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 inPersons Exposed to Ionizing Radiation as aResult of the Chernobyl Accident

by Konstantin N . Loganovsky and Tatiana K. Loganovskaja

Th e At Issue section of the Schizophrenia Bulletin con-tains viewpoints and arguments on controversial issues.Articles published in this section ma y not meet the stricteditorial and scientific standards that are applied tomajor articles in the Bulletin. In addition, the viewpointsexpressed in the following article do not necessarily rep-resent those of the staff or the Editorial Advisory Boardof the Bulletin. The Editors.

AbstractWe studied schizoph renia spectrum disord ers inChernobyl accident survivors by analyzing Chernobylexclusion zone (EZ) archives (1986-1997) and by con-duct ing a psychophys iological examinat ion of 100patients with acute radiation sickness (ARS) and 100workers of the Chernobyl EZ who had worked as "liq-u id ato rs -v o lu n te ers " for S or more years s in ce1986-1987. Beginning in 1990, there has been a signifi-cant increase in the incidence of schizophrenia in EZpersonnel in comparison to the general population (5.4per 10,000 in the EZ versus 1.1 per 10,000 in theUkraine in 1990). Those irradiated by moderate tohigh doses (more than 0.30 Sv or 30 rem), includingARS patients, had significantly more left frontotempo-ral l imbic and schizophreniform syndromes .1 W ehypothesized that ionizing radiation may be an envi-ronmental trigger that can actualize a predispositionto schizophrenia or indeed cause schizophrenia-likedisorders. The development of schizophrenia spectrumdisorders in overirradiated Chernobyl survivors maybe due to radiation-induced left frontotemporal limbicdysfunction, which may be the neurophysiologicalbasis of schizophrenia-like symptoms. Persons exposedto 0.30 Sv or more are at higher risk of schizophrenia

'l Gy (gray) = one unit of absorbed dose of ionizing radiation = 100rad (radiation absorbed dose). 1 Sv (sievert) = one unit of effective doseof ionizing radiation = 100 rem (roentgen equivalent man). Regardingthe Chernobyl accident, 1 Sv = 1 Gy .

spectrum disorders. An integration of internationalefforts to discuss and organize collaborative studies inthis field is of great importance for both clinical medi-cine and neuroscience.

Keywords: Schizophrenia spectrum disorders ,ionizing radiation, Chernobyl accident, laterality, psy-chophysiology, brain mapping of EEG, evoked poten-tials, limbic system.

Schizophrenia Bulletin, 26(4):751-773, 2000.Evidence is increasing in support of the etiologic hetero-geneity of schizophrenia (Coleman and Gillberg 1997;Garver 1997). Schizophrenia results from the interactionof multiple factors, including the person's genetic endow-ment and various environmental influences (Kirch 1993).The exact role of environmental hazards in the develop-ment of the illness, however, remains unclear (Shore1986; Buszewicz and Phelan 1994; McGuffin et al. 1994;Syvalahti 1994; Fuller Torrey [1995] 1996).

Evidence is dramatically increasing in support of theneuropathology of schizophrenia (Flor-Henry 1969a,19696, 1976, 1983, 1987, 1989; Gur and Pearlson 1993;Gruze l ie r and Raine 1994; Arnold 1997; Egan andWeinberger 1997; Willner 1997; Bullmore et al. 1998;O'Donnell and Grace 1998; Sachdev 1998). Left fron-totemporal abnormalities have been outlined as a cerebralbasis of schizophrenia (Flor-Henry 1969a, 19696, 1976,1983, 1987, 1989; Gruzelier and Hamm ond 1976; Deakinet al. 1989; Gruzelier 1997; Bullmore et al. 1998).Neurobiological studies suggest that abnorm alities of bothanatomy and function occur in the limbic-cortical struc-tures of schizophrenia patients. An anatomical circuit thatlinks functioning of the ventral striatum with the hip-pocampus and other limbic-cortical structures lies at thesite of these neurobiological abnormalities (Csernanskyand Bardgett 1998).

Send reprint requests to Dr. K.N. Loganovsky, 16D Heroes ofStalingrad St., Apt. 173, Kyiv, 04210, Ukraine; e-mail:[email protected].

