Retinal plasticity in retinopathy of prematurity, and phototherapy prospects
https://doi.org/10.21516/2072-0076-2020-13-1-77-84
Abstract
In premature babies, plastic changes develop in the neural retina, which, depending on the severity of retinopathy of prematurity (ROP), are a manifestation of adaptive or non-adaptive plasticity. In various experimental studies on animal ROP models, the conditioning effects of intermittent white light stimulation and various mechanisms of the positive effect of red and ultraviolet radiation on the plasticity of the retina have been demonstrated, which allows phototherapy to be considered as a promising modifying treatment for ROP supplementing the main therapy. Taking into account that light-dependent processes are involved in the pathogenesis of ROP, we also hypothesize that fractal phototherapy with complex-structured optical stimuli, as a method of activating adaptive neuroplasticity, can be most effective in the complex of methods for preventing and treating ROP.
About the Authors
M. V. Zueva
Helmholtz National Medical Research Center of Eye Diseases
Russian Federation
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
L. V. Kogoleva
Helmholtz National Medical Research Center of Eye Diseases
Russian Federation
Russian Federation
Lyudmila V. Kogoleva – Dr. of Med. Sci., head of the children's consultative and outpatient department.
14/19, Sadovaya Chernogryazskaya St., Moscow, 105062
L. A. Katargina
Helmholtz National Medical Research Center of Eye Diseases
Russian Federation
Russian Federation
Lyudmila A. Katargina – Dr. of Med. Sci., Professor, deputy director.
14/19, Sadovaya Chernogryazskaya St., Moscow, 105062
References
1. Katargina L.A. Retinopathy of prematurity, current state of the problem and tasks of organizing ophthalmologic care for premature babies in the Russian Federation. Rossijskaya Pediatricheskaya Oftalmologiya. 2012; (1): 5–7 (in Russian)
2. Gilbert C. Retinopathy of prematurity: a global perspective of the epidemics, population of babies at risk and implications for control. Early Hum. Dev. 2008; 84: 77–2. doi: 10.1016/j.earlhumdev.2007.11.009.
3. Saidasheva E.I., Buyanovskaya S.V., Kovshov F.V. Retinopathy of prematurity in infants with gestational age less than 27 weeks: features of the course and results of laser treatment. Rossijskaya pediatricheskaya oftalmologiya. 2014; 9 (4): 48–9 (in Russian)
4. Smith L.E. Pathogenesis of retinopathy of prematurity. Growth Horm. IGF Res. 2004; 14 (Suppl A): S140-S144. doi:10.1016/j.ghir.2004.03.030
5. Quinn G.E., Gilbert C., Darlow B.A., Zin A. Retinopathy of prematurity: an epidemic in the making. Chin. Med. J. (Engl). 2010; 123: 2929–37. doi: 10.3760/cma.j.issn.0366-6999.2010.20.033
6. Natoli R., Valter K., Barbosa M., et al. 670 nm photobiomodulation as a novel protection against retinopathy of prematurity: evidence from oxygen induced retinopathy models. PLoS ONE. 2013; 8 (8): e72135. doi: 10.1371/journal.pone.0072135
7. An International Committee for the Classification of retinopathy of prematurity. The international classification of ROP – Revisited. Arch. Ophthalmol. 2005; 123: 991–9. doi:10.1001/archopht.123.7.991
8. Christiansen S.P., Dobson V., Quinn G., et al. Progression of type 2 to type 1 retinopathy of prematurity in the early treatment for retinopathy of prematurity study. Arch. Ophthalmol. 2010; 128 (4): 461–5. doi: 10.1001/archophthalmol.2010.34
9. Early Treatment for Retinopathy of Prematurity Cooperative Group. Revised indications for the treatment of retinopathy of prematurity: results of the early treatment for retinopathy of prematurity randomized trial. Arch. Ophthalmol. 2003; 121: 1684–94. doi: 10.1001/archopht.121.12.1684
10. Ng E.Y., Connolly B.P., McNamara J.A., et al. A comparison of laser photocoagulation with cryotherapy for threshold retinopathy of prematurity at 10 years: part 1. Visual function and structural outcome. Ophthalmology. 2002; 109 (5): 928–34.
