At Issue: Schizophrenia Spectrum Disorders in Persons Exposed To Ionizing Radiation As A Result of The Chernobyl Accident

At Issue: Schizophrenia Spectrum Disorders in Persons Exposed to Ionizing Radiation as a Result of the Chernobyl Accident
by Konstantin N. Loganovsky and Tatiana K. Loganovskaja
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The At Issue section of the Schizophrenia Bulletin contains viewpoints and arguments on controversial issues. Articles published in this section may not meet the strict editorial and scientific standards that are applied to major articles in the Bulletin. In addition, the viewpoints expressed in the following article do not necessarily represent those of the staff or the Editorial Advisory Board of the Bulletin.The Editors.
spectrum disorders. An integration of international efforts to discuss and organize collaborative studies in this field is of great importance for both clinical medicine and neuroscience. Keywords: Schizophrenia spectrum disorders, ionizing radiation, Chernobyl accident, laterality, psychophysiology, brain mapping of EEG, evoked potentials, limbic system. Schizophrenia Bulletin, 26(4):751-773, 2000. Evidence is increasing in support of the etiologic heterogeneity of schizophrenia (Coleman and Gillberg 1997; Garver 1997). Schizophrenia results from the interaction of multiple factors, including the person's genetic endowment and various environmental influences (Kirch 1993). The exact role of environmental hazards in the development of the illness, however, remains unclear (Shore 1986; Buszewicz and Phelan 1994; McGuffin et al. 1994; Syvalahti 1994; Fuller Torrey [1995] 1996). Evidence is dramatically increasing in support of the neuropathology of schizophrenia (Flor-Henry 1969a, 19696, 1976, 1983, 1987, 1989; Gur and Pearlson 1993; Gruzelier and Raine 1994; Arnold 1997; Egan and Weinberger 1997; Willner 1997; Bullmore et al. 1998; O'Donnell and Grace 1998; Sachdev 1998). Left frontotemporal abnormalities have been outlined as a cerebral basis of schizophrenia (Flor-Henry 1969a, 19696, 1976, 1983, 1987, 1989; Gruzelier and Hammond 1976; Deakin et al. 1989; Gruzelier 1997; Bullmore et al. 1998). Neurobiological studies suggest that abnormalities of both anatomy and function occur in the limbic-cortical structures of schizophrenia patients. An anatomical circuit that links functioning of the ventral striatum with the hippocampus and other limbic-cortical structures lies at the site of these neurobiological abnormalities (Csernansky and Bardgett 1998).
Send reprint requests to Dr. K.N. Loganovsky, 16D Heroes of Stalingrad St., Apt. 173, Kyiv, 04210, Ukraine; e-mail: kosti@morion.kiev.ua.
Abstract
We studied schizophrenia spectrum disorders in Chernobyl accident survivors by analyzing Chernobyl exclusion zone (EZ) archives (1986-1997) and by conducting a psychophysiological examination of 100 patients with acute radiation sickness (ARS) and 100 workers of the Chernobyl EZ who had worked as "liquidators-volunteers" for S or more years since 1986-1987. Beginning in 1990, there has been a significant increase in the incidence of schizophrenia in EZ personnel in comparison to the general population (5.4 per 10,000 in the EZ versus 1.1 per 10,000 in the Ukraine in 1990). Those irradiated by moderate to high doses (more than 0.30 Sv or 30 rem), including ARS patients, had significantly more left frontotemporal limbic and schizophreniform syndromes. 1 We hypothesized that ionizing radiation may be an environmental trigger that can actualize a predisposition to schizophrenia or indeed cause schizophrenia-like disorders. The development of schizophrenia spectrum disorders in overirradiated Chernobyl survivors may be due to radiation-induced left frontotemporal limbic dysfunction, which may be the neurophysiological basis of schizophrenia-like symptoms. Persons exposed to 0.30 Sv or more are at higher risk of schizophrenia
'l Gy (gray) = one unit of absorbed dose of ionizing radiation = 100 rad (radiation absorbed dose). 1 Sv (sievert) = one unit of effective dose of ionizing radiation = 100 rem (roentgen equivalent man). Regarding the Chernobyl accident, 1 Sv = 1 Gy.
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Schizophrenia Bulletin, Vol. 26, No. 4, 2000
K.N. Loganovsky and T.K. Loganovskaja
Exposure to ionizing radiation causes brain damage with limbic system dysfunction (Grigoriev 1958; Lebedinsky and Nakhilnitzkaja 1960; Gangloff 1962; Haley 1962; Lebedinsky 1962; Livanov 1962; Kimeldorf and Hunt [1965] 1969; Hunt 1987). Moreover, the hippocampus is a very radiosensitive structure (Kimeldorf and Hunt [1965] 1969; Davydov and Ushakov 1987). Xray irradiation of the hippocampus by low doses of 6-8 mGy (0.6-0.8 rad) produces the endogenous (pacemaker) generation of nervous impulses (Peimer et al. 1985; Dudkin 1988). Thus, the hypothesis arises that exposure to ionizing radiation can trigger schizophrenia in predisposed individuals or cause schizophrenia-like disorders as a consequence of radiation-induced limbic dysfunction. Studies on the relationship between schizophrenia and radiation exposure are practically absent in the available literature. One study describes an atypical clinical pattern of schizophrenia secondary to chronic irradiation with prominent asthenia, autonomic instability, and hypochondriac and psychosensory symptoms but does not link schizophrenia onset to the ionizing radiation exposure (Golodetz 1962). Nakane and Ohta (1986) reported a significant increase in the prevalence of schizophrenia in the A-bomb survivors in Nagasaki. The Life Span Study (LSS), started by the Radiation Effect Research Foundation in Japan, did not include data on severe mental disorders. The Japanese authors combined the schizophrenia register of the Department of Neuropsychiatry, University School of Medicine, Nagasaki, with the LSS register to fill in this information. They revealed that, in 1978, there were 1,589 patients with schizophrenia in the LSS register (n 26,678). The schizophrenia register had been in operation only since 1960, and it was not possible to calculate annual inception rates back to the bombing in 1945. Moreover, migration out of Nagasaki cannot be estimated. In spite of these methodological limitations, the prevalence of schizophrenia in the A-bomb survivors was still very high (6 percent), while the prevalence of schizophrenia is no more than 1 percent in the general population (Shore 1986; Fuller Torrey [1995] 1996). The first information about an increase in schizophrenia incidence among the Chernobyl EZ personnel was presented by Loganovsky and Nyagu (1997) at the International Conference on Low Doses of Ionizing Radiation: Biological Effects and Regulatory Control. The purpose of this study is to investigate the schizophrenia spectrum disorders (schizophrenia, schizotypal, schizoaffective, organic schizophrenia-like, and schizoid personality disorders) among the irradiated Chernobyl accident survivors. The study includes two parts: (1) an epidemiological study of severe mental disorders in the Chernobyl EZ personnel and (2) a psychophysiological
assessment of the irradiated personspatients who had ARS as well as the workers who cleaned up the Chernobyl accident consequences (so-called "liquidators").
Design
Background. At 1:23 AM, April 26, 1986, the fourth unit of the Chernobyl Nuclear Power Plant (ChNPP) was destroyed and about 300 MCi (11 X 1018 Bq) of radioactive materials exploded into the environment. At the present time in the Ukraine, there are about 3 million Chernobyl accident survivors. About 100,000 people have been evacuated from the 30-km zone surrounding the ChNPP (the Chernobyl EZ). More than 600,000 people from the former USSR took part in cleaning up the Chernobyl accident consequences from 1986 to 1989; these workers are called "liquidators." The most critical group from the radiological point of view is the 126,000 liquidators who worked from April 26, 1986, to the beginning of 1987. Their average dose of irradiation was 120-180 mSv (12-18 rem), but 6-15 percent (7,560-18,900 workers) were irradiated by more than 250 mSv (25 rem). The effective doses of irradiation for other Chernobyl accident survivor contingents were significantly lower. The average dose per year of irradiation of "non-Chernobyl" origin for the Ukrainian population is 5.3 mSv/year (0.53 rem/year; Likhtarev et al. 1994; Los' and Likhtarev 1994; Likhtarev 1996; Ministry of Ukraine 1996). ARS has been diagnosed in 237 persons, 29 of whom died as a result of the exposure 7-96 days after the accident (Kindselsky et al. 1995; Romanenko et al. 1995). Only 134 patients had verified ARS (absorbed doses 0.7-13 Gy or 70-1300 rad) (Wagemaker and Bebeshko 1996). The remaining 103 patients in whom ARS was diagnosed are considered to have a subclinical form of ARS. At the present time, 180 persons who had been diagnosed with ARS in 1986 are living in the Ukraine and are in a followup study at the Scientific Center for Radiation Medicine, Kiev (Bebeshko et al. 1996). The ARS patients and the liquidators of 1986-1987 clearly have the highest radiation risk. However, until now, epidemiological data concerning severe mental disorders among the liquidators have been practically absent, possibly due to (1) lack of radioepidemiologic interest in this problem in comparison with traditional topics such as radiation-induced malignancies and hereditary disorders; (2) a deficiency of psychiatric information in the radiological registers, and vice versa; and (3) high rates of migration among the liquidators. The particular group of Chernobyl accident survivors focused on in this study is the Chernobyl EZ personnel, primarily composed of liquidators, who are volunteers
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and work according to a watch regime (i.e., 2 weeks within the EZ and 2 weeks at home). They were medically monitored and available for epidemiological assessment. Consequently, the 12-year followup study of the Chernobyl EZ personnel is a unique opportunity to investigate the epidemiology of severe mental disorders in this population. Epidemiological Study. The data for the epidemiological part of the study was obtained from the psychiatric archives (1986-1997) of the Medical and Sanitary Department in Chernobyl. Since 1986, this department has undertaken the somatic and mental health monitoring of EZ personnel. The number surveyed each year is presented in table 1. The number of EZ personnel decreased since 1988-1990, when the emergency cleanup was complete. It was intended that all ill workers or those who were at a high risk for any disease (especially mental disorders) would not be employed in the EZ or would be eliminated from the EZ personnel if disease developed after they had begun work. Further, it should be noted that the EZ personnel are volunteers. Therefore, it is doubtful that workers would present fictitious symptoms (e.g., malingering) in order to be transferred out of the area and, consequently, lose their jobs, which have a higher salary than jobs outside the EZ. Among the EZ personnel, 78.9 percent were men, with 32.9 percent ranging in age from 40 to 49 years, 30.2 percent from 30 to 39 years, and 24.7 percent from 50 to 59 years. The majority were engineers and technicians. The percentage working in the EZ for 5 or more years was 60.6 percent. The distribution of EZ personnel according to the effective doses of irradiation was as follows: < 0.05 Sv (5 rem), 81.8 percent; 0.05-0.24 Sv (5-24 rem), 13.6 percent; 0.25-0.99 Sv (25-99 rem), 3.7 percent; > 1 Sv
(100 rem), 0.82 percent (Vokhmekov et al..l994). All records in the psychiatric archives of the Medical and Sanitary Department of Chernobyl were studied. Control data for the epidemiological part of the study came from the official statistical data of the Ministry of Public Health of Ukraine (1970-1997). In the Ukraine, the incidence of psychiatric illness, particularly of severe mental disorders, is calculated on the basis of hospital admissions. The diagnosis of psychotic disorder is verified during hospitalization and is included in the calculation of base rate statistics. Until April 1999 in the Ukraine, ICD-9 diagnostic criteria were used. This same methodology is used in the Chernobyl EZ to diagnose disorders in current personnel, and a nonstandardized interview and medical documentation are used to review prospective EZ personnel. If a mental disorder is revealed during the interview or the candidate has been registered with national mental health care, the candidate is not accepted for employment in the EZ. A screening for severe mental disorders is carried out if abnormal behavior or acute symptoms are present. Individuals are transferred by colleagues, ambulance, or the police to the psychiatrist of the Medical and Sanitary Department of Chernobyl, who decides whether to transfer the patient to the mental hospital. If a severe mental disorder is verified in the hospital, data about the disorder are included in the register. This common diagnostic procedure leads to a general underestimation of mental disorders but makes possible a comparison of data in the EZ with data from the general population. It should be noted that the epidemiological data on the basis of the psychiatric archives of Chernobyl are accurate only for severe mental disorders. Borderline mental disorders irf'EZ personnel are classified as a comorbidity of physical diseases and, consequently, are excluded from the psychiatric archives and registration.
Table 1. Schizophrenia onset during 1986-1997 in Chernobyl exclusion zone personnel