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Schizophrenia Bulletin, Vol. 26, N o. 4 , 2000 K.N. Loganovsky and T.K. Loganovskaja

Exposure to ionizing radiation causes brain damagewi th l imb ic sys te m dys func t i on (G r igor ie v 1958 ;Lebedin sky and Nakhiln itzkaja 1960; Gangloff 1962;Haley 1962; Lebedinsky 1962; Livanov 1962; Kimeldorfand Hunt [1965] 1969; Hunt 1987). Moreover, the hip-pocampus is a very radiosensitive structure (Kimeldorfand Hunt [1965] 1969; Davydov and Ushakov 1987). X-ray irradiation of the hippocampus by low doses of 6-8mGy (0.6-0.8 rad) produces the endogenous (pacemaker)generation of nervous impulses (Peimer et al. 1985;Dudkin 1988). Thus, the hypothesis arises that exposureto ionizing radiation can trigger schizophrenia in predis-posed individuals or cause schizophrenia-like disorders asa consequence of radiation-induced limbic dysfunction.

Studies on the relationship between schizophreniaand radiation exposure are practically absent in the avail-able literature. One study describes an atypical clinicalpattern of schizophrenia secondary to chronic irradiationwith prominent as thenia , autonomic ins tabi l i ty , andhypochondriac and psychosensory symptoms but does notlink schizophrenia onset to the ionizing radiation expo-sure (Golodetz 1962).Nakane and Ohta (1986) repor ted a s ignif icantincrease in the prevalence of schizophrenia in the A-bombsurvivors in Nagasaki. The Life Span Study (LSS), startedby the Radiation Effect Research Foundation in Japan, didnot include data on severe mental disorders. The Japaneseauthors combined the schizophrenia regis te r of the

Department of Neuropsychiatry, University School ofMedicine, Nagasaki, with the LSS register to fill in thisinformation. Th ey revealed that, in 1978, there were 1,589patients with schizophrenia in the LSS register (n -26,678). The schizophrenia register had been in operationonly since 1960, and it was not possible to calculateannual inception rates back to the bombing in 1945.Moreover, migration out of Nagasaki cannot be estimated.In spite of these methodological limitations, the preva-lence of schizophrenia in the A-bomb survivors was stillvery high (6 percent), while the prevalence of schizophre-nia is no more than 1 percent in the general population(Shore 1986; Fuller Torrey [1995] 1996).The first information about an increase in schizophre-nia incidence among the Chernobyl EZ personnel waspresented by Loganovsky and Nyagu (1997) a t theInte rna t iona l Conference on Low Doses of Ioniz ingRadiation: Biological Effects and Regulatory Control.

The purpose of this study is to investigate the schizo-phrenia spectrum disorders (schizophrenia, schizotypal,schizoaffective, organic schizophrenia-like, and schizoidpersonality disorders) among the irradiated Chernobylaccident survivors. The study includes two parts: (1) anepidemiological study of severe mental disorders in theChernobyl EZ personnel and (2) a psychophysiological

assessment of the irradiated personspatients who hadARS as well as the workers who cleaned up the C hernobylaccident consequences (so-called "liquidators").DesignBackground. At 1:23 AM, April 26, 1986, the fourth unitof the Chernobyl Nuclear Power Plant (ChNPP) wasdestroyed and about 300 MCi (11 X 10 18 Bq) of radioac-tive materials exploded into the environment. At the pres-ent t ime in the Ukra ine , there a re about 3 mil l ionChernoby l accident survivors. About 100,000 people hav ebeen evacuated from the 30-km zone surrounding theChNPP (the Chernobyl EZ). More than 600,000 peoplefrom the former USSR took part in cleaning up theChernobyl accident consequences from 1986 to 1989;these workers are called "liquidators." The most criticalgroup from the radiological point of view is the 126,000liquidators who worked from Ap ril 26, 19 86, to the begin-ning of 1987. Their average dose of irradiation was1 2 0 - 1 8 0 m S v ( 1 2 - 1 8 r e m ) , b u t 6 - 1 5 p e r c e n t(7,560-18,900 workers) were irradiated by more than 250mSv (25 rem). The effective doses of irradiation for otherChernobyl accident survivor contingents were signifi-cantly lower. The average dose per year of irradiation of"non-Chernobyl" origin for the Ukrainian population is5.3 mSv/year (0.53 rem/year; Likhtarev et al. 1994; Los'and Likhtarev 1994; Likhtarev 1996; Ministry of Ukraine1996).ARS has been diagnosed in 237 persons, 29 of whomdied as a result of the exposure 7-96 days after the acci-dent (Kindselsky et al. 1995; Romanenko et al. 1995).Only 134 patients had verified ARS (absorbed doses0.7-13 Gy or 70-1300 rad) (Wagemaker and Bebeshko1996). The remaining 103 patients in whom ARS wasdiagnosed are considered to have a subclinical form ofA R S . At the present time, 180 persons who had beendiagnosed with ARS in 1986 are living in the Ukraine andare in a followup study at the Scientific Center forRadiation M edicine, Kiev (Bebeshko et al. 1996).

