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Structure–function associations between contrast sensitivity and widefield swept–source optical coherence tomography angiography in diabetic macular edema

  • Retinal Disorders
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Abstract

Purpose

To evaluate the relationship between contrast sensitivity (CS) and widefield swept–source optical coherence tomography angiography (WF SS-OCTA) vascular metrics in diabetic macular edema (DME) was the purpose.

Methods

This prospectively enrolled cross-sectional observational study included 61 eyes of 48 patients that were tested with the quantitative CS function (qCSF) test on the same day as imaging with WF SS-OCTA (PLEX® Elite 9000, Carl Zeiss Meditec) 3 × 3, 6 × 6, and 12 × 12 mm scans. Outcomes included visual acuity (VA) and multiple qCSF metrics. Vascular metrics included vessel density (VD) and vessel skeletonized density (VSD) in the superficial (SCP) and deep capillary plexus (DCP) and whole retina (WR) and foveal avascular zone (FAZ) parameters. Mixed effects multivariable linear regression models controlling for age, lens status, and diabetic retinopathy stage were performed. Standardized beta coefficients were calculated by refitting the standardized data.

Results

SS-OCTA metrics had a significant association with CS and VA. The effect size of OCTA metrics was larger on CS compared to VA. For example, the standardized beta coefficients for VSD and CS at 3 cpd (βSCP = 0.76, βDCP = 0.71, βWR = 0.72, p < 0.001) were larger than those for VA (βSCP =  − 0.55, p < 0.001; βDCP =  − 0.43, p = 0.004; βWR =  − 0.50, p < 0.001). On 6 × 6 mm images, AULCSF, CS at 3 cpd, and CS at 6 cpd were significantly associated with VD and VSD in all three slab types (SCP, DCP, and WR), while VA was not.

Conclusion

Structure–function associations in patients with DME leveraging the qCSF device suggest microvascular changes on WF SS-OCTA are associated with larger changes in contrast sensitivity than VA.

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Data availability

Data are available upon reasonable request. Deidentified participant data, protocols, and statistical analysis are available from the corresponding author (ORCID ID: 0000–0003-0109–9738).

References

  1. Lee R, Wong TY, Sabanayagam C (2015) Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss. Eye Vision 2:1–25

    Article  Google Scholar 

  2. Ting DSW, Cheung GCM, Wong TY (2016) Diabetic retinopathy: global prevalence, major risk factors, screening practices and public health challenges: a review. Clin Exp Ophthalmol 44:260–277

    Article  PubMed  Google Scholar 

  3. Vingopoulos F, Wai KM, Katz R, Vavvas DG, Kim LA, Miller JB (2021) Measuring the contrast sensitivity function in non-neovascular and neovascular age-related macular degeneration: the quantitative contrast sensitivity function test. J Clin Med 10 https://doi.org/10.3390/jcm10132768

  4. Sokol S, Moskowitz A, Skarf B, Evans R, Molitch M, Senior B (1985) Contrast sensitivity in diabetics with and without background retinopathy. Arch Ophthalmol 103:51–54. https://doi.org/10.1001/archopht.1985.01050010055018

    Article  CAS  PubMed  Google Scholar 

  5. Pondorfer SG, Terheyden JH, Heinemann M, Wintergerst MWM, Holz FG, Finger RP (2019) Association of vision-related quality of life with visual function in age-related macular degeneration. Sci Rep 9:15326. https://doi.org/10.1038/s41598-019-51769-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Preti RC, Ramirez LM, Monteiro ML, Carra MK, Pelayes DE, Takahashi WY (2013) Contrast sensitivity evaluation in high risk proliferative diabetic retinopathy treated with panretinal photocoagulation associated or not with intravitreal bevacizumab injections: a randomised clinical trial. Br J Ophthalmol 97:885–889. https://doi.org/10.1136/bjophthalmol-2012-302675

    Article  PubMed  Google Scholar 

  7. Murugappan M, Vayalil J, Bade A, Bittner AK (2016) Reliability of quick contrast sensitivity function testing in adults without ocular disease and patients with retinitis pigmentosa. Invest Ophthalmol Vis Sci 57:616–616

    Google Scholar 

  8. Pearce E, Sivaprasad S, Chong NV (2014) Factors affecting reading speed in patients with diabetic macular edema treated with laser photocoagulation. PLoS ONE 9:105696. https://doi.org/10.1371/journal.pone.0105696

