2023 / 03

Следующая статья
DOI: 10.47183/mes.2023.029

ОБЗОР

Влияние средних и малых доз ионизирующего излучения на высшую нервную деятельность человека и животных

Н. И. Атаманюк
Информация об авторах

Уральский научно-практический центр радиационной медицины Федерального медико-биологического агентства, Челябинск, Россия

Для корреспонденции: Наталья Игоревна Атаманюк
ул. Воровского, д. 68 А, г. Челябинск, 454141, Россия; ur.liam@arhlup_ativ

Статья получена: 24.06.2023 Статья принята к печати: 07.08.2023 Опубликовано online: 25.09.2023
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  1. Kovalchuk A, Kolb B. Low dose radiation effects on the brain — from mechanisms and behavioral outcomes to mitigation strategies. Cell Cycle. 2017; 16 (13): 1266–70. PubMed PMID: 28656797.
  2. Britten RA, Wellman LL, Sanford LD. Progressive increase in the complexity and translatability of rodent testing to assess spaceradiation induced cognitive impairment. Neurosci Biobehav Rev. 2021; 126: 159–74. PubMed PMID: 33766676.
  3. Pasqual E, Boussin F, Bazyka D, Nordenskjold A, Yamada M, Ozasa K, et al. Cognitive effects of low dose of ionizing radiation — Lessons learned and research gaps from epidemiological and biological studies. Environ Int. 2021; 147: 106295. PubMed PMID: 33341586.
  4. Sources, effects and risks of ionizing radiation. UNSCEAR 2012 Report. United Nations sales publication E.16.IX.1. 2015. Available from: https://www.unscear.org/docs/reports/2012/ UNSCEAR2012Report_15-08936_eBook_website.pdf.
  5. Stewart FA, Akleyev AV, Hauer-Jensen M, Hendry JH, Kleiman NJ, Macvittie TJ, et al. 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; (1-2): 1–322. DOI: 10.1016/j.icrp.2012.02.001.
  6. Sources, effects and risks of ionizing radiation. Volume II: Scientific annex B. UNSCEAR 2013 Report. United Nations sales publication E.14.IX.2. 2013. Available from: https://www.unscear.org/docs/publications/2013/UNSCEAR_2013_Report_Vol.II.pdf.
  7. Report № 183. Radiation exposure in space and the potential for central nervous system effects: Phase II. 2019. Available from: https://www.researchgate.net/publication/337440807_Radiation_Exposure_in_Space_and_the_Potential_for_Central_Nervous_System_Effects_Phase_II
  8. Tanguturi SK, Alexander BM. Neurologic complications of radiation therapy. Neurol Clin. 2018; 36 (3): 599–625. PubMed PMID: 30072073.
  9. Gorbunov NV, Kiang JG. brain damage and patterns of neurovascular disorder after ionizing irradiation. Complications in radiotherapy and radiation combined injury. Radiat Res. 2021; 196 (1): 1–16. PubMed PMID: 33979447.
  10. Sultana N, Sun C, Katsube T, Wang B. Biomarkers of brain damage induced by radiotherapy. dose response. 2020; 18 (3): 1559325820938279. PubMed PMID: 32694960.
  11. Hall P, Adami HO, Trichopoulos D, Pedersen NL, Lagiou P, Ekbom A et al. Effect of low doses of ionising radiation in infancy on cognitive function in adulthood: Swedish population based cohort study. BMJ. 2004; 328 (7430): 19. PubMed PMID.
  12. Буртовая Е. Ю., Кантина Т. Э., Белова М. В., Аклеев А. В. Когнитивные нарушения у лиц, подвергшихся радиационному воздействию в период пренатального развития. Журнал неврологии и психиатрии им. C. C. Корсакова. 2015; 115 (4): 20–23.
  13. Pasqual E, Bosch de Basea M, López-Vicente M, Thierry-Chef I, Cardis E. Neurodevelopmental effects of low dose ionizing radiation exposure: A systematic review of the epidemiological evidence. Environ Int. 2020; 136: 105371. PubMed PMID: 32007921.
