Implications of Radiation Dose and Exposed Populations on Radiation Protection in the 21st Century
Boice, John D. Jr.*†
*National Council on Radiation Protection and Measurements, 7910 Woodmont Avenue, Suite 400, Bethesda, MD 20814-3095; †Department of Medicine, Vanderbilt-Ingram Cancer Center, Vanderbilt School of Medicine, Nashville, TN 37240.
The author declares no conflicts of interest.
For correspondence contact the author at: National Council on Radiation Protection and Measurements, 7910 Woodmont Avenue, Suite 400, Bethesda, MD 20814-3095, or email at Boice@NCRPonline.org.
Supplemental Digital Content is available in the HTML and PDF versions of this article on the journal’s Web site (www.health-physics.com).
(Manuscript accepted 28 August 2013)
Abstract: Radiation is in the public eye because of Fukushima, computed tomography examinations, airport screenings, and possible terrorist attacks. What if the Boston Marathon pressure cooker had also contained a radioactive source? Nuclear power may be on the resurgence. Because of the increasing uses of radiation, the increases in population exposures, and the increasing knowledge of radiation effects, constant vigilance is needed to keep up with the changing times. Psychosocial disorders associated with the inappropriate (but real) fear of radiation need to be recognized as radiation detriments. Radiation risk communication, radiation education, and communication must improve at all levels: to members of the public, to the media, to other scientists, and to radiation professionals. Stakeholders must continue to be involved in all radiation protection initiatives. Finally, we are at a crisis as the number of war babies (me) and baby boomers (you?) who are also radiation professionals continues its rapid decline, and there are few in the pipeline to fill the current and looming substantial need: “The old road is rapidly agin’” (Dylan). NCRP has begun the WARP initiative—Where Are the Radiation Professionals?—an attempt to rejuvenate the pipeline of future professionals before the trickle becomes tiny drops. A Workshop was held in July 2013 with government agencies, military, private sector, universities, White House representatives, and societies to develop a coordinated and national action plan. A “Manhattan Project” is needed to get us “Back to the Future” in terms of the funding levels that existed in years past that provided the necessary resources to train, engage, and retain (a.k.a., jobs) the radiation professionals needed for the nation. If we don’t keep swimmin’ (Disney’s Nemo) we’ll “sink like a stone” (Dylan).Introduction of Implications of Radiation Dose and Exposed Populations (Video 2:06, http://links.lww.com/HP/A25)
THIS 2013 National Council on Radiation Protection and Measurements (NCRP) Annual Meeting addressed the range of radiation doses people receive in medical, occupational, and environmental circumstances, including accidents, and the impact these exposures have on individuals and society (Table 1). The meeting was dedicated to the people of Fukushima who were affected by the reactor accident and the great 2011 earthquake and tsunami. The published Proceedings in Health Physics are available free of charge because of a generous grant from the Radiation Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute (NCI). The kick-off speaker was Dr. Shunichi Yamashita, whose 10th Warren K. Sinclair Keynote summarized the health surveys being conducted in Japan in response to the reactor accident (Yasumura et al. 2012). These surveys include thyroid ultrasound scans of children, blood studies, mail questionnaires sent to nearly two million residents, surveys of women who were pregnant or nursing at the time of the accident, and special psychosocial evaluations of the evacuees (Akiba 2012). The bookend presentation to end the first day was the 37th Lauriston S. Taylor Lecture delivered by Dr. John E. Till titled, “When Does Risk Assessment Get Fuzzy?” After being introduced by his good friend Ward Whicker, Admiral Till described the steps of an environmental assessment from source term to transport, exposure, dose, and risk estimation, with considerations of uncertainty, validation, stakeholder participation (Table 2), and communication (Table 3). After each step was presented, similar to Fuzzy Wuzzy, we learned that fuzzy wasn’t very fuzzy and that risk assessment has matured into a multidisciplinary field that is widely accepted as valid, credible, and useful (Till et al. 2012).
It is clear that “the times they are a-changin’” (Table 1), and we need to keep abreast of the rapidity of these changes in population exposures and doses (NCRP 2009) or we’ll “sink like a stone.” There’s a lot more to be done in radiation protection in all areas (medicine, occupation, regulations, research, environment, accidents, terrorism), and we are facing a human capital crisis: “the old road is rapidly agin’,” and where are the radiation professionals for the future? “The demand for a nuclear workforce for medicine, health physics, and energy is certainly not decreasing. All of these areas are important for national and world security and prosperity, yet their increasing needs come at a time when the nuclear workforce is shrinking” (NA/NAS 2013). The failure to communicate radiation risks (and benefits) in an informative and understandable way remains a serious problem (Slovic 2012). Mental health problems associated with the fear of radiation (which has no threshold) is gaining recognition as a serious consequence of exposure, even when the associated dose is trivial and of no possible future health consequence (Bromet 2012). Specific implications of the 2013 Annual Meeting are described below in four sections: Overview, Medical Exposures, Worker Exposures, and Public Exposures. The discussions below are my personal views on the implications of the Annual Meeting and not a summary of the proceedings. While I generally follow the outline of the presentations, I often add or emphasize topics or areas not covered that I believe are also of import to radiation protection in the 21st century.
