Morphological and functional retinal changes in postoperative hypotony
DOI: 10.32364/2311-7729-2021-21-4-187-193
V.P. Erichev, A.A. Antonov, A.A. Vitkov, E.A. Ragozina, A.V. Volzhanin
Scientific Research Institute of Eye Diseases, Moscow, Russian Federation
Aim: to analyze the retinal microvascular network changes in hypotony maculopathy after non-penetrating deep sclerectomy (NPDS).
Patients and Methods: the study enrolled 35 patients (35 eyes) with uncontrolled glaucoma stages II and III in whom the intraocular pressure (IOP) level was less than 10 mm Hg after NPDS. In addition to a standard eye exam, all patients underwent optical coherence tomography angiography (OCTA) before and one day after surgery. In addition, the radial peripapillary capillary (RPC) network vessel density (VD) on 4×4-mm optic nerve scans, superficial vascular plexus (SVP) VD on 6×6-mm macular scans, and foveal avascular zone (FAZ) area on 3×3-mm scans were evaluated.
Results: IOP-lowering effect was reported in all patients, i.e., IOP level reduced by, on average, 17.7±8.3 mm Hg. In 15 patients, baseline OCTA parameters worsened (group 1). In 17 patients, OCTA parameters improved (group 2). In 3 patients, OCTA parameters remained unchanged (group 3). In group 1, parafoveal VD reduced by 1.5% [2.45%; 0.85%] in the superior sector and 1.3% [1.75%; 0.85%] in the inferior sector. Peripapillary VD reduced by 0.6% [2.0%; 0.1%] in the superior sector and 1.1% [2.4%; 0.0%] in the inferior sector. In group 2, parafoveal VD improved by 0.85% [0.0%; 1.75%] in the superior sector and 1.2% [0.68%; 2.6%] in the inferior sector. Peripapillary VD improved by 1.2% [0.18%; 2.0%] in the superior sector and 0.95% [0.05%; 1.75%] in the inferior sector. IOP levels were similar. No correlations between OCTA parameters and IOP levels were revealed. Postoperatively, the FAZ area remained unchanged.
Conclusions: postoperative hypotoni a has a positive and negative impact on the retinal microvascular network. OCTA findings after NPDS demonstrate no correlations with IOP levels. Further studies are needed to identify prognostic factors of hypotony maculopathy and assess its long-term effects on retinal vessels.
Keywords: glaucoma, non-penetrating deep sclerectomy, hypotony maculopathy, OCTA.
For citation: Erichev V.P., Antonov A.A., Vitkov A.A. et al. Morphological and functional retinal changes in postoperative hypotony. Russian Journal of Clinical Ophthalmology. 2021;21(4):187–193 (in Russ.). DOI: 10.32364/2311-7729-2021-21-4-187-193.
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18. Goodkin M.L., Grewal D.S., Greenfield D.S. Three-dimensional high-speed optical coherence tomography for diagnosis of hypotony maculopathy after glaucoma filtration surgery. J Glaucoma. 2010;19(6):349–355. DOI: 10.1097/IJG.0b013e3181bd59c.
19. Trible J.R., Sergott R.C., Spaeth G.L. et al. Trabeculectomy is associated with retrobulbar hemodynamic changes. A color Doppler analysis. Ophthalmology. 1994;101(2):340–351. DOI: 10.1016/s0161-6420(13)31332-3.
20. Wang X., Jiang C., Ko T. et al. Correlation between optic disc perfusion and glaucomatous severity in patients with open-angle glaucoma: an optical coherence tomography angiography study. Graefes Arch Clin Exp Ophthalmol. 2015;253(9):1557–1564. DOI: 10.1007/s00417-015-3095-y.
21. Rao H.L., Pradhan Z.S., Weinreb R.N. et al. Regional Comparisons of Optical Coherence Tomography Angiography Vessel Density in Primary Open-Angle Glaucoma. Am J Ophthalmol. 2016;171:75–83. DOI: 10.1016/j.ajo.2016.08.030.
22. Patel N., McAllister F., Pardon L., Harwerth R. The effects of graded intraocular pressure challenge on the optic nerve head. Exp Eye Res. 2018;169:79–90. DOI: 10.1016/j.exer.2018.01.02.
23. Holló G. Influence of large intraocular pressure reduction on peripapillary OCT vessel density in ocular hypertensive and glaucoma eyes. J Glaucoma. 2017;26(1):e7–e10. DOI: 10.1097/IJG.0000000000000527.
