Top

Graefe's Archive for Clinical and Experimental Ophthalmology

15-02-2025 | Vascular System Imaging | Review Article Free for a limited time

Coronary artery and retinal vascularization by optical coherence tomography angiography: are eyes the window to the heart?

Authors: Gustavo Sakuno, David Sarraf, SriniVas R. Sadda, Rony C. Preti, Breno P M Oliveira, Francisco Max Damico

Published in: Graefe's Archive for Clinical and Experimental Ophthalmology

Abstract

Purpose

Coronary artery disease (CAD) is the leading cause of death in the United States and its assessment still relies on invasive diagnostic procedures requiring contrast, such as coronary angiography (CAG) or computed tomography angiography (CCTA). The retinal vasculature is the only microvascular site in the human body that can be assessed non-invasively, and it has been described as a promising method for predicting cardiovascular risk since the classification of hypertensive retinopathy in the 19th century. Unfortunately, most classifications still rely on qualitative findings, which exhibit high rates of interobserver and intraobserver variability. With advances in ophthalmology exams, particularly the advent of optical coherence tomography angiography (OCTA), the capability of quantitatively assessing retinal vasculature can enable a more reliable non-invasive exam that could aid in estimating cardiovascular risk and assessing coronary lesions. This review aims to provide an extensive overview of the available evidence establishing the correlation of retinal and choroidal microvascular damage observed in OCTA and parameters such as coronary stenosis grade, number of affected vessels and scores like Gensini and SYNTAX evaluated via CAG or CCTA.

Methods

Review of the literature published until December 2024 on PubMed/MEDLINE, SCOPUS and EMBASE by searching “optical coherence tomography angiography” or “OCTA” AND “Coronary artery disease” or “Coronary heart disease”.

Results

Findings from sixteen studies suggest a potential correlation between vascular parameters in OCTA and results from coronary exams. Reductions in vessel density analysis of the retinal plexus, especially the superficial capillary plexus (SCP), could improve patient selection and diagnostic yield for more invasive diagnostic procedures, such as CAG and CCTA.

Conclusion

OCTA is a non-invasive technology that can provide visualization and quantification of retinal microvascular disfunction that may correlate with macrovascular disease, particularly in the coronary circulation. Longitudinal assessment of quantitative OCTA parameters may provide biomarkers for monitoring CAD patients over time.

Gunn RM Opthalmoscopic evidence of (1) arterial changes associated with chronic renal diseases and (2) of increased arterial tension. Trans Ophthalmol Soc UK 1892;12:124–125

Keith NM, Wagener HP, Barker NW (1939) Some different types of essential hypertension. Am J Med Sci 197:332–343. https://doi.org/10.1097/00000441-193903000-00006CrossRef

Breslin DJ (1966) Prognostic importance of ophthalmoscopic findings in essential hypertension. JAMA: J Am Med Assoc 195:335. https://doi.org/10.1001/jama.1966.03100050043015CrossRef

Dimmitt SB, Eames SM, Gosling P, West JNW, Gibson JM, Littler WA (1989) Usefulness of ophthalmoscopy in mild to moderate hypertension. Lancet 333:1103–1106. https://doi.org/10.1016/S0140-6736(89)92384-2CrossRef

Mancia G, Kreutz R, Brunström M, Burnier M, Grassi G, Januszewicz A et al (2023) 2023 ESH guidelines for the management of arterial hypertension the task force for the management of arterial hypertension of the European society of hypertension. J Hypertens 41:1874–2071. https://doi.org/10.1097/HJH.0000000000003480CrossRefPubMed

van den Born B-JH, Hulsman CAA, Hoekstra JBL, Schlingemann RO, van Montfrans GA (2005) Value of routine funduscopy in patients with hypertension: systematic review. BMJ 331:73. https://doi.org/10.1136/bmj.331.7508.73CrossRefPubMedPubMedCentral

Rudnicka AR, Welikala R, Barman S, Foster PJ, Luben R, Hayat S et al (2022) Artificial intelligence-enabled retinal vasculometry for prediction of circulatory mortality, myocardial infarction and stroke. Br J Ophthalmol 106:1722–1729. https://doi.org/10.1136/bjophthalmol-2022-321842CrossRefPubMed

Spaide RF, Fujimoto JG, Waheed NK, Sadda SR, Staurenghi G (2018) Optical coherence tomography angiography. Prog Retin Eye Res 64:1–55. https://doi.org/10.1016/j.preteyeres.2017.11.003CrossRefPubMed

Nemiroff J, Kuehlewein L, Rahimy E, Tsui I, Doshi R, Gaudric A et al (2016) Assessing deep retinal capillary ischemia in paracentral acute middle maculopathy by optical coherence tomography angiography. Am J Ophthalmol 162:121–132e1. https://doi.org/10.1016/j.ajo.2015.10.026CrossRefPubMed

10.