Cases of schizophrenia onset 2 2 1 2 6 6 4 5 4 4 3 3 Population of the Chernobyl exclusion zone personnel 25,000 25,000 25,000 12,500 11,000 11,250 12,500 12,963 11,000 11,000 6,555 5,329 Incidence of schizophrenia per 10,000 of population 0.8 0.8 0.4 1.6 5.4 5.3 3.2 3.9 3.6 3.6 4.6 5.6
Year 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997
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We should note the following limitations of the epidemiological part of our study: (1) the absence of standardized diagnostic methods and the impossibility of being "blind" to radiation exposure status; (2) specific demographic characteristics and the relatively small number of EZ personnel; (3) migration; and (4) the impossibility of calculating the prevalence of schizophrenia in the personnel because (a) candidates had been medically examined before employment in the EZ and all psychiatric patients rejected, and (b) individuals who were diagnosed with schizophrenia were terminated from employment. As a result, a natural "accumulation" of schizophrenia is absent among personnel, which results in an artificial reduction of schizophrenia prevalence. Consequently it was only possible to assess schizophrenia incidence in EZ personnel. The data obtained have been analyzed with the chisquare test and vital statistics methods (measures of morbidity) (Kuzma 1984). Because of the large number of variables tested for significance, the Bonferroni correction (Kirk 1982) was used to reduce the probability of type I (i.e., false-positive) errors. Psychophysiological Assessment of Irradiated Persons. The psychophysiological part of the study was conducted in the Neurology Department, Institute of Clinical Radiology, Scientific Center for Radiation Medicine, Academy of Medical Sciences of the Ukraine, in 1996-1998. Composition of the groups was as discussed below. Group A comprises 100 acutely irradiated patients who had ARS (absorbed doses up to 6.6 Gy or 660 rad) as a result of the Chernobyl disaster. All were right-handed men and 3564 years old at the time of examination. Subclinical ARS has been diagnosed in 30 of these patients (average absorbed dose of relatively even 7 and p irradiation was 0.2 0.05 Gy [20 5 rad]); first degree ARS was diagnosed in 38 (1.07 0.12 Gy or 107 12 rad); and second or third degree ARS in 32 (2.69 0.2 Gy or 269 20 rad). All were treated in the Department of Radiation Pathology in the Institute of Clinical Radiology, Scientific Center for Radiation Medicine of the Academy of Medical Sciences of Ukraine. The psychophysiological investigations were carried out in the Neurology Department, 10-12 years after ARS. Group B is composed of 100 chronically irradiated staff members of the Chernobyl EZ who have been working as liquidators-volunteers in the EZ since 1986-1987 for 5 or more years. All were right-handed men and 25-48 years old at the time of examination. Fifty-four from this group (group Bl) were chronically irradiated at doses below 0.30 Sv or 30 rem (average dose 0.16 0.05 Sv or 16 5 rem), and 46 (group B2) were chronically irradi-
ated above 0.30 Sv or 30 rem (average dose 0.69 0.15 Sv or 69 15 rem). Group C is the control group: normal age- and gendermatched adults (n = 20), veterans of the Afghanistan war with post-traumatic stress disorder (PTSD; n = 50), and veterans with both PTSD and closed head injury (n = 50). Neurological examination and typical clinical psychiatric interview (nonstandardized) were used, together with the Brief Psychiatric Rating Scale (BPRS; Overall and Gorham 1962), the Scale for the Assessment of Negative Symptoms (SANS; Andreasen 1982), the General Health Questionnaire (GHQ-28; Goldberg 1981, Goldberg and Bridges 1987, Goldberg and Williams 1988), and the adapted version of the Minnesota Multiphasic Personality Inventory (MMPI; Sobchik 1990). Computerized electroencephalogram (EEG) and sensory evoked potentials were carried out with a 19-channel brain biopotentials analyzer ("Brain Surveyor," SAICO, Italy). The brain spontaneous electric activity was monopolarly registered with linked ears reference. Nineteen scalp electrodes were placed according to the 10-20 International System. Visual and spectral analyses of EEG were carried out. Epochs used in the analysis were 60 seconds. The obtained frequency band was 1-32 Hz. All of the EEG records were visually edited for artifacts; artifacts due to eye or muscle movements or respiration were deleted prior to analysis. Estimation and interpretation of the brain spontaneous electrical activity were conducted according to Zhirmunskaja's algorithm (1991) for clinical EEG, while spectral analysis was carried out using classical Fast Fourier Transformation methods (Niedermeyer and Lopes da Silva 1982; Zenkov and Ronkin 1991). Checkerboard, reversible-pattern visual evoked potentials (VEP) were registered binocularly on 50 chesspattern reversals with a frequency of 1 Hz. The 50 epochs selected for analysis were 400 ms in duration with amplitudes measured from peak to trough (mkV) and latency measured from onset of stimulation to its peak (ms). Somatosensory evoked potentials (SSEP) were registered with 40 pain threshold electrocutaneous stimulations of the right median nerve on the lower forearm. The left median nerve was not stimulated. The nerve was stimulated by bipolar skin electrode with right-angled electrical impulses of 0.1-ms duration and 0.5-Hz frequency (1 per 2,000 ms). The cathode was situated proximally. The epochs selected for analysis were 50 ms for the shortlatency SSEP and 1,000 ms for long-latency. Amplitudes were measured from peak to trough (mkV), latency from onset of stimulation to its peak (ms). Statistical processing included descriptive statistics, Student's t test, chi-square tests, and correlational analysis (Kuzma 1984). The paired t test was used to analyze data
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when a pair of measurements was obtained on each individual (Montgomery 1976). The Bonferroni correction was used when multiple statistical tests were performed (Kirk 1982).
Table 2. Severe mental disorders in the Chernobyl exclusion zone personnel (according to psychiatric archives data 1986-1997)
Mental disorder (ICD-9 code) Number of cases, 1986-1997 22 12 1 9 10 31 15
Results
Epidemiological Study of Severe Mental Disorders in Chernobyl EZ Personnel. Data on Chernobyl EZ personnel from the psychiatric archives on severe mental disorders are presented in table 2. The schizophrenia spectrum disorders register (1986-1997) includes 72 workers of the EZ suffering from schizophrenia, schizoaffective disorder, organic (nonalcoholic) schizophrenia-like psychoses, and schizoid personality disorder. There were 53 schizophrenia subjects according to the ICD-9 criteria of schizophrenia (code 295, excluding "slow progressive schizophrenia") who also met the criteria of ICD-10 code F20 (schizophrenia). A statistically significant increase in schizophrenia (among all psychoses) was found in EZ personnel relative to the general Ukrainian population (73% vs. 43%; x 2 = 18.5; df= \\p< 0.001). The relative risk was 1.7, indicating that working and living in the EZ are associated with a nearly twofold (85%) increase in the risk of schizophrenia within all psychoses.
Alcoholic psychoses (291) Alcoholic delirium (291.0) Alcoholic hallucinosis (291.3) Alcoholic paranoid (291.5) Organic nonalcoholic psychoses (294.8) Epileptiform syndrome (345) Alcoholic epileptiform syndrome (303,345) Schizophrenia (295)
Affective psychoses (296) Reactive psychoses (298) Mental retardation (317)
53 5 5 4
Among those 53 cases of schizophrenia, 42 (79.2%) onsets of schizophrenia occurred in the Chernobyl EZ, after the Chernobyl accident (April 26, 1986). Schizophrenia onset during 1986-1997 in the personnel is shown in table 1. The incidence of schizophrenia in EZ workers, in comparison with the Ukrainian population, is presented in figure 1.
Figure 1. Incidence of schizophrenia in Chernobyl exclusion zone personnel in comparison with the general Ukrainian population
Ukraine
|
a.
O Exclusion zone
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Since 1990, there has been a significant increase in schizophrenia in the EZ personnel in comparison with the general population (5.4 per 10,000 in the EZ vs. 1.1 per 10,000 in the Ukraine in 1990). The relative risks are 2.4 for 1986-1997 and 3.4 for 1990-1997, which indicate that working and living in the EZ are associated with more than a twofold and even a threefold increase in the risk of schizophrenia developing. Among the 42 patients who fell ill after the accident, 34 (80.9%) paranoid and 8 (19.1%) simple forms of schizophrenia were diagnosed. Of the 42 patients, there were 33 (78.6%) males and 40 (95.2%) in the 15-54 years age group; 16 (38%) of these patients had been evacuated between April 28 and May 5, 1986, and later came back to work at the Chernobyl EZ before they fell ill with schizophrenia; 31 (73.8%) of them had been taking part in the cleanup of the Chernobyl accident and its aftermath since 1986-1987 before they became ill with schizophrenia. Psychophysiological Assessment of Irradiated Persons. Neuropsychiatric symptoms in the irradiated persons are presented in table 3. Characteristic symptoms were seen
at significantly higher rates in the irradiated subjects than in the veterans with PTSD control group, including odd skin sensations, vertigo, mild neurological signs, autonomic nervous system dysfunction, paroxysmal attacks (sometimes epileptiform), cognitive dysfunction, and, particularly, negative psychopathological symptoms. Some symptoms, such as emotional lability, anxiety, "flashbacks," and nightmares, were observed at a significantly higher rate in the controls. The typical PTSD symptoms (flashbacks, nightmares, etc.) presented only in ARS patients who had been involved in the accident (technicians, construction workers, etc.). The number of neuropsychiatric symptoms was correlated with the dose of irradiation (table 4). The rate of paroxysmal attacks and negative symptoms was significantly higher in overirradiated persons (irradiated by more than 0.30 Sv or 30 rem, including the ARS patients). Pathopsychological investigations also demonstrated significant differences in irradiated persons compared with controls. The averaged MMPI profile of the irradiated persons showed peaks on the hypochondria, schizophrenia, and paranoia scales (figure 2). Some psychopathological
Table 3. Neuropsychiatric symptoms in irradiated persons and controls

