AU0221612

Review of the Controversy on Risks from Low Levels of DR DONALD fflGSON, Consultant 260 Glenmore Road, Paddington, NSW 2021

SUMMARY: The need for regulation of low levels of radiation exposure, and the estimation of risks from such exposures, are based on the assumption that risk is proportional to dose without a threshold, the "linear no- threshold (LNT) hypothesis". This assumption is not supported by scientific data. There is no clear evidence of harm from low levels of exposure, up to at least 20 mSv (acute dose) or total dose rates of at least 50 mSv per year. Even allowing for reasonable extrapolation from radiation levels at which harmful effects have been observed, the LNT assumption should not be used to estimate risks from doses less than 100 mSv. and epidemiological evidence, and evolutionary expectations of biological effects from low level radiation, suggest that beneficial health effects (sometimes called "radiation ") are at least as likely as harmful effects from such exposures. Controversy on this matter strikes at the basis of practice.

1. INTRODUCTION might be expected that any such effect from chronic exposures would be on-going. Moreover, there are It has been well established by the work of the other effects of low level radiation at the cellular and Radiation Effects Research Foundation (RERF) in molecular level, particularly (see below). Hiroshima, Japan, that acute doses of ionising radiation greater than about 200 mSv cause an There is also considerable evidence that a dose increase in the incidence of cancer in human incurred at a low dose rate, or from intermittent populations. An "acute dose", in this context, is a exposures, is less likely to cause cancer than an acute dose that is incurred at a very high rate in a short exposure to the same total dose. One reason for this is space of time, as in an atomic bomb explosion or in that, me lower the rate of damage, the greater the some medical procedures. The controversy to be chance for cellular DNA repair to be effective. addressed in this paper is whether there are risks from lower levels of exposure and from low dose Experiments reported last year at the IRPA-10 rates. Congress by Mitchel and Boreham [4] showed that human and rodent cells, exposed to low doses and/or Unfortunately, this has become a contentious issue low dose rates, responded by increasing their ability even among scientists, with opinions often tending to correctly repair broken . Cells unable to be polarised. The author is simply an observer of to adequately repair their chromosomes were this controversy and he is not presenting any new sensitised to die by apoptosis. These responses of evidence in mis paper. However, he is attempting to cells reduced their risk of being transformed into consider the evidence on both sides without cancer cells by exposure to radiation, and also prejudice. protected mem against their own inherent, spontaneous risk of transforming into cancer cells. 2. LABORATORY AND CLINICAL EVIDENCE Most human cancers arise from DNA damage due to agents other than radiation. Hence, DNA repair Damage caused by ionising radiation to DNA in systems exist primarily for damage other man living cells can lead to risks of cancer in exposed radiation damage. If low doses of radiation enhance persons and risks of hereditary effects in their repair of any such damage, the net effect could be a descendants. The UK National Radiological reduction in overall risk, in spite of any risk Protection Board (NRPB) [1] and me United Nations increment due to the radiation itself Such an effect, Scientific Committee on the Effects of Atomic sometimes called "radiation hormesis", has been Radiation (UNSCEAR) [2] argue that even the observed in cells from virtually all types of lowest possible dose and dose rate (a single , in whole plants and animal species other radiation track traversing a single living cell) might than humans, and in human cells. result in incorrectly repaired DNA damage and hence lead to cancer. One of the more striking illustrations of an adaptive response to radiation has been reported by There is considerable evidence that low levels of Sakamoto and his co-workers in Japan [5]. radiation exposure may induce or activate cellular Beneficial effects in the treatment of cancer have DNA repair capacity, additional to that which exists been reported from repeated therapeutic whole- normally [3]. This "adaptive response" to radiation body and half-body doses of the order of 100-150 may reduce the effects of damage from subsequent mGy. It has been suggested that this effect may be doses of radiation or from other causes. The effect of due to stimulation of the immune system and, single doses appears to be transitory. However, it