24. Юрьева Т.Н., Жукова С.И. ОКТ-ангиография в комплексной оценке эффективности гипотензивной терапии у больных с первичной открытоугольной глаукомой. Российский офтальмологический журнал. 2019;12(3):43–49. DOI: 10.21516/2072-0076-2019-12-3-43-49. [Yurieva T.N., Zhukova S.I. OCT angiography in a comprehensive assessment of hypotensive therapy effectiveness in patients with primary open-angle glaucoma. Russian Ophthalmological Journal. 2019;12(3):43–49 (in Russ.)]. DOI: 10.21516/2072-0076-2019-12-3-43-49.
25. Chihara E., Dimitrova G., Chihara T. Increase in the OCT angiograph- ic peripapillary vessel density by ROCK inhibitor ripasudil instillation: a comparison with brimonidine. Graefes Arch Clin Exp Ophthalmol. 2018;256(7):1257–1264. DOI: 10.1007/s00417-018-3945-5.
26. Lommatzsch C., Rothaus K., Koch J.M. et al. Retinal perfusion 6 months after trabeculectomy as measured by optical coherence tomography angiography. Int Ophthalmol. 2019;39(11):2583–2594. DOI: 10.1007/s10792-019-01107-7.
27. Zéboulon P., Lévêque P.M., Brasnu E. et al. Effect of surgical intraocular pressure lowering on peripapillary and macular vessel density in glaucoma patients: an optical coherence tomography angiography study. J Glaucoma. 2017;26(5):466–472. DOI: 10.1097/ IJG.0000000000000652.
28. Ch’ng T.W., Gillmann K., Hoskens K. et al. Effect of surgical intraocular pressure lowering on retinal structures — nerve fibre layer, foveal avascular zone, peripapillary and macular vessel density: 1 year results. Eye (Lond). 2020;34(3):562–571. DOI: 10.1038/s41433-019-0560-6.
29. Shin J.W., Sung K.R., Uhm K.B. et al. Peripapillary microvascular improvement and lamina cribrosa depth reduction after trabeculectomy in primary open-angle glaucoma. Invest Ophthalmol Vis Sci. 2017;58(13):5993–5999. DOI: 10.1167/iovs.17-22787.
30. Kim J.A., Kim T.W., Lee E.J. et al. Microvascular changes in peripapillary and optic nerve head tissues after trabeculectomy in primary open-angle glaucoma. Invest Ophthalmol Vis Sci. 2018;59(11):4614–4621. DOI: 10.1167/iovs.18-25038.
31. Юрьева Т.Н., Жукова С.И., Помкина И.В. Хориодальный кровоток у больных с глаукомой в условиях офтальмогипертензии и компенсированного внутриглазного давления. Сибирский научный медицинский журнал. 2020;40(4):91–97. DOI: 10.15372/SSMJ20200413. [Yurieva T.N., Zhukova S.I., Pomkina I.V. Choroidal blood flow in glaucoma patients in conditions of ophthalmic hypertension and compensated intraocular pressure. Siberian Scientific Medical Journal. 2020;40(4):91–97 (in Russ.)]. DOI: 10.15372/SSMJ20200413.
32. Jonas J.B., Schneider U., Naumann G.O. Count and density of human retinal photoreceptors. Graefes Arch Clin Exp Ophthalmol. 1992;230(6):505–510. DOI: 10.1007/BF00181769.
33. Ghassemi F., Mirshahi R., Bazvand F. et al. The quantitative measurements of foveal avascular zone using optical coherence tomography angiography in normal volunteers. J Curr Ophthalmol. 2017;29(4):293–299. DOI: 10.1016/j.joco.2017.06.004.
34. Tan P.E., Balaratnasingam C., Xu J. et al. Quantitative Comparison of Retinal Capillary Images Derived By Speckle Variance Optical Coherence Tomography With Histology. Invest Ophthalmol Vis Sci. 2015;56(6):3989–3996. DOI: 10.1167/iovs.14-15879.
35. Noscas F., Sellam A., Glacet-Bernard A. et al. Normative Data for Vascular Density in Superficial and Deep Capillary Plexuses of Healthy Adults Assessed by Optical Coherence Tomography Angiography. Invest Ophthalmol Vis Sci. 2016;57(9):OCT211–223. DOI: 10.1167/iovs.15-18793.
