The progress in clinical research of retinal angiomatous proliferation_Chinese Journal of Ocular Fundus Diseases

Authors：

Liu Xiaoxue ,  Chen Ning

Department of Ophthalmology, Yantai Yuhuangding Hospital, Yantai 264000, China (Liu Xiaoxue, on-job postgraduates, Qingdao University Medical College);

Corresponding author：

Chen Ning, Email: cny0174@sina.com

Keywords：

Retinal diseases/etiology; Retinal diseases/diagnosis; Retinal diseases/therapy; Review

DOI：

10.3760/cma.j.issn.1005-1015.2018.03.025

Video：

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Retinal angiomatous proliferation (RAP) is a genetic distinct subgroup of exudative age-related macular degeneration which shows a rapid and severe vision loss and high recurrence rates. The pathophysiological mechanisms of RAP is unclear. Recent histopathologic study and en face optical coherence tomography angiography have furthered our understanding of RAP. Clinical features frequently associated with RAP include bilateral disease, presence of reticular pseudodrusen and pigment epithelial detachments. Indocyanine green angiography is the gold standard diagnostic tool. Recently, more and more accurate optical coherence tomography has improved the acknowledgement of stage and diagnosis of RAP. The treatment efficacy of RAP is highly dependent on the stage. Anti-vascular endothelial growth factor therapy is currently the first line of treatment. Other treatment options including combination of photodynamic therapy with antiangiogenic agent intravitreal injections also achieve a reasonable therapeutic outcome. There remain several important questions such as pathogenesis and treatment regimen, to be answered in future RAP research studies.

Citation： Liu Xiaoxue, Chen Ning. The progress in clinical research of retinal angiomatous proliferation. Chinese Journal of Ocular Fundus Diseases, 2018, 34(3): 303-307. doi: 10.3760/cma.j.issn.1005-1015.2018.03.025 Copy

