Chapter 4

 

RADIATION RISKS OF LEUKEMIA AMONG RUSSIAN EMERGENCY WORKERS,
1986-1997

 

 

Introduction

 

In 1986 after the Chernobyl accident the All-Union Distributed Registry was established in the former USSR. After the disintegration of the USSR the Russian National Medical and Dosimetric Registry (RNMDR) was set up in 1992. The Registry places particular importance on the follow-up of emergency workers with the highest doses (mean dose 0.11 Gy).

Of the radiogenic malignant neoplasms leukemia is known to have the maximum radiation risk and minimum latent period of 2 years. Therefore, the excess of leukemia incidence rate above the spontaneous level can serve as the first indicator of health effects for those exposed after the Chernobyl accident.

The principal source of information about the dose-response for leukemia is data about the atomic bomb survivors in Japan (Preston et al., 1994). These data have been primarily obtained for the medium and high doses (>0.2 Gy) and acute exposure. Results on small doses and dose rates, on the other hand, are limited, because such studies require large size cohorts and long follow-up period. Of the studies on small doses and dose rates, mention should be made of the joint research of leukemia incidence among nuclear industry workers (Preston et al., 1994) in several countries, in which statistically significant radiation risks of leukemia were obtained for prolonged exposure and accumulated radiation doses less than 0.1 Gy. In this context, the cohort of emergency workers may be of value to gain new information about the dose-response in the dose range of less than 0.2 Gy.

An analysis of radiation risks of leukemia incidence in the Russian cohort of emergency workers was first performed in 1996. Results of the analysis were published in papers by Cardis et al., 1995 and Ivanov et al., 1997a. Cardis used the cohort method, with the control group being the population of Russia of corresponding sex and age. The analysis was based on data for 48 cases of leukemias diagnosed in males from 1986 to 1993 among males. A statistically significant excess of leukemia incidence among the emergency workers above the control was found. Under the assumption that this excess was due to radiation exposure, the risk of leukemia incidence due to radiation were estimated. The excess relative risk at dose 1 Gy was 4.3 with 95% Confidence Intervals (0.8, 7.8).

In the study by Ivanov et al., (1997b) the case-control method was used. The study did not reveal statistically significant risks, though a positive trend in the dose dependence of relative risk was demonstrated.

This study is a continuation of the research on leukemia incidence among emergency workers. In the period from 1993 to 1997 major changes have been observed in the distribution of leukemia cases: new cases were added, both registered in this period and those diagnosed earlier. Diagnoses were made more specific and diagnosis dates were determined more accurately. The number of leukemias diagnosed to date permits an analysis using the most reliable medical and dosimetric data. The practice of RNMDR shows that the information supplied by regional centers of RNMDR is not of equal quality. The present study uses medical and dosimetric data for males from six economic regions of Russia (North-West, Volgo-Vyatsky, Povolzhsky, Central-Chernozem, North-Caucasus and Urals). Data supplied from these regions are characterized by reliability and high percentage of annual check-ups for emergency workers (about 86%).

 

 

 

Materials and methods

 

General description of the study cohort

 

The overall size of the study cohort (as of December 31, 1997) was 71,217 persons. These are emergency workers who were examined at least once in the studied period, their doses being confirmed by documents. The analysis is based on individual information on date of birth, date of arrival to the controlled zone and date of departure, date of the last check-up, date of diagnosis (in the case of disease) and dose ascertained in documents.

The number of person-years from 1986 to 1997 is 743,845. Time under risk for each emergency worker was determined as date of the last check-up (or diagnosis in the case of disease) minus the date of arrival in the zone.

The loss of follow-up person-years does not exceed 14% (ratio of observed number of person years and the maximum attainable is 86%, given 100% attendance of annual check-ups).

Figure 1 shows dynamics of the number of emergency workers in the studied cohort. The curve rise in the initial period of follow-up is due to features of arrival of emergency workers at the zone and the following decline, mostly due to the decrease in the cohort size because of deaths. Rapid decrease in the cohort size by the end of the follow-up period is explained by 2-3 years delay in data accumulation and verification. For this reason, the considered period of the follow-up was limited by 1997.

 

Figure 1. Dynamics of the number of emergency workers in the studied cohort.

 

 

The studied cohort does not differ by basic dosimetric and demographic characteristics from the general emergency workers cohort. The RNMDR includes a total of 174,916 emergency workers as of January 1, 1999). The entire cohort is described in detail in Ivanov et al., (1997a).

