International Journal of Psychophysiology 30 Ž1998. 303]311
Psychophysiologic aftereffects of prenatal irradiation Angelina I. Nyagu, Konstantin N. LoganovskyU , Tatiana K. Loganovskaja Neurology Department, Institute of Clinical Radiology, Scientific Center for Radiation Medicine, Academy of Medical Sciences of the Ukraine, 53 Melniko¨ Street, Kie¨ 254050, Ukraine Received 23 January 1997; revised 2 February 1998; accepted 3 February 1998
Abstract Prenatally irradiated children Ž n s 544., who were born between 26 April 1986 and 26 February 1987, in regions of the Ukraine which were radioactively contaminated as a result of the Chernobyl disaster, their mothers and teachers have been examined with psychometric tests. The control group of relevant children Ž n s 759., their mothers and teachers, were living at the radioecological ‘clear’ regions ŽKharkov and Kharkov Region.. Further, we randomly selected 50 prenatally irradiated children whose mothers were evacuated from the Chernobyl exclusion zone and 50 age-and-gender-matched non-exposed children. At this phase clinical examinations, psychometric tests, computerized EEG, thyroid function assessment and dosimetric reconstruction were used. We found a significant increase in mental retardation ŽIQ - 70. and of borderline and low range IQ, as well as emotional and behavioral disorders and a decrease in high IQ ŽIQ ) 110. in children irradiated in utero as a result of the Chernobyl disaster, in comparison with the controls. One important biological mechanism in the genesis of mental disorders in prenatally irradiated children is the radiation-induced malfunction of the thyroid]pituitary system with the effect threshold of 0.30 Sv of thyroid exposure dose. We hypothesize that the cerebral basis of mental disorders in the prenatally irradiated children is the malfunction of the left hemisphere limbic]reticular structures, particularly in those exposed at the most critical period of cerebrogenesis Ž8]25 weeks of gestation.. The data obtained reveal mental disorders in prenatally irradiated children and obviously reflect developmental abnormalities of brain structure and function as a result of the interaction of prenatal and post-natal factors where it is possible to assume radiation effects on the developing brain. A follow-up study of the children irradiated in utero, who may be at risk for schizophrenia, is proposed because of its particular importance to clinical medicine and neuroscience. Q 1998 Elsevier Science B.V. All rights reserved. Keywords: Psychophysiology; Brain damage in utero; Chernobyl disaster; Prenatal irradiation
U
Corresponding author: Tel.: q380 44 4319839, q380 44 4649138 Žhome.; fax: q380 44 2137202, q380 44 4649138 Žhome..
0167-8760r98r$ - see front matter Q 1998 Elsevier Science B.V. All rights reserved. PII S0167-8760Ž98.00022-1
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If radiosensitivity of the mature nervous system is a basis for discussion during one century, then radiovulnerability of the developing nervous system is axiomatic ŽLebedinsky and Nakhilniztskaja, 1960; Livanov, 1962; Grigoriev, 1963; Kimeldorf and Hunt, 1969; Yaar et al., 1980, 1982; Kriegel et al., 1986; Davydov and Ushakov, 1987.. Japanese studies have pointed out stages in development during which the human brain is particularly susceptible to damage. Exposure at critical junctures in development increases the risk of mental retardation, small head size, subsequent seizures and poor performance on conventional tests of intelligence and in school. The most critical period, from 8 to 15 weeks of gestation, corresponds to that time in brain development when increases of neuronal production and migration of immature neurons to their cortical sites of function occur. A recent reanalysis of the dosimetry data ŽOtake et al., 1996. indicated that the dose threshold for mental retardation development after intrauterine irradiation at gestation terms of 8]15 weeks is 0.06]0.31 Gy w1 Gy } unit of absorbed dose of ionizing radiation s 100 rad