11. McCloskey M., Wang H., Jiang Y., et al. Anti-VEGF antibody leads to later atypical intravitreous neovascularization and activation of angiogenic pathways in a rat model of ROP. Invest. Ophthalmol. Vis. Sci. 2013; 54: 2020–6. doi: 10.1167/iovs.13-11625
12. O’Connor A.R., Stephenson T.J., Johnson A., et al. Strabismus in children of birth weight less than 1701 g. Arch. Ophthalmol. 2002; 120: 767–73. doi:10.1001/archopht.120.6.767
13. Terasaki H., Hirose T. Late-onset retinal detachment associated with regressed retinopathy of prematurity. Jap. J. Ophthalmol. 2003; 47 (5): 492–7. doi:10.1016/s0021-5155(03)00088-1
14. Larsson E., Martin L., Holmström G. Peripheral and central visual fields in 11-year-old children who had been born prematurely and at term. J. Pediatr. Ophthalmol. Strabismus. 2004; 41: 39–45. https://doi.org/10.3928/0191-3913-20040101-10
15. Tufail A., Singh A.J., Haynes R.J., et al. Late onset vitreoretinal complications of regressed retinopathy of prematurity. Br. J. Ophthalmol. 2004; 88 (2): 243–6. http://dx.doi.org/10.1136/bjo.2003.022962
16. Larsson E., Rydberg A., Holmström G. Contrast sensitivity in 10 year old preterm and full term children: a population based study. Br. J. Ophthalmol. 2006; 90: 87–90. doi:10.1136/bjo.2005.081653
17. Wu W.C., Lin R. I., Shin C.P. Visual acuity, optical components, and macular abnormalities in patients with a history of prematurity. Ophthalmology. 2012; 119: 1907–16. doi: 10.1016/j.ophtha.2012.02.040
18. Katargina L.A., Belova M.A., Kogoleva L.V. Secondary retinal dystrophies in children with retinopathy of prematurity. Rossijskaya Pediatricheskaya Oftalmologiya. 2014; (3): 62 (in Russian)
19. Kogoleva L.V., Katargina L.A., Rudnitskaya Ya.L. Structural and functional state of the macula in children with retinopathy of prematurity. Vestnik oftal’mologii. 2011; 127 (6): 25–9 (in Russian)
20. Kogoleva L.V., Rogova S.Yu. Impaired visual fields in patients with retinopathy of prematurity. Rossijskaya Pediatricheskaya Oftalmologiya. 2014; 9 (4): 24 (in Russian)
21. Fielder A., Blencowe H., O’Connor A., Gilbert C. Impact of retinopathy of prematurity on ocular structures and visual functions. Arch. Dis. Child Fetal Neonatal Ed. 2015; 100 (2): F179–84. doi: 10.1136/archdischild-2014-306207
22. Moskowitz A., Hansen R., Fulton A. Retinal, visual, and refractive development in retinopathy of prematurity. Eye and Brain. 2016; 8: 103–11. doi: 10.2147/EB.S9502
