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The scientific jigsaw puzzle: Fitting the pieces of the low-level debate Jan Beyea Bulletin of the Atomic Scientists 2012 68: 13 DOI: 10.1177/0096340212445025

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Feature Bulletin of the Atomic Scientists 68(3) 13–28 ! The Author(s) 2012 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav The scientific jigsaw puzzle: DOI: 10.1177/0096340212445025 Fitting the pieces of the http://thebulletin.sagepub.com low-level radiation debate

Jan Beyea

Abstract Quantitative risk estimates from exposure to are dominated by analysis of the one-time exposures received by the Japanese survivors at Hiroshima and Nagasaki. Three recent epidemiologic studies suggest that the risk from protracted exposure is no lower, and in fact may be higher, than from single exposures. There is near-universal acceptance that epidemiologic data demonstrates an excess risk of delayed cancer incidence above a dose of 0.1 (Sv), which, for the average American, is equivalent to 40 years of unavoidable exposure from natural . Model fits, both parametric and nonparametric, to the atomic-bomb data support a linear no-threshold model, below 0.1 Sv. On the basis of biologic arguments, the scientific establishment in the United States and many other countries accepts this dose-model down to zero-dose, but there is spirited dissent. The dissent may be irrelevant for developed countries, given the increase in medical diagnostic radiation that has occurred in recent decades; a sizeable percentage of this population will receive cumulative doses from the medical profession in excess of 0.1 Sv, making talk of a threshold or other sublinear response below that dose moot for future releases from nuclear facilities or a . The risks from both medical diagnostic doses and nuclear accident doses can be computed using the linear dose-response model, with uncertainties assigned below 0.1 Sv in a way that captures alternative scientific hypotheses. Then, the important debate over low-level radiation exposures, namely planning for accident response and weighing benefits and risks of technologies, can proceed with less distraction. One of the biggest paradoxes in the low-level radiation debate is that an individual risk can be a minor concern, while the societal riskÑthe total delayed cancers in an exposed populationÑcan be of major concern.

Keywords atomic bomb, debate, dose, linear no threshold model, low level radiation, one time exposure, protracted exposure, radiation, risk

o those outside the scientific com- exposuresÑthe kind that would be munity, it might come as a surprise expected from releases from nuclear T that, until 2005,1 essentially no reactors or dirty bombs. Historically, large-scale epidemiologic studies dir- atomic-bomb dataÑwhich look at the ectly demonstrated the existence of one-time exposures to Hiroshima and risks related to protracted radiation Nagasaki survivorsÑhave dominated

Downloaded from bos.sagepub.com at Stanford University Libraries on November 19, 2012 14 Bulletin of the Atomic Scientists 68(3) quantitative risk estimates for any type into the political sphere, wrapping itself of low-level exposure to ionizing radi- around arguments on energy policy and ation, including protracted exposure. the consequences of radioactive releases The standard approach to calculating like those at Chernobyl and the risk estimates for long-term exposure Fukushima Daiichi Nuclear Power has been to use biologic argu- Station. Quantitative estimates of mentsÑthat is, concepts of cancer initi- health risks affect public policy, ation, promotion, and repair, coupled although sometimes it takes many dec- with data from cellular experimentsÑto ades before scientific studies affect conclude that long-term exposure regulations (see Brock and Sherbini, entails lower risk than sudden exposure, 2012, in this issue of the Bulletin). by a factor of two to ten (Healy, 1981); Likewise, it also may take years before only in the last decade has the scientific these studies trickle down to the public community unofficially settled on a and industry stakeholders. factor of two (Preston, 2011; UNSCEAR, To some in the public, the quantita- 2006). tive aspects determined by experts are Presumably, a factor of two should irrelevant; they argue that experts are have had a rather minor impact on not to be trusted and that the existence policy, which should have meant a of any imposed risk of cancer is quick end to this portion of the story unacceptable. Others believe that evolu- on low-dose radiation risks. No such tion has provided humans with repair luck. In fact, there has been, and con- mechanisms that protect against natural tinues to be, considerable debate background radiation; they reason that among members of the scientific com- the radiation risk at doses close to the munity, political and industry leaders, background is, in fact, zero. But for and the public around the claim that researchers in the field, and committees atomic-bomb data is relevant to estimat- of scientists trying to reach consensus ing risks from protracted exposures. and assemble what amounts to a scien- This debate has contributed to the tific jigsaw puzzle, reaching quantitative delay in updating some US regulatory conclusions about risk is not so simple. dose limits that are based on a pre-1990 Researchers cannot solely rely on gut understanding of radiation risks. instincts; they must analyze data, scru- Three new studies could very well tinize their findings, and rigorously change the balance of the debate, as defend these findings. knowledge of themÑone on off-site citi- Though the debate takes on many zens and two on radiation workersÑ shapes, it always revolves around one percolates into the wider discussion. magical number: 0.1 sievert (Sv), the dividing line between what is con- Deconstructing the debate sidered high and low exposure today. It is equivalent to about 40 cumulative The debate over radiation risks has years of the average unavoidable back- many tentacles that extend into the ground radiation and to about 40 years fields of biology, , medi- of average medical diagnostic radiation cine, sociology, and political science. in the United States (Einstein, 2009; The biggest tentacle penetrates directly NCRP, 2009).2 And from this magical