Žradiation absorbed dose. regarding the Chernobyl accident 1 Svf 1 Gyx and at gestation terms from 16]25 weeks to 0.25]0.87 Gy. In persons irradiated in utero at gestation terms of 8]15 weeks the ‘dose]effect’ dependence concerning IQ decrease has been surveyed as follows: approximately 30 IQ point decrease per 1 Gy of prenatal irradiation ŽSchull and Otake, 1986; Otake et al., 1989; Yamazaki and Schull, 1990; Otake et al., 1991.. The question of the increased prevalence of schizophrenia in prenatally irradiated A-bomb survivors is open to discussion ŽImamura et al., 1995.. In contrast to studies noted above, results of psychophysiological investigations in prenatally irradiated populations are limited ŽNyagu et al., 1996a,b; Igumnov, 1996; Loganovskaya and Loganovsky, 1997.. The goal of this study is to investigate the psychophysiologic aftermath of prenatal exposure to ionizing radiation as a result of the Chernobyl disaster. This study includes two phases: Ž1. screening and Ž2. in-depth psychophysiologic research. The ‘experimental’ Ž n s 544. group Žprenatally
irradiated children. consisted of children of women who had been pregnant and lived in the selected areas Žsee below. on the day of the Chernobyl disaster. It is presumed that their pregnancies would have been completed between 26 April 1986 and 26 February 1987. In addition to the children, the mothers and the teachers were also involved in the study. The ‘experimental’ group included evacuated children from the 30-km Chernobyl exclusion zone, n s 115 Ž21%.; children living in so-called strictly controlled zones where contamination exceeds 15 Cirkm2 , n s 234 Ž43%.; and children living in the region with moderate contamination 1]15 Cirkm2 , n s 195 Ž36%.. The control group included 795 children, their parents and teachers, living in the radioactively ‘clean’ zones Žthe city of Kharkov and Kharkov province.. There were 289 boys Ž53%. and 255 girls Ž47%. in the ‘experimental’ group and 413 boys Ž54%. and 346 girls Ž46%. in the control group. Among the children of the ‘experimental’ group, there were 65 Ž12%. children with early terms of gestation Ž0]7 weeks. at the time of the Chernobyl disaster; 104 Ž19%. children at the critical period of early cerebrogenesis Ž8]15 weeks.; 167 Ž31%. children at the critical period of corticogenesis Ž16]25 weeks.; and 208 Ž38%. children with late terms of gestation Ž) 26 weeks.. The children were 6]8 years old. All the children involved in the study attended the public kindergartens and schools. The childrens’ non-verbal intelligence has been estimated with the ‘Draw-a-Man’ test and the ‘Raven Coloured Matrices’ ŽRaven, 1986. and a verbal one } the ‘British Picture Vocabulary Scale ŽBPVS.’ test ŽDunn and Dunn, 1982.. The emotional and behavioral disorders were evaluated with Rutter scales AŽ2., filled in by parents and the Rutter scale BŽ2., filled in by the teachers ŽVenables et al., 1983.. At the present time the Ukrainian norms for the above tests are absent. However, we used the western norms in both ‘experimental’ and control groups of children, that allowed us to analyze relative differences between groups. The general health questionnaire ŽGHQ28. has been used to estimate the mothers’ mental health. Verbal intelligence of parents was estimated with the Vocabulary subtest of the Wech-
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sler Adult Intelligence Scales ŽWAIS.. Statistical processing included descriptive summarizing data, Student’s t-test, x 2-test and correlation analysis ŽKuzma, 1984.. At the second phase of this study Ž1995]1996. we randomly selected 50 prenatally irradiated children born from women evacuated from the exclusion zone and 50 non-exposed children Žageand- gender-matched control group.. The subjects were right-handed, 9]10-year-old children. The average individual doses of a whole fetus of these prenatally irradiated children consisted of 7 " 2 mSv w1 Sv } unit of effective dose of ionizing radiation s 100 rem Žrad equivalent in man.x but the individual