The ARS patients and the liquidators of 1986 -198 7clearly have the highest radiation risk. However, untilnow, epidemiological data concerning severe mental dis-orders among the liquidators have been practically absent,possibly due to (1) lack of radioepidemiologic interest inthis problem in comparison with traditional topics such asradiation-induced malignancies and hereditary disorders;(2) a deficiency of psychiatric information in the radiolog-ical registers, and vice versa; and (3) high rates of migra-tion among the liquidators.The particular group of Chernobyl accident survivorsfocused 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 weekswithin the EZ and 2 weeks at home). They were medicallymonitored and available for epidemiological assessment.Consequently , the 12-year fol lowup s tudy of theChernobyl EZ personnel is a unique opportunity to inves-tigate the epidemiology of severe mental disorders in thispopulation.Epidemiological Study. The data for the epidemiologicalpart of the study was obtained from the psychiatricarchives (1986-1997) of the Medica l and Sani ta ryDepartment in Chernobyl. Since 1986, this departmenthas undertaken the somatic and mental health monitoringof EZ personnel. The number surveyed each year is pre-sented in table 1.The numbe r o f EZ pe r sonne l de c re a se d s inc e1988-1990, when the emergency cleanup was complete.It was intended that all ill workers or those who were at ahigh risk for any disease (especially mental disorders)would not be employed in the EZ or would be eliminatedfrom the EZ personnel if disease developed after they hadbegun work. Further, it should be noted that the EZ per-sonnel are volunteers. Therefore, it is doubtful that work-ers would present fictitious symptoms (e.g., malingering)in order to be transferred out of the area and, conse-quently, lose their jobs, which have a higher salary thanjobs outside the EZ.Among the EZ personnel, 78.9 percent were men,with 32.9 percent ranging in age from 40 to 49 years, 30.2percent from 30 to 39 years, and 24.7 percent from 50 to59 years. The majority were engineers and technicians.The p ercentage working in the EZ for 5 or more years was60.6 percent. The distribution of EZ personnel accordingto the effective doses of irradiation was as follows: < 0.05Sv (5 rem), 81.8 percent; 0.05-0.24 Sv (5-24 rem), 13.6percent; 0.25-0.99 Sv (25-99 rem), 3.7 percent; > 1 Sv

(100 rem), 0.82 percent (Vokhmekov et al..l994). Allrecords in the psychiatric archives of the Medical andSanitary Department of Chernobyl were studied. Controldata for the epidemiological part of the study came fromthe official statistical data of the Ministry of Public H ealthof Ukraine (1970-199 7).

In the Ukraine, the incidence of psychiatric illness,particularly of severe mental disorders, is calculated onthe basis of hospital admissions. The diagnosis of psy-chotic disorder is verified during hospitalization and isincluded in the calculation of base rate statistics. UntilApril 1999 in the Ukraine, ICD-9 diagnostic criteria wereused. This same methodology is used in the Chernobyl EZto diagnose disorders in current personnel, and a nonstan-dardized interview and medical documentation are used toreview prospective EZ personnel. If a mental disorder isrevealed during the interview or the candidate has beenregistered with national mental health care, the candidateis not accepted for employment in the EZ. A screening forsevere mental disorders is carried out if abnormal behav-ior or acute symptoms are present. Individuals are trans-ferred by colleagues, ambulance, or the police to the psy-chiatrist of the Medical and Sanitary Department ofChernobyl, who decides whether to transfer the patient tothe mental hospital. If a severe mental disorder is verifiedin the hospital, data about the disorder are included in theregister. This common diagnostic procedure leads to ageneral underestimation of mental disorders but makespossible a comparison of data in the EZ with data fromthe general population. It should be noted that the epi-demiological data on th e basis of the psychiatric archivesof Chernobyl are accurate only for severe mental disor-ders. Borderline mental disorders irf'EZ personnel areclassified as a comorbidity of physical diseases and, con-sequently, are excluded from the psychiatric archives andregistration.

