- Email: [email protected]
Cancer mortality around French nuclear sites
ELSEVIER
Cancer Mortality JEAN-MARC
around French Nuclear Sites
HATTCHOUEL,
MD,
AGNES LAPLANCHE,
MD,
AND CATHERINE
HILL
This study was designed to investigate cancer mortality in the population aged 0 to 64 years residing around the 13 main French nuclear sites in operation before 1985. Five hundred and three communes located within 16 km of the installation were identified and their populations were followed from 1968 to 1989. A total of 8,970,OCXJ person-years of observation was accumulared. The number of cancer deaths and the number of deaths for cancers possibly related zo radiation observed in these communes were compared to national mortality rates. There wa-s no difference in overall cancer mortality or in the risk of mortality by cancer site except for breast cancer, for which a deficit was observed in the vicinity of nuclear sites. After correction for the multiplicity of tests, this difference was not significant. Our study showed no excess cancer mortality in the population aged 0 to 64 years residing around French nuclear sites. Ann Epidemiol 1996;6: 126-129. KEY
WORDS:
Cancer, nuclear installations,
mortality,
INTRODUCTION Reports from the United Kingdom described increases in leukemia and lymphoma risks in children living near nuclear installations (l-3). Findings from studies around individual nuclear sites were confirmed by the analysis of cancer mortality around 15 nuclear plants in England and Wales (4,5). In the United States, a study of the population around 62 nuclear sites operating before 1982 reported no excess mortality from leukemia or from solid tumors in children or in the total population (6). Similarly, studies in Canada (7) and Germany (8) reported no excess of leukemia in the vicinity of nuclear installations. We report here the results of a study of leukemia and solid tumor mortality between 1968 and 1989 in the French population living near 13 nuclear installations, for the age groups 0 to 24 and 25 to 64 years.
MATERIALS
AND
METHODS
The 13 installations operating before 1985 were studied (Figure 1). We considered as exposed the population residing in one of the 503 administrative units-called “communes”located within 16 km of the installation. From the Institut National de la Sand et de la Recherche Medicale (INSERM, French National Institute for Health
From the Department of Bicscatisticsand Epidemiology and INSERM U351, Institut Gustave Roussy, Villejuif, France. Address reprint requests to: Agn& Laplanche, MD, D.+partemenr de Biostatistique ef d’Epid~miologie. Institut Gusrave Roussy, 94805 Villejuif, France. Received February 3, 1995; revised June 19, 1995; accepted July 12, 1995. 0 1996 by Elsevier Science Inc. 655 Avenue of the Americas, New York,
NY
10010
ionizing radiation.
and Medical Research, joint service no. 8), we obtained the cause of each death in the population aged 0 to 64 years occurring between 1968 and 1989 by year, sex, and 5-year age groups. The underlying cause of each death was coded according to the International Classification of Diseases (ICD), eighth revision before 1979, and ninth revision thereafter (9, 10). The cancer sites studied are described in Table 1. Census data by commune were obtained from the Institut National de la Statistique et des Etudes Economiques (INSEE, French National Institute of Economic and Statistical Information) for the four censuses that took place in 1968, 1975, 1982, and 1990. The population at risk was estimated from these data for the period 1968 to 1989 according to a method described previously (11, 12). For the 10 sites that started operating in 1968 or afterward, the study period was defined as beginning on January 1 of the year after the year of first operation. For the three sites that started operating before 1968, the study period began on January 1, 1968. To test for a possible increase in cancer mortality between the ages of 0 and 64 years around French nuclear sites, the observed number of deaths (0) was compared to the number expected(E) on the basis of national rates (13,14). Standardized mortality ratios (SMR = 100 x O/E) were compared to 100 by tests assuming a Poisson distribution (15). All significance tests were two sided.
RESULTS During the period under study, a total of 8,970,OOO personyears of observation was accumulated in the population aged 0 to 64 years residing in the exposed communes. Tables
SSDI
1047-2797/96/$15.00 1047-2797(95)00130-l
AEP Vol. 6, No. 2 March 1996: 126-129
CANCER MORTALITY
Harxhouel CI al. AROUND FRENCH NUCI.EAR SITES
127
lower than expected. Taking into account multiple testing, these results are not statistically significant.
