Problems of Radiation Medicine and Radiobiology

K.N. Loganovsky¹, P.A. Fedirko¹, K.V. Kuts¹, D. Marazziti², K.Yu. Antypchuk¹, I.V. Perchuk¹,
T.F. Babenko¹, T.K. Loganovska¹, O.O. Kolosynska¹, G.Yu. Kreinis¹, M.V. Gresko¹, S.V. Masiuk¹,
L.L. Zdorenko¹, N.A. Zdanevich¹, N.A. Garkava³, R.Yu. Dorichevska¹, Z.L. Vasilenko¹, V.I. Kravchenko¹, N.V. Drosdova¹, Yu.V. Yefimova¹

¹State Institution «National Research Center for Radiation Medicine of the National Academy of Medical
  Sciences of Ukraine», 53 Illyenko Street, Kyiv, 04050, Ukraine
²Dipartimento di Medicina Clinica e Sperimentale Section of Psychiatry, University of Pisa, Via Roma,
  67, I 56100, Pisa, Italy
³State Institution «Dnipropetrovsk Medical Academy of the Ministry of Health of Ukraine», 9 Vernadsky Street,
  Dnipro, 49044, Ukraine

BRAIN AND EYE AS POTENTIAL TARGETS FOR IONIZING RADIATION IMPACT. Part І. THE CONSEQUENCES OF IRRADIATION OF THE PARTICIPANTS OF THE LIQUIDATION OF THE CHORNOBYL ACCIDENT

Background.Exposure to ionizing radiation could affect the brain and eyes leading to cognitive and vision impairment, behavior disorders and performance decrement during professional irradiation at medical radiology, including interventional radiological procedures, long-term space flights, and radiation accidents.
Objective. The objective was to analyze the current experimental, epidemiological, and clinical data on the radiation cerebro-ophthalmic effects.
Materials and methods. In our analytical review peer-reviewed publications via the bibliographic and scientometric bases PubMed / MEDLINE, Scopus, Web of Science, and selected papers from the library catalog of NRCRM – the leading institution in the field of studying the medical effects of ionizing radiation – were used.
Results. The probable radiation-induced cerebro-ophthalmic effects in human adults comprise radiation cataracts, radiation glaucoma, radiation-induced optic neuropathy, retinopathies, angiopathies as well as specific neurocognitive deficit in the various neuropsychiatric pathology including cerebrovascular pathology and neurodegenerative diseases. Specific attention is paid to the likely stochastic nature of many of those effects. Those prenatally and in childhood exposed are a particular target group with a higher risk for possible radiation effects and neurodegenerative diseases.
Conclusions. The experimental, clinical, epidemiological, anatomical and pathophysiological rationale for visual system and central nervous system (CNS) radiosensitivity is given. The necessity for further international studies with adequate dosimetric support and the follow-up medical and biophysical monitoring of high radiation risk cohorts is justified. The first part of the study currently being published presents the results of the study of the effects of irradiation in the participants of emergency works at the Chornobyl Nuclear Power Plant (ChNPP).
Key words: ionizing radiation, cerebroophthalmic effects, neurocognitive deficit, radiation accident, radiation cataracts, macular degeneration.

Problems of Radiation Medicine and Radiobiology.
2020;25:90-129. doi: 10.33145/2304-8336-2020-25-90-129

full text

1. Loganovsky K. Do low doses of ionizing radiation affect the human brain? Data Science Journal. 2009;8:BR13-BR35. DOI: https://doi.org/10.2481/dsj.BR-04
2. Marazziti D, Baroni S, Catena-Dell'Osso M, Schiavi E, Ceresoli D, Conversano C, et al. Cognitive, psychological and psychiatric effects of ionizing radiation exposure. Curr Med Chem. 2012;19(12):1864-1869. doi: 10.2174/092986712800099776.
3. Bazyka D, Loganovsky K, Ilyenko I, Chumak S, Marazziti D, Maznichenko O, et al. Cellular immunity and telomere length correlate with cognitive dysfunction in clean–up workers of the Chernobyl accident. Clin Neuropsychiatry. J Treat Evaluation. 2019;10(6):280–281.
4. Cacao E, Cucinotta F. Modeling impaired hippocampal neurogenesis after radiation exposure. Radiat Res. 2016;185(3):319-331. doi: 10.1667/RR14289.S1.
5. Hladik D, Tapio S. Effects of ionizing radiation on the mammalian brain. Mutat Res. 2016;770(Pt B):219-230. DOI: 10.1016/j.mrrev.2016.08.003
6. Tang F. Radiation and Alzheimer's disease (AD). J Alzheimers Dis Parkinsonism. 2018;08(01):418. DOI: 10.4172/2161-0460.1000418.
7. Marazziti D, Piccinni A, Mucci F, Baroni S, Loganovsky K, Loganovskaja T. Ionizing radiation: brain effects and related neuropsychiatric manifestations. Probl Radiac Med Radiobiol. 2016;21:64-90. DOI: 10.33145/2304-8336-2016-21-64-90
8. Tang F, Loganovsky K. Low dose or low dose rate ionizing radiation-induced health effect in the human. J Environ Radioact. 2018;192:32-47. doi: 10.1016/j.jenvrad.2018.05.018.
9. Cekanaviciute E, Rosi S, Costes S. Central nervous system responses to simulated galactic cosmic rays. Int J Mol Sci. 2018;19(11):3669. doi: 10.3390/ijms19113669.
10. Cacao E, Cucinotta F. Meta-analysis of cognitive performance by novel object recognition after proton and heavy ion exposures. Radiat Res. 2019;192(5):463. doi: 10.1667/RR15419.1.