1.	Chakravarthy U, Wong TY, Fletcher A, et al. Clinical risk factors for age-related macular degeneration: a systematic review and meta-analysis[J]. BMC Ophthalmol, 2010, 10: 31. DOI: 10.1186/1471-2415-10-31.
2.	Li M, Dolz-Marco R, Messinger JD, et al. Clinicopathologic correlation of anti-vascular endothelial growth factor-treated type 3 neovascularization in age-related macular degeneration[J]. Ophthalmology, 2018, 125(2): 276-287. DOI: 10.1016/j.ophtha.2017.08.019.
3.	Rudnicka AR, Jarrar Z, Wormald R, et al. Age and gender variations in age-related macular degeneration prevalence in populations of European ancestry: a meta-analysis[J]. Ophthalmology, 2012, 119(3): 571-580. DOI: 10.1016/j.ophtha.2011.09.027.
4.	Caramoy A, Ristau T, Lechanteur YT, et al. Environmental and genetic risk factors for retinal angiomatous proliferation[J]. Acta Ophthalmol, 2014, 92(8): 745-748. DOI: 10.1111/aos.12437.
5.	Hayashi H, Yamashiro K, Gotoh N, et al. CFH and ARMS2 variations in age-related macular degeneration, polypoidal choroidal vasculopathy, and retinal angiomatous proliferation[J]. Invest Ophthalmol Vis Sci, 2010, 51(11): 5914-5919. DOI: 10.1167/iovs.10-5554.
6.	Jabbarpoor Bonyadi MH, Yaseri M, Bonyadi M, et al. Association of ARMS2/LOC387715 A69S, CFH Y402H, and CFH I62V polymorphisms with retinal angiomatous proliferation compared with typical age-related macular degeneration: a meta-analysis[J]. Int Ophthalmol, 2017, 37(6): 1397-1409. DOI: 10.1007/s10792-016-0413-2.
7.	Viola F, Massacesi A, Orzalesi N, et al. Retinal angiomatous proliferation: natural history and progression of visual loss[J]. Retina, 2009, 29(6): 732-739. DOI: 10.1097/IAE.0b013e3181a395cb.
8.	Gross NE, Aizman A, Brucker A, et al. Nature and risk of neovascularization in the fellow eye of patients with unilateral retinal angiomatous proliferation[J]. Retina, 2005, 25(6): 713-718. DOI: 10.1097/00006982-200509000-00005.
9.	Campa C, Harding SP, Pearce IA, et al. Incidence of neovascularization in the fellow eye of patients with unilateral retinal angiomatous proliferation[J]. Eye (Lond), 2010, 24(10): 1585-1589. DOI: 10.1038/eye.2010.88.
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14.	Freund KB, Ho IV, Barbazetto IA, et al. Type 3 neovascularization: the expanded spectrum of retinal angiomatous proliferation[J]. Retina, 2008, 28(2): 201-211. DOI: 10.1097/IAE.0b013e3181669504.
15.	Skalet AH, Miller AK, Klein ML, et al. Clinicopathologic correlation of retinal angiomatous proliferation treated with ranibizumab[J]. Retina, 2017, 37(8): 1620-1624. DOI: 10.1097/IAE.0000000000001672.
16.	Ravera V, Bottoni F, Giani A, et al. Retinal angiomatous proliferation diagnosis: a multiimaging approach[J]. Retina, 2016, 36(12): 2274-2281. DOI: 10.1097/IAE.0000000000001152.
17.	Rofagha S, Bhisitkul RB, Boyer DS, et al. Seven-year outcomes in ranibizumab-treated patients in ANCHOR, MARINA, and HORIZON[J]. Ophthalmology, 2013, 120(11): 2292-2299. DOI: 10.1016/j.ophtha.2013.03.046.
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19.	Su D, Lin S, Phasukkijwatana N, et al. An updated staging system of type 3 neovascularization using spectral domain optical coherence tomography[J]. Retina, 2016, 36 Suppl 1: S40-49. DOI: 10.1097/IAE.0000000000001268.
20.	Amarakoon S, de Jong JH, Braaf B, et al. Phase-resolved doppler optical coherence tomographic features in retinal angiomatous proliferation[J]. Am J Ophthalmol, 2015, 160(5): 1044-1054. DOI: 10.1016/j.ajo.2015.07.026.
21.	Yannuzzi LA, Freund KB, Takahashi BS. Review of retinal angiomatous proliferation or type 3 neovascularization[J]. Retina, 2008, 28(3): 375-384. DOI: 10.1097/IAE.0b013e3181619c55.
