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A comparative study on thyroid diseases among children in Gomel region, Belarus
International Congress Series 1234 (2002) 121 – 126
A comparative study on thyroid diseases among children in Gomel region, Belarus Yoshisada Shibata a,*, Vladimir B. Masyakin b, Galina D. Panasyuk b, Svetlana P. Gomanova c, Vladimir N. Arkhipenko b, Kiyoto Ashizawa d, Masahiro Ito e, Noboru Takamura a, Shunichi Yamashita a a
Atomic Bomb Disease Institute, Nagasaki University School of Medicine, 1-12-4 Sakamoto, Nagasaki 852-8523, Japan b Gomel Specialized Medical Dispensary, Gomel, Belarus c Mogilev Regional Medical Diagnostic Center, Mogilev, Belarus d The First Department of Internal Medicine, Nagasaki University School of Medicine, Nagasaki, Japan e Department of Clinical Laboratory, National Nagasaki Medical Center, Nagasaki, Japan
Abstract A study aimed at comparing the prevalence of thyroid diseases between children born before and after the accident was outlined with emphasis on rationale and design of the study. In the study, a total of 21 601 children in Gomel city and four districts in the neighborhood of Gomel city were examined from February 1998 to December 2000. There were 9720 children born from January 1, 1983 to April 26, 1986 (Group I), 2409 children born from April 27, 1986 to December 31, 1986 and 9472 children born from January 1, 1987 to December 31, 1989 (Group III). Out of the examined children, 32 (0.15%) thyroid cancers were found, among whom 31 were in Group I and one was in Group II, while no cases in Group III. Our findings demonstrate the likelihood that short-lived radioactive fallout due to the Chernobyl accident induced thyroid cancer in children living near Chernobyl. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Chernobyl accident; Causation; Epidemiology; Short-lived fallout; Thyroid cancer
1. Introduction An enormous increase in childhood thyroid cancer has been reported since the Chernobyl accident [1] but the cause of such dramatic increase has been the subject of *
Corresponding author. Tel.: +81-95-849-7170; fax: +81-95-849-7172. E-mail address: [email protected] (Y. Shibata).
0531-5131/02 D 2002 Elsevier Science B.V. All rights reserved. PII: S 0 5 3 1 - 5 1 3 1 ( 0 1 ) 0 0 6 0 2 - 1
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controversy. The Chernobyl Sasakawa Health and Medical Cooperation Project, a 5-year health screening program, which began in May 1991 and reached completion at the end of April 1996, was the most reliable and comparable program of its kind, revealing 62 thyroid cancers in total and 37 in the Gomel region of Belarus among about 120 000 and 19 000 children, respectively [2,3]. However, the lack of reliable estimates of individual thyroid dose has hindered conclusions about the exact effect of the Chernobyl accident on the thyroid glands of children. In contrast to radiation exposure by atomic bombing, the mode of radiation exposure received by general population is quite complicated in the case of the Chernobyl accident. In the former case, the source of radiation was in effect fixed and people received directly a high rate of external radiation instantaneously, while in the latter case, general population received external and internal radiation exposure caused by fallout. Dose estimation is a very difficult issue. Even in the case of the atomic bombing, which is quite simpler than the case of the Chernobyl accident, it took more than 40 years to reach a dosimetry system that deems most reliable: the system, however, is still under revision. Furthermore, we should note that the dosimetry system for the atomic bombing could be validated by measuring radiation activities of available exposed materials such as bricks collected in several places in Hiroshima and Nagasaki. In the case of the Chernobyl accident, however, dose estimation is totally dependent on a model whose validity is in principle impossible to prove. Even in the case in which 131I specific activity at the thyroid gland was measured, individual estimate of thyroid dose varies with the model adopted. To overcome the shortage of accurate dosimetry data, we launched a new study aimed at comparing children born before and after the accident on the basis of the hypothesis that if children’s thyroid glands were affected by the accident, the prevalence of thyroid diseases, especially thyroid cancer, would be significantly and selectively higher in children born before the accident than in those born after the accident.
