Mutagenesis, Vol. 14, No. 5, 473-478,
September 1999
© 1999 UK Environmental Mutagen Society/Oxford University Press
Biodosimetry results obtained by various cytogenetic methods and electron spin resonance spectrometry among inhabitants of a radionuclide contaminated area around the Siberian Chemical Plant (Tomsk-7)
Siberian Medical University, 634050 Tomsk-50, a/ya 808, Russia, 1 Department of Radiation and Chemical Mutagenesis, Leiden University, Leiden, The Netherlands, 2 Institute of General Genetics, Moscow and 3 Research Center of Spacecraft Radiation Safety, Moscow, Russia
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Abstract |
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On April 6, 1993, near the town of Tomsk (Russia) there was an accident at the Siberian Chemical Plant (SCP) which resulted in extensive contamination of an area of 250 km2 to the north of SCP with long-lived radionuclides such as 239Pu, 137Cs and 90Sr. Cytogenetic methods and electron spin resonance (ESR) spectrometry of tooth enamel were used to estimate the radiation doses received by the population. The ESR signal intensity and the chromosomal aberration frequency in lymphocytes of the tooth donors showed a good correlation. The data showed that 15% of the inhabitants of the Samus settlement received a radiation dose >90 cGy. The exceptions were results of an examination of fishermen, where ESR gave high values (80–210 cGy) but both the chromosome assay and the cytokinesis block micronucleus method gave lower ones (8–52 cGy). A large increase in chromosome damage was observed in people born between 1961 and 1969. It was found that during these years several serious accidents at the Siberian Chemical Plant had occurred causing radiation pollution of the area. The number of cells with chromosome aberrations was significantly less among the people arriving in Samus after 1980. We found good correlations between the level of carotene consumption and a decrease in frequency of both micronuclei in binucleated lymphocytes (r = 0.68, P < 0.01) and chromatid aberrations (r = 0.61, P < 0.01) among the inhabitants. We also examined the inhabitants of Samus for opisthorchis infection, which was present in 30% of the population. The Samus inhabitants affected by Opisthorchis felineus showed significantly increased levels of micronuclei in binucleated lymphocytes and chromatid aberrations as compared with the controls.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResults and DiscussionConclusionsReferences |
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On April 6, 1993, there was an accident at the Siberian Chemical Plant (SCP) (Figure 1
). As a result, an area of 250 km2 to the north of SCP was polluted by various radionuclides (Ilyinskikh et al., 1995; Ilyinskikh, 1998). The most severe pollution occurred at the settlement of Samus, located 12 km from a nuclear facility of SCP on the banks of the Tom river. The highest radiation level outside the plant area was as much as 0.4 µSv/h. Fallout of the radionuclide 239Pu was especially dangerous, however, there were also traces of 137Cs and 90Sr. It was proved that SCP had discarded radioactive waste into the Tom river, therefore, radionuclide absorption into inhabitants' bodies could be not only from soil and air but from water and fish as well. According to a state law of the Russian Federation adopted in 1995, people who have received a dose >50 mSv are entitled to certain privileges and compensation. The Ecological Committee of the Tomsk region was faced with the problem of estimating the doses that had been received by the inhabitants of the Samus settlement as a result of SCP action. It was obvious that we could not determine radiation doses affecting these people because most of the radionuclides in the environment had disintegrated by that time and the level of background radiation found in this area was not significantly different from the natural level. The Committee asked independent experts in Russia and abroad to determine these doses by retrospective methods of biodosimetry. The analysis of chromosome aberrations is the best validated and most powerful method (Edwards 1983; IAEA, 1986; Lloyd et al., 1988; Lloyd and Prosser, 1989). We also used the cytokinesis block micronucleus method (Fenech and Morley, 1986; Almassy et al., 1987; Littlefield et al., 1989; Prosser et al., 1989; Kolubaeva et al., 1991) and tooth enamel electron spin resonance (ESR) spectroscopy (Ikeya et al., 1984; Pass and Aldrich, 1985; Lloyd et al., 1988; Smirenniy and Fedoseev, 1993; Skvortsov et al., 1995, 1996; Smirenniy et al., 1995; Nakamura et al., 1996).
