Modern Methods for the Diagnosis of Morphological and Functional Features of the Retina in Dysbinocular and Anisometropic Amblyopia

Child health is a global health priority. Anomalies of refraction, complicated by amblyopia and squint, occupy one of the leading places in the pathology of the visual system of children. According to data obtained from 26 regions of Russia, the leading place in the ocular morbidity of children and adolescents is occupied by ametropia and strabismus with amblyopia. They account for up to 90 % of all cases of visual impairment in childhood. The term amblyopia is understood to mean a decrease in the maximum corrected visual acuity that occurred at an early age, which is caused by disorders of the functions of the visual analyzer, without changes in the fundus and organic lesions of the visual pathways and centers. Despite the outstanding achievements of 21st century medicine, today the questions of the pathophysiological essence of this condition remain open, which is the subject of discussions among pediatric ophthalmologists around the world. In this regard, the literature review presents the results of domestic and foreign authors who studied the morphological (optical coherence tomography) and functional (electroretinography, microperimetry) features of the retina in dysbinocular and anisometropic amblyopia. Some authors have demonstrated the presence of differences in the thickness of the central region and the layer of nerve fibers in patients with amblyopia compared with paired and healthy eyes, their correlation with functional parameters, as well as changes in the thickness of the choroid and microvasculature of the retina. Recently, there have been works devoted to the study of the photosensitivity of the retina in patients with amblyopia and visual rehabilitation using this equipment. A number of authors have shown that with amblyopia, the retinal photosensitivity parameters in the central region are reduced, and there is a correlation between these changes and morphological changes in the posterior pole. The microperimeter also makes it possible to carry out visual rehabilitation, in particular in pediatric patients, and isolated results have been published on the use of this method in patients with amblyopia. The literature data are quite contradictory, and more research remains to be done to determine whether these changes in the retina are primary in relation to this disease, or whether they can be the result of retrograde changes that are obscured by defocusing of visual images from birth.

1. Kravcenko I.A. Disease incidence in preschool children, findings of the sampling analysis. Children’s Hospital = Detskaja bol’nica. 2013;2:6–8 (In Russ.). DOI: 10.1289/ehp.6667

2. Katargina L.A., Mikhailova L.A. The current stage of the ophtalmological care service in the Russian Federation (2012–2013). Russian pediatric ophthalmology = Rossijskaya pediatricheskaya oftal’mologiya 2015;10(1):5–10 (In Russ.).

3. Avetisov E.S., Kovalevskiy E.M., Hvatova A.V. Eye damage. Guide to Pediatric Ophthalmology. Moscow: Medicina, 1987. P. 396–424 (In Russ.).

4. Avetisov E.S. Dysbinocular amblyopia and its treatment. Moscow: Medicina, 1968. 207 p. (In Russ.).

5. Ponomarchuk B.C., Terleckaya O.Yu., Slobodyanik S.B., Drozhenko B.C., CHaura A.G., Hramenko N.I., Lavrenko A.N. Phosphenelectrostimulation in ophthalmology. Experience in the laboratory of functional methods for the study of the organ of vision. News of medicine and pharmacy = Novosti mediciny i farmacii. 2011 (363) (In Russ.).

6. Pospelov V.I., Stal’nov V.S. Dysbinocular amblyopia: accommodation of the leading and amblyopic eyes. Nizhny Novgorod medical journal = Nizhegorodskiĭ medicinskiĭ zhurnal. 2005;3:233–235 (In Russ.).

7. Zueva M.V. Fundamental ophthalmology: the role of electrophysiological studies. The Russian Annals of Ophthalmology = Vestnik oftal’mologii. 2014;130(6):28–36 (In Russ.).

8. Zol’nikova I.V., Shamshinova A.M. Multifocal electroretinography: the origin and diagnostic value. The Russian Annals of Ophthalmology = Vestnik oftal’mologii. 2005;3:47–50 (In Russ.).

9. Fishman G.A., Birch D.G., Holder G.E., Brigell M.G. Electrophysiologic testing in disorders of the retina, optic nerve, and visual pathways. Br J Ophthalmol. 2001;85(8):1013. DOI: 10.1136/bjo.85.8.1013e

10. Heravian J., Daneshvar R., Dashti F., Azimi A., Ostadi Moghaddam H., Yekta A.A., Esmaily H. Simultaneous pattern visual evoked potential and pattern electroretinogram in strabismic and anisometropic amblyopia. Iran Red Crescent Med J. 2011;13(1):21–26.

11. Slyshalova N.N., Shamshinova A.M. Bioelectric activity of the retina with amblyopia. The Russian Annals of Ophthalmology = Vestnik oftal’mologii. 2008;124(4):32–36 (In Russ.).