thyroid doses were 100]1200 mSv. Thyroid function assessment and the content of thyroid hormones in blood serum has also been carried out in these children. Examination of the level of neuropsychiatric development of these children included the same methodology that was used at the first stage of the study. Mental disorders have been classified according to the ICD10 criteria. Moreover, we carried out a 19-channel computerized EEG ŽCEEG. evaluation. Distribution of the IQ scores according to the ‘Draw-A-Man’ test, ‘Raven Coloured Matrices’ and ‘BPVS’ in the prenatally irradiated children and non-exposed control children is presented in Fig. 1. In the ‘experimental’ group in comparison with the control one there was a statistically significant increase of children with reduced intellectual abilities ŽIQ s 70]90. as well as significant decrease of children with high intellectual abilities ŽIQ s 110]140. and intellectually gifted children ŽIQ ) 140. according to all three non-verbal and verbal intelligence tests. The IQ integral decrease calculation has been carried out on the basis of two algorithms: ŽA. IQ - 70 simultaneously according to the Raven’s and BPVS tests; ŽB. IQ - 70 according to any two used tests. Basing on the algorithm ‘A’ the IQ 70 has been revealed in 19 Ž3.49%. children from the ‘experimental’ group and 8 Ž1.05%. from the controls Ž x 2 s 8.9; P- 0.01.. According to the algorithm ‘B’ in 23 Ž4.34%. and 16 Ž2.1%. correspondingly Ž x 2 s 4.6; P- 0.05.. Therefore according to both ways, the IQ - 70 or mental retardation ŽICD-10., there were statistically sig-
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nificant increases in the prenatally irradiated children compared to controls. Emotional and behavioral disorders have been diagnosed significantly more frequently among the prenatally irradiated children than in the controls. According to the Rutter AŽ2. scale emotional and behavioral disorders have been revealed in 245 Ž45%. children of the ‘experimental’ group and in 220 Ž29%. children only in the control group Ž x 2 s 35.6, P- 0.001.. The Vocabulary subtest of the WAIS has indicated that mothers’ verbal intellectual level is lower in the ‘experimental’ group than in the controls: 33.6" 0.6 and 43.6" 0.5 raw scores respectively Ž P- 0.05.. According to data obtained from the GHQ-28 the mental health of parents from the ‘experimental’ group is worse Ž P- 0.05. than that of the controls: 24.26" 0.4 and 20.73" 0.5 scores respectively Žfollowing scale 0-0-1-2 estimation criteria .. No statistically significant differences have been revealed among anthropometry values Žnewborn weight and height. between children of the ‘experimental’ and control groups. The higher number of intranatal complications Ž P- 0.05. has been surveyed in the ’experimental‘ group compared to that in the control. The relative risks of 0.74 for the non-verbal IQ scores Ž‘Raven Coloured Matrices’. and 0.79 for the verbal IQ scores Ž‘BPVS’. indicate that exposure at the critical period of early cerebrogenesis Ž8]15 weeks of gestation. is associated with some reduction of children’s intelligence. The relative risks of 1.95 for non-verbal IQ scores Ž‘Draw-aMan’., 1.53 Ž‘Raven Coloured Matrices’. and 1.94 for verbal IQ scores Ž‘BPVS’. indicate that high level of mothers’ verbal IQ is associated with practically a twofold increase in high intelligence of children. In other words, in order to have high intelligence in a child the mother should also have high intelligence. However, as it had been shown earlier, the mothers of the ‘experimental’ group have lower verbal IQ than controls Ž P0.05.. According to the results of a correlation analysis, it has been revealed that both the mothers’ health and intranatal complications are significantly related Ž P- 0.01. to the mental disorders in children of both ‘experimental’ and con-
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Fig. 1. Distribution of IQ scores in the prenatally irradiated children Ž‘Experimental’ group. and non-exposed control children.