23. Shatz C.J. Emergence of order in visual system development. J. Physiol. Paris. 1996; 90: 141–50.
24. Wong R.O.L. Retinal waves and visual system development. Annu. Rev. Neurosci. 1999; 22: 29–47.
25. Tian N. Visual experience and maturation of retinal synaptic pathways. Vis. Res. 2004; 44 (28): 33. doi: 10.1016/j.visres.2004.07.041
26. Madan A., Good W.V. Preterm birth and the visual system. NeoReviews. 2005; 6(3): e153-159. doi: 10.1542/neo.6-3-e153
27. Xu H.P., Tian N. Retinal ganglion cell dendrites undergo a visual activity-dependent redistribution after eye opening. J. Comp. Neurol. 2007; 503 (2): 244–59. doi: 10.1002/cne.21379
28. Luciana M. Cognitive development in children born preterm: Implications for theories of brain plasticity following early injury. Dev. Psychopathol. 2003; 15: 1017–47. doi: 10.1017.S095457940300049X
29. Rothman A.L., Mangalesh S., Chen X., Toth C.A. Optical coherence tomography of the preterm eye: from retinopathy of prematurity to brain development. Eye and Brain. 2016; 8: 123–33. doi: 10.2147/EB.S97660
30. The effects of light reduction on retinopathy of prematurity (LightROP). ClinicalTrials.gov Identifier: NCT00000156. First Posted: September 24, 1999. Last Update Posted: June 5, 2006. Available at: https://clinicaltrials.gov/ct2/show/NCT00000156
31. Reynolds J.D., Hardy R.J., Kennedy K.A., et al. Lack of efficacy of light reduction in preventing retinopathy of prematurity. Light reduction in retinopathy of prematurity (LIGHT-ROP) Cooperative Group. N. Engl. J. Med. 1998; 338 (22): 1572–6. doi: 10.1056/NEJM199805283382202
32. Jorge E.C, Jorge E.N., El Dib R.P. Early light reduction for preventing retinopathy of prematurity in very low birth weight infants. Cochrane Database of Systematic Reviews. 2013; (8). Art. No.: CD000122. doi: 10.1002/14651858.CD000122.pub2
33. Okwundu C.I., Okoromah C.A.N., Shah P.S. Prophylactic phototherapy for preventing jaundice in preterm or low birth weight infants. Cochrane Database of Systematic Reviews. 2012, Issue 1. Art. No.: CD007966. doi: 10.1002/14651858.CD007966.pub2
34. Nguyen M.-T.T., Vemaraju S., Nayak G., et al. An opsin 5–dopamine pathway mediates light-dependent vascular development in the eye. Nature Cell Biology. 2019; 21 (4): 420 doi: 10.1038/s41556-019-0301-x
35. Grossniklaus H.E., Kang S.J., Berglin L. Animal models of choroidal and retinal neovascularization. Prog. Retin. Eye Res. 2010; 29: 500–19. doi:10.1016/j.preteyeres.2010.05.003
36. Rojas J.C., Lee J., John J.M., Gonzalez-Lima F. Neuroprotective effects of near-infrared light in an in vivo model of mitochondrial optic neuropathy. J. Neurosci. 2008; 28: 13511–21. doi:10.1523/JNEUROSCI.3457-08.2008
37. Albarracin R., Eells J., Valter K. Photobiomodulation protects the retina from light-induced photoreceptor degeneration. Invest. Ophthalmol. Vis. Sci. 2011; 52: 3582–92. doi:10.1167/iovs.10-6664
38. Albarracin R., Valter K. 670 nm red light preconditioning supports muller cell function: evidence from the white light-induced damage model in the rat retina. Photochem. Photobiol. 2012; 88 (6): 1418–27. doi: 10.1111/j.1751-1097.2012.01130.x
39. Ying R., Liang H.L., Whelan H.T., Eells J.T., Wong-Riley M.T. Pretreatment with near-infrared light via light-emitting diode provides added benefit against rotenone- and MPP+-induced neurotoxicity. Brain Res. 2008; 1243: 167–73. doi:10.1016/j.brainres.2008.09.057
40. Eells J.T., Wong-Riley M.T., VerHoeve J., et al. Mitochondrial signal transduction in accelerated wound and retinal healing by near-infrared light therapy. Mitochondrion. 2004; 4: 559–67. doi:10.1016/j.mito.2004.07.033
41. Natoli R., Zhu Y., Valter K., et al. Gene and noncoding RNA regulation underlying photoreceptor protection: microarray study of dietary antioxidant saffron and photobiomodulation in rat retina. Mol. Vis. 2010; 16: 1801–22.