Figure 2 shows the distribution function of the number of emergency workers by age at exposure. The mean age at the time of arrival in the Chernobyl zone was 34.7 years for healthy persons and 32.4 for emergency workers with diagnosed diseases. It can be seen from Figure 2 that those with diseases have a lower mean age at exposure than the healthy ones.

A total of 44 cases of leukemia were diagnosed (31 cases among emergency workers with known dose) in the considered time period (1986-1997) in the indicated 6 rayons (districts). The cases, which were not fully verified by the time of diagnosis, were not considered. Four cases were diagnosed during the latent period of 2 years and were excluded from the study. Thus, the analysis of the dose-response included 27 cases. The dynamics of incidence are shown in Table 1.

The structure of incidence is given in Table 2. As can be seen from Table 2, acute leukemias account for 39% of the total number of cases.

Figure 2. Distribution of emergency workers by age at exposure.

 

 

Table 1

Dynamics of verified leukemia cases in time

 

Calendar year

1986

1987

1988

1989

1990

1991

1992

1993

1994

1995

1996

1997

Number of cases

0

0

3

1

4

3

3

2

6

4

3

2

 

 

Table 2

Structure of leukemia incidence among emergency workers

 

Leukemia form (ICD-9)

Number of cases

Absolute

%

All acute leukemias

12

39

Acute lymphocytic leukemia (204.0)

2

7

Acute myeloid leukemia (205.0)

6

19

Other acute leukemias (206.0-208.0)

4

13

All chronic leukemias

19

61

Chronic lymphocytic leukemia (204.1)

8

26

Chronic myeloid leukemia (205.1)

11

35

Other myeloid leukemias

0

0

Total (204-208)

31

100

 

 

All the cases in the study were verified by the algorithm adopted in RNMDR. The verification of leukemia diagnosis was carried out at 2 levels: the place of residence and the RNMDR. Results of verification of diagnosis made at the residence level were sent to RNMDR where a medical expert specializing in hemoblastoses conducted final verification. The package to be provided to RNMDR included primary medical documents such as extracts from medical records, hematologist conclusion, autopsy record and, if necessary, diagnostic materials (blood smear and bone marrow samples).

 

Dosimetric characteristics of the cohort

 

The dosimetric data on emergency workers can be divided with respect to reliability into three groups depending on the dose estimation method:

       radiation or absorbed dose based on individual dosimeter;

       group dose assigned to members of a group based on data of individual dosimeter borne by one member of the group;

       route dose estimated by mean dose rate in the controlled zone and time spent there.

Doses for emergency workers were different and depended on time of working in the exposure area. The mean doses were maximum for emergency workers involved in the works in 1986. Table 3 contains mean doses, time spent in the zone and dose rate derived by dividing the individual dose by the time spent in the zone.

 

Table 3

Mean dose characteristics for emergency workers as a function
of time spent in the accident zone

 

Year

Number

Mean dose (Gy)*

Mean time spent in zone (days)*

Mean dose rate (mGy/day)*

1986

26867

0.17

78.3

4.3

1987

28845

0.09

82.8

1.6

1988

11918

0.03

111.6

0.5

1989

3736

0.03

107.3

0.5

1990

451

0.04

109.8

0.5

1986-1990

71817

0.11

87.4

2.3

 

* Averaging was carried out with the weight of the number of follow-up person-years.

 

 

Figure 3 shows distribution of emergency workers by external radiation dose. As can be seen from the figure, the distributions are different from each other and the mean dose among the cases is higher the dose among the healthy persons, which may be indicative of the effect of exposure.

Distribution of emergency workers by time spent in the zone and dose rate is illustrated in Figures 4 and 5. It can be seen that the dose rate does not exceed 2 mSv/day for half of the emergency workers.

Main characteristics of the emergency workers cohort are given in Table 4.

Figure 3. Distribution of emergency workers by external radiation dose.

Figure 4. Distribution density of the number of emergency workers by time spent in the zone.

Figure 5. Distribution of emergency workers by dose rate.

 

Table 4

Main characteristics of the emergency workers cohort

 

Status

Leukemia cases used for risk estimation (all types)*

Leukemia cases used for risk estimation
(all types except 204.1)*

Healthy

Total

27

21

71217

Mean dose (Gy)

0.135

0.153

0.108

Mean dose rate (Gy/day)

0.0037

0.0042

0.0023

Mean time spent in the zone (days)

77.1

77.7

87.4

 

* Cases with a dose for the considered period diagnosed after the 2 years latent period.

