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Intraretinal microvascular alterations in indirect traumatic optic neuropathy using optical coherence tomography angiography

Abstract

Purpose

To quantitatively evaluate macular and peripapillary microvascular alterations in patients with indirect traumatic optic neuropathy (TON) compared to normal controls using optical coherence tomography angiography (OCT-A) and determine their associations with other ocular parameters.

Methods

We enrolled 33 eyes of 33 patients with TON and 34 eyes of 34 healthy controls. OCT-A was used to generate microvascular structure images of the superficial retinal capillary plexus (SRCP), deep retinal capillary plexus (DRCP), and radial peripapillary capillary (RPC) segment in the macula and peripapillary area. Functional and structural parameters such as best-corrected visual acuity, visual field, peripapillary retinal nerve fibre layer (pRNFL) thickness, macular ganglion cell-inner plexiform layer (mGCIPL) thickness, OCT-A variables were compared between TON patients and controls. Age, gender, and spherical equivalent refractive errors were statistically adjusted for the analysis.

Results

OCT-A revealed a significant reduction of the average vessel density in the RPC segment in TON patients compared to controls (48.5% ± 6.28 vs. 57.88% ± 3.06%, P < 0.0001, corrected P < 0.0001). When comparing sectors, the vessel density of the RPC segment in TON patients was also significantly lower in all four quadrants compared to healthy controls. The inferior sector vessel density of the RPC segment was significantly associated with visual field defects (P = 0.0253) and visual acuity (P = 0.0369). The temporal sector vessel density of DRCP was also associated with visual field defects (P = 0.0377). The RPC segment in the superior and inferior sector vessel density displayed a significant association with the corresponding regional pRNFL thickness (P = 0.0248 and <0.0001, respectively).

Conclusions

Patients with indirect TON exhibit significant microvascular alterations compared to controls. This study confirms that TON can induce intraretinal microvascular changes and suggests that OCT-A may serve as a useful biomarker for assessing visual functional and structural changes.

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Fig. 1: Representative test results and scatter plots depicting association analyses.

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Data availability

The datasets generated and/or analysed during the current study are available from the corresponding author upon reasonable request.

References

  1. Warner N, Eggenberger E. Traumatic optic neuropathy: a review of the current literature. Curr Opin Ophthalmol. 2010;21:459–62.

    Article  PubMed  Google Scholar 

  2. Wang BH, Robertson BC, Girotto JA, Liem A, Miller NR, Iliff N, et al. Traumatic optic neuropathy: a review of 61 patients. Plast Reconstr Surg. 2001;107:1655–64.

    Article  CAS  PubMed  Google Scholar 

  3. al-Qurainy IA, Stassen LF, Dutton GN, Moos KF, el-Attar A. The characteristics of midfacial fractures and the association with ocular injury: a prospective study. Br J Oral Maxillofac Surg. 1991;29:291–301.

    Article  CAS  PubMed  Google Scholar 

  4. Holt GR, Holt JE. Incidence of eye injuries in facial fractures: an analysis of 727 cases. Otolaryngol Head Neck Surg. 1983;91:276–9.

    Article  CAS  PubMed  Google Scholar 

  5. Zachariades N, Papavassiliou D, Christopoulos P. Blindness after facial trauma. Oral Surg Oral Med Oral Pathol Oral Radio Endod. 1996;81:34–7.

    Article  CAS  Google Scholar 

  6. Steinsapir KD, Goldberg RA. Traumatic optic neuropathy: an evolving understanding. Am J Ophthalmol. 2011;151:928–33 e2.

    Article  PubMed  Google Scholar 

  7. Sarkies N. Traumatic optic neuropathy. Eye (Lond). 2004;18:1122–5.

    Article  CAS  PubMed  Google Scholar 

  8. Augstburger E, Zéboulon P, Keilani C, Baudouin C, Labbé A. Retinal and choroidal microvasculature in nonarteritic anterior ischemic optic neuropathy: an optical coherence tomography angiography study. Invest Ophthalmol Vis Sci. 2018;59:870–7.

    Article  PubMed  Google Scholar 

  9. Liu L, Jia Y, Takusagawa HL, Pechauer AD, Edmunds B, Lombardi L, et al. Optical coherence tomography angiography of the peripapillary retina in glaucoma. JAMA Ophthalmol. 2015;133:1045–52.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Mammo Z, Heisler M, Balaratnasingam C, Lee S, Yu DY, Mackenzie P, et al. Quantitative optical coherence tomography angiography of radial peripapillary capillaries in glaucoma, glaucoma suspect, and normal eyes. Am J Ophthalmol. 2016;170:41–9.

    Article  PubMed  Google Scholar 

  11. Mo J, Duan A, Chan S, Wang X, Wei W. Vascular flow density in pathological myopia: an optical coherence tomography angiography study. BMJ Open. 2017;7:e013571.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Kwapong WR, Peng C, He Z, Zhuang X, Shen M, Lu F. Altered macular microvasculature in neuromyelitis optica spectrum disorders. Am J Ophthalmol. 2018;192:47–55.

    Article  PubMed  Google Scholar 

  13. Ustymowicz A, Mariak Z, Obuchowska I, Mariak Z, Kochanowicz J. Blood flow disturbances in the central retinal artery in patients with traumatic optic neuropathy. Med Sci Monit. 2009;15:Cr366–71.

    PubMed  Google Scholar 

  14. Shi W, Wang HZ, Song WX, Yang WL, Li WY, Wang NL. Axonal loss and blood flow disturbances in the natural course of indirect traumatic optic neuropathy. Chin Med J (Engl). 2013;126:1292–7.