55 hence, that stimulation of the immune system by the average being about 170 for those employed in radiation might help in the treatment of diseases 1986. Several thousand of them probably received other than cancer. The use of radiation to achieve doses greater than 500 mSv. The average effective such effects is, of course, a matter for the medical doses (excluding the thyroid) to more than 100,000 profession to pursue but it has implications for the people evacuated from the most contaminated areas balance between benefit and harm in radiation of Ukraine and Belarus were about 30 and 40 mSv protection. respectively. The maximum estimated total dose commitment (due to the accident) for persons who Clearly, there are bio-positive effects of low level were not relocated was reported to be 250 mSv, radiation, as well as any bio-negative effects that with the average for the 1,500 most highly exposed occur. The net effect, if there is one, may be too small members of this group being 160. to be of any practical significance. This is not simply a matter of thresholds to or A study [9] of cancer mortality among workers with , although thresholds may exist. Any protracted occupational exposures in the nuclear significant net effect on health should be expected to industry in other parts of the world (US, UK and vary from person to person and it is unlikely that it Canada) has found that there is "no evidence of an would be known in advance for any specific association between radiation dose and mortality individual. It is even conceivable that a specific from all causes or from all cancers" for individual exposure to radiation could be harmful to one person doses up to 100 mSv. Significant dose-related and beneficial to another. The net effect on an increases were found in mortality from multiple exposed population might be measurable only by myeloma and most types of leukaemia, but these . One day, it may be possible to assess increases appeared to be balanced by dose-related the probability of such an effect individually. decreases for some other types of cancer. Tests of Currently, epidemiology appears to be important in statistical significance were applied to the increases the evaluation of this probability, viz: as an average in mortality which were observed but apparently for members of the exposed population. not to the decreases. 3. EPIDEMIOLOGICAL EVIDENCE Some other studies of this type, for example a recent study of health records of the Lucas Heights 3.1 Exposures caused or enhanced by "man" workforce [10], have shown that radiation workers As mentioned earlier, it is well established that have lower mortality rates from all causes and from "man-made" doses of ionising radiation greater all cancers than the general population (and than about 200 mSv cause an increase in the sometimes lower than other workers). This is incidence of cancer. Studies of the atomic bomb usually written-off as the "healthy worker" effect, survivors and the consequences of some medical but prompts the question: "are radiation workers exposures provide evidence that risks of increased more healthy because they are exposed to cancer may extend to doses less than 200 mSv radiation?" [6,7], but with lower levels of statistical significance. Wakeford [8] believes there is A clear risk of lung cancer, due to high levels of evidence that risks exist down to about 10 mSv but exposure to gas in poorly ventilated this (like many other matters relating to the effects underground mines, has been observed from of low doses) is controversial. occupational exposures of uranium miners which occurred before the potential for such a hazard was Acute radiation sickness and early fatalities of recognised. Many studies have been conducted of workers who were at the Chernobyl reactor at the the possible risk of lung cancer due to time of the accident in 1986, and thyroid cancers environmental radon in homes, which is usually at among children in the district around Chernobyl, much lower levels than in underground uranium were associated with high doses of radiation. Risks mines. The results range from positive to negative of thyroid cancer are still being evaluated. correlations. For example, Cohen [11] observed that UNSCEAR [2] has reported no evidence of any the higher exposures to domestic radon correlated other health effects attributable to radiation with the lower incidences of cancer (a negative exposures from Chernobyl. In particular, there has correlation), whereas Lubin and Boice [12] have been no increase in the incidence of cancer, apart reported a positive correlation. from the child thyroid cancers. The incidence of leukaemia, one of the main concerns due to its short 3.2 Natural exposures latency period (5-10 years after radiation exposure Natural is the main source of in adults), is not elevated in any of the exposed exposure for most people, and it is therefore a major groups, including the emergency response workers. potential source of information on the effects of radiation exposure. As would be expected, chronic This is despite the fact that about 100,000 workers exposure appears to cause less risk than acute involved in (he emergency responses and cleanup exposure to the same total dose. The dose rate from of Chernobyl incurred doses in excess of 100 mSv, background radiation ranges around the world from