    Article  CAS  Google Scholar 

  9. Okamoto Y, Okamoto F, Hiraoka T, Oshika T (2014) Vision-related quality of life and visual function following intravitreal bevacizumab injection for persistent diabetic macular edema after vitrectomy. Jpn J Ophthalmol 58:369–374. https://doi.org/10.1007/s10384-014-0323-7

    Article  CAS  PubMed  Google Scholar 

  10. Farahvash MS, Mahmoudi AH, Farahvash MM, Tabatabaee A, Riazi M, Mohammadzadeh S, Faghihi H, Nilli-Ahmadabadi M, Mirshahi A, Karkhaneh R, Aalami-Harandi Z, Javadian A, Abdolahi A, Lashey A (2008) The impact of macular laser photocoagulation on contrast sensitivity function in patients with clinically significant macular edema. Arch Iran Med 11:143–147

    PubMed  Google Scholar 

  11. Nixon DR, Flinn NA (2018) Evaluation of contrast sensitivity and other visual function outcomes in diabetic macular edema patients following treatment switch to aflibercept from ranibizumab. Clin Ophthalmol 12:191–197. https://doi.org/10.2147/opth.S158268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Beaulieu WT, Glassman AR, Baker CW, Maguire MG, Johnson CA, Melia M, Sun JK (2021) Effect of initial aflibercept, laser, or observation on low-contrast visual acuity in eyes with diabetic macular edema and good vision: ancillary study within a randomized clinical trial. Transl Vis Sci Technol 10:3. https://doi.org/10.1167/tvst.10.3.3

    Article  PubMed  PubMed Central  Google Scholar 

  13. Pelli DG, Robson JG, Wilkins AJ (1988) The design of a new letter chart for measuring contrast sensitivity. Clin Vis Sci 2:187–199

    Google Scholar 

  14. Rubin G (1988) Reliability and sensitivity of clinical contrast sensitivity tests. Clin Vision Sci 2:169–177

    Google Scholar 

  15. Wang J, Cui Y, Vingopoulos F, Kasetty M, Silverman RF, Katz R, Kim L, Miller JB (2020) Disorganisation of retinal inner layers is associated with reduced contrast sensitivity in retinal vein occlusion. Br J Ophthalmol. https://doi.org/10.1136/bjophthalmol-2020-317615

    Article  PubMed  Google Scholar 

  16. Thomas M, Silverman RF, Vingopoulos F, Kasetty M, Yu G, Kim EL, Omari AA, Joltikov KA, Choi EY, Kim LA, Zacks DN, Miller JB (2021) Active learning of contrast sensitivity to assess visual function in macula-off retinal detachment. J VitreoRetinal Dis 5:313–320. https://doi.org/10.1177/2474126420961957

    Article  Google Scholar 

  17. Joltikov KA, Sesi CA, de Castro VM, Davila JR, Anand R, Khan SM, Farbman N, Jackson GR, Johnson CA, Gardner TW (2018) Disorganization of retinal inner layers (DRIL) and neuroretinal dysfunction in early diabetic retinopathy. Invest Ophthalmol Vis Sci 59:5481–5486. https://doi.org/10.1167/iovs.18-24955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Laíns I, Wang JC, Cui Y, Katz R, Vingopoulos F, Staurenghi G, Vavvas DG, Miller JW, Miller JB (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.2021.100951

    Article  PubMed  Google Scholar 

  19. AttaAllah HR, Mohamed AAM, Ali MA (2019) Macular vessels density in diabetic retinopathy: quantitative assessment using optical coherence tomography angiography. Int Ophthalmol 39:1845–1859. https://doi.org/10.1007/s10792-018-1013-0

    Article  PubMed  Google Scholar 

  20. Tang FY, Chan EO, Sun Z, Wong R, Lok J, Szeto S, Chan JC, Lam A, Tham CC, Ng DS, Cheung CY (2020) Clinically relevant factors associated with quantitative optical coherence tomography angiography metrics in deep capillary plexus in patients with diabetes. Eye Vis 7:7. https://doi.org/10.1186/s40662-019-0173-y

    Article  Google Scholar 

  21. (1991) Grading diabetic retinopathy from stereoscopic color fundus photographs--an extension of the modified Airlie House classification. ETDRS report number 10. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology 98(5 Suppl):786–806

  22. Grover S, Murthy RK, Brar VS, Chalam KV (2009) Normative data for macular thickness by high-definition spectral-domain optical coherence tomography (spectralis). Am J Ophthalmol 148:266–271. https://doi.org/10.1016/j.ajo.2009.03.006