11. Ciarmatori A, Nocetti L, Mistretta G, Zambelli G, Costi T. Reducing absorbed dose to eye lenses in head CT examinations: the effect of bismuth shielding. Australas Phys Eng Sci. Med. 2016;39(2):583-589. doi: 10.1007/s13246-016-0445-y
12. Otake M, Finch S, Choshi K, Takaku I, Mishima H, Takase T. Radiation-related ophthalmological changes and aging among Hiroshima and Nagasaki a-bomb survivors: A reanalysis. Radiat Res. 1992;131(3):315-324.
13. Otake M, Schull W. Radiation-related posterior lenticular opacities in Hiroshima and Nagasaki atomic bomb survivors based on the DS86 dosimetry system. Radiat Res. 1990;121(1):3-13.
14. ICRP Publications 41. International Commission on Radiological Protection. Dose dependence of non-stochastic effects. Ann ICRP. 1984;14(3).
15. Fedirko P, Babenko T, Kolosynska O, Dorichevska R, Garkava N, Sushko V. Clinical types of cataracts in a long-term period after acute radiation sickness. Probl Radiac Med Radiobiol. 2019;24:493-502. https://doi.org: 10.33145/2304-8336-2019-24-493-502.
16. Babenko T, Fedirko P, Dorichevska R, Denysenko N, Samoteikina L, Tyshchenko O. The risk of macular degeneration development in persons antenatally irradiated as a result of Chornobyl NPP accident. Probl Radiac Med Radiobiol. 2016;21:172-177.
17. ICRP Publication 26. Recommendations of the International Commission on Radiological Protection. Ann ICRP. 1977;1(3).
18. ICRP Publication 103. The 2007 Recommendations of the International Commission on Radiological Protection. Ann ICRP. 2007;37(2-4):1-332.
19. ICRP Publication 118. ICRP statement on tissue reactions and early and late effects of radiation in normal tissues and organs–threshold doses for tissue reactions in a radiation protection context. Ann ICRP. 2012;41(1-2):1-322.
20. International Commission on Radiological protection ICRP, International Commission on Radiological protection. ICRP 2012 Annual Report. ICRP reference 4833-8730-1908. 2013-07-29. [Internet]. 2012 [cited 16 March 2020]. Available from: https://www.icrp.org/docs/ICRP%20Annual%20Report%202012.pdf
21. Hamada N, Fujimichi Y, Iwasaki T, Fujii N, Furuhashi M, Kubo E, et al. Emerging issues in radiogenic cataracts and cardiovascular disease. J Radiat Res. 2014;55(5):831-846. doi: 10.1093/jrr/rru036.
22. Vano E, Miller D, Dauer L. Implications in medical imaging of the new ICRP thresholds for tissue reactions. Ann ICRP. 2015;44(1_suppl):118-128. doi: 10.1177/0146645314562322.
23. Allen C, Kumar A, Qutob S, Nyiri B, Chauhan V, Murugkar S. Raman micro-spectroscopy analysis of human lens epithelial cells exposed to a low-dose-range of ionizing radiation. Phys Med Biol. 2018;63(2):025002. doi: 10.1088/1361-6560/aaa176.
24. Klein L, Miller D, Balter S, Laskey W, Haines D, Norbash A, et al. Occupational health hazards in the interventional laboratory: time for a safer environment. J Vasc Interv Radiol. 2009;20(7):S278-S283. doi: 10.1016/j.jvir.2009.04.027
25. Tonacci A, Baldus G, Corda D, Piccaluga E, Andreassi M, Cremonesi A, et al. Olfactory non-cancer effects of exposure to ionizing radiation in staff working in the cardiac catheterization laboratory. Int J Cardiol. 2014;171(3):461-463. doi: 10.1016/j.ijcard.2013.12.223.
26. Borghini A, Vecoli C, Mercuri A, Carpeggiani C, Piccaluga E, Guagliumi G, et al. Low-dose exposure to ionizing radiation deregulates the brain-specific microRNA-134 in interventional cardiologists. Circulation. 2017;136(25):2516-2518. doi: 10.1161/CIRCULATIONAHA.117.031251.
27. Chen H, Cheng Y, Zhou Z. Long-term brain tissue monitoring after semi-brain irradiation in rats using proton magnetic resonance spectroscopy. Chin Med J (Engl). 2017;130(8):957-963. doi: 10.4103/0366-6999.204097.
28. Tang F, Loke W, Khoo B. Low-dose or low-dose-rate ionizing radiation–induced bioeffects in animal models. J Radiat Res. 2016;58(2):165-182. doi: 10.1093/jrr/rrw120.
29. Wolkow N, Jakobiec F, Lee H, Sutula F. Long-term outcomes of globe-preserving surgery with proton beam radiation for adenoid cystic carcinoma of the lacrimal gland. Am J Ophthalmol. 2018;195:43-62. doi: 10.1016/j.ajo.2018.07.024.
30. Kim K, Seo S, Lee J, Seok J, Hong J, Chung J, et al. Inclined head position improves dose distribution during hippocampal-sparing whole brain radiotherapy using VMAT. Strahlenther Onkol. 2016;192(7):473-480. doi: 10.1007/s00066-016-0973-0.
31. Wu S, Rao M, Zhou J, Lin Q, Wang Z, Chen Y, et al. Distribution of metastatic disease in the brain in relation to the hippocampus: a retrospective single-center analysis of 6064 metastases in 632 patients. Oncotarget. 2015;6(41):44030–44036. doi: 10.18632/oncotarget.5828.
32. Gaddini L, Balduzzi M, Campa A, Esposito G, Malchiodi-Albedi F, Patrono C, et al. Exposing primary rat retina cell cultures to ?-rays: An in vitro model for evaluating radiation responses. Exp Eye Res. 2018;166:21-28. doi: 10.1016/j.exer.2017.09.009.