Liquidatorsvolunteers (n=100), % 92 95 58 46 73 52 95 54 14 2* 78* 46 48 88 15 68 62 Veterans with PTSD (n = 50), % 78 32* 42 38 36* 6* 72* 24* 68* 52* 84* 90* 44 48 6 24* 18* Veterans with PTSD and closed head injury (n = 50), % 84 54* 52 36 48* 30 86 38 72* 48* 90* 84* 42 58 10 44* 32*
Symptom Chronic pain Odd skin sensations Paresthesias Fatigue Vertigo Mild neurological signs Autonomic nervous system dysfunction Paroxysmal attacks Nightmares "Flashbacks" Emotional lability Anxiety Depression Hypochondriac ideation Paranoiac ideas Cognitive dysfunction Negative psychopathological symptoms
ARS patients (n = 100), % 86 98 60 54 78 44 98 68 20 18 52 29 42 74 21 85 81
Note.ARS = acute radiation sickness; PTSD = post-traumatic stress disorder. * p < 0.001 relative to ARS patients, according to the chi-square test
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Table 4. Neuropsychiatric symptoms in persons irradiated by small doses (< 0.3 Sv or 30 rem) and by moderate or large doses (> 0.3 Sv or 30 rem, including ARS patients) Small (<0.3Sv) doses, rate (%) (n = 54) 51 (94) 52 (96) 28 (52) 24 (44) 39 (72) 18(33) 51 (94) 22(41) 40 (74) 28 (52) 26 (48) 45 (83) 7(13) 34 (63) 26 (48) Moderate and large (> 0.3 Sv) doses, rate (%) (n = 146) 127(87) 141 (97) 90 (62) 76 (52) 112(77) 78 (53) 142(97)
Symptom Chronic pain Odd skin sensations Paresthesias Fatigue Vertigo Mild neurological signs Autonomic nervous system dysfunction Paroxysmal attacks Emotional lability Anxiety Depression Hypochondriac ideation Paranoiac ideas Cognitive dysfunction Negative symptoms
x2
2.24 0.01 1.56 0.25 0.43 6.82 0.93 12.76 5.48 6.50 0.06 0.26 1.27 7.54 19.80
df 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
P ns ns ns ns ns ns ns < 0.001 ns ns ns ns ns . ns < 0.001
100(68) 90 (62) 47 (32) 68 (47) 117(80) 29 (20) 119(81) 117(80)
sickness; ns = not significant. Note.ARS = acute radiation Figure 2. MMPI profiles in irradiated persons and controls
T scores
--Irradiated patients, n=200 Afghanistan war veterans with PTSD (n=100) - 6 - N o r m a l controls (n=20)
IHJ
2D
3Hy
4Pd
5Mf
6Pa
7Pt
8Sch
9Ma
OS!
Note.MMPI (Minnesota Multiphasic Personality Inventory) Scales: L = lie, F = trustworthiness, K = correction, 1 Hs = hypochondria, 2D = depression, 3Hy = hysteria, 4Pd = psychopathy, 5Mf = manliness-femininity, 6Pa = paranoia, 7Pt = psychasthenia, 8Sch = schizophrenia, 9Ma = mania, OSi = social introversion. PTSD = post-traumatic stress disorder.
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indexes were proportional to the dose of irradiation (table 5). The social introversion scale of MMPI, emotional withdrawal and blunted or inappropriate affect evaluated according to the BPRS, as well as the summarized BPRS score were significantly higher in the overirradiated persons (including the ARS patients). Correlation analysis showed no relationship between the dose of irradiation and neurotic symptoms (anxiety, depression, somatic concern, tension, aggressivity, health self-estimation, PTSD). On the other hand, negative symptoms (blunted or inappropriate affect, emotional and social withdrawal, alogia, avolition-apathy, anhedonia), suspiciousness, unusual thought content, as well as the summarized score of the BPRS were associated with the dose of irradiation (r = 0.3-0.5, p < 0.001). Neurophysiological patterns of irradiated persons were dramatically distinguished (table 6). All ARS patients and 72 percent of the liquidators demonstrated EEG abnormalities. The flat, low-voltage EEG was the
most characteristic. The abnormal EEG activity (spikes, acute waves, spike-waves, slow waves) was significantly lateralized, especially to the left frontotemporal area, in the overirradiated patients. Computerized EEG spectral analysis (table 7) revealed a significant increase of 8 and 3 power together with decrease of 9 and a power in irradiated persons. Moreover, 8 and 3 power were significantly lateralized toward the left frontotemporal region in all examined irradiated persons. In the ARS patients, 8 power was significantly lateralized toward the left temporal area, and a power was depressed in the left parieto-occipital region. SSEP were characterized by topographic abnormalities in the left temporoparietal area in irradiated persons (table 7). Their SSEP were characterized by increased contralateral latencies and decreased contralateral amplitudes of N^, at the C3 on right median nerve stimulation. Moreover, an increased latency and a decreased amplitude of the late (P300) component were found in irradiated patients.
Table 5. Pathopsychological indexes in persons irradiated by small doses (< 0.3 Sv or 30 rem) and by moderate or large doses (> 0.3 Sv or 30 rem, including ARS patients)
Small (< 0.3 Sv) doses, mean SD (n = 54) Moderate and large (> 0.3 Sv) doses, mean SD(n = 146)
Scale
df
MMPI 1.21 ns 198 69.5 9.5 Trustworthiness 67.4 11.3 89.7 18.2 ns 198 1.02 92.4 10.5 Hypochondria Depression ns 198 2.98 85.0 12.6 78.9 + 13.3 ns 198 -2.36 76.3 12.6 Paranoia 82.4 17.3 84.1 17.4 91.2 + 21.1 ns 198 -2.20 Schizophrenia < 0.001 198 -4.74 72.3 8.4 Social introversion 80.1 10.9 BPRS 4.1 1.7 ns 198 Somatic concern 4.2 1.6 -0.38 2.11 3.0 1.7 ns 198 2.4 1.8 Anxiety 2.2 1.7 3.5 2.1 < 0.001 198 -3.97 Emotional withdrawal 2.5 2.2 ns 198 3.20 3.6 2.0 Depressive mood -2.71 3.0 2.1 ns 198 2.1 2.0 Suspiciousness ns 198 2.2 1.8 Unusual thought content 2.9 1.9 -2.33 < 0.001 198 2.1 1.9 Blunted or 3.6 1.9 -4.93 inappropriate affect 29.6 8.2 < 0.001 198 38.2 9.5 -5.86 Summarized BPRS score (scales 1-16) SANS ns 198 2.6 1.8 Affective flattening 3.2 1.5 -2.36 or blunting ns -2.34 2.9 1.6 198 2.3 1.6 Alogia 2.7 1.4 ns Avolition-apathy 198 -2.36 2.1 1.5 ns 0.37 Anhedonia-asociality 3.1 1.7 198 3.2 1.6 ns -1.67 2.4 1.8 Attention 198 2.9 1.9 GHQ-28 ns 198 36.8 13.4 1.40 39.7 11.6 General score Note.ARS = acute radiation sickness; BPRS = Brief Psychiatric Rating Scale; GHQ = General Health Questionnaire; MMPI Minnesota Multiphasic Personality Inventory; ns = not significant; SANS = Scale for the Assessment of Negative Symptoms; SD standard deviation.
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Schizophrenia Bulletin, Vol. 26, No. 4,2000
Table 6. EEG patterns in irradiated persons and controls

