Прецизійна візуалізація судин сітківки in vivo за допомогою адаптивної оптики

Oleg Zadorozhnyy; Andrii Korol; Illia Nasinnyk; Taras Kustrin; Volodymyr Naumenko; Nataliya Pasechnikova

doi:10.31288/oftalmolzh202323138

Authors

Oleg Zadorozhnyy Filatov Institute of Eye Disease and Tissue Therapy https://orcid.org/0000-0003-0125-2456
Andrii Korol Filatov Institute of Eye Disease and Tissue Therapy https://orcid.org/0000-0003-0516-308X
Illia Nasinnyk Filatov Institute of Eye Disease and Tissue Therapy
Taras Kustrin Filatov Institute of Eye Disease and Tissue Therapy
Volodymyr Naumenko Filatov Institute of Eye Disease and Tissue Therapy
Nataliya Pasechnikova Filatov Institute of Eye Disease and Tissue Therapy

DOI:

https://doi.org/10.31288/oftalmolzh202323138

Keywords:

adaptive optics, retinal vessels, arterial hypertension, diabetic retinopathy

Abstract

Adaptive optics (AO) provides new, unique opportunities for in vivo visualization of retinal vasculature. AO retinal vessel imaging can be utilized as a component of multimodal imaging tools to complement conventional diagnostic imaging modalities. Non-invasive and highly promising AO imaging of fundus structures allows the qualitative and quantitative assessment of early signs of retinal vascular remodeling associated with age, arterial hypertension, diabetes mellitus and other disorders.

Author Biographies

Oleg Zadorozhnyy, Filatov Institute of Eye Disease and Tissue Therapy

д.мед.н.

Andrii Korol , Filatov Institute of Eye Disease and Tissue Therapy

д.мед.н.

Nataliya Pasechnikova, Filatov Institute of Eye Disease and Tissue Therapy

д.мед.н., професор, член-кор. НАМН України.

References

Nardin M, Coschignano MA, Rossini C, De Ciuceis C, Caletti S, Rizzoni M, et al. Methods of evaluation of microvascular structure: state of the art. Eur J Transl Clin Med. 2018;1(1):7-17. https://doi.org/10.31373/ejtcm/95161

Angel J. Ground-based imaging of extrasolar planets using adaptive optics. Nature. 1994; 368:203-207. https://doi.org/10.1038/368203a0

Hardy JW. Adaptive Optics for Astronomical Telescopes. Oxford University Press; 1998; 448 p.

Rodríguez C, Ji N. Adaptive optical microscopy for neurobiology. Curr Opin Neurobiol. 2018; 50:83-91. https://doi.org/10.1016/j.conb.2018.01.011

Wang K, Sun W, Richie CT, Harvey BK, Betzig E, Ji N. Direct wavefront sensing for high-resolution in vivo imaging in scattering tissue. Nat Commun. 2015; 6:7276. https://doi.org/10.1038/ncomms8276. https://doi.org/10.1038/ncomms8276

Akyol E, Hagag AM, Sivaprasad S, Lotery AJ. Adaptive optics: principles and applications in ophthalmology. Eye. 2021; 35(1):244-264. https://doi.org/10.1038/s41433-020-01286-z

Liang J, Williams DR, Miller DT. Supernormal vision and high-resolution retinal imaging through adaptive optics. J Opt Soc Am A Opt Image Sci Vis. 1997; 14(11):2884-92. https://doi.org/10.1364/josaa.14.002884.

Dubra A, Sulai Y, Norris JL, Cooper RF, Dubis AM, Williams DR, Carroll J. Noninvasive imaging of the human rod photoreceptor mosaic using a confocal adaptive optics scanning ophthalmoscope. Biomed Opt Express. 2011; 2(7):1864-76. https://doi.org/10.1364/BOE.2.001864.