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The aim of this work was a biodosimetric estimation of doses received by the Samus inhabitants who had been exposed to minor radiation doses as a result of environmental pollution by radionuclides from SCP.
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Materials and methods |
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Radiation-exposed and control individuals
As many as 264 people (150 males and 114 females), inhabitants of the settlement of Samus, were examined (3–5 days after the accident). In no case had individuals been exposed to radiation professionally or medically. There were workers at a shipbuilding yard, seasonal workers, fishermen, farmers, school teachers and secondary and professional school students in this group. The seasonal workers were not permanent residents of Samus and had come to work in Samus from other, non-contaminated places in Siberia. A group of infants of 1–3 years old was also examined. We simultaneously monitored 86 matched control inhabitants of the Loskutovo settlement located 42 km to the south of SCP (Figure 1
). In each case, an individual examined had to fill in a questionnaire by means of which we formed groups of people according to district of residence, place of birth, sex, smoking habit, year of birth, anamnesis of diseases, the presence of children with abnormalities in the family, stillborn children, cancers, X-ray examinations and the length of residence in the locality.
Diets and vitamins
Each of the persons also described their diet in their questionnaires. In this study the qualitative and quantitative evaluation of each diet was based on the method of Giovannucci et al. (1995). For each of 90 food and beverage items listed a commonly used unit or portion size was specified and participants were asked how often, on average, over the past year they had consumed that amount of each food. Participants chose from among nine possible responses, which ranged from `never' to `six or more times per day'. We also enquired about the brand, duration and frequency of multivitamin and individual vitamin supplement used and the types of fat commonly used. The questionnaire also contained an open-ended section for foods that were not listed.
We computed nutrient intakes by multiplying the consumption frequency of each unit of food by the nutrient levels of the specified portions. The specific brands of cereal and multivitamins were used in computing intakes (supplementation of vitamin A varies by brand of cereal from 0 to 100% of the recommended daily allowance). Since vitamin A has an antimutagenic effect and can decrease radiation-related chromosome damage, we calculated vitamin A intake among examined individuals. We calculated retinol (preformed vitamin A) intake as two thirds of the vitamin A activity (in IU) of dairy foods plus the total vitamin A activity in other animal products. We also added the specific carotenoid content of foods to our nutrient database, including 
-carotene, ß-carotene lutein, lycopene and ß-cryptoxanthin (Giovannucci et al., 1995). As for other nutrients, we estimated the amount of specific carotenoids in each food item and summed the contribution from each food to calculate an intake score for the specific carotenoid. The questionnaire contained 24 fruits and vegetables and related items (discounting the open-ended section). The residents also consumed seeds of a local evergreen tree (Pinus sibericus) and berries of a shrub of the Eleagnaceae family (Hippophae rhamnoides). The major contributors to specific carotenoids were as follows: ß-carotene–carrots, potatoes, mixed vegetables, Hippophae rhamnoides berries; -carotene–carrots and mixed vegetables; lutein–spinach, Hippophae rhamnoides berries, Pinus sibericus seeds, kale, mustard; lycopene–Hippophae rhamnoides berries; ß-cryptoxanthin—oranges.
Local fish consumption and the examination for opisthorchis infection
Between 1961 and 1994 the SCP discharged radioactive liquid waste into the Tom river, which resulted in considerable contamination of local fish with long-lived radionuclides such as 90Sr, 137Cs and 239Pu (Rikhvanov, 1994). Therefore, local fish consumption may be one of the principal sources of radiation among the residents. Each of the examined individuals indicated the sites of capture and the amount of fish consumed in their questionnaires. Furthermore, the Ob and Tom basin is the largest endemic area for helminthiasis caused by Opisthorchis felineus (Lepyekhin et al., 1992). Most of the local fish of the order Cypriniformes (the intermediate host) are infested with this trematode.The metacercariae, encysted larvae of O.felineus, are located within the muscles of infested fish. Man is infected with opisthorchiasis by consuming raw or undercooked fish. In the definitive host (man and predatory mammals) O.felineus causes chronic cholangitis and cholecystitis and can lead to cholangiocarcinoma or liver cancer (Lepyekhin et al., 1992). In this study the presence of infection among the examined individuals was established by stool analysis for helminth eggs. We also performed quantitative egg counts in the faeces to evaluate the worm burden in most individuals (Lepyekhin et al., 1992).