DISCUSSION Our study showed no excess mortality in the population aged 0 to 64 years residing near French nuclear sites. The causes of deaths studied included leukemia but also other cancers possibly related to radiation. These results confirm findings from previous studies reporting no excessleukemia mortality in the population aged 0 to 24 years living around La Hague (16-l@, or in the population residing in the vicinity of six (11) or 13 (12) nuclear facilities that included La Hague. This study relied on mortality data. We used mortality rather than incidence data because there is no national cancer registry in France, and the local registries that exist do not include the areas studied. The availability of incidence data would represent a substantial increase in power, particularly when studying cancers of the thyroid and breast, Hodgkin’s disease, and childhood leukemias, for which survival is fairly good. A limitation of our study is the lack of control for potential confounding factors, such as smoking habits, alcohol consumption, and so on. For instance, there may be systematic differences in smoking habits between the populations residing in the vicinity of nuclear sites, which are mostly rural, and the general population. This could explain the deficit in lung cancer mortality observed among females. An excess risk of leukemia after exposure to radiation has been observed with a minimum latent period of 2 years and much longer latent periods are expected for other cancer sites (19). If discharges from nuclear facilities were responsible for an increased occurrence of leukemia, excess cases (and probably deaths) would not be expected rn be observed
FIGURE 1. Nuclear sites and year of first operation. Black squares indicate reprocessing; black circles, production of electricity.
1 and 2 give, by cancer site, the number of deaths observed and expected, and the SMR with 95% confidence intervals (95% CIs) for the two broad age groups considered, for males and females, respectively. For males, the number of leukemia deaths among those under 25 years old and the number of myeloma deaths in the 25- to 64-year age group were significantly lower than expected; the total number of cancers in the 25- to 64-year age group was higher than expected. For females in the 25- to 64-year age group, the numbers of breast and lung cancer deaths were significantly
TABLE 1. Number of male deaths observed (0) and expected (E), standardized mortality ratio (SMR = 100 x CjEi, and 95% confidence interval (95% CI) Age 25-64 y
Age O-24 y Causes of death (ICD9 codes) Lung and pleura (162, 163)
Bone (170) Breast (175) Brain (191, 192) Thyroid (193) Hodgkin’s disease (201) Non-Hodgkin’s lymphomas (200, 202) Multiple myeloma (203) Leukemia (204-208) All cancers (140 -208) Person-y * P < 0.05.
E
0
SMR (95% CI)
3
2.2
10
11.0
91 (43-167)
0 9 1 6
0.1 16.2 0.1 4.3
0 56 (25-105) 844 (1 l-4698) 141 (51-307)
14 0 36 118
139 (28-406)
14.0 100 (55-168) 0.3 0 51.3 70 (49-97) 135.7 87 (72-104) 2,128,OOO
E
SMR (95% CI)
1207 48 16 114 7 31
1166.4 42.1 9.6 105.3 11.7 34.8
103 (98-109) 114 (84-151) 166 (95-270) 108 (89-130) 60 (24-124) 8Y (60- I26i
85 20 126 4918
80.4 106 (84-131) 32.1 62 (38-96)” 129.0 98 (81-116) 4768.2 103 (100-106) 2,475,OOO
0
1 ClLil .-__.-
-_--E
-SMR (95% CI)
1210 58 ih 123 8
: 168.6 53, I 9,; 121.5 il.?
104 (98-l 10) 109 (83-141) Ihi (94-268) 101 W-121) 68 (29-l 34)
?7
w. !
