Mutagenesis, Vol. 17, No. 2, 135-139,
March 2002
© 2002 UK Environmental Mutagen Society/Oxford University Press
The frequency of dicentrics and acentrics and the incidence of rogue cells in radiation workers
ica Rozgaj1,1
uba1
imi
2
1 Mutagenesis Unit and 2 Biomathematics Unit, Institute for Medical Research and Occupational Health, Ksaverska c. 2, HR-10001 Zagreb, Croatia
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Abstract |
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Occupational exposure to ionizing radiation causes chromosomal damage. Some of the damaged cells show a large number of aberrations such as dicentrics, polycentrics, rings and numerous acentric fragments. This paper describes an analysis of the frequency of dicentric chromosomes and acentric fragments in 1260 subjects occupationally exposed to X-rays and 241 controls. Special attention was paid to the incidence of multi-aberrant cells. The 3 year cumulative dose was a significant predictor for all analyzed aberrations. The duration of exposure was a highly significant predictor of the frequency of rogue cells, but not of acentrics and dicentrics. Age and sex were not found to be significant predictors of the analyzed aberrations.
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Introduction |
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The effects of ionizing radiation on genetic material are well known. Double-strand DNA breaks appear to be the primary lesions in the formation of chromosomal aberrations, which can easily be seen in metaphase chromosomes (Natarajan, 1993
; Pfeiffer et al., 2000). Dicentrics are considered to be appropriate biomarkers of radiation damage (Lloyd, 1992; Hoffmann and Schmitz-Feuerhake, 1999). Cells with a large number of dicentrics and subsequent fragments are also described in findings of chromosome aberration studies. Awa and Neel (1986) termed these multi-aberrant cells `rogue cells'. They defined them as cells containing five or more exchange-type aberrations for which precise karyotypic identification of the origin of aberrant chromosomes was usually impossible. Lloyd et al. (1988) defined rogue cells as cells with more than one dicentric or ring chromosome, while Bochkov and Katosova (1994) defined them as cells with three or more aberrations. Although very rare, they appear in individuals exposed to various physical, chemical or biological agents (Lloyd et al., 1988; Bochkov and Katosova, 1994; Neel et al., 1996; Fender and Wolf, 1998; Neel, 1998; Balakrishnan and Rao, 1999; Cheriyan et al., 1999; Jairkrishan et al., 1999), but also in individuals who do not seem to have been exposed to clastogenic agents (Tawn et al., 1985; Mustonen et al., 1998). Multi-aberrant cells were found in examinees exposed to ionizing radiation during the Chernobyl accident and in accident clean-up workers (Vorobjev et al., 1994; Domracheva et al., 2000). They were also observed in Namibian uranium miners (Zaire et al., 1997). Increased frequency of rogue cells was observed in astronauts' lymphocytes after space missions (Obe et al., 1997). Testard et al. (1996) suggested that these cells might result from irradiation with high LET particles of cosmic origin.
Bloom et al. (1973) and Lazutka et al. (1996) suggest viral infection as a cause of multiple chromosome damage. Lazutka found a significant correlation between elevated titers of human polyoma virus JC and BK and the occurrence of rogue cells. Neel's study of 1835 Hiroshima atomic bomb survivors showed that rogue cells were more frequent in subjects who received higher doses of radiation (Neel, 1998). He suggested that exposure to the bomb increased susceptibility to the periodic clastogenic effects of polyoma and other viruses. Bacterial restriction endonucleases could also be agents of multiple chromosome damage. These enzymes, produce chromosomal-type aberrations, including double minutes (Ahuja and Obe, 1994). Some authors suggest mutations as a possible cause of rogue cells (Hsu, 1983; Neel et al., 1996; Little et al., 1997).
This paper presents the results of a follow-up study of subjects occupationally exposed to ionizing radiation. We analyzed the association between the frequency of chromosomal aberrations and possible influencing factors: age, sex, smoking, occupational dose and duration of exposure. Particular attention was paid to the occurrence of rogue cells.
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Materials and methods |
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The study comprised 1260 individuals of various professions who were identified as occupationally exposed to ionizing radiation. Control subjects, chosen among volunteer donors (students and clerks) were analyzed in the same period. The subjects were of both sexes with a mean age of 28.9 years in the control group and 39 years in the exposed group. The exposed subjects had been monitored regularly before the study began. The average annual occupational dose per person ranged between the detection limit of the monitoring dosimetric film and 20 000 µGy. As chromosome aberrations may be seen years after irradiation due to the long life of lymphocytes (Buckton et al., 1967
; Léonard et al., 1988), we considered individual occupational doses recorded over a 3 year period before we took the blood samples, which was suggested as the average half-life for phytohemagglutinin-responsive T lymphocytes in circulation (Dolphin et al., 1973; Lloyd, 1992). The study included only healthy individuals. Subjects with a history of radiotherapy or chemotherapy were excluded from the study.
