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Epidemiologic Reviews Copyright © 1997 by The Johns Hopkins University School of Hygiene and Public Health All rights reserved Vol. 19, No. 2 Printed in U.S.A. Chernobyl, 10 Years After: Health Consequences Denis Bard, Pierre Verger, and Philippe Hubert INTRODUCTION On April 26, 1986, reactor no. 4 at the Chernobyl (Ukraine) nuclear power plant exploded. Over the next 10 days, considerable quantities of radionuclides were discharged into the atmosphere (table 1). The passage of the radioactive cloud over Europe led to varying degrees of contamination according to region (figures 1 and 2); the most contaminated regions were in south- ern Belarus, northern Ukraine, and the Bryansk and Kaluga regions of Russia. The heavier particles (e.g., fuel elements) were deposited less than 100 km from the plant, but the more volatile fission products (such as cesium and iodine) were able to travel great dis- tances (1). The biologic effects of ionizing radiation are fairly well known, especially the carcinogenic potential. These effects are a function of the amount of energy absorbed by tissues per unit time (dose and dose rate). At high doses and high dose rates, above dose thresh- olds that vary for different organs and tissues, ionizing radiation can cause tissue destruction (table 2). Below these thresholds, or at low dose rates, the biologic damage is compatible with cell or tissue survival (causing, for example, DNA mutations or chromo- somal alterations) and can be repaired. The effects of doses below 200 mSv at low dose rates are still little understood (8). The existence of a threshold dose below which there is no effect remains controversial. Humanity, it must be remembered, is continuously exposed to natural radiation at a mean rate, worldwide, of 2.4 mSv/year, or approximately 170 mSv for a mean lifetime of 70 years (7). Received for publication January 16, 1996, and accepted for publication June 12, 1997. Abbreviations: Cl, confidence interval; ECLIS, European Child- hood Leukaemia-Lymphoma Incidence Study; EUROCAT, Euro- pean Registration of Congenital Anomalies; OR, odds ratio; SIR, standardized incidence ratio. From the Institute of Protection and Nuclear Safety (IPSN), Hu- man Health Protection and Dosimetry Department, Risk Assess- ment and Management Division, Laboratory of Epidemiology and Health Detriment Analysis. Reprint requests to Dr. Denis Bard, Laboratory of Epidemiology and Health Detriment Analysis, Institute of Protection and Nuclear Safety, P.O. Box 6, F-92265 Fontenay-aux-Roses, Cedex, France. The accident at Chernobyl resulted in the exposure of a huge number of people to doses and dose rates that varied substantially, creating a new situation for the epidemiology of ionizing radiation. Based on what has been learned so far, the occurrence of thyroid cancer and leukemia was, or is, plausible (10). The effects of stress may result from all types of accidents or catastrophes (11). Finally, various unexpected and ill-defined effects (digestive, respiratory, endocrine) have been mentioned and related to the accident. This presentation reviews reports in the interna- tional scientific literature and discusses the plausibility of these reports in the light of current knowledge about both radiation and postdisaster effects. DOSE UNITS The Gray (Gy) refers to absorbed dose, i.e., the quantity of energy delivered by ionizing radiation per unit mass. One Gy equals 1 Joule/kg. When an indi- vidual is homogeneously and externally exposed, each part of the body receives the same dose; whole-body dose is then an appropriate concept. When exposure is heterogeneous, however, different organs or tissues receive different quantities of energy; in such events, the use of organ dose is more appropriate. The equivalent dose takes into account the biologic potency of different types of radiation (x, gamma, beta, alpha, and neutrons) by applying weighting fac- tors (respectively, 1, 1, 1, 20, and 10). The equivalent dose unit is the Sievert (Sv). The effective dose, also expressed as Sv, results from a calculation that provides a single summary value to be used in different cases of irradiation. It sums and weights the equivalent doses received by tissues and/or organs according to their sensitivity to the effects of ionizing radiation. The weighting factors used in such cases are derived from previous epide- miologic studies of radio-induced cancers. Using the effective dose is more appropriate for radioprotection purposes. For clarity's sake, external or predominantly exter- nal doses are expressed in Gy throughout this presen- tation. Sometimes the reports we reviewed expressed doses in Sv—in such instances, we made the appro- 187 at Francis A Countway Library of Medicine on June 7, 2010 http://epirev.oxfordjournals.org Downloaded from

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Page 1: Chernobyl, 10 Years After: Health Consequenceswilsonweb.physics.harvard.edu/freshman_seminar... · Chernobyl, 10 Years After 189 Cesium-137 ground contamination levels 1 - 5 Ci

Epidemiologic ReviewsCopyright © 1997 by The Johns Hopkins University School of Hygiene and Public HealthAll rights reserved

Vol. 19, No. 2Printed in U.S.A.

Chernobyl, 10 Years After: Health Consequences

Denis Bard, Pierre Verger, and Philippe Hubert

INTRODUCTION

On April 26, 1986, reactor no. 4 at the Chernobyl(Ukraine) nuclear power plant exploded. Over the next10 days, considerable quantities of radionuclides weredischarged into the atmosphere (table 1). The passageof the radioactive cloud over Europe led to varyingdegrees of contamination according to region (figures1 and 2); the most contaminated regions were in south-ern Belarus, northern Ukraine, and the Bryansk andKaluga regions of Russia. The heavier particles (e.g.,fuel elements) were deposited less than 100 km fromthe plant, but the more volatile fission products (suchas cesium and iodine) were able to travel great dis-tances (1).

The biologic effects of ionizing radiation are fairlywell known, especially the carcinogenic potential.These effects are a function of the amount of energyabsorbed by tissues per unit time (dose and dose rate).At high doses and high dose rates, above dose thresh-olds that vary for different organs and tissues, ionizingradiation can cause tissue destruction (table 2). Belowthese thresholds, or at low dose rates, the biologicdamage is compatible with cell or tissue survival(causing, for example, DNA mutations or chromo-somal alterations) and can be repaired. The effects ofdoses below 200 mSv at low dose rates are still littleunderstood (8). The existence of a threshold dosebelow which there is no effect remains controversial.

Humanity, it must be remembered, is continuouslyexposed to natural radiation at a mean rate, worldwide,of 2.4 mSv/year, or approximately 170 mSv for amean lifetime of 70 years (7).

Received for publication January 16, 1996, and accepted forpublication June 12, 1997.

Abbreviations: Cl, confidence interval; ECLIS, European Child-hood Leukaemia-Lymphoma Incidence Study; EUROCAT, Euro-pean Registration of Congenital Anomalies; OR, odds ratio; SIR,standardized incidence ratio.

From the Institute of Protection and Nuclear Safety (IPSN), Hu-man Health Protection and Dosimetry Department, Risk Assess-ment and Management Division, Laboratory of Epidemiology andHealth Detriment Analysis.

Reprint requests to Dr. Denis Bard, Laboratory of Epidemiologyand Health Detriment Analysis, Institute of Protection and NuclearSafety, P.O. Box 6, F-92265 Fontenay-aux-Roses, Cedex, France.

The accident at Chernobyl resulted in the exposureof a huge number of people to doses and dose ratesthat varied substantially, creating a new situation forthe epidemiology of ionizing radiation. Based on whathas been learned so far, the occurrence of thyroidcancer and leukemia was, or is, plausible (10). Theeffects of stress may result from all types of accidentsor catastrophes (11). Finally, various unexpected andill-defined effects (digestive, respiratory, endocrine)have been mentioned and related to the accident.