oi 167--l 30)
09
“4.i ;2.4 180.3
105 (85-128) 62 (38-95) 90 Q-105) 101 (loo-106)
0
20 162 5036
1903.3
4,~i’i,ocO -~
128
Hattchouel et al. CANCER MORTALITY
AROUND
TABLE
2. Number of female deaths observed and 95% confidence interval (95% CI)
(0) and expected
(E), standardized
Lung and pleura (162, 163) Bone (170) Breast (174) Brain (191, 192) Thyroid (193) Hodgkin’s disease (201) Non-Hodgkin’s lymphomas (200, 202) Multiple myeloma (203) Leukemia (204-208) All cancers (140-208) Person-y
0 0 9 0 8 0 5 7 0 33 87
mortality
ratio (SMR
= 100 x O/E), Total
Age 25-64 y
Age O-24 y Causes of death (lCD9 codes)
AEP Vol. 6, No. 2 March 19%: 126-129
FRENCH NUCLEAR SITES
0
E
SMR (95% CI)
0.9 7.2 1.1 11.8 0.1 2.8
0 126 (58-240) 0 68 (29-134) 0 177 (57-413)
95 23 557 68 9 17
6.1 115 (46-238) 0.1 0 34.9 95 (65-133) 91.3 95 (76-117) 2,003,OOO
51 25 74 2344
E
SMR (95% CI)
0
80 (65-98) 150 (95-225) 88 (81-96) 108 (84-237) 67 (31-127) 97 (57-155)
95 32 557 76 9 22
43.7 117 (87-153) 24.7 101 (66-149) 87.5 85 (66-106) 2335.5 100 (96-105) 2,364,OOO
58 25 107 2431
118.4 15.3 630.0 62.8 13.4 17.5
E 119.3 22.5 631.1 74.6 13.5 20.3
SMR (95% Cl) 80 (64-97)” 142 (97-201) 88 (81-96) 102 (80-128) 66 (30-126) 108 (68-164)
116 (88-151) 49.8 101 (65-149) 24.8 87 (72-106) 122.4 2426.8 100 (96-104) 4,367,OCQ
aP < 0.05.
for several years after the beginning of operation. Our study had a follow-up time varying between 5 and 22 years according to the installation, which may not be sufficient to exclude long-term effects. Our study provided no data on the risk among nuclear workers, although some may have resided within 16 km of the installation. A recent study of 96,000 workers in Canada, United Kingdom, and the United States observed an excess risk of death from leukemia of 2.2 per sievert (20). The power of our study is reasonable: With an expected number of deaths around installations equal to 200, the probability of detecting an increase of 10% is 40%, and the probability of detecting an increase of 25% is 95%, with a type I error of 5% (15). Such an increase of 25% would probably require a very substantial radiation dose. Therefore, we cannot exclude the possibility of smaller increases. We used the same methodology as Forman and coworkers (4) and found no excess mortality due to leukemia or other cancers around reprocessing or nuclear power plants in France, contrary to their results for leukemia. We conclude that no excess cancer mortality was observed in the vicinity of the nuclear sites studied.
We thank Florent de Vathaire and Serge Koscielny for methodologic advice and Lorna Saint-Ange for the linguistic revision of the manuscript. This work was partly supported by a grant from Commission of European Communities (CEC)/National Radiological Protection Board (NRPB) (contract 920064) and EDF.
REFERENCES
dren born to mothers resident in Seascale, West Cumbria (birth cohort), BMJ. 1987;295:822-827. 3. Darby SC, Doll R. Fallout, radiation doses near Dounreay, and childhood leukaemia, BMJ. 1987;294:603-607. 4. Forman D, Cook-Mozaffari P, Darby S, et al. Cancer near nuclear installations, Nature. 1987;329:499-505. 5. Cook-Mozaffari PJ, Darby SC, Doll R, et al. Geographical variation in mortality from leukaemia and other cancers in England and Wales in relation to proximity to nuclear installations, 1969-78, Br J Cancer. 1989;59:476-485. 6. Jablon S, Hrubec Z, Boice JD. Cancer in populations living near nuclear facilities: A survey of mortality nationwide and incidence in two states, JAMA. 1991;265:1403-1408. 7. McLaughlin JR, Clarke EA, Nishri ED, Anderson TW. Childhood leukemia in the vicinity of Canadian nuclear facilities, Cancer Causes Control. 1993;4:51-58. 8. Michaelis J, Keller B, Haaf G, Kaatsch P. Incidence of childhood malignancies in the vicinity of West German nuclear power plants, Cancer Causes Control. 1992;3:255-263. 9. World Health Organization (WHO). International Disease. 8th rev. Geneva: WHO; 1%5.
