Preview

Russian Ophthalmological Journal

Advanced search

Structural and functional correlations in the pre-perimetric and the initial stages of glaucomatous optic neuropathy

https://doi.org/10.21516/2072-0076-2021-14-2-14-22

Abstract

Purpose:to study morphological and functional relationships in the early and preclinical diagnosis of glaucomatous optical neuropathy based on optical coherence tomography (OCT) of the retina and the data of electrophysiological research. Material and methods. Two clinical groups: (I) 35 patients (60 eyes) aged 49–70 (ave. 58.0 ± 5.3 yrs) with suspected glaucoma and (II) 21 patients (30 eyes) aged 46-68 (ave. 61.0 ± 4.8 yrs) with initial primary open-angle glaucoma (POAG), and a comparison group consisting of 36 relativelyhealthy subjects (41 eyes) aged 54–70 (ave. 62.0 ± 4.5 yrs), were subjected to spectral OCT by OСT Spectralis (Heidelberg Engineering, Germany). The thickness of the peripapillary layer of retinal nerve fibers (pRNFL), the minimum rim width (MRW), and the thickness of theretinal layers in the macular region that make up the ganglion cell complex (GCC) were evaluated. Spearman correlation analysis was used to identify correlations between OCT and electroretinography (ERG) data. Results.In patients with suspected glaucoma, changes in the parameters of transient pattern-ERG correlated with RNFL thinning in the macular region, inner plexiform layer (IPL), and ganglion cell layer(GCL) in the parafoveal area. In patients with initial glaucoma, changes in the retinal GCL were detected for the upper, lower, and temporal quadrants, while the nasal and central quadrants remained intact in all three GCC layers (RNFL, GCL, and IPL). In patients with suspected glaucoma, no statistically significant changes in the thickness of the pRNFL as compared with the norm were detected. Yet the MRW differed significantly from the comparison group. The highest number of correlations was found between the parameters of the ERGs and the thickness of the pRNFL. In patients with the initial stage of POAG, there was a significant increase in the thickness of RNFL in the temporal quadrant of the paramacular region. In our opinion, this phenomenon may be associated with the development of reactive gliosis being thereaction of neuroglia in response to changes in vascular and/or dystrophic homeostasis. Conclusion.Specific combinations of changes in the structural parameters of the retina and optic nerve head and the temporal and amplitude indices of the PERG and phototopic negative response have been found, justifying their use as combined markers of early and preclinical diagnosis of POAG.

About the Authors

M. O. Kirillova
Helmholtz National Medical Research Center of Eye Diseases
Russian Federation

Maria O. Kirillova— PhD student, glaucoma department

14/19, Sadovaya-Chernogryazskaya St., Moscow, 105062



A. N. Zhuravleva
Helmholtz National Medical Research Center of Eye Diseases
Russian Federation

Anastasiya N. Zhuravleva — Cand. of Med. Sci., researcher, glaucoma 
department

14/19, Sadovaya-Chernogryazskaya St., Moscow, 105062



M. V. Zueva
Helmholtz National Medical Research Center of Eye Diseases
Russian Federation

Marina V. Zueva— Dr. of Biol. Sci., professor, head of the department 
of clinical physiology of vision named after S.V. Kravkov

14/19, Sadovaya-Chernogryazskaya St., Moscow, 105062



I. V. Tsapenko
Helmholtz National Medical Research Center of Eye Diseases
Russian Federation

Irina V. Tsapenko — Cand. of Biol. Sci., senior researcher, department 
of clinical physiology of vision named after S.V. Kravkov

14/19, Sadovaya-Chernogryazskaya St., Moscow, 105062



References

1. Tham Y.C., Li X., Wong T.V., Quigley H.A., Aung T., Cheng C.Global prevalence of glaucoma and projeections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology. 2014; 121 (11): 2081–90. https://doi.org/10.1016/j.ophtha.2014.05.013

2. Wollstein G., Kagemann L, Bilonick R.A., et al.Retinal nerve fibre layer and visual function loss in glaucoma: the tipping point. Br. J. Ophthalmol. 2012; 96 (1): 47–52. https://doi.org/10.1136/bjo.2010.196907

3. Tan O., Chopra V., Lu A.T., et al.Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography. Ophthalmol. 2009; 116 (12): 2305–14. https://doi.org/10.1016/j.ophtha.2009.05.025

4. Chien J.L., Ghassibi M.P., Patthanathamrongkasem T., et al. Glaucoma diagnostic capability of global and regional measurements of isolated ganglion cell layer and inner plexiform layer. Journal of Glaucoma. 2017; 26 (3): 208–15. https://doi.org/10.1097/ijg.0000000000000572