This presentation reviews reports in the interna-tional scientific literature and discusses the plausibilityof these reports in the light of current knowledge aboutboth radiation and postdisaster effects.

DOSE UNITS

The Gray (Gy) refers to absorbed dose, i.e., thequantity of energy delivered by ionizing radiation perunit mass. One Gy equals 1 Joule/kg. When an indi-vidual is homogeneously and externally exposed, eachpart of the body receives the same dose; whole-bodydose is then an appropriate concept. When exposure isheterogeneous, however, different organs or tissuesreceive different quantities of energy; in such events,the use of organ dose is more appropriate.

The equivalent dose takes into account the biologicpotency of different types of radiation (x, gamma,beta, alpha, and neutrons) by applying weighting fac-tors (respectively, 1, 1, 1, 20, and 10). The equivalentdose unit is the Sievert (Sv).

The effective dose, also expressed as Sv, resultsfrom a calculation that provides a single summaryvalue to be used in different cases of irradiation. Itsums and weights the equivalent doses received bytissues and/or organs according to their sensitivity tothe effects of ionizing radiation. The weighting factorsused in such cases are derived from previous epide-miologic studies of radio-induced cancers. Using theeffective dose is more appropriate for radioprotectionpurposes.

For clarity's sake, external or predominantly exter-nal doses are expressed in Gy throughout this presen-tation. Sometimes the reports we reviewed expresseddoses in Sv—in such instances, we made the appro-

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188 Bard et al.

TABLE 1. Main radionuclide release into the environmentfrom the Chernobyl accident*

Radionuclide

Cesium-134Cesium-137lodine-131lodine-132/tellurium-132lodine-133Strontium-89Strontium-90

Physicalhalf-life

2 years30 years8 days3 days20 hours50 days28 years

Estimates ofreleased activity

MCi

0.5-1.30.8-2.417-4511-4967.5

0.6-2.20.03-0.2

PBq

18.5-4829.6-88.8629-1,665407-1,813

2,497.522.6-81.41.1-7.4

* Based on Khan (2), the International Chernobyl Project (3),and Sich (4).

priate conversions. These conversions do not in anyway change the order of magnitude of the doses inquestion.

EXPOSED POPULATIONS AND THEIR DOSES

The personnel at the Chernobyl plant and the rescueteams present on-site during the first hours after theaccident received external beta and gamma radiationfrom reactor parts, from the plume, and from theradioactive debris and particles deposited on theground. Their extremely high doses ranged, roughly,from 1 to 15 Gy (12, 13). Exposure by inhalation oringestion was relatively very low (1).

The "liquidators," i.e., cleanup workers (numberingabout 600,000), are the personnel who participated inthe decontamination and cleaning on-site, in the 30 kmzone around the site, and in other highly contaminatedareas (14). Very few of these liquidators wereequipped with dosimeters (15). They were irradiatedfor a mean period of 2 months, primarily externally;10 percent of these liquidators received doses esti-mated to exceed 250 mGy, and 30 to 50 percent ofthem received doses ranging between 100 and 250mGy (3, 16). Another estimate concluded that 25,000liquidators received up to 700 mGy of external radia-tion between the accident and the beginning of 1987,and that a half million more who began this work latersustained a mean dose of 100 mGy (17).

The third group is composed of the 115,000 personsevacuated from the 30 km zone around the plant (14).They were irradiated externally and, to a lesser extent,by inhalation. Their average external dose has beenestimated at 140 mGy (calculated from (7)). Otherauthors, however, have estimated the average externaldose received by the 30,000 evacuees of Pripyat,Ukraine, and other towns in the 30 km perimeter at 15mGy (range 0.1-383 mGy) (18).

The fourth group comprises the inhabitants of thecontaminated zones who were continuously subjectedto external and internal irradiation. Among them are

the 270,000 inhabitants of the so-called "strictly con-trolled zones," that is, the zones contaminated by acesium-137 level of at least 0.6 MBq/m2 (15 Ci/km2).Protective measures were and still are applied to theseareas; in particular, restrictions on the consumption ofagricultural products (19).

The less contaminated zones (1-15 Ci/km2) house afifth group of 3,700,000 people who have been sub-jected to less strict protection. The 70-year effectivedoses received by this group are shown in table 3.

The general population of the three republics (Be-larus, the Ukraine, and Russia) surrounding Chernobyl(roughly 280 million people in 1991) live in areaswhere the cesium-137 contamination level was lowerthan 0.04 MBq/m2 (1 Ci/km2). The average effectivedose that they received during the first year is esti-mated to be 0.26 mSv and, lifetime, 0.82 mSv (14).

In western Europe, the cesium-137 contaminationlevels ranged between approximately 1 kBq/m2 (25mCi/km2) and 0.04 MBq/m2 (1 Ci/km2). Contamina-tion in southern Germany, Austria, and northern Italyhas been measured in this upper range (14, 21). Esti-mates of cumulative effective doses over 50 yearsrange from less than 0.03 to 2 mSv (table 4).

These dose estimates actually indicate only ordersof magnitude. They were calculated using data aboutground contamination levels, plausible mean transferfactors, and hypotheses of food consumption patterns.They are thus applicable to groups and do not take intoaccount individual characteristics that may be impor-tant from an epidemiologic point of view (e.g., age atexposure).

Work continues on the reconstitution or measure-ment of the individual doses received by inhabitants ofthe three contiguous republics. Large individual vari-ations will probably be found, as they already havebeen for the thyroid doses received by Kiev (Ukraine)residents (22).

EFFECTS INDUCED (OR LIKELY TO BEINDUCED) BY IONIZING RADIATION

Short-term effects

Acute mortality. Five hundred people were hospi-talized, 237 for acute radiation sickness. This syn-drome caused 28 deaths. Three other deaths werecaused by traumas or burns (23).

Congenital malformations after in utero exposure.In animals, in utero exposure to ionizing radiation hasbeen shown to cause congenital malformations withdose thresholds on the order of 0.1 Gy (24). In hu-mans, developmental anomalies (microcephaly andmental retardation) related to such exposure have beendetected only in children of Hiroshima and Nagasaki

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Chernobyl, 10 Years After 189

Cesium-137 groundcontamination levels

1 - 5 Ci / km. -

5-15 Ci /km -

15-40 Ci /km

> 40 Ci / km.2

FIGURE 1. Cesium-137 ground contamination in the Ukraine, Belarus, and Russia after the accident at Chernobyl (Ukraine).

survivors. The data suggest there is a threshold dosefor mental retardation (0.12 to 0.2 Gy) but not formicrocephaly (25, 26).

Lazjuk et al. (27, 28) conducted a three-part studyon this subject. In the first portion, more than 21,000embryos and fetuses aged 5 to 12 weeks (the productsof legal medical abortions throughout all of Belarusfrom 1980 through 1991) were examined by stereomi-croscope. More than half the abortions took place afterthe accident. Only 56 percent of the embryos andfetuses from the control region (Minsk, Belarus) and

28 percent of those from contaminated zones could beexamined thoroughly. The authors did not statewhether the pathologists were blinded to the zone andtime period from which the samples came. The prev-alence of congenital malformations (all types) washigher for contaminated zones (>0.6 MBq/m2) from1986 to 1991 than for Minsk between 1980 and 1991(8 percent and 4.9 percent, respectively). The periodswere not matched and selection bias cannot be ruledout. Thus, no conclusions can be reached.