 

 

Statistical methods

 

To estimate risk coefficients we used the maximum likelihood method in the assumption that all the cases are independent Poisson values. The criteria of significance were determined from the asymptotic properties of the likelihood relations. The analysis was based on individual data on external radiation dose, number of observation person-years and spontaneous incidence rate.

The authors believe that it is preferable to use individual information for estimating risks to minimize the impact of subjectivity and loss of information in grouping and stratification of data.

The logarithm of likelihood function L for the given sample is written as

(1)

where l is the parameter to determine (here the leukemia incidence rate); t is the period of follow up of a cohort member (in case of disease - time from start of follow-up to time of diagnosis, for a healthy member of cohort - time of monitoring the cohort); n is the number of cases for the observation period; N is the number of healthy members of the cohort considered in the analysis in the observation time.

The confidence intervals for the estimated parameters were found using the asymptotic properties of the likelihood function from equation (Handbook of applicable mathematics, 1984):

(2)

In estimation of risk coefficients the linear and linear-quadratic functions were used:

(3)

and . (4)

Here li0 is the spontaneous leukemia incidence rate averaged over the follow-up period corresponding to the age of the i-th member of the cohort. The value of the mean rate was determined from the following equation:

(5)

where liR is the age dependence of the spontaneous incidence rate; ui is age at exposure for the i-th member of the cohort. As spontaneous incidence rate we use the age dependence of the incidence rate for Russia in general (Aksel and Dvoirin, 1992); di is the external radiation dose for the i-th member of the cohort; ERR1Gy is the excess relative risks per unit dose.

Since the values of external radiation doses and dose rates are relatively low, we use a linear model to estimate the effect of dose rate on incidence rate under the assumption that the influence of these factors is additive:

. (6)

Here dr is dose rate [Gy/day]; k is the coefficient accounting for the difference of the spontaneous rate in the emergency workers cohort in the studied period from the population of Russia of corresponding age. In the model studied this coefficient is equal to the standardized incidence ratio (SIR) for spontaneous rate among unexposed emergency workers. The difference of coefficient k from unity can be due to the difference in how cases are registered (for example, emergency workers are subject to regular annual check-ups) and quality of diagnosis verification. It was assumed in calculations that this coefficient is the same in all age groups. Thus, to determine the risk only relative age distribution of spontaneous incidence rates is used.

The temporal trend of risk in the studied period is considered within the linear model (6) with the only difference in that g and dr have the meaning of change in risk per unit time and time after exposure, respectively.

The ratio ERR1Gy/a is the estimate of dose and dose rate factor (DDREF) in the considered dose range (0~0.25 Gy).

A question arises about the reliability of data on age distribution of spontaneous incidence rates. It is reasonable to assume that the distribution of spontaneous incidence rates for leukemia by age is rather a conservative value and is weakly dependent on geographic and ethnic attributes.

To verify this hypothesis and analyze the quality of Russian data within the above hypothesis we use the age functions of the distributions of leukemia incidence rates from the worlds largest cancer registries (Cancer Incidence in Five Continents, 1987). The distribution function fj was calculated from the formula below:

. (7)

umax-umin is the considered age range; l0k is the age distribution of the incidence rate in the registry selected as the control; i is the registry index.

Figure 6 shows the distribution function of normalized incidence rates by age at diagnosis for registries of USA (white), UK, Belarus and Russia (Cancer Incidence in Five Continents, 1987). The distribution is normalized by corresponding rates of the cancer registry selected as control (data for Russia in general). The distribution function was derived for males with the attained age of 20-70 years.

Figure 6. Distribution function of leukemia incidence (males) by attained age for different countries.

 

 

The results presented in Figure 6 confirm the assumption about the similarity of relative distributions of age incidence rates for leukemia in different countries and reliability of this characteristic in Russian data used as the control.

In this work we compared the radiation risks derived for the studied cohort of emergency workers with risks of radiogenic leukemia of all types in the cohort LSS (Life Span Study) of atomic bomb survivors in Japan (Preston et al., 1994). For comparison to be correct (the LSS cohort has a different age structure, other spontaneous incidence rates) the following approach was pursued. Preston et al., (1994) gives the following approximations of the spontaneous incidence rates and excess absolute risk for all leukemias and individual types for the LSS:

Leukemias of all types (ICD-9: 204-208) (designations are borrowed from (Preston et al., 1994)).

The spontaneous incidence rate

,

where a is attained age; g is the age at exposure.

Excess absolute rate EAR (10-4PY)

where d is dose (Sv); t is time after exposure.