5. Gupta N., Ang L.C., Noel de Tilly L., Bidaisee L., Yucel Y.H. Human glaucoma and neural degeneration in intracranial optic nerve, lateral geniculate nucleus, and visual cortex. Br. J. Ophthalmol. 2006; 90 (6):674–78. https://doi.org/10.1136/bjo.2005.086769

6. Calkins D.J., Horner P.J.The cell and molecular biology of glaucoma: axonopathy and the brain. Invest. Ophthalmol. Vis. Sci. 2012; 53(5): 2482–4. https://doi.org/10.1167/iovs.12-9483i

7. Kasi A., Faiq M.A., Vhan K.C. In vivo imaging of structural, metabolic and functional brain changes in glaucoma. Neural Regen. Res. 2019; 14 (3): 446–9. https://doi.org/10.4103/1673-5374.243712

8. North R.V., Jones A.L., Drasdo N., Wild J.M., Morgan J.E.Electro- physiological evidence of early functional damage in glaucoma and ocular hypertension. Invest. Ophthalmol. Vis. Sci. 2010; 51 (2): 1212–6. https://doi.org/10.1167/iovs.09-3409

9. Cvenkel B., Sustar M., Perovšek D.Ganglion cell loss in early glaucoma, as assessed by photopic negative response, pattern electroretinogram, and spectraldomain optical coherence tomography. Doc. Ophthalmol. 2017; 135 (1): 17–28. https://doi.org/10.1007/s10633-017-9595-9

10. Sehi M., Grewal D.S., Goodkin M.L., Greenfield D.S. Reversal of retinal ganglion cell dysfunction after surgical reduction of intraocular pressure. Ophthalmology. 2010; 117 (12): 2329–36. https://doi.org/10.1016/j.ophtha.2010.08.049

11. Niyadurupola N., Luu C.D., Nguyen D.Q., et al.Intraocular pressure lowering is associated with an increase in the photopic negative response (PhNR) amplitude in glaucoma and ocular hypertensive eyes. Invest. Ophthalmol. Vis. Sci. 2013; 54 (3): 1913–9. https://doi.org/10.1167/iovs.12-10869

12. Kirillova M.O., Zueva M.V., Tsapenko I.V., Zhuravleva A.N. Electrophysiological markers of preclinical diagnosis of glaucoma optic europathy. Russian ophthalmological journal. 2021; 14 (1): 35–41 (in Russian)]. https://doi.org/10.21516/2072-0076-2021-14-1-35-41

13. Moghimi S., Fatehi N., Nguyen A.H., et al.Relationship of the macular ganglion cell and inner plexiform layers in healthy and glaucoma eyes. Transl. Vis. Sci. Technol. 2019; 8 (5): 27. https://doi.org/10.1167/tvst.8.5.27

14. Martinez-de-la-Casa J.M., Cifuentes-Canorea P., Berrozpe C., et al.Diagnostic ability of macular nerve fiber layer thickness using new segmentation software in glaucoma suspects. Invest. Ophthalmol. Vis. Sci. 2014; 55 (12): 8343–8. https://doi.org/10.1167/iovs.14-15501

15. Curcio C.A., Allen K.A. Topography of ganglion cells in human retina. J. Comp. Neurol. 1990; 300(1): 5–25. https://doi.org/10.1002/cne.903000103

16. Pazos M., Dyrda A., Biarnés M., et al. Diagnostic accuracy of Spectralis SD OCT automated macular layers segmentation to discriminate normal from early glaucomatous eyes. Ophthalmology. 2017; 124 (8): 1218–28. https://doi.org/10.1016/j.ophtha.2017.03.044

17. Bosco A., Steele M.R., Vetter M.L.Early microglia activation in a mouse model of chronic glaucoma. The Journal of Comparative Neurology. 2011; 519 (4): 599–620. https://doi.org/10.1002/cne.22516

18. Bowd C., Tafreshi A., Zangwill L.M., et al.Pattern electroretinogram association with spectral domain-OCT structural measurements in glaucoma. Eye (Lond). 2011; 25 (2): 224–32. https://doi.org/10.1038/eye.2010.203

19. Kalesnykas G., Oglesby E.N., Zack D.J., et al. Retinal ganglion cell morphology after optic nerve crush and experimental glaucoma. Invest. Ophthalmol. Vis. Sci. 2012; 53 (7): 3847–7. doi: https://doi.org/10.1167/iovs.12-9712

20. Ahmed F.A., Chaudhary P., Sharma S.C. Effects of increased intraocular pressure on rat retinal ganglion cells. Int. J .Dev. Neurosci. 2001; 19 (2): 209–18. doi: 10.1016/s0736-5748(00)00073-3

21. Tao X., Sabharwal J., Seilheimer R.L., Wu S.M., Frankfort B.J.Mild intraocular pressure elevation in mice reveals distinct retinal ganglion cell functional thresholds and pressure-dependent properties. J. Neurosci. 2019 Mar 6; 39 (10): 1881–91. doi: 10.1523/JNEUROSCI.2085-18.2019.