56 less than 1 to more than 100 inSv per year locally, 33 Discussion of epidemiology with lifetime doses up to several thousand mSv, but there is no conclusive evidence of increased The lack of clear evidence of risks from low doses incidences of cancer or other adverse health effects of "man-made" or "man-enhanced" radiation may at the higher levels of radiation. Populations be because there are no harmful effects of radiation exposed to very high environmental dose rates for at such low levels or because the health effects, long periods, and for many generations, may well whatever they may be, are too few to be statistically be too small for reliable statistically based significant. The "absence of evidence" of such conclusions to be drawn. However, it can effects should not be confused with "evidence of reasonably be said that exposures to chronic dose absence". rates up to (say) 50 mSv per year are not doing any On the other hand, mere are many observations of demonstrable harm ("harm" as defined in paragraph apparently bio-positive effects of radiation in human 42 of reference [6]). populations, which are consistent with the laboratory observations of an adaptive response (discussed In fact, the reverse has been reported [11,13,14], viz: earlier) and the evolutionary expectation (discussed comparatively low rates of cancer have been observed below). Hence, it is reasonable to postulate that where levels of radiation are comparatively high. For radiation hormesis may occur in humans, although example, Jagger [13] has compared radiation levels the reasons for it and its overall significance are not and cancer mortality rates in three Gulf Coast states fully understood. Many scientists who have studied and three Rocky Mountain states of the US, and this matter consider that evidence of radiation estimated that - hormesis in humans is conclusive. Luckey [14] • the average natural background level of radiation suggests that the dose rate for optimal health is about is 3.2 times higher in the Rocky Mountain states, 10 mSv per year. Others reject the possibility of but the total cancer rate is 21% lower, than in the hormesis out of hand, or ignore it. Gulf Coast states; and It should be recognised that epidemiology tends to • the average radon level in air is 3.9 to 5.2 times be a rather "blunt instrumenf' at the best of times higher in the Rocky Mountain states, but the lung and that some studies, which are said to be cancer rate is 31% lower, than in the Gulf Coast epidemiological, tend to be very fuzzy. Other states. studies are carefully case-controlled, with allowances for confounding factors built in from A problem with epidemiological studies conducted in the beginning. It can be argued that none of the the USA is said to be that the population is far too claimed observations of radiation hormesis in mobile. This contrasts with the situation in much of humans is the finding of a properly conducted China, where populations have been stationery for epidemiological study. Jagger [13] himself (see thousands of years and have moved little even findings above) states: "It is possible that recently because of restrictions on movement confounding factors, such as smoking, poverty, or between regions. Of 150,000 Han peasants, living environmental pollution contribute to the near each other for six generations, about half differences... (but) the factor of disproportion is so receive around three times the background radiation great... that it strains credulity to assume that such exposure of the other half. Various studies of doses confounding factors could reverse ... (the) ... and health effects have shown either that there are correlation." Unfortunately, it appears that funds no discernible differences in the health of these and effort for major epidemiological studies tend to populations OTtha t mortality rates for some cancers be forthcoming only when harmful effects are to be and other adverse health effects are lower in the investigated, not for beneficial effects. It has also more highly exposed population. been suggested mat studies have sometimes been In 1999, there was a preliminary report of a 9-year commissioned with the specific aim of government funded study of 100,000 inhabitants of demonstrating that harmful effects occur. a small coastal area in Kerala, southern India, 4. HEREDITARY EFFECTS where background radiation (mainly due to in beach sands) is up to 30 times the global average. Where there is a risk of cancer, there is a risk of Further information on this work has been filtering genetic damage, which might cause hereditary through, to the effect that no excess incidence of effects. At high doses and high dose rates, radiation cancer had been found in the region and that cancer certainly has discernible effects at the molecular and rates may be lower than in other parts of India cellular level that change genetic material in living where radiation levels are lower. The final report organisms, and there is substantial evidence of has not yet come to hand and it will be interesting hereditary effects in non-human species. There is no to see whether biologically positive effects of direct evidence that radiation causes hereditary effects radiation were found (or sought). in humans, although it must be assumed that it may do so.