Downloaded from bos.sagepub.com at Stanford University Libraries on November 19, 2012 Beyea 15 number, more disputes spring, specific- quantitative risk estimates todayÑis ally on the radiation risks below 0.1 Sv, as that the vast data set, including regular well as the risks from protracted radi- follow-ups on the study population, has ation exposures above and below this produced consistent epidemiologic number. The debates can be brutalÑso results, providing little room for conten- much so that, at times, they make the tion on the radiation risks related to acute spats between William Jennings Bryan exposures above 0.1 Sv. Despite some and Clarence Darrow look tame. limitations (see Richardson, 2012, in this issue of the Bulletin), analysis of the One-time exposure above atomic-bomb dose data presents a clear the dividing line picture that a linear no-threshold (LNT) modelÑthe theory that radiation risk Since the United States dropped atomic declines in proportion to dose, but bombs over Hiroshima and Nagasaki in never goes to zeroÑ holds for a large 1945, it has worked with Japan to pro- range of survivor doses (see Figure 1).3 duce 14 periodic joint reports, known But atomic-bomb data, some argue, as Life Span Studies, on the fate of focus on high doses and are there- more than 80,000 bomb survivors. fore irrelevant to the low-dose debate.7 What makes these regular reports so for- However, as Figure 1 shows, the data mativeÑand why analysis of the atomic- set contains a wide-range of dosesÑ bomb data continues to dominate including those that are quite relevant to

1.5

1

.5 Excess relative risk

0

0123 Weighted colon dose (Gy)

Figure 1. Solid cancer-incidence dose response for atomic-bomb survivors. Source: Preston et al. (2007). This figure is reproduced with permission from the Radiation Research Society. Notes: This figure shows excess relative risk versus “weighted colon dose” in units of (Gy)Ñthese units are equivalent to Sv.4 The solid line represents a smoothed version of the data that does not assume the data are linear.5 Dashed curves represent one standard deviation. Note the tight error bands around the central curve. The horizontal access on the chart refers to colon dose, which is taken as a surrogate for the tissue dose to all organs; this may differ slightly. Each small tick mark corresponds to 0.2 Gy; half of this is what is considered to be low-dose radiation today. The vertical axis has units of excess relative risk (ERR) that have been found to fit radiation data better than absolute risk models.6 It is important to note that this figure illustrates a dose response for an entire population.

Downloaded from bos.sagepub.com at Stanford University Libraries on November 19, 2012 16 Bulletin of the Atomic Scientists 68(3) occupational exposure limits, as well as are diagnosed five years to more than 50 those that match accumulated background years after exposure. Delayed cancers are radiation and medical-diagnostic doses, the usual focus of the low-level radiation which are normally considered to be low. debate, but delayed stroke and heart dis- Bear in mind that these doses are in add- ease account for Òabout one third as ition to the natural background radiation many radiation-associated excess deaths that the survivors had already received. as do cancers among atomic bomb sur- Over the decades, as new excess can- vivorsÓ (Shimizu et al., 2010). cers have emerged in the atomic-bomb cohort at lower and lower doses, the Protracted exposures above number that defines Òlow doseÓ has the dividing line shrunk fivefold to its current value of 0.1 Sv. At the same time, the estimated For years, nuclear power advocates have risk has risen tenfold since 1980;8 thus, argued that the atomic-bomb cancer data it is of little surprise why there is conti- were insignificant to regu- nuing concern about low-dose radiation. lations and irrelevant to nuclear reactor So the natural question is: When will risk assessmentsÑnot just because the the estimated-risk increases stop? atomic-bomb doses were supposedly too Fortunately, further dramatic changes high, but because the bomb exposures are not expected in the atomic-bomb occurred suddenly. These advocates, dataÑcertainly not for adults at doses along with a number of researchers, above 0.1 SvÑbecause a sufficient argued that the bodyÕs DNA repair mech- number of excess cancers has ensured anisms assist in the recovery from slow tight confidence bounds, or limits.9 exposures caused by routine reactor Epidemiologic data can include many releases. Even doses from accidental individual variations, including sub- releases would not be as bad as atomic- groups of people with different genetic bomb doses, these advocates claimed, susceptibilities (see Greenland, 2012, and because radioisotopes in the body or on Richardson, 2012, both in this issue of the the ground decay with predictable half- Bulletin). These variations are too often lives, protracting the radiation dose.10 But lost in the debate over low-level radi- conventional wisdom was upset in 2005, ation effects. For instance, some when an international study, which researchers argue that raw, dose-cate- focusedonalargepopulationofexposed gory data, specific to children, indicates nuclear workers, presented results that an LNT response down to 0.01 Sv. shocked the commu- Further evidence of a strong difference nityÑand foreshadowed a sequence of in susceptibilities among groupsÑsuch research results over the following years. as from DNA sequence variationsÑmay lead to calls for tighter health and indus- 15-country nuclear worker data try regulations (Locke, 2009). The LNT theory predicts that back- It all started when epidemiologist Elaine ground radiation exposure and medical Cardis and 46 colleagues surveyed some diagnostic exposures slightly increase a 400,000 nuclear workers from 15 coun- populationÕs future cancer rates. The tries in North America, Europe, and cancers donÕt appear immediately but AsiaÑworkers who had experienced