    Article  PubMed  Google Scholar 

  23. Chalam KV, Bressler SB, Edwards AR, Berger BB, Bressler NM, Glassman AR, Grover S, Gupta SK, Nielsen JS (2012) Retinal thickness in people with diabetes and minimal or no diabetic retinopathy: Heidelberg Spectralis optical coherence tomography. Invest Ophthalmol Vis Sci 53:8154–8161. https://doi.org/10.1167/iovs.12-10290

    Article  PubMed  PubMed Central  Google Scholar 

  24. Lesmes LA, Lu Z-L, Baek J, Albright TD (2010) Bayesian adaptive estimation of the contrast sensitivity function: the quick CSF method. J Vis 10:17–17

    Article  Google Scholar 

  25. Busch C, Wakabayashi T, Sato T, Fukushima Y, Hara C, Shiraki N, Winegarner A, Nishida K, Sakaguchi H, Nishida K (2019) Retinal microvasculature and visual acuity after intravitreal aflibercept in diabetic macular edema: an optical coherence tomography angiography study. Sci Rep 9:1561. https://doi.org/10.1038/s41598-018-38248-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Balaratnasingam C, Inoue M, Ahn S, McCann J, Dhrami-Gavazi E, Yannuzzi LA, Freund KB (2016) Visual acuity is correlated with the area of the foveal avascular zone in diabetic retinopathy and retinal vein occlusion. Ophthalmol 123:2352–2367. https://doi.org/10.1016/j.ophtha.2016.07.008

    Article  Google Scholar 

  27. McAnany JJ, Park JC, Liu K, Liu M, Chen YF, Chau FY, Lim JI (2020) Contrast sensitivity is associated with outer-retina thickness in early-stage diabetic retinopathy. Acta Ophthalmol 98:e224–e231. https://doi.org/10.1111/aos.14241

    Article  PubMed  Google Scholar 

  28. Srinivasan S, Sobha S, Rajalakshmi R, Anjana RM, Malik RA, Kulothungan V, Raman R, Muna B (2021) Retinal structure-function correlation in type 2 diabetes. Eye.https://doi.org/10.1038/s41433-021-01761-1

  29. Montesano G, Ometto G, Higgins BE, Das R, Graham KW, Chakravarthy U, McGuiness B, Young IS, Kee F, Wright DM, Crabb DP, Hogg RE (2021) Evidence for structural and functional damage of the inner retina in diabetes with no diabetic retinopathy. Invest Ophthalmol Vis Sci 62:35. https://doi.org/10.1167/iovs.62.3.35

    Article  PubMed  PubMed Central  Google Scholar 

  30. Joltikov KA, de Castro VM, Davila JR, Anand R, Khan SM, Farbman N, Jackson GR, Johnson CA, Gardner TW (2017) Multidimensional functional and structural evaluation reveals neuroretinal impairment in early diabetic retinopathy. Invest Ophthalmol Vis Sci 58:BIO277. https://doi.org/10.1167/iovs.17-21863

    Article  PubMed  PubMed Central  Google Scholar 

  31. Arend O, Remky A, Evans D, Stüber R, Harris A (1997) Contrast sensitivity loss is coupled with capillary dropout in patients with diabetess. Invest Ophthalmol Vis Sci 38:1819–1824

    CAS  PubMed  Google Scholar 

  32. Vingopoulos F, Baldwin G, Katz R, Garg I, Cui Y, Moon JY, Patel NA, Wu DM, Husain D, Miller JW, Kim LA, Vavvas DG, Miller JB (2022) Structure-function associations between contrast sensitivity (CS) and vascular metrics on wide field swept source optical coherence tomography angiography (WF SS OCTA) across stages of diabetic retinopathy. Invest Ophthalmol Vis Sci 63:2206–269

    Google Scholar 

  33. Nixon DR, Flinn N (2021) Visual function for driving in diabetic macular edema and retinal vein occlusion post-stabilization with anti-vascular endothelial growth factor. Clin Ophthalmol 15:1659–1666. https://doi.org/10.2147/opth.S304229

    Article  PubMed  PubMed Central  Google Scholar 

  34. Reynaud A, Hess RF (2017) Characterization of spatial frequency channels underlying disparity sensitivity by factor analysis of population data. Frontiers in Computational Neuroscience 11 https://doi.org/10.3389/fncom.2017.00063

  35. Lupión Durán T, García-Ben A, Rodríguez Méndez V, Gálvez Alcázar L, García-Ben E, García-Campos JM (2021) Study of visual acuity and contrast sensitivity in diabetic patients with and without non-proliferative diabetic retinopathy. Int Ophthalmolhttps://doi.org/10.1007/s10792-021-01930-x