57 At low doses and low dose rates, the position is January 1996. It is now the position of the ANS that similar to that for cancers, as follows: Hereditary there is insufficient scientific evidence to support effects have many causes not attributable to ionising the use of the LNT hypothesis in the projection of radiation, and no specific case could be identified the health effects of low level radiation. The ANS with certainty as being caused by exposure to recommends that an independent, multidisciplinary radiation. If there is a change in the total incidence of group of reputable scientists should be established hereditary effects in humans, due to low levels of to conduct an open scientific review of all data and radiation exposure, it is too small a change to be analyses on this subject and that new, determined. interdisciplinary research should be initiated on the health effects of low-level radiation. In the Genetic effects of radiation may have been an meantime, the ANS agrees with the HPS that important factor in the evolutionary process. The quantitative estimation of health risks should not be human race (as it now exists) represents only the made for individual doses less than 50 mSv in one small, successful part of all the trials and errors of year, or less than 100 mSv in a lifetime, in addition evolution. Parsons argues that radiation hormesis to background radiation. The treatment of risks in must be expected because evolution has occurred in this dose range should be strictly qualitative, the presence of ionising radiation [15]. During the accentuating a range of hypothetical health evolution of life on earth, natural background outcomes with an emphasis on the likely possibility radiation has previously been substantially higher of zero adverse health effects. than it is today and it has ranged (in space and time) from less than 2 to significantly more than 20 mSv Mitchel and Boreham [4] have reported that no per year for the human race, during its evolution. actual scientific data support the LNT approach at occupational and public exposure levels^. They It is a fundamental tenet of evolutionary biology have tested the LNT hypothesis and found that it is that organisms adapt to their environment. Fitness not consistent with laboratory observations of the measures, including health, longevity and resistance responses of plants and animals, and of human and to diseases, should be maximal for organisms in the animal cells, to low or chronic doses of low LET habitats in which they normally occur. The radiation. This does not, by itself, obviate the utility evolutionary expectation leads to what Parsons calls of the LNT hypothesis in the practice of radiation "background radiation hormesis", viz: because protection. The LNT hypothesis is simple to apply radiation is part of our normal environment on and, in so far as it defines the upper boundary to the earth, it follows that fitness should be at its highest range of uncertainty in radiological risk estimation, within the range of natural background radiation - it is usually considered to be conservative. somewhere between (say) 2 and 20 mSv per year. However, Mitchel and Boreham have also This effect has been well-documented in lower concluded: "data indicate that the use of the LNT organisms. hypothesis and ALARA* is not conservative, but Parsons also postulates, on the basis of evolutionary may actually increase the overall risk of cancer." biology, that "stress-derived radiation hormesis" This is a possibility that the radiation protection should be expected from short bursts at 100-1000 profession cannot afford to ignore. times background levels. Gonzelez [17] has pointed out that regulators can 5. THE LNT HYPOTHESIS only regulate radiation exposure that is attributable to a particular source. Source-related exposures are For radiation protection purposes, the International incurred in addition to the prevalent background Commission on Radiological Protection 0CRP) exposure, which is 2.4 mSv per year on average and recommends the assumption that the risk of radiation typically up to 10. However, background radiation induced cancer is proportional to dose without a exceeds 100 mSv per year in some places. Given threshold [6]. The use of this assumption, the "linear the ubiquitous of radiation and the practical no-threshold (LNT) hypothesis", was reconfirmed in feet that regulators cannot change standards from June 2000 by UNSCEAR [2]. However, the words "for radiation protection purposes" are essential. The LNT hypothesis is not intended to be used, for 5 The occupational dose limit recommended by the example, to estimate the number of casualties due ICRP is 20 mSv per year, averaged over a 5-year to an accidental release of radioactive material (viz: period, with a maximum of 50 mSv in any one year. multiplying very large numbers of people by the The recommended dose limit for members of the very small doses to which they might be exposed). public is 1 mSv per year [6]. In June 2001, the American Nuclear Society (ANS) * ALARA is the acronym for the ICRP's updated its own position statement on the health recommendation that radiation exposures from any effects of low level radiation [16] to include the particular source should be "as low as reasonable Position Statement "Radiation Risk in Perspective", achievable", economic and social factors being issued by the Society (HPS) in taken into account [6].