    Article  PubMed  Google Scholar 

  15. Lee JY, Eo DR, Park KA, Oh SY. Choroidal thickness in traumatic optic neuropathy. Curr Eye Res. 2017;42:1628–33.

    Article  PubMed  Google Scholar 

  16. Ma H, Gao Y, Li JM, Bao YK, Nie C, Yin P, et al. Analysis of retinal vasculature changes in indirect traumatic optic neuropathy using optic coherence tomography angiography. Int J Ophthalmol. 2022;15:1344–51.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Gao Y, Li J, Ma H, Nie C, Lv X, Lin X, et al. The retinal vasculature pathophysiological changes in vision recovery after treatment for indirect traumatic optic neuropathy patients. Graefes Arch Clin Exp Ophthalmol. 2021;259:3093–105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Wu N, Yin ZQ, Wang Y. Traumatic optic neuropathy therapy: an update of clinical and experimental studies. J Int Med Res. 2008;36:883–9.

    Article  CAS  PubMed  Google Scholar 

  19. Lee GI, Kim Y, Park KA, Oh SY, Kong DS, Hong SD. Parafoveal and peripapillary vessel density in pediatric and juvenile craniopharyngioma patients. Sci Rep. 2022;12:5355.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Fenner BJ, Tan GSW, Tan ACS, Yeo IYS, Wong TY, Cheung GCM. Identification of imaging features that determine quality and repeatability of retinal capillary plexus density measurements in OCT angiography. Br J Ophthalmol. 2018;102:509–14.

    Article  PubMed  Google Scholar 

  21. Medeiros FA, Moura FC, Vessani RM, Susanna R Jr. Axonal loss after traumatic optic neuropathy documented by optical coherence tomography. Am J Ophthalmol. 2003;135:406–8.

    Article  PubMed  Google Scholar 

  22. López-de-Eguileta A, Casado A. Different follow-up OCT analyses of traumatic optic neuropathy. A case report. Am J Ophthalmol Case Rep. 2020;20:100879.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Cunha LP, Costa-Cunha LV, Malta RF, Monteiro ML. Comparison between retinal nerve fiber layer and macular thickness measured with OCT detecting progressive axonal loss following traumatic optic neuropathy. Arq Bras Oftalmol. 2009;72:622–5.

    Article  PubMed  Google Scholar 

  24. Sung JY, Lee HM, Lee SB, Kim KN, Lee YH. Progression of optic atrophy in traumatic optic neuropathy: retrograde neuronal degeneration in humans. Neurol Sci. 2022;43:1351–8.

    Article  PubMed  Google Scholar 

  25. Lee JY, Cho K, Park KA, Oh SY. Analysis of retinal layer thicknesses and their clinical correlation in patients with traumatic optic neuropathy. PLoS One. 2016;11:e0157388.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Chan JW, Hills NK, Bakall B, Fernandez B. Indirect traumatic optic neuropathy in mild chronic traumatic brain injury. Invest Ophthalmol Vis Sci. 2019;60:2005–11.

    Article  PubMed  Google Scholar 

  27. Yan H, Yi C, Wen F, Hu Z, Hu S, Liu S, et al. [Angiographic changes in optic disc and its surrounding choroid after contusion of optic nerve]. Yan Ke Xue Bao. 2002;18:80–3.

    PubMed  Google Scholar 

  28. Steinsapir KD, Goldberg RA. Traumatic optic neuropathy. Surv Ophthalmol. 1994;38:487–518.

    Article  CAS  PubMed  Google Scholar 

  29. Hepschke JL, Laws E, Bin Saliman NH, Juncu S, Courtie E, Belli A, et al. Modifications in macular perfusion and neuronal loss after acute traumatic brain injury. Invest Ophthalmol Vis Sci. 2023;64:35.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Liu J, Chen C, Li L, Yi Z, Zheng H. Peripapillary and macular flow changes in nonarteritic anterior ischemic optic neuropathy (NAION) by optical coherence tomography angiography (OCT-A). J Ophthalmol. 2020;2020:3010631.

    PubMed  PubMed Central  Google Scholar 

  31. Wright Mayes E, Cole ED, Dang S, Novais EA, Vuong L, Mendoza-Santiesteban C, et al. Optical coherence tomography angiography in nonarteritic anterior ischemic optic neuropathy. J Neuroophthalmol. 2017;37:358–64.

    Article  PubMed  Google Scholar 

  32. Engelke H, Shajari M, Riedel J, Mohr N, Priglinger SG, Mackert MJ. OCT angiography in optic disc drusen: comparison with structural and functional parameters. Br J Ophthalmol. 2020;104:1109–13.

    Article  PubMed  Google Scholar 

  33. Leal-González M, Pessanha F, Azevedo González-Oliva M, Pérez-Fernández E, Gili P. Study of peripapillary vascular flow using optical coherence tomography angiography in optic nerve head drusen. Clin Exp Ophthalmol. 2020;48:775–82.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

Authors

Contributions

SYO and KAP designed and conducted the study. GIL, MCK and JH collected the data, managed the study, and interpreted the data. KAP contributed to the review of the manuscript. MCK and JH drafted and revised the manuscript. SYO and KAP have reviewed and approved the final version of the manuscript.

Corresponding authors

Correspondence to Kyung-Ah Park or Sei Yeul Oh.

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Kang, M.C., Han, JY., Lee, GI. et al. Intraretinal microvascular alterations in indirect traumatic optic neuropathy using optical coherence tomography angiography. Eye 38, 1133–1139 (2024). https://doi.org/10.1038/s41433-023-02839-8

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