobi R, Lotery AJ, et al. Photodynamic therapy for central serous choriore tinopathy[J]. Eye, 2014, 28(8): 944-957. DOI: 10.1038/eye.2014.134.
23. Seo EJ, Um T, Yoon YH. Abnormal choroidal flow on optical coherence tomography angiography in central serous chorioretinopathy[J]. Clin Exp Ophthalmol, 2019, 47(4): 505-512. DOI: 10.1111/ceo.13454.
24. Wu JS, Chen SN. Optical coherence tomography angiography for diagnosis of choroidal neovascu larization in chronic central serous chorioretinopathy after photodynamic therapy[J/OL]. Sci Rep, 2019, 9(1): 9040[2019-06-21]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6588615/. DOI: 10.1038/s41598-019-45080-8.
25. Fung A, Yannuzzi L, Freund KB. Type 1(sub-retinal pigment epithelial) neovascularization in central serous chorioretinopathy masquerading as neovascular age-related macular degeneration[J]. Retina, 2012, 32(9): 1829-1837. DOI: 10.1097/IAE.0b013e3182680a66.
26. Spaide RF. Choriocapillaris flow features follow a power law distribution: implications for characterization and mechanisms of disease progression[J]. Am J Ophthalmol, 2016, 170: 58-67. DOI: 10.1016/j.ajo.2016.07.023.

Chinese Journal of Ocular Fundus Diseases

The changes of choriocapillaris blood flow in chronic central serous chorioretinopathy before and after photodynamic therapy

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