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Офтальмохирургия. 2021; : 30-38

Оптическая когерентная томография-ангиография в исследовании ретинального кровотока у беременных с сахарным диабетом

Помыткина Н. В., Сорокин Е. Л., Пашенцев Я. Е.

https://doi.org/10.25276/0235-4160-2021-1-30-38

Аннотация

Цель. Исследовать ретинальный кровоток у беременных с сахарным диабетом (СД) с помощью оптической когерентной томографии- ангиографии (ОКТ-А).

Материал и методы. Обследованы 60 беременных: 24 женщины с СД 1-го и 2-го типа (СД1 и СД2) и 36 здоровых женщин с физиологическим течением беременности, составивших группу контроля. Беременные с СД обследовались в трех триместрах, группы контроля – в III триместре. Проводилась ОКТ-А (RTVue XR Avanti, Optovue, США) с протоколом HD Angio Retina 6,0 мм. Исследовались общая плотность сосудов (ОПС), фовеальная плотность сосудов (ФПС), площадь фовеальной аваскулярной зоны (ПФАЗ) в поверхностном сосудистом сплетении.

Результаты. В III триместре ФПС у беременных с СД была значимо меньше, чем в группе контроля, при отсутствии различий ОПС и ПФАЗ. ОПС была значимо меньше, а ПФАЗ значимо больше у беременных с диабетической ретинопатией (ДР), чем у беременных с СД без ДР. Значимых различий значений параметров кровотока в группах беременных с СД, вне зависимости от проведения им лазеркоагуляции сетчатки, выявлено не было. При анализе значений ОПС, ФПС и ПФАЗ у беременных с СД в разных триместрах беременности статистически значимых различий не отмечалось.

У 11 беременных с ДР выявлены зоны ретинальной неперфузии, которые у 6 пациенток на протяжении беременности имели тенденцию к расширению. У 2 пациенток с СД1 без ДР в III триместре выявлены зоны неперфузии.

Заключение. Полученные данные имеют практическое значение для диагностики манифестации ДР во время беременности. ОКТ-А является ценным диагностическим методом, позволяющим неинвазивно диагностировать наличие зон ретинальной неперфузии при отсутствии офтальмоскопических признаков ДР у беременных с СД, а так- же оценивать состояние зон ретинальной неперфузии на протяжении беременности у пациенток с ДР.

Список литературы

1. IDF Diabetes Atlas. 6th ed. International Diabetes Federation. Brussels: International Diabetes Federation; 2014.

2. Bourne RR, Stevens GA, White RA, Smith JL, Flaxman SR, Price H, et al. Vision loss expert group. Causes of vision loss worldwide, 1990–2010: a systematic analysis. Lancet Glob Health. 2013;1(6): e339–349. doi: 10.1016/S2214-109X(13)70113-X

3. Clustering of long-term complications in families with diabetes in the diabetes control and complications trial. The diabetes control and complications trial research group. Diabetes. 1997;46(11): 1829–1839. doi: 10.2337/diab.46.11.1829

4. Egan AM, McVicker L, Heerey A, Carmody L, Harney F, Dunne FP. Diabetic retinopathy in pregnancy: a population-based study of women with pregestational diabetes. J Diabetes Res. 2015;2015: 310239. doi: 10.1155/2015/310239

5. Phelps RL, Sakol P, Metzger BE, Jampol LM, Freinkel N. Changes in diabetic retinopathy during pregnancy. Correlations with regulation of hyperglycemia. Arch Ophthalmol. 1986;104(12): 1806–1810. doi: 10.1001/archopht.1986.01050240080044

6. Arun CS, Taylor R. Influence of pregnancy on long-term progression of retinopathy in patients with type 1 diabetes. Diabetologia. 2008;5(6): 1041–1045. doi: 10.1007/s00125-008-0994-z

7. Chanwimol K, Balasubramanian S, Nassisi M, Gaw SL, Janzen C, Sarraf D, Sadda SR, Tsui I. Retinal vascular changes during pregnancy detected with optical coherence tomography angiography. Invest Ophthalmol Vis Sci. 2019;60(7): 2726–2732. doi: 10.1167/iovs.19-26956

8. Rosenn B, Miodovnik M, Kranias G, Khoury J, Combs CA, Mimouni F, Siddiqi TA, Lipman MJ. Progression of diabetic retinopathy in pregnancy: association with hypertension in pregnancy. Am J Obstet Gynecol. 1992;166(4): 1214–1218. doi: 10.1016/s0002-9378(11)90608-5

9. Hwang TS, Gao SS, Liu L, Lauer AK, Bailey ST, Flaxel CJ, et al. Automated quantification of capillary nonperfusion using optical coherence tomography angiography in diabetic retinopathy. JAMA Ophthalmol. 2016;134(4): 367–373. doi: 10.1001/jamaophthalmol.2015.5658