Classification of
10. World Health Organization (WHO). International Disease. 9th rev. Geneva: WHO; 1978.
Classification of
11. Hill C, Laplanche A. Overall mortality and cancer mortality around French nuclear sites, Nature. 1990;347:755-757. 12. Hattchouel JM, Laplanche A, Hill C. Leukaemia mortality French nuclear sites, Br J Cancer. 1995;71:651-653.
around
13. Hill C, Benhamou E, Doyon F, Flamant R. Evolution de la mortalite par cancer en France, 1950-1985. Paris: Editions INSERM; 1989. 14. Hill C, Koscielny S, Doyon F, Benhamou E. Evolution de la mortalite par cancer en France, 1950-1990, mise a jour 1986-1990. Paris: Editions INSERM; 1993. 15. Breslow NE, Day NE. Statistical Methods in Cancer Research, v. IIThe Design and Analysis of Cohort Studies. IARC scientific publication no. 82. Lyon: International Agency for Research on Cancer; 1987. 16. Dousset M. Cancer mortality around La Hague nuclear facilities, Health Phys. 1989;56:875-884.
1. Gardner M], Winter PD. Mortality in Cumberland during 1959-78 with reference to cancer in young people around Winscale, Lancet. 1984;1:216-217.
17. Vie1 JF, Richardson ST. Childhood leukaemia around the La Hague nuclear waste reprocessing plant, BMJ. 1990;300:580-581.
2. Gardner MJ, Hall A]. Downes S, Terre11 JD. Follow up study of chil-
18. Vie1 JF, Richardson S, Dane1 P, et al. Childhood leukemia incidence
AEP Vol. 6, No. 2 March 1996: 126-129
in the vicinity of La Hague nuclear-waste reprocessing facility (France), Cancer Causes Control. 1993;4:341-343. 19. Committee on the Biological Effects of Ionizing Radiation (BEIR V). Health Effects of Exposure to Low Levels of Ionizing Radiation. Washington, DC: National Academy Press; 1990.
CANCER MORTALITY
AROUND
Hanchouel er al. FRENCH NUCLEAR SITES
129
20. IARC study group on cancer risk among nuclear industry workers. Direct estimates of cancer mortality due to low doses of kmising radiations: An international study, Lancet. 1994;344:1039-1043.
Cancer Mortality JEAN-MARC
around French Nuclear Sites
HATTCHOUEL,
MD,
AGNES LAPLANCHE,
MD,
AND CATHERINE
HILL
This study was designed to investigate cancer mortality in the population aged 0 to 64 years residing around the 13 main French nuclear sites in operation before 1985. Five hundred and three communes located within 16 km of the installation were identified and their populations were followed from 1968 to 1989. A total of 8,970,OCXJ person-years of observation was accumulared. The number of cancer deaths and the number of deaths for cancers possibly related zo radiation observed in these communes were compared to national mortality rates. There wa-s no difference in overall cancer mortality or in the risk of mortality by cancer site except for breast cancer, for which a deficit was observed in the vicinity of nuclear sites. After correction for the multiplicity of tests, this difference was not significant. Our study showed no excess cancer mortality in the population aged 0 to 64 years residing around French nuclear sites. Ann Epidemiol 1996;6: 126-129. KEY
WORDS:
Cancer, nuclear installations,
mortality,
INTRODUCTION Reports from the United Kingdom described increases in leukemia and lymphoma risks in children living near nuclear installations (l-3). Findings from studies around individual nuclear sites were confirmed by the analysis of cancer mortality around 15 nuclear plants in England and Wales (4,5). In the United States, a study of the population around 62 nuclear sites operating before 1982 reported no excess mortality from leukemia or from solid tumors in children or in the total population (6). Similarly, studies in Canada (7) and Germany (8) reported no excess of leukemia in the vicinity of nuclear installations. We report here the results of a study of leukemia and solid tumor mortality between 1968 and 1989 in the French population living near 13 nuclear installations, for the age groups 0 to 24 and 25 to 64 years.