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

Year198619871988198919901991199219931994199519961997

Cases of schizophreniaonset221266454433

Population of theChernobyl exclusion zonepersonnel

25,00025,00025,00012,50011,00011,25012,50012,96311,00011,0006,5555,329

Incidence of schizophreniaper 10,000 of population0.80.80.41.65.45.33.23.93.63.64.65.6

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We should note the following limitations of the epi-demiological part of our study: (1) the absence of stan-dardized diagnostic methods and the impossibility ofbeing "blind" to radiation exposure status; (2) specificdemographic characteristics and the relatively small num-ber of EZ personnel; (3) migration; and (4) the impossi-bility of calculating the prevalence of schizophrenia in thepersonnel because (a) candidates had been medicallyexamined before employment in the EZ and all psychi-atric patients rejected, and (b) individuals who were diag-nosed with schizophrenia were terminated from employ-me nt . As a r e su l t , a na tu ra l "a c c umula t ion" o fschizophrenia is absent among personnel, which results inan a r t i f ic ia l reduc t ion of schizophrenia preva lence .Consequently it was only possible to assess schizophreniaincidence in EZ personnel.

The data obtained have been analyzed with the chi-square test and vital statistics methods (measures of mor-bidity) (Kuzma 1984). Because of the large number ofvariables 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 conductedin the Neurology Depar tment , Ins t i tute of Clinica lRadiology, Scientific Center for Radiation Medicine,Ac a de my of Me dic a l Sc ie nc e s o f the Ukra ine , in1996-1998. Composition of the groups was as discussedbelow.Group A comprises 100 acutely irradiated patientswho had ARS (absorbed doses up to 6.6 Gy or 660 rad) asa result of the Chernobyl disaster. All were right-handedmen and 3564 years old at the time of examination.Subcl inica l ARS has been diagnosed in 30 of thesepatients (average absorbed dose of relatively even 7 and pirradiation was 0.2 0.05 Gy [20 5 rad]); first degreeARS was diagnosed in 38 (1.07 0.12 Gy or 107 12rad); and second or third degree ARS in 32 (2.69 0.2 Gyor 269 20 rad). All were treated in the Department ofRadiation Pathology in the Institute of Clinical Radiology,Scientific Center for Radiation Medicine of the Academyof Medical Sciences of Ukraine. The psychophysiologicalinve s t iga t ions we re c a r r ie d ou t in the Ne uro logyDepartment, 10-12 years after ARS.

Group B is composed of 100 chronically irradiatedstaff members of the Chernobyl EZ who have been work-ing as liquidators-volunteers in the EZ since 1986-1987for 5 or more years. All were right-handed men and 25-48years old at the time of examination. Fifty-four from thisgroup (group Bl) were chronically irradiated at dosesbelow 0.30 Sv or 30 rem (average dose 0.16 0.05 Sv or16 5 rem), and 46 (group B2) were chronically irradi-

ated above 0.30 Sv or 30 rem (average dose 0.69 0.15Sv or 69 15 rem).Group C is the control group: normal age- and gender-matched adults (n = 20), veterans of the Afghanistan warwith post-traumatic stress disorder (PTSD; n = 50), and vet-erans with both PT SD and closed head injury (n = 50).

Neurological examination and typical clinical psychi-atric interview (non standardized) were used, together withthe Brief Psychiatric Rating Scale (BPRS; Overall andGorham 1962), the Scale for the Assessment of NegativeSymptoms (SANS; Andreasen 1982), the General HealthQuestionnaire (GH Q-2 8; Goldberg 1981, Goldberg andBridges 1987, Goldberg and Williams 1988), and theadapted version of the Minnesota Multiphasic PersonalityInventory (MMPI; Sobchik 1990).Computerized electroencephalogram (EEG) and sen-sory evoked potentials were carried out with a 19-channelbrain biopotentials analyzer ("Brain Surveyor," SAICO,

