IS THERE A WAY TO RESOLVE THE CONTROVERSY ON LOW DOSE EFFECTS? D. J. Higson
Consultant 260 Glenmore Rd, Paddington, NSW 2021, Australia
INTRODUCTION The controversy which is addressed in this paper is whether there are risks or benefits to health from exposure to low levels of ionising radiation or, indeed, whether there are any significant health effects at all. The background to this controversy was outlined in 1998 in the report of a Task Group on Low Dose Effects, convened by the International Nuclear Societies Council (INSC) [1]. For the purpose of the INSC report, low levels of radiation were defined as acute1 doses less than 10 mSv and chronic dose rates less than 20 mSv per year. The INSC Task Group itself concluded that, either there is no risk, or there may be health benefits from such exposures. The scientific aspects of the matter were reviewed by the author in 2001 at the IRPA Regional Congress on Radiation Protection in Central Europe, in Dubrovnik [2], and are summarised in the next section of this paper. In Dubrovnik, the author concluded that there is at least as much evidence of beneficial health effects as harmful effects from low level radiation. Controversy on the biological effects of low level radiation continues to be polarised to an extent which should be considered unacceptable in a rational community, and it is aggravated by the multiplicity of different viewpoints from which to consider the information available on this subject. These viewpoints include not only – S the scientific and regulatory positions, but also S public and political perceptions, and S the news media; and they lead to a wide variety of views, each of which is considered to be legitimate by most of those who adopt it. Scientific research is continually improving our understanding of low dose effects but it tends not to provide the quick, definitive answers which are often sought by the news media and the public. Hence, the scientific approach is not always comprehensible and acceptable to the lay- public and it can be very frustrating for politicians and journalists. (There is a story, which is no doubt apocryphal, of a politician who was looking for a one-handed scientist so as to get a straightforward answer to a scientific question.) The regulatory approach must essentially be pragmatic. Scientific evidence on the biological effects of low level radiation is often neither clear nor simple. At present, the scientific
1 In this context, an “acute dose” is a dose that is incurred at a very high rate in a short space of time, as in an atomic bomb explosion or in some medical procedures. approach does not provide answers that can readily be used in regulations. In the practices of radiation protection and regulation, it has therefore proved to be necessary to make simplifying assumptions to facilitate decisions about complex situations – specifically, the assumption that the risk of incurring cancer is proportional to dose without a threshold. This assumption, the “linear no-threshold (LNT) hypothesis”, is recommended by the International Commission on Radiological Protection (ICRP) [3] and is the basis of regulatory requirements in most countries. For members of the radiation protection profession, the LNT hypothesis is a convenient tool, without which their work would be difficult to perform. However, although the assumption of linearity has been shown to be a reasonable approximation for high dose exposures, it is not supported by scientific data at low doses and low dose rates. In recent years, it has become clear that many scientists are concerned that the LNT assumption, when applied to low levels of radiation, is not consistent with the scientific evidence [1,2,4-6]. Strict adherence to ICRP’s recommendation has led to the view that the LNT relationship can be extrapolated reliably, over more than four orders of magnitude in terms of dose and over an even greater range in terms of dose rate, to estimate cancer fatality risks from dose rates less than 0.02 mSv per year. Regulatory concern is thus being directed toward dose rates which are minute fractions of natural background radiation (much smaller than natural variations). The consequences of such concerns have included: S inappropriate countermeasures adopted after the Chernobyl accident, some of which did more harm than good [7]; S excessively stringent standards for clean-up of radioactive contamination, which appear to be unnecessarily costly and to be a misallocation of scarce national resources; S inappropriate uses of collective dose (tiny doses multiplied by huge populations) as a measure of collective risk. Some consequences outside the field of radiation protection, which were probably not envisaged at the time that LNT was first propounded, include: S the erroneous view that there is no safe dose of radiation; S disincentives for patients to undertake medical treatment which would be beneficial for them; S the myth that nuclear power is a threat to the environment, even though it generates no “greenhouse” gases or acid rain; S unnecessary mental anguish to exposed persons, e.g. former residents of the Chernobyl area [7]; S provision of an unwarranted basis for anti-nuclear propaganda. The search for consistency between regulation and science should lie between the regulatory and scientific communities but it is made difficult by the entrenched positions of some political and “public interest” groups (and, indeed, some scientists) and the needs of the news media and popular science publications to exploit controversy. The purpose of this paper is not to present any new evidence but to propose a practical way forward, based on the understanding that low-level radiation does not have discernible adverse health effects.