The second part of the articles by Lazjuk et al. (27,

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190 Bard et al.

SI PETERSBURG

\

BUDAPEST

April 30/00

FIGURE 2. Trajectory over Europe of radionuclides discharges from the damaged reactor at Chernobyl (Ukraine); emissions at 0 and 12hours, and distance in 12 hours (based on references (5) and (6)).

28) examined the prevalence over time of variousmalformations among live births, using data collectedby the congenital malformation monitoring systemthat began functioning in Belarus in 1979. The authorsconsidered the following malformations: anencephaly,spina bifida, cleft palate and cleft lip, polydactyly,phocomelia, esophageal atresia, anal atresia, Downsyndrome, and multiple malformations. The preva-lence of congenital malformations (all types) increasedsignificantly after the accident, in both contaminatedand noncontaminated zones, suggesting the influenceof a detection bias.

Finally, a geographic correlation analysis, carriedout at a district level and only in contaminated zones,observed no correlation between the indicators ofmean exposure per inhabitant and the observed prev-alence of congenital malformations.

Kulakov et al. (29) conducted a cross-sectionalstudy of 688 pregnant women and their offspring andalso retrospectively analyzed the hospital records of7,000 pregnancies (1982-1990). Subjects lived in twodistricts, one in the region of Gomel (Belarus), the

other in Kiev. They had similar socioeconomic char-acteristics but different levels of contamination. Theprevalence of congenital malformations (congenitalheart disease, esophageal atresia, anencephaly, hydro-cephaly, multiple malformations) increased twice asmuch in the more contaminated zone. The article con-tains few details about the methods underlying theseobservations (e.g., neither maternal age distributionnor the methods for selecting subjects or ascertainingcongenital malformations are described). There areobvious errors in contamination units (kCi instead ofCi?), and it is difficult to know exactly how contam-inated these zones were.

Overall, since cumulative in utero doses over theentire pregnancy did not exceed 100 mSv for any ofthe exposed women (27), it is unlikely that even aproperly designed epidemiologic study could showany excess risk for congenital malformations attribut-able to ionizing radiation alone. No study of the pop-ulations affected by Chernobyl that we know of mea-sures their folate levels, although these are known toinfluence the occurrence of neural tube defects (30).

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TABLE 2. Effects of ionizing radiation observed at variousdose levels (high dose rates)*

Dose level(organ)t

Observed effect

3-5 Gy Dose at which half the individuals would beexpected to die within 60 days

5 Gy (eyes) Cataract with impaired vision>0.5 Gy Depression of hematopoiesis0.2 Gy Significant increase of leukemias and solid

tumors (incidence and mortality)^0.1 Gy (thyroid) Significant increase of thyroid cancers§

* Based on Sources, Effects, and Risks of Ionising Radiation(7,8) and the International Commission on Radiological Protection(8)-

t If not specified, whole body.t In Hiroshima and Nagasaki survivors.§ After external irradiation of children for medical purposes.

The lifestyle of the populations directly touched by theaccident changed, however, and their subjection tofood restrictions may have modified their vitaminintake.

Mental retardation. Kozlova et al. (31) studied2,189 children from contaminated zones (15 to over 40Ci/km2) in the three countries; they had been irradiatedin utero at different periods of gestation. The referencegroup comprised 2,021 children from zones with lessthan 1 Ci/km2 of contamination who were matched forage, socioeconomic level, and parents' educationallevel. They observed reduced intellectual performance(on psychometric tests) in the exposed group. Theseresults are descriptive and do not take into account theparents' psychologic condition, even though this samestudy also finds a higher prevalence of psychologicdisorders among exposed parents.

Case clusters in Europe and Asia Minor

Down syndrome. Clusters of Down syndromecases have been reported in several different Europeancountries after the accident at Chernobyl: in WestBerlin, 12 cases were observed 9 months after theaccident, while only 2-3 were expected (32). An ab-normally high prevalence was also noted in the region

TABLE 3. Estimated effective doses (mSv) over 70 years forthe population in the contaminated zones

Type ofexposure

Strictly controlledzones (3)

InternationalAtomicEnergyAgency

"Official"*

Othercontaminated

zones (20)

External irradiation 60-130 80-160 40Internal irradiation 20-30 60-240 30-180Total irradiation 80-160 150-400 70-220

* First estimates of experts from the former USSR.

TABLE 4. Estimates of the cummulative effective doses over50 years after the Chernobyl accident in various westernEuropean countries*

CountriesEffective dose

equivalent(mSv)

Austria and FinlandGreece, Norway, and SwedenGermany, Italy, and SwitzerlandIrelandBelgium, Denmark, France, Luxembourg,

the Netherlands, and TurkeyUnited KingdomPortugal and Spain

1-20.5-1

0.25-0.50.12-0.250.06-0.12

0.03-O.06<0.03

Based on Bengtsson (21).

of Lothian, Scotland (33). EUROCAT (European Reg-istration of Congenital Anomalies), a network of re-gional registers monitoring congenital malformations,was called upon to assess the significance of theseclusters. In 1991, EUROCAT included 24 registersin 14 European countries, covering approximately350,000 births a year (about 10 percent of the births inthese countries). Its comparison of the incidence ofDown syndrome before and after the accident at Cher-nobyl revealed no significant differences between thetwo periods (34).

The apparent clusters that have been reported mayresult from different biases (e.g., improved screeningand awareness, selection) (35). It is also highly prob-able that the medical teams studying the consequencesof Chernobyl would observe some isolated clusters,and that they would be published more frequently thannegative results (34).

Neural tube defects. The prevalence of neural tubedefects apparently increased in some regions of Tur-key in the months after the accident (36-39), althoughit did not rise in other areas in the country (40, 41).The first-year average effective dose for the Turkishpopulation is estimated to be 190 JLASV (14). Comparedwith the estimated yearly dose of about 2 mSv fromnatural background radiation, this incremental doseappears trivial, and the purported effect implausible.The chronologic differences in their occurrence indifferent parts of Turkey suggest that these observa-tions result from screening or selection biases.

Another EUROCAT study considered developmentalanomalies of the central nervous system and the eyes. Itanalyzed the registers and found that the prevalence rateamong the cohort exposed in utero during the first 5months after Chernobyl did not differ from the expectedrate based on the period 1980-1985, nor was any relationto exposure detected. Nonetheless, during the individualregister analyses, a significant increase in neural tubedefects was observed for Odense, Denmark (four casesobserved versus 0.9 expected) (34).

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Data from congenital malformation registers in Fin-land, Norway, and Sweden did not reveal an increasein the prevalence of malformations in the regions mostexposed to the Chernobyl radioactive fallout (42-44).

Because in utero doses in the western Europeancountries were evaluated at a maximum of 1.5 mSv(35), the detection of an excess of congenital malfor-mations secondary to the accident at Chernobyl ishighly improbable, even in the absence of a thresholddose. Obviously, it becomes progressively more im-probable at current exposure levels. The issue ofcongenital malformations is discussed in detail byLittle (45).