12. Sargsyan I.S. Electrophysiological monitoring of amblyopia pleoptic treatment in children. New Armenian Medical Journal. 2013;7(4):82–89.

13. Teping C., Kamps I., Reim M. Retinal and retinocortical times to pattern stimulation in amblyopic children. Doc Ophthalmol. 1989;73:111–117. DOI: 10.1007/bf00155028

14. Parisi V., Scarale M.E., Balducci N., Fresina M., Campos E.C. Electrophysiological detection of delayed postretinal neural conduction in human amblyopia. Invest Ophthalmol Vis Sci. 2010;51(10):5041–5048. DOI: 10.1167/iovs.10-5412

15. Deline P.J., Weissenbruch C., Berendschot T.T., Norren D.V. Photoreceptors function in unilateral amblyopia. Vision Res. 1998;38(4):613–617. DOI: 10.1016/j.jcjo.2011.07.013

16. Al-Haddad C., Bou Ghannam A., El Moussawi Z. Elza Rachid, Karine Ismail, Marwan Atallah, Larissa Smeets, Hasan Chahine. Multifocal electroretinography in amblyopia. Graefes Arch Clin Exp Ophthalmol. 2020;(258):683–691. DOI: 10.1007/s00417-019-04558-x

17. Feng L.X., Zhao K.X. Study on anisometropic amblyopia by simultaneously recording multifocal VEP and multifocal ERG. Zhonghua Yan Ke Za Zhi. 2005;41(1):41–46.

18. Ju H., Zhao K.X., Zhou N., Zhang W. Investigation of multifocal electroretinogram in amblyopia. Chinese Journal of Ophthalmology. 2004;40(10):655–662.

19. Chu P.H., Chan H.H., Leat S.J. Effects of unsteady fixation on multifocal electroretinogram (mfERG). Graefes Arch Clin Exp Ophthalmol. 2006;244(10):1273–1282. DOI: 10.1007/s00417-006-0304-8

20. Rudolph, G., Kalpadakis P. The role of fixation for reliable mfERG results. Graefe’s Arch Clin Exp Ophthalmol. 2002;(240):874–875. DOI: 10.1007/s00417-002-0549-9

21. Ozge G.F., Erdem U., Sobaci G. Functional and structural changes of retina in amblyopic eyes. Invest Ophthalmol Vis Sci. 2010; 51(13):3280.

22. Korolenko A.V., Savina Yu.N., Shchuko A.G., Oliferovskaya N.V., Putintseva N.P. Study of regional blood circulation with dysbinocular amblyopia; Novosibirsk State University Bulletin: Biology, clinical medicine = Vestnik Novosibirskogo gosudarstvennogo universiteta: Biologija, klinicheskaja medicina. 2012;10(5):117–122 (In Russ.).

23. Betul Tugcu, Bilge Araz-Ersan, Murat Kilic, Ezgi Tuna Erdogan, Ulviye Yigit, Sacit Karamursel. The Morpho-functional Evaluation of Retina in Amblyopia. Current Eye Research. 2013;38(7):802–809. DOI: 10.3109/02713683.2013 0,779721

24. Wiesel T.N., Hubel D.H. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol. 1963;(26):1003–1017.

25. Yen M.Y., Cheng C.Y., Wang A.G., Retinal nerve fiber layer thickness in unilateral amblyopia. Invest Ophthalmol Vis Sci. 2004;45(7):2224–2230. DOI: 10,1167/iovs.03-0297

26. Wu S.Q., Zhu L.W., Xu Q.B., Xu J.L., Zhang Y. Macular and peripapillary retinal nerve fiber layer thickness in children with hyperopic anisometropic amblyopia. Int J Ophthalmol. 2013;6(1):85–89. DOI: 10,3980/j.issn.2222-3959.2013.01.18

27. Boychuk I.M., Yakhnitsa E.I. Morphometric peculiarities of nerve fiber layer and optic disc in children with amblyopia and hypermetropic refraction. Journal of ophthalmology = Oftal’mologicheskiy zhurnal. 2013;6:17–22 (In Russ.).