Rate (%) Liquidatorsvolunteers (n=100) 28 (28)* Veterans with PTSD (n = 50) 37 (74)* Veterans with PTSD and closed head injury (n = 50) 30 (60)*
EEG pattern Normal Organized with predominance of a activity Abnormal Hypersynchronic Flat polymorphic Disorganized with predominance of a activity Disorganized with predominance of 8 activity Laterality of abnormal activity Bilateral Left hemisphere Right hemisphere
ARS patients (n=100) 0
Normals (n = 20) 16(80)*
10(10) 58 (58) 16(16)
8(8) 45 (45) 10(10)
9(18) 3(6)* 1(2)
8(16) 6(12)* 4(8)
4(20) 0* 0
16(16)
9(9)
2(4)
20 (20) 57 (57) 23 (23)
7(7) 31 (31)* 34 (34)
9(18) 1(2)* 3(6)
10 (20) 4(8)* 6(12)
3(15) 1(5)* 0
Note.ARS = acute radiation sickness; EEG = electroencephalogram; PTSD = post-traumatic stress disorder. * p < 0.001 relative to ARS patients, according to the chi-square test
Table 7. Neurophysiological indexes in irradiated persons and controls

Mean SD Liquidatorsvolunteers (n = 100) Veterans with PTSD and closed head injury (n = 50)
Index
ARS patients (n=100)
Veterans with PTSD (n = 50)
Normals (n = 20)
Delta (1-4 Hz) power (%) of EEG in: 49.4 10.3 46.0 9.5 2.38 3.67 f=6.48, p < 0.001 48.5 7.8 46.1 8.9 1.98+3.4 f = 5.82, p < 0.001 48.3 9.3 44.1 10.1 3.21 4.67 f=6.87, p < 0.001 59.6 + 11.3* 56.0 12.1* 2.31 3.98 f=5.8, p < 0.001 52.1 11.3 50.1 9.8 1.77 + 3.86 / = 4.59, p < 0.001 56.3 9.6* 52.9 10.5* 2.96 4.95 f=5.98, p < 0.001 30.4 9.3* 31.0 9.5* -0.21 2.87 t = -0.52, ns 28.5 8.8* 29.1 8.7* -0.31 3.05 t = -0.72, ns 28.3 9.5* 31.1 10.1* -0.28 4.03 35.7 10.2* 37.1 12.2* -0.31 3.87 t = -0.57, ns 34.1 10.8* 35.9 8.9* -0.19 2.45 t = 0.55, ns 32.1 10.5* 33.4 10.9* -0.18 3.75 f=-0.34, ns 28.6 7.5* 28.0 8.9* 0.12 2.27 f=0.24, ns 23.4+9.7* 23.1 8.1* 0.1 1.78 t = 0.25, ns 23.9 9.9* 25.1 10.3* -0.11 2.01 t =-0.24, ns
Laterality (F3-F4) Paired ftest
c3 c4
Laterality (C3-C4) Paired Mest
T3 T4 Laterality (T3-T4) Paired Hest
t = -0A9,ns
Theta (4-7 Hz) power (%) of EEG in:
c3 c4
Laterality (C3-C4)
9.5 3.8 8.1 2.9 1.1 2.2
12.1 4.3* 12.0 3.8* 0.3 2.1
16.1 4.3* 16.0 3.5* 0.1 1.98
18.7 5.2* 18.9 5.4* -0.1 2.12
15.5 5.7* 16.1 4.1* -0.12 2.69
759
Table 7. Neurophysiological indexes in irradiated persons and controlsContinued