22. Журавлева А.Н., Зуева М.В. Гипотензивная терапия глаукомы и нейропротекция. Российский офтальмологический журнал. 2020; 13 (2): 78–82. [Zhuravleva A.N., Zueva M.V. Hypotensive glaucoma therapy and neuroprotection. Russian ophthalmological journal. 2020; 13 (2): 78–82 (in Russian)]. https://doi.org/10.21516/2072-0076-2020-13-2-78-82

23. Awe M., Khalili-Amiri S., Volkmann I.R., et al. The minimum rim width based on Bruch's membrane opening. Ophthalmologist. 2019; 116: 33–42. https://doi.org/10.1007/s00347-017-0616-6

24. Chauhan B.C., O'Leary N., Almobarak F.A., et al. Enhanced detection of openangle glaucoma with an anatomically accurate optical coherence tomographyderived neuroretinal rim parameter. Ophthalmology. 2013 Mar; 120 (3): 535–43. doi: 10.1016/j.ophtha.2012.09.055

25. Demir S. T., Oba M.E., Erdoğan E.T., et al.Comparison of pattern electroretinography and Optical Coherence Tomography parameters in patients with primary open-angle glaucoma and ocular hypertension. Turk. J. Ophthalmol. 2015; 45 (6): 229–34. http://dx.doi.org/10.4274/tjo.39260

26. Harwerth R.S., Wheat J.L. Modeling the effects of aging on retinal ganglion cell density and nerve fiber layer thickness. Graefe’s Arch. Clin. Exp. Ophthalmol. 2008; 246 (2): 305–14. doi:10.1007/s00417-007-0691-5

27. Zueva M.V., Arapiev M.U., Tsapenko I.V., Lovpache D.N., Maglakelidze N.M., Lantuh E.P. Morphological and functional features of changes in retinal ganglion cells during physiological aging and in the early stage of glaucoma. Vestnik oftal'mologii. 2016; 1: 36–42 (in Russian)]. https://doi.org/10.17116/oftalma2016132136-42

28. Gmeiner J., Schrems W. A., Mardin C. Y., et al. Comparison of Bruch's membrane opening minimum rim width and peripapillary retinal nerve fiber layer thickness in early glaucoma assessment. Invest. Ophthalmol. Vis. Sci. 2016; 57 (9): OCT575-OCT584. doi: https://doi.org/10.1167/iovs.15-18906

29. Ventura L. M., Sorokac N., Santos R. D. L., Feuer W.J., Porciatti V.The relationship between retinal ganglion cell function and retinal nerve fiber thickness in early glaucoma. Invest. Ophthalmol. Vis. Sci. 2006; 47 (9): 3904–11. https://doi.org/10.1167/iovs.06-0161

30. Parisi V., Manni G., Centofanti M., et al. Correlation between optical coherence tomography, pattern electroretinogram, and visual evoked potentials in openangle glaucoma patients. Ophthalmology. 2001; 108: 905–12. https://doi.org/10.1016/s0161-6420(00)00644-8

31. Falsini B., Marangoni D., Salgarello T., et al. Structure-function relationship in ocular hypertension and glaucoma: interindividual and interocular analysis by OCT and pattern ERG. Graefe’s Arch. Clin. Exp. Ophthalmol. 2008; 246 (8): 1153–62. https://doi.org/10.1007/s00417-008-0808-5

32. Mavilio A., Scrimieri F., Errico D.Can variability of pattern ERG signal help to detect retinal ganglion cells dysfunction in glaucomatous eyes? BioMed. Research International. 2015; 2015: 1–11. http://dx.doi.org/10.1155/2015/571314

33. Kirkiewicz M., Lubiński W., Penkala K. Photopic negative response of full-field electroretinography in patients with different stages of glaucomatous optic neuropathy. Doc. Ophthalmol. 2016; 132: 57–65. https://doi.org/10.1007/s10633-016-9528-z

34. Machida S., Toba Y., Ohtaki Y., Gotoh Y., Kaneko M., Kurosaka D.Photopic negative response of focal electoretinograms in glaucomatous eyes. Invest. Ophthalmol. Vis. Sci. 2008; 49 (12): 5636–44. https://doi.org/10.1167/iovs.08-1946


Review

For citations:


Kirillova M.O., Zhuravleva A.N., Zueva M.V., Tsapenko I.V. Structural and functional correlations in the pre-perimetric and the initial stages of glaucomatous optic neuropathy. Russian Ophthalmological Journal. 2021;14(2):14-22. (In Russ.) https://doi.org/10.21516/2072-0076-2021-14-2-14-22

Views: 732


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2072-0076 (Print)
ISSN 2587-5760 (Online)