Bakhoum MF, Freund KB, Dolz-Marco R, Leong BCS, Baumal CR, Duker JS et al (2018) Paracentral acute middle maculopathy and the ischemic cascade associated with retinal vascular occlusion. Am J Ophthalmol 195:143–153. https://doi.org/10.1016/j.ajo.2018.07.031CrossRefPubMed

11.

Sarraf D, Rahimy E, Fawzi AA, Sohn E, Barbazetto I, Zacks DN et al (2013) Paracentral acute middle maculopathy a new variant of acute macular neuroretinopathy associated with retinal capillary ischemia. JAMA Ophthalmol 131:1275–1287. https://doi.org/10.1001/jamaophthalmol.2013.4056CrossRefPubMed

12.

Bousquet E, Santina A, Abraham N, Daily MJ, Sarraf D (2023) Detection of paracentral acute middle maculopathy can prevent blindness and death. Retina 43:1827–1832. https://doi.org/10.1097/IAE.0000000000003939CrossRefPubMed

13.

Long CP, Chan AX, Bakhoum CY, Toomey CB, Madala S, Garg AK et al Prevalence of subclinical retinal ischemia in patients with cardiovascular disease – a hypothesis driven study. EClinMed. https://doi.org/10.1016/j.eclinm.2021.100775

14.

Madala S, Adabifirouzjaei F, Lando L, Yarmohammadi A, Long CP, Bakhoum CY et al (2022) Retinal ischemic perivascular lesions, a biomarker of cardiovascular disease. Ophthalmol Retina 6:865–867. https://doi.org/10.1016/j.oret.2022.05.005

15.

Hanssen H, Streese L, Vilser W (2022) Retinal vessel diameters and function in cardiovascular risk and disease. Prog Retin Eye Res 91:101095. https://doi.org/10.1016/j.preteyeres.2022.101095CrossRefPubMed

16.

Gulati M, Levy PD, Mukherjee D, Amsterdam E, Bhatt DL, Birtcher KK et al (2021) AHA/ACC/ASE/CHEST/SAEM/SCCT/SCMR guideline for the evaluation and diagnosis of chest pain: a report of the American college of cardiology/American heart association joint committee on clinical practice guidelines. J Am Coll Cardiol 78:e187–285. https://doi.org/10.1016/j.jacc.2021.07.053CrossRefPubMed

17.

Duggan JP, Peters AS, Trachiotis GD, Antevil JL (2022) Epidemiology of coronary artery disease. Surg Clin North Am 102:499–516. https://doi.org/10.1016/j.suc.2022.01.007CrossRefPubMed

18.

Sulava EF, Johnson JC (2022) Management of coronary artery disease. Surg Clin North Am 102:449–464. https://doi.org/10.1016/j.suc.2022.01.005CrossRefPubMed

19.

Gensini GG (1983) A more meaningful scoring system for determining the severity of coronary heart disease. Am J Cardiol 51:606. https://doi.org/10.1016/S0002-9149(83)80105-2CrossRefPubMed

20.

Lawton JS, Tamis-Holland JE, Bangalore S, Bates ER, Beckie TM, Bischoff JM et al (2022) 2021 ACC/AHA/SCAI Guideline for coronary artery revascularization: a report of the American college of cardiology/American heart association joint committee on clinical practice guidelines. J Am Coll Cardiol 79:e21–129. https://doi.org/10.1016/j.jacc.2021.09.006CrossRefPubMed

21.

Marano R, Rovere G, Savino G, Flammia FC, Carafa MRP, Steri L et al (2020) CCTA in the diagnosis of coronary artery disease. Radiologia Med 125:1102–1113. https://doi.org/10.1007/s11547-020-01283-yCrossRef

22.