  14. Azizova TV, Bannikova MV, Grigoryeva ES, Rybkina VL, Hamada N. Occupational exposure to chronic ionizing radiation increases risk of Parkinson's disease incidence in Russian Mayak workers. Int J Epidemiol. 2020; 49 (2): 435–47. PubMed PMID: 31722376.
  15. Laurent O, Samson E, Caër-Lorho S, Fournier L, Laurier D, Leuraud K. Updated Mortality Analysis of SELTINE, the French Cohort of Nuclear Workers, 1968–2014. Cancers (Basel). 2022; 15 (1): 79. PubMed PMID: 36612076.
  16. Ishihara K, Kato N, Misumi M, Kitamura H, Hida A, Yamada M. Radiation effects on late-life neurocognitive function in childhood atomic bomb survivors: a radiation effects research foundation adult health study. Radiat Res. 2022; 197 (4): 403–7. PubMed PMID: 35042238.
  17. Kinoshita H, Tanaka K, Nakao R, Iso F, Honda S, Tanaka G, et al. Comparison of mental cognitive function of A-bomb survivors and non-A-bomb survivors in Nagasaki. Psychiatry Clin Neurosci. 2019; 73 (9): 594. PubMed PMID: 31206900.
  18. Lopes J, Leuraud K, Klokov D, Durand C, Bernier MO, Baudin C. Risk of developing non-cancerous central nervous system diseases due to ionizing radiation exposure during adulthood: systematic review and meta-analyses. Brain Sci. 2022; 12 (8): 984. PubMed PMID: 35892428.
  19. Loganovsky K, Marazziti D. Mental health and neuropsychiatric aftermath 35 years after the chernobyl catastrophe: current state and future perspectives. Clin Neuropsychiatry. 2021; 18 (2): 101– 6. PubMed PMID.
  20. Collett G, Craenen K, Young W, Gilhooly M, Anderson RM. The psychological consequences of (perceived) ionizing radiation exposure: a review on its role in radiation-induced cognitive dysfunction. Int J Radiat Biol. 2020; 96 (9): 1104–18. PubMed PMID: 32716221.
  21. Lopes J, Baudin C, Leuraud K, Klokov D, Bernier MO. Ionizing radiation exposure during adulthood and risk of developing central nervous system tumors: systematic review and meta-analysis. Sci Rep. 2022; 12 (1): 16209. PubMed PMID: 36171442.
  22. Little MP, Wakeford R, Bouffler SD, Abalo K, Hauptmann M, Hamada N, et al. Review of the risk of cancer following low and moderate doses of sparsely ionising radiation received in early life in groups with individually estimated doses. Environ Int. 2022; 159: 106983. PubMed PMID.
  23. Perez WD, Perez-Torres CJ. Neurocognitive and radiological changes after cranial radiation therapy in humans and rodents: a systematic review. Int J Radiat Biol. 2023; 99 (2): 119–37. PubMed PMID: 35511499.
  24. Severyukhin YS, Lalkovičová M, Utina DM, Lyakhova KN, Kolesnikova IA, Ermolaeva ME, et al. Comparative analysis of behavioral reactions and morphological changes in the rat brain after exposure to ionizing radiation with different physical characteristics. Cell Mol Neurobiol. 2023; 43 (1): 339–53. PubMed PMID: 34982311.
  25. Njamnshi AK, Ahidjo N, Ngarka L, Nfor LN, Mengnjo MK, Njamnshi WY, et al. Characterization of the cognitive and motor changes revealed by the elevated plus maze in an experimental rat model of radiation-induced brain injury. Adv Biomed Res. 2020; 9: 72. PubMed PMID: 33816391.
  26. Kempf SJ, Casciati A, Buratovic S, Janik D, von Toerne C, Ueffing M, et al. The cognitive defects of neonatally irradiated mice are accompanied by changed synaptic plasticity, adult neurogenesis and neuroinflammation. Mol Neurodegener. 2014; 9: 57. PubMed PMID.
  27. Cacao E, Kapukotuwa S, Cucinotta FA. Modeling reveals the dependence of hippocampal neurogenesis radiosensitivity on age and strain of rats. Front Neurosci. 2018; 12: 980. PubMed PMID.