22.	徐海峰, 徐怡婷, 白曜, 等.视网膜血管瘤样增生的眼底影像检查特征[J]. 中华眼底病杂志, 2012, 28(4): 401-403. DOI: 10.3760/cma.j.issn.1005-1015.2012.04.022.Xu HF, Xu YT, Bai Y, et al. Fundus imaging features of retinal angiomatous proliferation[J]. Chin J Ocul Fundus Dis, 2012, 28(4): 401-403. DOI: 10.3760/cma.j.issn.1005-1015.2012.04.022.
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24.	杨丽红, 王光璐, 田蓓, 等.视网膜血管瘤样增生的眼底影像特征[J]. 中华眼底病杂志, 2011, 27(6): 584-586. DOI: 10.3760/cma.j.issn.1005-1015.2011.06.020.Yang LH, Wang GL, Tian B, et al. Fundus imaging features of retinal angiomatous proliferation[J]. Chin J Ocul Fundus Dis, 2011, 27(6): 584-586. DOI: 10.3760/cma.j.issn.1005-1015.2011.06.020.
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27.	Kim YK, Park SJ, Woo SJ, et al. Choroidal thickness change after intravitreal anti-vascular endothelial growth factor treatment in retinal angiomatous proliferation and its recurrence[J]. Retina, 2016, 36(8): 1516-1526. DOI: 10.1097/IAE.0000000000000952.
28.	Tan ACS, Dansingani KK, Yannuzzi LA, et al. Type 3 neovascularization imaged with cross-sectional and en face optical coherence tomography angiography[J]. Retina, 2017, 37(2): 234-246. DOI: 10.1097/IAE.0000000000001343.
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33.	Kim JM, Kim JH, Chang YS, et al. Treatment of bilateral retinal angiomatous proliferation with anti-vascular endothelial growth factor: 12-month outcome[J]. Korean J Ophthalmol, 2017, 31(3): 240-248. DOI: 10.3341/kjo.2016.0026.
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35.	王怀华, 王敏, 徐楠楠, 等.玻璃体腔注射雷珠单抗治疗视网膜血管瘤样增生疗效观察[J]. 中华眼底病杂志, 2014, 30(5): 466-469. DOI: 10.3760/cma.j.issn.1005-1015.2014.05.009.Wang HH, Wang M, Xu LL, et al. Effect observation of intravitreal injection of ranibizumab for retinal angiomatous proliferation[J]. Chin J Ocul Fundus Dis, 2014, 30(5): 466-469. DOI: 10.3760/cma.j.issn.1005-1015.2014.05.009.
36.	Gharbiya M, Parisi F, Cruciani F, et al. Intravitreal anti-vascular endothelial growth factor for retinal angiomatous proliferation in treatment-naive eyes: long-term functional and anatomical results using a modified PrONTO-style regimen[J]. Retina, 2014, 34(2): 298-305. DOI: 10.1097/IAE.0b013e3182979e62.
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1. Chakravarthy U, Wong TY, Fletcher A, et al. Clinical risk factors for age-related macular degeneration: a systematic review and meta-analysis[J]. BMC Ophthalmol, 2010, 10: 31. DOI: 10.1186/1471-2415-10-31.
2. Li M, Dolz-Marco R, Messinger JD, et al. Clinicopathologic correlation of anti-vascular endothelial growth factor-treated type 3 neovascularization in age-related macular degeneration[J]. Ophthalmology, 2018, 125(2): 276-287. DOI: 10.1016/j.ophtha.2017.08.019.
3. Rudnicka AR, Jarrar Z, Wormald R, et al. Age and gender variations in age-related macular degeneration prevalence in populations of European ancestry: a meta-analysis[J]. Ophthalmology, 2012, 119(3): 571-580. DOI: 10.1016/j.ophtha.2011.09.027.
4. Caramoy A, Ristau T, Lechanteur YT, et al. Environmental and genetic risk factors for retinal angiomatous proliferation[J]. Acta Ophthalmol, 2014, 92(8): 745-748. DOI: 10.1111/aos.12437.
5. Hayashi H, Yamashiro K, Gotoh N, et al. CFH and ARMS2 variations in age-related macular degeneration, polypoidal choroidal vasculopathy, and retinal angiomatous proliferation[J]. Invest Ophthalmol Vis Sci, 2010, 51(11): 5914-5919. DOI: 10.1167/iovs.10-5554.
6. Jabbarpoor Bonyadi MH, Yaseri M, Bonyadi M, et al. Association of ARMS2/LOC387715 A69S, CFH Y402H, and CFH I62V polymorphisms with retinal angiomatous proliferation compared with typical age-related macular degeneration: a meta-analysis[J]. Int Ophthalmol, 2017, 37(6): 1397-1409. DOI: 10.1007/s10792-016-0413-2.