Abdelrahman KM, Chen MY, Dey AK, Virmani R, Finn AV, Khamis RY et al (2020) Coronary computed tomography angiography from clinical uses to emerging technologies: JACC State-of-the-art review. J Am Coll Cardiol 76:1226–1243. https://doi.org/10.1016/j.jacc.2020.06.076CrossRefPubMedPubMedCentral

23.

Lu MT, Meyersohn NM, Mayrhofer T, Bittner DO, Emami H, Puchner SB et al (2018) Central core laboratory versus site interpretation of coronary CT angiography: agreement and association with cardiovascular events in the PROMISE trial. Radiology 287:87–95. https://doi.org/10.1148/radiol.2017172181CrossRefPubMed

24.

Yu D-Y, Cringle SJ (2001) Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease. Prog Retin Eye Res 20:175–208. https://doi.org/10.1016/S1350-9462(00)00027-6CrossRefPubMed

25.

Hormel TT, Jia Y, Jian Y, Hwang TS, Bailey ST, Pennesi ME et al (2021) Plexus-specific retinal vascular anatomy and pathologies as seen by projection-resolved optical coherence tomographic angiography. Prog Retin Eye Res 80. https://doi.org/10.1016/j.preteyeres.2020.100878

26.

Cuenca N, Ortuño-Lizarán I, Sánchez-Sáez X, Kutsyr O, Albertos-Arranz H, Fernández-Sánchez L et al (2020) Interpretation of OCT and OCTA images from a histological approach: clinical and experimental implications. Prog Retin Eye Res 77:100828. https://doi.org/10.1016/j.preteyeres.2019.100828CrossRefPubMed

27.

Iwasaki M, Inomata H (1986) Relation between superficial capillaries and foveal structures in the human retina. Invest Ophthalmol Vis Sci :1698–1705

28.

Borrelli E, Sarraf D, Freund KB, Sadda SR (2018) OCT angiography and evaluation of the choroid and choroidal vascular disorders. Prog Retin Eye Res 67:30–55. https://doi.org/10.1016/j.preteyeres.2018.07.002CrossRefPubMed

29.

Kur J, Newman EA, Chan-Ling T (2012) Cellular and physiological mechanisms underlying blood flow regulation in the retina and choroid in health and disease. Prog Retin Eye Res 31:377–406. https://doi.org/10.1016/j.preteyeres.2012.04.004CrossRefPubMedPubMedCentral

30.

Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG, Chang W et al (1991) Optical coherence tomography. Science 254(5035):1178–1181. https://doi.org/10.1126/science.1957169CrossRefPubMedPubMedCentral

31.

Drexler W, Fujimoto JG (2008) State-of-the-art retinal optical coherence tomography. Prog Retin Eye Res 27:45–88. https://doi.org/10.1016/j.preteyeres.2007.07.005CrossRefPubMed

32.

Laíns I, Wang JC, Cui Y, Katz R, Vingopoulos F, Staurenghi G et al (2021) Retinal applications of swept source optical coherence tomography (OCT) and optical coherence tomography angiography (OCTA). Prog Retin Eye Res 84:100951. https://doi.org/10.1016/j.preteyeres.2021.100951CrossRefPubMed

33.

Lu Y, Wang JC, Cui Y, Zhu Y, Zeng R, Lu ES et al (2021) A quantitative comparison of four optical coherence tomography angiography devices in healthy eyes. Graefe’s Arch Clin Exp Ophthalmol 259:1493–1501. https://doi.org/10.1007/s00417-020-04945-9CrossRef

34.

Mehta N, Liu K, Alibhai AY, Gendelman I, Braun PX, Ishibazawa A et al (2019) Impact of binarization thresholding and brightness/contrast adjustment methodology on optical coherence tomography angiography image quantification. Am J Ophthalmol 205:54–65. https://doi.org/10.1016/j.ajo.2019.03.008CrossRefPubMed

35.

Arrigo A, Aragona E, Battaglia Parodi M, Bandello F (2023) Quantitative approaches in multimodal fundus imaging: state of the art and future perspectives. Prog Retin Eye Res 92:101111. https://doi.org/10.1016/j.preteyeres.2022.101111CrossRefPubMed

36.