Spontaneous abortions and miscarriages. No sig-nificant excess of untoward pregnancy outcomes hasbeen observed in the descendants of Hiroshima andNagasaki survivors (mean gonadal dose 0.3-0.6 Gy)(46). A synthesis of the data supplied by the govern-ments of the three contiguous republics on this subject(3) provides no details about the methods used anddoes not allow a conclusion to be drawn on this point.In Norway, Irgens et al. (47) reported a statisticallysignificant 1 percent increase in spontaneous abortionrates in the 12 months after, compared with the 12months before, the accident; it was most marked dur-ing the second and third trimesters after the explosion.They provide little detail about their methods. A studyin Styria (Austria) (48), where greater environmentalcontamination occurred and whose population re-ceived higher doses (14), found no such increase.

Genetic damage. Ionizing radiation can damagegenetic material of both somatic and germline cells(24, 49). Cytogenetic studies in blood cells (findingand counting such chromosomal aberrations asdicentrics, acentric fragments, and chromatid rings andaberrations) have been performed on small groups inthe neighboring republics, yielding conflicting results(3, 50-54). All of these studies are marred bymethodological weaknesses (e.g., too few subjects,geographically-based comparisons, absence of controlgroups and of dose estimates). These problems make itdifficult to draw any conclusions.

Geographic studies in western Europe have alsoproduced contradictory results (55-57). No clear linkappears to associate the excess of chromosomal anom-alies with the doses received by inhabitants, estimatedgeographically on the basis of fallout measurements.

The possibility that germline mutations may bepassed on to offspring is suggested by observationsamong 64 children of atomic bomb survivors (58).

Following the accident at Chernobyl, a relation be-tween the mutation rate of minisatellites of humanlymphocyte chromosomes and exposure to radioactivecontamination was observed in an ecologic study (59).

The reference population, from the United Kingdom,probably differed from the Belarussian population forgenetic and environmental risk factors for mutations.The two groups do not appear to have been matchedfor age, although the risk of mutation probably in-creases with age, as it does for stable chromosomalaberrations (60). The unavailability of adequately de-tailed information about the study subjects means thatthis hypothesis cannot be ruled out.

Immunologic effects. Lymphocyte disorders last-ing many years have been noted among patients irra-diated by high doses (typically above 1 Gy) in somestudies (14, 61), but these results have not been repro-duced in other studies (62). In a group of workersoccupationally exposed to very low doses (around 10mSv) in Austria (63), some changes in the lympho-cytic subsets were the opposite of previous results.This study suffers from several methodological weak-nesses (cross-sectional study, too few subjects, nocontrol for such confounding factors as immunity sta-tus or age before exposure, no statistical analysis).

A cross-sectional study after Chernobyl discernedno difference in the immunologic status of residents ofcontaminated zones and those living in control zones(3, 15). It involved 1,356 subjects from five age brack-ets (children born in 1988, 1985, and 1980 and adultsborn in 1950 and 1930) nonrandomly selected in con-taminated (>5 Ci/km2) and uncontaminated villages.In 1991, the comparison of 71 healthy subjects with 30liquidators close in age whose external exposure hadvaried between 0.1 and 0.5 Gy showed reduced CD8+lymphocytes in the exposed subjects, results fairlyconsistent with those previously reported (64). Thearticle furnishes few details about its sampling tech-nique, however, and the sex ratio differed between thetwo groups. These drawbacks raise questions about thereliability of the results. A clinical study of children 10to 15 years of age (34 from a zone contaminated by 16Ci/km2, and 30 from a zone with less than 1 Ci/km2)showed no significant correlation between cesium-137physical activity and natural killer-cell activity (65).Immunologic studies of Hiroshima and Nagasaki sur-vivors have shown no change in natural killer-cellactivity (61).

Medium and long-term effects

Lens changes. Posterior capsular lens changeswere observed among Hiroshima and Nagasaki survi-vors with a threshold dose estimated at 200 mGy (3).The prevalence of lens changes was studied amongUkrainian children between the ages of 5 and 17 years,in part randomly selected. The control children wererandomly selected, came from an uncontaminatedzone, and were matched by age and sex. In all, 996

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subjects representing 35-40 percent of the eligiblechildren in the high exposure zone were included, with791 controls. The exposed group showed a slight butsignificant excess (p < 0.001) of subclinical posteriorsubcapsular lens changes (66). Nonetheless, the exter-nal mean cumulative doses (estimated between 29 and85 mGy, depending on the dose reconstructionmethod) received by the exposed group were belowthose generally considered the threshold for such ef-fects (3). Information about the beta radiation dosesrelated to exposure to contaminated dust is apparentlynot available. The authors concede that bias couldexplain their results (e.g., the investigators knew thechildren's exposure status) (66).

Cardiovascular disease. Studies among Hiroshimaand Nagasaki survivors who were exposed to at least2 Gy have reported a relation between external irradi-ation and various factors (arterial calcification, coag-ulation impairment, hypertension) that contribute toarteriosclerosis and, thus, to coronary disease. No ev-idence of myocardial infarction risk was seen below 1Gy (67, 68). Nonetheless, Darby et al. did not observean excess risk of cardiovascular disease among pa-tients with ankylosing spondylitis treated with x-rays(69). A causal association remains to be demonstratedbetween cardiovascular risk and exposure to relativelyprolonged low-dose radiation.

In a short statement, Russian doctors (3) have re-ported an increase in cardiovascular diseases amongthe exposed population. Despite the lack of method-ological detail, these results may be connected to thefindings in Hiroshima and Nagasaki survivors. Thecardiovascular impact of stress should probably alsobe taken into account.

Benign thyroid disorders. Studies of atomic bombsurvivors (70) and persons exposed to the fallout fromnuclear testing (71, 72) suggest that ionizing radiationmay affect the risk of benign thyroid nodules. Transitoryfunctional thyroid disorders (levels of circulating T3 andT4 hormones, antithyroglobulin or antimicrosomal frac-tion antibodies) have been reported in the Ukraine (73)and in Russia (74). Among children examined in Russia,the prevalence of goiter varies substantially from onedistrict to another (5-25 percent of children examined)(74). Unfortunately, the procedures for selecting the sub-jects are not detailed in these studies. The intensity of thescreening may not be entirely independent of the degreeof ground contamination. Moreover, the endemic char-acter of iodine deficiency, a risk factor for goiter, hasbeen confirmed in the regions affected by the accident atChernobyl (75).

.Other effects. Since the accident, doctors from theCommunity of Independent States have reported ob-serving an abnormally frequent rate of a series of

disease symptoms (e.g., endocrine, digestive, neuro-logic, respiratory, etc.) among the exposed populations(3). It is thus appropriate to discuss these problems aspossible effects of ionizing radiation, although epide-miologic verification is required.