Cytogenetic methods
Determination of effective equivalent dose of radiation (EED) was by analysis of unstable chromosome aberrations, micronuclei in binucleated lymphocytes and ESR spectrometry of tooth enamel. Samples for investigation were obtained between June 6 and July 6, 1993, 2–3 months after the accident at SCP. In the case of the settlement inhabitants who underwent extraction of molars for medical reasons, blood samples were simultaneously taken for cytogenetic analysis. Extracted teeth were sent to the Research Center of Spacecraft Radiation Safety, Moscow. Lymphocyte cultures obtained from peripheral blood of the same people were incubated in RPMI-1640 medium (Sigma, USA) with phytohaemoagglutinin (Difco, USA) and 15% fetal calf serum. After cultivation for 52 h, standard chromosome preparations (with colcemid added for the last 3 h; Buckton et al., 1973) and those for the cytokinesis block micronucleus method (without colcemid, according to Fenech and Morley, 1986) were prepared. We used standard Giemsa straining. For the cytokinesis block method, cytochalasin B was added for the last 24 h to evaluate binuclear cell frequency and micronucleus levels in them.
Radiation doses were determined by analysis of dicentric chromosome frequency in T lymphocytes according to the recommendations of the IAEA (1986). To evaluate effective equivalent radiation doses using micronucleus analysis in binucleated lymphocytes we took into account suggestions made by Fenech and Morley (1986). Generally, 1000 metaphase spreads were examined per individual to assess chromosome aberrations and 1000 binucleated lymphocytes per individual were assessed to score micronuclei. We used standard calibration curves to determine the EED (for the micronucleus and dicentric chromosome assays) worked out in our laboratory (Ilyinskikh, 1998). Statistical analysis of the data was by Student's t-test and ANOVA (analysis of variance). In statistical analysis of the results we used procedures available in the SAS statistical package (SAS Institute Inc., 1989).
Tooth enamel ESR spectrometry
Retrospective dose reconstructions were carried out according to the recommendations in Individual Radiation Dose Determination Using Tooth Enamel ESR Spectrometry developed at the Research Center of Spacecraft Radiation Safety (Russia).
The ESR assay detects radicals (atoms with unpaired electrons) caused by radiation exposure and tooth enamel and bone are well suited to this purpose. Since bones are continuously remodelled and not readily accessible, teeth have been mainly used in ESR studies to date. Enamel, the covering of the tooth surface, consists mostly of hydroxyapatite (a compound of crystalline structure consisting of calcium phosphate) and is free of any metabolic activity. Tooth enamel is a unique inorganic structure. Although laboratory studies of ESR have been published since the 1960s, in the past decade ESR has received renewed attention. In Japan, M. Ikeya, now at Osaka University, has actively promoted ESR studies (Ikeya et al., 1984).
For enamel separation, a disc-shaped diamond cutter was used with running water. This is an entirely mechanical separation with no chemical treatment. The enamel was then crushed in an agate mortar until the grain size approached homogeneity (0.5–1.4 mm in diameter). A field modulation of 100 kHz in frequency and of 0.32 mT in width was used at a microwave power of 5 mW, with a time constant of 0.1 s and a field sweep of 10 mT in 16 min. The enamel sample and an internally located manganese marker were measured simultaneously.
ESR measurements were carried out using X-band ESR spectrometers BRUKER-ER-420 and Radiopan-SE/X-2544 with a PC to execute the ESR spectra accumulation program. Additive irradiation of the samples investigated was performed with a Start 
-irradiation device (137Cs) or one of the same type at a dose rate of 30 rad/min. The necessary dose was obtained by varying the time of irradiation and the distance the between the -ray source and the sample. ESR spectrometers and radiation devices were certified by Gosstandard of the Russian Federation. The results of 264 sample measurements were subjected to systematization and computer treatment using different statistical methods with the help of the STATGRAPHICS v.2.6 program. The statistical analysis shows that the probability density distribution is described by Weibull's law:
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= 1.47 and 
= 43, mode 12 cGy, median 38 cGy and arithmetic mean value 39 cGy.