10. de Carlo TE, Chin AT, Bonini Filho MA, Adhi M, Branchini L, Salz DA, et al. Detection of microvascular changes in eyes of patients with diabetes but not clinical diabetic retinopathy using optical coherence tomography angiography. Retina. 2015;35(11): 2364–2370. doi: 10.1097/IAE.0000000000000882

11. Goudot MM, Sikorav A, Semoun O, Miere A, Jung C, Courbebaisse B, et al. Parafoveal OCT angiography features in diabetic patients without clinical diabetic retinopathy: a qualitative and quantitative analysis. J Ophthalmol. 2017;2017: 8676091. doi: 10.1155/2017/8676091

12. Ishibazawa A, Nagaoka T, Takahashi A, Omae T, Tani T, Sogawa K, et al. Optical coherence tomography angiography in diabetic retinopathy: a prospective pilot study. Am J Ophthalmol. 2015;160(1): 35–44. doi: 10.1016/j.ajo.2015.04.021

13. Spaide RF, Klancnik JM, Cooney MJ. Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol. 2015;133(1): 45–50. doi: 10.1001/jamaophthalmol.2014.3616

14. Pan J, Chen D, Yang X, Zou R, Zhao K, Cheng D, et al. Characteristics of neovascularization in early stages of proliferative diabetic retinopathy by optical coherence tomography angiography. Am J Ophthalmol. 2018;192: 146–156. doi: 10.1016/j.ajo.2018.05.018

15. Фабрикантов О.Л., Проничкина М.М., Яблокова Н.В., Овсянникова Н.В. Инновационные возможности неинвазивной прижизненной оценки состояния сосудов микроциркуляторного ложа при диабетической ретинопатии. Вестник Волгоградского Государственного медицинского университета. 2018;4: 41–45.

16. Takase N, Nozaki M, Kato A, Ozeki H, Yoshida M, Ogura Y. Enlargement of foveal avascular zone in diabetic eyes evaluated by en face optical coherence tomography angiography. Retina. 2015;35(11): 2377–2383. doi: 10.1097/IAE.0000000000000849

17. Agemy SA, Scripsema NK, Shah CM, Chui T, Garcia PM, Lee JG, et al. Retinal vascular perfusion density mapping using optical coherence tomography angiography in normals and diabetic retinopathy patients. Retina. 2015;35(11): 2353–2363. doi: 10.1097/IAE.0000000000000862

18. Salz DA, de Carlo TE, Adhi M, Moult E, Choi W, Baumal CR, et al. Select features of diabetic retinopathy on swept-source optical coherence tomographic angiography compared with fluorescein angiography and normal eyes. JAMA Ophthalmol. 20161;134(6): 644–650. doi: 10.1001/jamaophthalmol.2016.0600

19. Conti FF, Qin VL, Rodrigues EB, Sharma S, Rachitskaya AV, Ehlers JP, Singh RP. Choriocapillaris and retinal vascular plexus density of diabetic eyes using split-spectrum amplitude decorrelation spectraldomain optical coherence tomography angiography. Br J Ophthalmol. 2019;103(4):452–456. doi: 10.1136/

20. bjophthalmol-2018-311903

21. Bresnick GH, Condit R, Syrjala S, Palta M, Groo A, Korth K. Abnormalities of the foveal avascular zone in diabetic retinopathy. Arch Ophthalmol. 1984;102(9): 1286–1293. doi: 10.1001/archopht.1984.01040031036019

22. Бурнашева М.А., Мальцев Д.С., Куликов А.Н. Персонализированная оценка площади фовеальной аваскулярной зоны с помощью оптической когерентной томографии-ангиографии. Современные технологии в офтальмологии. 2017;7: 19–21.

23. Коленко О.В., Сорокин Е.Л., Ходжаев С.Н., Чижова Г.В., Филь А.А., Помыткина Н.В., Пашенцев Я.Е. Состояние показателей ангио-ОКТ макулярной зоны у беременных женщин с преэклампсией во взаимосвязи с содержанием фактора эндотелиальной дисфункции, их значение для прогнозирования сосудистой ретинальной патологии в постродовом периоде. Офтальмохирургия. 2019;3: 63–71.

24. Motulsky E, Zheng F, Liu G, Gregori G, Rosenfeld PJ. Swept-source OCT angiographic imaging of a central retinal vein occlusion during pregnancy. Ophthalmic Surg Lasers Imaging Retina. 2018;49(3): 206–208. doi: 10.3928/23258160-20180221-09

25. Soma-Pillay P, Nelson-Piercy C, Tolppanen H, Mebazaa A. Physiological changes in pregnancy. Cardiovasc J Afr. 2016;27(2): 89–94. doi: 10.5830/CVJA-2016-021

26. Яблокова Н.В., Фабрикантов О.Л. Исследование влияния панретинальной лазеркоагуляции по поводу диабетической ретинопатии на сосудистую систему глаза. Современные технологии в офтальмологии. 2019;6: 157–163.