7. Viola F, Massacesi A, Orzalesi N, et al. Retinal angiomatous proliferation: natural history and progression of visual loss[J]. Retina, 2009, 29(6): 732-739. DOI: 10.1097/IAE.0b013e3181a395cb.
8. Gross NE, Aizman A, Brucker A, et al. Nature and risk of neovascularization in the fellow eye of patients with unilateral retinal angiomatous proliferation[J]. Retina, 2005, 25(6): 713-718. DOI: 10.1097/00006982-200509000-00005.
9. Campa C, Harding SP, Pearce IA, et al. Incidence of neovascularization in the fellow eye of patients with unilateral retinal angiomatous proliferation[J]. Eye (Lond), 2010, 24(10): 1585-1589. DOI: 10.1038/eye.2010.88.
10. Mcbain VA, Kumari R, Townend J, et al. Geographic atrophy in retinal angiomatous proliferation[J]. Retina, 2011, 31(6): 1043-1052. DOI: 10.1097/IAE.0b013e3181fe54c7.
11. Tsai ASH, Cheung N, Gan ATL, et al. Retinal angiomatous proliferation[J]. Surv Ophthalmol, 2017, 62(4): 462-492. DOI: 10.1016/j.survophthal.2017.01.008.
12. Yannuzzi LA, Negrao S, Iida T, et al. Retinal angiomatous proliferation in age-related macular degeneration[J]. Retina, 2001, 21(5): 416-434. DOI: 10.1097/00006982-200110000-00003.
13. Gass JD, Agarwal A, Lavina AM, et al. Focal inner retinal hemorrhages in patients with drusen: an early sign of occult choroidal neovascularization and chorioretinal anastomosis[J]. Retina, 2003, 23(6): 741-751. DOI: 10.1097/00006982-200312000-00001.
14. Freund KB, Ho IV, Barbazetto IA, et al. Type 3 neovascularization: the expanded spectrum of retinal angiomatous proliferation[J]. Retina, 2008, 28(2): 201-211. DOI: 10.1097/IAE.0b013e3181669504.
15. Skalet AH, Miller AK, Klein ML, et al. Clinicopathologic correlation of retinal angiomatous proliferation treated with ranibizumab[J]. Retina, 2017, 37(8): 1620-1624. DOI: 10.1097/IAE.0000000000001672.
16. Ravera V, Bottoni F, Giani A, et al. Retinal angiomatous proliferation diagnosis: a multiimaging approach[J]. Retina, 2016, 36(12): 2274-2281. DOI: 10.1097/IAE.0000000000001152.
17. Rofagha S, Bhisitkul RB, Boyer DS, et al. Seven-year outcomes in ranibizumab-treated patients in ANCHOR, MARINA, and HORIZON[J]. Ophthalmology, 2013, 120(11): 2292-2299. DOI: 10.1016/j.ophtha.2013.03.046.
18. 杨帆, 窦宏亮.视网膜血管瘤样增生的研究概况[J]. 国外医学眼科学分册, 2005, 29(4): 252-255. DOI: 10.3760/cma.j.issn.1673-5803.2005.04.011.Yang F, Dou HL. Review of retinal angiomatous proliferation[J]. Int Rev Ophthalmol, 2005, 29(4): 252-255. DOI: 10.3760/cma.j.issn.1673-5803.2005.04.011.
19. Su D, Lin S, Phasukkijwatana N, et al. An updated staging system of type 3 neovascularization using spectral domain optical coherence tomography[J]. Retina, 2016, 36 Suppl 1: S40-49. DOI: 10.1097/IAE.0000000000001268.
20. Amarakoon S, de Jong JH, Braaf B, et al. Phase-resolved doppler optical coherence tomographic features in retinal angiomatous proliferation[J]. Am J Ophthalmol, 2015, 160(5): 1044-1054. DOI: 10.1016/j.ajo.2015.07.026.
21. Yannuzzi LA, Freund KB, Takahashi BS. Review of retinal angiomatous proliferation or type 3 neovascularization[J]. Retina, 2008, 28(3): 375-384. DOI: 10.1097/IAE.0b013e3181619c55.
22. 徐海峰, 徐怡婷, 白曜, 等.视网膜血管瘤样增生的眼底影像检查特征[J]. 中华眼底病杂志, 2012, 28(4): 401-403. DOI: 10.3760/cma.j.issn.1005-1015.2012.04.022.Xu HF, Xu YT, Bai Y, et al. Fundus imaging features of retinal angiomatous proliferation[J]. Chin J Ocul Fundus Dis, 2012, 28(4): 401-403. DOI: 10.3760/cma.j.issn.1005-1015.2012.04.022.
23. Rouvas AA, Papakostas TD, Ntouraki A, et al. Angiographic and OCT features of retinal angiomatous proliferation[J]. Eye (Lond), 2010, 24(11): 1633-1642. DOI: 10.1038/eye.2010.134.