The 
2 test was used to test the correlation between the experimental results and chosen approximate distributions.
In the evaluation of radiation doses received by the inhabitans of Samus we have taken into account the natural dose in this area of 0.1 cGy/year (Rikhvanov, 1994).
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Results and Discussion |
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Based on the results given in Table I
we concluded that most of the inhabitants of Samus had been exposed to considerable radiation doses. An abnormally high frequency of lymphocytes with dicentric and ring chromosomes in peripheral blood and the results of tooth enamel ESR spectroscopy led to this conclusion. The elevation in the level of micronuclei in binucleated T lymphocytes in peripheral blood confirms this indirectly. The indices of EED recorded by all three methods correlate significantly (P < 0.01) with each other (r = 0.78–0.82). In the case of the controls, the EED values did not differ from those which would be received from natural radiation. According to the data in Table I, of the 264 Samus inhabitants examined, 222 showed a clear increase in EED indicators in comparison with the values expected in individuals exposed to natural radiation during their lifetime (0.1 cGy/year). All of the seasonal workers, who were absent from Samus at the time of the accident on April 6, 1993, showed levels of EED similar to the controls. The chromosome analysis made it possible to estimate the doses in a group of children born between 1990 and 1992 as 10–20 cGy, but ESR spectrometry did not confirm this. Probably, the damage to stem haematopoietic cells in children led to the persistence of high levels of chromosome aberrations, whereas accumulation of changes in tooth enamel needs a longer period. The ESR spectrometry method recorded the largest increase in EED in fishermen, but cytogenetic methods did not show this.
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We observed no correlation between the EED value and sex or nationality among the Samus inhabitants. Also, we observed no correlation between the EED value and smoking habit (r = –0.17, P > 0.05), fat consumption (r = 0.24, P > 0.05) or carotene consumption (r = 0.33, P > 0.05) among individuals. The individuals with high EED values showed clear decreases in body mass index and metabolic equivalents, which is typical of people who have received a high radiation dose (Poluyartsev, 1987
). Deficiency of folic acid, vitamin B12 or carotenes is known to lead to genomic instability in man (Ilyinskikh et al., 1990, 1997). Both the controls and the radiation-exposed individuals were approximately equal in consumption of these vitamins. In this study both groups showed no correlation between level of vitamin B12 or folic acid consumption and frequency of chromosome damage. On the other hand, we found good correlations between the level of carotene consumption and the frequency of both micronuclei in binucleated cells (r = 0.68, P < 0.01) and chromatid aberrations (r = 0.61, P < 0.01).
Furthermore, lower levels of micronuclei in binucleated cells and chromatid aberrations were observed in the Samus inhabitants who regularly consumed Hippophae rhamnoides berries, which have a high carotene content. However, there was no correlation between the frequency of dicentric or ring chromosomes and the level of carotene consumption (P > 0.05). There was a good correlation between cigarette smoking habit and increased levels of micronuclei in binucleated lymphocytes (r = 0.56, P < 0.05) (Figure 2).
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According to the data in Table I
, individuals, especially fishermen, who regularly consumed local fish showed increased EED. The chromosome and micronucleus tests revealed levels of EED in non-fisherman and fisherman as high as 14.2 ± 0.9 and 24.9 ± 1.0 cGy, respectively (Figure 3). The reconstructed dose determined at the same time by tooth enamel ESR spectrometry was 136.0 ± 3.8 cGy. Therefore, the inhabitants of Samus received a major part of their dose by consuming contaminated fish from the Tom river. Our previous data demonstrated that fish and molluscs in the Tom basin have various radionuclides in their bodies arising from the disposal of radioactive waste from the Siberian Chemical Complex (Ilyinskikh et al., 1995, 1996). According to Rikhvanov (1994), one of the main emitters in local fish is radiophosphorus. We surmise that local fish consumption can lead to the accumulation of radiophosphorus within tooth enamel. As a result, tooth enamel ERS spectrometry showed the largest increase in EED among fishermen.