33. More S, Beach J, McClelland C, Mokhtarzadeh A, Vince R. In vivo assessment of retinal biomarkers by hyperspectral imaging: early detection of Alzheimer’s disease. ACS Chem Neurosci. 2019;10(11):4492-4501. doi: 10.1021/acschemneuro.9b00331.
34. Doustar J, Torbati T, Black K, Koronyo Y, Koronyo-Hamaoui M. Optical coherence tomography in alzheimer’s disease and other neurodegenerative diseases. Front Neurol. 2017;8:701. doi: 10.3389/fneur.2017.00701.
35. Hart N, Koronyo Y, Black K, Koronyo-Hamaoui M. Ocular indicators of Alzheimer’s: exploring disease in the retina. Acta Neuropathol. 2016;132(6):767-787. doi: 10.1007/s00401-016-1613-6.
36. Frost S, Guymer R, Zaw Aung K, Lance Macaulay S, R Sohrabi H, Bourgeat P, et al. Alzheimer's disease and the early signs of age-related macular degeneration. Curr Alzheimer Res. 2016;13(11):1259-1266. doi: 10.2174/1567205013666160603003800.
37. Silverstein S, Rosen R. Schizophrenia and the eye. Schizophr Res Cogn. 2015;2(2):46-55. doi: 10.1016/j.scog.2015.03.004
38. Miranda A, Martins Rosa A, Patricio Dias M, Harvey B, Loureiro da Silva M, de Sa e Sousa Castelo-Branco M, et al. Optical properties influence visual cortical functional resolution after cataract surgery and both dissociate from subjectively perceived quality of vision. Invest Opthalmol Vis Sci. 2018;59(2):986-994. doi: 10.1167/iovs.17-22321.
39. Guerreiro M, Putzar L, Roder B. The effect of early visual deprivation on the neural bases of multisensory processing. Brain. 2015;138(6):1499-1504. doi: 10.1093/brain/awv076.
40. Lin H, Zhang L, Lin D, Chen W, Zhu Y, Chen C, et al. Visual restoration after cataract surgery promotes functional and structural brain recovery. EBioMedicine. 2018;30:52-61. doi: 10.1016/j.ebiom.2018.03.002.
41. Graw J. From eyeless to neurological diseases. Exp Eye Res. 2017;156:5-9. doi: 10.1016/j.exer.2015.11.006.
42. Wiessner M, Roos A, Munn C, Viswanathan R, Whyte T, Cox D, et al. Mutations in INPP5K, encoding a phosphoinositide 5-phosphatase, cause congenital muscular dystrophy with cataracts and mild cognitive impairment. Am J Hum Genet. 2017;100(3):523-536. doi: 10.1016/j.ajhg.2017.01.024.
43. Plaisier E, Ronco P. COL4A1-Related Disorders. 2009 Jun 25 [updated 2016 Jul 7]. In: Adam MP, Ardinger HH, Pagon RA, Wallace SE, Bean LJH, Stephens K, Amemiya A, editors. GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle; 1993–2020. [cited 20 March 2020]. Available from: https://www.ncbi.nlm.nih.gov/books/NBK7046/
44. Elsaid M, Chalhoub N, Ben-Omran T, Kamel H, AL Mureikhi M, Ibrahim K, et al. Homozygous nonsense mutation in SCHIP1/IQCJ-SCHIP1 causes a neurodevelopmental brain malformation syndrome. Clin Genet. 2017;93(2):387-391. doi: 10.1111/cge.13122.
45. Myers K, Bello-Espinosa L, Kherani A, Wei X, Innes A. TUBA1A mutation associated with eye abnormalities in addition to brain malformation. Pediatr Neurol. 2015;53(5):442-444. doi: 10.1016/j.pediatrneurol.2015.07.004.
46. Zhao T, Goedhart C, Sam P, Sabouny R, Lingrell S, Cornish A, et al. PISD is a mitochondrial disease gene causing skeletal dysplasia, cataracts, and white matter changes. Life Sci Alliance. 2019;2(2):e201900353. doi: 10.26508/lsa.201900353.
47. Wortmann S, Zietkiewicz S, Kousi M, Szklarczyk R, Haack T, Gersting S, et al. CLPB mutations cause 3-methylglutaconic aciduria, progressive brain atrophy, intellectual disability, congenital neutropenia, cataracts, movement disorder. Am J Hum Genet. 2015;96(2):245-257. doi: 10.1016/j.ajhg.2014.12.013.
48. Daneault V, Dumont M, Masse E, Forcier P, Bore A, Lina J, et al. Plasticity in the sensitivity to light in aging: decreased non-visual impact of light on cognitive brain activity in older individuals but no impact of lens replacement. Front Physiol. 2018;9:1557. doi: 10.3389/fphys.2018.01557.
49. Ebitz R, Moore T. Selective modulation of the pupil light reflex by microstimulation of prefrontal cortex. J Neurosci. 2017;37(19):5008-5018. doi: 10.1523/JNEUROSCI.2433-16.2017.
50. Daneault V, Dumont M, Masse E, Forcier P, Bore A, Lina J et al. Plasticity in the sensitivity to light in aging: decreased non-visual impact of light on cognitive brain activity in older individuals but no impact of lens replacement. Front Physiol. 2018;9:1557. doi: 10.3389/fphys.2018.01557.
51. Loganovsky K, Vasilenko Z. Depression and ionizing radiation. Probl Radiac Med Radiobiol. 2013;18:200–219.
52. Lu C, Li Q, Li Y, Lin H, Qu J, Wang Y, et al. Light deprivation produces distinct morphological orchestrations on RGCs and cortical cells in a depressive-like YFP-H mouse model. Neurosci Lett. 2017;659:60-68. doi: 10.1016/j.neulet.2017.08.073.