Chromosome aberrations in lymphocytes were analyzed according to a standard protocol (IAEA, 1986). Whole blood cultures were prepared using F-10 medium (Gibco). The cultures were incubated at 37°C for 48 h. Using the fluorescence plus Giemsa technique we have formerly shown that under our experimental conditions most metaphases were M1. Giemsa stained slides were coded and scored blind under the light microscope. Two hundred metaphases per subject were analyzed for acentric fragments, double minutes, dicentrics, polycentrics and rings. Polycentric chromosomes were expressed as dicentric `equivalents', where dicentric equivalents equaled the number of centromeres minus one (Savage, 1976; Littlefield et al., 1991). Cells with three or more dicentrics or dicentric equivalents were considered to be rogue cells.
Statistical analysis
The associations between the frequency of acentrics, dicentrics and rogue cells per 200 cells and group, smoking habit, duration of occupational exposure, age and 3 year cumulative dose were analyzed using the Poisson regression model with the canonical logarithmic link function (Lindsey, 1997):
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2 and the deviance. Pearson's 2 divided by the degrees of freedom was used as a scale factor to account for over- or under-dispersion. Since the analyzed model is log-linear, exp(ßi) can be interpreted as relative risk (RR). RRs for each analyzed variable estimated in this way are controlled for the other variables included in the analysis. Choice of the model was based on the AIC criterion. The analyses were performed with SAS 6.12 on a PC using PROC GENMOD.
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Results |
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To analyze chromosome aberrations, we scored 300 200 first metaphase cells, i.e. two hundred per subject. The control value for dicentrics (including dicentric equivalents) was 1/2008.33 analyzed cells and the ratio in the exposed group was 1/456.52 cells. The results are shown in Tables I–IV
and Figure 1. Table I shows the demographic data, sex and age of the subjects, duration of occupational exposure to radiation, smoking and cumulative radiation dose over 3 years. The groups did not match in age, as the control group was dominated by younger subjects who underwent pre-employment screening. Neither was a match possible for sex: while women slightly prevailed in the control group (53%), 56% of the exposed subjects were men. The contribution of smokers was 43% in both groups. The average dose in the exposed group was 56.5 µGy.
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Figure 1
shows the frequencies of cells with acentrics, dicentrics, including rings and dicentric equivalents. The frequency of dicentrics was four times higher in the exposed group than in the controls, while multi-aberrant cells were five times more frequent in the exposed group. We found 46 subjects with multi-aberrant cells among the exposed individuals (54 rogue cells) and two among the controls.
In the Poisson regression analysis the magnitude of the association among the variables was expressed in terms of RR, 95% confidence limits and the corresponding P values. Tables II–IV show the results of Poisson regression for the number of acentrics (including double minutes), dicentrics and dicentric equivalents and rogue cells.
Table II shows that group (exposure to radiation) was a statistically significant predictor of the number of acentrics, even after accounting for dose and exposure. The data are consistent with the 30–167% increase in the number of acentrics in the exposed group. The 3 year cumulative dose was a significant predictor, indicating a 4.1% increase in the number of acentrics per 0.25 mGy. Other variables were not significant predictors of the number of acentrics.
Table III shows the results of the Poisson regression for dicentrics. Just as for the acentrics, group and radiation dose were statistically significant predictors. The expected number of dicentrics in the exposed group was 3.3 times as high as in the controls. The number of dicentrics increased 6.4% per 0.25 mGy in the cumulative 3 year dose. Other predictors did not explain the frequency of dicentrics.
The results of Poisson regression for rogue cells presented in Table IV indicate both duration of exposure and dose as significant predictors. The number of rogue cells increased by 34.1% for every 5 years of exposure and an additional 8.1% per 0.25 mGy increase in the 3 year cumulative dose. After accounting for dose and exposure, there was no significant difference between the control and the exposed group.
The analysis of residuals revealed one extreme case of a woman with a dose of 12 305 µGy but with no dicentrics. The exclusion of this outlier from the analysis of rogue cells did not significantly influence the parameter values and confidence levels for exposure and sex. The parameter for dose, however, almost doubled, yielding an RR of 1.138/0.25 µGy (95% confidence limits 1.066–1.216, P = 0.0001).