Pregnancy disorders. The study by Kulakov et al.,discussed above, concludes that miscellaneous preg-nancy disorders not specifically related to the repro-ductive system (anemia, renal disorders, transient hy-pertension, abnormalities of fat metabolism) haveincreased from 23.1 to 33.9 percent in the most con-taminated district they studied, and from 7.1 to 51.2percent in the less contaminated zone (29). Since theannual migration rate is evaluated at less than 3 per-cent, the increase is probably not due to a change inthe population structure. The two districts differed bya factor of three in their prevalence of these disordersbefore the accident, suggesting that the attention paidto these problems varied between the two zones andthat more intensive screening since the accident mayexplain these increases. The authors also reported anincreased incidence of toxemia and complications oflabor in both districts. The very brief description ofmethods makes it impossible to draw a conclusionabout the reality of these results, especially since, tothe best of our knowledge, similar facts have neverbeen reported in connection with exposure to ionizingradiation.

Changes in neonatal health. The same study (29)also reports that neonatal morbidity increased in theperiod 1986-1990, compared with the levels of 1983-1985, by three times in the more contaminated districtand by two times the in the less contaminated district.For specific problems, however, such as hemorrhagesin newborns (incidence multiplied by nine after theaccident), the increase was not greater in the morecontaminated district. Another study (3) concludedthat perinatal mortality had declined since the acci-dent, perhaps because of improvements in the qualityof care. Other reports do not suggest any excess ofpathologic symptoms, with the possible exception ofpostnatal respiratory distress, among newborns in theUkraine strictly controlled zones in the first post-accident year. Nonetheless, these reports are declara-tions rather than epidemiologic studies presented in ascientific format (76).

In the southern regions of West Germany, that is,those most contaminated by the fallout from Cher-nobyl, a marked change towards excess infant mortal-ity was observed from the previous rate, beginning inMay 1986 (77). A causal relation with the accidentremains to be shown. In Sweden, a significant increasein the number of infants with birth weights below1,500 g (odds ratio (OR) = 1.37, 95 percent confi-

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dence interval (CI) 1.03-1.73) and in perinatal mor-tality (OR = 1.50, 95 percent CI 1.12-2.0) was ob-served in June and July of 1986, after adjustment formaternal age and parity (44).

On the whole, the reports published so far do notshow any clear trend related to population exposure.

Vegetative dystonia. A syndrome called "vegetativedystonia" is said to be very frequent among Ukrainianchildren. Its symptoms include fatigue, pallor, inatten-tion, abdominal pain, headaches, and poor school per-formance. Clinical examination and complementarytests that are not practiced in Western countries, suchas whole-body thermography, are said to allow theclinical form of vegetative dystonia to be diagnosed(78). The author points out the resemblance of thissyndrome to "chronic fatigue syndrome," which isalso the subject of much debate and skepticism.

The appositeness of grouping these symptoms to-gether in a separate syndrome remains problematic aslong as serious clinical epidemiology studies have notbeen performed. It is no less true, however, that itseffect on public health may be substantial, even if itsextent is difficult to assess.

Cancer

Thyroid cancer. Thyroid cancer is rare among chil-dren younger than 15 years. The incidence in the Westis 0.1 to 0.3 cases per 100,000 annually (79, 80),similar to that in Belarus between 1986 and 1988 (81).In the Ukraine, the incidence between 1981 and 1988was lower (0.04-0.07 per 100,000). The incidence isapproximately three times greater among girls thanamong boys (82). The great majority of differentiatedthyroid cancers are of two morphologic types, papil-lary and follicular (83).

Thyroid cancer and ionizing radiation. Exposure toacute external radiation is a well-documented riskfactor for this disease in children and adolescents (84).Populations in whom this risk has been observed in-clude Hiroshima and Nagasaki survivors as well asadolescents and children who underwent irradiation ofthe head or neck for therapeutic purposes. A jointanalysis of seven cohorts has shown that the humanthyroid is a very radiosensitive organ. A significantexcess risk (at or above 100 mGy) has been estab-lished for external thyroid doses (85). The risk ofthyroid cancer is highest for those who were youngestat exposure. In most studies, the increased incidencebecomes clear between 10 and 15 years after exposure.Several studies have pointed out more moderate in-creases between 3 and 7 years after exposure (84). Onthe other hand, no increased risk of cancer has beenobserved after internal thyroid irradiation by iodine-131 alone (treatment for hyperthyroidism and diagnos-

tic use) among adults (86), or among children andadolescents (84). Nonetheless the information aboutchildren younger than 15 years is limited. The carci-nogenicity of iodine-131 has been shown in animals,particularly among rats and mice (87, 88). Some ex-perimental studies suggest that malignant thyroid tu-mors can be induced four to 10 times less effectivelywith iodine-131 than with x-rays, although anotherstudy could not replicate this result (89). Studies of theinhabitants of the Marshall Islands, who were exposedto fallout from nuclear tests on the Pacific atoll ofBikini in 1954 have shown a significant excess risk ofthyroid cancer in children and adolescents. They wereexposed to high doses (mean, 12.4 Gy) of short-livediodine isotopes (iodine-132, iodine-133, and iodine-135). Iodine-131 and external gamma radiation eachrepresented 10 percent or less of the exposure (84).

Thyroid doses due to Chernobyl in the three repub-lics. The iodine family represents a significant portionof the emissions from the Chernobyl reactor (see table1). Stable iodine taken prophylactically saturates thethyroid gland, preventing radioactive iodine from con-centrating there. After the accident at Chernobyl, sta-ble iodine appears to have been administered in a verylimited fashion (90). The half-lives of radionuclidesfrom the iodine family (see table 1) are such that 99percent of them have decayed and disappeared fromthe environment after 54 days.

The estimations of the thyroid doses received byexposed populations are based partly on thyroid spec-trometric measurements of approximately 400,000people performed in the three countries in the weeksafter the accident (22, 79, 91-93). These measure-ments, involving only iodine-131 and not short-livediodine isotopes, were not taken in a standardized way(93). Estimations of individual thyroid doses in agiven territory vary by up to four orders of magnitude(22, 79, 91). In addition, they are two to 10 timeshigher in children than in adults living in areas ofequivalent contamination (22, 79, 91-93). This is be-cause children have a smaller thyroid mass and greateriodine uptake; therefore, the thyroid dose is higher inchildren than in adults after the incorporation of thesame quantity of radioactive iodine (14). Children arealso likely to consume relatively more milk, whichwas in most cases the principal exposure pathway foriodine-131.

In the Ukraine, among inhabitants evacuated fromthe town of Pripyat, the average individual thyroiddose is estimated as 2.8 Gy for those aged 0 to 7 yearsat the time of the accident, and as 0.4 Gy for other agegroups (93) (figure 3). Estimations for the populationof Kiev are lower (22).

In Belarus, in the most contaminated zones, the

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average individual thyroid dose is estimated at 0.1 to0.3 Gy for the population as a whole and at 0.4 to 0.7Gy for children aged less than 8 years at the time of thecatastrophe (19) (figure 3).

In Russia, in the region of Bryansk in the zonescontaminated by more than 0.6 MBq/m2, the averagethyroid dose, depending on the district, is estimated atbetween 0.07 and 2 Gy for children younger than 7years and between 0.014 and 0.05 Gy among adults(74). For the region of Kaluga, 25 percent of thechildren and adolescents are thought to have receivedthyroid doses between 0.03 and 2 Gy, while approxi-mately 2 percent are thought to have received morethan 2 Gy (74).

