Thyroid absorbed radiation dose after the Chernobyl accident
The Chernobyl catastrophe and thyroid diseases
Can after radioactive fallout thyroid dose be minimalized by preventive measures?
Ten years ago, on April 26, 1986, at 1.23 A.M. a major accident occurred at the No. 4 reactor of the Chernobyl Power Station. It is now generally recognized (1,2) that this was the greatest catastrophe of a civil nuclear power stationin the history of mankind. The accident was characterized by two explosions and a subsequent fire which damaged both the reactor and the containment structure. As a result there was a prolonged release into the atmosphere of large quantities of radioactive material including gases, halogens and particulate matter. The majority of the release occurred over a period of about 10 days with two distinct peaks in release rate (first on April 26 and second on May 6). In following days due to a variety of mitigative measures the situation was put under control and, although the release continued for several weeks, the rate of it was much lower (3). The expelled fission products and fuel elements released during the first peak (characterized in fact by the two explosions, the first due to steam and a second due to hydrogen) accumulated in a cloud which centered at approximately 4,500 m altitude. A complex and varying set of meteorological conditions present in April and May 1986 in Europe dispersed the radioactive cloud over the whole Northern Hemisphere (4,5). Initially, as wind direction was north-west, the cloud of radioactive material was carried over the Baltic Sea to Scandinavia. Within the next 24 hrs this cloud split into three segments: one started to travel east, across northern former USSR finally reaching China and Japan, the second travelled across Norway being finally detected in the United States and the third turned south-westwards pushing clouds over central Europe. By the end of April the wind direction rotated clockwise, pushing incoming clouds first eastwards across former USSR and then south finally reaching Turkey. During the first week of May the direction of the wind changed again, this time to south-east carrying radionuclides over eastern Mediterranean. The meteorological situation between April 26 and May 6 was also characterized by a number of rainstorms which resulted in numerous, still poorly identified "hot spots" where deposition of radioactive material could be more than 100 times greater than in the surrounding areas (6). All together the deposition of radionuclides in a given country was a consequence of the distance from the place of the accident, wind direction and rainfalls at the time of passage of the radioactive cloud. Although, several nuclides were present in contaminated air masses, this review will for obvious reasons concentrate on radioiodines. Preliminary Russian estimates of 131I released to atmosphere amounted to about 0.264 EBq (=1018 Bq) (3), while more recent calculations suggest (7,8,9), that 131I release could be as high as 1.3 EBq, or even 1.7-1.8 EBq. Data on other radioiodine isotopes are sparse. It is well recognized (7,8) that they are present with higher core inventories and as their half-life is short they are of special significance in first days and near the place of nuclear accident. Due to a very unusual position taken by local and central authorities of the former USSR in the first days of the Chernobyl catastrophe (LA Ilyin - personal communication) spectroscopy of the environmental radionuclides was not immediately performed. The characteristics of the nuclear fuel of reactor No 4 in Chernobyl may suggest however (10) that 132Te and 133I released in the accident amounted to about 3.5 EBq. In Warsaw, Poland, on April 28 and 29 approximately 28% of the air radioactivity was present as short-lived isotopes of iodine (11). In Seibersdorf, Austria, on May 1 the activity of 132I at ground level was over twice the activity of 131I (12) and in the United Kingdom on May 2 activities of 131I and 132I in the air were equal (13). It can be therefore suggested, that in some parts of Belarus or Ukraine the radioactivity due to short-lived radioiodines could be higher than due to 131I.
All these data suggest, that the total release of radioiodines from Chernobyl which occurred between April 26 and May 6 was only about 100 times lower than the respective total release of radioiodines from all 77 nuclear tests performed above the ground by the USA and former USSR in the record year of 1962 (2). Available estimates also show, that the release of radioiodines during the Chernobyl catastrophe was approximately 2000 times higher than the release during the Windscale accident and about 3000000 times higher than the release of 131I during the Three Mile Island accident (2). It is estimated that the released radioactivity in Chernobyl was 200 times greater than the combined release of the atomic bombs at Hiroshima and Nagasaki. It should be pointed out that Chernobyl catastrophe was also unique in a sense, that the release of radioactivity was prolonged and that at least in areas closer to the burning reactor (but also elsewhere), short-lived iodine isotopes could significantly contribute to the total radioactive contamination.