2. Subjects and methods The prevalence of childhood thyroid cancer in Gomel region observed in the 5-year health examination of the Chernobyl Sasakawa Health and Medical Cooperation Project was about 1.9 per 1000 persons. We therefore estimated the number of children to be examined in the new project as enough to detect, with probability of 90% or more, a decrease in the prevalence of thyroid cancer by 1/10 in the children born after the accident as compared with those born before the accident. We assumed the prevalence of thyroid cancer in children born before the accident to be 1 per 1000 persons and calculated the sample size necessary for assuring the above-mentioned power for the statistical hypothesis test of the 5% significance level. The sample size thus calculated was 12 000 for each group. We reviewed the population in several districts in the neighborhood of Gomel city and reached a decision, taking feasibility and other issues into account, to screen children born from January 1, 1983 to December 31, 1989 and living in Gomelskii, Hoynikskii, Loevskii and Rechitskii districts and Gomel city in the Gomel region of Belarus. These areas are within a radius of 150 km from the Chernobyl Nuclear Power Plant (Fig. 1). We conducted
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the health screening at all schools except Gomel city, where we sampled seven schools with an enrolment over 1000 using the stratified random sampling procedure. In effect, therefore, we examined all of the targeted children in the four districts and about 10% of those in Gomel city. The thyroid gland examination consisted of an ultrasound examination as well as measurement of the serum thyroid-stimulating hormone and free thyroxine levels and antithyroid peroxidase antibody. Ultrasound examinations were performed with Logic a100 (7.5 MHz) equipped with a digital image recorder (GE Yokogawa Medical Systems, Tokyo). Children with thyroid ultrasonographs showing nodules of over 5 mm in diameter or abnormal echogenity further underwent echo-guided fine-needle aspiration biopsy. To reach a final diagnosis in suspected cases, the ultrasonographs, microscopic cytology of echo-guided fine-needle aspiration biopsy, results of thyroid examinations and other important information were sent to Nagasaki University School of Medicine from Gomel Specialized Medical Dispensary via the telemedicine system (developed by us and operating from February 1999) [4]. All of the data are processed in an Oracle database developed by two computer technicians of the Mogilev Regional Medical Diagnostic Center (SPG) and Gomel Specialized Medical Dispensary (VNA). Data entry has been conducted using special software that displays on the computer screen a form similar to that used for health examination.
Fig. 1. Districts of the Gomel region with 137Cs contamination levels (Ci/km2) as measured in 1992. aThe triplets give the 25th, 50th and 75th sample percentiles of contamination levels. bMinimum and maximum levels of contamination.
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3. Results A total of 21 601 children were examined from February 1998 to December 2000: 9720 were born from January 1, 1983 to April 26, 1986 (Group I); 2409 were born from April 27, 1986 to December 31, 1986 (Group II); and 9472 were born from January 1, 1987 to December 31, 1989 (Group III). A total of 32 (0.15%) thyroid cancers were detected: 31 of them were in Group I (0.32%), one in Group II (0.04%) and no cases in Group III. All of the patients underwent surgery at the Thyroid Oncology Center in Minsk and were confirmed by histological diagnosis: all were cases of papillary adenocarcinoma and 13 had undergone surgery prior to screening, i.e., from October 1993 to January 1998. A significant difference in the prevalence of thyroid cancer among the three groups is apparent, as shown in Fig. 2. However, the distribution of age at the time of the examination is different among the three groups as well. Since the age as well as the sex is a major factor to increase the risk of thyroid cancer, as shown in the upper right hand side of Fig. 3, we compared the prevalence of thyroid cancer among children aged 11– 13 years. Out of 10 055 children in this age class, 2627 were in Group I, 2086 in Group II and 5342 in Group III. A significant difference in the prevalence of thyroid cancer among the three groups is also seen in the left-hand side of Fig. 3. A formal statistical analysis on the
Fig. 2. Prevalence of thyroid cancer (per 1000) by sex and birth period in 21 601 children living in Gomelskii, Hoynikskii, Loevskii and Rechitskii districts and Gomel city in the Gomel region of Belarus. Examination was carried out at schools from February 1998 to December 2000. The parenthetic entry refers to the number of children examined and the figure on the bar indicates the number of cancer cases. Group I = children born from January 1, 1983 to April 26, 1986; Group II = children born from April 27, 1986 to December 31, 1986; Group III = children born from January 1, 1987 to December 31, 1989. The age (years) refers to that at the time of examination.
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Fig. 3. Upper right hand side: prevalence of thyroid cancer (per 1000) by sex and age at the time of examination. The group of children aged 14 – 17 years included those in Group I and Group II; the parenthetic entry in the lower line refers to the number of children in Group II while that in the upper line refers to the total number of children in Group I or II. Left-hand side: prevalence of thyroid cancer (per 1000) by sex and age at the time of examination in children aged 11 – 13 years. See Fig. 2 for details.
basis of individual data demonstrated a significant ( p = 0.006) difference in the prevalence of thyroid cancer among the three groups after adjustment for sex and age [5].