Linderman RE, Muthiah MN, Omoba SB, Litts KM, Tarima S, Visotcky A et al Variability of foveal avascular zone metrics derived from optical coherence tomography angiography images. Transl Vis Sci Technol 2018;7. https://doi.org/10.1167/tvst.7.5.20

37.

Piao H, Guo Y, Zhang H, Sung MS, Park SW (2021) Acircularity and circularity indexes of the foveal avascular zone in high myopia. Sci Rep 11. https://doi.org/10.1038/s41598-021-96304-9

38.

Greig EC, Duker JS, Waheed NK (2020) A practical guide to optical coherence tomography angiography interpretation. Int J Retina Vitreous 6. https://doi.org/10.1186/s40942-020-00262-9

39.

Saha PK, Jin D, Liu Y, Christensen GE, Chen C (2018) Fuzzy object skeletonization: theory, algorithms, and applications. IEEE Trans Vis Comput Graph 24:2298–2314. https://doi.org/10.1109/TVCG.2017.2738023CrossRefPubMed

40.

Wang JJ, Liew G, Wong TY, Smith W, Klein R, Leeder SR et al (2006) Retinal vascular calibre and the risk of coronary heart disease-related death. Heart 92:1583–1587. https://doi.org/10.1136/hrt.2006.090522CrossRefPubMedPubMedCentral

41.

Wong TY, Klein R, Richey Sharrett MA, Duncan BB, Couper DJ, Tielsch JM et al (2002) Retinal arteriolar narrowing and risk of coronary heart disease in men and women the atherosclerosis risk in communities study. JAMA 287:1153–1159. https://doi.org/10.1001/jama.287.9.1153

42.

McGeechan K (2009) Meta-analysis: retinal vessel caliber and risk for coronary heart disease. Ann Intern Med 151:404. https://doi.org/10.7326/0003-4819-151-6-200909150-00005CrossRefPubMedPubMedCentral

43.

Bakhoum CY, Madala S, Lando L, Yarmohammadi A, Long CP, Miguez S et al (2023) Retinal ischemic perivascular lesions in individuals with Atrial Fibrillation. J Am Heart Assoc 12. https://doi.org/10.1161/JAHA.122.028853

44.

Bousquet E, Santina A, Au A, Somisetty S, Abraham N, Voichanski S et al (2024) Retinal ischemic perivascular lesions are associated with myocardial infarction in patients with coronary artery disease. Am J Ophthalmol 264:224–228. https://doi.org/10.1016/j.ajo.2024.03.017CrossRefPubMed

45.

Seecheran NA, Rafeeq S, Maharaj N, Swarath S, Seecheran V, Seecheran R et al (2023) Correlation of RETINAL artery diameter with coronary artery disease: the RETINA CAD pilot study—are the eyes the windows to the heart? Cardiol Ther 12:499–509. https://doi.org/10.1007/s40119-023-00320-xCrossRefPubMedPubMedCentral

46.

Arnould L, Guenancia C, Azemar A, Alan G, Pitois S, Bichat F et al (2018) The EYE-MI pilot study: a prospective acute coronary syndrome cohort evaluated with retinal optical coherence tomography angiography. Invest Ophthalmol Vis Sci 59:4299–4306. https://doi.org/10.1167/iovs.18-24090CrossRefPubMed

47.

Goff DC, Lloyd-Jones DM, Bennett G, Coady S, D’Agostino RB, Gibbons R et al (2014) 2013 ACC/AHA guideline on the assessment of cardiovascular risk. Circulation 129:S49-73. https://doi.org/10.1161/01.cir.0000437741.48606.98CrossRefPubMed

48.

Fox KAA, Dabbous OH, Goldberg RJ, Pieper KS, Eagle KA, Van De Werf F et al (2006) Prediction of risk of death and myocardial infarction in the six months after presentation with acute coronary syndrome: prospective multinational observational study (GRACE). Br Med J 333:1091–1094. https://doi.org/10.1136/bmj.38985.646481.55CrossRef

49.

Wilson PWF, D’Agostino R, Bhatt DL, Eagle K, Pencina MJ, Smith SC et al (2012) An international model to predict recurrent cardiovascular disease. Am J Med 125:695-703e1. https://doi.org/10.1016/j.amjmed.2012.01.014CrossRefPubMed

50.