Thyroid absorbed radiation dose after the Chernobyl accident
The radioiodine thyroid committed dose depends on the scale of radiation contamination of the environment, the time during which radioiodines are present in the environment, and on the quantity of radioiodines taken up and retained within the thyroid gland. In general the radioiodine uptake in the gland is inversely related to the daily intake of stable iodine (14). Radioiodines can reach the thyroid gland through inhalation of contaminated air, through ingestion of contaminated food and through the skin if there is prolonged contact with contaminated material. With the exception of the area close to the Chernobyl power station, where contamination through the skin was important, in all other places only inhalation and alimentary components were significant for the thyroid adsorbed dose. Although short-lived radioiodines with their high dose rate of radiation are likely to be more carcinogenic per unit absorbed than 131I (15), only thyroid committed dose of this latter radioiodine was evaluated. The contribution of contaminated air to total thyroidal radiation amounted in the Ukraine and Belarus to 80%, in Poland to 30% and in other European countries contribution varied from 2% in Switzerland to 80% in Belgium (16). Evaluation of the thyroid absorbed dose was done either by direct methods or by indirect one, based either on a modified MIRD scheme (17,18) or on the 5-compartment model of iodine metabolism developed by Johnson (19). This second indirect method is using 131I in air, milk and other foods, standard values for inhalation rate, milk and food consumption and parameters such as age, sex, thyroid size, and thyroid iodine uptake rates. According to former USSR data (3,20) about 200000 direct measurements of 131I in the thyroid were performed in Ukraine, Belarus and Russia, but because of obsolete equipment used, their accuracy may be questioned. In regions of Ukraine close to Chernobyl the thyroid dose equivalent was estimated by using the relationship between the thyroid dose and the 137-Cs deposition (21). With this approach the highest mean thyroid dose for infants was calculated to be about 3.3 Gy and for adults 0.5 Gy. In Kiew thyroid committed doses for 1-3 years, 4-6 years, 7-9 years and 12-15 years old children were 104, 62, 19 and 41 mGy respectively (22). There is a difference in the collective thyroid dose calculated for Ukraine with a value of about 29000 persons/Gy (22) and 64000 persons/Gy (23). In highly contaminated regions of Belarus, thyroid recorded doses in children varied from 0.3 Gy to 50 Gy and in adults from 0.1 Gy to 50 Gy(24,25). In the Russian Federation the highest radioactive contamination was recorded in Bryansk and Kaluga regions. The average thyroidal absorbed dose in children varied between 10 mGy and 2.2 Gy and in adults the highest recorded dose was 2 Gy (24,25,26). In Poland about 1500 measurements were performed by a direct, standardized method (27), while the population study was based on the Johnson model (28) assuming, however, appropriate iodine intake . The highest thyroid doses were recorded in children 1 year old or under being in the range of 60-80 mGy regardless of prophylactic measures taken. The average country-wide thyroid committed dose in children up to 16 years old was estimated to about 20 mSv giving a collective thyroid dose of about 210000 persons/Sv. The average thyroid committed dose in adults was about 6 mSv giving a collective thyroid dose of about 162000 person/Sv. Taking into account the results of a population study (29), which clearly showed, that the entire population of Poland is mildly or moderately iodine deficient, the Polish data may be underestimated and both average individual and collective thyroid dose may be higher. In Western Europe approximately 3000 direct measurements were performed and data on thyroid absorbed dose are therefore very general. Average thyroid absorbed dose estimates taken from different sources (16,20-28) are presented in Table 1.
Table 1
Average 131I thyroid committed dose in some Western European countries
and range of 131I thyroid committed doses in children and adults in Belarus,
Poland, Russian Federation and Ukraine in first year after the Chernobyl
accident.