Downloaded from bos.sagepub.com at Stanford University Libraries on November 19, 2012 Beyea 17 chronic exposures, with doses measured another blow to the theory that pro- on radiation badges (Cardis et al., 2005). tracted doses were not so bad. This The prediction of total excess cancers 2009 report looked at 175,000 radiation for these nuclear workers was striking: workers in the United Kingdom, and Cancer deaths in this population was an update to earlier reports of the increased by 1 to 2 percent, making past same data set. Sufficient diseases had nuclear work a rather dangerous indus- appeared since the previous assessment, trial occupation relative to others. making the cancer risk statistically sig- (It should be noted that CardisÕs study nificant and the same as in the atomic- looked at workers exposed many years bomb data. Again, protracted exposures ago, when efforts to reduce workersÕ did not turn out to be less dangerous radiation exposure were less effective than acute exposures. than they are today.) This study revealed a higher inci- 12 worker studies combined dence for protracted exposure than found in the atomic-bomb data, repre- After the UK update was published, sci- senting a dramatic contradiction to entists combined results from 12 post- expectations based on expert opinion. 2002 occupational studies, including Further, this challenged the relevance the two mentioned above, concluding of cell dose-rate experiments to human that protracted radiation was 20 percent epidemiology. However, the dose more effective in increasing cancer rates response did not include as tight error than acute exposures (Jacob et al., 2009). lines as in the atomic-bomb data. Even The studyÕs authors saw this result as a though the incidence data were statistic- challenge to the cancer-risk values cur- ally significant, some researchers, along rently assumed for occupational radi- with industry and medical radiation ation exposures. That is, they wrote advocates, quickly attacked the study. that the radiation risk values used for Seizing on the data from CanadaÑthe workers should be increased over the country with the highest excess relative atomic-bomb-derived values, not low- risk (ERR)-per-Sv rateÑthe critics con- ered by a factor of two or more. tended that the study was flawed; they If history is any guide, it is question- charged that it be repudiated by the able that this analysis and the results of authors, which it never was. Atomic other studies will lead to actual changes Energy of Canada LimitedÕs industry in what defines worker-exposure limits. consultants continue to focus on the Industry pushback is very strong, as can Canadian segment of the data, particu- be seen by the efforts of the California- larly on the reliability of the dose esti- based Electric Power Research Industry mates.11 Their relentless attacks have (EPRI), a nonprofit energy consortium. been effective in neutralizing the study, In 2009, the group issued a damning despite the authorsÕ defenses.12 report that dismissed all of the new, high results in the 12 occupational stu- dies, citing the work as either flawed or UK radiation workers irrelevant to the exposures received by A second major occupational study the most exposed nuclear workers appeared a few years later, delivering (EPRI, 2009), which, EPRI says, are