Mean SD Liquidatorsvolunteers (n = 100) f= 1.43, ns 11.3 3.6* 10.9 3.5* 0.76 2.05 f=3.71,p< 0.001 Veterans with PTSD and closed head injury (n = 50) f = -0.33, ns 19.1 6.8* 19.9 5.9* -0.58 + 2.45 f = -1.67, ns
Index Paired ftest T3 T4 Laterality (T 3 -T 4 ) Paired ftest
ARS patients (n=100) f=5.0, p < 0.001 9.4 2.3 8.0 4.1 1.26 1.97 f=6.4, p < 0.001
Veterans with PTSD (n = 50) f=0.36, ns 16.5 3.8* 16.9 3.5* -0.27 2.13 f =-0.9, ns
Normals (n = 20) f = -0.20, ns 17.9 4.9* 15.1 6.3* 1.95 3.7 f = 2.36, ns
Alpha (7-12 Hz) power (%) of EEG in:
1 O
2
Laterality (O-,-O2) Paired ftest
41.2 10.8 45.4 12.9 -3.46 5.42 f=-6.38, p < 0.001
45.1 8.3* 47.0 7.8 -1.78 5.12 f=-3.48, p< 0.001
56.1 14.3* 55.0 13.5* 1.1 6.9 f= 1.13, ns
48.7 15.2* 48.9 15.4* -0.1 6.8 f=-0.1,/7S
54.5 12.7* 60.4 14.1* -4.3 6.75 f = -2.85, ns
Beta (12-32 Hz) power (%) of EEG in:
c3
Laterality (C 3 -C 4 ) Paired ftest T3 T4 Laterality (T 3 -T 4 ) Paired ftest SSEP, latencies, ms N2o C3
25.5 4.8 25.1 3.9 0.35 1.85 f= 1.89, ns 24.4 4.3 23.0 4.1 1.3 1.92 f=6.77, p < 0.001
19.1 4.8* 17.9 3.9* 0.95 1.92 f = 4.95, p < 0.001 18.95.1* 17.4 5.2* 1.22.15 f=5.58, p < 0.001
12.6 5.3* 12.8 4.8* -0.1 2.11 f = -0.34, ns 12.3 3.4* 12.9 + 3.5* -0.4 1.91 f =-1.48, ns
14.1 4.3* 14.0 4.8* 0.05 2.4 f = 0.15, ns 14.3 4.6* 14.9 4.5* -0.42 + 2.07 f =-1.43, ns
12.5 3.7* 13.1 4.2* -0.6 2.75 f = -0.98, ns 11.9 4.9* 12.1 4.3* -0.15 2.25 f = -0.3, ns
Laterality (C 3 -C 4 ) Paired f test

p 3 oo
c4
21.2 3.2 19.4 3.1 1.54 2.25 f=6.84, p < 0.001 272.3 27.9 271.2 31.0 1.13 12.8 f = 0.88, ns
20.5 3.8 19.6 3.9 0.75 2.05 f=3.66, p < 0.001 276.3 37.7 275.2 33.1 0.89 15.7 f=0.57, ns
19.2 3.0* 19.5 3.4 -0.17 1.95 f=-0.62, ns
19.7 4.5* 19.8 4.1 -0.05 2.2 f = -0.16, ns
18.8 1.3 19.2 1.4 -0.3 0.95 f = -1.41, ns
C3 Laterality (C 3 -C 4 ) Paired f test
c4
239.3 19.0* 242.2 23.1* -2.15 11.4 f =-1.33, ns
245.3 33.7* 252.2 31.1* -5.2 17.45 f = -2.11,ns
242.1 16.3* 245.2 16.4* -2.95 9.76 f = 1.35, ns
vkV SSEP, amplitudes, 1 N 20 C3 Laterality (C 3 -C 4 ) Paired ftest

P
c4
1.0 0.7 1.9 1.2 -0.75 1.05 f = -7.14,p< 0.001 15.3 4.5 17.2 4.3 -1.36 2.74
1.3 0.8 1.9+0.9 -0.54 0.92 f=-5.87, p < 0.001 17.6 3.7* 17.5 3.3 0.05 2.55
3.2 0.3* 2.9 0.3* 0.27 0.52 f=3.67,p< 0.001 19.3 3.9* 19.2 3.1 0.07 2.86
2.9 0.4* 2.7 0.4* 0.19 0.45 f = 2.99, ns 22.3 9.7* 22.2 11.1* 0.06 4.75
3.3 0.4* 3.0 + 0.4* 0.28 0.42 f = 2.98, ns 22.3 6.3* 20.9 6.4 1.52 3.72
300
Laterality (C 3 -C 4 )
c4
760
At Issue
Paired ftest VEP, latencies, ms

^100 Ni45 ^200
f=-4.96, p < 0.001
f= 0.20, ns
t= 0.17, ns
f = 0.00, ns
f= 1.83, ns
O2 O2 02
82.0 14.1 128.1 14.5 237.3 14.7
89.2 11.1* 138.2 13.5* 221.4 12.7*
88.8 + 15.0 140.0 13.6* 187.0 13.6*
102.6 16.0 158.0 14.4* 221.0 14.6*
96.8 + 12.0* 147.0 11.6* 208.0 12.6*
VEP, amplitudes, mkV

^100 Ni45 P 200
O2 O2 02
4.2 3.6 7.6 4.8 5.9 3.8
3.2 2.7 5.6 3.9 4.9 3.6
3.6 2.2 4.2 1.8* 5.5 3.4
3.6 1.3 5.2 2.6 4.6 3.3
2.6 1.2 4.2 1.6 5.6 3.3
Note.ARS = acute radiation sickness; EEG = electroencephalogram; ns = not significant; PTSD = post-traumatic stress disorder; SD = standard deviation; SSEP = somatosensory evoked potentials; VEP = visual evoked potentials. * p < 0.001 relative to ARS patients, according to the Student's f test
VEP were characterized by a decreased latency of P100 and N145 components and an increased latency of P200 in irradiated persons as compared to controls, as well as an increased amplitude of N145 component in ARS patients (table 7). According to the correlation data analysis, we found that the negative (affective flattening, alogia, apathy, and social withdrawal) and paranoid symptoms as well as dysmnesia were closely associated with 8 and p power increase (r = 0.49-0.72, p < 0.001) in the left hemisphere in overirradiated persons (including ARS patients). Hypochondria was connected with left 8 power increase (r = 0.66, p < 0.001) as well as left a power decrease (r = -0.35, p < 0.001) and right 6 power decrease (r = -0.34, p < 0.001). The affective symptoms (depression and anxiety) were closely correlated with both right 8 and p power increase (r = 0.35-0.62, p < 0.001) and right a power decrease (; = -0.45-[-0.58], p < 0.001) (figure 3). In light of these data, we have compressed the EEG and evoked potential findings into two neurophysiological syndromes: left frontotemporal limbic (88 persons [44%]) and right-hemispheric (70 [35%]). We have also integrated the psychopathological data into two syndromes: schizophreniform (68 patients [34%]) and affective (73 (36.5%]). The schizophreniform syndrome includes negative symptoms, paranoid ideation, and sometimes elementary verbal hallucinations. The affective syndrome includes depression and anxiety. In both syndromes, cognitive dysfunction, such as deterioration of planning skills (including the formation of long-range goals, the ability to marshal one's resources to achieve those goals, the capacity to consider and anticipate the future, and the ability to develop alternative problem-solving strategies and consider a range of ideas simultaneously) and short-term memory disorders were observed. The distribution of the neurophysiological and psychopathological syndromes in proportion to dose of irradiation is shown in table 8. Persons irradiated by moder-
ate or large doses (more than 0.30 Sv or 30 rem, including ARS patients) had significantly more left frontotemporal limbic and schizophreniform syndromes. Persons irradiated by small doses (less than 0.30 Sv or 30 rem) had significantly more right-hemispheric and affective and neurotic syndromes. However, among the persons irradiated by small doses, correlation analysis showed no relationship between the dose of irradiation and neurotic symptoms (anxiety, depression, somatic concern, tension, aggressivity, health self-estimation, PTSD) or neurophysiological parameters. This lack of correlation led us to conclude that neuropsychiatric and neurophysiological changes in Chernobyl accident survivors irradiated by small doses were likely a result of psychogenic trauma or other reasons rather than irradiation itself. At the same time, the schizoform symptoms together with the electrophysiological signs of the left frontotemporal dysfunction did correlate with the large effective dose of ionizing radiation (r = 0.23-0.45; p < 0.001).Thus, we suppose that overirradiation by doses more than 0.30 Sv or 30 rem can induce left frontotemporal limbic dysfunction, which may be the neurophysiological basis of schizophreniform symptoms in these patients.
Discussion
An increase in psychopathology among Chernobyl disaster survivors is not surprising. Etiological factors in the genesis of mental disorders in the survivors may be due to (1) psychological trauma and stress related to the disaster itself, (2) psychological trauma and stress related to the post-Soviet changes in the society, or (3) radiation effects (Napreyenko and Loganovsky, 1992, 1995, 1997; Nyagu et al. 1992; Loganovsky and Nyagu 1995; Loganovsky 1996a, 1996b; Nyagu and Loganovsky 1996,1997a, 1998a). Kamenchenko (1993), in a review of PTSD, related the prevalence of PTSD in American veterans of the
761
Figure 3. EEG correlates of some psychiatric symptoms in 146 overirradiated patients (dose more 0.30 Sv)
LEFT HEMISPHERE RIGHT HEMISPHERE
Delta (1-4 Hz) power (%)
Delta (1-4 Hz) power (%)
Theta (4-7 Hz) power (%)
Theta (4-7 Hz) power (%)
Alpha (7-12 Hz) power (%)
Alpha (7-12 Hz) power (%)
Beta (12-32 Hz) power (%)
Beta (12-32 Hz) power (%)
Table 8. Brain laterality and psychopathological syndromes in persons irradiated by small doses (< 0.3 Sv or 30 rem) and by moderate or large doses (> 0.3 Sv or 30 rem, including ARS patients)1
Small (< 0.3 Sv) doses, rate (%) (n = 54) 12(22) 7(13) 29 (54) 34 (63) Moderate or large (> 0.3 Sv) doses, rate (%) (n = 146)
76 (52) 61 (42) 41 (28) 39 (27)
Syndrome Left frontotemporal limbic Schizophreniform Right hemispheric Affective