Data from Belarus, Russian Federation and Ukraine are from heavily contaminated regions.
| Country | Thyroid committed dose (mSv) |
| Austria | 2.30 |
| Belgium | 0.30 |
| Belarus adults | 300-5000 |
| Belarus children | 100-5000 |
| Denmark | 0.06 |
| Finland | 0.92 |
| Germany | 1.50 |
| Greece | 2.80 |
| Italy | 2.00 |
| Poland adults | 3.1-68 |
| Poland children | 3.9-18 |
| Russian Federation adults | 100-2200 |
| Russian Federation children | 30-2000 |
| Ukraine adults | 100-2000 |
| Ukraine children | 30-1500 |
Thyroid and radiation
The thyroid gland is highly sensitive to the tumorigenic effects of external radiation. A causal relationship between X-ray exposure and thyroid cancer was for the first time suggested in 1950 (30) and then confirmed in several studies. The elevated risk of thyroid neoplasia was demonstrated in patients treated with radiation for tinea capitis (31), enlarged thymus gland (32), lymphnodes abnormalities (33), or for a variety of benign neck and head conditions (34). The average dose of ionizing radiation varied from 10 mGy to 6 Gy. Extensive studies indicated a linear dose response relationship between radiation exposure and the induction of both malignant and benign thyroid tumors with no clear threshold and extending through 0.7-10 Gy (35-37). In other words there is no threshold below which exposure of the thyroid to external radiation does not carry a risk of cancer. The risk per unit dose of radiogenic thyroid tumors was found to be significantly higher among children as compared to adults. It was suggested (33) that there are three age groups with different sensitivity to carcinogenic effects of X-ray exposure. The highest sensitivity would be characteristic for very young children aged up to 5 years, followed by the age group of 6 to 20 years while the lowest sensitivity was found in persons aged above 20 years. In general it can be stated that infants and young children might be up to 8 times more sensitive than adults to the effects of external radiation (35-37). It was also concluded that females are more sensitive to the thyroidal tumorigenic effects of radiation than males, and the absolute excess risk per Gy was found to be 2 to 3 times higher as compared to males (32). Generally the risk compared to the spontaneous rate of occurrence of thyroid malignancies is 2-3 fold for individuals exposed to 100-200 mGy and 50-100 fold for individuals exposed to 5 Gy (35-38). There is a well-established latency period between external radiation and occurrence of thyroid neoplasia (36,37). The latency period has a log-normal distribution and varies from 5 to 40 years with a peak incidence of around 15 years after exposure. External radiation of the thyroid gland leads not only to significantly higher incidence of thyroid malignancies but also to damage of thyroid tissue. With larger doses in the range of 30-50 Gy the damage to thyroid cells is rapid, extensive and results in hypothyroidism. Doses below 100 mGy can produce fibrosis, hyperplasia, some damage to vascular tissues and possibly immune mediated changes in the thyroid (37).
In survivors of the atomic bombings of Hiroshima and Nagasaki (39) and residents of the Marshall Islands (40) accidentally exposed to both external and internal radiation from fallout of nuclear weapons testing, an increased risk for both malignant and benign thyroid neoplasia has been observed. In Nagasaki, in survivors directly exposed to a dose of radiation below 1 Gy, the prevalence of thyroid nodularity and malignancy was about 7 fold increased, while in those exposed to a dose above 1 Gy the frequency of malignant tumors was up to 10 times higher than in non-exposed age and sex matched controls (41). In addition to radiation induced thyroid nodularity, a significant increase in the prevalence of hypothyroidism was observed in a group of survivors exposed to low radiation in a range of 1 mGy to 49 mGy (40). The Marshall Islands experience was the first to show the risk from radioactive iodine fallout to the thyroid gland in man (40,42). In the Rongelap Island accident the external radiation in adults, 9 year old and 1 year old children contributed to about 16%, 9% and 4%, respectively, of total thyroid absorbed dose estimates. In the same age groups, who were exposed to a maximal dose of radiation, the external radiation contributed to 4.5%, 2.3% and 0,95% of total thyroid adsorbed dose respectively, thus showing first time, that internal radiation can be carcinogenic in men (42). In Rongelap Island the mean total thyroid uptake of radioactivity from short-lived radioiodines (132I, 133I, 134I and 135I) and tellurium (131Te and 132Te) was about 8000 uCi while that from 131I was 100uCi (42). Resulting thyroid cancer risk for all Marshallese was calculated to be about 2/106 persons/10 mGy/year, a value similar to that for survivors of Hiroshima and Nagasaki and a person exposed in childhood to X-ray therapy (38,39,42). The medical findings in the Marshallese population gave a proof that radiation by short-lived isotopes of iodine is tumorigenic for the thyroid.