The stage was set by addressing the “Who,” “Why,” and “What” of radiation dose and risk key questions. Who are the exposed people? We know that radiation causes cancer, so why study these people? What are the impacts from exposure, not just disease but psychosocial and societal? With apologies to Pogo, we have met the exposed populations, and he is us! Every person alive is exposed to ionizing radiation. Steve Simon presented an alphabetized list of over 100 exposed populations who have been studied, literally from A (atomic veterans) to Z (zirconium refractory plant workers). Read his compilation and see if you can add to it! The sources of radiation and opportunities for exposure for people around the world are numerous and varied. When Willie Sutton was asked why he robbed banks, he responded, “Because that’s where the money was.” Similarly, where is the population dose, and where might radiation protection emphasis be placed? It’s in medicine (NCRP 2009). It’s in new diagnostic imaging techniques and new radiation therapy innovations. The increase in medical radiation doses is coupled with an increase in benefit but also in an increase in the number of exposed patients and medical workers. It is encouraging that both NCRP and the International Commission on Radiological Protection (ICRP) have strong committees addressing the complex issues of radiation protection in medicine. There are some occupational groups, however, such as industrial radiographers and interventional radiologists, whose exposures can reach and exceed regulatory guidelines. There is the possibility of nuclear incidents, nuclear accidents, and nuclear terrorism, and nuclear weapons exist throughout the world. What will be the decision process in radiation protection if some of these catastrophic incidents ever happen on our soil (Chen and Tenforde 2012)? As the need for radiation protection changes in this 21st century, there is a need for constant improvement, constant vigilance, and continued guidance.
Martha Linet clearly explained why radiation-exposed populations are still studied. Not all is known about the health consequences of radiation exposure and at what dose levels they might occur. Epidemiological studies continue to provide new and critical information about health outcomes and are able to address public concerns, clinical needs, and public health requirements (Gilbert 2009). New knowledge on radiation effects is then synthesized by national and international committees, and guidelines on total detriment (health consequences) are updated (ICRP 2007). Some examples of recent new knowledge include the absence of genetic risk to the children of cancer survivors treated with radiation, confirming the studies of atomic bomb survivors (Signorello et al. 2010, 2012); learning that risk of cancer may be greater for exposure in early childhood than in utero (Preston et al. 2008); recognizing that cataracts and cardiovascular disease may occur at doses much lower than previously assumed (ICRP 2012); finding that myelodysplastic syndrome was increased in Nagasaki atomic bomb survivors 40–60 y after exposure (Iwanaga et al. 2011); and that central nervous system effects may be a concern for astronauts (Cherry et al. 2012; NASA 2012). There is a need to learn more about the effects of dose rate, radiation energy types and levels, internal radiation emitters, and individual characteristics.
Roy Shore emphasized that while the effects of radiation at high doses are rather well known (e.g., from the studies of Japanese atomic bomb survivors and medically exposed patients), at lower doses the understanding is in fact fuzzy (unlike the previous reference to our favorite bear who wasn’t), and at very low doses the effects are really unknown. The need to learn more in the fuzzy and unknown regions was stressed given the ever-increasing exposure to computed tomography (CT) scans performed in the United States every year, now over 85 million. Estimates of cumulative individual doses for multiple CT examinations range above 100 mSv for 15% of patients and over 250 mSv for 4% of patients (Sodickson et al. 2009). Childhood exposures to multiple CT examinations are of particular concern because of susceptibility and length of life for any harmful effects to develop. Several studies have been published on childhood CT exposure and cancer risk but are not easily interpretable because the reasons for the examinations were unknown, and confounding by indication (reverse causation) was likely (i.e., the CT exams did not cause the associated cancer, but the symptoms leading up to the diagnosis of the cancer caused the CT exams) (NCRP 2012a).†
Beyond solid cancers and leukemia occurring as late effects, other possible health concerns include cataracts, cardiovascular diseases, and cerebrovascular diseases. There is also a need to learn more about protracted and fractionated exposures compared with acute doses. A refreshing and balanced overview of the epidemiologic data on risk from low-dose, protracted, or highly fractionated radiation exposures (i.e., presenting both the positive and the negative investigations) suggested that while much has been done, there is no clear picture yet as to whether, and at what level, chronic exposures might be less effective than acute exposures in causing cancer. To this end, the Million U.S. Worker and Veteran Study may provide additional scientific guidance. This national effort, directed by NCRP and Vanderbilt University, is to understand radiation risk when exposures are delivered gradually over time (Boice 2012a). The study has identified nearly nine million workers or atomic veterans, and one million were selected for study. It is 10 times larger than the atomic bomb survivor study and has more high-dose subjects! There will not be a need for dose and dose-rate effectiveness factor adjustments since the doses are all received in small amounts over many years. But risks for individual cancer sites can be contrasted, at least in principle, with those reported for the Japanese atomic bomb survivors. The study will address directly the dose rate issue in humans and whether the risk from 100 or 1,000 mSv received over years is the same, lower, or higher in comparison with brief exposures such as to the atomic bombings in Japan. Results will be directly applicable to radiation protection, compensation, and risk projection in medical and environmental circumstances.
The question of fuzzy findings in the low dose domain is important. Policy continues to be set to protect people against the presumed chance (i.e., risk or probability) that low doses may cause bad things in the distant future. Assumptions are made as to the level of risk associated with doses below ~100 mSv where epidemiology cannot provide answers because of inherent statistical limitations (the signal is too weak to detect) and because of the impossibility to control for subtle confounding factors that have more influence on cancer occurrence than the exposures to be studied (ICRP 2005). Low doses are ubiquitous, and policies are set to protect workers, compensate prior workers, clean up former radiation legacy sites, protect the public living near nuclear facilities, and address patient exposures in this burgeoning era of medical advances. Protection is not cheap, and huge resources are expended in these arenas. Obtaining a better handle on the risks involved, if only a better upper bound as to the possible level of risk, is a matter of importance. We need to bring these fuzzy risks into sharper focus.
