Особенности глазного кровотока и методы его исследования

В обзоре представлены сведения о базовых знаниях, касающихся регуляции кровотока в сетчатке, основанных на данных, полученных в экспериментах на животных с помощью инвазивных методов. Наряду с хорошо известными инструментальными методами диагностики сосудистой патологии органа зрения применяются новые высокотехнологичные методы исследования микроциркуляции глаза, позволяющие наиболее достоверно оценивать степень нарушения кровообращения в сосудах глазного яблока. Благодаря развитию неинвазивных ультразвуковых методов исследования появилась возможность более детально изучать состояние кровотока в сосудах глазного яблока у лиц с сосудистой патологией органа зрения. Важной особенностью гемодинамики глаза является ее зависимость от внутриглазного давления и наличие саморегуляции кровотока в сетчатке, в том числе при изменении освещенности сетчатки, артериального давления и так далее. На кровоснабжение глаза могут влиять и фармакологические агенты, которые обычно используются в лечении системных заболеваний.

1. Киселева Т.Н. Цветовое допплеровское картирование в офтальмологии Вестник офтальмологии. 2001;6:51–53.

2. Киселева Т.Н., Ежов М.В., Аджемян Н.А., Танковский В.Э., Ильина Н.В. Особенности регионарного глазного кровотока при артериальной гипертензии I–II степени и субклиническом атеросклерозе. Российский офтальмологический журнал. 2016;9(3):26–33.

3. Киселева Т.Н., Котелин В.И., Лосанова О.А., Луговкина К.В. Неинвазивные методы оценки гемодинамики переднего сегмента глаза: перспективы применения в клинической практике. Офтальмология. 2017;14(4):283–290. DOI: 10.18008/1816-5095-2017-4-283-290

4. Киселева Т.Н. Ультразвуковые методы исследования кровотока в диагностике ишемических поражений глаза. Вестник офтальмологии. 2004;4:3–5.

5. Мамиконян В.Р., Казарян Э.Э., Козлова И.В. Исследование пульсовового глазного кровотока в диагностике и мониторинге первичной открытоугольной глаукомы. Глаукома. 2008;3:21–25.

6. Rizzoni D, Agabiti Rosei C, Agabiti Rosei E. Hemodynamic consequences of changes in microvascular structure. Am J Hypertens. 2017;30:939–946. DOI: 10.1093/ajh/hpx032

7. Burns SA, Elsner AE, Thomas J. Gast Imaging the Retinal Vasculature. Ann Rev Vis Sci. 2021 Sep 15;7:129–153. DOI: 10.1146/annurev-vision-093019-113719

8. LaBarbera M. The design of fluid transport systems: a comparative perspective. / In Bevan JA, Kaley G, Rubanyi GM (eds): Flow Dependent Regulation of Vascular Function. New York, Oxford University Press, 1995.

9. Riva CE, Grunwald JE, Sinclair SH, O’Keefe K. Fundus camera based retinal LDV. Appl Opt 1981;20:117–120. https://opg.optica.org/ao/abstract.cfm?URI=ao-20-1-117

10. Glucksberg MR, Dunn R: Direct measurement of retinal microvascular pressures in the live, anesthetized cat. Microvasc Res. 1993;45:158–165. DOI: 10.1006/mvre.1993.1015

11. Alarcon Martinez L, Yemisci M, Dalkara T. Pericyte morphology and function. Histopathol. 2021 Jun;36(6):633–643. DOI: 10.14670/HH-18-314

12. Riva CE, Petrig BL. Retinal blood flow: laser Doppler velocimetry and blue field simulation technique / In Masters BR (ed): Noninvasive Diagnostic Techniques in Ophthalmology. New York, Springer, 1990. P. 390–394.

13. Leitgeb RA, Schmetterer L, Drexler W, Fercher AF. Real-time assessment of retinal blood flow with ultrafast acquisition by color Doppler Fourier domain optical coherence tomography. Opt Express. 2003;11:3116–3121. DOI: 10.1364/oe.11.003116

14. Reiner A, Fitzgerald MES, Del Mar N, Chunyan Li. Neural control of choroidal blood flow. Prog Retin Eye Res. 2018 May;64:96–130. DOI: 10.1016/j.preteyeres.2017.12.001

15. Yazdanfar S, Rollins AM, Izatt JA: Imaging and velocimetry of the human retinal circulation with color Doppler optical coherence tomography. Opt Lett 2000;25:1448–1450. DOI: 10.1364/ol.25.001448

16. Noonan JE, Lamoureux EL, Sarossy M. Neuronal activity dependent regulation of retinal blood flow. Clin Exp Ophthalmol. 2015 Sep Oct;43(7):673–682. DOI: 10.1111/ceo.12530

17. Pournaras CJ, Rungger Brändle E, Riva CE, Hardarson SH, Stefansson E. Regulation of retinal blood flow in health and disease. Prog Retin Eye Res. 2008 May;27(3):284–330. DOI: 10.1016/j.preteyeres.2008.02.002

18. Fry BC, Harris A, Siesky B, Arciero A. Blood flow regulation and oxygen transport in a heterogeneous model of the mouse retina. Math Biosci. 2020 Nov;329:108476. DOI: 10.1016/j.mbs.2020.108476

19. Guran T, Zeimer RC, Shahidi M, Mori MT: Quantitative analysis of retinal hemodynamics using targeted dye delivery. Invest Ophthalmol Vis Sci. 1990;31:2300–2306.