53. Zhang Y, Li Q, Qu J, Sun C, Wang Y. Alterations of motor cortical microcircuit in a depressive-like mouse model produced by light deprivation. Neuroscience. 2017;341:79-94. doi: 10.1016/j.neuroscience.2016.11.026.
54. Salari V, Scholkmann F, Vimal R, Csaszar N, Aslani M, Bokkon I. Phosphenes, retinal discrete dark noise, negative afterimages and retinogeniculate projections: A new explanatory framework based on endogenous ocular luminescence. Prog Retin Eye Res. 2017;60:101-119. doi: 10.1016/j.preteyeres.2017.07.001.
55. Loganovsky K, Bomko M, Abramenko I, Kuts K, Belous N, Masiuk S, et al. Neuropsychobiological mechanisms of affective and cognitive disorders in the Chornobyl clean-up workers taking into account the specific gene polymorphisms. Probl Radiac Med Radiobiol. 2018;23:373-409. doi: 10.33145/2304-8336-2018-23-373-409.
56. Ahl M, Avdic U, Skoug C, Ali I, Chugh D, Johansson U, et al. Immune response in the eye following epileptic seizures. J Neuroinflammation. 2016;13(1):155. doi: 10.1186/s12974-016-0618-3.
57. You Y, Joseph C, Wang C, Gupta V, Liu S, Yiannikas C, et al. Demyelination precedes axonal loss in the transneuronal spread of human neurodegenerative disease. Brain. 2019;142(2):426-442. doi: 10.1093/brain/awy338.
58. Mendez-Gomez J, Pelletier A, Rougier M, Korobelnik J, Schweitzer C, Delyfer M, et al. Association of retinal nerve fiber layer thickness with brain alterations in the visual and limbic networks in elderly adults without dementia. JAMA Network Open. 2018;1(7):e184406. doi: 10.1001/jamanetworkopen.2018.4406.
59. Liu S, Ong Y, Hilal S, Loke Y, Wong T, Chen C, et al. The association between retinal neuronal layer and brain structure is disrupted in patients with cognitive impairment and Alzheimer’s disease. J Alzheimer's Dis. 2016;54(2):585-595. doi: 10.3233/JAD-160067.
60. Nishioka C, Poh C, Sun S. Diffusion tensor imaging reveals visual pathway damage in patients with mild cognitive impairment and Alzheimer's disease. J Alzheimer's Dis. 2015;45(1):97-107. doi: 10.3233/JAD-141239.
61. Millington R, James-Galton M, Maia Da Silva M, Plant G, Bridge H. Lateralized occipital degeneration in posterior cortical atrophy predicts visual field deficits. NeuroImage: Clin. 2017;14:242-249. doi: 10.1016/j.nicl.2017.01.012.
62. Yoshimine S, Ogawa S, Horiguchi H, Terao M, Miyazaki A, Matsumoto K, et al. Age-related macular degeneration affects the optic radiation white matter projecting to locations of retinal damage. Brain Struct Funct. 2018;223(8):3889-3900. doi: 10.1007/s00429-018-1702-5.
63. Burton C, Schaeffer D, Bobilev A, Pierce J, Rodrigue A, Krafft C, et al. Microstructural differences in visual white matter tracts in people with aniridia. Neuroreport. 2018;29(17):1473-1478. doi: 10.1097/WNR.0000000000001135.
64. Ohno N, Murai H, Suzuki Y, Kiyosawa M, Tokumaru A, Ishii K, et al. Alteration of the optic radiations using diffusion-tensor MRI in patients with retinitis pigmentosa. Br J Ophthalmol. 2015;99(8):1051-1054. doi: 10.1136/bjophthalmol-2014-305809.
65. Rose K, Krema H, Durairaj P, Dangboon W, Chavez Y, Kulasekara S, et al. Retinal perfusion changes in radiation retinopathy. Acta Ophthalmologica. 2018;96(6):e727-e731. doi: 10.1111/aos.13797.
66. Tofilon P, Fike J. The radioresponse of the central nervous system: a dynamic process. Radiat Res. 2000;153(4):357-370. doi: 10.1667/0033-7587(2000)153[0357:trotcn]2.0.co;2.
67. Bennet B, Repacholi M, Carr Zh, editors.Health effects of the Chernobyl accident and special health care programmes. Report of the UN Chernobyl Forum Expert Group «Health» (EGH). Geneva: World Health Organization; 2006.
68. Bazyka D, Buzunov V, Ilyenko I, Loganovsky K. Epidemiology and molecular studies in cerebrovascular disease at the late period after radiation exposure in Chernobyl. In: Mishra K, editor. Biological responses, monitoring and protection from radiation exposure [Internet]. New York: Nova Science Publishers Inc; 2015 [cited 30 March 2020]. p. 69–84. Available from: https://www.novapublishers.com/catalog/ product_info.php?products_id= 53310%7b5%7d10&osCsid
69. Loganovsky K, Bomko M, Chumak S, Loganovska T, Antypchuk K, Perchuk I, et al. Mental health and neuropsychiatric effects. In: Bazyka D, Sushko V, Chumak A, Chumak V, Yanovych L, editors. Health effects of Chornobyl accident - thirty years aftermath [Internet]. Kyiv: DIA; 2016 [cited 30 March 2020]. p. 320–381. Available from: http://nrcrm.gov.ua/downloads/2017/monograph_last.pdf
70. Loganovsky K, Loganovskaja T, Marazziti D. Ecological psychiatry/neuropsychiatry: Is it the right time for its revival? Clin Neuropsychiatry. 2019;16(2):124.
71. Bromet E. Mental health consequences of the Chernobyl disaster. J Radiol Prot. 2012;32(1):71-75. doi: 10.1088/0952-4746/32/1/N71.
72. Bromet E. Emotional consequences of nuclear power plant disasters. Health Phys. 2014;106(2):206-210. doi: 10.1097/HP.0000000000000012.