I t a ly ) . The bra in spontaneous e lec tr ic ac t ivi ty wasmonopolar ly regis te red with l inked ears re fe rence .Nineteen scalp electrodes were placed according to the10-20 International System. Visual and spectral analysesof EEG were carried out. Epochs used in the analysiswere 60 seconds. The obtained frequency band was 1-32Hz. All of the EEG records were visually edited for arti-facts; artifacts due to eye or muscle movements or respi-ration were deleted prior to analysis. Estimation and inter-pretation of the brain spontaneous electrical activity wereconducted according to Zhirmunskaja's algorithm (1991)for clinical EEG, while spectral analysis was carried outusing classical Fast Fourier Transformation methods(Niedermeyer and Lopes da Silva 1982; Zenkov andRonkin 1991).

Checkerboard, revers ible -pa t te rn visua l evokedpotentials (VEP) were registered binocularly on 50 chess-pattern reversals with a frequency of 1 Hz. The 50 epochsselected for analysis were 400 ms in duration with ampli-tudes measured from peak to trough (mkV) and latencymeasured from onset of stimulation to its peak (ms).Somatosensory evoked potentials (SSEP) were registeredwith 40 pain threshold electrocutaneous stimulations ofthe right median nerve on the lower forearm. The leftmedian nerve was not stimulated. The nerve was stimu-lated by bipolar skin electrode w ith right-angled electricalimpulses of 0.1-ms duration and 0.5-Hz frequency (1 per2,000 ms). The cathode was situated proximally. Theepochs selected for analysis were 50 ms for the short-latency SSEP and 1,000 ms for long-latency. Amplitudeswere measured from peak to trough (mkV), latency fromonset of stimulation to its peak (m s).

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 indi-vidual (Montgomery 1976). The Bonferroni correctionwas used when multiple statistical tests were performed(Kirk 1982).ResultsEpidemiological Study of Severe Mental Disorders inChernobyl EZ Personnel. Data on Chernobyl EZ per-sonnel from the psychiatric archives on severe mental dis-orders are presented in table 2. The schizophrenia spec-trum disorders register (1986-1997) includes 72 workersof the EZ suffering from sc hizophre nia, schizoaffectivedisorder, organic (nonalcoholic) schizophrenia-like psy-choses, and schizoid personality disorder. There were 53schizophrenia subjects according to the ICD-9 criteria ofschizophrenia (code 295, excluding "slow progressiveschizophrenia") who also met the criteria of ICD-10 codeF20 (schizophrenia). A statistically significant increase inschizophrenia (among all psychoses) was found in EZpersonnel relative to the general Ukrainian population(73% vs. 43%; x 2 = 18.5; df= \\p< 0.001). The relativerisk was 1.7, indicating that working and living in the EZare associated with a nearly twofold (85%) increase in therisk of schizophrenia w ithin all psychoses.

Table 2. Severe mental disorders in theChernobyl exclusion zone personnel (accord-ing to psychiatric archives data 1986 -1997 )Mental disorder (ICD-9 code)Alcoholic psychoses (291)Alcoholic delirium (291.0)Alcoholic hallucinosis (291.3)Alcoholic parano id (291.5)Organic nonalcoholic psychosesEpileptiform syndrome (345)Alcoholic epileptiform syndromeSchizophrenia (295)Affective psychoses (296)Reactive psychoses (298)Mental retardation (317)

Number of cases,1986-1997221219

(294.8) 1031

(303,345) 1553554

Among those 53 cases of schizophrenia, 42 (79.2%)onsets of schizophrenia occurred in the Chernobyl EZ,a f te r the Che rnoby l a c c ide n t (Apr i l 26 , 1986) .Schizophrenia onset during 1986-1997 in the personnel isshown in table 1. The incidence of schizophren ia in EZworkers, in comparison with the Ukrainian population, ispresented in figure 1.Figure 1. Incidence of schizophrenia in Chernobyl exclusion zone personnel in comparison w ith thegeneral Ukrainian population

|a.I4

Ukraine

O Exclusion zone

-

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Schizophrenia Bulletin, Vol. 26, No. 4 , 2000 K.N. Loganovsky and T.K. Loganovskaja