36. Zivkovic M., Dayanir V., Kocaturk T. et al. Foveal Avascular Zone in Normal Tension Glaucoma Measured by Optical Coherence Tomography Angiography. Biomed Res Int. 2017;2017:3079141. DOI: 10.1155/2017/3079141.
37. Kwon J., Choi J., Shin J.W. et al. Alterations of the Foveal Avascular Zone Measured by Optical Coherence Tomography Angiography in Glaucoma Patients With Central Visual Field Defects. Invest Ophthalmol Vis Sci. 2017;58(3):1637–1645. DOI: 10.1167/iovs.16-21079.
38. Heickell A.G., Bellezza A.J., Thompson H.W., Burgoyne C.F. Optic disc surface compliance testing using confocal scanning laser tomography in the normal monkey eye. J Glaucoma. 2001;10(5):369–382. DOI: 10.1097/00061198-200110000-00002.
39. Lesk M.R., Spaeth G.L., Azuara-Blanco A. et al. Reversal of optic disc cupping after glaucoma surgery analyzed with a scanning laser tomograph. Ophthalmology. 1999;106(5):1013–1018. DOI: 10.1016/S0161-6420(99)00526-6.
40. Lim H.B., Kim Y.W., Kim J.M. et al. The Importance of Signal Strength in Quantitative Assessment of Retinal Vessel Density Using Optical Coherence Tomography Angiography. 2018;8:12897. DOI: 10.1038/s41598-018-31321-9.
2. Tham Y.C., Li X., Wong T.Y. et al. Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology. 2014;121(11):2081–2090. DOI: 10.1016/j.ophtha.2014.05.013.
3. Schubert H.D. Postsurgical hypotony: relationship to fistulization, inflammation, chorioretinal lesions, and the vitreous. Surv Ophthalmol. 1996;41(2):97–125. DOI: 10.1016/s0039-6257(96)80001-4.
4. Pederson J.E. Ocular hypotony. Trans Ophthalmol Soc U K. 1986;105(2):220–226.
5. Nuyts R.M., Greve E.L., Geijssen H.C., Langerhorst C.T. Treatment of hypotonous maculopathy after trabeculectomy with mitomycin C. Am J Ophthalmol. 1994;118(3):322–331. DOI: 10.1016/s0002-9394(14)72956-3.
6. Fannin L.A., Schiffman J.C., Budenz D.L. Risk factors for hypotony maculopathy. Ophthalmology. 2003;110(6):1185–1191. DOI: 10.1016/S0161-6420(03)00227-6.
7. Tseng V.L., Kim C.H., Romero P.T. et al. Risk Factors and Long-Term Outcomes in Patients with Low Intraocular Pressure after Trabeculectomy. Ophthalmology. 2017;124(10):1457–1465. DOI: 10.1016/j.ophtha.2017.05.014.
8. Saeedi O.J., Jefferys J.L., Solus J.F. et al. Risk factors for adverse consequences of low intraocular pressure after trabeculectomy. J Glaucoma. 2014;23(1):e60–68. DOI: 10.1097/IJG.0000000000000008.
9. Suner I.J., Greenfield D.S., Miller M.P. et al. Hypotony maculopathy after filtering surgery with mitomycin C. Incidence and treatment. Ophthalmology. 1997;104(2):207–214; discussion 214–205. DOI: 10.1016/s0161-6420(97)30332-7.
10. Costa V.P., Wilson R.P., Moster M.R. et al. Hypotony maculopathy following the use of topical mitomycin C in glaucoma filtration surgery. Ophthalmic Surg. 1993;24(6):389–394.
11. Rasheed el-S. Initial trabeculectomy with intraoperative mitomycin-C application in primary glaucomas. Ophthalmic Surg Lasers. 1999;30(5):360–366.
12. Dellaporta A. Fundus changes in postoperative hypotony. Am J Ophthalmol. 1955;40(6):781–785. DOI: 10.1016/0002-9394(55)91105-3.
13. Еричев В.П., Петров С.Ю., Орехова Н.А., Эльмурзаева Л.Х. Гипотоническая макулопатия после глаукомной хирургии: механизмы развития, методы профилактики и терапии. РМЖ. Клиническая офтальмология. 2020;20(1):26–31. DOI: 10.32364/2311-7729-2020-20-1-26-31. [Erichev V.P., Petrov S.Yu., Orekhova N.A., El’murzaeva L.Kh. Hypotony maculopathy after glaucoma surgery: pathogenic mechanisms, diagnostic tools, and treatment modalites. RMJ Clinical Ophthalmology. 2020;20(1):26–31 (in Russ.)]. DOI: 10.32364/2311-7729-2020-20-1-26-31.