58 place to place, Gonzalez argues that the relevant community. On the one hand, ICRP-adherents exposure is the highest background level that exists. promote the view that LNT can be extrapolated At those levels, the biological effects of radiation reliably, over more than four orders of magnitude in exposure can be observed under the microscope terms of dose and over an even greater range in even though harm may not be evident. (Paragraph terms of dose rate, to estimate cancer fatality risks 42 of ICRP-60 [6] clearly distinguishes between from dose rates down to zero - or, at least, down to change, damage and harm. Changes that can be 0.02 mSv per year. Those who disagree are at risk observed are not necessarily harmful.) of being ostracised. There may well be a better case for applying the At the other extreme, there are claims that public LNT hypothesis to dose increments above 100 mSv fears about low level radiation are being per year than there is for dose increments above 2.4 deliberately exploited for a variety of improper mSv per year. However, the logical conclusion to purposes. One critic of LNT in the US has stated Gonzalez' argument is that Australian authorities, that the head of a national radiation protection who are planning the establishment of a radioactive authority accused him, at an international waste repository where the background radiation is conference, of trying "to kill the golden goose". around (say) 2 mSv per year, should be constrained to ensure that the increment of individual dose from The radiation protection profession is the meat in its operation is less than 0.1 mSv per year because this sandwich. For its members, the LNT background dose rates in some parts of the world hypothesis is a convenient tool, without which their (e.g. at Ramsar in Iran) are higher than 100 mSv per work would be difficult to perform. Most of them year. It might also be claimed that Gonzalez' are not involved in research. Their job is to apply argument justifies the expenditure of billions of nationally approved standards, not to question those dollars to meet an environmental protection standards or evaluate the results of research or standard of 0.15 mSv per year in the clean up of develop independent ideas about radiological risks. contaminated sites in the US, regardless of whether It does not seem possible to know for sure whether there are or are not risks from such exposures. there are risks from low level radiation, although Perhaps it would be controversial to suggest that some people are obviously convinced that they do. national regulatory authorities could set standards On the other hand, it may be possible to find out for to suit conditions within their national boundaries. certain whether there can be health benefits from exposure to low level radiation. There is a lot that 6. CONCLUDING REMARKS we might be able to find out about radiation hormesis, if we chose to do so, for example: It is generally agreed that the lowest dose at which a statistically significant increase in the incidence of • Does radiation hormesis really occur in cancer has been shown to occur is about 100 mSv. humans? This risk has been observed from doses incurred at very high dose rates, as in an atomic bomb explosion • If so, what are the relevant dose-response or from some medical procedures. There is a wide relationships? range of disagreement about the biological effects of Mitchel and Boreham [4] appear to be making good lower doses and low dose rates. In recent years, it progress in laboratory investigations of the biological has become clear mat many scientists are concerned mechanisms that might explain, and help to quantify, that the practices of radiation protection and hormesis in human populations. However, most (if regulation, applied to low levels of radiation, are not not all) significant epidemic-logical studies appear to consistent with the scientific evidence. be directed toward the investigation of harm, not The main reason for the belief that there are risks hormesis. Funding and effort should be provided for from low level radiation is mat the ICRP recommends