20. Riva CE, Alm A, Pournaras CJ: Ocular circulation; in Levin LA, Nilsson SFE, Ver Hoeve J, Wu S, Kaufman PL, Alm A (eds): Adler’s Physiology of the Eye, ed 11. New York, Elsevier, 2011.

21. Khoobehi B, Aly OM, Schuele KM, Stradtmann MO, Peyman GA. Determination of retinal blood velocity with respect to the cardiac cycle using laser-triggered release of liposome encapsulated dye. Lasers Surg Med. 1990;10:469–475. DOI: 10.1002/lsm.1900100512

22. Arend O, Harris JA, Shoemaker WE, Sponsel HK, Knabben H, Reim M. Perifoveal capillary microcirculation: comparison of blue light stimulation and scanning laser technique. Invest Ophthalmol Vis Sci. 1993;34 (suppl):1391.

23. James CB, Trew DR, Clark K. Factors influencing the ocular pulse axial length. Graefe’s Arch Clin Exp Ophthalmol. 1991;229:341–344. DOI: 10.1007/BF00170692

24. Lam AK, Chan ST, Chan B. The effect of axial length on ocular blood flow assessment in anisometropes. Ophthalmic Physiol Opt. 2003;23:315–320. DOI: 10.1046/j.1475-1313.2003.00122.x

25. Geyer O, Silver DM, Mathalon N. Gender and age effects on pulsatile ocular blood flow. Ophthalmic Res. 2003;35:247–250. DOI: 10.1159/000072144

26. Gunvant P, Baskaran M, Vijaya L. Effect of corneal parameters on measurements using the pulsatile ocular blood flow tonograph and goldmann applanation tonometer. Br J Ophthalmol. 2004;88:518–522. DOI: 10.1136/bjo.2003.019331

27. Gunvant P, Baskaran M, Vijaya L. Comparison of pulsatile ocular blood flow in Indians and Europeans. Eye. 2005;19:1163–1168. DOI: 10.1038/sj.eye.6701710

28. Lam AK, Chan ST, Chan H. The effect of age on ocular blood supply determined by pulsatile ocular blood flow and color Doppler ultrasonography. Optom Vis Sci. 2003;80:305–311. DOI: 10.1097/00006324-200304000-00008

29. Lam AK, Lam CH. Effects of breath––holding on pulsatile ocular blood flow measurement in normal subjects. Optom Vis Sci. 2004;81:597–600 DOI: 10.1097/01.opx.0000141795.95597.98

30. Rizzoni D. New Methods to Study the Microcirculation. American Journal of Hypertension. 2018;31(3):265 273. DOI: 10.1093/ajh/hpx211

31. Bosley TM, Savino PJ, Sergott RC, Eagle RC, Sandy R, Gee W. Ocular pneumoplethysmography can help in the diagnosis of giant cell arteritis. Arch Ophthalmol. 1989;107:379–381. DOI: 10.1001/archopht.1989.01070010389030

32. Bienfang DC. Loss of the ocular pulse in the acute phase of temporal arteritis. Acta Ophthalmol(Copenh). 1989;67:35–37. DOI: 10.1111/j.1755-3768.1989.tb07085.x

33. Pache M, Nagel E, Flammer J: Reproducibility of measurements with the retinal vessel analyzer under optimal conditions. Klin Monatsbl Augenheilkd. 2002;219:523–527. DOI: 10.1055/s-2002-33589

34. Riva CE, Logean E, Falsini B. Visually evoked hemodynamical response and assessment of neurovascular coupling in the optic nerve and retina. Prog Retin Eye Res. 2005;24:183–215. DOI: 10.1016/j.preteyeres.2004.07.002

35. Warner RL, de Castro A, Sawides L, Gast T, Sapoznik K, Ting Luo, Burns SA. Fullfield flicker evoked changes in parafoveal retinal blood flow. Sci Rep. 2020 Sep 29;10(1):16051. DOI: 10.1038/s41598-020-73032-0

36. Wang JJ, Liew G, Klein R, Rochtchina E, Knudtson MD, Klein BE, Wong TY, Burlutsky G, Mitchell P. Retinal vessel diameter and cardiovascular mortality: pooled data analysis from two older populations. Eur Heart J. 2007;28:1984–1992. DOI: 10.1093/eurheartj/ehm221

37. Mendrinos E, Mangioris G, Papadopoulou DN, Dosso AA, Pournaras CJ. Retinal vessel analyzer measurements of the effect of panretinal photocoagulation on the retinal arteriolar diameter in diabetic retinopathy. Retina 2010;30:55. DOI: 10.1097/IAE.0b013e3181bd2f79

38. Loukovaara S, Harju M, Kaaja R, Immonen I: Retinal capillary blood flow in diabetic and nondiabetic women during pregnancy and postpartum period. Invest Ophthalmol Vis Sci. 2003;44:1486–1491. DOI: 10.1167/iovs.02-0293

39. Riva CE, Petrig BL. Laser Doppler techniques in ophthalmology: principles and applications / In Fankhauser F, Kwasniewska S (eds): Lasers in Ophthalmology — Basic, Diagnostic and Surgical Aspects. The Hague, Kugler 2003. P. 51–59.