Since 1990, there has been a significant increase inschizophrenia in the EZ personnel in comparison with thegeneral population (5.4 per 10,000 in the EZ vs. 1.1 per10,000 in the Ukraine in 1990). The relative risks are 2.4for 1986-1997 and 3.4 for 1990-1997, which indicate thatworking and living in the EZ are associated with morethan a twofold and even a threefold increase in the risk ofschizophrenia developing. Among the 42 patients who fellill after the accident, 34 (80.9%) paranoid and 8 (19.1%)simple forms of schizophrenia were diagnosed. Of the 42patients, there were 33 (78.6%) males and 40 (95.2%) inthe 15-54 years age group; 16 (38%) of these patients hadbeen evacuated between April 28 and May 5, 1986, andlater came back to work at the Chernobyl EZ before theyfell ill with schizophrenia; 31 (73.8%) of them had beentaking part in the cleanup of the Chernobyl accident andits aftermath since 1986-1987 before they became ill withschizophrenia.Psychophysiological Assessment of Irradiated Persons.Neuropsychiatric symptoms in the irradiated persons arepresented in table 3. Characteristic symptoms were seen

at significantly higher rates in the irradiated subjects thanin the veterans with PTSD control group, including oddskin sensations, vertigo, mild neurological signs, auto-nomic nervous system dysfunction, paroxysmal attacks(sometimes epileptiform), cogn itive dysfunction, and, par-ticularly, negative psychopathological symptoms. Somesymptoms, such as emotional lability, anxiety, "flash-backs," and nightmares, were observed at a significantlyhigher rate in the controls. The typical PTSD symptoms(flashbacks, nightmares, etc .) presented only in ARSpatients who had been involved in the accident (techni-cians, construction workers, etc.).The number of neuropsychiatric symptoms was cor-related with the dose of irradiation (table 4). The rate ofparoxysmal attacks and negative symptoms was signifi-cantly higher in overirradiated persons (irradiated by

more than 0.30 Sv or 30 rem, including the ARS patients).Pathopsychological investigations also demonstrated sig-nificant differences in irradiated persons compared withcontrols. The averaged M MPI profile of the irradiated per-sons showed peaks on the hypochondria, schizophrenia,and paranoia scales (figure 2). Some psychopathological

Table 3. Neurop sychiatric symp toms in irradiated persons and controls

SymptomChronic painOdd skin sensationsParesthesiasFatigueVertigoMild neurological signsAutonomic nervoussystem d ysfunctionParoxysmal attacksNightmares"Flashbacks"Emotional labilityAnxietyDepressionHypochondriac ideationParanoiac ideasCognitive dysfunctionNegativepsychopathologicalsymptoms

ARS patients(n = 100), %8698605478449868201852294274218581

Liquidators-volunteers( n = 1 0 0 ) , %9295584673529554142*

78 *464888156862

Veterans withPTSD(n = 50), %7832*423836 *6*

72 *24 *68*52 *84 *90 *44486

24*18*

Veterans withPTSD and closedhead injury (n =50), %8454 *523648 *30863872 *48 *90*84*425810

44 *32 *

Note.ARS = acute radiation sickness; PTSD = post-traumatic stress disorder.* p < 0.001 relative to AR S patients, according to the chi-square test

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Table 4. Neuropsychiatric symptoms in persons irradiated byby moderate or large doses (> 0.3 Sv or 30 rem, including ARS

small doses (< 0.3 Sv or 30 rem) andpatients)

SymptomChronic painOdd skin sensationsParesthesiasFatigueVertigoMild neurological signsAutonomic nervoussystem dysfunctionParoxysmal attacksEmotional labilityAnxietyDepressionHypochondriac ideationParanoiac ideasCognitive dysfunctionNegative symptomsNote.ARS = acute radiation

Smal l (0.3 Sv) doses, rate (%)(n = 146)

127(87)141 (97)90 (62)76 (52)112(77)78 (53)142(97)100(68)90 (62)47 (32)68 (47)117(80)29 (20)119(81)117(80)

Figure 2. MMPI profiles in irradiated persons and controls

T scores

--Irradiated patients, n=200 Afghanistan war veterans with PTSD(n=100)-6 -N or m al controls (n=20)

IHJ 2D 3Hy 4Pd 5Mf 6Pa 7Pt 8Sch 9Ma OS!