1
X2 14.24 14.59 11.37 22.35

,
df
i
P
< 0.001 < 0.001 < 0.001 < 0.001
1 1 1 1
Note.ARS = acute radiation sickness. The x

2
tests were performed on 2 x 2 tables of small and higher doses by syndrome presence and absence.
Vietnam War as 9-15 percent and reported that about 10-20 percent of patients developed PTSD following a natural disaster. Moreover, in the Report of the Scientific Center of Mental Health of the Russian Academy of Medical Sciences (1994), the prevalence of all mental disorders in the general population (including borderline cases) has been estimated as 20-27 percent. So, at least one-third of all Chernobyl accident survivors would be expected to have mental disorders theoretically. However, the real prevalence of mental disorders among the Chernobyl population is significantly higher.
Vokhmekov et al. (1994) discussed the increasing prevalence of all mental disorders (ICD-9: 290-310) from 156.6 per 1,000 EZ workers in 1986 to 225.2 per 1,000 in 1992. Moreover, in 1992 those workers exposed to ionizing radiation in doses more than 0.25 Sv had a prevalence of borderline mental disorders 3.76 times higher than other EZ personnel: 805.1 and 214.0 per 1,000 workers, respectively. This is very similar to other data in the literature. The prevalence of autonomic nervous system dysfunction in chemical factory personnel is 86 percent and increases with the length of work (Vein et
762
At Issue
al. 1991). At the same time, there are psychiatric symptoms in 89 percent of patients suffering from autonomic nervous system dysfunction (Zharikov et al. 1996). In other words, it is scientifically reasonable to suppose that at least 76 percent of the Chernobyl EZ personnel probably suffer from mental disorders, predominantly of the borderline category. However, it is not clear what factor or factors could produce an increase in schizophrenia incidence in the Chernobyl EZ personnel. Schizophrenia diagnostic criteria were the same in and out of the Chernobyl EZ. It is unlikely that workers faked mental disorders in order to be rejected from the personnel, because the workers are volunteers with relatively high salary. There was not a relative increase in the number of younger individuals in the personnel of the Chernobyl EZ, which would have resulted in a concomitant increase in risk for new cases of schizophrenia. A self-selection of some individuals who are marginally adapted to society to go or remain in the accident region could be a possible explanation. However, this does not explain why the increase in schizophrenia only began 3 years after the disaster. Moreover, all candidates were medically examined before employment in the EZ. Therefore, it seems reasonable to associate the increase in schizophrenia incidence with exposure to radiation (Loganovsky and Nyagu 1997; Loganovsky 1998; Loganovsky and Loganovskaja 1998). We suppose that ionizing radiation is an environmental trigger that can actualize schizophrenia in predisposed individuals. There is another important question: If exposure to ionizing radiation is associated with risk for schizophrenia, one might expect a decline in risk over the past decade with an eventual return to baseline levels. Instead, we have found an increase in incidence 3 years after the accident, which remained relatively stable over the next 8 years. There were no changes in diagnostic practice, screening procedures, or population composition. Also, 31 (73.8%) of the cases of schizophrenia onset that occurred at the Chernobyl EZ were among the cleanup workers of the Chernobyl accident (the liquidators) of 1986-1987, those with the greatest risk for irradiation. We propose the hypothesis that some cases of schizophrenia onset may be a delayed stochastic aftereffect of irradiation, similar to thyroid cancer, which has been increasing in the Chernobyl survivors since 1990-1991. The clinical and psychophysiological patterns in overirradiated persons are of the greatest interest. Previously published data (Loganovsky and Nyagu 1995; Napreyenko and Loganovsky 1995, 1997; Nyagu and Loganovsky 1996, 1997a) testify to a significant overlapping of diagnoses, according to the ICD-10 criteria, in survivors who meet the criteria of different disorders simultaneously, which produces difficulties and contradic-
tions. Moreover, the neuropsychiatric symptoms in ARS patients were classified as postradiation encephalopathy and the symptoms in overirradiated persons as mixed exogenous-somatogenous encephalopathy (Nyagu et al. 1997; Nyagu and Loganovsky 1998). According to the data obtained, overirradiation by doses more than 0.30 Sv or 30 rem (including the development of radiation sickness) can induce left frontotemporal limbic dysfunction, which may be the neurophysiological basis of schizophreniform symptoms in these patients. A majority of the Chernobyl accident survivors had been exposed to low-dose irradiation (less than 0.30 Sv or 30 rem), which together with other factors of the accident (predominantly psychogenic trauma) may have led to the right-hemispheric dysfunction and consequent affective symptoms. We cannot conclude that the righthemispheric dysfunction and associated affective and neurotic symptoms are radiation induced. Our psychophysiological findings are consistent with much of the literature data (Izumi and Hayakawa 1955; Nishikawa and Tsuiki 1962; Sosnovskaja 1971; Yaar et al. 1980; Chayanov and Monosova 1992; Zhavoronkova and Kholodova 1994; Zhavoronkova et al. 1995; Viatleva et al. 1996) and reflect an overlap of pathophysiological patterns of schizophrenia and postradiation brain injury (table 9). Currently, dysfunction of the limbic system is considered to be the key neuropathological event underlying schizophrenia (Csernansky and Bardgett 1998). The hippocampal hypothesis of psychoses was proposed by Port and Seybold (1995). Left frontotemporal limbic dysfunction is the determining pattern of cerebral disorganization leading to schizophrenia (Flor-Henry 1976, 1983, 1989; Gruzelier and Hammond 1976; Gur 1978, 1997; Gruzelier 1997). The limbic system, particularly the hippocampus, is extremely radiosensitive (Lebedinsky and Nakhilnitzkaja 1960; Ganglof 1962; Haley 1962; Livanov 1962; Kimeldorf and Hunt [1965] 1969; Peimer et al. 1985; Hunt 1987; Dudkin 1988). The data obtained in our laboratory demonstrated the left frontotemporal lateralization of EEG abnormalities in the Chernobyl accident survivors (Noshchenko and Loganovsky 1990, 1994; Nyagu et al. 1992, 1996). Other authors have obtained identical (Chayanov and Monosova 1992) or similar results (Zhavoronkova et al. 1995,1998). A dysfunction of the diencephalo-limbic-reticular complex and left frontotemporal cortex was recognized as the neurophysiological basis of ionizing radiation effects (Nyagu and Loganovsky 19976, 1998). We propose that the left hemisphere is more vulnerable, in right-handed men, to whole-body irradiation than the right. Our data are consistent with other types of evidence also indicating a specific vulnerability of the left hemisphere: After unilateral nondominant or bilat-
763
Table 9. Psychophysiological and neuropathological patterns in schizophrenia and postradiation brain injury
5?
3-
Schizophrenia Psychophysiological Symptomatology
Postradiation brain injury
i
S'
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Left-sided EEG abnormalities, especially on the left temporal area (FlorHenry 1969a, 1969/?, 1976, 1983, 1987, 1989; Hughes 1996) Lateralization of EEG abnormal activity to the left frontotemporal area (Nyagu et al. 1992,1996,1997,1998; Noschenko and Loganovsky 1994; Zhavoronkova and Kholodova 1994; Zhavoronkova et al. 1995; Loganovsky, 1995,1996a, 19966,1998; Loganovsky and Nyagu, 1995; Loganovskaja and Loganovsky 1997,1998; Loganovsky and Loganovskaja 1997,1998; Nyagu and Loganovsky 1997a, 1997b, 1998)
I
o o o o
Increase in temporal p 2 power (Kessler and Kling 1991); increase in the higher p (16-25.5 Hz) range (Michel et al. 1993); dysrhythmic EEG with an increase of p activity (Herrmann and Winterer 1996)
Increase of p activity (Sosnovskaja 1971) or p power, particularly in the left hemisphere (frontotemporal area) (Izumi and Hayakawa 1955; Yaar et al. 1980; Nyagu et al. 1992,1996,1997,1998; Noschenko and Loganovsky 1994; Loganovsky 1995,1996a, 1996b, 1998; Loganovsky and Nyagu 1995; Zhavoronkova et al. 1995; Viatleva et al. 1996; Loganovskaja and Loganovsky 1997,1998; Loganovsky and Loganovskaja 1997, 1998; Nyagu and Loganovsky 1997b, 1998) Increase of a activity (Sosnovskaja 1971) or a power (Nishikawa and Tsuiki 1962; Court 1979) shifted to the left frontotemporal area (Nyagu et al. 1992,1996,1997,1998; Chayanov and Monosova 1992; Khomskaja et al. 1993; Noschenko and Loganovsky 1994; Zhavoronkova and Kholodova 1994; Loganovsky 1995,1996a, 1996b, 1998; Loganovsky and Nyagu 1995; Viatleva et al. 1996; Loganovskaja and Loganovsky 1997,1998; Loganovsky and Loganovskaja 1997,1998; Nyagu and Loganovsky 1997b, 1998) Redistribution of a power to the frontal areas (Nyagu et al. 1992,1996, 1997, 1998; Noschenko and Loganovsky 1994; Loganovsky 1995,1996a, 1996b, 1998; Loganovsky and Nyagu 1995; Loganovskaja and Loganovsky 1997,1998; Loganovsky and Loganovskaja 1997, 1998; Nyagu and Loganovsky 1997b, 1998; Zhavoronkova and Kholodova 1994; Viatleva et al. 1996); dysrhythmic (low-voltage) EEG (Nyagu et al. 1996, 1997,1998; Loganovsky and Loganovskaja 1997, 1998; Nyagu and Loganovsky 1996,1997b, 1998; Zhavoronkova et al. 1998) Reduced left frontal and left frontotemporal coherence on EEG (Zhavoronkova and Kholodova 1994; Zhavoronkova et al. 1995,1998) Topographic abnormalities of SSEP and VEP at left temporoparietal areas (C3); abnormal cortical-subcortical interactions during analysis of afferent information; disorders of brain information processing (Loganovsky 1995, 1996a, 1996b; Loganovsky and Nyagu 1995; Loganovskaja and Loganovsky 1997,1998; Loganovsky and Loganovskaja 1997,1998; Nyagu and Loganovsky 1997b, 1998)