Downloaded from bos.sagepub.com at Stanford University Libraries on November 19, 2012 18 Bulletin of the Atomic Scientists 68(3) around 0.02 Sv per year. Their concerns exposure, before any linear fit is made. about the irrelevance of protracted stu- The distinction between acute and dies are puzzling, because an annual chronic exposures no longer exists in exposure at 0.02 Sv over a period of 10 epidemiologic data. But as with the years would be 0.2 SvÑan accumulated 15-country study, the Techa River study exposure well above the low-dose divid- was attacked, particularly on the reli- ing line of 0.1 Sv. ability of doses. EPRI discounted the study, claiming it contradicted other stu- dies on low background-radiation areas Techa River data in India and China. However, EPRI So what about the risks to the general failed to mention in its 2009 report the population? In 2007, one studyÑthe limitations of such studies in high- first of its sizeÑlooked at low-dose radi- background-radiation regions,14 not to ation risk in a large, chronically exposed mention that the confidence bounds civilian population; among the epi- around the estimate were consistent demiological community, this data set with the risks from the atomic-bomb is known as the ÒTecha River cohort.Ó study (Tao et al., 2012). From 1949 to 1956 in the Soviet Union, Too much is at stake in terms of the while the Mayak weapons complex cost of worker and public protection to dumped some 76 million cubic meters expect the nuclear industry to be any- of radioactive waste water into the thing but skeptical of studies that under- river, approximately 30,000 of the off- mine past practices and positions. The site populationÑfrom some 40 villages industry will want unequivocal evi- along the riverÑwere exposed to dence. Thus, the debate over protracted chronic releases of radiation; residual exposures will continue, probably even contamination on riverbanks still pro- after the next US National Academy of duced doses for years after 1956. Sciences and the Institute of MedicineÕs Here was a study of citizens exposed Biological Effects of Ionizing to radiation much like that which would (BEIR) scientific committee issues a be experienced following a reactor acci- communal judgment five to ten years dent. About 17,000 members of the from now.17 cohort have been studied in an inter- national effort (Krestinina et al., 2007), Protracted exposures below the largely funded by the US Energy dividing line Department; and to many in the depart- ment, this study was meant to defini- Though they inspire and instigate tively prove that protracted exposures forward-thinking research, the above were low in risk. The results were unex- studies do not put the debate over low- pected. The slope of the LNT fit turned risk radiation to rest. In fact, the debate out to be higher than predicted by the goes beyond this, to an even thornier atomic-bomb data, providing additional issue: namely, the dose response below evidence that protracted exposure does the divide at 0.1 Sv.18 The debate over not reduce risk.13 Furthermore, as seen in low doses is as intense as the debate Figure 2, the raw data showed cancer over protracted-versus-acute exposure. excess around 0.1 Sv of protracted Why? Because doses in this range are

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.6

.4

.2 Excess relative risk

0

0.1.2.3.4 .5 Weighted colon dose (Gy)

Figure 2. Solid cancer-incidence dose response for the Techa River cohort. Source: Krestinina et al. (2007). This figure is reproduced with permission from the authors; ! Oxford University Press. Notes: This figure shows excess relative risk versus weighted dose in units of Gy (equivalent to Sv for the purposes of this article).15 The solid line represents the linear fit. The thick dashed line represents a nonparametric fit to the data.16 The thinner dashed curves represent one standard deviation. The scale of the dose axis is expanded compared with Figure 1, with tick marks in this graph set to intervals of 0.1 Gy. The bounds on the curves are quite wide. And the slope is higher than for the atomic-bomb survivor curve in Figure 1. those of most concern to a public skep- Sv, particularly below 0.01 Sv, are noth- tical about nuclear powerÕs side effects. ing to worry about, while nuclear activ- Without low-dose risk estimates, it is ists contend they are very dangerous. not possible to predict the full conse- Personal interests can play a role in fan- quences of events like Fukushima and ning the flames of the debate. In sum- Chernobyl; it is not possible to make mary, there are scientific, medical, estimates of the consequences of relying governmental, and political reasons for on nuclear power; nor is it possible to knowing the risks below 0.1 Sv: for exam- understand the consequences of relying ple, creating an informed public, choos- on a high-level waste-storage site like ing energy sources, advancing scientific Yucca Mountain. knowledge, facilitating an appropriate Medical-diagnostic doses also often balance of risks from medical diagnos- fall in this range, although the public is tics. But there are obstacles, as well: less concerned about them than doses like sabotaging lucrative business ven- from nuclear power or nuclear waste tures and potentially amplifying risk (see Slovic, 2012, in this issue of the perceptions. Bulletin). Still, doctors, public health officials, emergency planners, and Setting the record responders need to understand the risks at these doses. Experts, governments, industry, and the Some public officials and nuclear public arenÕt left to their own devices to energy supporters say doses below 0.1 settle this debate. Due to the complex