To allow for the difference in the spontaneous incidence rates we passed from estimators of absolute risk to estimators of excess relative risk using the relation ERRJ(d,g,t)=EARJ(d,g,t)/lJ(g,g+t) (l is approximation of the spontaneous incidence rate of leukemia in the LSS cohort).

Since leukemias belong to rare diseases, the number of cases (C) can be described with a fairly good accuracy by:

. (8)

Summation is done for all members of the cohort in question using several parameters of model (3).

For the cohort in question C=27, the number of leukemias considered in the analysis. The expected number of leukemias can be derived by using the risk approximation ERRJ(di,gi,i) from the LSS cohort and data for each emergency worker from formula (8) with substitution of excess relative risk ERR by:

(9)

the mean value of risk over the follow-up interval (tl is the latent period).

Then the excess relative risk averaged over the studied period per unit dose for the whole cohort is determined according to (8) as follows:

. (10)

In estimation of the number of radiogenic leukemias the latent period of 2 years was taken.

 

Results

 

Based on the experience of Japanese studies and research in other countries suggesting no radiation dependence of chronic lymphocytic leukemia (CLL) (Preston et al., 1994) the analysis was performed both with inclusion and exclusion of such cases.

Results of estimating the model (3) parameters are presented in Table 5. For leukemia of all types the values of radiation risk are not statistically significant (P=0.04), given 95% confidence intervals. If CLL is excluded, the risk becomes statistically significant and equals 11.7 (3.3, 20.1 95%CI) per 1 Gy (P<0.001). The values of the coefficient k less than unity are explained by the fact that the leukemia cases considered were only those verified at the time of analysis (at the time when analysis was carried out the list of emergency workers with diseases also included 11 persons for whom the leukemia diagnosis had to be ascertained).

Table 5

Estimated risk of induction of radiogenic leukemia in the emergency workers cohort
(using data on spontaneous incidence rate in Russia)

 

Parameter

All leukemias (95% CI)

All leukemia excluding CLL (95% CI)

All leukemia (arrival in 1986-1987) (95% CI)

ERR/Gy

3.5 (-0.5, 7.5)

11.7 (3.3, 20.1)

10.2 (2.8, 17.4)

Coefficient k

0.7 (0.4, 0.9)

0.4 (0.2, 0.6)

0.4 (0.2, 0.6)

 

 

The risk of radiogenic leukemias becomes statistically significant for all types of leukemias, if the emergency workers exposed in 1988-1990 and receiving, on the average, lower dose than those exposed in 1986-1987 are excluded.

Results of calculations by the linear-quadratic model (4) indicate that in the considered range of doses and dose rates the influence of quadratic term is not significant (the coefficient value with linear term is 9.7 (1.69, 17.67). The level of significance of the linearity hypothesis is P=0.89. The value of the dose and dose rate factor DDREF=11.7/9.7=1.2.

Parameters of model (6) are presented in Table 6. Introduction of the dose rate factor has virtually not modified the value of the excess relative risk, which suggests weak influence of this factor on risk of induction of radiogenic cancers for the considered range of doses and dose rates. The significance level of the hypothesis indicates that the risk coefficient is not dependent on dose rate P=0.79. The value of the coefficient of risk sensitivity to dose rate is statistically insignificant.

 

Table 6

Estimated coefficients of risk sensitivity to dose and dose rate

 

Parameter

All leukemias excluding CLL (95% CI)

ERR/Gy

10.7 (2.2, 19.1)

Risk per Gy/day

43.7 (-213.4, 300.8)

 

 

Using the same model we estimated the temporal trend of excess relative risk in the considered time period. The calculation shows that the excess relative risk decreases with time (the hypothesis significance level suggests that the trend is absent P=0.02).

As can be seen from Figure 6, the age distribution of incidence rate by data of different cancer registries are similar and therefore risk was estimated using spontaneous incidence rate for different countries. Results of calculations are shown in Table 7. It can be seen that results of risk estimation are practically the same, no matter data which registry data were used in computation. The spontaneous incidence rate for the considered range of age and sex is similar.

 

 

Table 7

Estimated leukemia risks for emergency workers using data
on spontaneous incidence rate from different cancer registries

 

Registry

Russia

USA

Belarus

UK

ERR/Gy

3.5 (-0.5, 7.5)

3.6 (-0.5, 7.7)

3.7 (-0.4, 7.8)

3.8 (-0.4, 8.0)

Coefficient k

0.7 (0.4, 0.9)

0.5 (0.3, 0.7)

0.5 (0.3, 0.7)

0.7 (0.4, 1.0)

What is remarkable about the obtained result is that it demonstrates that incidence data can in principle be used from different registries which have an established system of data collection and verification and contain a large body of cancer data. This can be useful for analysis of data for small populations especially with rare diseases such as leukemia.