Evie Bromet was the cleanup hitter for the Overview Session, bringing to our attention once again that psychological problems and mental health disorders are far and away the most important consequence of the aftermath of nuclear reactor accidents. Mental health problems associated with stress, depression, anxiety, the evacuation, loss of loved ones, inability to return home, stigma, and fear of radiation effects for self and children are being recognized as the most serious health consequences of the accident (Bromet 2012; Slovic 2012). Cancer risk pales in comparison. Mental disorders today are more important than possible future cancers tomorrow! There is a debilitating fear of radiation and anxiety over potential and future health concerns arising in people who believe that they were exposed—irrespective of whether they were or not or the actual levels of exposure. The stress for young families is so severe that a new term has been developed by the media called “atomic divorce” to represent the splitting of family units because of the effects of the evacuation and fear of radiation (Haworth 2013). These mental health disorders are often enhanced by the reactions that people receive from poorly trained medical personnel, who receive insufficient instruction in mental health issues in medical school, and made worse by post-event discrimination and stigma by others (Vano et al. 2011).
Compounding the stress of dealing with a reactor accident were the problems in communication (or lack thereof). Shunichi Yamashita had highlighted that inadequate communication equals inadequate protection. The Japanese authorities acted properly and did protect the public with sheltering in place, evacuation, and food restrictions. But because of poor communication by experts with the media, there was a loss of credibility for scientific and government officials (González et al. 2013). The Japanese public still does not accept scientific results, and there has been an increase in public anger, anxiety, and distrust. These conditions are related to poor communication, lack of education and understanding, and occurred even when there was essentially no dose, or at most a tiny dose. Radiation risk communicators (Table 2) must overcome the challenges posed by three basic observations about people under stress, who typically:
* want to know that you care before they care about what you know;
* have difficulty hearing, understanding, and remembering information; and
* focus more on negative information than positive information (Covello 2011).
Without sound communication of content, skilled communicators of message, and effective outreach to the proper audiences (policy setters, members of the public, patients, and professionals), the message perishes. We must do better (Locke 2011; IAEA 2012)! In this regard, the NCRP Board of Directors recently approved the creation of a new Program Area Committee 7: Radiation Education, Risk Communication, Outreach, and Policy.
Medicine is where the population dose is delivered in developed countries (Mettler et al. 2009; NCRP 2009). The dose is not only to patients receiving diagnostic procedures and radiotherapy treatments but also to the medical staff involved. Recognizing that there are many topics in medicine that deserve attention (Table 4), this section focused on radiation protection issues for medical staff, patients radiologically examined, and patients treated with radiation. The principles of radiation apply to all these groups: justification, optimization, and limitation (Table 5) (NCRP 1987, 1993).
Larry Dauer provided a tour de force on protection challenges in medicine today. Medical personnel are increasingly involved with traditional and novel uses of radiation and radioactive materials in medical practice. The use of CT examinations has skyrocketed over the years, increasing total population exposure. Challenges in the emergency room setting cannot be overstated (Linton et al. 2011; Sierzenski et al. 2013). Although rare, CT examinations have been administered incorrectly, and deterministic effects (e.g., hair loss) have been reported (Bogdanich 2010; Bogdanich and Ruiz 2010). Interventional procedures have resulted in ulcers and skin burns (ICRP 2000). Deterministic effects or tissue reactions are more frequent in the treatment of patients where very high doses are delivered to small volumes of tissue for the purpose of killing malignant cells. Collateral damage, unfortunately, includes damaging the good tissues along the way (NCRP 2011; ICRP 2012). Staff involved with interventional radiology receive the largest proportion of medical dose, and cumulative exposures sufficient to result in cataracts are being reported and at levels lower than previously supposed (ICRP 2000; Vano et al. 2013). Whether the current guidelines for dose to the lens should be lowered in the United States is currently being discussed, including stakeholder involvement. Regulations to minimize eye exposures could impact on the way some procedures are done and on how many certain providers could perform (e.g., cardiologists and interventional radiographers) in their work. NCRP limits for annual and cumulative effective dose (NCRP 1993) and for equivalent dose to the lens differ from those of ICRP (2007, 2012), and there is a need to update and reassess guidance in these areas. There is an expanding use of radioactive elements in medicine: diagnostic imaging, positron emission tomography (PET) imaging, multimodal imaging, nuclear medicine tracers and stress tests, and sentinel node and radiation seed location. The “brave new world” of nuclear medicine includes expanding uses of anti-matter (i.e., positron emitters). Positron emitters such as 89Zr require a cyclotron to produce, result in higher gamma energy emissions than most radionuclides in current use, and may impact the design of medical facilities. New types of treatment modalities, such as proton beam therapy, require new types of radiation protection programs and especially skilled physicists and engineers to operate. The present and future challenges include improved dosimetry to cope with new radiations (higher energy gamma rays, protons, neutrons), measuring lens dose, measuring extremity dose, recognizing and addressing the novel uses of a variety of radionuclides, and coping with the new technologies of cyclotrons, proton machines, and possibly carbon ion therapy in the future. The “old road is rapidly agin’ … The order is rapidly fadin’ … For the times they are a-changin’.” Changing times require changing minds!