Downloaded from bos.sagepub.com at Stanford University Libraries on November 19, 2012 20 Bulletin of the Atomic Scientists 68(3) of the issueÑand the many opin- The BEIR committee, which does not ions that it elicitsÑtwo major scientific answer to any government, is more committees oversee this matter, period- direct in its pronouncements. Based on ically reporting on new evidence related their extensive review of the biologic to quantitative risk estimates. They are evidence, including epidemiology, the BEIR committee and the UN animal data, cellular data, and cancer Scientific Committee on the Effects of theory, they conclude that the risk Atomic Radiation (UNSCEAR). decreases with dose, but never goes to UNSCEARÕs reports are compiled by zero. In fact, their exact words are: staff and a small group of knowledgeable consultants (UNSCEAR, 2006). The A comprehensive review of the biology data BEIR reports, on the other hand, have a led the committee to conclude that the risk would continue in a linear fashion at lower more elaborate procedure that has a doses without a threshold and that the smallest more transparent process (National dose has the potential to cause a small increase Research Council, 2006).19 The reportsÕ in risk to humans. (National Research Council, conclusions usually agree, but the 2006) UNSCEAR report, being a product of the United Nations, must be cognizant Still, science is a contested territory, of national politics in UN coun- so scientific dissent from these reports is triesÑthis means that the report never to be expected. For the sake of under- states that some risk continues down to standing how layered the arguments zero dose. Such careful phrasing ensures are, it is worth exploring these theoret- that the LNT, and the risk numbers asso- ical dissents. ciated with it, can be used around the world for cost”benefit analyses and Supralinear response other regulatory purposes. Agencies can justify the use of the LNT solely on One theory that uses biologic evidence the basis of adopting a conservative or to predict a response greater than precautionary approach, thereby escap- the LNT is a supralinear response. ing strong objections from industry Such evidence is based on studies of leaders and dissenting researchers. cellular communication from radiation- In the UNSCEAR reports, for exam- damaged cellsÑchemical communica- ple, the dose models have risks going tion that transfers damage to an toward zero dose, but the authors do undamaged cell, multiplying the dele- not write that the risks definitely reach terious effect of the original radiation zeroÑrather, they provide an obtuse (the bystander effect).21 Other evidence explanation that Òthe inability to detect comes from studies of genomic instabil- increases in risks at very low doses using ity, a phenomenon in which radiation epidemiological methods does not mean damage doesnÕt show up until several that the cancer risks are not elevated.Ó cell generations have passed (Morgan No doubt, there is concern at the and Sowa, 2009; see also, Hill, 2012, in United Nations that too much talk this issue of the Bulletin). about cancer risk at low doses will amp- In a 2012 study on atomic-bomb sur- lify risk perception (see Kasperson, 2012, vivor mortality data (Ozasa et al., 2012), in this issue of the Bulletin).20 low-dose analysis revealed unexpectedly

Downloaded from bos.sagepub.com at Stanford University Libraries on November 19, 2012 Beyea 21 strong evidence for the applicability of short report advocating for a quasi- the supralinear theory. From 1950 to threshold based largely on cellular data 2003, more than 80,000 people studied (Aurengo et al., 2005) and criticizing revealed high risks per unit dose in the those who think otherwise. In turn, low-dose range, from 0.01 to 0.1 Sv. The the French study has been criticized, studyÕs authors, themselves, did not go so not just on the merits, but also for lack far as to suggest a supralinear response, of objectivity.23,24 For LNT dissenters, saying only that the results were difficult the French AcademyÕs study has been to interpret. However, advocates for their counterpoint when the authority supralinear response are likely to see a of the US BEIR report is invoked. Thus, simple explanation, namely supralinear- any layperson wishing to engage in ity. Note that such effects do not show up the discussion must reach a decision in studies of cancer incidence in the on which of these reports is likely to atomic-bomb studies. contain the most credible scientific judgments. Zero response theory In contrast to theories of supralinear responses, some industry stakeholders Demonstration of a quasi-threshold argue that the response might be would be unlikely to assuage those who zero for doses up to a threshold, below abhor radiation-producing technology 0.1 Sv. A completely zero response is on existential grounds, but it might unlikely, given the heterogeneity of eventually affect regulations and overall human populations, including differing opinion. The radiation hormesis the- immune and repair systems among oryÑthat some radiation is benefi- people. However, a quasi-threshold, cialÑwould provide more comfort, if it with a dose response below 0.1 Sv, is a could be demonstrated. The best evi- standard theoretical possibility and a dence for this concept in humans can hypothesis that some researchers be found in national data on home strongly believe will be vindicated one measurements and lung cancer day, thereby confounding the conven- rates at the county level. However, the tional view of an LNT dose response. reliance on cancer data aggregated to the In 2007, the latest cancer-incidence county level has been roundly criticized results were released on atomic-bomb by epidemiologists (Lubin, 2002). survivors from 1950 to 1998; in this Results from more sophisticated epide- update, there was a mathematical fit to miologic studies of the same association a threshold at 0.04 Sv, as well as a fit to do show the expected dose response the LNT model.22 However, these find- when individual cancers are matched ings were not reiterated in the 2012 to dose (Darby et al., 2005; Krewski update on cancer mortality, which et al., 2006). reported a response that appeared to Though it still is a pet topic of enter- rise above the LNT prediction at low prising journalists, the radiation horm- doses. esis theory is no longer of much The French National Academy and interest to researchers. The BEIR VII Institute of Medicine put out their own report, published in 2006, discounted