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Discussion |
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The results of numerous studies on the effect of received dose on aberration yield are inconsistent, particularly those investigating radiation workers exposed to very low doses of radiation. Chung et al. (1996) studied chromosome aberrations of workers from a nuclear power plant. The results showed a dose-dependent increase in chromosome aberrations with respect to total cumulative dose and recent 5 year dose when both control and exposed groups were considered. No dose-dependent increase was found when only the exposed group was considered. Analyzing chromosomal aberrations in male workers exposed to
-radiation, Balakrishnan and Rao (1999) reported that physical doses accumulated over 10 years work were in good agreement with the biological dose estimate. Analyzing hospital workers occupationally exposed to X-rays, Paz-y-Miño et al. (1995) did not find a correlation between exposure dosage and the percentage of chromosome aberrations. Littlefield et al. (1998) did not find a correlation between aberration frequency and recorded measurement of physical dose among clean-up workers who were sent to Chernobyl after the reactor accident. The comparison between physical and biological dosimetry in occupationally exposed subjects is often contradictory due to various factors: cumulative effects of radiation, repair mechanisms, adaptive response to chronic exposure, interindividual differences in sensitivity to radiation and elimination of damaged cells, but also due to failure to wear the dosimeter during irradiation and earlier acute overexposure (Lloyd and Purrot, 1981; Sasaki, 1990; Jha and Sharma, 1991; Barquinero et al., 1993). Lloyd et al. (1992) presented the results of a collaborative experiment involving six laboratories which examined the yields of unstable chromosomal aberrations in human lymphocytes induced in vitro by X-rays over the dose range 0–300 mGy. They found a relatively high number of cells containing more than one exchange-type aberration, while none was observed in the zero dose material. Although some authors who reported finding rogue cells did not associate their occurrence with exposure to ionizing radiation, they found it possible that radiation may increase the susceptibility of cells to the clastogenic effects of some viruses (Neel, 1998).
Assessing the influence of the duration of work in a radiation field, Chung et al. (1996) and Jha and Sharma (1991) did not find significant differences among individuals with different durations of exposure at work. Analyzing exposure duration in addition to received dose, we found a significant correlation with rogue cell incidence. The increase was 34.1% per 5 years of continued employment. After accounting for sex, dose and exposure, there was no significant difference between the control and exposed groups. On the other hand, the frequency of acentrics and dicentrics did not increase significantly with time of exposure. However, after accounting for age, sex, smoking, dose and exposure, there was still a significant difference between the exposed and control groups. This may be due to factors not included in the analysis [e.g. viral infection (Bloom et al., 1973; Lazutka et al., 1996; Neel, 1998) and non-linearities of dose and/or exposure effect and/or interaction between predictors.
The effect of age on aberration yield was reported by Littlefield et al. (1998) and Ramsey et al. (1995). Pressl et al. (1999) found an increase in translocation yield with age, but no significant effect of sex. Bolognesi et al. (1997) found an increase in the frequency of chromosome aberrations, micronucleus occurrence and sister chromatid exchange in older age classes. Evans et al. (1979) reported a positive correlation between dose and age in their follow-up study in nuclear dockyard workers. In a study of nuclear power plant workers Chung et al. (1996) reported negative results for the effect of age on chromosome damage. Neither age nor sex were significant predictors of aberrations analyzed in our study. Statistical analysis did not show a significant sex–age association.
Reports on smoking as the cause of chromosome aberrations are conflicting. Ramsey et al. (1995) found a significant association between smoking and stable aberrations in a study of 91 subjects measured by the FISH technique. Tawn and Cartmell (1989) reported an increase in chromosome aberrations (CA) in smokers not exposed to other clastogenic agents, but the results were not significant. Pressl et al. (1999) found an insignificant increase in chromosome damage. Chung et al. (1996) reported negative results on CA rate in smokers employed in nuclear power plants. The Poisson regression analysis in this study did not show any influence of smoking on the induction of acentric or dicentric chromosomes, which is in agreement with our earlier results (Rozgaj et al., 1999a).
The results presented in this paper corroborate the importance of chromosomal analysis in evaluation of radiation-induced damage. The significant increase in dicentrics in the exposed group confirms our previous results (Rozgaj et al., 1999b). Of special concern was the frequency of rogue cells. It was five times as high in the exposed group as in controls (1 rogue cell/4667 analyzed cells versus 1/24 100). Other authors report different frequencies of rogue cells in subjects exposed to radiation: 1/10 000 (Bochkov and Katosova, 1994); 1/100–1/10 000 (Lazutka, 1996); 1/9800 (Mustonen et al, 1998).
Our results show a significant association between all analyzed aberrations and the 3 year accumulated dose. Further analyses will include additional data on medical X-ray exposure and recent viral and bacterial infections as potential causes of multiple cell damage.
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Acknowledgments |
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This investigation was in part supported by the Ministry of Science and Technology of the Republic of Croatia (grant no. 00220107).
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Notes |
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1 To whom correspondence should be addressed. Tel: +385 1 4673 188; Fax: +385 1 4673 303; Email: rrozgaj{at}imi.hr
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References |
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Received on May 14, 2001; accepted on October 15, 2001.
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