Incidence of childhood thyroid cancer in Belarus,the Ukraine, and Russia. The incidence of thyroidcancers among children aged less than 15 years (at thetime of diagnosis) began rising in Belarus in 1990 andcontinued to do so through 1994 (figure 4) (81, 9 4 -96). Half of the registered cases came from the espe-cially contaminated Gomel region. In the Ukraine, anincrease in incidence, evident from 1990 onward, hasbeen reported among children less than 15 years andamong adolescents (15-18 years); more than half thecases came from the five regions most exposed tofallout from the accident (73, 96, 97). Lastly, an in-crease among children under 15 years of age wasreported later in Russia for the regions of Bryansk and

Kaluga (74, 98). The majority of cases came from theregion of Bryansk, and the increase was first detectedonly in 1992.

Between the period 1981-1985 and the period1990-1994, the incidence of childhood thyroid cancerwas multiplied by 100 throughout Belarus as a whole(by 200 for Gomel alone), by seven for the Ukraine asa whole (by more than 100 for the five most contam-inated zones of the Ukraine), and, finally, by eight forthe period 1986-1991 for the Russian regions of Bry-ansk and Kaluga (96).

In absolute terms, these figures represent 300 newcases of thyroid cancer among children younger than15 years in Belarus, more than 200 in the Ukraine, andmore than 20 in the Russian region of Bryansk (98).Furthermore, in the Ukraine, roughly 100 new caseswere observed among adolescents (15-18 years) be-tween 1986 and 1993 (73).

The characteristics of the cancers observed in Bela-rus (79, 82, 98-101) and in the Ukraine (102) amongchildren younger than 15 years (80 to 120 cases ex-amined, according to the series) have been analyzed indetail. The diagnosis of thyroid cancer was confirmedin more than 90 percent of the cases. These cancerswere primarily papillary (96.5 percent from a series of93 cases diagnosed in Belarus between 1986 and1991) (99), and two thirds of them were little ormoderately differentiated. In the above-mentioned se-

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FIGURE 3. Thyroid dose distribution among children with thyroid measurements after the Chernobyl (Ukraine) accident (A. Bouville, USNational Cancer Institute, personal communication).

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196 Bardetal.

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FIGURE 4. Trend of incidence of childhood thyroid cancer in Belarus, Ukraine, and Russia, 1986-1993 (based on references (73), (96), and(97)).

ries, extra-thyroid extension was noted in 60.5 percentof the cases, regional lymphatic metastases in 74 per-cent, and distant metastases in 7 percent. The tumorsize at diagnosis exceeded 1 cm in 88 percent of thecases from a series of 84 diagnosed in Belarus in 1991and 1992 (100). Similar findings have been made inthe other series (99). In the 1986-1991 series, thefemale-male ratio was approximately 1.3:1; the meanage at diagnosis, 9 years; and the mean age at the timeof the accident, 4.6 years (99, 100). What all thestudies taken together show is that the younger the ageat exposure, the greater the risk and the more likely itis to manifest itself at a younger age (79, 103).

Thyroid cancer among adults in the general popu-lation. In Belarus, which has had a cancer registrysince 1978, the incidence of thyroid cancer amongadults has apparently increased from 2.2 per 100,000in 1986 to 6.5 per 100,000 in 1993 (81). These datahave not been validated.

Discussion. The first published reports that thyroidcancer was increasing among children were greetedskeptically for a variety of reasons (104-106). Threequestions must be asked: 1) Is the increased incidencereal? 2) If so, is it attributable to the accident? and 3)If so, what are the reasons for it?

Several analysts have suggested that this increasemay actually be due to the increased detection ofoccult thyroid carcinomas (tumors only a few milli-meters in diameter, asymptomatic, and slow-growing).Their prevalence among adults at autopsy ranges be-tween 2.7 and 35.6 percent, according to the series andcountry (107). A high prevalence (9 percent) has alsobeen observed in a nonrandom sample of 215 Bela-russian adults aged 19 to 88 years who died in 1990and 1991 (108). There is little documentation of theprevalence of this form of thyroid cancer among chil-

dren younger than 15 years of age (109, 110). Thesetting-up of screening programs, especially those us-ing ultrasonography, could have contributed to reveal-ing tumors of this type that existed before the accidentand which would not otherwise have been detected. Inchildren, the extent of the increase makes it clear thatit is not simply the result of increased medical atten-tion, or of more effective diagnostic methods, or both.Furthermore, the tumors observed are mainly invasiveand fast-growing (111). It is now generally agreed thatthe increase in thyroid cancers observed among chil-dren and adolescents in the zones exposed to Cher-nobyl fallout is real (87, 111-113). Conversely, theincrease observed among Belarussian adults is morelikely to result from more intensive screening becauseof a relatively high prevalence of occult carcinomas inadults. Cancers may have appeared (or may still ap-pear) in adulthood for the cohort of children exposedin 1986, however.

The role the accident plays in the epidemic of child-hood thyroid cancers has also been debated, partlybecause this increase occurred earlier than expected(106) and partly because the carcinogenicity of iodine-131 has not been established in humans. Three prin-cipal points support the attribution of responsibility toChernobyl's radioactive fallout. The first is, in fact,the distribution over time of the epidemic, the in-creased risk having been observed among childrenborn before the catastrophe or exposed in utero and notin those born later. The relatively brief time lag be-tween exposure and the increase in incidence is com-patible with the available data (84). The second pointis the geographic distribution, the highest incidencerates having been found in the zones most contami-nated by iodine-131 (the region of Gomel in southernBelarus and parts of northern Ukraine) (97, 100),

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while they have increased little or not at all in lesscontaminated zones (Vitebsk, Belarus, for example)(100). A geographic correlation study in the five mostcontaminated regions of the Ukraine shows a statisti-cally significant association between the mean dosesof iodine-131, estimated at the district level ("raion")on the basis of direct thyroid spectrometric measure-ments and the age-adjusted incidence of thyroid cancerbetween 1990 and 1994, for subjects aged between 0and 18 years of age at the moment of the accident(103). Finally, a dose-response relation (individualthyroid dose) has been observed in a yet-unpublishedstudy (cited by Beebe (114) and A. Bouville, USNational Cancer Institute, personal communication,1995) of Belarussian children aged less than 15 yearsin 1986 (119 cases and 238 controls).

The respective roles of radioactive agents (externalgamma irradiation, internal irradiation by iodine-131and short-lived iodine isotopes) have not been estab-lished, even if it seems probable that iodine-131, theprincipal component of the thyroid dose after Cher-nobyl, is important. The dose rate of the short-livedisotopes is high because of their short half-lives; theirrole was probably greatest in the zones contaminatedimmediately after the initial radioactivity release(113). In children born more than a few months afterthe accident, the number of cases drops steeply, sug-gesting that the causative agent did not persist at highlevels in the environment. Williams et al. (102) con-sider that this fact points strongly to radioactive iodineas the major or even sole cause of this epidemic. Otherrisk factors may also be important. Iodine deficiency,endemic in the region (75), is believed to be a riskfactor for thyroid cancer (113, 115), although mainlyfor follicular cancers (83). Experimental animal stud-ies have shown that an iodine-deficient diet promotescancer by its stimulation of thyroid-stimulating hor-mone secretion and the resulting cell proliferation(88). They have also demonstrated that combined ex-posure to iodine-131 or x-rays and a promoting agentshortens the latency period of this cancer (88).