Ren Y, Hu Y, Li C, Zhong P, Liu H, Wang H et al (2023) Impaired retinal microcirculation in patients with non-obstructive coronary artery disease. Microvasc Res 148:104533. https://doi.org/10.1016/j.mvr.2023.104533CrossRefPubMed

51.

Zhong P, Hu Y, Jiang L, Peng Q, Huang M, Li C et al (2021) Retinal microvasculature changes in patients with coronary total occlusion on optical coherence tomography angiography. Front Med (Lausanne) 8:1–8. https://doi.org/10.3389/fmed.2021.708491CrossRef

52.

Zhong P, Li Z, Lin Y, Peng Q, Huang M, Jiang L et al (2022) Retinal microvasculature impairments in patients with coronary artery disease: an optical coherence tomography angiography study. Acta Ophthalmol 100:225–233. https://doi.org/10.1111/aos.14806CrossRefPubMed

53.

Matulevičiūtė I, Sidaraitė A, Tatarūnas V, Veikutienė A, Dobilienė O, Žaliūnienė D (2022) Retinal and choroidal thinning—A. Predictor coron artery occlusion? Diagnostics 12:2016. https://doi.org/10.3390/diagnostics12082016CrossRefPubMedPubMedCentral

54.

Sideri A-M, Kanakis M, Katsimpris A, Karamaounas A, Brouzas D, Petrou P et al (2023) Correlation between coronary and retinal microangiopathy in patients with STEMI. Transl Vis Sci Technol 12:8. https://doi.org/10.1167/tvst.12.5.8CrossRefPubMedPubMedCentral

55.

Wang J, Jiang J, Zhang Y, Qian YW, Zhang JF, Wang ZL (2019) Retinal and choroidal vascular changes in coronary heart disease: an optical coherence tomography angiography study. Biomed Opt Express 10:1532. https://doi.org/10.1364/boe.10.001532CrossRefPubMedPubMedCentral

56.

Zong D, Xi H, Ni Y, Liang T, Li M, Zhou J et al (2024) SS-OCTA assessment of fundus microvascular changes and their correlation with coronary lesion severity in severe coronary heart disease. Sci Rep 14. https://doi.org/10.1038/s41598-024-83467-4

57.

Agca FV, Sensoy B, Aslanci ME, Ulutas HG, Gunes A (2023) Retinal microvascular changes in patients with coronary artery disease and apnea. Microvasc Res 148. https://doi.org/10.1016/j.mvr.2023.104514

58.

Aschauer J, Aschauer S, Pollreisz A, Datlinger F, Gatterer C, Mylonas G et al (2021) Identification of subclinical microvascular biomarkers in coronary heart disease in retinal imaging. Transl Vis Sci Technol 10. https://doi.org/10.1167/tvst.10.13.24

59.

Ay İE, Dural İE, Er A, Doğan M, Gobeka HH, Yilmaz ÖF (2023) Is it useful to do OCTA in coronary artery disease patients to improve SYNTAX-based cardiac revascularization decision? Photodiagnosis Photodyn Ther 42. https://doi.org/10.1016/j.pdpdt.2023.103540

60.

Sun MT, Huang S, Chan WO, Craig JE, Knight LSW, Sanders P et al (2021) Impact of cardiometabolic factors on retinal vasculature: A 3 × 3, 6 × 6 and 8 × 8-mm ocular coherence tomography angiography study. Clin Exp Ophthalmol 49:260–269. https://doi.org/10.1111/ceo.13913CrossRefPubMed

61.

Jeremic N, Pawloff M, Lachinov D, Rokitansky S, Hasun M, Weidinger F et al (2024) Severity stratification of coronary artery disease using novel inner ellipse-based foveal avascular zone biomarkers. Invest Ophthalmol Vis Sci 65:15. https://doi.org/10.1167/iovs.65.12.15CrossRefPubMedPubMedCentral

62.

Kim DS, Kim BS, Cho H, Shin J-H, Shin YU (2022) Associations between choriocapillaris flow on optical coherence tomography angiography and cardiovascular risk profiles of patients with acute myocardial infarction. J Pers Med 12:839. https://doi.org/10.3390/jpm12050839CrossRefPubMedPubMedCentral

63.