Contrary to X-ray, or radiation by short-lived radioiodines data on effects of 131I in humans are insufficient to draw firm conclusions. In four independent studies, which when combined consisted of more than 60000 thyrotoxic adult patients no relation was found between 131I treatment and subsequent development of thyroid carcinoma (43-46). Also Safa et al (47), studying hyperthyroid children were unable to show, that administration of therapeutic doses of 131I can lead to carcinogenesis in the thyroid. Finally, thyroid cancer cases which were suggested to result from 131I treatment did not share characteristics of radiation induced malignant tumors (48). The theoretical but not proven risk for thyroid cancer after exposure to therapeutic doses of 131I in a person younger than 20 years of age was calculated to be 0.064/106 persons/ 10 mGy/year. The largest study up to date on the effects of diagnostic doses of 131I also failed to show carcinogenicity (49). Until the Chernobyl catastrophe it was therefore suggested, that 131I in humans does not increase the risk of thyroid cancer, or if it does, its carcinogenic effectiveness is several times lower, than that of external radiation (48,50). It should be pointed out that contrary to humans, 131I in rats is carcinogenic to the thyroid and this effect is comparable to that of external X-ray radiation in the same species (51).
The Chernobyl catastrophe and thyroid diseases
The possibility, that the Chernobyl catastrophe can lead to an increase in the incidence of thyroid cancer was first time reported in 1991 (52). The study from Belarus presented thyroid cancer in 18 children diagnosed between 1986 and 1989. As thyroid cancer in children is very rare with an incidence of about 1/million/year, the findings seemed significant for a population of children amounting to about 2.5 million. At the same time, however, the results of the International Chernobyl Project (53) led to conclusion that "There were significant non-radiation related health disorders in the population of both surveyed contaminated and surveyed control settlements studied under the Project, but no health disorders that could be attributed directly to radiation exposure". In addition to this general conclusion the Report of the International Advisory Committee stated (53) that abnormalities in either TSH, free T4, mean thyroid size and the size distribution in the population, as well as the number of thyroid nodules were the same in the population of surveyed contaminated and control settlements and similar to those reported for other countries. The significance of these conclusions published also elsewhere (54) was such, that the response to the Belarus and Ukraine data on the rise of incidence of thyroid cancer after Chernobyl were received with scepticism. It was even suggested that the pathological findings of removed thyroid tissue could be grossly over-interpreted. The first report about the rise in the incidence of thyroid cancer in children was published in international journals in September 1992 (55) and the Belarus findings were supported by a group of international experts (56). Soon thereafter several other reports were published (24,25,57-59) all presenting significant increases in the incidence of thyroid cancers in children. The results of the IPHECA pilot project presented in 1995 showed (24), that until the end of 1994 there were 333 cases of childhood thyroid cancer in Belarus, 208 in the Ukraine and 24 cases in the Russian Federation. The incidence of thyroid cancer in 1994 (rounded) per million of children in Belarus, the Russian Federation and the Ukraine was 36, 22 and 31 respectively (vs 0.9, 0. 0 and 0.7 in 1986) thus showing a significant rise. More than 98% of thyroid cancers diagnosed until the end of 1994 were of the papillary type, and more than half of them the solid variant. Very few were microcarcinomas and the majority showed aggressive histologic features including local and extrathyroidal invasion (24,25,57,59-61). In general, the histological findings were similar to those described in childhood thyroid cancer (62,63). From the age of children at diagnosis it can be concluded that very young children were much more sensitive to the radiation than teenagers. The incidence of thyroid cancers in girls (59,7%) only slightly exceeded the incidence in boys (40,3%). It is of interest that of the children who developed thyroid cancer 66% had a thyroid radiation dose of less than 0,3 Gy, 22% a committed dose from 0.3 to 1.0 Gy and only 12% a dose of 1.0 Gy or more (59). The Belarus Cancer Registry also shows that 241 thyroid adenomas were diagnosed in children between 1987 and August 1995, while only 1 case was seen in 1986 (64). Finally, both the Belarus and Ukraine studies on the geographical and time distribution of thyroid cancers and adenomas suggest, that they are related to radiation contamination after the Chernobyl accident (24,25). During the International Conference jointly sponsored by the European Commission, the International Atomic Energy Agency and the World Health Organization (65), drs. Williams, Becker, Dimidchik, Nagataki, Pinchera and Tronko presented data showing a further increase of thyroid cancer incidence in children both in Belarus (424 cases diagnosed till end of 1995) and the Ukraine (211 cases diagnosed till end of 1994). The authors stated that although absolute proof of the relationship between exposure to radioiodine and the increase in the incidence of childhood cancer is not available, the circumstantial evidence is very strong.