Pallikaris A, Williams DR, Hofer H. The reflectance of single cones in the living human eye. Invest Ophthalmol Vis Sci. 2003; 44:4580-4592. https://doi.org/10.1167/iovs.03-0094.

https://doi.org/10.1167/iovs.03-0094

Rossi EA, Granger CE, Sharma R, Yang Q, Saito K, Schwarz C, et al. Imaging individual neurons in the retinal ganglion cell layer of the living eye. Proc Natl Acad Sci U S A. 2017; 114(3):586-591. https://doi.org/10.1073/pnas.1613445114

Scoles D, Sulai YN, Dubra A. In vivo dark-field imaging of the retinal pigment epithelium cell mosaic. Biomed Opt Express. 2013; 4(9):1710-1723. https://doi.org/10.1364/BOE.4.001710.

Laforest T, Künzi M, Kowalczuk L, Carpentras D, Behar-Cohen F, Moser C. Transscleral Optical Phase Imaging of the Human Retina. Nat Photonics. 2020; 14(7):439-445. https://doi.org/10.1038/s41566-020-0608-y. https://doi.org/10.1038/s41566-020-0608-y

Rizzoni D, Docchio F. Assessment of retinal arteriolar morphology by noninvasive methods: the philosopher's stone? J Hypertens. 2016; 34(6):1044-6.

https://doi.org/10.1097/HJH.0000000000000908

Zacharria M, Lamory B, Chateau N. New view of the eye. Nature Photon. 2011; 5:24-26. https://doi.org/10.1038/nphoton.2010.298.

Bakker E, Dikland FA, van Bakel R, Andrade De Jesus D, Sánchez Brea L, et al. Adaptive optics ophthalmoscopy: a systematic review of vascular biomarkers. Surv Ophthalmol. 2022; 67(2):369-387. https://doi.org/10.1016/j.survophthal.2021.05.012.

https://doi.org/10.1016/j.survophthal.2021.05.012

Scoles D, Sulai YN, Langlo CS, Fishman GA, Curcio CA, Carroll J, Dubra A. In vivo imaging of human cone photoreceptor inner segments. Invest Ophthalmol Vis Sci. 2014; 55(7):4244-4251. https://doi.org/10.1167/iovs.14-14542.

https://doi.org/10.1167/iovs.14-14542

Zhang B, Li N, Kang J, He Y, Chen XM. Adaptive optics scanning laser ophthalmoscopy in fundus imaging, a review and update. Int J Ophthalmol. 2017; 10(11):1751-1758. https://doi.org/10.18240/ijo.2017.11.18.

https://doi.org/10.18240/ijo.2017.11.18

Carroll J, Kay DB, Scoles D, Dubra A, Lombardo M. Adaptive optics retinal imaging - clinical opportunities and challenges. Curr Eye Res. 2013; 38(7):709-21. https://doi.org/10.3109/02713683.2013.784792.

https://doi.org/10.3109/02713683.2013.784792

Jonnal RS, Kocaoglu OP, Zawadzki RJ, Liu Z, Miller DT, Werner JS. A Review of Adaptive Optics Optical Coherence Tomography: Technical Advances, Scientific Applications, and the Future. Invest Ophthalmol Vis Sci. 2016; 57(9):51-68. https://doi.org/10.1167/iovs.16-19103.

https://doi.org/10.1167/iovs.16-19103

Chui TY, Gast TJ, Burns SA. Imaging of vascular wall fine structure in the human retina using adaptive optics scanning laser ophthalmoscopy. Invest Ophthalmol Vis Sci. 2013; 54(10):7115-24. https://doi.org/10.1167/iovs.13-13027.

https://doi.org/10.1167/iovs.13-13027

Ikram MK, Cheung CY, Lorenzi M, Klein R, Jones TL, Wong TY; NIH/JDRF Workshop on Retinal Biomarker for Diabetes Group. Retinal vascular caliber as a biomarker for diabetes microvascular complications. Diabetes Care. 2013; 36(3):750-9. https://doi.org/10.2337/dc12-1554.

https://doi.org/10.2337/dc12-1554

Rosenbaum D, Alessandro M, Koch E, Rossant F, Gallo A, Kachenoura N, et al. Effects of age, blood pressure and antihypertensive treatments on retinal arterioles remodeling assessed by adaptive optics. J Hypertens. 2016; 34:1115-1122. https://doi.org/10.1097/HJH.0000000000000894.