Lateralization for temporal <r and frontal p1 activity (Kessler and Kling 1991); increase of a, 6^ and p 3 amplitude (Galderisi et al. 1991); increased a, fast a, and p power in particular at left frontal sites (Gattaz et al. 1992)
Relative abundance of a 2 power value shifts from the occipital to the frontal regions, supporting the hypofrontal hypothesis of schizophrenia (Nakagawa etal. 1991)
Reduced bilateral alpha interhemispheric coherence on EEG during the activation task (Morrison-Stewart et al. 1996), more on the left side (Michelogiannis et al. 1991)
Topographic differences of SSEP and VEP at left temporoparietal areas (Shagass and Roemer 1991); abnormal cortical-subcortical interactions during analysis of visual information (Jutai et al. 1984); impaired auditory sensory gating (Adler and Waldo 1991) and sensorimotor gating, sensory flooding, and cognitive fragmentation (Swerdlow and Geyer 1998)
P300 ERP abnormalities (Blackwood et al. 1991); lower P300 amplitude (Kidogami et al. 1991) and prolonged N 400 latency of ERP (Koyama et al. 1991) P300 SSEP and P2Oo VEP abnormalities; lower amplitude of P300 SSEP and P200 VEP; prolonged latency of P300 and N 400 SSEP and P200 VEP (Loganovsky 1995,1996a, 1996b; Loganovsky and Nyagu 1995; Loganovsky and Loganovskaja 1997,1998; Nyagu and Loganovsky 1997a, 1997b, 1998) Memory and learning disorders (Nyagu et al. 1992,1996,1997, 1998; Nyagu and Loganovsky 1997b; Noschenko and Loganovsky 1994; Loganovsky 1995,1996a, 1996b, 1998; Khomskaja 1995; Loganovsky and Nyagu 1995; Loganovskaja and Loganovsky 1997,1998; Loganovsky and Loganovskaja 1997,1998; Nyagu and Loganovsky 1997a, 1998) and verbal memory impairment associated with medial temporal lobe dysfunction (Meshkov et al. 1998) Autonomic nervous system dysfunction (Nyagu et al. 1992,1996,1997,1998; Nyagu and Loganovsky 1997b; Noschenko and Loganovsky 1994; Loganovsky 1995,1996a, 1996b, 1998; Nyagu and Loganovsky 1997a, 1998) Negative symptomsblunted affect, avolition-apathy, inattention, difficulty with problem solving, impoverished thinkingrelated to frontal lobe dysfunction, particularly on the left (Loganovsky 1995,1996a, 1996b, 1998; Loganovsky and Nyagu 1995; Loganovsky and Loganovskaja 1997,1998)
Working memory dysfunction (Goldman-Rakic 1994), verbal memory dysfunction (Heinrichs 1994), selective impairments in learning and memory consistent with medial temporal lobe dysfunction (Arnold 1997)
Autonomic nervous system dysfunction (Hollister et al. 1994)
Negative symptoms are related to left frontal lobe dysfunction (Suzuki et al. 1992); frontal lobe dysfunctionblunted affect, difficulty with problem solving, impoverished thinking (Weinberger et al. 1994)
Significant positive correlations between the total negative symptoms and the 8 power, predominantly over the temporal region (Gattaz et al. 1992)
KJ
Significant positive correlations between the total negative symptoms and 8 power, predominantly over the left frontotemporal region (Loganovsky 1995,1996a, 1996b, 1998; Loganovsky and Loganovskaja 1997,1998)
Neuroanatomical Syndromology Left frontotemporal-limbic dysfunction (Loganovsky 1995,1996a, 1996b, 1998; Loganovskaja and Loganovsky 1997, 1998; Loganovsky and Loganovskaja 1997,1998)
Left frontotemporal abnormalities (Flor-Henry 1969a, 1969b, 1976,1983, 1987,1989; Deakin et al. 1989; Bullmore et al. 1998); left temporal lobe abnormalities (Shenton et al. 1992; Rossi et al. 1994)
Temporal-limbic seizure system involvement (Flor-Henry 1976,1987); medial temporal lobe abnormalities (Roberts 1991; Arnold 1997); schizophrenia-like psychosismediobasal temporal (left) lobe epilepsy (Flor-Henry 1969a, 1969b, 1983; Jibiki et al. 1993; Sachdev 1998)
Left frontotemporal cortex and diencephalo-limbic-reticular complex dysfunction (Nyagu et al. 1996,1997,1998; Loganovsky 1995,1996a, 1996b, 1998; Loganovsky and Nyagu 1995; Loganovskaja and Loganovsky 1997,1998; Loganovsky and Loganovskaja 1997,1998; Nyagu and Loganovsky 1997b, 1998) Frontal-subcortical-limbic-reticular complex dysfunction with the prominent impairment of brain stem and mediobasal structures (Zhavoronkova et al. 1995,1998) Limbic system dysfunction (Gangloff 1962; Haley 1962; Livanov 1962); very high radiosensitivity of hippocampus (Peimer et al. 1985; Davydov and Ushakov 1987; Dudkin 1988)
5'
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Limbic system dysfunction (Gruzelier and Raine 1994); limbic structure abnormalities (Bogerts 1993); limbic-cortical (temporal and frontal) neuronal damage (Arnold and Trojanowski 1996; Bachus and Kleinman 1996; Csernansky and Bardgett 1998)
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eral electroconvulsive therapy (ECT) the post-ECT EEG slow activity is lateralized to the left hemisphere (Green 1957; Abrams et al. 1970; Abrams 1988; Deglin 1996). Thus, the left hemisphere seems to be generally more vulnerable to exogenous factors in right-handed men compared with the right hemisphere. A possible explanation of such specific left-hemisphere vulnerability is the increasing number of reports showing a relative reduction of cerebral blood flow in the left hemisphere (Amsterdam and Mozley 1992; Seitz and Roland 1992; Klingelhofer et al. 1997; Hugdahl 1998). Some authors (Risberg et al. 1975; Kawahata et al. 1997) found no hemispheric differences. Thus, the radiation-induced left frontotemporal limbic dysfunction may be the neurophysiological basis of schizophrenia-like symptoms in overirradiated persons.
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Conclusions
The problem of schizophrenia spectrum disorders in individuals exposed to ionizing radiation is under discussion. The data obtained relating an increase of schizophrenia incidence in the Chernobyl EZ personnel support our hypothesis that ionizing radiation is an environmental trigger that can actualize a predisposition to schizophrenia or indeed cause symptomatic schizophrenia. The development of schizophrenia spectrum disorders in overirradiated Chernobyl survivors may be the consequence of the radiation-induced left frontotemporal limbic dysfunction, which may be the neurophysiological basis of schizophrenia-like symptoms in individuals exposed to ionizing radiation in doses more than 0.30 Sv or 30 rem, including ARS patients. Thus, those exposed to 0.30 Sv (30 rem) or more are at higher risk of schizophrenia spectrum disorders. Prenatally irradiated children in the Chernobyl accident, especially those exposed at the second trimester of gestation, are at higher risk for schizophrenia too (Loganovskaja and Loganovsky 1997, 1998; Nyagu et al. 19986). An integration of international efforts to discuss and organize collaborative studies in this field is of great importance for both clinical medicine and neuroscience.
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References
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Abrams, R. Electroconvulsive Therapy. New York, NY: Oxford University Press, 1988. Abrams, R.; Volavka, J.; Dornbush, R.; Roubicek, J.; and Fink, M. Lateralized EEG changes after unilateral and bilateral electroconvulsive therapy. Diseases of the Nervous System GWAN Supplement, 31:28-33, 1970. Adler, L.E., and Waldo, M.C. Counterpoint: A sensory gatinghippocampal model of schizophrenia. Schizophrenia Bulletin, 17(l):19-24,1991.
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Acknowledgments
We express our cordial gratitude to Prof. Pierre FlorHenry (Edmonton, Canada) for his creative advice, kind support, and encouragement during this study. We are indebted to Dr. John Lind (Edmonton, Canada) for constructive suggestions, criticism, and help in the statistical analysis. We thank all our anonymous referees, who have spent a great deal of time evaluating our manuscript, for their criticism, helpful comments, and patience.
The Authors
Konstantin N. Loganovsky, M.D., Ph.D., is Leading Scientist and Psychiatrist, and Tatiana K. Loganovskaja, M.D., is Scientist and Psychiatrist, Department of Neurology, Institute of Clinical Radiology, Scientific Center for Radiation Medicine, Academy of Medical Sciences of the Ukraine, Kiev, Ukraine.
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At Issue: Schizophrenia Spectrum Disorders in Persons Exposed To Ionizing Radiation As A Result of The Chernobyl Accident