42. Karu T. Primary and secondary mechanisms of action of visible to near-IR radiation on cells. J. Photochem. Photobiol. B. Biol. 1999; 49: 1–17. doi:10.1016/S1011-1344(98)00219-X
43. Silveira P.C., Streck E.L., Pinho R.A. Evaluation of mitochondrial respiratory chain activity in wound healing by low-level laser therapy. J. Photochem. Photobiol. B. Biol. 2007; 86: 279–82. doi:10.1016/j.jphotobiol.2006.10.002
44. Karu T.I., Afanas’eva N.I. Cytochrome c oxidase as the primary photoacceptor upon laser exposure of cultured cells to visible and near IR-range light. Dokl. Akad. Nauk. 1995; 342: 693–5 (in Russian)
45. Zhou X., Pardue M.T., Iuvone P.M., Qu J. Dopamine signaling and myopia development: what are the key challenges? Prog. Retin. Eye Res. 2017; 61: 60–71. doi:10.1016/j.preteyeres.2017.06.003
46. Bhattacharya R., Sinha S., Yang Su-Ping, et al. The neurotransmitter dopamine modulates vascular permeability in the endothelium. J. Mol. Signal. 2008; 3: 14. doi: 10.1186/1750-2187-3-14
47. Tarttelin E.E., Bellingham J., Hankins M.W., Foster R.G., Lucas R.J. Neuropsin (Opn5): a novel opsin identified in mammalian neural tissue. FEBS Letters. 2003; 554 (3): 410–6. doi:10.1016/S00145793(03)01212-2
48. Tomonari S., Migita K., Takagi A., Noji S., Ohuchi H. Expression patterns of the opsin 5-related genes in the developing chicken retina. Dev. Dynamics. 2008; 237 (7): 1910–22. doi: 10.1002/dvdy.21611
49. Nakane Y., Ikegami K., Ono H., et al. A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds. PNAS U.S.A. 2010; 107 (34): 15264–8. doi: 10.1073/pnas.1006393107
50. Sato K., Yamashita T., Haruki Y., et al. Two UV-sensitive photoreceptor proteins, Opn5m and Opn5m2 in ray-finned fish with distinct molecular properties and broad distribution in the retina and brain. PLoS One. 2016; 11 (5): e0155339. doi: 10.1371/journal.pone.0155339
51. Kojima D., Mori S., Torii M., et al. UV-sensitive photoreceptor protein OPN5 in humans and mice. PLoS One. 2011; 6: e26388. https://doi.org/10.1371/journal.pone.0026388
52. Rivera J.C., Holm M., Austeng D., et al. Retinopathy of prematurity: inflammation, choroidal degeneration, and novel promising therapeutic strategies. J. Neuroinflam. 2017; 14 (1): 165. doi: 10.1186/s12974-017-0943-1
53. Fulton A.B., Hansen R.M., Moskowitz A., Akula J.D. The neurovascular retina in retinopathy of prematurity. Prog. Retin. Eye Res. 2009; 28 (6): 452–82. doi: 10.1016/j.preteyeres.2009.06.003
54. Hansen R.M., Moskowitz A., Akula J.D., Fulton A.B. The neural retina in retinopathy of prematurity. Prog. Retin. Eye Res. 2017; 56: 32–57. doi:10.1016/j.preteyeres.2016.09.004
55. Harris M.E., Moscowitz A., Fulton A.B., Hansen R.M. Long-term effects of retinopathy of prematurity (ROP) on rod and rod-driven function. Doc. Ophthalmol. 2011; 122 (1): 19–27. doi: 10.1007/s10633-010-9251-0
56. Akula J.D., Hansen R.M., Martinez-Perez M.E., Fulton A.B. Rod photoreceptor function predicts blood vessel abnormality in retinopathy of prematurity. Invest. Ophthalmol. Vis. Sci. 2007; 48 (9): 4351–9. doi: 10.1167/iovs.07-0204
57. Liu K., Akula J.D., Falk C., Hansen R.M., Fulton A.B. The retinal vasculature and function of the neural retina in a rat model of retinopathy of prematurity. Invest. Ophthalmol. Vis. Sci. 2006; 47: 2639–47. doi: 10.1167/iovs.06-0016
58. Hansen R.M., Tavormina J.L., Moskowitz A., Fulton A.B. Effect of retinopathy of prematurity on scotopic spatial summation. Invest. Ophthalmol. Vis. Sci. 2014; 55 (5): 3311–3. doi: 10.1167/iovs.1414344
59. Hansen R.M., Moskowitz A., Tavormina J.L., Bush J.N., Fulton A.B. Temporal summation in children with a history of retinopathy of prematurity. Invest. Ophthalmol. Vis. Sci. 2015; 56: 914–7. doi: 10.1167/iovs.14-16102
60. Hansen R.M., Fulton A.B. Dark-adapted thresholds at 10- and 30-deg eccentricities in 10-week-old infants. Vis. Neurosci. 1995; 12 (3 May-Jun.): 509–12. doi:10.1017/s0952523800008415
61. Hansen R.M., Fulton A.B. The course of maturation of rod-mediated visual thresholds in infants. Invest. Ophthalmo.l Vis. Sci. 1999; 40 (8 Jul.): 1883–6. PMID: 10393066
62. Palmer E.A., Flynn J.T., Hardy R.J., et al. Incidence and early course of retinopathy of prematurity. The Cryotherapy for Retinopathy of Prematurity Cooperative Group. Ophthalmology. 1991; 98: 1628–40.