Jim Brink discussed the extremely important need for dose tracking for patients. Such a system would be beneficial to the patient, the clinical practitioner, and perhaps to epidemiologists in the future who wish to correlate or include medical exposures in studies of cancer risk. The variability of patients (age, weight, life expectancy) and their treatments makes dose estimation difficult, and there is a need for common metrics of dose (effective dose, whole-body dose, organ dose, cumulative dose – preferably organ dose) and for how long (indefinitely to enable long-term follow-up). Most new CT machines include some measure of dose, which is a good first step. Tracking patient doses would also minimize unnecessary repeat examinations by avoiding, for example, needless double CT scans (Bogdanich and McGinty 2011). Tracking might be focused first in the areas of most use (e.g., the emergency room setting). The selection of types of examinations for patients based on diagnostic algorithms also might be standardized based on appropriateness criteria. A goal is to reduce the error in the use of radiation and also of contrast media. It is encouraging that the medical community has banded together to provide practical educational tools and advocacy to accelerate radiation protection for children and adults worldwide through the Image Gently™ and Image Wisely™ initiatives (Goske et al. 2010; Brink and Amis 2010), as well as increased awareness in emergency medicine (Linton et al. 2011; Sierzenski et al. 2013).
The diagnostic uses of radiation are with CT, nuclear medicine, radiography, and fluoroscopy. The American College of Radiology has supported a Dose Index Registry, which currently collects dose information for CT scans but will expand to other modalities and will start collecting data based on patient size (ACR 2011; Morin et al. 2011). Reference levels and achievable doses can provide guidance as to the optimal use of imaging procedures (NCRP 2012b). Patient size matters, and image quality as well as organ dose can be affected if suboptimal machine settings are used during scans (Israel et al. 2010; AAPM 2011). There are many, many publications on the possible future risk of cancer among patients receiving CT examinations (Berrington de González et al. 2009). However, there are few studies contrasting patient outcomes from the underlying condition requiring care with the possible future risk of radiation-induced cancer. Among young adults undergoing body CT examination, the risk of death from the underlying condition being evaluated was more than an order of magnitude greater than the theoretical future death from radiation-induced cancer (Zondervan et al. 2013). The patient’s underlying medical morbidity, rather than possible CT-induced cancer, was the dominant factor driving a potentially adverse outcome. Managing incidental findings on CT examination remains a challenging endeavor but is being addressed (Berland et al. 2010). Communicating radiation risks with patients and obtaining true informed consent continues to be a challenge (Dauer et al. 2011; Brink et al. 2012). Constant vigilance is required in the use of diagnostic imaging procedures, since the impact of multiple repeat examinations, even when clinically indicated, can result in organ doses that approach the range where epidemiologic investigation has revealed risk (Katz et al. 2006; Sodickson et al. 2009).
Lois Travis provided a marvelous overview of the risk of cancer and cardiovascular disease following radiation therapy for cancer patients (Travis et al. 2012; NCRP 2011). With the success of cancer treatments, patients are now living much longer and the risk for late effects has increased accordingly, not only for developing new second cancers, but also serious heart conditions. NCRP Report No. 170, prepared under the leadership of Lois Travis, provides a recent review including quantitative estimates of risk following curative therapies and examination of dose-response relationships (NCRP 2011). In 2007, there were 13.7 million survivors of first cancers in the United States, which indicates the future burden of and the continued need to evaluate late effects of therapy (Siegel et al. 2012). Children with cancer are one of the great treatment success stories of the past 50 y. Treatment has improved survival dramatically, and now many can live almost disease free, although not without the consequences of their curative therapies. Because children continue to grow after treatment and because of their long life expectancy, they are particularly susceptible to late effects, and constant monitoring and concern are warranted (Robison et al. 2009). One remarkable statistic is that the absolute number of new second cancers in a year is greater than the number of any single cancer diagnosed in that same year (i.e., greater than prostate, greater than lung, greater than breast)! Further, the burden for diagnostic and therapeutic radiation services will only increase as the baby boomers start requiring substantial medical care due to their age and longevity. NCRP Report No. 170 (NCRP 2011) makes several recommendations, including the long-term, large-scale follow-up of cancer survivors to allow development of guidelines for prevention and intervention.
Error prevention in radiotherapy is particularly important because the tolerances are so small. A mistake when treating a cancer patient can be pretty serious. If the delivered dose is too large or inappropriately distributed, then serious tissue damage can result. If the dose is too low, the consequence is also serious, because there will not be enough malignant cells killed to cure the patient. Another theme that came up repeatedly in all sessions was genetic susceptibility (underlying predisposition) to radiation-induced cancer and noncancer diseases. Individual susceptibility is an important issue, and it would be wonderful to be able to profile patients as to the effectiveness of different therapies and the likelihood of future adverse events. It’s not possible now, but the explosion of research on inherited mutated genes and polymorphism bodes well for the future, at least in some limited circumstances. NCRP might consider another summary of genetic susceptibility and the interaction with radiation, as well as with other cofactors such as smoking and lifestyle. An update of the medical doses in Report No. 160 (NCRP 2009) might be considered given the rapidity of change across the country. There are different treatment modalities, different ways in which patients are diagnosed, and different ways in which patients are monitored and screened. NCRP is in tune with the need for electronic record systems and the tracking of individual radiation doses.