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At Issue: Schizophrenia Spectrum Disorders in Persons Exposed to Ionizing Radiation as a Result of the Chernobyl Accident

by Konstantin N. Loganovsky and Tatiana K. Loganovskaja

Downloaded from http://schizophreniabulletin.oxfordjournals.org/ by guest on February 25, 2013

Schizophrenia Bulletin, Vol. 26, No. 4, 2000

K.N. Loganovsky and T.K. Loganovskaja

Downloaded from http://schizophreniabulletin.oxfordjournals.org/ by guest on February 25, 2013

Schizophrenia Bulletin, Vol. 26, No. 4, 2000

Downloaded from http://schizophreniabulletin.oxfordjournals.org/ by guest on February 25, 2013

Table 1. Schizophrenia onset during 1986-1997 in Chernobyl exclusion zone personnel

Schizophrenia Bulletin, Vol. 26, No. 4, 2000

K.N. Loganovsky and T.K. Loganovskaja

Downloaded from http://schizophreniabulletin.oxfordjournals.org/ by guest on February 25, 2013

Schizophrenia Bulletin, Vol. 26, No. 4, 2000

Affective psychoses (296) Reactive psychoses (298) Mental retardation (317)

Downloaded from http://schizophreniabulletin.oxfordjournals.org/ by guest on February 25, 2013

Schizophrenia Bulletin, Vol. 26, No. 4, 2000

K.N. Loganovsky and T.K. Loganovskaja

Downloaded from http://schizophreniabulletin.oxfordjournals.org/ by guest on February 25, 2013

Table 3. Neuropsychiatric symptoms in irradiated persons and controls

ARS patients (n = 100), % 86 98 60 54 78 44 98 68 20 18 52 29 42 74 21 85 81

Schizophrenia Bulletin, Vol. 26, No. 4, 2000

P ns ns ns ns ns ns ns < 0.001 ns ns ns ns ns . ns < 0.001

100(68) 90 (62) 47 (32) 68 (47) 117(80) 29 (20) 119(81) 117(80)

Schizophrenia Bulletin, Vol. 26, No. 4, 2000

K.N. Loganovsky and T.K. Loganovskaja

Downloaded from http://schizophreniabulletin.oxfordjournals.org/ by guest on February 25, 2013

Schizophrenia Bulletin, Vol. 26, No. 4,2000

Table 6. EEG patterns in irradiated persons and controls

ARS patients (n=100) 0

Normals (n = 20) 16(80)*

10(10) 58 (58) 16(16)

8(8) 45 (45) 10(10)

9(18) 3(6)* 1(2)

8(16) 6(12)* 4(8)

20 (20) 57 (57) 23 (23)

7(7) 31 (31)* 34 (34)

9(18) 1(2)* 3(6)

10 (20) 4(8)* 6(12)

Table 7. Neurophysiological indexes in irradiated persons and controls

ARS patients (n=100)

Veterans with PTSD (n = 50)

Laterality (F3-F4) Paired ftest

Laterality (C3-C4) Paired Mest

T3 T4 Laterality (T3-T4) Paired Hest

Theta (4-7 Hz) power (%) of EEG in:

9.5 3.8 8.1 2.9 1.1 2.2

12.1 4.3* 12.0 3.8* 0.3 2.1

16.1 4.3* 16.0 3.5* 0.1 1.98

18.7 5.2* 18.9 5.4* -0.1 2.12

15.5 5.7* 16.1 4.1* -0.12 2.69

Schizophrenia Bulletin, Vol. 26, No. 4, 2000

K.N. Loganovsky and T.K. Loganovskaja

Table 7. Neurophysiological indexes in irradiated persons and controlsContinued

Index Paired ftest T3 T4 Laterality (T 3 -T 4 ) Paired ftest

Alpha (7-12 Hz) power (%) of EEG in:

Laterality (O-,-O2) Paired ftest

41.2 10.8 45.4 12.9 -3.46 5.42 f=-6.38, p < 0.001

45.1 8.3* 47.0 7.8 -1.78 5.12 f=-3.48, p< 0.001

56.1 14.3* 55.0 13.5* 1.1 6.9 f= 1.13, ns

48.7 15.2* 48.9 15.4* -0.1 6.8 f=-0.1,/7S

54.5 12.7* 60.4 14.1* -4.3 6.75 f = -2.85, ns

Beta (12-32 Hz) power (%) of EEG in:

Laterality (C 3 -C 4 ) Paired f test