Downloaded from bos.sagepub.com at Stanford University Libraries on November 19, 2012 22 Bulletin of the Atomic Scientists 68(3) the concept; the French Academy of for deleterious bystander effects and Sciences took it more seriously, while genomic instability. discounting other evidence that sug- gests the response might be supralinear LNT as matter of convenience at low doses. Given the increase in radiation from It should be noted that all of these cellu- medical diagnostics and the interest in lar effectsÑincluding bystander effect, protracted exposure, the possible exist- genomic instability, and adaptive ence of a threshold or hormetic effect for response, some of which are thought to public policy appears to be a moot issue have effects working in opposite direc- for developed countries when it comes tionsÑcould already be incorporated to future exposures. Even if the level of into the linear human dose-response medical diagnostic exposures does not curve (Morgan and Sowa, 2009), increase in the future, over the course making the debate much ado about of 40 years most people in developed nothing. countries will receive an average of 0.1 Many professional risk analysts, espe- Sv from medical procedures, alone. With cially those with calm temperaments, do this in mind as a dose starting point for not fret much about the debate over dose millions of people, it is fair to say that response below 0.1 Sv. They simply any exposure to radioactive elements handle it as a standard problem in uncer- from a nuclear accident or a dirty tainty management, much as they handle bomb would definitely contribute to many other parts of risk assessment cal- their delayed cancer risk. culations: They take the LNT as the mid- range, add uncertainty bounds around it, and possibly use subjective-likelihood Adaptive response distributions to accommodate alterna- Of more current interest than hormesis tive scientific hypotheses. This is essen- is the concept of adaptive response, tially the approach that has been where low doses of radiation can prime followed in calculations supporting cells to withstand later, higher doses of compensation of weapons-test veterans radiation (see Hill, 2012, in this issue of and workers in the weapons complex the Bulletin). The idea is that very low (Kocher et al., 2008), although the possi- doses, like a vaccination, teach the bility of a threshold or hormesis has not body how to recognize and repair or been included in this work. If non-linear, remove radiation-damaged cells. Thus, dose-response models are includedÑfor subsequent chronic doses would be example, threshold or hormesis less dangerous. Under some theories, modelsÑconsistency would be neces- this effect can lead to a sublinear sary and dose terms would need to be response at doses below 0.1 Sv (Morgan added for medical technology and, pos- and Sowa, 2009). In other words, the sibly, background radiation. excess risk at low doses could be less Dealing with the uncertainty compo- than predicted by the LNT. The range nentsfromgapsinknowledgeabout of doses for which this effect might low-level radiation effects is essential be applicable is not known; nor is it (Hoffman et al.,2011).Accordingtothese known whether it might compensate risk analysts, by quantifying uncertainty,