The third session addressed worker exposures within U.S. Department of Energy (DOE) weapons and nuclear industry facilities, after nuclear reactor accidents, and associated with military activities, especially the humanitarian assistance provided during the Fukushima natural disaster and nuclear accident. Presentations were made by scientists from NCI; the National Institute for Occupational Safety and Health (NIOSH); and the Defense Threat Reduction Agency (DTRA), U.S. Department of Defense (DOD).
Jim Neton (NIOSH) described the methods used to estimate radiation doses to DOE workers covered by the Energy Employees’ Occupational Illness Compensation Program Act (EEOICPA 2000; Neton et al. 2008). EEOICPA was created by Congress in October 2000 and provides compensation for adverse health effects assumed to be related to work involved in the production of nuclear weapons. The program covers work performed for DOE (or its predecessor agencies). Part B of the Act provides monetary benefits for workers who developed cancer. A probability of causation [PC (or more correctly termed the assigned share)] interactive radioepidemiological computer program is used to establish eligibility for an award. There are about 750,000 former workers from more than 200 facilities who may be eligible for compensation under EEOICPA. To support the dose reconstruction of almost 40,000 workers to date, NIOSH has collected literally millions of pieces of supporting information. Because the doses are estimated with “claimant favorable” methods, they are not directly appropriate for epidemiological uses without modification. As of September 2012, 28.8% of 9,072 claims received compensation [i.e., the computed PC was greater than 50% (or to be more technically correct, compensation was awarded when the upper 99th percentile of the probability distribution accounting for uncertainty exceeded 50%)]. Recently the uncertainties associated with the PC computations were evaluated by NCRP (2012a; Preston et al. 2013). One limitation of the current approach is that tying the award to the uncertainty distribution inadvertently awards uncertainty. For example, cases of lymphoma and malignant melanoma, which have uncertain associations with radiation, are more likely to be compensated than cases of stomach cancer and breast cancer, which are more strongly associated with radiation (UNSCEAR 2008). The most common cancers for which compensation claims were made were of the lung, prostate, and skin, comprising together >50% of the claims. Missed (unknown) dose for intakes of insoluble actinides (e.g., uranium, plutonium, americium, and others) were estimated and incorporated into the dose reconstruction; the incorporation of these missed doses often produced PCs that resulted in compensation. Cancers of organs that do not concentrate internal radionuclides (e.g., prostate or brain) have low compensation rates unless there were high external doses. Relatively low doses for cancers with high excess relative risk per sievert coefficients (e.g., nonchronic lymphocytic leukemia) can result in compensation. The July 2009 issue of Health Physics (Vol. 95, No. 1) is entirely devoted to the NIOSH Dose Reconstruction Program.
Andre Bouville (NCI) summarized worker exposures at early nuclear plants and fuel reprocessing facilities in the United States (Hanford in Washington state) and in the former Soviet Union (Mayak). He also discussed worker exposures following the nuclear reactor accidents at Windscale, Three Mile Island, Chernobyl, and Fukushima. The Hanford Works (1944+) produced plutonium for military uses with nine nuclear reactors and five plutonium processing plants. The counterpart in Russia was the Mayak complex (1948+), with five nuclear reactors and one radiochemical plant. The average doses from external radiation during the early operations were 100 to 1,000 times greater among Mayak workers compared with Hanford workers. For example, in 1949 the average doses were 0.65, 950, and 400 mSv for the Hanford, Mayak Reactor, and Mayak radiochemical workers, respectively.
The Windscale accident in the United Kingdom occurred in 1957 and involved 471 workers. No worker received >50 mSv, and no health effects were reported or are anticipated. In 1959, an accident occurred at the Santa Susana Field Laboratory in California when a sodium reactor experiment, which had produced electricity for the city of Moorpark, California, in 1957, experienced a core melting (Boice et al. 2011). Worker exposure during the accident and cleanup activities appeared minimal with mean career doses <20 mSv, although doses were not described per se for the accident workers. No health effects have been reported. The Three Mile Island accident in Pennsylvania occurred in 1979 and involved thousands of workers over time. No worker received >50 mSv and no health effects were reported or are anticipated. The Chernobyl nuclear rector accident in the former Soviet Union occurred in 1986 and is the most severe nuclear reactor accident that has ever occurred in the nuclear power industry (UNSCEAR 2011). Hundreds of emergency workers were involved in stopping the burning reactor and getting it under control. Doses were so high (up to 16 Gy) for 134 emergency workers that they developed acute radiation sickness, and 28 died within a few months of the accident. Over 500,000 workers were involved in the recovery/cleanup efforts through 1990, and the mean recorded dose was 117 mGy. Studies are ongoing with complex dose reconstruction schemes but are challenging because doses were not recorded for all workers. Proxy interviews are being conducted, the radiation fields were complex, and time and location parameters were not known accurately. The Fukushima accident in Japan occurred in 2013 and involved over 25,000 workers, both Tokyo Electric Power Company and contract workers. The average dose was 12 mSv, and at least six workers received >250 mSv. The high effective doses were related to the inhalation of radioactive iodine during the early phase of the accident and not to whole body external exposures. Fewer than 200 workers received above 100 mSv external dose.