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trol group. The data analysis has also revealed the statistically significant correlation between intellectual development worsening and exposure to ionizing radiation according to the amount of radioactive contamination in the territory, 137 Cs Ž r s 0.3, P- 0.01.. Thus, in the screening phase of the study we established a significant increase of both mental retardation ŽIQ - 70. as well as borderline and low range IQ Ž70]90 scores. concurrent with a significant decrease of high IQ Ž) 110 scores. in the children irradiated in utero as a result of the Chernobyl disaster in comparison with the control. Moreover, emotional and behavioral disorders have been diagnosed significantly more frequently among the prenatally irradiated children than in the controls. At the same time the mental health of mothers of irradiated in utero children is worse than that in the control. We propose that the mental morbidity increase in the prenatally irradiated children could be explained by a combination of prenatal exposure to ionizing radiation and social, non-favorable, factors of the Chernobyl disaster aftermath. In the second phase of the study we found a statistically significant increase in the number of children with reduced intellectual abilities ŽIQ s 70]90. according to all three non-verbal and verbal intelligence tests, as well as significant decreases in children with high verbal intellectual abilities ŽIQ s 110]140. according to the ‘BPVS’. According to the Rutter AŽ2. scale, emotional and behavioral disorders have been revealed in 29 Ž58%. exposed children and in only 12 Ž24%. children in the control group Ž x 2 s 11.9, P0.01.. The Vocabulary subtest of the WAIS has indicated that mothers‘’verbal intellectual level is lower in the ‘experimental’ group than in the controls: 37.8" 1.2 and 45.3" 1.1 raw scores respectively Ž P- 0.05.. According to the data obtained from the GHQ-28, the mental health of parents from the ‘experimental’ group is worse Ž P- 0.01. than that in controls: 27.4" 1.1 and 18.1" 1.2 scores respectively Žfollowing scale 0-01-2 estimation criteria .. Hence, it is possible to assume, that those randomly selected 50 prenatally children and 50 non-exposed children are representative for the cohort of children irradi-
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ated in utero as a result of the Chernobyl disaster and control children of Ukraine. According to the clinical data obtained, the exposed children aged 9]10 years manifested a significant increase of mental and behavioral disorders in comparison with the control group children ŽTable 1.. In the prenatally irradiated children we found a higher frequency of autonomic nervous system instability and soft neurological signs, as well as disorders of psychological development and behavioral and emotional disorders, with onset usually occurring in childhood and adolescence. As a result, one or more mental disorders according to the ICD-10 criteria has been diagnosed in 36 Ž72%. of the exposed children in comparison with 14 Ž28%. of the control children only Ž P- 0.01.. In 50 children born from pregnant women evacuated from the Chernobyl exclusion zone we revealed a significantly higher frequency Ž P0.01. of abnormalities of thyroid gland Žnodular goiter, thyroid tissue fibrosis and sclerosis. as compared to the control group. In hormonal data analysis depending on in utero thyroid exposure individual doses the confidential Ž P- 0.01. and moderate Ž r s 0.5]0.6. unidirectional dependence ‘dose-effect’ has been revealed: the thyrotropic hormone ŽTTH. level grows with thyroid exposure dose increase with a 0.30 Sv threshold. Taking into account the free T4 serum content normal levels, the present data confirm the direct dependence between hypothyroidism development risk level and prenatal thyroid exposure dose with a threshold of 0.30 Sv. The correlation analysis has revealed the emotional and behavioral disorders wRutter scale AŽ2.x increase with prenatal thyroid exposure Ž P- 0.05.. In addition, the non-verbal intellect estimated with the ‘Draw-a-Man’ test was worse Ž P- 0.05. for children with prenatal thyroid exposure Ždoses over 0.30 Sv. than for those with less than 0.30 Sv. The mental disorders registration, including mental retardation, in case of thyroid disorders are well known ŽHetzel, 1994; Xue-Yi et al., 1994.. Thus it seems possible to connect the revealed intellectual and emotional disorders in the prenatally irradiated children with radiation-induced pathology of the thyroid. The abnormal EEG-patterns in these 50 prena-
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Table 1 Mental disorders according to ICD-10 criteria in prenatally irradiated and control children ICD-10 code
F80]F89 disorders of psychological development F80 Specific developmental disorders of speech and language
Irradiated in utero Ž n s 50.
x2
P
Control Ž n s 50.
11 Ž22%.
5.32
- 0.05
3 Ž6%.
F80 Specific developmental disorders of scholastic skills
15 Ž30%.
6.25
- 0.05
5 Ž10%.
F82 Specific developmental disorders of motor function
8 Ž16%.
4.0
- 0.05
2 Ž4%.
6 Ž12%.
3.84
- 0.05
1 Ž2%.
F93 Emotional disorders with onset specific to childhood
16 Ž32%.
9.0
- 0.01
4 Ž8%.
F94 Disorders of social functioning with onset specific to childhood and adolescence
1 Ž2%.