4. Discussion Since the design of our health examination was school-based, differences in environmental factors after the accident were deemed small. The major difference in background was that the children in Group III were not exposed to fallout caused by the Chernobyl accident, while the children in Groups I and II were probably exposed to fallout directly or in utero, respectively. Our findings demonstrate the likelihood that thyroid cancers detected in children after the Chernobyl accident were caused by direct external or internal exposure to short-lived radioactive fallout including 131I and 133I. People exposed to the Chernobyl accident in their childhood are at high risk for thyroid cancer, and establishment of a global support system to provide careful and continuous follow-up is urgently needed.
Acknowledgements The authors thank Dr. Vladimir S. Vorobey (Chief Physician, Gomel Specialized Medical Dispensary) and Dr. Tadeush A. Kroupnik (Chief Physician, Mogilev Regional Medical Diagnostic Center) for their cooperation in carrying out the project. We express
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our special thanks to Dr. Itsuzo Shigematsu, Prof. Kenzo Kiikuni and Dr. Shigenobu Nagataki (Sasakawa Chernobyl Scientific Committee) for their support and encouragement without which the present study would not have been realized.
References [1] V.S. Kazakov, E.P. Demidchik, L.N. Astakova, Thyroid cancer after Chernobyl, Nature 359 (1992) 21. [2] S. Yamashita, Y. Shibata (Eds.), Chernobyl: A Decade, Elsevier, Amsterdam, 1997. [3] S. Yamashita, M. Ito, K. Ashizawa, Y. Shibata, S. Nagataki, K. Kiikuni, Monitoring and prevention of the thyroid carcinoma in a population exposed to radiation, in: G. Thomas, A. Karaoglou, E.D. Williams (Eds.), Radiation and Thyroid Cancer, World Scientific, Singapore, 1999, pp. 369 – 376. [4] S. Yamashita, Y. Shibata, N. Takamura, K. Ashizawa, N. Sera, K. Eguchi, Satellite communication and medical assistance for thyroid disease diagnosis from Nagasaki to Chernobyl, Thyroid 9 (1999) 969. [5] Y. Shibata, S. Yamashita, V.B. Masyakin, G.D. Panasyuk, S. Nagataki, 15 years after Chernobyl: new evidence of thyroid cancer, Lancet 358 (2001) 1965 – 1966.
A comparative study on thyroid diseases among children in Gomel region, Belarus Yoshisada Shibata a,*, Vladimir B. Masyakin b, Galina D. Panasyuk b, Svetlana P. Gomanova c, Vladimir N. Arkhipenko b, Kiyoto Ashizawa d, Masahiro Ito e, Noboru Takamura a, Shunichi Yamashita a a
Atomic Bomb Disease Institute, Nagasaki University School of Medicine, 1-12-4 Sakamoto, Nagasaki 852-8523, Japan b Gomel Specialized Medical Dispensary, Gomel, Belarus c Mogilev Regional Medical Diagnostic Center, Mogilev, Belarus d The First Department of Internal Medicine, Nagasaki University School of Medicine, Nagasaki, Japan e Department of Clinical Laboratory, National Nagasaki Medical Center, Nagasaki, Japan
Abstract A study aimed at comparing the prevalence of thyroid diseases between children born before and after the accident was outlined with emphasis on rationale and design of the study. In the study, a total of 21 601 children in Gomel city and four districts in the neighborhood of Gomel city were examined from February 1998 to December 2000. There were 9720 children born from January 1, 1983 to April 26, 1986 (Group I), 2409 children born from April 27, 1986 to December 31, 1986 and 9472 children born from January 1, 1987 to December 31, 1989 (Group III). Out of the examined children, 32 (0.15%) thyroid cancers were found, among whom 31 were in Group I and one was in Group II, while no cases in Group III. Our findings demonstrate the likelihood that short-lived radioactive fallout due to the Chernobyl accident induced thyroid cancer in children living near Chernobyl. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Chernobyl accident; Causation; Epidemiology; Short-lived fallout; Thyroid cancer
1. Introduction An enormous increase in childhood thyroid cancer has been reported since the Chernobyl accident [1] but the cause of such dramatic increase has been the subject of *
Corresponding author. Tel.: +81-95-849-7170; fax: +81-95-849-7172. E-mail address: [email protected] (Y. Shibata).