63. Fulton A.B., Hansen R.M., Moskowitz A., Barnaby A.M. Multifocal ERG in subjects with a history of retinopathy of prematurity. Doc. Ophthalmol. 2005; 111: 7–13. doi: 10.1007/s10633-005-2621-3
64. Hammer D.X., Iftimia N.V., Ferguson R.D., et al. Foveal fine structure in retinopathy of prematurity: an adaptive optics Fourier domain optical coherence tomography study. Invest. Ophthalmol. Vis. Sci. 2008; 49 (5): 2061–70. doi: 10.1167/iovs.07-1228
65. Yanni S.E., Wang J., Cheng C.S., et al. Normative reference ranges for the retinal nerve fiber layer, macula, and retinal layer thicknesses in children. Am. J. Ophthalmol. 2013; 155 (2): 354–60; e1. doi: 10.1016/j.ajo.2012.08.010
66. Kogoleva L.V., Arakelyan M.A., Shamshinova A.M., Katargina L.A. The role of electrophysiological studies in assessing and predicting vision in retinopathy of prematurity. Russian ophthalmological journal. 2013; 6 (3): 44–4 (in Russan)
67. Akula J.D., Mocofanescu A., Ferguson R.D., et al. Retinal remodeling in retinopathy of prematurity. Invest. Ophthalmol. Vis. Sci. April 2014, 55: 3505. Available at: https://iovs.arvojournals.org/article.aspx?articleid=2268939
68. Francardo V., Schmitz Y., Sulzer D., Cenci M.A. Neuroprotection and neurorestoration as experimental therapeutics for Parkinson's disease. Exp. Neurol. 2017; 298: 137–47. https://doi.org/10.1016/j.expneurol.2017.10.001
69. Goldberger A.L., Amaral L.A.N., Hausdorff J.M., et al. Fractal dynamics in physiology: Alterations with disease and aging. Proc. Natl. Acad. Sci. USA. 2002; 99 (Suppl.1): 2466–72. https://doi.org/10.1073/pnas.012579499
70. Manor B., Lipsitz L.A. Physiologic complexity and aging: implications for physical function and rehabilitation. Prog. Neuropsychopharmacol. Biol. Psychiatry. 2013; 45: 287–93. https://doi.org/10.1016/j.pnpbp.2012.08.020
71. Zueva M. Fractality of sensations and the brain health: the theory linking neurodegenerative disorder with distortion of spatial and temporal scale-invariance and fractal complexity of the visible world. Front. Aging Neurosci. 2015; 7: 135. https://doi.org/10.3389/fnagi.2015.00135
72. Zueva M.V. Dynamic fractal flickering as a tool in research of nonlinear dynamics of the evoked activity of a visual system and the possible basis for new diagnostics and treatment of neurodegenerative diseases of the retina and brain. World Applied Sciences Journal. 2013; 27 (4): 462–8. doi: 10.5829/idosi.wasj.2013.27.04.13657
73. Zueva M.V. Technologies of nonlinear stimulation: role in the treatment of diseases of the brain and the potential applications in healthy individuals. Human physiology. 2018; 44 (3): 289–99. doi: 10.1134/S0362119718030180
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For citations:
Zueva M.V., Kogoleva L.V., Katargina L.A. Retinal plasticity in retinopathy of prematurity, and phototherapy prospects. Russian Ophthalmological Journal. 2020;13(1):77-84. (In Russ.) https://doi.org/10.21516/2072-0076-2020-13-1-77-84
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