28. Yakar K., Kan E., Alan A., Alp M.H., Ceylan T. Retinal nerve fibre layer and macular thicknesses in adults with hyperopic anisometropic amblyopia. J Ophthalmol. 2015;946467. DOI: 10.1155/2015/946467

29. Manal Ali Kasem, Amani Badawi E. Changes in macular parameters in different types of are a amblyopia: optical coherence tomography study. Clin Ophthalmol. 2017;4(11):1407–1416. DOI: 10.2147/OPTH.S143223

30. Huynh S.C., Samarawickrama C., Wang X.Y., Rochtchina E., Wong T.Y., Gole GA, Rose K.A., Mitchell P. Macular and nerve fiber layer thickness in amblyopia: the Sydney Childhood Eye Study. Ophthalmology. 2009;116(9):1604–1609. DOI: 10.1016/j.ophtha.2009.03.013

31. Agrawal S., Singh V., Singhal V. Cross-sectional study of macular thickness variations in unilateral amblyopia. J Clin Ophthalmol Res. 2014;2(1):15–17. DOI: 10.4103/2320-3897.122630

32. Repka M.X., Kraker R.T., Tamkins S.M., Suh D.W., Sala N.A., Beck R.W. Retinal nerve fiber layer thickness in amblyopic eyes. Am J Ophthalmol. 2009;148(1):143–147. DOI: 10.1016/j.ajo.2009.01.015

33. Altindag S., Sahin M. Evaluation of the macular thickness by optical coherence tomography in amblyopia. J Clin Exp Invest. 2016;7:178–183. DOI: 10.5799/ahinjs.01.2016.02.0593

34. Rajavi Z., Sabbaghi H., Behradfar N., Yaseri M., Aghazadeh Amiri M., Faghihi M. Macular Thickness in Moderate to Severe are a amblyopia. Korean Journal of Ophthalmology. 2018;32(4):312. DOI: 10.3341/kjo.2017.0101

35. Pang Y., Goodfellow G.W., Allison C., Block S., Frantz K.A. A prospective study of macular thickness in amblyopic children with unilateral high myopia. Invest Ophthalmol Vis Sci. 2011;52(5):2444–2449. DOI: 10.1167/iovs.10-5550

36. Tarutta E.P., Markosyan G.A., Ryabina M.V., Zolnikova I.V., Kruzhkova G.V. Morphometric and functional features of the macular region in patients with high congenital myopia. The Russian Annals of Ophthalmology = Vestnik oftal’mologii. 2012;1:3–8 (In Russ.).

37. Pang Y., Frantz K.A., Block S., Goodfellow G.W., Allison C. Effect of amblyopia treatment on macular thickness in eyes with myopic anisometropic amblyopia. Invest Ophthalmol Vis Sci. 2015;56(4):2677–2683. DOI: 10.1167/iovs.14-15532

38. Kavitha V., Heralgi M.M., Harishkumar P.D., Harogoppa S., Shivaswamy H.M., Geetha H. Analysis of macular, foveal, and retinal nerve fiber layer thickness in children with unilateral anisometropic amblyopia and their changes following occlusion therapy. Indian J Ophthalmol. 2019;(67):1016–1022. DOI: 10.4103/ijo.IJO_1438_18

39. Nishi T., Ueda T., Hasegawa T., Miyata K., Ogata N. Choroidal thickness in children with hyperopic anisometropic amblyopia. Br. J. Ophthalmol. 2014;98(2):228–232. DOI: 10.1136/bjophthalmol-2013-303938

40. Szigeti A., Tátrai E., Szamosi A., Vargha P., Nagy Z.Z., Németh J., DeBuc D.C., Somfai G.M. A morphological study of etinal changes in unilateral amblyopia using optical coherence tomography image segmentation. PLoS One. 2014;9(2):e88363. DOI: 10.1371/journal.pone.0088363

41. Park K.A., Park D.Y., Oh S.Y. Analysis of spectral-domain optical coherence tomography measurements in amblyopia: a pilot study. British Journal of Ophthalmology. 2011;95(12):1700–1706. DOI: 10.1136/bjo.2010.192765

42. Niyaz L., Yucel O.E., Ariturk N., Terzi O. Choroidal thick-ness in strabismus and amblyopia cases. Strabismus. 2017;25(2):56–59. DOI: 10.1080/09273972.2017.1318152

43. Miki A., Shirakashi M., Yaoeda K., Kabasava Y., Ueki S., Takagi M., Abe H. Retinal nerve fiber layer thickness in recovered and persistent amblyopia. Clin Ophtalmol. 2010;4:1061–1064. DOI: 10,2147/opth.s13145

44. Walker R.A., Rubab S., Voll A.R., Erraguntla V., Murphy P.H. Macular and peripapillary retinal nerve fibre layer thickness in adults with amblyopia. Can J Ophtalmol. 2011;46(5):425–427. DOI: 10.1016/j.jcjo.2011.07.013

45. Kim Y.W., Kim S.J., Yu Y.S. Spectral-domain optical coherence tomography analysis in deprivational amblyopia: a pilot study with unilateral pediatric cataract patients. Graefes Arch Clin Exp Ophthalmol. 2013;251(12):2811–2819. DOI: 10.1007/s00417-013-2494-1

46. Khan A.O. A comparison between the amblyopic eye and normal fellow eye ocular architecture in children with hyperopic anisometropic amblyopia. J AAPOS. 2013;17(1):115–116. DOI: 10.1016/j.jaapos.2012.06.00