  28. Serrano C, Dos Santos M, Kereselidze D, Beugnies L, Lestaevel P, Poirier R, et al. Targeted dorsal dentate gyrus or whole brain irradiation in juvenile mice differently affects spatial memory and adult hippocampal neurogenesis. Biology (Basel). 2021; 10 (3): 192. PubMed PMID: 33806303.
  29. Casciati A, Dobos K, Antonelli F, Benedek A, Kempf SJ, Bellés M, et al. Age-related effects of X-ray irradiation on mouse hippocampus. Oncotarget. 2016; 7 (19): 28040–58. PubMed PMID: 27057631.
  30. Ung MC, Garrett L, Dalke C, Leitner V, Dragosa D, Hladik D, et al. Dose-dependent long-term effects of a single radiation event on behaviour and glial cells. Int J Radiat Biol. 2021; 97 (2): 156–69. PubMed PMID: 33264576.
  31. Acharya MM, Patel NH, Craver BM, Tran KK, Giedzinski E, Tseng BP, et al. Consequences of low dose ionizing radiation exposure on the hippocampal microenvironment. PLoS One. 2015; 10 (6): e0128316. PubMed PMID: 26042591.
  32. Eriksson P, Buratovic S, Fredriksson A, Stenerlöw B, SundellBergman S. Neonatal exposure to whole body ionizing radiation induces adult neurobehavioural defects: Critical period, dose-response effects and strain and sex comparison. Behav Brain Res. 2016; 304: 11–9. PubMed PMID: 26876140.
  33. Liu Y, Ma H, Wang Y, Ren B, Liu L, Sun A, et al. Neonatal exposure to low-dose X-ray causes behavioral defects and abnormal hippocampal development in mice. IUBMB Life. 2023; 75 (6): 530–47. PubMed PMID: 36629313.
  34. Verreet T, Rangarajan JR, Quintens R, Verslegers M, Lo AC, Govaerts K, et al. Persistent Impact of in utero irradiation on mouse brain structure and function characterized by mr imaging and behavioral analysis. Front Behav Neurosci. 2016; 10: 83. PubMed PMID: 27199692.
  35. Buratovic S, Stenerlöw B, Fredriksson A, Sundell-Bergman S, Viberg H, Eriksson P. Neonatal exposure to a moderate dose of ionizing radiation causes behavioural defects and altered levels of tau protein in mice. Neurotoxicology. 2014; 45: 48–55. PubMed PMID: 25265567.
  36. Mouton L, Etienne O, Feat-Vetel J, Barrière DA, Pérès EA, Boumezbeur F, et al. Noninvasive assessment of neurodevelopmental disorders after in utero irradiation in mice: an in vivo anatomical and diffusion mri study. Radiat Res. 2021; 195 (6): 568–83. PubMed PMID: 33826744.
  37. Barazzuol L, Hopkins SR, Ju L, Jeggo PA. Distinct response of adult neural stem cells to low versus high dose ionising radiation. DNA Repair (Amst). 2019; 76: 70–75. PubMed PMID: 30822688.
  38. Betlazar C, Middleton RJ, Howell N, Storer B, Davis E, Davies J, et al. Mitochondrial Translocator protein (TSPO) expression in the brain after whole body gamma irradiation. Front Cell Dev Biol. 2021; 9: 715444. PubMed PMID: 34760884.
  39. Hladik D, Buratovic S, Von Toerne C, Azimzadeh O, Subedi P, Philipp J, et al. Combined Treatment with low-dose ionizing radiation and ketamine induces adverse changes in CA1 neuronal structure in male murine hippocampi. Int J Mol Sci. 2019; 20 (23): 6103. PubMed PMID: 31817026.
  40. Matar M, Gokoglu SA, Prelich MT, Gallo CA, Iqbal AK, Britten RA, et al. Machine Learning models to predict cognitive impairment of rodents subjected to space radiation. Front Syst Neurosci. 2021; 15: 713131. PubMed PMID: 34588962.
  41. Whoolery CW, Walker AK, Richardson DR, Lucero MJ, Reynolds RP, Beddow DH, et al. Whole-Body exposure to 28Si-Radiation dosedependently disrupts dentate gyrus neurogenesis and proliferation in the short term and new neuron survival and contextual fear conditioning in the long term. Radiat Res. 2017; 188 (5): 532–51. PubMed PMID: 28945526.