Many lessons are continuing to be learned from these accidents that are relevant to protection activities in the 21st century. For Fukushima, these include but are not limited to:
* assessing the importance of internal exposures;
* managing emergency crises;
* protecting rescuers and volunteers;
* responding with medical aid;
* justifying necessary but disruptive protective actions;
* transiting from an emergency to an existing situation;
* rehabilitating evacuated areas;
* restricting individual doses to members of the public;
* caring for infants and children;
* categorizing public exposures due to an accident;
* considering pregnant women and their fetuses or embryos;
* monitoring public protection;
* coping with contaminated territories, rubble, and residues and consumer products;
* fostering the sharing of information; and
* recognizing the importance of psychological consequences (González et al. 2013).
Paul Blake (DTRA) provided a unique overview of radiation exposure of U.S. military personnel. The extensive military program of radiation protection in the United States has received little recognition and has an interesting history. One of the first uses of radiation in the military was during the Spanish-American War in 1898, where diagnostic x-ray units were deployed just 3 y after x-rays were discovered by Roentgen (Borden 1900). The U.S. military maintains occupational radiation exposure records from 1945 to the present on 2.3 million unique individuals. About 2% (or 70,000) of the 1.4 million active duty military personnel, 1.3 million National Guard and reserves, and 0.7 million civilian employees are monitored annually for radiation exposure. Radioepidemiological studies have been conducted over the years and include atomic veterans (Caldwell 1983; Watanabe et al. 1995; Johnson et al. 1996; Dalager et al. 2000; Thaul et al. 2000), workers at shipyards involved with the overhaul of nuclear powered ships (Fry et al. 1996; Matanoski et al. 2008), submariners who received nasopharyngeal radium treatments (Kang et al. 2000), nuclear submariners (Charpentier et al. 1993; Friedman-Jimenez et al. 2003), and veterans of the Gulf War exposed to depleted uranium (McDiarmid et al. 2013).
It was impressive to learn that the U.S. Navy has more operational nuclear reactors, 104, than there are commercial nuclear power reactors in the United States. The Naval vessels include 71 nuclear submarines and 11 nuclear aircraft carriers. The responsible organization, Naval Reactors, is consistently recognized for its record of excellence with no reactor accidents after 151 million miles of sea travel. Occupational exposures for vessel operators have been and remain historically low. The majority of radiation exposure occurs at four Navy shipyards that maintain nuclear powered vessels.
After the 2011 Japanese earthquake and tsunami, the U.S. Department of Defense (DOD) launched a large-scale humanitarian effort to help the Japanese called “Operation Tomodachi,” involving 24,000 U.S. service members, 189 aircraft, and 24 Naval ships. Although personnel were not in the direct vicinity of the Fukushima reactors, the radiological releases potentially exposed 53,000 DOD-affiliated individuals on shore, and 17,000 individuals on ships. DOD conducted extensive environmental monitoring and estimated exposures for 70,000 individuals. This registry is unique in many ways, including the inclusion of military spouses of personnel stationed at military bases throughout Japan and their children. To date, the estimates of radiation dose are tiny, much less than received by natural background radiation in a month, and as such will not result in any observable health effects. DOD has five repositories of radiation exposure:
* Operation Tomodachi Registry;
* Army Dosimetry Center;
* Naval Dosimetry Center;
* Air Force Dosimetry Center; and
* DTRA’s Nuclear Test Personnel Review.
The Nuclear Test Personnel Review provides the foundation for compensating atomic veterans for presumptive and nonpresumptive radiogenic diseases. The military compensation program covers ~220,000 participants at above-ground weapons tests and the 200,000 early military entrants to Hiroshima and Nagasaki after the 1945 detonations. Presumptive diseases are defined by Congress, so that the veteran (with DTRA assistance) just has to prove that he or she was present at a nuclear test or in Japan after the bombings to receive compensation. Nonpresumptive diseases require complex dose reconstruction and probability of causation computations similar to that described for the DOE worker compensation program. NCRP and Vanderbilt University are directing an epidemiologic follow-up of 115,000 participants at eight above ground test series at the Nevada Test Site and the Pacific Proving Grounds with dose reconstructions based on best estimates of organ dose and not high-sided ones used for compensation purposes (Boice 2012b).
The final session covered radiation exposures to the general public. Highlighted were the continued studies of Japanese atomic bomb survivors, the studies of cancer rates in populations living near nuclear facilities and following nuclear reactor accidents, and the studies of populations living on the Techa River and exposed to radioactive wastes from the Mayak Reactor facilities in Russia.