https://doi.org/10.1097/HJH.0000000000000894

Hillard JG, Gast TJ, Chui TY, Sapir D, Burns SA. Retinal Arterioles in Hypo-, Normo-, and Hypertensive Subjects Measured Using Adaptive Optics. Transl Vis Sci Technol. 2016; 5(4):16. https://doi.org/10.1167/tvst.5.4.16.

https://doi.org/10.1167/tvst.5.4.16

Rizzoni D, Porteri E, Boari GE, De Ciuceis C, Sleiman I, Muiesan ML, et al. Prognostic significance of small-artery structure in hypertension. Circulation. 2003; 108(18):2230-5. https://doi.org/10.1161/01.CIR.0000095031.51492.C5.

https://doi.org/10.1161/01.CIR.0000095031.51492.C5

Meixner E, Michelson G. Measurement of retinal wall-to-lumen ratio by adaptive optics retinal camera: a clinical research. Graefes Arch Clin Exp Ophthalmol. 2015; 253(11):1985-95. https://doi.org/10.1007/s00417-015-3115-y.

https://doi.org/10.1007/s00417-015-3115-y

Koch E, Rosenbaum D, Brolly A, Sahel JA, Chaumet-Riffaud P, Girerd X, et al. Morphometric analysis of small arteries in the human retina using adaptive optics imaging: relationship with blood pressure and focal vascular changes. J Hypertens. 2014; 32(4):890-898. https://doi.org/10.1097/HJH.0000000000000095.

https://doi.org/10.1097/HJH.0000000000000095

Arichika S, Uji A, Ooto S, Muraoka Y, Yoshimura N. Effects of age and blood pressure on the retinal arterial wall, analyzed using adaptive optics scanning laser ophthalmoscopy. Sci Rep. 2015; 5:12283. https://doi.org/10.1038/srep12283.

https://doi.org/10.1038/srep12283

Baleanu D, Ritt M, Harazny J, Heckmann J, Schmieder RE, Michelson G. Wall-to-lumen ratio of retinal arterioles and arteriole-to-venule ratio of retinal vessels in patients with cerebrovascular damage. Invest Ophthalmol Vis Sci. 2009; 50(9):4351-9. https://doi.org/10.1167/iovs.08-3266.

https://doi.org/10.1167/iovs.08-3266

Rizzoni D, Porteri E, Duse S, De Ciuceis C, Rosei CA, La Boria E, et al. Relationship between media-to-lumen ratio of subcutaneous small arteries and wall-to-lumen ratio of retinal arterioles evaluated noninvasively by scanning laser Doppler flowmetry. J Hypertens. 2012; 30(6):1169-75. https://doi.org/ 10.1097/HJH.0b013e328352f81d.

https://doi.org/10.1097/HJH.0b013e328352f81d

Salvetti M, Agabiti Rosei C, Paini A, Aggiusti C, Cancarini A, Duse S, et al. Relationship of wall-to-lumen ratio of retinal arterioles with clinic and 24-hour blood pressure. Hypertension. 2014; 63(5):1110-5. https://doi.org/10.1161/HYPERTENSIONAHA.113.03004.

https://doi.org/10.1161/HYPERTENSIONAHA.113.03004

Zaleska-Żmijewska A, Piątkiewicz P, Śmigielska B, Sokołowska-Oracz A, Wawrzyniak ZM, Romaniuk D, et al. Retinal Photoreceptors and Microvascular Changes in Prediabetes Measured with Adaptive Optics (rtx1™): A Case-Control Study. J Diabetes Res. 2017; 2017:4174292. https://doi.org/10.1155/2017/4174292.

https://doi.org/10.1155/2017/4174292

Arichika S, Uji A, Murakami T, Suzuma K, Gotoh N, Yoshimura N. Correlation of retinal arterial wall thickness with atherosclerosis predictors in type 2 diabetes without clinical retinopathy. Br J Ophthalmol. 2017; 101(1):69-74. https://doi.org/ 10.1136/bjophthalmol-2016-309612.

https://doi.org/10.1136/bjophthalmol-2016-309612

Zaleska-Żmijewska A, Wawrzyniak ZM, Dąbrowska A, Szaflik JP. Adaptive Optics (rtx1) High-Resolution Imaging of Photoreceptors and Retinal Arteries in Patients with Diabetic Retinopathy. J Diabetes Res. 2019; 2019:9548324. https://doi.org/ 10.1155/2019/9548324.