24. 杨丽红, 王光璐, 田蓓, 等.视网膜血管瘤样增生的眼底影像特征[J]. 中华眼底病杂志, 2011, 27(6): 584-586. DOI: 10.3760/cma.j.issn.1005-1015.2011.06.020.Yang LH, Wang GL, Tian B, et al. Fundus imaging features of retinal angiomatous proliferation[J]. Chin J Ocul Fundus Dis, 2011, 27(6): 584-586. DOI: 10.3760/cma.j.issn.1005-1015.2011.06.020.
25. Scott AW, Bressler SB. Retinal angiomatous proliferation or retinal anastomosis to the lesion[J]. Eye (Lond), 2010, 24(3): 491-496. DOI: 10.1038/eye.2009.311.
26. Lim EH, Han JI, Kim CG, et al. Characteristic findings of optical coherence tomography in retinal angiomatous proliferation[J]. Korean J Ophthalmol, 2013, 27(5): 351-360. DOI: 10.3341/kjo.2013.27.5.351.
27. Kim YK, Park SJ, Woo SJ, et al. Choroidal thickness change after intravitreal anti-vascular endothelial growth factor treatment in retinal angiomatous proliferation and its recurrence[J]. Retina, 2016, 36(8): 1516-1526. DOI: 10.1097/IAE.0000000000000952.
28. Tan ACS, Dansingani KK, Yannuzzi LA, et al. Type 3 neovascularization imaged with cross-sectional and en face optical coherence tomography angiography[J]. Retina, 2017, 37(2): 234-246. DOI: 10.1097/IAE.0000000000001343.
29. Dansingani KK, Naysan J, Freund KB. En face OCT angiography demonstrates flow in early type 3 neovascularization (retinal angiomatous proliferation)[J]. Eye (Lond), 2015, 29(5): 703-706. DOI: 10.1038/eye.2015.27.
30. Miere A, Querques G, Semoun O, et al. Optical coherence tomography angiography changes in early type 3 neovascularization after anti-vascular endothelial growth factor treatment[J]. Retina, 2017, 37(10): 1873-1879. DOI: 10.1097/IAE.0000000000001447.
31. Haq A, Kapoor B, Logendran M, et al. Successful treatment of retinal angiomatous proliferation with intravitreal triamcinolone and ranibizumab injections in a 67-year-old male[J]. Opthalmology, 2014, 5(3): 392-399. DOI: 10.1159/000369611.
32. Donati G, Pournaras CJ. Ranibizumab treatment for retinal angiomatous proliferation lesions: a case report with life-long expectancy (seven years) follow-up[J]. Klin Monbl Augenheilkd, 2015, 232(4): 570-572. DOI: 10.1055/s-0034-1396332.
33. Kim JM, Kim JH, Chang YS, et al. Treatment of bilateral retinal angiomatous proliferation with anti-vascular endothelial growth factor: 12-month outcome[J]. Korean J Ophthalmol, 2017, 31(3): 240-248. DOI: 10.3341/kjo.2016.0026.
34. Cho HJ, Lee TG, Han SY, et al. Long-term visual outcome and prognostic factors of Intravitreal anti-vascular endothelial growth factor treatment for retinal angiomatous proliferation[J]. Graefe's Arch Clin Exp Ophthalmol, 2016, 254(1): 23-30. DOI: 10.1007/s00417-015-2993-3.
35. 王怀华, 王敏, 徐楠楠, 等.玻璃体腔注射雷珠单抗治疗视网膜血管瘤样增生疗效观察[J]. 中华眼底病杂志, 2014, 30(5): 466-469. DOI: 10.3760/cma.j.issn.1005-1015.2014.05.009.Wang HH, Wang M, Xu LL, et al. Effect observation of intravitreal injection of ranibizumab for retinal angiomatous proliferation[J]. Chin J Ocul Fundus Dis, 2014, 30(5): 466-469. DOI: 10.3760/cma.j.issn.1005-1015.2014.05.009.
36. Gharbiya M, Parisi F, Cruciani F, et al. Intravitreal anti-vascular endothelial growth factor for retinal angiomatous proliferation in treatment-naive eyes: long-term functional and anatomical results using a modified PrONTO-style regimen[J]. Retina, 2014, 34(2): 298-305. DOI: 10.1097/IAE.0b013e3182979e62.
37. Hufendiek K, Hufendiek K, Panagakis G, et al. Visual and morphological outcomes of bevacizumab (Avastin(R)) versus ranibizumab (Lucentis(R)) treatment for retinal angiomatous proliferation[J]. Int Ophthalmol, 2012, 32(3): 259-268. DOI: 10.1007/s10792-012-9562-0.
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