Harry Cullings (Radiation Effects Research Foundation, Japan) discussed the latest results of the study of Japanese atomic bomb survivors that has continued since 1946 when President Harry S Truman approved the creation of the Atomic Bomb Casualty Commission “to undertake a long range, continuing study of the biological and medical effects of the atomic bomb on man.” Now directed by the Radiation Effects Research Foundation, the Life Span Study (LSS) is the longest running epidemiologic study in history, with the 1948 Framingham Heart Study a close second (Scheindlin 2010)! Like “Old Man River,” the LSS just keeps rollin’ along and after all these years still has more to offer, in particular learning about the lifetime risk of radiation exposure following childhood and adolescent exposures that occurred in 1945 (Ozasa et al. 2012). The study of Japanese atomic bomb survivors has provided important information on radiation risks used for guidance in setting radiation protection guidelines (NCRP 1993; ICRP 2007). Included among the many important scientific findings is that the children of atomic bomb survivors are not at increased risk of heritable affects; childhood exposures carry more of a cancer burden than exposures in utero; a single exposure in 1945 apparently increases cancer risk for life; women are more susceptible than men to radiogenic disease; some cancers are not clearly associated with cancer (e.g., chronic lymphocytic leukemia, prostate cancer, testicular cancer, cervical cancer, and lymphoma, among others); myelodysplastic disease may occur some 40–50 y after exposure; age at exposure strongly influences future cancer risk, with children being at higher risk than adults for many but not all cancers (Mettler et al. 2013; UNSCEAR 2013); surgically-defined cataracts continue to occur with an estimated threshold dose of ~500 mGy; and other noncancers such as heart disease and stroke may be occurring at doses lower than previously assumed (UNSCEAR 2008). Remarkably, all of these conclusions are based on relatively small numbers of excess cases: 537 excess solid cancers out of 10,928 could be statistically attributed to radiation, as could 94 excess leukemias out of 312, and 353 noncancer (cardiovascular and cerebrovascular deaths) out of 35,685. About half of the cohort of 93,741 survivors (including 86,671 in-city members of the LSS with estimated doses) remains alive, so there’s more to be learned. Interestingly, it was estimated that on average, about 10 y of life were lost per gray among women and 15 y of life were lost per gray among men. Acute effects of high radiation doses were not a focus of the LSS, but 500 mGy was estimated as a rough threshold for the most sensitive acute symptoms such as nausea. Additionally, there is renewed interest in the so-called “black rain” fallout (Kerr et al. 2013). “Black rain” refers to the color of the rain that fell in some sections of Hiroshima, but it does not necessarily imply that radioactive fission products were present in the rain. Fallout has been assumed to be minimal because the detonation was in the sky and not on ground, and because of the prevailing winds, individual dose estimates from residual radioactivity are not currently included in the LSS dosimetry systems. Because of the important role the LSS study plays in radiation protection schemes worldwide, there is continued evaluation of all sources of radiation (gamma radiation, neutrons, and fallout) to improve as needed estimates of doses to individuals.
There are some circumstances of the LSS that limit the strength of the generalization that can be made with respect to U.S. and other healthy populations. First and foremost is that the exposure occurred in a fraction of a second (i.e., it was brief), whereas most exposure situations today are chronic and occur gradually over time. The Japanese population was exposed in 1945, survived a nuclear detonation, lived in a war-torn country, and was confronted with malnutrition, deprivation, infection, and other overriding health and psychosocial concerns. Thus, the population is not very similar to healthy populations today experiencing occupational, environmental, and medical exposures. Mortality follow-up did not occur until 1950, or 5 y after exposure, and cancer incidence follow-up did not occur until 1957 or 13 y after exposure. Because the exposure occurred in a single year, 1945, there are uncertainties associated with the confounding effects of birth cohort on baseline disease rates. That is, age at exposure and birth cohort are perfectly correlated, so that factors associated with birth cohort (such as smoking habits, diet, and viral infections) could affect the pattern of risk with age at exposure but cannot be accounted for in the analysis. The existing epidemiologic data on human health effects (ICRP 2007; NCRP 2012a) thus have been transformed and transported, modulated and manipulated, and there is a potential procrustean problem (i.e., forced conformity to a somewhat arbitrary set of statistical models) (Mettler et al. 2013). Recall that Procrustes was the mythological highwayman who cut off (or stretched on a rack) the legs of travelers so they would fit his iron bed (i.e., he forced conformity to an arbitrary set of conditions). Nonetheless, the LSS is the single most important radiation study by far and will remain so for the immediate future.
Next was Bruce Napier (Pacific Northwest National Laboratory), who provided a comprehensive overview of the history of the Mayak Production Association in central Russia, covering its operations, radionuclide releases, and associated doses to the public. Environmental releases from Mayak exposed people living in the nearby city of Ozersk, along the Techa River where radioactive wastes were released, and in the area downwind of Mayak, which was called the East Urals Radioactive Trace following the 1957 “Kyshtym Explosion,” a chemical explosion of a liquid radioactive waste storage tank. Each of these cohorts is providing information on protracted exposures for which the magnitude of cancer risk from low dose and low dose-rate radiation exposure remains uncertain. The Techa River cohort of 29,730 is particularly informative (Kossenko et al. 2005; Krestinina et al. 2007; Schonfeld et al. 2013). The population lived along the Techa River between 1950–1960 and was exposed to radioactive and chemical wastes released into the river from Mayak. The exposure was to both external gamma radiation and internal 90Sr, 137Cs, and other radionuclides. Although fraught with uncertainties in estimating exposures to the population living along the banks of the Techa River, individualized doses have been reconstructed based on the Techa River Dosimetry System (Degteva et al. 2000, 2006). It was estimated that about 2% (or 50) of the 2,303 solid cancer deaths were statistically associated with the radiation exposure. While the study supports an increased risk of solid cancer mortality following protracted radiation exposure from the Techa River contamination, the wide confidence intervals around the estimates of risk reflect “the challenges of quantifying and describing the shape of the dose-response relationship in the low dose range” (Schonfeld et al. 2013).