Note.MMPI (Minnesota Multiphasic Personality Inventory) Sca les: L = lie, F = trustworthiness, K = correction, 1 Hs = hypochondria, 2D= depression, 3Hy = hysteria, 4Pd = psychopathy, 5Mf = manliness-femininity, 6Pa = paranoia, 7Pt = psychasthenia, 8Sch = schizophre-nia, 9Ma = mania, OSi = social introversion. PTSD = post-traumatic stress disorder.

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indexes were proportional to the dose of irradiation (table5). The social introversion scale of MMPI, emotionalwithdrawal and blunted or inappropriate affect evaluatedaccording to the BPRS, as well as the summarized BPRSscore were significantly higher in the overirradiated per-sons (including the ARS patients).

Correlation analysis showed no relationship betweenthe dose of irradiation and neurotic symptoms (anxiety,depression, somatic concern, tension, aggressivity, healthse lf -es t imation, PTSD). On the other hand, nega t ivesymptoms (blunted or inappropriate affect, emotional andsocial withdrawal, alogia, avolition-apathy, anhedonia),suspiciousness, unusual thought content, as well as thesummarized score of the BPRS were associated with thedose of irradiation (r = 0 .3-0 .5, p < 0.001).Neurophysiological patterns of irradiated persons

were dramati ca l ly di s t ing uish ed ( table 6) . All ARSpatients and 72 percent of the liquidators demonstratedEEG abnormalities. The flat, low-voltage EEG was the

most characteristic. The abnormal EEG activity (spikes,acute waves, spike-waves, slow waves) was significantlylateralized, especially to the left frontotemporal area, inthe overirradiated patients.Compute r iz e d EEG spe c t ra l a na lys i s ( t a b le 7 )revealed a significant increase of 8 and 3 power togetherwith decrease of 9 and a power in irradiated persons.Moreover, 8 and 3 power were significantly lateralizedtoward the left frontotemporal region in all examined irra-diated persons. In the ARS patients, 8 power was signifi-cantly lateralized toward the left temporal area, and apower was depressed in the left parieto-occipital reg ion.SSEP were characterized by topographic abnormalitiesin the left temporoparietal area in irradiated persons (table

7) . Their S SEP were characterized by increased contralaterallatencies and decreased contralateral amplitudes of N^, atthe C 3 on right median nerve stimulation. Moreover, anincreased latency and a decreased amplitude of the late(P300) component were found in irradiated patients.

Table 5. Pathop sycholog ical indexes in persons irradiated by small doses (< 0.3 Sv or 30 rem) andby m oderate or large doses (> 0.3 Sv or 30 rem , including ARS patients)Small (< 0.3 Sv)doses, mean SDScale

MMPITrustworthinessHypochondriaDepressionParanoiaSchizophreniaSocial introversionBPRSSomatic concernAnxietyEmotional withdrawalDepressive moodSuspiciousnessUnusual thought contentBlunted orinappropriate affectSummarized BPRSscore (scales 1-16)SANSAffective flatteningor bluntingAlogiaAvolition-apathyAnhedonia-asocialityAttentionGHQ-28General score

(n = 54 )69.5 9.592.4 10.585.0 12.676.3 12.684.1 17.472.3 8.4

4.1 1.73.0 1.72.2 1.73.6 2.02.1 2.02.2 1.82.1 1.929.6 8.2

2.6 1.82.3 1.62.1 1.53.2 1.62.4 1.8

39.7 11.6

f1.211.022.98-2.36-2.20-4.74

-0.382.11-3.973.20-2.71-2.33-4.93-5.86

-2.36-2.34-2.360.37-1.67

1.40

df

198198198198198198198198198198198198198198

198198198198198198

Pnsnsnsnsns

< 0.001nsns

< 0.001nsnsns< 0.001< 0.001

nsnsnsnsnsns

Moderate and large (>0.3 Sv) doses, mean S D ( n = 146)67.4 11.389.7 18 .278.9 + 13.382.4 17 .391.2 + 21.180.1 10 .9

4.2 1.62.4 1.83.5 2.12.5 2.23.0 2.12.9 1.93.6 1.938.2 9.5

3.2 1.52.9 1.62.7 1.43.1 1.72.9 1.9

36.8 13.4Note.ARS = acute radiation sickness; BPRS = Brief Psychiatric Rating Scale; GHQ = General Health Questionnaire; MMPIMinnesota Multiphasic Personality Inventory; ns = not significant; SANS = Scale for the Assessment of Negative Symptoms; SDstandard deviation.