SCIENTIFIC EVIDENCE It has been well established by the work of the Radiation Effects Research Foundation (RERF) in Hiroshima, Japan, that individual acute doses of ionising radiation greater than about 200 mGy cause an increase in the incidence of cancer in human populations. Epidemiological studies of the atomic bomb survivors and the consequences of some medical exposures provide evidence that risks of increased cancer may extend to acute doses less than 200 mSv [3,8], but with lower levels of statistical significance. Wakeford [9] believes there is evidence that risks exist in utero down to about 10 mSv. There is considerable evidence that a dose that is in any way protracted, incurred at a low dose rate or from intermittent exposures, is less likely to be harmful than an acute exposure to the same total dose. This effect appears to be significant when exposure is spread over a few days or more, as in the Chernobyl reactor accident in 1986. UNSCEAR [10] has reported that, apart from – S radiation sickness and early fatalities of workers who were on the plant at the time of the accident, incurring doses well in excess of the threshold for deterministic effects; and S thyroid cancers among children, in some districts around Chernobyl, who were exposed to very high thyroid doses from radioactive iodine; there is no evidence of any other health effects attributable to radiation exposure from Chernobyl. In particular, there has been no discernible increase in the incidence of leukaemia, which was one of the main concerns due to its short latency period (5-10 years after radiation exposure in adults). No increase has been observed in the incidence of any cancer (other than child thyroid cancer) in any of the exposed groups, including emergency response workers, evacuees and the residents who were not relocated. About 100,000 workers involved in the emergency responses and cleanup of Chernobyl incurred doses in excess of 100 mSv, the average being about 170 mSv for those employed in 1986. Several thousand of them probably received doses greater than 500 mSv. The maximum estimated individual dose commitment (due to the accident) for local residents was reported to be 250 mSv, with the average for the 1,500 most highly exposed members of this group being 160 mSv. The lack of clear evidence of risks from low doses of radiation may be because there are no harmful effects of radiation at low levels or because the health effects, whatever they may be, are too few to be statistically significant. A study of cancer mortality among radiation workers with protracted occupational exposures in the nuclear industry in the US, UK and Canada was reported in 1995 [11]. The purpose of this study was to look only for significant dose-related increases in mortality. Data showing significant dose-related decreases were, in effect, excluded. With this vital limitation, the study found that there is “no evidence of an association between radiation dose and mortality from all causes or from all cancers”, for individual doses up to 100 mSv. It appears that funds and effort for major epidemiological studies tend to be forthcoming only when harmful effects are to be investigated, not for beneficial effects. Other studies [12-17] have nevertheless shown that radiation workers, occupationally exposed to lifetime doses up to about 100 mSv, have lower mortality rates from all causes and from all cancers than the general population – and sometimes lower than other workers doing similar or identical work but not exposed to radiation [12,15]. British radiologists who first registered in the period 1897-1920 incurred lifetime doses of the order of 20 Sv (20,000 mSv). Even these highly exposed radiation workers, who experienced elevated rates of cancer mortality, had substantially decreased rates of non-cancer mortality [14,15]. It has been suggested that this “healthy worker” effect, including reduction of the incidence of diseases other than cancer, may be due to stimulation of the immune system by radiation [15,18]. This is an effect that has been well documented using animal systems [18]. It would also be consistent with observations reported by Sakamoto and his co-workers in Japan, that beneficial effects in the treatment of cancer have been achieved from repeated therapeutic whole-body and half-body doses of the order of 100-150 mGy [19]. Laboratory experiments on the biological effects of radiation have shown that there are a variety of effects at the molecular and cellular levels, some of which are potentially harmful and some potentially beneficial. These effects include – S incorrectly repaired damage to DNA, which can lead to cancer [10,20]; S induction or activation of cellular DNA repair capacity, additional to that which exists normally [4,13,18]; S apoptosis, whereby cells that are unable adequately to repair their chromosomes are sensitised to die [4,18]. Any significant net effect on human health should be expected to vary from person to person. Mitchel and Boreham [4,18] have shown experimentally that low doses and dose rates have a much higher probability of being protective than harmful. This is not simply a matter of thresholds to carcinogenesis, although thresholds may exist. Most human cancers arise from DNA damage due to agents other than radiation. Hence, DNA repair systems exist primarily for damage other than radiation damage. If low doses of radiation enhance repair of any such damage, the net effect could be a reduction in overall risk, in spite of any small risk increment due to the radiation itself. Such an effect, sometimes called “radiation