0531-5131/02 D 2002 Elsevier Science B.V. All rights reserved. PII: S 0 5 3 1 - 5 1 3 1 ( 0 1 ) 0 0 6 0 2 - 1
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Y. Shibata et al. / International Congress Series 1234 (2002) 121–126
controversy. The Chernobyl Sasakawa Health and Medical Cooperation Project, a 5-year health screening program, which began in May 1991 and reached completion at the end of April 1996, was the most reliable and comparable program of its kind, revealing 62 thyroid cancers in total and 37 in the Gomel region of Belarus among about 120 000 and 19 000 children, respectively [2,3]. However, the lack of reliable estimates of individual thyroid dose has hindered conclusions about the exact effect of the Chernobyl accident on the thyroid glands of children. In contrast to radiation exposure by atomic bombing, the mode of radiation exposure received by general population is quite complicated in the case of the Chernobyl accident. In the former case, the source of radiation was in effect fixed and people received directly a high rate of external radiation instantaneously, while in the latter case, general population received external and internal radiation exposure caused by fallout. Dose estimation is a very difficult issue. Even in the case of the atomic bombing, which is quite simpler than the case of the Chernobyl accident, it took more than 40 years to reach a dosimetry system that deems most reliable: the system, however, is still under revision. Furthermore, we should note that the dosimetry system for the atomic bombing could be validated by measuring radiation activities of available exposed materials such as bricks collected in several places in Hiroshima and Nagasaki. In the case of the Chernobyl accident, however, dose estimation is totally dependent on a model whose validity is in principle impossible to prove. Even in the case in which 131I specific activity at the thyroid gland was measured, individual estimate of thyroid dose varies with the model adopted. To overcome the shortage of accurate dosimetry data, we launched a new study aimed at comparing children born before and after the accident on the basis of the hypothesis that if children’s thyroid glands were affected by the accident, the prevalence of thyroid diseases, especially thyroid cancer, would be significantly and selectively higher in children born before the accident than in those born after the accident.
2. Subjects and methods The prevalence of childhood thyroid cancer in Gomel region observed in the 5-year health examination of the Chernobyl Sasakawa Health and Medical Cooperation Project was about 1.9 per 1000 persons. We therefore estimated the number of children to be examined in the new project as enough to detect, with probability of 90% or more, a decrease in the prevalence of thyroid cancer by 1/10 in the children born after the accident as compared with those born before the accident. We assumed the prevalence of thyroid cancer in children born before the accident to be 1 per 1000 persons and calculated the sample size necessary for assuring the above-mentioned power for the statistical hypothesis test of the 5% significance level. The sample size thus calculated was 12 000 for each group. We reviewed the population in several districts in the neighborhood of Gomel city and reached a decision, taking feasibility and other issues into account, to screen children born from January 1, 1983 to December 31, 1989 and living in Gomelskii, Hoynikskii, Loevskii and Rechitskii districts and Gomel city in the Gomel region of Belarus. These areas are within a radius of 150 km from the Chernobyl Nuclear Power Plant (Fig. 1). We conducted
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the health screening at all schools except Gomel city, where we sampled seven schools with an enrolment over 1000 using the stratified random sampling procedure. In effect, therefore, we examined all of the targeted children in the four districts and about 10% of those in Gomel city. The thyroid gland examination consisted of an ultrasound examination as well as measurement of the serum thyroid-stimulating hormone and free thyroxine levels and antithyroid peroxidase antibody. Ultrasound examinations were performed with Logic a100 (7.5 MHz) equipped with a digital image recorder (GE Yokogawa Medical Systems, Tokyo). Children with thyroid ultrasonographs showing nodules of over 5 mm in diameter or abnormal echogenity further underwent echo-guided fine-needle aspiration biopsy. To reach a final diagnosis in suspected cases, the ultrasonographs, microscopic cytology of echo-guided fine-needle aspiration biopsy, results of thyroid examinations and other important information were sent to Nagasaki University School of Medicine from Gomel Specialized Medical Dispensary via the telemedicine system (developed by us and operating from February 1999) [4]. All of the data are processed in an Oracle database developed by two computer technicians of the Mogilev Regional Medical Diagnostic Center (SPG) and Gomel Specialized Medical Dispensary (VNA). Data entry has been conducted using special software that displays on the computer screen a form similar to that used for health examination.
Fig. 1. Districts of the Gomel region with 137Cs contamination levels (Ci/km2) as measured in 1992. aThe triplets give the 25th, 50th and 75th sample percentiles of contamination levels. bMinimum and maximum levels of contamination.