Regardless of all recent data there is still scepticism whether the rise of thyroid tumors incidence can be related to 131I radiation (63). Sceptics suggest that diagnostic and therapeutic doses of 131I have never showed to lead to a significant increase of thyroid cancer incidences. As the significant rise in the number of thyroid cancer in childhood can not be questioned, the most probable explanation then for the increase would be that increased awareness leading to intensive screening, or that thyroid cancer is a consequence of radiation contamination by compounds other than 131I like short-lived isotopes of iodine and isotopes of tellurium and caesium. The aggressiveness of tumors and type of cancer is against the first of these arguments. The majority of thyroid cancers diagnosed in Belarus or Ukraine were in more than 98% of cancers of the papillary type. In regions of iodine deficiency at least 25-30% of cancers are of the follicular type. Regarding the second argument, it is true that 131I in humans has never shown to cause thyroid cancer, but such data were never derived from very young children. On the other hand, as already mentioned, the Chernobyl catastrophe led to a significant release of short-lived radioiodines which are as tumorigenic as X-ray radiation. From the core inventory of Reactor No 4 it can be assumed (10), that the amount of short-lived radioiodines could well exceed that of 131I. The Marshall Island experience has shown that a 8:1 mixture of short-lived radioiodines and 131I was highly carcinogenic (41). This factor and the relative iodine deficiency which is present in many regions of Belarus and Ukraine can explain the high incidence of thyroid papillary cancer in childhood. Although a higher incidence of thyroid cancer in adults is also suggested by the Belarus Cancer Register, further data are needed to come to a definite conclusion. Further studies should be also performed to assess the number of benign thyroid tumors in Belarus, Ukraine and Russia, as well as the possible impact of the Chernobyl accident in other European countries.
Can after radioactive fallout thyroid dose be minimalized by preventive measures?
Administration of pharmacological doses of stable iodine can significantly decrease thyroid committed dose by the following mechanisms (14):
a) by saturating active iodine transport into the thyroid and
diluting the radioiodines taken up by the gland,
b) by increasing storage of stable iodine in the thyroid, thus leading
to attainment of a new steady-state at lower level of (radio)iodine uptake,
c) by lowering circulating radioiodine and its thyroidal (re)uptake.