14. Azuma K., Saito H., Takao M., Araie M. Frequency of hypotonic maculopathy observed by spectral domain optical coherence tomography in post glaucoma filtration surgery eyes. Am J Ophthalmol Case Rep. 2020;19:100786. DOI: 10.1016/j.ajoc.2020.100786.
15. Budenz D.L., Schwartz K., Gedde S.J. Occult hypotony maculopathy diagnosed with optical coherence tomography. Arch Ophthalmol. 2005;123(1):113–114. DOI: 10.1001/archopht.123.1.113.
16. Klink T., Lieb W.E., Göbel W. Early and late findings with optical coherence tomography (OCT) in patients with postoperative hypotonia. Ophthalmologe. 2000;97(5):353–358. DOI: 10.1007/s003470050536.
17. Lima V.C., Prata T.S., Castro D.P. et al. Macular changes detected by Fourier-domain optical coherence tomography in patients with hypotony without clinical maculopathy. Acta Ophthalmol. 2011;89(3):e274–277. DOI: 10.1111/j.1755-3768.2009.01719.x.
18. Goodkin M.L., Grewal D.S., Greenfield D.S. Three-dimensional high-speed optical coherence tomography for diagnosis of hypotony maculopathy after glaucoma filtration surgery. J Glaucoma. 2010;19(6):349–355. DOI: 10.1097/IJG.0b013e3181bd59c.
19. Trible J.R., Sergott R.C., Spaeth G.L. et al. Trabeculectomy is associated with retrobulbar hemodynamic changes. A color Doppler analysis. Ophthalmology. 1994;101(2):340–351. DOI: 10.1016/s0161-6420(13)31332-3.
20. Wang X., Jiang C., Ko T. et al. Correlation between optic disc perfusion and glaucomatous severity in patients with open-angle glaucoma: an optical coherence tomography angiography study. Graefes Arch Clin Exp Ophthalmol. 2015;253(9):1557–1564. DOI: 10.1007/s00417-015-3095-y.
21. Rao H.L., Pradhan Z.S., Weinreb R.N. et al. Regional Comparisons of Optical Coherence Tomography Angiography Vessel Density in Primary Open-Angle Glaucoma. Am J Ophthalmol. 2016;171:75–83. DOI: 10.1016/j.ajo.2016.08.030.
22. Patel N., McAllister F., Pardon L., Harwerth R. The effects of graded intraocular pressure challenge on the optic nerve head. Exp Eye Res. 2018;169:79–90. DOI: 10.1016/j.exer.2018.01.02.
23. Holló G. Influence of large intraocular pressure reduction on peripapillary OCT vessel density in ocular hypertensive and glaucoma eyes. J Glaucoma. 2017;26(1):e7–e10. DOI: 10.1097/IJG.0000000000000527.
24. Юрьева Т.Н., Жукова С.И. ОКТ-ангиография в комплексной оценке эффективности гипотензивной терапии у больных с первичной открытоугольной глаукомой. Российский офтальмологический журнал. 2019;12(3):43–49. DOI: 10.21516/2072-0076-2019-12-3-43-49. [Yurieva T.N., Zhukova S.I. OCT angiography in a comprehensive assessment of hypotensive therapy effectiveness in patients with primary open-angle glaucoma. Russian Ophthalmological Journal. 2019;12(3):43–49 (in Russ.)]. DOI: 10.21516/2072-0076-2019-12-3-43-49.
25. Chihara E., Dimitrova G., Chihara T. Increase in the OCT angiograph- ic peripapillary vessel density by ROCK inhibitor ripasudil instillation: a comparison with brimonidine. Graefes Arch Clin Exp Ophthalmol. 2018;256(7):1257–1264. DOI: 10.1007/s00417-018-3945-5.
26. Lommatzsch C., Rothaus K., Koch J.M. et al. Retinal perfusion 6 months after trabeculectomy as measured by optical coherence tomography angiography. Int Ophthalmol. 2019;39(11):2583–2594. DOI: 10.1007/s10792-019-01107-7.