more objectively based studies, and opportunities for the use of the LNT hypothesis in the practice of such work do exist. Apart from those small areas of radiation protection. Unfortunately, many people are the world (like Kerala and Ramsar) where now placing an entirely unwarranted level of background radiation levels are extremely high, and confidence in the accuracy and validity of risks that the different regions of the USA (which are the are estimated using it The LNT assumption is almost subject of Jagger's paper [13]) with many millions of certainly not correct, but is claimed by its advocates population and good health records, there are to be a reasonable and conservative approximation. significant areas in the UK (for example) and elsewhere in Europe where background radiation Others have criticised it as being seriously misleading levels are high. in some applications. Controversy about the health effects of low levels I have been told mat Boulder, Colorado, where the of ionising radiation, and the LNT hypothesis in background dose rate is around three times the particular, has become polarised to an extent which national average for the US, is home to one of the should be considered unacceptable in a rational principle centres of the Green movement in that country. This prompts me to leave you with the

59 question: "Would any of you let an environmental [8] Wakeford, R. (2001), from a private dose rate between 1 and 10 mSv per year determine communication. your choice of where to live?" [9] Cardis, E., Gilbert, E.S. et al (1995), References Effects of Low Doses and Low Dose Rates of External : Cancer [1] National Radiological Protection Board Mortality among Nuclear Industry (1995), Risk of Radiation-induced Cancer at Workers in Three Countries. Radiation Low Doses and Low Dose Rates for Research, 142, 117-132,1995. Radiation Protection Purposes. Documents oftheNRPB, 6(1), 1995. [ 10] Habib, R. (2001), doctoral thesis submitted to the University of New South Wales. [2] United Nations Scientific Committee on the Effects of Atomic Radiation (2000), Report [11] Cohen, B.L. (1995), Test of the Linear No- to the General Assembly, 6 June 2000. threshold Theory of Radiation Carcinogenesis for Inhaled Radon Decay [3] United Nations Scientific Committee on the Products. Health Physics, 68,157,1995. Effects of Atomic Radiation (1994), Adaptive Responses to Radiation in Cells [12] Lubin, J.H. and Boice, J.D. (1997), Lung and Organisms. Document A/AC.82/R.542, Cancer Risk from Residential Radon: Meta- approved 11 March 1994. analysis of Eight Epidemiological Studies. J. National Cancer Inst., 89 (1), 49-57, Jan.l, [4] Mitchel, R.E.J. and Boreham, D.R. (2000), 1997. Radiation Protection in the World of Modern : Time for a New [13] Jagger, J. (1998), Natural Background Approach. 10th International Congress of Radiation and Cancer Death in Rocky the International Radiation Protection Mountain States and Gulf Coast States. Association (IRPA-10); May 14-19, 2000; Health Physics, 75(4), 428, October 1998. Hiroshima, Japan; PS-1-2, P-2a-87. [14] Luckey, T.D. (1991), Radiation Hormesis. [5] Sakamoto, K., Myojin, M. et al (1997), CRC Press. Fundamental and Clinical Studies on [15] Parsons, P.A. (2000), Hormesis: an Cancer Control with Total or Upper Half Adaptive Expectation with Emphasis on Body Irradiation. J. Jpn. Soc. Ther. Ionizing Radiation. J. Appl. Toxicol., 20, Radiol. Oncol., 9,161-175,1997. 103-112,2000. [6] International Commission on Radiological [16] American Nuclear Society (2001), Health Protection, 1990 Recommendations of the Effects Of Low-Level Radiation. Position International Commission on Radiological Statement 41 on WebSite www.ans.org Protection. ICRP Publication 60, Pergamon (for which an Acrobat Reader will be Press, Oxford (1990). needed). [7] Pierce, D.A. and Preston, D.L. (2000), [17] Gonzalez, A. (2000), Regulating Radiation-Related Cancer Risks at Low Radioactive Waste: Real & Perceived Doses among Atomic Bomb Survivors. Issues. IAEA Bulletin, 42 (3), 2000. Radiation Research 154,178-186,2000.

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