Both the tumors and the Belarussian children af-flicted by them appear to have different characteristicsthan those associated with spontaneous tumors (seriesobserved in the United Kingdom); the former includea higher percentage of papillary tumors and, amongthem, more follicular-solid tumors. The children alsohave a higher proportion of invasive tumors, a youngermean age at diagnosis, and a lower female-male sexratio (82, 99). The comparison of these series mustnonetheless remain tentative, especially in view of thedifferences in selection and screening. On-going stud-ies seek to confirm these data and are searching forpossible markers indicating the origin of the post-

Chernobyl tumors.Quantifying the excess risk associated with different

modes of exposure, testing the effect of screening, andexamining the role of other possible risk factors allrequire analytic epidemiologic studies (case-controland cohort). These are now underway, as is the recon-struction of individual thyroid doses. Nonetheless, ob-taining precise estimates of individual thyroid doseswill be difficult since satisfactory individual spectro-metric measurements were not taken during the expo-sure period (79, 113).

Finally, in the likely hypothesis that this epidemic isradio-induced, we must expect its cumulative preva-lence to increase over the next 50 years, like theepidemic already seen among the children treated byexternal radiotherapy for an enlarged thymus (116).

Leukemia. Because of the doses they received, theevacuated populations and liquidators are likely to beaffected by an excess number of leukemia cases (117).Demonstrating this excess, on the other hand, is prob-lematic; it might be difficult to attain sufficient statis-tical power. That is, even under the most pessimisticestimates of the dose-response relation (117) and doseestimates in the evacuees, we can expect to see ap-proximately 10 additional cases per year for the period1991-1996. This would represent a threefold increaseover the "spontaneous" annual incidence in the region,which is roughly 5 per 100,000 per year (80). Athorough follow-up of these 115,000 people is re-quired to observe these cases, but does not seem tohave been arranged. Ivanov et al. (118) have examinedthe data from the Belarus Childhood Leukemia Reg-ister from 1982 through 1994 and observed no in-crease in the incidence of childhood leukemia casesafter the accident, not even in the most contaminatedzones, even though case registration probably im-proved from then on. In the most contaminated regionsof the Ukraine and in the 12 regions of the threerepublics contiguous to Chernobyl, the incidence ofleukemia among all age groups shows no significantincrease from the trend observed before the accident(119, 120). These data come from an active search forcases, but its practical details are described verysketchily. Moreover, leukemias and lymphomas arecombined in the trend analysis, even though no asso-ciation has been established between lymphoma andionizing radiation (8). Finally, the size of the popula-tions living in the contaminated zones of the Ukraineis fairly low, making it difficult to demonstrate a weakeffect. These descriptive studies are too briefly de-scribed and do not allow any definitive conclusion thatthere is no excess of leukemia.

The European Childhood Leukaemia-LymphomaIncidence Study (ECLIS) examined data from 36 can-

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cer registries in 23 European countries, subdividedinto 35 regions by dose level. It collected 23,756 casesof childhood leukemia between 1980 and 1991, for655 million person-years of observation, and con-cluded that the incidence after the catastrophe has notbeen influenced by exposure to fallout (121). Dosesfrom natural irradiation vary in the regions of Europe,we should note (7), and the amplitude of that variationis close to that of the doses due to Chernobyl every-where except in Belarus, where the doses were high-est. Finding evidence of an effect from the Chernobylaccident in these regions was, thus, improbable. Twoother studies of childhood leukemia, in Sweden (122)and Finland (123), also failed to show an associationwith fallout. The follow-up time has, of course, beenshort, but the result is consistent with the knowneffects of radiation (14).

Other cancers. Ionizing radiation exposure and theoccurrence of cancers in other organs are known to berelated. Nonetheless, the expected excess relative risksare markedly lower than for leukemia and thyroidcancer. The latency period is longer (10). Thus, dem-onstrating an excess risk is problematic. It is hardlysurprising that studies conducted among the popula-tion of the most contaminated zones of the three re-publics have thus far yielded negative results (120).

Other cancers in Europe. Under the hypothesisthat no threshold level of ionizing radiation is re-quired, the doses received in Europe, outside the statesof the former USSR, are or will be responsible forsome cases of cancer, in particular, leukemia andthyroid cancer. It is theoretically possible to calculatethe number by using estimates of the doses differentEuropean populations received. Nonetheless, the ad-ditional expected cases are very few and, thus, impos-sible to verify epidemiologically. One exception, how-ever, is southern Bavaria (Germany) where the dosesreceived may cause an estimated 15 percent excessnumber of childhood cancers (35), which is at the limitof sensitivity of epidemiologic methods. Elsewhere,calculation of the lifetime external dose depends onprecise knowledge of local doses.

Cancer in the liquidators. Using data from the Reg-istry of Russian Liquidators (annual medical examina-tion), Ivanov et al. (124) observed a significant trendtowards increased cancer incidence and mortality (allcancers together) according to external dose. The anal-ysis concerned 1,026 cases of cancers in a cohort of143,000 liquidators, 114,000 of whom had a docu-mented dosimetry (number of person-years not speci-fied). The authors calculated the relative risk using asthe reference the group whose dose was between 0 and50 mGy. A significantly higher relative risk was seenat exposure over 100 mGy, but the dose-effect relation

is both unclear and untested. The authors do not seemto have taken age into account in calculating the rel-ative risk. These data must be interpreted cautiously,however, for the low level of confirmation of cancersin this registry has been pointed out (125). In Belarus,a similar register contains data for 45,000 liquidators(155 cancer cases for the period 1993-1994) (126).The standardized incidence ratios (SIR) were calcu-lated using the population of Belarus as the reference.The incidence of bladder cancer increased signifi-cantly among men (SIR = 219, 95 percent CI 123-361) while that of thyroid cancer was significantlyhigher among women (SIR = 376, 95 percent CI122-878). Male liquidators who had worked at least 1month in the 30 km zone around Chernobyl have a riskof thyroid cancer significantly higher than that of thereference population (SIR = 625, 95 percent CI 129-1,826) as well as a greater risk of leukemia, the his-tologic types of which have not been specified (SIR =342, 95 percent CI 126-746). These results, however,are based on a relatively small number of cases and onactive follow-up of the liquidators, while cancer reg-istration in the reference population is passive. Theincidence of cancer in the reference population may beunderestimated. In particular, more intensive screen-ing may explain the reported excess of thyroid cancersand leukemia.

INDIRECT EFFECTS

The effects that we call "indirect" here are those thatmay be causally linked to the catastrophe withouthaving a direct relation to the action of ionizing radi-ation.

Psychologic impact

It is now generally agreed that disasters have seriousnegative consequences to the mental health of affectedpopulations. Their victims can suffer both short- andlong-term psychologic consequences, but individualreactions to these events are extremely variable (11,127). The consequences to psychologic health are oneof the primary public health problems arising from theaccident at Chernobyl (98).

The International Chernobyl Project study describedabove (3, 15) also examined this subject in 1990. Anonstandardized checklist (11) was used to ask aboutsleep problems, various subjective complaints, andalcohol consumption. The high-stress levels shown byresidents of the contaminated and control zones didnot differ particularly.