27. Zéboulon P., Lévêque P.M., Brasnu E. et al. Effect of surgical intraocular pressure lowering on peripapillary and macular vessel density in glaucoma patients: an optical coherence tomography angiography study. J Glaucoma. 2017;26(5):466–472. DOI: 10.1097/ IJG.0000000000000652.
28. Ch’ng T.W., Gillmann K., Hoskens K. et al. Effect of surgical intraocular pressure lowering on retinal structures — nerve fibre layer, foveal avascular zone, peripapillary and macular vessel density: 1 year results. Eye (Lond). 2020;34(3):562–571. DOI: 10.1038/s41433-019-0560-6.
29. Shin J.W., Sung K.R., Uhm K.B. et al. Peripapillary microvascular improvement and lamina cribrosa depth reduction after trabeculectomy in primary open-angle glaucoma. Invest Ophthalmol Vis Sci. 2017;58(13):5993–5999. DOI: 10.1167/iovs.17-22787.
30. Kim J.A., Kim T.W., Lee E.J. et al. Microvascular changes in peripapillary and optic nerve head tissues after trabeculectomy in primary open-angle glaucoma. Invest Ophthalmol Vis Sci. 2018;59(11):4614–4621. DOI: 10.1167/iovs.18-25038.
31. Юрьева Т.Н., Жукова С.И., Помкина И.В. Хориодальный кровоток у больных с глаукомой в условиях офтальмогипертензии и компенсированного внутриглазного давления. Сибирский научный медицинский журнал. 2020;40(4):91–97. DOI: 10.15372/SSMJ20200413. [Yurieva T.N., Zhukova S.I., Pomkina I.V. Choroidal blood flow in glaucoma patients in conditions of ophthalmic hypertension and compensated intraocular pressure. Siberian Scientific Medical Journal. 2020;40(4):91–97 (in Russ.)]. DOI: 10.15372/SSMJ20200413.
32. Jonas J.B., Schneider U., Naumann G.O. Count and density of human retinal photoreceptors. Graefes Arch Clin Exp Ophthalmol. 1992;230(6):505–510. DOI: 10.1007/BF00181769.
33. Ghassemi F., Mirshahi R., Bazvand F. et al. The quantitative measurements of foveal avascular zone using optical coherence tomography angiography in normal volunteers. J Curr Ophthalmol. 2017;29(4):293–299. DOI: 10.1016/j.joco.2017.06.004.
34. Tan P.E., Balaratnasingam C., Xu J. et al. Quantitative Comparison of Retinal Capillary Images Derived By Speckle Variance Optical Coherence Tomography With Histology. Invest Ophthalmol Vis Sci. 2015;56(6):3989–3996. DOI: 10.1167/iovs.14-15879.
35. Noscas F., Sellam A., Glacet-Bernard A. et al. Normative Data for Vascular Density in Superficial and Deep Capillary Plexuses of Healthy Adults Assessed by Optical Coherence Tomography Angiography. Invest Ophthalmol Vis Sci. 2016;57(9):OCT211–223. DOI: 10.1167/iovs.15-18793.
36. Zivkovic M., Dayanir V., Kocaturk T. et al. Foveal Avascular Zone in Normal Tension Glaucoma Measured by Optical Coherence Tomography Angiography. Biomed Res Int. 2017;2017:3079141. DOI: 10.1155/2017/3079141.
37. Kwon J., Choi J., Shin J.W. et al. Alterations of the Foveal Avascular Zone Measured by Optical Coherence Tomography Angiography in Glaucoma Patients With Central Visual Field Defects. Invest Ophthalmol Vis Sci. 2017;58(3):1637–1645. DOI: 10.1167/iovs.16-21079.
38. Heickell A.G., Bellezza A.J., Thompson H.W., Burgoyne C.F. Optic disc surface compliance testing using confocal scanning laser tomography in the normal monkey eye. J Glaucoma. 2001;10(5):369–382. DOI: 10.1097/00061198-200110000-00002.
39. Lesk M.R., Spaeth G.L., Azuara-Blanco A. et al. Reversal of optic disc cupping after glaucoma surgery analyzed with a scanning laser tomograph. Ophthalmology. 1999;106(5):1013–1018. DOI: 10.1016/S0161-6420(99)00526-6.
40. Lim H.B., Kim Y.W., Kim J.M. et al. The Importance of Signal Strength in Quantitative Assessment of Retinal Vessel Density Using Optical Coherence Tomography Angiography. 2018;8:12897. DOI: 10.1038/s41598-018-31321-9.
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