Downloaded from bos.sagepub.com at Stanford University Libraries on November 19, 2012 Beyea 23 the most important debates over low- bombs, even using the hypothetical level radiation exposures can proceed dose-response models of the LNT dis- with less distraction (e.g., planning for senters. There is no longer a conveni- accident response and weighing benefits ent excuse to avoid using the LNT to and risks of technologies). However, this estimate consequences from real or approach does not satisfy critics of the projected releases of radioactive mater- LNT, because the average risks usually ials, even when the dose of concern is come quite close to the LNT predictions, below 0.1 Sv. even though the uncertainty bounds on Particularly when it comes to the resulting predictions may include cost”benefit decisions on retrofitting their views. reactors or planning for spent-fuel pools, regulations that depend on esti- Conclusion mates of cancer risks are using LNT slope coefficients that are decades out The public, legislators, and journalists of date (see Brock and Sherbini, 2012, in are often at a loss to deal with the this issue of the Bulletin). Thus, pressure charges and counter charges that surface to update regulations may build, as in the debate over low-level radiation awareness grows of the five-to-tenfold exposures. It does not help to listen to disparity between the risk estimates industry leaders, nuclear activists, or per unit dose recommended by scien- individual researchers, who, one after tists today and the older values still another, propound their competing used by regulators in cost”benefit calcu- images of the underlying truth. Given lations for determining allowable doses. the complexities, the only alternative for most people is to rely on scientific Funding committees, like the BEIR committee and UNSCEAR, recognizing that the sci- This research received no specific grant from any funding agency in the public, commercial, or not- entific jigsaw puzzle is incomplete. Not for-profit sectors. all pieces fit correctly, but a reasonable idea of the true situation emerges from the recognizable image visible from the Notes pieces already assembled. 1. There had been hints in some earlier, smal- It is now reasonably clear that pro- ler, occupational studies, e.g., Wing et al. (1991). tracted exposure does not protect against 2. When exposures are only to gamma and beta radiation-induced cancer. Rather, it is the rays, they are usually measured in units of cumulative radiation exposure from all grays (Gy). But when other types of radi- sources that must be examined. In devel- ation are involved in a dose calculationÑfor oped countries, the average accumulated example, neutrons and alpha particlesÑthe dose from medical procedures is now comparable unit is either a Òweighted so high that a significant percentage grayÓ or a sievert. These latter units weigh of the population in these countries different types of radiation by their esti- will be above 0.1 Sv. Therefore, this mated effectiveness in increasing delayed cancer rates; therefore, doses and health population will be primed for radia- risks can be compared among epidemiologic tion-induced, delayed cancers from studies that involve different mixtures of releases from nuclear reactors or dirty radiation types.

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3. Some analysts add a quadratic term to account 10. At the time, this theory was supported by for any curvature in the dose-response curve. the interpretation of experiments on cells However, at low doses, this linear-quadratic showing that, for the same total dose, cellu- model becomes a linear model. lar damage increased the faster the dose 4. Weighted colon dose multiplies the neutron was delivered. Consequently, there was dose component by an effectiveness factor strong support for scaling down the risks of 10 (Chomentowski et al., 2000). determined from the bomb data, when it 5. No model is assumed, which means the fit is came to predicting cancer from chronic, nonparametric. Instead, the data are protracted exposures. These experiments smoothed and used to define straight-line did not involve human cancer, in which segments. The circles indicate the excess development is a more complex process relative risk at the mean dose in each of the than can be inferred from experiments on 22 specific dose categories. isolated cells. Furthermore, the dose 6. An ERR of 0.1 means that the cancer rate has response measured in these experiments increased by 10 percent. To get an absolute was for the total cellular damage, not the risk, one multiplies the ERR by the baseline damage restricted to those components cancer rate. that affect cancer development, which 7. Some critics also argue, incorrectly, that the could have their own, distinct dose atomic-bomb data have no control groups. response. In fact, it has the best types of control 11. CardisÕs critics do not accept that the groups epidemiologic methods can offer. Canada results simply reflect the highest When a study can present excess health data point among a set with wide variance; effects as a function of dose, it has internal they have spent extensive energy focusing controls for comparison. Subjects in each on the weaknesses of only this study, while dose category serve as controls for each overlooking or ignoring weaknesses in other other, all the way down to zero dose. studies with lower ERR/Sv results 8. The 1980 Biologic Effects of Ionizing (Ashmore et al., 2010; Boice, 2010). If Radiation (BEIR) report found that the Canada, the study with the highest ERR/ slope of the response was 10 times lower Sv, is removed from the study, as the critics than the value in the 2006 BEIR report; the wish, the overall results will no longer be 1995 BEIR report found it was twice as low statistically significant. Blind reliance on (Marshall, 1990; National Research Council, 95 percent confidence limits is no longer 2006; Reissland, 1981). Interestingly, as the the practice in epidemiology, but it remains slope of the birth-defect response decreased a widespread practice among stake- considerably over time, so, too, did public holdersÑwhen they will benefit from dis- interest in the matter; perhaps the direction counting data. Studies are assessed as a of change in these slopes defines, in part, group, for instance, in the context of the public concern. other studies discussed in this article. 9. Some caveats: First of all, unexpected results 12. The findings were not greatly influenced by are always a possibility and could very well data from any one country: Formal statis- appear in the next study. Second, molecular tical tests provided no evidence for differ- analysis of future tumors may one day lead ences in risk between countries. Thus, there to identification of subgroups with dose- was no statistical basis for removing the responses that are much higher than the highest data point. Analyses excluding one population average. Also, new cancer cases country at a time produced excess relative will emerge in the future for those exposed risks per Sv ranging from 0.58 (excluding at young ages; possibly, these rates will be Canada) to 1.25 (excluding the United dramatically different in old age than cur- Kingdom). Only by excluding Canada did rent projections expect. As a result, lifetime the results lose statistical significance. risks for those exposed at young ages could 13. To date, none of the epidemiology studies conceivably change significantly. dealing with protracted exposures have