40. Makita S, Fabritius T, Yasuno Y. Quantitative retinal blood flow measurement with three dimensional vessel geometry determination using ultrahigh resolution Doppler optical coherence angiography. Opt Lett. 2008;33:836–838. DOI: 10.1364/ol.33.000836

41. Savastano C.M., Lumbroso B., Rispoli M. In Vivo Characterization of Retinal Vascularization Morphology Using Optical Coherence Tomography Angiography. Retina. 2015 Nov;35(11):2196–2203. DOI: 10.1097/IAE.0000000000000635

42. Riva CE, Harino S, Petrig BL, Shonat RD. Laser Doppler flowmetry in the optic nerve. Exp Eye Res. 1992;55:499–506. DOI: 10.1016/0014-4835(92)90123-a

43. Riva CE, Schmetterer L. Microcirculation of the ocular fundus / In Tuma RF, Duran WN, Ley K (eds): Handbook of Physiology: Microcirculation. Amsterdam, Academic Press, 2008. P. 735–765.

44. Briers JD, Fercher AF: Retinal blood flow visualization by means of laser speckle photography. Invest Ophthalmol Vis Sci. 1982;22:255–259.

45. Leske MC, Wu SY, Hennis A, Honkanen R, Nemesure B. Risk factors for incident openangle glaucoma: the Barbados Eye Studies. Ophthalmology. 2008;115:85–93. DOI: 10.1016/j.ophtha.2007.03.017

46. Grunwald JE, Riva CE, Stone RA, Keates EU, Petrig BL. Retinal autoregulation in open-angle glaucoma. Ophthalmology. 1984;91:1690–1694.

47. Nagel E, Munch K, Vilser W. Measurement of the diameter of segments of retinal branch vessels in digital fundus images: an experimental study of the method and reproducibility. Klin Monatsbl Augenheilkd. 2001;218: 616–620. DOI: 10.1055/s-2001-17640

48. Garhofer G, Zawinka C, Resch H, Huemer KH, Schmetterer L, Dorner GT. Response of retinal vessel diameters to flicker stimulation in patients with early open angle glaucoma. J Glaucoma. 2004;13:340–344. DOI: 10.1097/00061198-200408000-00013

49. Ma Z, Pan X, Zhou D, Zhu Z, Xu A, Shi P, Chen H. Changes of retinal and choroidal capillary blood flow in macula after an acute intraocular pressure elevation. Medicine (Baltimore). 2020 Jun 26;99(26):e21007. DOI: 10.1097/MD.0000000000021007

50. Gilmore ED, Hudson C, Nrusimhadevara RK, Ridout R, Harvey PT, Mandelcorn M, Lam WC, Devenyi RG. Retinal arteriolar hemodynamic response to an acute hyperglycemic provocation in early and sightthreatening diabetic retinopathy. Microvasc Res. 2007;73:191–197. DOI: 10.1016/j.mvr.2007.01.001

51. Pemp B, Garhofer G, Weigert G, Karl K, Resch H, Wolzt M, Schmetterer L. Reduced retinal vessel response to flicker stimulation but not to exogenous nitric oxide in type 1 diabetes. Invest Ophthalmol Vis Sci. 2009;50:4029–4032. DOI: 10.1167/iovs.08-3260

52. Dawczynski J, Mandecka A, Blum M, Muller UA, Ach T, Strobel J. Endothelial dysfunction of central retinal vessels: a prognostic parameter for diabetic retinopathy? Klin Monatsbl Augenheilkd. 2007;224:827–831 (in German). DOI: 10.1055/s-2007-963675

53. Grunwald JE, Brucker AJ, Grunwald SE, Riva CE. Retinal hemodynamics in proliferative diabetic retinopathy. A laser Doppler velocimetry study. Invest Ophthalmol Vis Sci. 1993 Jan;34(1):66–71.

54. Hanaguri J, Yokota H, Watanabe M, Yamagami S, Kushiyama A, Lih Kuo, Taiji Retinal blood flow dysregulation precedes neural retinal dysfunction in type 2 diabetic mice. NagaokaSci Rep. 2021 Sep 15;11(1):18401. DOI: 10.1038/s41598-021-97651-3

55. Nippert AR, Newman EA. Regulation of blood flow in diabetic retinopathy. Vis Neurosci. 2020 Jul 20;37:E004. DOI: 10.1017/S0952523820000036

56. Polak K, Luksch A, Frank B, Jandrasits K, Polska E, Schmetterer L. Regulation of human retinal blood flow by endothelin 1. Exp Eye Res. 2003 May;76(5):633–640. DOI: 10.1016/s0014-4835(02)00312-3