  36. Nixon DR, Flinn N, Enderlein C (2021) Contrast sensitivity changes in center involving diabetic macular edema treated with aflibercept. Clin Ophthalmol 15:4439–4445. https://doi.org/10.2147/opth.S338478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Sun JK, Glassman AR, Jampol LM (2022) Managing center-involved diabetic macular edema with good visual acuity. JAMA Ophthalmol 140:95–96. https://doi.org/10.1001/jamaophthalmol.2021.4664

    Article  PubMed  Google Scholar 

  38. Adamsons I, Rubin GS, Vitale S, Taylor HR, Stark WJ (1992) The effect of early cataracts on glare and contrast sensitivity: a pilot study. Arch Ophthalmol 110:1081–1086. https://doi.org/10.1001/archopht.1992.01080200061025

    Article  CAS  PubMed  Google Scholar 

  39. Vingopoulos F, Kasetty M, Garg I, Silverman RF, Katz R, Vasan RA, Lorch AC, Luo ZK, Miller JB (2022) Active learning to characterize the full contrast sensitivity function in cataracts. Clin Ophthalmol 16:3109–3118. https://doi.org/10.2147/OPTH.S367490

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors would like to thank all the staff for their help and assistance in research and patient recruitment from retina clinics at Massachusetts Eye and Ear, and Yan Zhao for her help with statistical analysis.

Funding

Lions International Fund (Grant 530125 and 530869).

Author information

Authors and Affiliations

  1. Harvard Retinal Imaging Lab, Boston, MA, USA

    Grace Baldwin, Filippos Vingopoulos, Itika Garg, Jade Y. Moon, Rebecca Zeng, Ying Cui, Raviv Katz, Rongrong Le, Edward S. Lu, Diane N. Sayah, Zakariyya Hassan & John B. Miller

  2. Retina Service, Massachusetts Eye and Ear, 243 Charles St, Boston, MA, 02114, USA

    Grace Baldwin, Filippos Vingopoulos, Itika Garg, Jade Y. Moon, Rebecca Zeng, Edward S. Lu, Diane N. Sayah, Leo A. Kim, Deeba Husain & John B. Miller

  3. Guangdong Eye Institute, Department of Ophthalmology, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou, China

    Ying Cui

  4. Wenzhou Medical University Affiliated Eye Hospital, Wenzhou Medical University, Wenzhou, Zhejiang, People’s Republic of China

    Rongrong Le

  5. Schepens Eye Research Institute of Massachusetts Eye and Ear, Boston, MA, USA

    Tobias Elze

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Contributions

Concept and design: GB, FV, LAK, TE, DH, and JBM. Data collection: GB, FV, IG, JYM, RZ, YC, RK, RL, ESL, DNS, and ZH. Original manuscript draft: GB and FV. Critical revision of the manuscript: GB, FV, IG, JYM, RZ, YC, RK, RL, ESL, DNS, ZH, DNS, LAK, TE, DH, and JBM. Guarantors: GB, FV, and JBM.

Corresponding author

Correspondence to John B. Miller.

Ethics declarations

Ethics approval

The study was conducted in accordance with the tenets set forth in the Declaration of Helsinki and all necessary authorizations were obtained from the MEE Institutional Review Board (Protocol #: 2019P001863).

Consent

Written informed consent was obtained from all participants prior to the inclusion in this study.

Competing interest

L.A.K. has received research support from the National Eye Institute (R01EY027739), CureVac AG, and INGENIA Therapeutics and has a financial arrangement with Pykus Therapeutics. D.H. is a consultant for Allergen, Genentech, and Omeicos Therapeutics and has received financial support from National Eye Institute, Lions VisionGift, Commonwealth Grant, Lions International, Syneos LLC, and the Macular Society. J.B.M. is a consultant for Alcon, Allergan, Topcon, Carl Zeiss, Sunovion, and Genentech.

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The work from this manuscript has been presented at the Association for Research in Vision and Ophthalmology (ARVO) Annual Meeting 2022, May 1st, Denver, Colorado.

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Baldwin, G., Vingopoulos, F., Garg, I. et al. Structure–function associations between contrast sensitivity and widefield swept–source optical coherence tomography angiography in diabetic macular edema. Graefes Arch Clin Exp Ophthalmol 261, 3113–3124 (2023). https://doi.org/10.1007/s00417-023-06086-1

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