MATERIALS
AND
METHODS
The 13 installations operating before 1985 were studied (Figure 1). We considered as exposed the population residing in one of the 503 administrative units-called “communes”located within 16 km of the installation. From the Institut National de la Sand et de la Recherche Medicale (INSERM, French National Institute for Health
From the Department of Bicscatisticsand Epidemiology and INSERM U351, Institut Gustave Roussy, Villejuif, France. Address reprint requests to: Agn& Laplanche, MD, D.+partemenr de Biostatistique ef d’Epid~miologie. Institut Gusrave Roussy, 94805 Villejuif, France. Received February 3, 1995; revised June 19, 1995; accepted July 12, 1995. 0 1996 by Elsevier Science Inc. 655 Avenue of the Americas, New York,
NY
10010
ionizing radiation.
and Medical Research, joint service no. 8), we obtained the cause of each death in the population aged 0 to 64 years occurring between 1968 and 1989 by year, sex, and 5-year age groups. The underlying cause of each death was coded according to the International Classification of Diseases (ICD), eighth revision before 1979, and ninth revision thereafter (9, 10). The cancer sites studied are described in Table 1. Census data by commune were obtained from the Institut National de la Statistique et des Etudes Economiques (INSEE, French National Institute of Economic and Statistical Information) for the four censuses that took place in 1968, 1975, 1982, and 1990. The population at risk was estimated from these data for the period 1968 to 1989 according to a method described previously (11, 12). For the 10 sites that started operating in 1968 or afterward, the study period was defined as beginning on January 1 of the year after the year of first operation. For the three sites that started operating before 1968, the study period began on January 1, 1968. To test for a possible increase in cancer mortality between the ages of 0 and 64 years around French nuclear sites, the observed number of deaths (0) was compared to the number expected(E) on the basis of national rates (13,14). Standardized mortality ratios (SMR = 100 x O/E) were compared to 100 by tests assuming a Poisson distribution (15). All significance tests were two sided.
RESULTS During the period under study, a total of 8,970,OOO personyears of observation was accumulated in the population aged 0 to 64 years residing in the exposed communes. Tables
SSDI
1047-2797/96/$15.00 1047-2797(95)00130-l
AEP Vol. 6, No. 2 March 1996: 126-129
CANCER MORTALITY
Harxhouel CI al. AROUND FRENCH NUCI.EAR SITES
127
lower than expected. Taking into account multiple testing, these results are not statistically significant.
DISCUSSION Our study showed no excess mortality in the population aged 0 to 64 years residing near French nuclear sites. The causes of deaths studied included leukemia but also other cancers possibly related to radiation. These results confirm findings from previous studies reporting no excessleukemia mortality in the population aged 0 to 24 years living around La Hague (16-l@, or in the population residing in the vicinity of six (11) or 13 (12) nuclear facilities that included La Hague. This study relied on mortality data. We used mortality rather than incidence data because there is no national cancer registry in France, and the local registries that exist do not include the areas studied. The availability of incidence data would represent a substantial increase in power, particularly when studying cancers of the thyroid and breast, Hodgkin’s disease, and childhood leukemias, for which survival is fairly good. A limitation of our study is the lack of control for potential confounding factors, such as smoking habits, alcohol consumption, and so on. For instance, there may be systematic differences in smoking habits between the populations residing in the vicinity of nuclear sites, which are mostly rural, and the general population. This could explain the deficit in lung cancer mortality observed among females. An excess risk of leukemia after exposure to radiation has been observed with a minimum latent period of 2 years and much longer latent periods are expected for other cancer sites (19). If discharges from nuclear facilities were responsible for an increased occurrence of leukemia, excess cases (and probably deaths) would not be expected rn be observed
FIGURE 1. Nuclear sites and year of first operation. Black squares indicate reprocessing; black circles, production of electricity.
1 and 2 give, by cancer site, the number of deaths observed and expected, and the SMR with 95% confidence intervals (95% CIs) for the two broad age groups considered, for males and females, respectively. For males, the number of leukemia deaths among those under 25 years old and the number of myeloma deaths in the 25- to 64-year age group were significantly lower than expected; the total number of cancers in the 25- to 64-year age group was higher than expected. For females in the 25- to 64-year age group, the numbers of breast and lung cancer deaths were significantly
TABLE 1. Number of male deaths observed (0) and expected (E), standardized mortality ratio (SMR = 100 x CjEi, and 95% confidence interval (95% CI) Age 25-64 y
Age O-24 y Causes of death (ICD9 codes) Lung and pleura (162, 163)
Bone (170) Breast (175) Brain (191, 192) Thyroid (193) Hodgkin’s disease (201) Non-Hodgkin’s lymphomas (200, 202) Multiple myeloma (203) Leukemia (204-208) All cancers (140 -208) Person-y * P < 0.05.
