Abstract
Aims
To perform an automated functional assessment of retinal and choroidal microvasculature in eyes with low-grade diabetic retinopathy (DR) using optical coherence tomography angiography (OCT-A) and to identify potential perfusion changes in case of early vascular damage.
Methods
This is an observational, case–control study of consecutive diabetic patients with level 20 DR severity scale score and age-matched healthy subjects. A prototypal OCT-angiography was used to obtain the OCT-angiograms of the superficial capillary plexus (SCP), deep capillary plexus (DCP) and choriocapillaris (CC) layer. A validated automated microstructural analysis provided data on SCP, DCP and CC vascular perfusion density (VPD). A comparative assessment between different vascular layers and different groups was performed.
Results
Twenty-nine diabetic patients (7 females, 24%) and 20 healthy controls were enrolled. VPD values were significantly lower in the DCP (25.1% vs. 26.5%; p = 0.04) and CC (71.2% vs. 86.6%; p = 0.0001) of diabetic patients compared with controls. A statistically significant negative linear correlation was reported between CC VPD and DCP VPD in diabetic patients; at the reverse, a positive linear correlation between the same parameters was noticed in controls.
Conclusion
Retinal and choroidal vascular networks, although distinct entities, seem functionally interconnected: varying the degree of perfusion may be a mutual compensatory mechanism in response to an ischemic injury.
Similar content being viewed by others
References
Klein R, Klein BE, Moss SE et al (1994) The Wisconsin epidemiologic study of diabetic retinopathy. XIV. Ten-year incidence and progression of diabetic retinopathy. Arch Ophthalmol 112:1217–1228
Engerman RL, Kern TS (1995) Retinopathy in animal models of diabetes. Diabetes Metab Rev 11:109–120
Hammes HP, Lin JH, Renner O et al (2002) Pericytes and the pathogenesis of diabetic retinopathy. Diabetes 51:3107–3112
Hidayat A, Fine B (1985) Diabetic choroidopathy: light and electron microscopic observations of seven cases. Ophthalmology 67:512–522
Lutty GA (2017) Diabetic choroidopathy. Vision Res 139:161–167
Cao J, McLeod DS, Merges CA, Lutty GA (1998) Choriocapillaris degeneration and related pathologic changes in human diabetic eyes. Arch Ophthalmol 116:589–597
Weinberger D, Kramer M, Priel E et al (1998) Indocyanine green angiographic findings in nonproliferative diabetic retinopathy. Am J Ophthalmol 126:238–247
Shiragami C, Shiraga F, Matsuo T et al (2002) Risk factors for diabetic choroidopathy in patients with diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 240(6):436–442
Hua R, Liu L, Wang X, Chen L (2013) Imaging evidence of diabetic choroidopathy in vivo: angiographic pathoanatomy and choroidal-enhanced depth imaging. PLoS ONE 8(12):e83494
Coscas G, Lupidi M, Coscas F (2017) Optical coherence tomography angiography in diabetic maculopathy. Dev Ophthalmol 60:38–49
Ishibazawa A, Nagaoka T, Takahashi A et al (2015) Optical coherence tomography angiography in diabetic retinopathy: a prospective pilot study. Am J Ophthalmol 160:35–44
Coscas G, Lupidi M, Coscas F, Chhablani J, Cagini C (2018) Optical coherence tomography angiography in healthy subjects and diabetic patients. Ophthalmologica 239(2–3):61–73
Lupidi M, Coscas G, Coscas F et al (2017) Retinal microvasculature in non-proliferative diabetic retinopathy: automated quantitative optical coherence tomography angiography assessment. Ophthalmic Res 58(3):131–141
Choi W, Waheed NK, Moult EM et al (2017) Ultrahigh speed swept source optical coherence tomography angiography of retinal and choriocapillaris alterations in diabetic patients with and without retinopathy. Retina 37(1):11–21
Carnevali A, Sacconi R, Corbelli E et al (2017) Optical coherence tomography angiography analysis of retinal vascular plexuses and choriocapillaris in patients with type 1 diabetes without diabetic retinopathy. Acta Diabetol 54(7):695–702
Early Treatment Diabetic Retinopathy Study (ETDRS) Research Group (1991) Grading diabetic retinopathy from stereoscopic color fundus photographs and extension of the modified Airlie house classification. ETDRS report number 10. Ophthalmology 98(5 suppl):786–806
Aiello LP, Beck RW, Bressler NM et al (2011) Rationale for the diabetic retinopathy clinical research network treatment protocol for center-involved diabetic macular edema. Ophthalmology 118(12):e5–e14
Cardillo Piccolino F, Lupidi M, Cagini C et al (2018) Choroidal vascular reactivity in central serous chorioretinopathy. Invest Ophthalmol Vis Sci 59:3897–3905
Freund KB, Sarraf D, Leong BCS et al (2018) Association of optical coherence tomography angiography of collaterals in retinal vein occlusion with major venous outflow through the deep vascular complex. JAMA Ophthalmol 136(11):1262–1270
Vujosevic S, Martini F, Cavarzeran F, Pilotto E, Midena E (2012) Macular and peripapillary choroidal thickness in diabetic patients. Retina 32(9):1781–1790
Querques G, Lattanzio R, Querques L et al (2012) Enhanced depth imaging optical coherence tomography in type 2 diabetes. Invest Ophthalmol Vis Sci 53(10):6017
Nesper PL, Roberts PK, Onishi AC et al (2017) Quantifying microvascular abnormalities with increasing severity of diabetic retinopathy using optical coherence tomography angiography. Invest Ophthalmol Vis Sci 58:BIO307–BIO315
Scarinci F, Nesper PL, Fawzi AA (2016) Deep retinal capillary nonperfusion is associated with photoreceptor disruption in diabetic macular ischemia. Am J Ophthalmol 168:129–138
Birol G, Wang S, Budzynski E et al (2007) Oxygen distribution and consumption in the macaque retina. Am J Physiol Heart Circ Physiol 293(3):H1696–H1704
Borrelli E, Palmieri M, Viggiano P et al (2019) Photoreceptor damage in diabetic choroidopathy. Retina. https://doi.org/10.1097/IAE.0000000000002538
Yi J, Liu W, Chen S et al (2015) Visible light optical coherence tomography measures retinal oxygen metabolic response to systemic oxygenation. Light Sci Appl 4:e334
Funding
This study was supported by Fondazione per la Macula Onlus, Genova, Italy, and Fondazione Ferrero, Alba, Italy.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standards
This study was conducted in accordance with the Declaration of Helsinki after approval by the Perugia Institutional Ethics Committee (IEC).
Informed consent
Written informed consent was obtained from all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article belongs to the topical collection Eye Complications of Diabetes, managed by Giuseppe Querques.
Rights and permissions
About this article
Cite this article
Lupidi, M., Cerquaglia, A., Gujar, R. et al. Functional correlation between choroidal and retinal vascularity in low-grade diabetic retinopathy. Acta Diabetol 57, 983–990 (2020). https://doi.org/10.1007/s00592-020-01507-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00592-020-01507-7