It is well known (66) that a single dose of 130 mg of potassium iodine (KI) completely blocks the thyroid radioiodine uptake approximately 30 minutes after administration and keeps the suppression constant for about 24-30 hours. Such a dose will be about 25% effective 40 hrs after administration. It was also shown, that a KI dose of 65 mg is an effective thyroid blocking dose in children and teenagers (67-71). This dose would be also effective in adults, although, at least 60 minutes are required before radioiodine entry into thyroid is blocked (69,70). In addition to the dose, the time of KI administration is another factor influencing the effectiveness of thyroid protection. Implementation of KI administration shortly before, or within 1-2 hours after exposure to radioiodines would effectively protect the thyroid (68,70). KI given 12 to 24 hrs after the thyroid exposure to radioiodines will lead to minimal gland protection, however, limited benefit is still possible. Following previous accidents in Windscale and Three Miles Island, protective KI administration was not implemented. After the Chernobyl accident a total of 5.4 million people including 1.7 million children received KI prophylaxis in regions of former USSR relatively close to Chernobyl (3,26). The data concerning KI dose in different age groups, the formula of KI and the period of KI administration, as well as efficiency of this action was never investigated and published. It can be only assumed that in Prypyat and a few nearby population centers iodine prophylaxis was implemented on April 27, 1986 (i.e. one day after the explosion), prior to the decision of evacuation (26). In Poland, KI prophylaxis and other protective measures were institutioned on April 29, as a mandatory action for all children up to 16 years old (72,73). Pregnant and lactating women were advised to take KI. As was estimated (73) about 10.5 million children and about 7 million adults received a single KI dose. A KI dose was determined of as 15 mg for newborns, 50 mg for children 5 years or under and 75 mg for all others. A follow-up study revealed (73), that in those who took KI on April 29, the reduction in thyroid absorbed radioiodine dose amounted to about 40%, while in those who received KI on April 30, the thyroid radioiodine dose reduction was about 25%. As already published in detail (73), the prophylactic measures in Poland were aimed to reduce the final thyroid committed dose and keep it below the desired 50 mSv limit. The predicted scenario assumed, that the accident was very serious and would lead to prolonged radioiodine release. The KI administration was found to be safe. Transient intrathyroidal side effects (mild increase of serum TSH and decrease of serum fT4) were observed in 12 of 3212 neonates who were given KI on first day of life. This form of Wolff-Chaikoff phenomenon completely disappeared after 3-5 days and thyroid function was found normal 2-3 years later (73). The extrathyroidal side-effects were mild and transient. They were observed in 0.35% of children and 0.2% of adults who received one or two doses of KI (72,73).
Administration of iodine as prophylaxis to a population requires a number of planing decisions. The logistics of a policy of implementation of stable iodide following a nuclear accident have been described in detail elsewhere (74). One of the most important general actions which is significant to health, and would also reduce thyroid radioiodine committed dose is appropriate iodine intake in every day diet. It has been established (75) that in countries where daily iodine intake exceeds 150 ug, 24 hr 131I thyroid uptake varied between 19 and 22%. On the contrary in countries with mild or moderate iodine deficiency 24 hr 131I thyroid uptake lies between 40 and 60% (75). It must be pointed out that even in countries with appropriate iodine intake protective measures in case of nuclear accident should be considered and if necessary implemented at least for high risk groups.
Conclusions
The Chernobyl accident was in fact a tragic catastrophe with health impacts that are still far from being fully evaluated. In case of the thyroid it has led most likely (but not yet scientifically proven) to a significant increase in the incidence of thyroid cancer in children. The first tumors occurred 2-3 years after the accident and the majority of cases appeared in those children, who were 1 year or under, or even in utero at the time of radioiodine contamination. In this age group the thyroid is especially sensitive to radiation. The TSH level is significantly higher than in adults. In addition at this very young age, thyroid follicular cells undergo developmental growth, rendering them more sensitive to mutagenic action of radiation (60,76). Finally, carcinogenic effects of short-lived radioiodines, certainly in combination with iodine deficiency, might be other important factors. The health impacts of the Chernobyl accident should be carefully followed in coming years.
Janusz A. Nauman,
M.D., Ph.D.,
is professor of Medicine and head of the Department of Endocrinology, University Medical School, Warsaw, Poland. He is also head of the Department of Experimental Endocrinology, Medical Center of Experimental and Clinical Endocrinology, Polish Academy of Sciences, Warsaw, Poland.Dr Janusz Nauman is a well-known endocrinologist with a special interest in thyroidology. His early work in 1967, concerning the determination of total and free triiodothyronine, attracted international attention. He authored around 200 scientific papers and his research area is related to the pathophysiology of the thyroid, thyroid hormone metabolism and mode of action. He has a special interest in Graves' disease and Graves' ophthalmopathy. Since 1986 he became involved in actions implemented in Poland after the accident in the Chernobyl nuclear power station. He shared responsibility for actions to protect the thyroid, resulting in administration of potassium iodine to about 19 million people in Poland, including all persons up to the age of 16 year. Since this time Dr Nauman served several times at temporary advisor to the World Health Organization and the International Atomic Energy Agency in matters concerning thyroid protection following nuclear accidents. Dr Nauman was twice a recipient of the Postdoctoral Foggarty Research Fellowship and worked at the Columbia University, New York, with Sidney C. Werner and at the National Institutes of Health, Bethesda, with J. Wolff.