E
0
SMR (95% CI)
3
2.2
10
11.0
91 (43-167)
0 9 1 6
0.1 16.2 0.1 4.3
0 56 (25-105) 844 (1 l-4698) 141 (51-307)
14 0 36 118
139 (28-406)
14.0 100 (55-168) 0.3 0 51.3 70 (49-97) 135.7 87 (72-104) 2,128,OOO
E
SMR (95% CI)
1207 48 16 114 7 31
1166.4 42.1 9.6 105.3 11.7 34.8
103 (98-109) 114 (84-151) 166 (95-270) 108 (89-130) 60 (24-124) 8Y (60- I26i
85 20 126 4918
80.4 106 (84-131) 32.1 62 (38-96)” 129.0 98 (81-116) 4768.2 103 (100-106) 2,475,OOO
0
1 ClLil .-__.-
-_--E
-SMR (95% CI)
1210 58 ih 123 8
: 168.6 53, I 9,; 121.5 il.?
104 (98-l 10) 109 (83-141) Ihi (94-268) 101 W-121) 68 (29-l 34)
?7
w. !
oi 167--l 30)
09
“4.i ;2.4 180.3
105 (85-128) 62 (38-95) 90 Q-105) 101 (loo-106)
0
20 162 5036
1903.3
4,~i’i,ocO -~
128
Hattchouel et al. CANCER MORTALITY
AROUND
TABLE
2. Number of female deaths observed and 95% confidence interval (95% CI)
(0) and expected
(E), standardized
Lung and pleura (162, 163) Bone (170) Breast (174) Brain (191, 192) Thyroid (193) Hodgkin’s disease (201) Non-Hodgkin’s lymphomas (200, 202) Multiple myeloma (203) Leukemia (204-208) All cancers (140-208) Person-y
0 0 9 0 8 0 5 7 0 33 87
mortality
ratio (SMR
= 100 x O/E), Total
Age 25-64 y
Age O-24 y Causes of death (lCD9 codes)
AEP Vol. 6, No. 2 March 19%: 126-129
FRENCH NUCLEAR SITES
0
E
SMR (95% CI)
0.9 7.2 1.1 11.8 0.1 2.8
0 126 (58-240) 0 68 (29-134) 0 177 (57-413)
95 23 557 68 9 17
6.1 115 (46-238) 0.1 0 34.9 95 (65-133) 91.3 95 (76-117) 2,003,OOO
51 25 74 2344
E
SMR (95% CI)
0
80 (65-98) 150 (95-225) 88 (81-96) 108 (84-237) 67 (31-127) 97 (57-155)
95 32 557 76 9 22
43.7 117 (87-153) 24.7 101 (66-149) 87.5 85 (66-106) 2335.5 100 (96-105) 2,364,OOO
58 25 107 2431
118.4 15.3 630.0 62.8 13.4 17.5
E 119.3 22.5 631.1 74.6 13.5 20.3
SMR (95% Cl) 80 (64-97)” 142 (97-201) 88 (81-96) 102 (80-128) 66 (30-126) 108 (68-164)
116 (88-151) 49.8 101 (65-149) 24.8 87 (72-106) 122.4 2426.8 100 (96-104) 4,367,OCQ
aP < 0.05.
for several years after the beginning of operation. Our study had a follow-up time varying between 5 and 22 years according to the installation, which may not be sufficient to exclude long-term effects. Our study provided no data on the risk among nuclear workers, although some may have resided within 16 km of the installation. A recent study of 96,000 workers in Canada, United Kingdom, and the United States observed an excess risk of death from leukemia of 2.2 per sievert (20). The power of our study is reasonable: With an expected number of deaths around installations equal to 200, the probability of detecting an increase of 10% is 40%, and the probability of detecting an increase of 25% is 95%, with a type I error of 5% (15). Such an increase of 25% would probably require a very substantial radiation dose. Therefore, we cannot exclude the possibility of smaller increases. We used the same methodology as Forman and coworkers (4) and found no excess mortality due to leukemia or other cancers around reprocessing or nuclear power plants in France, contrary to their results for leukemia. We conclude that no excess cancer mortality was observed in the vicinity of the nuclear sites studied.