1.01
) 0.05
0
F98 Other behavioral and emotional disorders with onset usually occurring in childhood and adolescence
13 Ž26%.
4.34
- 0.05
5 Ž10%.
36 Ž72%.
19.36
- 0.01
14 Ž28%.
F90]F98 Behavioral and emotional disorders with onset usually occurring in childhood and adolescence F90 Hyperkinetic disorders
One or more diagnoses
tally irradiated children have been revealed significantly more frequently than that in the nonexposed ones Ž74% vs. 10%, x 2 s 29.27, P0.001.. It obviously reflects the developing brain functional-structural organization disorders in the exposed children. The disorganized slow EEGpattern with d-activity domination Ž46% vs. 16%, x 2 s 10.52, P- 0.01. characterized with the disorganized activity of moderate or high amplitude with mainly d-range slow activity domination and non-regular a-activity, where hyperventilation led to bilateral paroxysmal activity discharges. The disorganized EEG-pattern with paroxysmal activity Ž28% vs. 4%, x 2 s 10.71, P- 0.01. was similar in general with that described above, but characterized by generalized paroxysmal discharges and bursts of acute, u-waves and d-waves of high amplitude, where hyperventilation led to bilateral
paroxysmal activity increase. The irradiated in utero children differed also from the controls in the epileptiform activity presence Ž16% vs. 0%, x 2 s 8.7, P- 0.01., in the form of ‘spike’ or ‘polyspike-wave’ complexes in fronto-temporal regions of left hemispheres and bilateral paroxysmal activity in the form of acute and d-waves of high amplitude Žhigher than 100 mV.. The interhemispheric asymmetry in EEG has been revealed significantly more frequently in the exposed children as compared to the control children Ž86% vs. 36%, x 2 s 26.27, P- 0.001. according to the asymmetry index ) 5%. The symmetrical EEG pattern characteristic for normally developing children has been revealed in 32 Ž64%. of the non-exposed children and has been significantly less in children irradiated in utero Ž7 Ž14%., x 2 s 26.27, P- 0.001.. The left-hemispherical EEG-
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pattern was characterized with abnormal activity shifted into the fronto-temporal region together with a-activity depression in the left hemisphere. The left-hemispherical type of EEG-laterality has been found more often among the children exposed in utero in comparison with the control Ž40% vs. 12%, x 2 s 10.19, P- 0.01.. According to the data obtained from the spectral EEG-analysis, a significant difference between the exposed and non-exposed children was found. We averaged a spectral power Žin percent. for d Ž1]4 Hz., u Ž4]7 Hz., a Ž7]12 Hz. and b Ž12]32 Hz. ranges of EEG for the left hemisphere ŽF1 ,F3 ,F7 ,C 3 ,T3 ,T5 ,P3 and O 1 leads. and the right ŽF2 ,F4 ,F8 ,C 4 ,T4 ,T6 ,P4 and O 2 leads. in both groups. In prenatally irradiated children we observed an increase Ž P- 0.05. of d-power in the left hemisphere Žparticularly in the left fronto-temporal region., a decrease Ž P- 0.05. of u-power in the left hemisphere, as well as a significant increase of b-power in the left hemisphere Ž P - 0.01. and in the right Ž P- 0.05. as compared to the control children. In children exposed at 8]25 weeks of prenatal development at the time of the Chernobyl we revealed a significant Ž P- 0.05. increase of both d- and bpower together with decrease Ž P- 0.05. of upower in the left hemisphere as compared to the control. Moreover, the lateralization of b-power to the left hemisphere was greater Ž P- 0.01. in the children irradiated at 16]25 weeks of gestation in comparison to controls. At the present time there are many publications concerning the mental health of the prenatally irradiated children as a result of the Chernobyl disaster ŽNyagu et al., 1993; Gayduk et al., 1994; Kozlova et al., 1995; Nyagu et al., 1995; Prilipko et al., 1995; Souchkevitch and Tsyb, 1995; Nyagu et al., 1996a,b,c; Yule, 1996.. All authors came to the conclusion that the prevalence rate of disorders of psychological development, emotional and behavior disorders, as well as mental retardation, is higher in children irradiated in utero as compared to the non-exposed children. We propose that one of the important biological mechanisms of mental disorders genesis in the prenatally irradiated children is the radiation induced malfunction of the thyroid]pituitary sys-