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3. Results A total of 21 601 children were examined from February 1998 to December 2000: 9720 were born from January 1, 1983 to April 26, 1986 (Group I); 2409 were born from April 27, 1986 to December 31, 1986 (Group II); and 9472 were born from January 1, 1987 to December 31, 1989 (Group III). A total of 32 (0.15%) thyroid cancers were detected: 31 of them were in Group I (0.32%), one in Group II (0.04%) and no cases in Group III. All of the patients underwent surgery at the Thyroid Oncology Center in Minsk and were confirmed by histological diagnosis: all were cases of papillary adenocarcinoma and 13 had undergone surgery prior to screening, i.e., from October 1993 to January 1998. A significant difference in the prevalence of thyroid cancer among the three groups is apparent, as shown in Fig. 2. However, the distribution of age at the time of the examination is different among the three groups as well. Since the age as well as the sex is a major factor to increase the risk of thyroid cancer, as shown in the upper right hand side of Fig. 3, we compared the prevalence of thyroid cancer among children aged 11– 13 years. Out of 10 055 children in this age class, 2627 were in Group I, 2086 in Group II and 5342 in Group III. A significant difference in the prevalence of thyroid cancer among the three groups is also seen in the left-hand side of Fig. 3. A formal statistical analysis on the
Fig. 2. Prevalence of thyroid cancer (per 1000) by sex and birth period in 21 601 children living in Gomelskii, Hoynikskii, Loevskii and Rechitskii districts and Gomel city in the Gomel region of Belarus. Examination was carried out at schools from February 1998 to December 2000. The parenthetic entry refers to the number of children examined and the figure on the bar indicates the number of cancer cases. Group I = children born from January 1, 1983 to April 26, 1986; Group II = children born from April 27, 1986 to December 31, 1986; Group III = children born from January 1, 1987 to December 31, 1989. The age (years) refers to that at the time of examination.
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Fig. 3. Upper right hand side: prevalence of thyroid cancer (per 1000) by sex and age at the time of examination. The group of children aged 14 – 17 years included those in Group I and Group II; the parenthetic entry in the lower line refers to the number of children in Group II while that in the upper line refers to the total number of children in Group I or II. Left-hand side: prevalence of thyroid cancer (per 1000) by sex and age at the time of examination in children aged 11 – 13 years. See Fig. 2 for details.
basis of individual data demonstrated a significant ( p = 0.006) difference in the prevalence of thyroid cancer among the three groups after adjustment for sex and age [5].
4. Discussion Since the design of our health examination was school-based, differences in environmental factors after the accident were deemed small. The major difference in background was that the children in Group III were not exposed to fallout caused by the Chernobyl accident, while the children in Groups I and II were probably exposed to fallout directly or in utero, respectively. Our findings demonstrate the likelihood that thyroid cancers detected in children after the Chernobyl accident were caused by direct external or internal exposure to short-lived radioactive fallout including 131I and 133I. People exposed to the Chernobyl accident in their childhood are at high risk for thyroid cancer, and establishment of a global support system to provide careful and continuous follow-up is urgently needed.
Acknowledgements The authors thank Dr. Vladimir S. Vorobey (Chief Physician, Gomel Specialized Medical Dispensary) and Dr. Tadeush A. Kroupnik (Chief Physician, Mogilev Regional Medical Diagnostic Center) for their cooperation in carrying out the project. We express
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Y. Shibata et al. / International Congress Series 1234 (2002) 121–126
our special thanks to Dr. Itsuzo Shigematsu, Prof. Kenzo Kiikuni and Dr. Shigenobu Nagataki (Sasakawa Chernobyl Scientific Committee) for their support and encouragement without which the present study would not have been realized.
References [1] V.S. Kazakov, E.P. Demidchik, L.N. Astakova, Thyroid cancer after Chernobyl, Nature 359 (1992) 21. [2] S. Yamashita, Y. Shibata (Eds.), Chernobyl: A Decade, Elsevier, Amsterdam, 1997. [3] S. Yamashita, M. Ito, K. Ashizawa, Y. Shibata, S. Nagataki, K. Kiikuni, Monitoring and prevention of the thyroid carcinoma in a population exposed to radiation, in: G. Thomas, A. Karaoglou, E.D. Williams (Eds.), Radiation and Thyroid Cancer, World Scientific, Singapore, 1999, pp. 369 – 376. [4] S. Yamashita, Y. Shibata, N. Takamura, K. Ashizawa, N. Sera, K. Eguchi, Satellite communication and medical assistance for thyroid disease diagnosis from Nagasaki to Chernobyl, Thyroid 9 (1999) 969. [5] Y. Shibata, S. Yamashita, V.B. Masyakin, G.D. Panasyuk, S. Nagataki, 15 years after Chernobyl: new evidence of thyroid cancer, Lancet 358 (2001) 1965 – 1966.