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Table 6. EEG patterns in irradiated persons and controls

EEG patternNormal

Organized withpredominance ofa activity

AbnormalHypersynchronicFlat polymorphicDisorganized with

predominance ofa activity

Disorganized withpredominance of8 activity

Laterality of abnormalactivityBilateralLeft hemisphereRight hemisphere

ARS patients(n=100)

0

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

16(16)

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

Liquidators-volunteers(n=100)

28 (28)*

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

9(9)

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

Rate (%)Veterans

with PTSD(n = 50)37 (74)*

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

0

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

Veterans withPTSD and

closed headinjury (n = 50)

30 (60)*

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

2(4)

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

Normals(n = 20)

1 6 (8 0 ) *

4 ( 2 0 )0*0

0

3 (1 5 )1 (5 ) *

0Note.ARS = acute radiation sickness; EEG = electroencephalogram; PTSD = post-traumatic stress disorder.* p < 0.001 relative to ARS patients, according to the chi-square testTable 7. Neurophysiological indexes in irradiated persons and controls

IndexARS patients

(n=100)Delta (1-4 Hz) power (%) of EEG in:

Laterality (F3-F4)Paired ftestc3c4Laterality (C3-C4)Paired MestT 3T4Laterality (T3-T4)Paired Hest

49.4 10.346.0 9.52.38 3.67f=6.48, p 3co re CD t o

1 in 1-Q (TJ Cfi> i\ *- C w.o S E

X ) CO C CD.? In03 S UJO "^ Jrt* ro CO X Ic 5 to &m - i nS Q_ Q- W

fflC

S

COoIg

aE ooI?ce >12

1 5

w co colif ltsii^ c ? co

" . CD - ^

UJ

o

if III? s 1 -I iS I -2 g o**- S E S EO "O 05 C X)ut re T - re re

^ rellE o2 eno "iO *Di t T-

o . -II!0 C- cog . s11ro E# 8" 8 "TOl l11

1 Q-O Q.

0)COCD

reQ.OX)XIreQ .

c\TtoCO

CO CO

s iIn NT 3 COO .CO1 8-E Q- seoS "coDC O

_ : "O

O COQ.a>os 0 r?

If 0 H ror-ro 9 1l-sS i

2 -2 "g e g s 1u- w > E

re sisre o>c is0 to1 ^r fl2 s3 a3 totr o

IcI!COi>nQ_>as

cCDaI

eral electroconvulsive therapy (ECT) the post-ECT EEGslow activity is lateralized to the left hemisphere (Green1957; Abrams et al. 1970; Abrams 1988; Deglin 1996).Thus, the left hemisphere seems to be generally more vul-nerable to exogenous factors in right-handed men com-pared with the right hemisphere. A possible explanation ofsuch specific left-hemisphere vulnerability is the increas-ing number of reports showing a relative reduction of cere-bral blood flow in the left hemisphere (Amsterdam andMozley 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 lim-bic dysfunction may be the neurophysiological basis ofschizophrenia-like sym ptoms in overirradiated p ersons.

ConclusionsThe problem of schizophrenia spectrum disorders in indi-viduals exposed to ionizing radiation is under discussion.The data obtained relating an increase of schizophreniaincidence in the Chernobyl EZ personnel support ourhypothesis that ionizing radiation is an environmentaltrigger that can actualize a predisposition to schizophreniaor indeed cause symptomatic schizophrenia. The develop-ment of schizophrenia spectrum disorders in overirradi-ated Chernobyl survivors may be the consequence of theradiation-induced left frontotemporal limbic dysfunction,which m ay be the neurophysiological basis of schizophre-nia-like symptoms in individuals exposed to ionizing radi-ation in doses more than 0.30 Sv or 30 rem, includingARS patients. Thus, those exposed to 0.30 Sv (30 rem) ormore are at higher risk of schizophrenia spectrum disor-ders. Prenatally irradiated children in the Chernobyl acci-dent, especially those exposed at the second trimester ofges ta t ion, a re a t higher r isk for schizophrenia too(Loganovskaja and Loganovsky 1997, 1998; Nyagu et al.19986). An integration of international efforts to discussand organize collaborative studies in this field is of greatimportance for both clinical m edicine and neuroscience.

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Documents

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