73. Bromet E, Havenaar J, Guey L. A 25 year retrospective review of the psychological consequences of the Chernobyl accident. Clin Oncol (R Coll Radiol). 2011;23(4):297-305. doi: 10.1016/j.clon.2011.01.501.
74. Havenaar J, Bromet E, Gluzman S. The 30-year mental health legacy of the Chernobyl disaster. World Psychiatry. 2016;15(2):181-182. doi: 10.1002/wps.20335.
75. Monje M, Mizumatsu S, Fike J, Palmer T. Irradiation induces neural precursor-cell dysfunction. Nat Med. 2002;8(9):955-962. doi: 10.1038/nm749.
76. Pascolini D, Mariotti S. Global estimates of visual impairment: 2010. Br J Ophthalmol. 2011;96(5):614-618. doi: 10.1136/bjophthalmol-2011-300539.
77. Asbell P, Dualan I, Mindel J, Brocks D, Ahmad M, Epstein S. Age-related cataract. Lancet. 2005;365(9459):599–609. doi: 10.1016/S0140-6736(05)17911-2.
78. Hall P, Granath F, Lundell M, Olsson K, Holm L. Lenticular opacities in individuals exposed to ionizing radiation in infancy. Radiat Res. 1999;152(2):190–195.
79. Kleiman N. Radiation cataract. Ann ICRP. 2012;41:80–97. doi: 10.1016/j.icrp.2012.06.018.
80. Medvedovsky C. Criteria for the subjective assessment of cataracts. In: NATO advanced research workshop “Ocular radiation risk assessment in populations exposed to environmental radiation contamination”: Program & Abstracts. Kyiv; 1997. p. 23.
81. Merriam G, Focht E. A clinical study of radiation cataract and the relationship to dose. Am J Roentgenol Radium Ther Nucl Med. 1957;77(5):759–785.
82. Rollins W. Notes on x-light. The effect of x-light on the crystalline lens. Boston Med Surg. J. 1903;148:364–365.
83. ICRP. International recommendations on radiological protection. Br J Radiol. 1951;24:46–53.
84. ICRP. Recommendations of the International Commission on Radiological Protection. Br J Radiol. 1955;28(Suppl. 6):1–92.
85. Khan D, Lacasse M, Khan R, Murphy K. Radiation cataractogenesis: the progression of our understanding and its clinical consequences. J Vasc Intervent Radiol. 2017;28(3):412-419. doi: 10.1016/j.jvir.2016.11.043.
86. Ainsbury E, Barnard S, Bright S, Dalke C, Jarrin M, Kunze S, et al. Ionizing radiation induced cataracts: Recent biological and mechanistic developments and perspectives for future research. Mutat Res. 2016;770(Pt B):238-261. doi: 10.1016/j.mrrev.2016.07.010.
87. Fedirko P. [Radiation cataracts as a delayed effect of the Chornobyl accident]. Data Sci Res. 2000;2:46–48. Ukrainian.
88. Fedirko P. Eye: clinic, diagnostics, regularities and risks for development of eye pathology in Chornobyl catastrophe victims. In: Bazyka D, Sushko V, Chumak A, Chumak V, Yanovych L, editors. Health Effects of the Chornobyl Accident – thirty years aftermath. Kyiv: DIA; 2016. p. 406–455.
89. Hamada N. Ionizing radiation sensitivity of the ocular lens and its dose rate dependence. Int J Radiat Biol. 2016;93(10):1024-1034. doi: 10.1080/09553002.2016.1266407.
90. Shore R. Radiation and cataract risk: Impact of recent epidemiologic studies on ICRP judgments. Mutat Res. 2016;770(Pt B):231-237. doi: 10.1016/j.mrrev.2016.06.006.
91. Bouffler S, Ainsbury E, Gilvin P, Harrison J. Radiation-induced cataracts: the Health Protection Agency’s response to the ICRP statement on tissue reactions and recommendation on the dose limit for the eye lens. J Radiol Prot. 2012;32(4):479-488. doi: 10.1088/0952-4746/32/4/479.
92. Loganovsky K, Buzunov V, Napryeyenko O, Antypchuk Y, Bomko M, Chuprovska N, et al. [Mental health and neuropsychiatric effects in clean-up workers]. In: Serdyuk A, Bebeshko V, Bazyka D, editors. [Health Effects of the Chornobyl Catastrophe 1986–2011]. Ternopil: TSMU; Ukrmedknyga; 2011. p. 522–549. Ukrainian.
93. Hamada N, Fujimichi Y, Iwasaki T, Fujii N, Furuhashi M, Kubo E, et al. Emerging issues in radiogenic cataracts and cardiovascular disease. J Radiat Res. 2014;55(5):831-846. doi: 10.1093/jrr/rru036.
94. Bahia S, Blais E, Murugkar S, Chauhan V, Kumarathasan P. Oxidative and nitrative stress-related changes in human lens epithelial cells following exposure to X-rays. Int J Radiat Biol. 2018;94(4):366-373. doi: 10.1080/09553002.2018.1439194.
95. Allen C, Kumar A, Qutob S, Nyiri B, Chauhan V, Murugkar S. Raman micro-spectroscopy analysis of human lens epithelial cells exposed to a low-dose-range of ionizing radiation. Phys Med Biol. 2018;63(2):025002. doi: 10.1088/1361-6560/aaa176.
96. Fedirko P. [Clinical and epidemiological study of occupational diseases of the organ of vision in the victims of the Chornobyl accident (patterns of development, risks, prognosis)] [Dissertation of Doctor of Medical Sciences]. Kyiv: Institute of Occupational Medicine, Academy of Medical Sciences of Ukraine, 2002. Ukrainian.