Using the approximants derived in the LSS cohort, the excess relative risk per unit dose averaged over the considered period for all types of leukemia was estimated. Likewise the dynamics of excess risk for the emergency workers cohort with time was calculated (Figure 7). The excess relative risk per 1 Gy is equal to 12.1 and differs from the value of 3.5 calculated with the data set under study. The expected cumulative number of cases, when using the Japanese risk coefficients, is C1=45.6 (the observed value is 27 cases). However, considering that there are virtually no CLL cases in the LSS cohort (Preston et al., 1994), the value 12.1 is consistent with 11.7 derived for the cohort of emergency workers with exclusion of this type of leukemia.

As follows from Figure 7, the excess relative risk decreases in the considered period. Over the entire period, the risk has decreased by a factor of 4.

Figure 7. Excess relative risk in the cohort of emergency workers as a function of time
after the accident (the dynamics is estimated using estimators (Preston et al., 1994)).

 

 

 

Discussion

 

The present work is a logical continuation of the Russian study of leukemia incidence rate among emergency workers (Ivanov et al., 1997a; Ivanov et al., 1997b). Obviously, this issue remains topical, as emergency workers, on the average, received higher radiation doses than the population of the affected regions and radiogenic leukemia is the first indicator of long-term radiation effects. A study by Ivanov et al., (1997a) has been conducted for the entire cohort of emergency workers using an external control, a corresponding age category of the Russian population. It is known that use of an external control can lead to a shift in risk estimates due to differences in the systems of collection, registration and verification of diagnoses in the study and reference groups. An estimation of risk was made under a cautious assumption that the excess of the observed incidence rate above the control is likely to be due to the radiation factor (Ivanov et al., 1997a). Thus, the primary goal of Ivanovs study was to identify the current trends in leukemia incidence rate among the emergency workers and bring the subject to the attention of researchers, rather than to estimate leukemia risk.

In another study by Ivanov et al., (1997b) the case-control approach has been taken to analyze risks. The analysis has not revealed statistically significant risks, but the positive trend in leukemia incidence rate as a function of an external radiation dose was established. It cannot be ruled out that no significant risks were found because application of the case-control methodology for the cohort of emergency workers is rather problematic, since direct dose measurements were limited and maximum permissible levels are limited.

The information about the cohort of emergency workers used in the presented analysis is reliable. The data used are the verified RNMDR data and the system of data collection and verification have been tuned up (it has taken some time to fix the operation of a large dynamic information system of RNMDR including more than 170 thousand persons). The analysis uses, to the extent possible, a priori information on leukemia incidence rate.

When all types of radiogenic leukemia are included the increase is not statistically significant for the entire cohort of emergency workers, given the confidence intervals of 95%. This is most probably because of the relatively small number of cases that were studied (27) and a possible shift in the estimate because of allowing for chronic lymphocytic leukemia, for which no dose response has ever been established. Exclusion of CLL from the analysis results in increase in the risk and the risk becomes statistically significant. This result confirms the modern concept that CLLs are clearly not dose dependent.

The risk of radiogenic leukemia becomes statistically significant for all types of leukemia with the exclusion of emergency workers exposed in 1988-1990 who received, on the average, lower doses than those exposed in 1986-1987.

The risk model that was studied using a priori information on spontaneous incidence rate allows use of individual information and immediate estimation of two main characteristics, the risk coefficient and standardized incidence ratio ¾ the difference in the incidence rate in the studied cohort from the national level (or the reference group). It has been shown that information of other cancer registries having a large volume of data and established systems of collection and verification of leukemia data such as registries of the USA or UK can be used for risk analysis with good accuracy. The gained experience may be useful for analysis of incidence rates of rare diseases such as leukemia in small populations.

The data set used in the analysis is adequately described by a linear dose function, the significance level of the hypothesis is P=0.89 and as a consequence the value of the dose factor and dose rate DDREF is close to unity.

In the considered range of doses (to 0.25 Gy) and dose rates (to 0.01 Gy/day) the effect of the dose rate factor on radiogenic cancer risk is not statistically significant. The study was carried out within the linear model. This approximation seems justified as the values of doses and dose rates received by emergency workers are relatively low.