Fyodorov Journal of Ophthalmic Surgery. 2021; : 30-38

Optical coherence tomography angiography in the study of retinal blood flow in pregnant women with diabetes

Pomytkina N. V., Sorokin E. L., Pashentsev Ya. E.

https://doi.org/10.25276/0235-4160-2021-1-30-38

Abstract

Purpose. To study retinal blood flow in pregnant women with diabetes using optical coherence tomography angiography (OCTA).

Material and methods. 60 pregnant women were examined: 24 women had type 1 and 2 diabetes (T1D and T2D) and 36 healthy women with physiological pregnancy consisted the control group. Pregnant women with diabetes were examined in three trimesters of pregnancy, the control group – in the third trimester. OCTA imaging was performed using the RTVue XR Avanti OCT 6×6 mm Angio Retina scan protocols (Optovue, USA). The vascular density (VD), vascular density in the fovea (VDF), and foveal avascular zone (FAZ) area in the superficial capillary plexus were studied.

Results. In the third trimester, VDF in pregnant women with diabetes was significantly less than in the control group, in the absence of differences in VD and FAZ area. VD was significantly lower, and FAZ area was significantly higher in pregnant women with diabetic retinopathy (DR) than in pregnant women with diabetes without DR. There were no significant differences in the values of blood flow parameters in the groups of pregnant women with diabetes, regardless of underwent them the laser coagulation of the retina. At analyzing the values of VD, VDF, FAZ area in pregnant women with diabetes in different trimesters of pregnancy, statistically significant differences were not observed.

In 11 pregnant women with DR areas of retinal nonperfusion were revealed, which in 6 patients tended to expand during pregnancy. In 2 patients with T1D without DR in the third trimester areas of nonperfusion were identified.

Conclusion. Obtained data have practical importance for the diagnosis of DR manifestations during pregnancy. OCTA is a valuable diagnostic method that allows non-invasive diagnostics of the presence of areas of retinal nonperfusion in the absence of ophthalmoscopic signs of DR in pregnant women with diabetes, as well as assess the state of areas of retinal nonperfusion during pregnancy in patients with DR.

References

1. IDF Diabetes Atlas. 6th ed. International Diabetes Federation. Brussels: International Diabetes Federation; 2014.

2. Bourne RR, Stevens GA, White RA, Smith JL, Flaxman SR, Price H, et al. Vision loss expert group. Causes of vision loss worldwide, 1990–2010: a systematic analysis. Lancet Glob Health. 2013;1(6): e339–349. doi: 10.1016/S2214-109X(13)70113-X

3. Clustering of long-term complications in families with diabetes in the diabetes control and complications trial. The diabetes control and complications trial research group. Diabetes. 1997;46(11): 1829–1839. doi: 10.2337/diab.46.11.1829

4. Egan AM, McVicker L, Heerey A, Carmody L, Harney F, Dunne FP. Diabetic retinopathy in pregnancy: a population-based study of women with pregestational diabetes. J Diabetes Res. 2015;2015: 310239. doi: 10.1155/2015/310239

5. Phelps RL, Sakol P, Metzger BE, Jampol LM, Freinkel N. Changes in diabetic retinopathy during pregnancy. Correlations with regulation of hyperglycemia. Arch Ophthalmol. 1986;104(12): 1806–1810. doi: 10.1001/archopht.1986.01050240080044

6. Arun CS, Taylor R. Influence of pregnancy on long-term progression of retinopathy in patients with type 1 diabetes. Diabetologia. 2008;5(6): 1041–1045. doi: 10.1007/s00125-008-0994-z

7. Chanwimol K, Balasubramanian S, Nassisi M, Gaw SL, Janzen C, Sarraf D, Sadda SR, Tsui I. Retinal vascular changes during pregnancy detected with optical coherence tomography angiography. Invest Ophthalmol Vis Sci. 2019;60(7): 2726–2732. doi: 10.1167/iovs.19-26956

8. Rosenn B, Miodovnik M, Kranias G, Khoury J, Combs CA, Mimouni F, Siddiqi TA, Lipman MJ. Progression of diabetic retinopathy in pregnancy: association with hypertension in pregnancy. Am J Obstet Gynecol. 1992;166(4): 1214–1218. doi: 10.1016/s0002-9378(11)90608-5

9. Hwang TS, Gao SS, Liu L, Lauer AK, Bailey ST, Flaxel CJ, et al. Automated quantification of capillary nonperfusion using optical coherence tomography angiography in diabetic retinopathy. JAMA Ophthalmol. 2016;134(4): 367–373. doi: 10.1001/jamaophthalmol.2015.5658