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We examined the inhabitants of Samus and Loskutovo for opisthorchis infection, which was present at a level of 30%. The Samus inhabitants affected by O.felineus showed significantly increased levels of micronuclei in binucleated lymphocytes, chromatid aberrations and dicentric chromosomes whereas the infected Lockutovo inhabitants showed only comparatively insignificant increases in micronuclei in binucleated lymphocytes and chromatid aberrations (Figure 4
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Thus, according to the results of all the methods of biodosimetry, the largest increases in EED were detected among the Samus inhabitants infected with opisthorchiasis. We surmise that these data may be associated with the consumption of local radionuclide-contaminated fish by the inhabitants of this settlement. It is possible that immunosuppression among radiation-exposed individuals may lead to the impairment of antihelminthic immunity and a decrease in human resistance to reinfection (Ilyinskikh et al., 1982
, 1984).
According to Table I, the Samus inhabitants with the highest EED values (>90 cGy) showed a significant increase in the number of cancer cases in their pedigrees as well as the highest levels of worm burden (38.3 ± 4.2%). Since O.felineus can lead to cholangiocarcinoma or liver cancer (Lepyekhin et al., 1992; Ilyinskikh, 1998) these cancer cases may be associated with both the regular consumption of radionuclide-contaminated fish and the high level of worm burden in these families.
Chromosome analysis and tooth enamel ESR spectrometry show the presence of a clear gradient, the highest levels of EED being recorded in older people. The younger the people examined, the lower the level of EED found. The first radiation accidents at SCP occurred in 1961 and 1963. In connection with this, the accumulation of radiation began in 1961. Individuals born before 1961 had EED levels practically the same as that of individuals born between 1961 and 1963 according to the results of the cytogenetic techniques and ESR spectrometry. Our findings allow us to propose that a high level of micronucleated lymphocytes can be maintained for a very long time after irradiation if it occurred in the pre-natal and early post-natal periods. The data can also be interpreted as simply that older individuals were more sensitive to the more recent exposure occuring in 1993.
The analysis of chromosomal aberration levels shows that dicentric chromosomes often do not have accompanying fragments. This occurs as a rule when a considerable period of time has passed after irradiation. We suggest that there were two factors making a major contribution to the dose received by the inhabitants of Samus, the accidents at SCP from 1961 to 1963 and consumption of fish by the inhabitants. The genotoxic effects of the accident in 1993 are less important, but were registered by the chromosome and micronucleus tests in children born between 1990 and 1992. From the dose that can be reconstructed by cytogenetic methods in infants it is possible to conclude that the accident in 1993 contributed a dose of ~10–20 cGy to the inhabitants.
The estimation of chromosome aberrations in cultivated lymphocytes of peripheral blood is a universally recognized method of biological dosimetry in the case of even irradiation of the body at a dose of >0.5 Gy (IAEA, 1986). However, in the case of small doses or chronic irradiation, different and unsatisfactory data are obtained (in the sense of biological dosimetry) by cytogenetic assay. There is no general agreement about the nature of induction of chromosome aberrations at doses <0.5 Gy. The first point of view arises from a linear non-threshold relation (as part of the general linear quadratic relationship for chromosome aberration production by ionizing radiation). According to another opinion, the dose–response relation varies with different ranges of low doses, with the consequence that the true response values at low doses cannot be determined by extrapolation from the response at higher doses (Lloyd and Prosser, 1989; Lloyd et al., 1988; Sevankaev, 1991). Nevertheless, reconstruction of irradiation doses by chromosome analysis was successfully applied to examine a population living near the Semipalatinsk Atomic Test Ground (Shevchenko et al., 1995), where air explosions had ceased >30 years ago. A high correlation of reconstructed doses was also demonstrated by Nakamura et al. (1996) by simultaneous chromosome and ESR spectrometry testing of people that had been irradiated at an atomic bomb explosion 50 years ago.