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tem at a 0.30 Sv of thyroid exposure dose. We suggest that the EEG-abnormalities revealed in the exposed children Žbilateral paroxysmal activity, epileptiform activity shifted to the left frontotemporal region, increase of d- and b-power shifted to the left hemisphere. could reflect the malfunction of limbic]reticular structures ŽFlorHenry, 1983; Zhirmunskaya, 1991.. Lateralization of paroxysmal, d- and b-activity to the left hemisphere in the prenatally irradiated children could reflect left hemisphere dysfunction. On the other hand, the left-hemispherical EEG-patterns were typically for the children exposed at the most critically periods of cerebrogenesis Ž8]25 weeks of gestation. and particularly at 16]25 weeks. Thus, our data suggest that the left hemisphere is more vulnerable than the right with respect to prenatal exposure. We hypothesize that the cerebral basis of mental disorders of the prenatally irradiated children is the malfunction of the left hemisphere limbic]reticular structures. This assertion should be confirmed or rejected with further investigations including also PET, MRI, etc. Nevertheless, it is clear that mental disorders in the prenatally irradiated children reflect the developing brain functional-structural abnormalities as a result of an interaction of prenatal and post-natal factors, where the ionizing radiation effects on the developing brain are not to be excluded. Finally, left hemisphere malfunction is being considered by some authors as a biological marker of schizophrenia and the right hemisphere dysfunction as a marker for affective disorders ŽFlor-Henry, 1976; Gruzelier and Hammond, 1976; Gur, 1978; Flor-Henry, 1983.. The data obtained concerning the possible malfunction of the left hemisphere limbic]reticular structures in the prenatally irradiated children closely correspond to the data published by this laboratory regarding the left hemisphere limbic]reticular structure dysfunction and associated schizophrenia spectrum disorders in persons exposed to ionizing radiation as a result of the Chernobyl disaster ŽLoganovsky, 1995; Loganovsky and Loganovskaya, 1997.. It would be important to organize the schizophrenia study in prenatally irradiated children as a result of the Chernobyl
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disaster as did the Japanese study ŽImamura et al., 1995. of schizophrenia prevalence rate in prenatally exposed A-bomb survivors. The results of the WHO Pilot Project ‘Brain Damage in Utero’, a component of the International Programme on the Health Effects of the Chernobyl Accident ŽIPHECA. have shown the reality of the problem. The study of endogenic mental diseases, especially schizophrenia, in the children irradiated in utero is of particular interest to the scientific community and for clinical practice. Acknowledgements The authors express their thanks for the kind assistance of Prof. J.L.Andreassi ŽUSA. in the preparation of this manuscript and his very important remarks and advice. References Davydov, B.I., Ushakov, I.B., 1987. Ionizing Radiation and Brain: Behavior and Structural-Functional Patterns, Science and Technical Outcomes, Radiation Biology, vol. 8, VINITI, Moscow, p. 336. Dunn, L.M., Dunn, L.M., 1982. British Picture Vocabulary Scale, NFER Nelson, London, p. 245. Flor-Henry, P., 1976. Lateralized temporal]limbic dysfunction and psychopathology. Ann. New York Acad. Sci. 280, 777]795. Flor-Henry, P., 1983. Cerebral Basis of Psychopathology, John Wright, PSG Inc., Boston, p. 357. Gayduk, F.M., Igumnov, S.A., Shalkevich, V.B., 1994. Complex estimation of neuro-psychic development of children undergone to radiation exposure in prenatal period as a result of Chernobyl disaster. Soc. Clin. Psychiatry 1, 44]49. Grigoriev, Yu.G., 1963. Radiation Damages and Compensation of Dysfunctions, Gosatomizdat, Moscow, p. 204. Gruzelier, J.H., Hammond, N., 1976. Schizophrenia: a dominant hemisphere temporal]limbic disorder? Res. Commun. Psychol. Psychiatry Behav. 