97. Merriam G, Worgul B. Experimental radiation cataract – its clinical relevance. Bull N Y Acad Med. 1983;59:372–392.
98. . Nakashima E, Neriishi K, Minamoto A. A reanalysis of atomic-bomb cataract data, 2000–2002: a threshold analysis. Health Phys. 2006;90(2):154-160. doi: 10.1097/01.hp.0000175442.03596.63.
99. Neriishi K, Nakashima E, Minamoto A, Fujiwara S, Akahoshi M, Mishima H, et al. Postoperative cataract cases among atomic bomb survivors: radiation dose response and threshold. Radiat Res. 2007;168(4):404-408. doi: 10.1667/RR0928.1.
100. Worgul B, Kundiyev Y, Sergiyenko N, Chumak V, Vitte P, Medvedovsky C, et al. Cataracts among Chernobyl clean-up workers: implications regarding permissible eye exposures. Radiat Res. 2007;167(2):233-243. doi: 10.1667/rr0298.1.
101. Bazyka D, Tronko M, Antypkin Y, Serdiuk A, Sushko V. Thirty years of Chornobyl catastrophe: radiological and health effects. National Report of Ukraine [Internet]. Kyiv: State Instititution “National Research Centre for Radiation Medicine of National Academy of Medical Sciences of Ukraine”; 2016. Available from: http://nrcrm.gov.ua/en/publications/reports
102. Fedirko P. [Methods of detecting lens radiation damage]: methodical recommendations. Kyiv; 1993. Ukrainian.
103. Fedirko P. Specific radiation damages of the eye. In: Thirty Years of Chornobyl Catastrophe: Radiological and Health Effects: National Report of Ukraine. Kyiv; 2016. p. 103-105.
104. Kleiman N, David J, Elliston C, Hopkins K, Smilenov L, Brenner D, et al. Mrad9 and Atm haploinsufficiency enhance spontaneous and X-ray-induced cataractogenesis in mice. Radiat Res. 2007;168(5):567-573. doi: 10.1667/rr1122.1.
105. Fedirko P, Garkava N. [Patterns of development of retinal vascular pathology at remote time period after radiation exposure]. Journal of Ophthalmology (Ukraine). 2016;6:24-28. https://doi.org/10.31288/oftalmolzh201662428. Ukrainian.
106. Fedirko P, Babenko T, Dorichevska R, Garkava N. Retinal vascular pathology risk development in the irradiated at different ages as a result of Chornobyl NPP accident. Probl Radiac Med Radiobiol. 2015;20:467–573.
107. Fedirko P, Garkava N. Microcirculation violations of the conjunctiva in clean-up workers of the Chornobyl NPP accident. Probl Radiac Med Radiobiol. 2016;21:345–351.
108. Korol A. R, Zborovska O, Kustryn T, Dorokhova O, Pasyechnikova N. Intravitreal Aflibercept for choroidal neovascularization associated with Chorioretinitis: a pilot study. Clin Ophthalmol. 2017;11:1315-1320. https: //doi.org: 10.2147/OPTH.S132923.
109. Korol A, Kustryn T, Zadorozhnyy O, Pasyechnikova N, Kozak I. Top of form bottom of form comparison of efficacy of intravitreal ranibizumab and aflibercept in eyes with myopic choroidal neovascularization: 24-month follow-up. J Ocul Pharmacol Ther. 2020;36 (2):122-125 DOI: 10.1089/jop.2019.0080
110. Pasyechnikova N. V, Naumenko V. O, Korol A. R. et. al. Top of form bottom of form intravitreal ranibizumab for the treatment of choroidal neovascularizations associated with pathologic myopia: a prospective study. Ophthalmologica. 2015;233 (1):2-7 DOI: 10.1159/000369397
111. Fedirko P, Babenko T, Kolosynska O, Dorichevska R, Garkava N, Grek L, et al. Morphometric parameters of retinal macular zone in reconvalescents of acute radiation sickness (in remote period). Probl Radiac Med Radiobiol. 2018;23:481-489. https://doi.org: 10.33145/2304-8336-2018-23-481-489
112. Purves D, Augustine G, Fitzpatrick D, Hall W, LaMantia A, Mooney R. et al, editors. Neuroscience. 6th ed. Sunderland, Massachusetts: Oxford University Press; 2018.
113. Flammer J, Mozaffarieh M. What is the present pathogenetic concept of glaucomatous optic neuropathy? Surv Ophthalmol. 2007;52(6):S162-S173. doi: 10.1016/j.survophthal.2007.08.012.
114. Panchenko N. V, Gonchar E. N, Arustamova G. S, et al. [Influence of the fetal neuropeptide complex on changes in retinal light sensitivity over time in patients with primary open-angle glaucoma]. Oftalmologicheskii Zhurnal. 2017;(6):16-19. Ukrainian.
115. Kiuchi Y, Yokoyama T, Takamatsu M, Tsuiki E, Uematsu M, Kinoshita H, et al. Glaucoma in atomic bomb survivors. Radiat Res. 2013;180(4):422-430. doi: 10.1667/RR3273.2.
116. Kiuchi Y, Yanagi M, Itakura K, Takahashi I, Hida A, Ohishi W, et al. Association between radiation, glaucoma subtype, and retinal vessel diameter in atomic bomb survivors. Sci Rep. 2019;9(1):8642. doi: 10.1038/s41598-019-45049-7.
117. Garkava N, Fedirko P, Babenko T, Dorichevska R. Radiation induced violations of blood circulation in the ciliary body and changes of the anterior chamber angle in the pathogenesis of glaucoma in clean/up workers of the Chornobyl NPP accident and residents of contaminated areas. Probl Radiac Med Radiobiol. 2017;22:332-338.