In our opinion, the main cause of discrepancy between results obtained by the use of models of radiation dose for a population and direct measurements using tooth enamel ESR spectrometry is due to limitations of those prerequisites which have been used in model calculations of expected densities of contamination and population radiation dose. The reconstruction of past events using today's data is not easy. The problem of reconstruction can be mathematically described with the help of Bayes theorem. It can be written in the form
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The crux of the theorem is that for all today's observations P(A/Hi) can only specify the value of the a priori probability of the cause P(Hi); using this theorem one can state that the more the multistage process of reconstruction is researched, the more a priori values of P(Hi/A) are introduced into the probability of its existence. An increase in the number of probable causes of Hi considerably decreases both the trustworthiness of P(Hi/A) and the precision of its reproducibility. As to the problem of dose reconstruction by different methods, one can say that they have in common an a priori probability which states that `radiation is associated with the accident at the Siberian Chemical Plant on April 6, 1993' (and there is no other reason). Those methods of dose reconstruction which, for example, are based on analysis of daughter products of decay require the introduction of fallout characteristics, the isotope composition of the radioactive cloud and decay chains and involve the introduction of several a priori probabilities that considerably decrease the trustworthiness of these methods in comparison with direct dose measurement.
In view of the applicability of ESR to dating fossil teeth, it seems very likely that tooth enamel can accumulate radiation doses imparted at extremely low dose rates. This means that human teeth may be distinct natural biodosimeters not only for acute exposures, such as atomic bomb explosions, but also for repeated small doses or chronic -ray exposures, such as that of radiation workers and people residing in a contaminated environment. One serious disadvantage of tooth ESR is that the availability of teeth depends entirely on chance. In contrast, blood samples are readily available from virtually anybody and thus cytogenetic examination is superior for dose reconstruction on an individual. The drawback to the use of chromosome aberration data for dose reconstruction of chronically exposed people is the lack of information on the dose rate factor. In theory, the linear quadratic model predicts that the quadratic component disappears when the dose rate is much reduced. Thus, one may use the fitted linear coefficient of the acute dose–response curve of chromosome aberration induction obtained in vitro. However, it is desirable to collect information on both tooth ESR and chromosome aberration data from the same donors to substantiate the theory. Another problem arises: most of the chromosome aberrations remaining in the human body many years after radiation exposure are stable aberrations. These aberrations are known to require considerable skill for proper detection and interlaboratory comparisons cannot be made without careful standardization of the technique. Although the recently developed fluorescence in situ hybridization (FISH) technique is well suited to the counting of stable aberrations, this method is expensive. Lastly, it should be noted that the conventional staining method (i.e. the standard Giemsa staining method) can detect as much as 70–80% of stable chromosome aberrations when compared with the FISH method (Nakamura et al., 1996). However, the conventional method does not require expensive reagents and fluorescence microscopy and is an alternative choice for a large scale survey.
We suggest that the simultaneous use of various methods of biodosimetry make the determination of doses of radiation that have been accumulated by man over a long period of irradiation with small doses possible with high precision, especially when radionuclides are incorporated into the organism.
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Conclusions |
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The results of the retrospective reconstruction of EEDs of inhabitants of Samus using analysis of unstable chromosome aberrations, the cytokinesis block micronucleus method and ESR spectrometry of tooth enamel allow us to conclude that:
- all findings show that most of the Samus inhabitants received doses of radiation which exceeded natural levels;
- the highest radiation doses were detected in fishermen, probably explained by the consumption of radionuclide-contaminated fish;
- the data obtained suggest that the accidents at SCP between 1961 and 1963 made a major contribution to the dose received by the Samus inhabitants.
- opisthorchis infection as well as smoking habit can induce an increase in chromosome damage (micronucleated lymphocytes and chromatid aberrations) among both radiation-exposed and non-exposed inhabitants.;
- the regular consumption of high carotene foods may have caused a decrease in chromosome damage among the Samus inhabitants.
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4 To whom correspondence should be addressed. Tel:+7 3822 413679; Fax: +7 3822 233309; Email: root{at}ecogen.tomsk.su
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References |
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Received on January 6, 1999; accepted on June 7, 1999.
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