  42. Parihar VK, Maroso M, Syage A, Allen BD, Angulo MC, 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. PubMed PMID: 29540322.
  43. Klein PM, Alaghband Y, Doan NL, Ru N, Drayson OGG, Baulch JE, et al. Acute, Low-dose neutron exposures adversely impact central nervous system function. Int J Mol Sci. 2021; 22 (16): 9020. PubMed PMID: 34445726.
  44. Laiakis EC, Pinheiro M, Nguyen T, Nguyen H, Beheshti A, Dutta SM, et al. Quantitative proteomic analytic approaches to identify metabolic changes in the medial prefrontal cortex of rats exposed to space radiation. Front Physiol. 2022; 13: 971282. PubMed PMID: 36091373.
  45. Britten RA, Jewell JS, Duncan VD, Hadley MM, Macadat E, Musto AE, et al. Impaired attentional set-shifting performance after exposure to 5 cgy of 600 mev/n 28si particles. Radiat Res. 2018; 189 (3): 273–82. PubMed PMID: 29309264.
  46. Soler I, Yun S, Reynolds RP, Whoolery CW, Tran FH, Kumar PL, et al. Multi-domain touchscreen-based cognitive assessment of C57BL/6J female mice shows whole-body exposure to 56Fe particle space radiation in maturity improves discrimination learning yet impairs stimulus-response rule-based habit learning. Front Behav Neurosci. 2021; 15: 722780. PubMed PMID: 34707486.
  47. Acharya MM, Baulch JE, Klein PM, Baddour AAD, Apodaca LA, Kramár EA, 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. PubMed PMID: 31383727.
  48. Krishnan B, Natarajan C, Bourne KZ, Alikhani L, Wang J, Sowa A, et al. Chronic low dose neutron exposure results in altered neurotransmission properties of the hippocampus-prefrontal cortex axis in both mice and rats. Int J Mol Sci. 2021; 22 (7): 3668. PubMed PMID: 33915974.
  49. Koturbash I, Jadavji NM, Kutanzi K, Rodriguez-Juarez R, Kogosov D, Metz GAS, et al. Fractionated low-dose exposure to ionizing radiation leads to DNA damage, epigenetic dysregulation, and behavioral impairment. Environ Epigenet. 2017; 2 (4): dvw025. PubMed PMID: 29492301.
  50. Peng S, Yang B, Duan MY, Liu ZW, Wang WF, Zhang XZ, et al. The disparity of impairment of neurogenesis and cognition after acute or fractionated radiation exposure in adolescent BALB/c mice. Dose Response. 2019; 17 (1): 1559325818822574. PubMed PMID: 30670940.
  51. Alaghband Y, Klein PM, Kramár EA, Cranston MN, Perry BC, Shelerud LM, et al. Galactic cosmic radiation exposure causes multifaceted neurocognitive impairments. Cell Mol Life Sci. 2023; 80 (1): 29. PubMed PMID: 36607431.
  52. Schmal Z, Rübe CE. Region-specific effects of fractionated lowdose versus single-dose radiation on hippocampal neurogenesis and neuroinflammation. Cancers (Basel). 2022; 14 (22): 5477. PubMed PMID: 36428572.
  53. Biological Mechanisms of Radiation Actions at Low doses. A white paper to guide the Scientific Committee's future programme of work. United Nations Scientific Committee on the Effects of Atomic Radiation, United Nations. 2012. Available from: https:// www.unscear.org/docs/reports/Biological_mechanisms_WP_1257831.pdf.
  54. Котеров А. Н., Вайсон А. А. Биологические и медицинские эффекты излучения с низкой ЛПЭ для различных диапазонов доз. Медицинская радиология и радиационная безопасность. 2015; 60 (3): 5–31.
  55. Boyd A, Byrne S, Middleton RJ, Banati RB, Liu GJ. Control of neuroinflammation through radiation-induced microglial changes. Cells. 2021; 10 (9): 2381. PubMed PMID: 34572030.
  56. Kempf SJ, Janik D, Barjaktarovic Z, Braga-Tanaka I 3rd, Tanaka S, Neff F, et al. Chronic low-dose-rate ionising radiation affects the hippocampal phosphoproteome in the ApoE-/- Alzheimer's mouse model. Oncotarget. 2016; 7 (44): 71817–32. PubMed PMID: 27708245.