47. Kok P.H., de Kinkelder R., Braaksma-Besselink Y.C., Kalkman J., Prick L.J., Sminia M.L., Mourits M.P., Verbraak F.D. Anomalous relation between axial length and retinal thickness in amblyopic children. J AAPOS. 2013;17(6):598–602. DOI: 10.1016/j.jaapos.2013.09.005

48. Xu J., Zheng J., Yu S., Sun Z., Zheng W., Qu.P., Chen Y., Chen W., Yu X. Macular choroidal thickness in unilateral amblyopic children. Invest Ophthalmol Vis Sci. 2014;55(11):7361–7368. DOI: 10.1167/iovs.14-14439

49. Guo L., Tao J., Xia F., Yang Z., Ma X., Hua R. In vivo optical imaging of amblyopia: digital subtraction autofluorescence and split-spectrum amplitude-decorrelation angiography. Lasers Surg Med. 2016;48(7):660–667. DOI: 10.1002/lsm.22520

50. Aslan Bayhan S., Bayhan H.A. Effect of amblyopia treatment on choroidal thickness in children with hyperopic anisometropic amblyopia. Curr Eye Res. 2017;42(9):1254–1259. DOI: 10,1080/02713683.2017.1315141

51. Borrelli E., Lonngi M., Balasubramanian S., Tepelus T.C., Baghdasaryan E., Pineles S.L., Velez F.G., Sarraf D., Sadda S.R., Tsui I. Increased choriocapillaris vessel density in amblyopic children: a case-control study. J AAPOS. 2018. PII: S1091-8531(18)30118-6. DOI: 10.1016/j.jaapos.2018.04.005

52. Lonngi M., Velez F.G., Tsui I., Davila J.P., Rahimi M., Chan C., Sarraf D., Demer J.L., Pineles S.L. Spectral-domain optical coherence tomography angiography in children with amblyopia. JAMA Ophthalmol. 2017;135(10):1086–1091. DOI: 10.1001/jamaophthalmol.2017.3423

53. Repka M.X., Kraker R.T., Tamkins S.M., Suh D.W., Sala N.A., Beck R.W. Pediatric Eye Disease Investigator Group. Retinal nerve fiber layer thickness in amblyopic eyes. Am J Ophthalmol. 2009;148(1):143–147. DOI: 10.1016/j.ajo.2009.01.015

54. Sobral I., Rodrigues T.M., Soares M., Seara M., Monteiro M., Paiva C., Castela R. OCT angiography findings in children with amblyopia. J AAPOS. 2018;22(4):286–289. DOI: 10.1016/j.jaapos.2018.03.009

55. Dickmann A., Petroni S., Perrotta V., Salerni A., Parrilla R., Aliberti S., Savastano M.C., Centra D., Discendenti S., Balestrazzi E. A morpho-functional study of amblyopic eyes with the use of optical coherence tomography and microperimetry. J AAPOS. 2018;15(4):338–341. DOI: 10.1016/j.jaapos.2011.03.019

56. Trabucco P., Mafrici M., Salomone M., Valente S., Di Crescenzo Ch., Spadea L., Vingolo E.M. Microperimetric findings in children with amblyopia. Investigative Ophthalmology & Visual Science. 2014;(55):794 [обновлено 18 мая 2020; процитировано 19 мая 2020]. https://iovs.arvojournals.org/article.aspx?articleid=2272314

57. Zurevinsky J. Eccentric Fixation and Inverse Occlusion: Renewing Our Interest?. Journal of Binocular Vision and Ocular Motility. 2019;4(69):136–140. DOI: 10.3109/08820538.2015.1123739

58. Kashchenko M.A., Kashchenko T.P., Magaramova M.D., Pedanova E.K., Golyakhovsky S.E.: Influence of pleoptic treatment on the deviation of the fixation point from the center of the macular zone in children with amblyopia of varying degrees when studied by the method microperimetry. The Russian Journal of Pediatrics = Rossijskaya detskaya oftal’mologiya. 2019;2:22–24 (In Russ.). DOI: 10.25276/2307-6658-2019-2-22-24

59. Vingolo E.M., Salvatore S., Domanico D., Spadea L., Nebbioso M. Visual rehabilitation in patients with myopic maculopathy: our experience. Can J Ophthalmol. 2013;48(5):438–442. DOI: 10.1016/j.jcjo.2013.08.004

60. Toto L., Di Antonio L., Mastropasqua A., De Nicola C., Mastropasqua L. Rehabilitation with MP1 biofeedback training of a posterior microphthalmos case. Can J Ophthalmol. 2013;48(5):107–e111. DOI: 10.1016/j.jcjo.2013.02.006