In 1993, Viinamaki et al. (128) conducted a cross-sectional study in the region of Bryansk (Russia); 325subjects lived in a contaminated village (> 1,300 kBq/

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m2) and 278 lived in a control village (<37 Bq/m2).The survey evaluated the psychologic state of subjectsolder than 14 years with a version of the GeneralHealth Questionnaire. It allows the calculation of ascore between 0 and 12 and covers anxiety, depres-sion, self-esteem, and day-to-day difficulties. In bothgroups, the participation rate was approximately 70percent. Some sociodemographic features differed be-tween the two groups. They were not taken into ac-count in the analysis. The results, adjusted for age,showed a significantly higher mean score among theexposed group. The analysis also showed that scoresrose with age (for women only), with inadequate so-cial support (exposed women and control men), andwith money problems. The sampling method is sum-marily described, and the lack of control for somevariables makes it difficult to generalize these results.

Havenaar et al. (129) studied a nonrandom sampleof all segments of the population in a highly contam-inated region (Gomel, Belarus) and in a socioeconom-ically comparable region that was much less touched(Tver, Russia). Each subject (1,617 in the first region,1,427 in the second) completed a self-reported ques-tionnaire (General Health Questionnaire). In both re-gions, approximately half the respondents report un-satisfactory health or psychologic well-being. Theauthors calculated odds ratios adjusted for age, sex,civil status, and education. The risk of psychologicdistress was higher (OR = 2.0, 95 percent CI 1.8-2.4)in the contaminated zone, as was the use of medication(OR = 1.4, 95 percent CI 1.2-1.6). A high score onthe General Health Questionnaire was predicted formothers with children and evacuees, but not by thelevel of contamination of the residence area. In thenext phase, a stratified sampling of each group (322 inthe exposed group, 284 in the other) underwent astandardized physical and psychiatric examination(Diagnostic and Statistical Manuel of Mental Disor-ders: DSM III-R criteria). The two groups did notdiffer significantly.

Results similar to those in the two preceding studies(increased risks for mothers of young children andthose with low social support) were also observed afterthe accident at Three Mile Island (Pennsylvania,United States) among the local population, which hadreceived very low exposure to ionizing radiation (130,131).

A 1993 opinion poll surveyed a sample of 3,067people selected by the quota method in Belarus, Rus-sia, and the Ukraine. These subjects lived in differentzones: contaminated, non-contaminated adjacent tocontaminated, relocation, forbidden, and control. Thedegree of psychologic distress related to the accident,evaluated on a scale from one to five, was generally

high. People in the contaminated and resettled areas,as well as the 30 km zone, rated themselves morehighly than respondents in the control and nonre-stricted areas. The best predictor of personal distressdue to the accident was fear of health effects to oneselfand one's family. Between 25 and 50 percent of thosequestioned said they used sedatives; the highest per-centage lived in the relocation zones (132).

Studies on this subject have also been performedamong patients hospitalized for acute radiation sick-ness after the accident (133) and among liquidators(134). The articles provide few if any details about theselection conditions, the methods of data collection,and the diagnostic criteria. Furthermore, the nosogra-phy is different from that used in the West. It istherefore difficult to interpret these data.

Different analyses (132, 135) underline the multi-plicity and interrelation of the stress factors: an initialpublic policy marked by secrecy and by authoritarianadministration of protection measures; the absence ofpublic confidence in the authorities, in medical pro-fessionals, and in the media; major political and eco-nomic transformations since 1989 in what was theUSSR; the perception of risks linked to the accident;and a lack of confidence in the future.

Other problems

The 2,400 tons of lead poured on the melted core ofthe reactor were partly vaporized. According toBurkart (136), this caused a marked increase in levelsof lead in the blood of children in the area, but thisstatement has not been documented. No increasedlevels of lead were detected in sampled populations(15). Another issue, apparently not studied at all, is theconsequences of the restrictions on food products inthe controlled regions (micronutrient deficiencies orsubdeficiencies).

Voluntary abortions

Western Europe saw an increase in voluntary abor-tions. In Switzerland, in June 1986, there were 60percent more voluntary abortions than expected, basedon the trend between 1984 and 1988 (137), and similarreports came from northern Italy (138) and Greece(139). This undue choice of voluntary abortions maybe considered a consequence of the stress to womenwho were pregnant at the moment of the catastrophe.It also reflects the inadequacy of the medical profes-sion's knowledge of the risks linked to ionizing radi-ation. Irgens et al. (47) did not observe such an in-crease in six counties in Norway where the declarationof elective abortion is a legal obligation. On the otherhand, Burkart (136) indicates, without mentioning the

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source of the data, that Belarussian doctors were rec-ommending abortions during 1987 and pointed outthat this advice may have been justified to the extentthat these doctors suspected, without being able toverify, that their patients had received high doses ofradiation.

Fecundity

In the three contiguous republics, birth rates fell inthe months following the accident nationally as well asin the contaminated zones (3). This observation is alsotrue for numerous regions of the former Soviet Union(45). The number of pregnancies also decreased inSweden (44), Norway (47), and Italy (138) in the earlyyears after the accident. The demonstration of a causallink with the accident is problematic.

CONCLUSION

The increase in thyroid cancer in children and ado-lescents of the three contiguous republics of Belarus,the Ukraine, and Russia is well-documented and thecausal relation with the accident is now undisputed.Uncertainty remains about the relative contributions ofvarious radioactive agents and other risk factors andabout the future extent of the epidemic, depending onage group at exposure. Research needs to concentrateon screening cases, so that early treatment can beprovided, and on investigating the dose-response rela-tion in this particular epidemiologic situation.

The risk of leukemia is expected to increase mod-erately among those who were relatively highly ex-posed (i.e., liquidators) or in the more radiosensitivegroups (such as children). Both descriptive and ana-lytic studies should be carried out. Despite the unlike-lihood of a detectable increase of other cancer types,careful monitoring is needed among all populationgroups for verification purposes and because of thegreat public concern.

As expected from previous scientific knowledge, noexcess in congenital malformations has been shown;nonetheless available data should be validated.

The existence of a post-accident psychologic impactis reasonably certain, although its nature, extent, andspecific risk factors remain to be determined.

Different articles have reported increases in variousphysical disorders. These claims originate from eco-logic studies, so that no causal link can be establishedwith the accident. These claims often appear in non-scientific reports and their basis in fact cannot beascertained (no specification of diagnostic and selec-tion criteria, poor or no characterization of controlgroups, no consideration of confounding factors suchas age and sex, superficial analyses, and paucity of

preaccident reference data). Many reports appear toconcern artificial increases corresponding to a betterscreening. In addition, some of these pathologies havenot been previously related to ionizing radiation(changes in female reproductive functions and neona-tal health, vegetative dystonia, endocrine and respira-tory effects), or only at doses much higher than thoseresulting from the accident (immunologic, cardiovas-cular, neurologic, and digestive effects, lens changes).Lastly, some likely effects of social changes (e.g.,nutritional) in the three republics have not been exam-ined or documented. Epidemiologic studies are neededon all these topics and should start with accuratedescriptions.

Many epidemiologic studies have begun or are be-ing planned in the three countries of the former USSRmost touched by the accident. These studies are in-tended to answer, insofar as possible, the questionsposed above about thyroid cancer, and to verifywhether any other chronic disorders can be discerned.They involve many international partners and are be-ing conducted among the general population as well asamong the liquidators (140).

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