We thank Florent de Vathaire and Serge Koscielny for methodologic advice and Lorna Saint-Ange for the linguistic revision of the manuscript. This work was partly supported by a grant from Commission of European Communities (CEC)/National Radiological Protection Board (NRPB) (contract 920064) and EDF.
REFERENCES
dren born to mothers resident in Seascale, West Cumbria (birth cohort), BMJ. 1987;295:822-827. 3. Darby SC, Doll R. Fallout, radiation doses near Dounreay, and childhood leukaemia, BMJ. 1987;294:603-607. 4. Forman D, Cook-Mozaffari P, Darby S, et al. Cancer near nuclear installations, Nature. 1987;329:499-505. 5. Cook-Mozaffari PJ, Darby SC, Doll R, et al. Geographical variation in mortality from leukaemia and other cancers in England and Wales in relation to proximity to nuclear installations, 1969-78, Br J Cancer. 1989;59:476-485. 6. Jablon S, Hrubec Z, Boice JD. Cancer in populations living near nuclear facilities: A survey of mortality nationwide and incidence in two states, JAMA. 1991;265:1403-1408. 7. McLaughlin JR, Clarke EA, Nishri ED, Anderson TW. Childhood leukemia in the vicinity of Canadian nuclear facilities, Cancer Causes Control. 1993;4:51-58. 8. Michaelis J, Keller B, Haaf G, Kaatsch P. Incidence of childhood malignancies in the vicinity of West German nuclear power plants, Cancer Causes Control. 1992;3:255-263. 9. World Health Organization (WHO). International Disease. 8th rev. Geneva: WHO; 1%5.
Classification of
10. World Health Organization (WHO). International Disease. 9th rev. Geneva: WHO; 1978.
Classification of
11. Hill C, Laplanche A. Overall mortality and cancer mortality around French nuclear sites, Nature. 1990;347:755-757. 12. Hattchouel JM, Laplanche A, Hill C. Leukaemia mortality French nuclear sites, Br J Cancer. 1995;71:651-653.
around
13. Hill C, Benhamou E, Doyon F, Flamant R. Evolution de la mortalite par cancer en France, 1950-1985. Paris: Editions INSERM; 1989. 14. Hill C, Koscielny S, Doyon F, Benhamou E. Evolution de la mortalite par cancer en France, 1950-1990, mise a jour 1986-1990. Paris: Editions INSERM; 1993. 15. Breslow NE, Day NE. Statistical Methods in Cancer Research, v. IIThe Design and Analysis of Cohort Studies. IARC scientific publication no. 82. Lyon: International Agency for Research on Cancer; 1987. 16. Dousset M. Cancer mortality around La Hague nuclear facilities, Health Phys. 1989;56:875-884.
1. Gardner M], Winter PD. Mortality in Cumberland during 1959-78 with reference to cancer in young people around Winscale, Lancet. 1984;1:216-217.
17. Vie1 JF, Richardson ST. Childhood leukaemia around the La Hague nuclear waste reprocessing plant, BMJ. 1990;300:580-581.
2. Gardner MJ, Hall A]. Downes S, Terre11 JD. Follow up study of chil-
18. Vie1 JF, Richardson S, Dane1 P, et al. Childhood leukemia incidence
AEP Vol. 6, No. 2 March 1996: 126-129
in the vicinity of La Hague nuclear-waste reprocessing facility (France), Cancer Causes Control. 1993;4:341-343. 19. Committee on the Biological Effects of Ionizing Radiation (BEIR V). Health Effects of Exposure to Low Levels of Ionizing Radiation. Washington, DC: National Academy Press; 1990.
CANCER MORTALITY
AROUND
Hanchouel er al. FRENCH NUCLEAR SITES
129
20. IARC study group on cancer risk among nuclear industry workers. Direct estimates of cancer mortality due to low doses of kmising radiations: An international study, Lancet. 1994;344:1039-1043.