118. Sushko VO, Fedirko P, Harkava N, Kadoshnikova I, Sushko V. [Actual problems of eye protection of the personnel performing works for transformation of the Chornobyl NPP “Shelter” object into the ecologically safe system: retinal vascular changes and data of fluorescent angiography]. Probl Radiac Med Radiobiol. 2012;17:317–323. Ukrainian.
119. Fedіrko P, Vasylenko V, Babenko T, et al. [The peculiarities of angle of anterior chamber and iris in persons, radiation exposed as a result of the Chornobyl accident and their significance for choice of open angle glaucoma treatment]. Tavricheskiy Mediko-Biologicheskiy Vestnik. 2013;16(4):139–141. Ukrainian.
120. Fedirko P, Kadoshnikova I. [The peculiarities of clinical course and treatment of open angle glaucoma in persons, radiation exposed as a result of Chornobyl accident]. Tavricheskiy Mediko-Biologicheskiy Vestnik. 2012;15(3, part 3):194–197. Ukrainian.
121. Shields C, Shields J, Cater J, Othmane I, Singh A. D, Micaily B. Plaque radiotherapy for retinoblastoma: long-term tumor control and treatment complications in 208 tumors. Ophthalmology. 2001;108(11):2116-2121. doi: 10.1016/s0161-6420(01)00797-7.
122. Shields C, Cater J, Shields J, Chao A, Krema H, Materin M, Brady LW. Combined plaque radiotherapy and transpupillary thermotherapy for choroidal melanoma: tumor control and treatment complications in 270 consecutive patients. Arch Ophthalmol. 2002;120(7):933–940. doi: 10.1001/archopht.120.7.933.
123. Dieckmann K, Georg D, Zehetmayer M, Bogner J, Georgopoulos M, Potter R. LINAC based stereotactic radiotherapy of uveal melanoma: 4 years clinical experience. Radiother Oncol. 2003;67(2):199-206. doi: 10.1016/s0167-8140(02)00345-6.
124. Takeda A, Shigematsu N, Suzuki S, Fujii M, Kawata T, Kawaguchi O et al. Late retinal complications of radiation therapy for nasal and paranasal malignancies: relationship between irradiated-dose area and severity. Int J Radiat Oncol Biol Phys. 1999;44(3):599-605. doi: 10.1016/s0360-3016(99)00057-7.
125. Hamada N, Azizova T, Little M. Glaucomagenesis following ionizing radiation exposure. Mutat Res. 2019;779:36-44. doi: 10.1016/j.mrrev.2019.01.001.
126. Azizova T, Haylock R, Moseeva M, Bannikova M, Grigoryeva E. Cerebrovascular diseases incidence and mortality in an extended mayak worker cohort 1948–1982. Radiat Res. 2014;182(5):529–544. doi: 10.1667/RR13680.1.
127. Ivanov V. Late cancer and noncancer risks among Chernobyl emergency workers of Russia. Health Phys. 2007;93(5):470-479. doi: 10.1097/01.HP.0000282195.34508.b0.
128. Buzunov V, Strapko N, Pirogova Y, et al. Epidemiology of non-cancer diseases among Chernobyl accident recovery operation workers. International Journal of Radiation Medicine. 2001;3(3-4):9–25.
129. Boucard C, Hanekamp S, Curcic-Blake B, Ida M, Yoshida M, Cornelissen F. Neurodegeneration beyond the primary visual pathways in a population with a high incidence of normal-pressure glaucoma. Ophthalmic Physiol Opt. 2016;36(3):344-353. doi: 10.1111/opo.12297.
130. Qu X, Wang Q, Chen W, Li T, Guo J, Wang H, et al. Combined machine learning and diffusion tensor imaging reveals altered anatomic fiber connectivity of the brain in primary open-angle glaucoma. Brain Res. 2019;1718:83-90. doi: 10.1016/j.brainres.2019.05.006.
131. Wang R, Tang Z, Sun X, Wu L, Wang J, Zhong Y, et al. White matter abnormalities and correlation with severity in normal tension glaucoma: a whole brain atlas-based diffusion tensor study. Invest Opthalmol Vis Sci. 2018;59(3):1313–1322. doi: 10.1167/iovs.17-23597.
132. Murphy M, Conner I, Teng C, Lawrence J, Safiullah Z, Wang B, et al. Retinal structures and visual cortex activity are impaired prior to clinical vision loss in glaucoma. Sci Rep. 2016;6(1):31464. doi: 10.1038/srep31464.
133. Dunbar S, Tarbell N, Kooy H, Alexander E, Black P, Barnes P, et al. Stereotactic radiotherapy for pediatric and adult brain tumors: Preliminary report. Int J Radiat Oncol Biol Phys. 1994;30(3):531-9. doi: 10.1016/0360-3016(92)90938-e.
134. Armstrong C, Stern C, Corn B. Memory performance used to detect radiation effects on cognitive functioning. Appl Neuropsychol. 2001;8(3):129-39. doi: 10.1207/S15324826AN0803_1.
135. Goldstein B, Obrzut J, John C, Ledakis G, Armstrong C. The impact of frontal and non-frontal brain tumor lesions on Wisconsin Card Sorting Test performance. Brain Cogn. 2004;54(2):110-116. doi: 10.1016/S0278-2626(03)00269-0.
136. Shimizu Y, Kodama K, Nishi N, Kasagi F, Suyama A, Soda M, et al. Radiation exposure and circulatory disease risk: Hiroshima and Nagasaki atomic bomb survivor data, 1950-2003. BMJ. 2010;340(jan14 1):b5349. doi: 10.1136/bmj.b5349.
137. Axmacher N, Mormann F, Fernandez G, Elger C, Fell J. Memory formation by neuronal synchronization. Brain Res Rev. 2006;52(1):170-182. doi: 10.1016/j.brainresrev.2006.01.007.