1, 33]72. Gur, R.E., 1978. Left hemisphere dysfunction and left hemisphere overactivation in schizophrenia. J. Abnorm. Psychol. 2, 226]238. Hetzel, B.S., 1994. Iodine deficiency and fetal brain damage. N. Engl. J. Med. 26, 1770]1771. Igumnov, S.A., 1996. Psychological development of children exposed to radiation in prenatal period as a result of Chernobyl disaster. Acta Med. Nagasaki. 41, 20]25. Imamura, Y., Nakane, Y., Kondo, H., Kishikawa, M., Ohta, Y., 1995. Lifetime prevalence of schizophrenia of people pre-
natally exposed to A-bomb radiation in Nagasaki. In: Proceedings of the International Conference on the Mental Health Consequences of the Chernobyl Disaster: Current State and Future Prospects, May 24]28, 1995, Kiev, pp. 314]315. Kimeldorf, D.J., Hunt, E.L., 1969. Effect of Ionizing Radiation on the Function of Nervous System, Atomizdat, Moscow, pp. 376. Kozlova, I.A., Pukhovsky, A.A., Riaboukhine, V.Yu., 1995. Psychologic and psychiatric study of children, living in Kaluga and Bryansk regions of Russia ŽChernobyl accident aftermath .. Zurnal Nevropatologii i Psykhiatrii imeni S.S.Korsakova 1, 70]74. Kriegel, H., Schmahl, W., Gerber, G.B., Stieve, F.-E. ŽEds.., 1986. Radiation Risks to the Developing Nervous System. Gustav Fischer Verlag, Stuttgart, New York, p. 435. Kuzma, J.W., 1984. Basic Statistics for the Health Sciences. Mayfield Publish., Palo Alto, p. 274. Lebedinsky, A.V., Nakhilniztskaja, Z.N., 1960. Effects of Ionizing Radiation on the Nervous System. Atomizdat, Moscow, p. 188. Livanov, M.N., 1962. Some Problems of Ionizing Radiation Effects on the Nervous System. Medgiz, Moscow, p. 196. Loganovskaya, T., Loganovsky, K., 1997. Brain laterality and psychopathology in children irradiated in utero. In: Abstracts of the 4th Laterality and Psychopathology Conference, June 19]21, 1997, London, p. 34. Loganovsky, K.N., 1995. Ionizing radiation effect on human brain information processes. In: Proceedings of the International Conference on the Mental Health Consequences of the Chernobyl Disaster: Current State and Future Prospects, May 24]28, 1995, Kiev, pp. 52]53. Loganovsky, K., Loganovskaya, T., 1997. Brain laterality and psychopathology in the remote period of acute radiation sickness. In: Abstracts of the 4th Laterality and Psychopathology Conference, June 19]21, 1997, London, p. 34. Nyagu, A.I., Cheban, A.K., Salamatov, V.A., Limanskaja, G.F., Yaschenko, A.G., Zvonareva, G.N., Yakimenko, G.D., Melina, K.V., Plachinda, Yu. I., Chumak, A.A., Bazyka, D.A., Gulko, G.M., Chumak, V.V., Volodina, I.A., 1993. Psychosomatic health of children exposed to ionizing radiation in utero as a result of the Chernobyl disaster. In: Proceedings of the International Conference on the Social, Psychologic and Psychoneurologic Aspects of the Chernobyl Disaster Aftermath, September 28]30, 1992, Kiev, pp. 265]270. Nyagu, A.I., Cheban, A.K., Bugayev, V.N., Korol, N.A., Treskunova, T.V., 1995. Health of children irradiated in utero. In: Baryakhtar, V.G. ŽEd.., Chernobyl Disaster, Naukova Dumka, Kiev, pp. 429]434. Nyagu, A.I., Loganovsky, K.N., Cheban, A.K., et al., 1996a. Mental health of children exposed to radiation in utero: psychophysiologic study. Social Clin. Psychiatry 1, 23]36. Nyagu, A.I., Loganovsky, K.N., Cheban, A.K., Podkorytov, V.S., Plachinda, Yu.I., Yuriev, K.L., Loganovskaja, T.K., Antipchuk, Ye.Yu., 1996. Mental health of irradiated in
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