hormesis”, has been observed in cells from virtually all types of organisms, in whole plants and animal species other than humans, and in human cells [4,18]. Animal experiments tend to show that protective effects predominate up to about 100 mGy. Above this dose, the detrimental effects begin to show [18]. Natural background radiation is the main source of exposure for most people, and it is therefore a major potential source of information on the effects of radiation exposure. The dose rate from natural background radiation (including inhaled, ingested and external sources) ranges around the world from less than 1 to more than 50 mSv per year in some places, e.g. up to 260 mSv per year at Ramsar in Iran [21] and 70 mSv per year in Kerala, India [22]. Lifetime doses from natural radiation range up to several thousand mSv. Even at the highest levels of dose and dose rate, there is no evidence of increased incidences of cancer or other adverse health effects. In fact, the reverse has been reported [23-25 and many other references]. This should not come as a surprise. Radiation hormesis should be expected because evolution has occurred in the presence of ionising radiation [26]. During the evolution of life on earth, natural background radiation has previously been substantially higher than it is today and it is a fundamental tenet of evolutionary biology that organisms adapt to their environment. Fitness measures, including health, longevity and resistance to diseases, should be maximal for organisms in the habitats in which they normally occur. With radiation being part of our normal environment on earth, it follows that fitness should be at its highest within the range of natural background radiation, viz: somewhere between (say) 1 and 50 mSv per year. Levels of natural radiation tend to be enhanced in enclosed spaces, such as caves and buildings. Many studies have been conducted of the possible risk of lung cancer due to environmental radon which accumulates inside homes. The results range from negative to positive correlations. For example, Cohen [25] observed that the higher exposures to domestic radon correlated with the lower incidences of cancer (a negative correlation), whereas Lubin and Boice [27] have reported a positive correlation. The only conclusion that can be stated with any level of confidence is that the attribution of large numbers of lung cancer deaths to domestic radon (as claimed by some environmental protection agencies) is speculative. The epidemiology of lung cancer and radon is usually subject to the potential confounding factor of tobacco smoking, which is not fully understood. This was certainly a factor in a recent study of a large population in China, who have been exposed to very high levels of radon in underground dwellings [28]; also to air pollution from stoves used for cooking and heating. The data show that the incidence of lung cancer is elevated at the higher levels of radon, but they do not demonstrate a continuous correlation and would be consistent with a threshold in the relationship.
THE LNT HYPOTHESIS The main reason for the belief that there are risks from low levels of radiation is that the ICRP recommends the use of the LNT hypothesis in the practice of radiation protection. Unfortunately, many people are now placing an entirely unwarranted level of confidence in the accuracy and validity of risks that are estimated using it. The LNT assumption is simple to apply and it is claimed by its advocates to be a reasonable and conservative approximation, even by those who acknowledge that it may not be correct at very low doses. Others2 have criticised it as being seriously misleading in some applications. In June 2001, the American Nuclear Society (ANS) updated its own position statement on the health effects of low level radiation [5] to include the Position Statement "Radiation Risk in Perspective", issued by the Health Physics Society (HPS) in January 1996. It is now the position of both societies that there is insufficient scientific evidence to support the use of the LNT hypothesis in the projection of the health effects of low level radiation. The ANS recommends that an independent, multidisciplinary group of reputable scientists should be
2 An extreme view expressed by some critics of LNT, unfortunately, is that advocates of LNT are being unscientific and even dishonest. established to conduct an open scientific review of all data and analyses on this subject and that new, interdisciplinary research should be initiated on the health effects of low-level radiation. In the meantime, the ANS agrees with the HPS that quantitative estimation of health risks should not be made for individual doses less than 50 mSv in one year, or less than 100 mSv in a lifetime3, in addition to background radiation. The treatment of risks in this dose range should be strictly qualitative, accentuating a range of hypothetical health outcomes with an emphasis on the likely possibility of zero adverse health effects. Mitchel and Boreham [4] have reported that no actual scientific data support the LNT approach at occupational and public exposure levels. They have tested the LNT hypothesis and found that it is not consistent with laboratory observations of the responses of plants and animals, and of human and animal cells, to low or chronic doses of beta, gamma or x-radiation. They have also concluded that the “data indicate that the use of the LNT hypothesis and ALARA is not conservative, but may actually increase the overall risk of cancer.” This is a possibility that the radiation protection profession cannot afford to ignore.