138. Cohen M. Analyzing neural time series data: theory and practice (Issues in clinical and cognitive neuropsychology). Massachusetts Institute of Technology; 2014.
139. Loganovsky K, Loganovskaja T, Kuts K. Psychophysiology research in the detection of ionizing radiation effects. In: Chiappelli F, editor. Advances in Psychobiology. New York, USA: Nova Science Publisher; 2018. p. 63-152.
140. Loganovsky K, Kuts K. Cognitive evoked potentials P300 after radiation exposure. Probl Radiac Med Radiobiol. 2016;21:264–290.
141. Loganovsky K, Kuts K. Evoked bioelectrical brain activity following exposure to ionizing radiation. Probl Radiac Med Radiobiol. 2017;22:38-68.
142. Kuts K. [Neurocognitive deficit in chronic cerebrovascular pathology in the individuals exposed to ionizing radiation in low doses range due to the Chornobyl accident] [PhD Dissertation]. Kyiv: State Institution “National Research Center for Radiation Medicine of National Academy of Medical Sciences of Ukraine”; 2018. Ukrainian.
143. Acharya M, Baulch J, Klein P, Baddour A, Apodaca L, Kramar E, et al. New concerns for neurocognitive function during deep space exposures to chronic, low dose-rate, neutron radiation. eNeuro. 2019;6(4):ENEURO.0094-19.2019. doi: 10.1523/ENEURO.0094-19.2019.
144. Parihar V, Maroso M, Syage A, Allen B, Angulo M, Soltesz I, et al. Persistent nature of alterations in cognition and neuronal circuit excitability after exposure to simulated cosmic radiation in mice. Exp Neurol. 2018;305:44-55. doi: 10.1016/j.expneurol.2018.03.009.
145. Cucinotta F, Alp M, Sulzman F, Wang M. Space radiation risks to the central nervous system. Life Sciences in Space Research. 2014;2:54-69. https://doi.org/10.1016/j.lssr.2014.06.003
146. Husain M, Scott J. Oxford textbook of cognitive neurology and dementia. Oxford University Press; 2016.
147. Purves D, Augustine G, David Fitzpatrick D, Hall W, LaMantia A, Mooney R et al, editors. Neuroscience. 6th ed. Sunderland, Massachusetts: Oxford University Press; 2018.
148. Ungerleider L, Mishkin M. Two cortical visual streams. In: Ingle D, Goodale M, Mansfield R, editors. Analysis of Behavior. Cambridge, MA: MIT Press; 1983. p. 549–586.
149. Siegel A, Sapru H. Case histories written by Heidi E. Siegel. In: Siegel A, editor. Essential neuroscience. 3rd ed. Lippincott Williams & Wilkins; 2015. p. 604.
150. Epstein R, Kanwisher N. A cortical representation of the local visual environment. Nature. 1998;392(6676):598-601.
151. McGugin R, Gatenby J, Gore J, Gauthier I. High-resolution imaging of expertise reveals reliable object selectivity in the fusiform face area related to perceptual performance. Proc Natl Acad Sci U S A. 2012;109(42):17063-8. doi: 10.1073/pnas.1116333109.
152. Gauthier I, Tarr M, Bub D. Perceptual expertise: bridging brain and behavior. Oxford: Oxford University Press; 1990.
153. Loganovsky K, Loganovskaja T, Nechayev S, Antipchuk Y, Bomko M. Disrupted Development of the dominant hemisphere following prenatal irradiation. J Neuropsychiatry Clin Neurosci. 2008;20(3):274-291.
154. Buckley M, Gaffan D. Perirhinal cortex ablation impairs visual object identification. J Neurosci. 1998;18(6):2268-2275. doi: 10.1523/JNEUROSCI.18-06-02268.1998.
155. Bussey T, Saksida L, Murray E. Impairments in visual discrimination after perirhinal cortex lesions: testing ‘declarative’ vs. ‘perceptual-mnemonic’ views of perirhinal cortex function. Eur J Neurosci. 2003;17(3):649-660. doi: 10.1046/j.1460-9568.2003.02475.x.
156. Buckley M, Booth M, Rolls E, Gaffan D. Selective perceptual impairments after perirhinal cortex ablation. J Neurosci. 2001;21(24):9824-9836. doi: 10.1523/JNEUROSCI.21-24-09824.2001.
157. Barense M, Rogers T, Bussey T, Saksida L, Graham K. Influence of conceptual knowledge on visual object discrimination: insights from semantic dementia and MTL amnesia. Cereb Cortex. 2010;20(11):2568-2582. doi: 10.1093/cercor/bhq004.
158. Barense M, Ngo J, Hung L, Peterson M. Interactions of memory and perception in amnesia: the figure-ground perspective. Cereb Cortex. 2012;22(11):2680-2691. doi: 10.1093/cercor/bhr347.
159. Banich T, Compton R. Cognitive neuroscience. 3rd ed. Cambridge: Cambridge University Press; 2011.
160. Gazzaniga M, Bogen J, Sperry R. Observations on visual perception after disconnexion of the cerebral hemispheres in man. Brain. 1965;88(2):221-236.
161. McTighe S, Cowell R, Winters B, Bussey T, Saksida L. Paradoxical false memory for objects after brain damage. Science. 2010;330(6009):1408-1410. doi: 10.1126/science.1194780.
162. Yeung L, Ryan J, Cowell R, Barense M. Recognition memory impairments caused by false recognition of novel objects. J Exp Psychol General. 2013;142(4):1384-1397. doi: 10.1037/a0034021.
163. Loganovsky KN, Marazziti D, Fedirko PA, Kuts KV, Antypchuk KY, Perchuk IV, et al. Radiation-induced cerebro-ophthalmic effects in humans. Life. 2020;10(4):41. https://doi.org/10.3390/life10040041.