10. de Carlo TE, Chin AT, Bonini Filho MA, Adhi M, Branchini L, Salz DA, et al. Detection of microvascular changes in eyes of patients with diabetes but not clinical diabetic retinopathy using optical coherence tomography angiography. Retina. 2015;35(11): 2364–2370. doi: 10.1097/IAE.0000000000000882

11. Goudot MM, Sikorav A, Semoun O, Miere A, Jung C, Courbebaisse B, et al. Parafoveal OCT angiography features in diabetic patients without clinical diabetic retinopathy: a qualitative and quantitative analysis. J Ophthalmol. 2017;2017: 8676091. doi: 10.1155/2017/8676091

12. Ishibazawa A, Nagaoka T, Takahashi A, Omae T, Tani T, Sogawa K, et al. Optical coherence tomography angiography in diabetic retinopathy: a prospective pilot study. Am J Ophthalmol. 2015;160(1): 35–44. doi: 10.1016/j.ajo.2015.04.021

13. Spaide RF, Klancnik JM, Cooney MJ. Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol. 2015;133(1): 45–50. doi: 10.1001/jamaophthalmol.2014.3616

14. Pan J, Chen D, Yang X, Zou R, Zhao K, Cheng D, et al. Characteristics of neovascularization in early stages of proliferative diabetic retinopathy by optical coherence tomography angiography. Am J Ophthalmol. 2018;192: 146–156. doi: 10.1016/j.ajo.2018.05.018

15. Fabrikantov O.L., Pronichkina M.M., Yablokova N.V., Ovsyannikova N.V. Innovatsionnye vozmozhnosti neinvazivnoi prizhiznennoi otsenki sostoyaniya sosudov mikrotsirkulyatornogo lozha pri diabeticheskoi retinopatii. Vestnik Volgogradskogo Gosudarstvennogo meditsinskogo universiteta. 2018;4: 41–45.

16. Takase N, Nozaki M, Kato A, Ozeki H, Yoshida M, Ogura Y. Enlargement of foveal avascular zone in diabetic eyes evaluated by en face optical coherence tomography angiography. Retina. 2015;35(11): 2377–2383. doi: 10.1097/IAE.0000000000000849

17. Agemy SA, Scripsema NK, Shah CM, Chui T, Garcia PM, Lee JG, et al. Retinal vascular perfusion density mapping using optical coherence tomography angiography in normals and diabetic retinopathy patients. Retina. 2015;35(11): 2353–2363. doi: 10.1097/IAE.0000000000000862

18. Salz DA, de Carlo TE, Adhi M, Moult E, Choi W, Baumal CR, et al. Select features of diabetic retinopathy on swept-source optical coherence tomographic angiography compared with fluorescein angiography and normal eyes. JAMA Ophthalmol. 20161;134(6): 644–650. doi: 10.1001/jamaophthalmol.2016.0600

19. Conti FF, Qin VL, Rodrigues EB, Sharma S, Rachitskaya AV, Ehlers JP, Singh RP. Choriocapillaris and retinal vascular plexus density of diabetic eyes using split-spectrum amplitude decorrelation spectraldomain optical coherence tomography angiography. Br J Ophthalmol. 2019;103(4):452–456. doi: 10.1136/

20. bjophthalmol-2018-311903

21. Bresnick GH, Condit R, Syrjala S, Palta M, Groo A, Korth K. Abnormalities of the foveal avascular zone in diabetic retinopathy. Arch Ophthalmol. 1984;102(9): 1286–1293. doi: 10.1001/archopht.1984.01040031036019

22. Burnasheva M.A., Mal'tsev D.S., Kulikov A.N. Personalizirovannaya otsenka ploshchadi foveal'noi avaskulyarnoi zony s pomoshch'yu opticheskoi kogerentnoi tomografii-angiografii. Sovremennye tekhnologii v oftal'mologii. 2017;7: 19–21.

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24. Motulsky E, Zheng F, Liu G, Gregori G, Rosenfeld PJ. Swept-source OCT angiographic imaging of a central retinal vein occlusion during pregnancy. Ophthalmic Surg Lasers Imaging Retina. 2018;49(3): 206–208. doi: 10.3928/23258160-20180221-09

25. Soma-Pillay P, Nelson-Piercy C, Tolppanen H, Mebazaa A. Physiological changes in pregnancy. Cardiovasc J Afr. 2016;27(2): 89–94. doi: 10.5830/CVJA-2016-021

26. Yablokova N.V., Fabrikantov O.L. Issledovanie vliyaniya panretinal'noi lazerkoagulyatsii po povodu diabeticheskoi retinopatii na sosudistuyu sistemu glaza. Sovremennye tekhnologii v oftal'mologii. 2019;6: 157–163.