The risks of radiogenic leukemias in the emergency workers cohort were compared with the risks for the same cohort calculated using the estimators derived for the LSS cohort. The risk estimators are a function of sex, age at exposure and time since exposure, which makes correct comparison possible. The excess relative risk per unit dose has been estimated to be 12.1. Since the number of CLL in the LSS cohort is small (due to geographic and ethnic features of the cohort), the approximations presented by Preston et al., (1994) for all types of leukemia virtually correspond to the risk derived with exclusion of CLL. Then it may be more adequate to compare the risk value of 12.1 with the risk value of 11.7 derived in the regression analysis with exclusion of CLL.

Considering that the above values of the risk coefficients are similar and the temporal trends are alike, it can be argued that the risk model presented by Preston et al., (1994) adequately describes leukemia incidence rate in the emergency workers cohort.

The derived risk value of 11.7 (excluding chronic lymphocytic leukemia) suggests that at the mean dose of 0.1 Gy the attributive risk is about 50%, i.e. half of the diagnosed cases are radiation-induced.

The results of the above analysis lead us to conclude that the dose factor has an effect on leukemia incidence rate among emergency workers living in Russia. Growth of the leukemia rate among emergency workers is probably the first indication of distant consequences of the population exposure after the Chernobyl accident.

Main conclusions:

1.     For all types of lymphocytic leukemia the radiation risk coefficients for the time of monitoring the cohort of emergency workers from 1986 to 1997 were not statistically significant. The value of the excess relative risk is 3.5 (-0.5, 7.5 95% CI).

2.     Exclusion of chronic lymphocytic leukemia increases the confidence of radiation risk values and makes it statistically significant. The value of ERR [Gy]-1 is 11.7 (3.3, 20.1 95% CI).

3.     The risk of radiogenic leukemia is statistically significant for all types of leukemia and equals 10.2 (2.8, 17.4 95% CI), if we exclude emergency workers exposed in 1988-1990 who received lower dose than those exposed in 1986-1987.

4.     The impact of the dose rate factor for the considered range of doses and dose rates is not statistically significant.

5.     The attributive risk of inducing radiogenic leukemia (excluding chronic lymphocytic leukemia) is 50%. This means that radiation may be a factor in causing disease in half of the diagnosed cases of leukemia.

6.     The excess relative risk for all types of leukemia in the studied period is 3.5. This is in agreement with the risk estimate of 3.4 calculated using the estimators derived for the cohort LSS.

 

References

 

Aksel E., Dvoirin V. Statistics of Malignant Neoplasms. - Moscow: VONTS AMN SSSR, 1992 (in Russian).

Cancer Incidence in Five Continents. D.M.Parkin et al. (Eds.), Vol. VI, IARC Scientific Publication. - Lyon, 1987.

Cardis E., Gilbert E.S., Carpenter L., Howe G., Kato I., Armstrong B.K., Beral V., Cowper G., Douglas A., Fix J., Fry S.A., Kaldor J., Lave C., Salmon L., Smith P.G., Voelz G.L., Wiggs L.D. Effects of low doses and low doses rates of external ionizing radiation: Cancer mortality among nuclear workers in three countries//Radiat. Res. - 1995. - V. 143. - P. 117-132.

Handbook of Applicable Mathematics. W.Ledermann (Ed.), Vol. VI Statistics, Part A. - New York: John Wiley&Sons Ltd, 1984.

Ivanov V.(a), Tsyb A., Gorsky A., Maksyutov M., Rastopchin E., Konogorov A., Korelo A., Biryukov A. Matyash V. Leukemia and thyroid cancer in emergency workers of the Chernobyl accident: estimation of radiation risks (1986-1995)//Radiat. Environ. Biophys. - 1997. - V. 36. - P. 9-16.

Ivanov V.K.(b), Tsyb A.F., Konogorov A.P., Rastopchin E.M., Khait S.E. Case-control analysis of leukaemia among Chernobyl accident emergency workers residing in the Russian Federation, 1986-1993//J. Radiol. Prot. - 1997. - V. 17. - P.137-157.

Preston D., Kusumi S., Tomonaga M., Izumi S., Ron E., Kuramoto A., Kamada N., Dohy H., Matsuo T., Nonaka H., Thompson D., Soda M., Mabuchi K. Cancer incidence in atomic bomb survivors. Part III: Leukemia and multiple myeloma, 1950-1987//Radiat. Res. - 1994. - V. 137. - P. S94.