https://doi.org/10.1155/2019/9548324

Cristescu IE, Zagrean L, Balta F, Branisteanu DC. Retinal microcirculation investigation in type I and II diabetic patients without retinopathy using an adaptive optics retinal camera. Acta Endocrinol (Buchar). 2019; 15(4):417-422. https://doi.org/10.4183/aeb.2019.417.

https://doi.org/10.4183/aeb.2019.417

Streese L, Brawand LY, Gugleta K, Maloca PM, Vilser W, Hanssen H. New frontiers in noninvasive analysis of retinal wall-to-lumen ratio by retinal vessel wall analysis. Trans Vis Sci Tech. 2020; 9(6):7, https://doi.org/10.1167/tvst.9.6.7.

https://doi.org/10.1167/tvst.9.6.7

Ueno Y, Iwase T, Goto K, Tomita R, Ra E, Yamamoto K, Terasaki H. Association of changes of retinal vessels diameter with ocular blood flow in eyes with diabetic retinopathy. Sci Rep. 2021; 11(1):4653. https://doi.org/10.1038/s41598-021-84067-2.

https://doi.org/10.1038/s41598-021-84067-2

Sadowski J, Targonski R, Cyganski P, Nowek P, Starek-Stelmaszczyk M, Zajac K, et al. Remodeling of Retinal Arterioles and Carotid Arteries in Heart Failure Development - A Preliminary Study. J. Clin. Med. 2022; 11:3721. https://doi.org/10.3390/jcm11133721.

https://doi.org/10.3390/jcm11133721

Baltă F, Cristescu IE, Mirescu AE, Baltă G, Zemba M, Tofolean IT. Investigation of Retinal Microcirculation in Diabetic Patients Using Adaptive Optics Ophthalmoscopy and Optical Coherence Angiography. J Diabetes Res. 2022; 2022:1516668. https://doi.org/10.1155/2022/1516668.

https://doi.org/10.1155/2022/1516668

Martin JA, Roorda A. Direct and noninvasive assessment of parafoveal capillary leukocyte velocity. Ophthalmology. 2005; 112(12):2219-24. https://doi.org/ 10.1016/j.ophtha.2005.06.033.

https://doi.org/10.1016/j.ophtha.2005.06.033

Martin JA, Roorda A. Pulsatility of parafoveal capillary leukocytes. Exp Eye Res. 2009; 88(3):356-60. https://doi.org/10.1016/j.exer.2008.07.008.

https://doi.org/10.1016/j.exer.2008.07.008

Antonios TF. Microvascular rarefaction in hypertension--reversal or over-correction by treatment? Am J Hypertens. 2006; 19(5):484-5. https://doi.org/10.1016/j.amjhyper.2005.11.010.

https://doi.org/10.1016/j.amjhyper.2005.11.010

Levy BI, Ambrosio G, Pries AR, Struijker-Boudier HA. Microcirculation in hypertension: a new target for treatment? Circulation. 2001; 104(6):735-40. https://doi.org/10.1161/hc3101.091158.

https://doi.org/10.1161/hc3101.091158

Izzard AS, Rizzoni D, Agabiti-Rosei E, Heagerty AM. Small artery structure and hypertension: adaptive changes and target organ damage. J Hypertens. 2005; 23(2):247-50. https://doi.org/10.1097/00004872-200502000-00002.

https://doi.org/10.1097/00004872-200502000-00002

Park JB, Schiffrin EL. Small artery remodeling is the most prevalent (earliest?) form of target organ damage in mild essential hypertension. J Hypertens. 2001; 19(5):921-30. https://doi.org/10.1097/00004872-200105000-00013.

https://doi.org/10.1097/00004872-200105000-00013

Harazny JM, Ritt M, Baleanu D, Ott C, Heckmann J, Schlaich MP, et al. Increased wall:lumen ratio of retinal arterioles in male patients with a history of a cerebrovascular event. Hypertension. 2007; 50(4):623-9. https://doi.org/10.1161/HYPERTENSIONAHA.107.090779.