Arnett DK, Blumenthal RS, Albert MA, Buroker AB, Goldberger ZD, Hahn EJ et al (2019) 2019 ACC/AHA guideline on the primary prevention of cardiovascular disease: a report of the American college of cardiology/American heart association task force on clinical practice guidelines. Circulation 140:e596-646. https://doi.org/10.1161/CIR.0000000000000678CrossRefPubMedPubMedCentral

64.

Antman EM, Cohen M, Bernink PJLM, McCabe CH, Horacek T, Papuchis G et al (2000) The TIMI risk score for unstable Angina/Non–ST Elevation MI. JAMA 284:835. https://doi.org/10.1001/jama.284.7.835CrossRefPubMed

65.

Zheng Z, Liu J, Sun J, Zhang Y, Gu X, Song S et al (2024) Quantitative analysis of three-dimensional choroidal changes in coronary artery disease patients with swept-source optical coherence tomography angiography. Photodiagnosis Photodyn Ther 50. https://doi.org/10.1016/j.pdpdt.2024.104366

66.

Zhong P, Qin J, Li Z, Jiang L, Peng Q, Huang M et al (2022) Development and validation of retinal vasculature nomogram in suspected angina due to coronary artery disease. J Atheroscler Thromb 29:579–596. https://doi.org/10.5551/jat.62059CrossRefPubMed

67.

Stone PH, Libby P, Boden WE (2023) Fundamental pathobiology of coronary atherosclerosis and clinical implications for chronic ischemic heart disease management - the plaque hypothesis: a narrative review. JAMA Cardiol 8:192–201. https://doi.org/10.1001/jamacardio.2022.3926CrossRefPubMedPubMedCentral

68.

McClintic BR, McClintic JI, Bisognano JD, Block RC (2010) The relationship between retinal microvascular abnormalities and coronary heart disease: a review. Am J Med 123. https://doi.org/10.1016/j.amjmed.2009.05.030

69.

Rizzoni D, Mengozzi A, Masi S, Rosei CA, De Ciuceis C, Virdis A (2022) New noninvasive methods to evaluate microvascular structure and function. Hypertension 79:874–886. https://doi.org/10.1161/HYPERTENSIONAHA.121.17954CrossRefPubMed

70.

Wagner SK, Fu DJ, Faes L, Liu X, Huemer J, Khalid H et al Insights into systemic disease through retinal imaging-based oculomics. Transl Vis Sci Technol 2020;9. https://doi.org/10.1167/tvst.9.2.6

71.

Wu JH, Liu TYA (2023) Application of deep learning to retinal-image-based oculomics for evaluation of systemic health: a review. J Clin Med 12. https://doi.org/10.3390/jcm12010152

72.

Vaidya K, Tucker B, Patel S, Ng MKC (2021) Acute coronary syndromes (Acs)—unravelling biology to identify new therapies—the microcirculation as a frontier for new therapies in acs. Cells 10. https://doi.org/10.3390/cells10092188

Title: Coronary artery and retinal vascularization by optical coherence tomography angiography: are eyes the window to the heart?
Authors: Gustavo Sakuno
David Sarraf
SriniVas R. Sadda
Rony C. Preti
Breno P M Oliveira
Francisco Max Damico
Publication date: 15-02-2025
Publisher: Springer Berlin Heidelberg
Keywords: Vascular System Imaging
Diagnostics in Ophthalmology
Cardiac Diagnostics
Eye Examinations
Angiography
General Diseases with Eye Involvement
Coronary Heart Disease
Circulatory Disease
Retinal Diseases
Cardiovascular Disease in General Practice
Diagnostics in Cardiology
Circulatory Disease
Published in: Graefe's Archive for Clinical and Experimental Ophthalmology
Print ISSN: 0721-832X
Electronic ISSN: 1435-702X
DOI: https://doi.org/10.1007/s00417-025-06769-x

Podcast | Sexual health in older age

Springer Medicine

Coronary artery and retinal vascularization by optical coherence tomography angiography: are eyes the window to the heart?

Abstract

Purpose

Methods

Results

Conclusion

Podcast | Sexual health in older age

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusion

Please log in to get access to this content