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explicitly accounted for the effect of uncer- Techa River cohort study. Thus, from this tainty in dose estimation. Paying attention perspective, the study of high background to uncertainty in dose estimation is perhaps radiation in China is not at all inconsistent most important with the Techa River data with studies showing risks of protracted and some of the studies of background radi- exposure greater than predicted by analysis ation discussed later in the text, because of the atomic-bomb data. The study in India mathematical models are used in part to did not provide an analysis with liver reconstruct individual exposures, filling in cancer removed, so a comparison cannot gaps in direct measurements. Accounting be made. For a more positive view of these for measurement uncertainty strengthened types of studies, see Boice et al. (2010). For a the findings of an association with radiation discussion of other studies in high- in studies of thyroid disease following background-radiation regions, see Hendry nuclear weapons tests (Lyon et al., 2006). et al. (2009). 14. Two epidemiologic studies, one in India 15. The weights here correspond to different (Nair et al., 2009) and one in China (Tao times spent near the riverbank (Standring et al., 2012), are notable because they et al., 2009). include individualized doses, which typic- 16. To obtain this curve, no model was ally would mean they rely on internal con- assumed, which means the fit is called non- trols by dose category, like the analysis of parametric: Instead of fitting to a model the atomic-bomb survivors. However, the (e.g., a linear model), a running average of individualized dose method is weakened the data was used to define the curve. in these studies, because the authors 17. The next BEIR report is not yet in the mixed together distinct geographic regions, planning. some with low doses and some with high. 18. Because many more cancers are expected in No separate analyses were given in the stu- the atomic-bomb cohort in the next 20 dies to account for different baseline cancer years, more information can be expected rates in each region; nor was there stratifi- to emerge on the low-dose range in the cation by region. Had there been, it is likely future. Given the 50 years it has taken for that the confidence intervals would have the atomic-bomb analyses to produce increased. As it was, the confidence inter- powerful results, we cannot expect vals around their slightly negative slopes Fukushima data to contribute much for a were quite wide, limiting their usefulness great many decades, particularly because in potentially contradicting other studies, the average dose is likely to be lower. as EPRI maintains they do. Early markers However, the ability to perform genetic of cancer risk, namely dose-related sequencing of removed tumors offers a chromosomal aberrations (China) and new opportunity to expand the power of mitochondrial DNA mutations (India) epidemiologic studies. have been found in these high-background 19. Presentations to the BEIR committee are regions, casting some doubt on the null epi- open to the public. The biographies of the demiologic findings in these studies. Both committee members appear in the report. studies exclude persons under 30, the age So, too, are the names of the numerous out- period when radiation-induced is side reviewers listed in the final report. extremely high according to atomic-bomb Both of these procedures allow outsiders results. In the Chinese mortality study the to assess whether or not the committee is authors note the difficulty in diagnosing balanced. liver cancer mortality. When liver cancer 20. It is perhaps out of the same concern to is removed from the analysis, the ERR/Sv avoid social amplification of risk that the is positive and the upper confidence inter- UNSCEAR authors have declined to use val for the ERR/Sv is much greater than that the LNT to predict the total number of for the other studies mentioned in this art- excess cancers that will result over time icle, including the 15-country study and the as a result of the Chernobyl accident.

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Wing S, Shy CM, Wood JL, et al. (1991) Mortality reviewer of numerous studies for the National among workers at Oak Ridge National Research Council, most recently serving as a . JAMA: Journal of the American committee member for the completed study Medical Association 265(11): 1397”1402. AmericaÕs Energy Future, and the ongoing study, The Feasibility of Inertial Fusion Energy. He currently is a member of the Author biography World Trade Center Health Registry Scientific Advisory Committee. He advises Guest editor of the BulletinÕs special issue on plaintiff law firms on litigation strategy in low-dose radiation risks, Jan Beyea is a nuclear large, toxic tort cases, where he has watched physicist, who, for 40 years, has listened to, and some of the most prominent researchers in sometimes participated in, the debate over the world go head to head, debating the risks risks from low-level radiation exposure. He of low-level radiation. He is chief scientist at is a co-author of papers on environmental epi- Consulting in the Public Interest. demiology, including a study of the Three Mile Island accident. Beyea has been a member and

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