RESOLVING THE CONTROVERSY Controversy about the health effects of low levels of ionising radiation, and the LNT hypothesis in particular, does not serve any legitimate purpose but it will not be going away until it is resolved. A major programme of work to investigate the potential for health benefits (hormesis) from exposure to low level radiation is therefore imperative. This matter cannot be ignored for ever. Mitchel and Boreham [4] appear to be making good progress in laboratory investigations of the biological mechanisms that might explain, and help to quantify, hormesis in human populations. However, more is needed. Most (if not all) significant epidemiological studies appear to be directed toward the investigation of harm, not hormesis. Funding and effort should be provided for more objectively based studies. In the meantime, the public must have adequate reassurance of safety, but it needs to be recognised that the assumption of LNT has had some unfortunate consequences, as outlined above in the introduction to this paper. Even if the possibility of radiation hormesis were to be completely set aside, none of these consequences should be seen as being in society’s best interests. In other fields, risks are consciously accepted to derive benefits. It is widely recognised that most human activities (even being at home) involve risks, and that the dictionary concept of safety as being “freedom from risk” is not attainable. Nevertheless, when it comes to the uses of low level radiation and radioactive materials, zero (or extraordinarily low) risk tends to be sought by many. This paper therefore suggests a pragmatic way towards the perception and regulation of radiological risks, giving due cognisance to all the conflicting points of view, as follows: 1. It must surely be agreed by anyone who has studied this subject that a single acute dose up to 10 mSv (50 mSv for adults), or a total chronic dose rate up to at least 20 mSv per year,
3 It would not be unreasonable to extend the latter figure to 1,000 mSv in a lifetime. causes no discernible harm4 to humans5. This is regardless of the source of exposure. However, 20 mSv per year is well within the range of variations in natural background radiation around the world. Natural radiation is generally accepted as harmless and it causes no concern to the public. Hence, these levels of exposure can reasonably be described as “safe”. 2. The vast majority of the world’s population is exposed to background dose rates that are significantly less than 10 mSv per year, i.e. less than half the level described above as “safe”. In this environment, 10 mSv per year (the other half of the safe rate) could reasonably be regarded as safe for sources which are subject to regulation. It would then be a matter for national authorities to decide how to regulate radiological risks in the areas where natural background radiation exceeds 10 mSv per year, and whether to site nuclear installations in such areas. 3. It follows from 1 & 2 above that no regulatory action need be taken to avert exposure to dose rates less than 10 mSv per year, from sources which are subject to regulation, or to an acute dose less than 10 mSv provided the average rate over a number of years does not exceed 10 mSv per year. These figures apply to all members of the population. They could be increased to 50 mSv per year and 50 mSv (acute dose) for application to radiation workers who are subject to health physics monitoring.
CONCLUSIONS This paper leads to the proposal that no regulatory action need be taken to avert the exposure of any member of the general public to – S dose rates less than 10 mSv per year, from sources which are subject to regulation; or S an acute dose less than 10 mSv from any such source, provided the average rate over (say) a 5-year period does not exceed 10 mSv per year. These figures could be increased by a factor of five for application to radiation workers who are subject to health physics monitoring. This is not to say that risks to a particular individual would be zero from doses at these levels (although they are likely to be trivial, if not zero), or that these doses would necessarily be beneficial to a particular individual (although there is significant evidence that they might be). However, the biological effects (if they exist) are not such as to warrant action to avert or change them. This would be an entirely pragmatic approach to finding a way through the controversy over the biological effects of exposure to low levels of ionising radiation. It would not resolve the scientific issues in this controversy but it is consistent with scientific observations. The proposed dose levels, below which there would be no need for regulatory action, could arguably be increased or decreased marginally. However, a variation by more than a factor of
4 “Harm” as defined in paragraph 42 of reference [3]. 5 Such exposures may, in fact, be inducing a discernible adaptive response to radiation [10,21]. about two (up or down) would, in the author’s opinion, reflect a concession to one or other of the extremes in this controversy. Even this small step toward reconciliation could only take place through the auspices of the radiation protection community. If our profession continues to maintain that radiation-induced risk must be assumed to be proportional to dose from zero, and regulated accordingly, it appears that there can be no resolution of the controversy.
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