https://doi.org/10.1161/HYPERTENSIONAHA.107.090779

Ritt M, Schmieder RE. Wall-to-lumen ratio of retinal arterioles as a tool to assess vascular changes. Hypertension. 2009; 54(2):384-7. https://doi.org/10.1161/HYPERTENSIONAHA.109.133025.

https://doi.org/10.1161/HYPERTENSIONAHA.109.133025

Сhui TY, Dubow M, Pinhas A, Shah N, Gan A, Weitz R, et al. Comparison of adaptive optics scanning light ophthalmoscopic fluorescein angiography and offset pinhole imaging. Biomed Opt Express. 2014; 5(4):1173-89. https://doi.org/10.1364/BOE.5.001173.

https://doi.org/10.1364/BOE.5.001173

Burns SA, Elsner AE, Chui TY, Vannasdale DA Jr, Clark CA, Gast TJ, et al. In vivo adaptive optics microvascular imaging in diabetic patients without clinically severe diabetic retinopathy. Biomed Opt Express. 2014; 5(3):961-74. https://doi.org/10.1364/BOE.5.000961.

https://doi.org/10.1364/BOE.5.000961

Lombardo M, Parravano M, Serrao S, Ducoli P, Stirpe M, Lombardo G. Analysis of retinal capillaries in patients with type 1 diabetes and nonproliferative diabetic retinopathy using adaptive optics imaging. Retina. 2013; 33(8):1630-9. https://doi.org/10.1097/IAE.0b013e3182899326.

https://doi.org/10.1097/IAE.0b013e3182899326

Chen Y, Chen SDM, Chen FK. Branch retinal vein occlusion secondary to a retinal arteriolar macroaneurysm: a novel mechanism supported by multimodal imaging. Retin Cases Brief Rep. 2019; 13(1):10-14. https://doi.org/10.1097/ICB.0000000000000517.

https://doi.org/10.1097/ICB.0000000000000517

Paques M, Brolly A, Benesty J, Lermé N, Koch E, Rossant F, et al. Venous Nicking Without Arteriovenous Contact: The Role of the Arteriolar Microenvironment in Arteriovenous Nickings. JAMA Ophthalmol. 2015; 133(8):947-50. https://doi.org/10.1001/jamaophthalmol.2015.1132.

https://doi.org/10.1001/jamaophthalmol.2015.1132

Errera MH, Laguarrigue M, Rossant F, Koch E, Chaumette C, Fardeau C, et al. High-Resolution Imaging of Retinal Vasculitis by Flood Illumination Adaptive Optics Ophthalmoscopy: A Follow-up Study. Ocul Immunol Inflamm. 2020; 28(8):1171-1180. https://doi.org/10.1080/09273948.2019.1646773.

https://doi.org/10.1080/09273948.2019.1646773

Tan W, Yao X, Le TT, Tan B, Schmetterer L, Chua J. The New Era of Retinal Imaging in Hypertensive Patients. Asia Pac J Ophthalmol. 2022; 11(2):149-159. https://doi.org/10.1097/APO.0000000000000509.

https://doi.org/10.1097/APO.0000000000000509

Novais EA, Baumal CR, Sarraf D, Freund KB, Duker JS. Multimodal Imaging in Retinal Disease: A Consensus Definition. Ophthalmic Surg Lasers Imaging Retina. 2016; 47(3):201-5. doi: 10.3928/23258160-20160229-01.

https://doi.org/10.3928/23258160-20160229-01

Camino A, Zang P, Athwal A, Ni S, Jia Y, Huang D, Jian Y. Sensorless adaptive-optics optical coherence tomographic angiography. Biomed Opt Express. 2020; 11(7):3952-3967. doi: 10.1364/BOE.396829.

https://doi.org/10.1364/BOE.396829

Chui TYP, Mo S, Krawitz B, Menon NR, Choudhury N, Gan A, et al. Human retinal microvascular imaging using adaptive optics scanning light ophthalmoscopy. Int J Retina Vitreous. 2016; 2:11. doi: 10.1186/s40942-016-0037-8.

https://doi.org/10.1186/s40942-016-0037-8