As with all observational studies, the Techa River Cohort Study is not without limitations, which weaken the strength of conclusions that can be made. The study suffers from uncertainties in dose reconstructions, incomplete population identification, potential screening bias, concomitant high dose medical screening exposures, losses to follow-up, and uncertain quality and completeness of outcome ascertainment (NCRP 2012a). The methodological limitations are notable in comparison with other cohort studies of exposed populations: 22.7% of the Techa River population was lost to follow-up, mainly due to migration out of the catchment area; cause of death was missing for 9% of those known to have died; less than half of the solid cancer cases were histologically confirmed; and 20% of cancers were either ascertained solely on the basis of clinical notes or the method of diagnosis was not specified clearly (Krestinina et al. 2007; Schonfeld et al. 2013). Further, the small number of excess cancers, only 50 overall, limited the evaluation of site-specific risk estimates so that only total cancers could be evaluated for dose response. Such analyses of all solid cancers combined, however, do not take into account heterogeneity of the magnitude and/or the shapes of different dose-response curves across tumor sites. Thus, informative comparisons with other population studies with different underlying baseline rates and confounding influences are not straightforward. Nonetheless, the Techa River studies including the Techa River Cohort (30,000 individuals), the Techa River Offspring Cohort (31,000 individuals), and the East Urals Radioactive Trace Cohort (18,000 evacuated; 8,000 resident) are continuing to provide important information on the level of risks following chronic exposure to relatively high levels of radiation following environmental contamination.
Because there are few prospective studies of children exposed in utero and followed into adulthood, a recent cohort study of over 8,000 children of female workers at the Mayak Nuclear Facility is noteworthy (Schonfeld et al. 2012). The in utero gamma-ray doses were large (mean 54.5 mGy; max ~800 mGy) and accumulated throughout the pregnancy, and thus not received briefly at one point in time. The exposures were measured by film badges and not estimated—a notable strength and uniqueness of the study. There was no evidence that prenatal gamma radiation received during pregnancy increased the risk of solid cancer or leukemia mortality up to 60 y of follow-up. The small number of cancers, however, limited the precision of the study, and thus the negative findings were consistent in a statistical sense with the positive observations of 2,452 children born to Japanese atomic-bomb survivors who received comparable doses in utero (Preston et al. 2008). Although speculative, the absence of a radiation effect among the offspring of Mayak female workers is also consistent with the possibility that chronic exposures during pregnancy are less effective in causing cancer later in life than if the exposure were received acutely, as was the case for the children of atomic bomb survivors exposed in utero.
Daniel O. Stram (University of Southern California) provided an overview and extremely well balanced evaluation of the recent National Academy of Sciences (NAS) feasibility study on investigating cancer occurrence in populations residing near nuclear facilities in the United States (NA/NAS 2012). Based on historical radiation release data from commercial nuclear facilities, the population doses would be tiny (maximum 100–200 µSv y−1) and the statistical power of any study to find effects at such low dose would be extremely low to nonexistent. It is clear, however, that these studies are of societal important to provide reassurance to the populations living around nuclear facilities and, of course, to identify any unforeseen circumstances resulting in clusterings of cancer of etiologic and scientific import. The U.K. Sellafield Nuclear Facility cluster (in the village of Seascale), for example, generated much research that generally concluded that leukemia in children was not related to radiation releases but may have been related to a rare response to a common infectious agent due to population mixing (Doll 1999). The NA/NAS committee recommended that a limited pilot study of seven facilities in six states be initiated, focusing on childhood leukemia incidence occurring within smaller geographical units that were used in the previous NCI study (Jablon et al. 1991) (i.e., census tracts rather than counties). Other limitations of the previous NCI ecological study included follow-up only through 1984. Absence of information on population doses, use of mortality rather than incidence of cancer, the fact that the size of the county may be too large a geographical area to detect localized increases in cancer rates, the plethora of comparisons that were made increased the likelihood that chance played a role in highlighting areas with seemingly high or low cancer rates, and unknown factors associated with migration and selection of residence and occupation could contribute to cancer occurrence in these areas. Nonetheless, the large NCI survey included more than 900,000 cancer deaths in 113 counties in the United States containing or adjacent to 62 nuclear facilities that were compared with 1,800,000 cancer deaths in control counties with similar population and socioeconomic characteristics (Jablon et al. 1991). There was no evidence that mortality for any cancer, including childhood leukemia, was higher in counties with nuclear reactors than in the control counties. For childhood leukemia, the relative risk in the study counties versus their controls before start-up was 1.08, and it was 1.03 (i.e., lower) after plant start-up.
Other than the Seascale cluster, the most notable cluster of childhood leukemia was around the Krümmel Nuclear Power Plant in Northern Germany (Kaatsch et al. 2008). The study was extended to include all nuclear power plants in Germany, and the large, very well conducted, investigation found a positive association with proximity to nuclear power plants in Germany. Noting that the population exposures from emissions from nuclear power plants are much lower than average doses from background and medical sources, the authors commented that, “The reported findings were thus not to be expected under radiation biological and epidemiological considerations.” One methodological concern surrounding the extended German study was the inclusion of Krümmel Nuclear Power Plant data, which generated the hypothesis. Removal of the Krümmel cluster from the combined analysis apparently reduced the finding for childhood leukemia to nonstatistical significance (COMARE 2011; Kinlen 2011a, 2011b). The most recent comprehensive evaluation by the British around their nuclear facilities actually found a negative correlation with distance (i.e., the closer the residence to the nuclear facility, the lower the risk of childhood leukemia) (Bithell et al. 2008). Further, the recent COMARE (2011) report, which reviewed all studies up through 2011 (and should be required reading for anyone interested in this area), concluded that “there is no evidence to support the view that there is an increased risk of childhood leukemia and other cancers in the vicinity of NPPs (nuclear power plants) due to radiation effects.” Nonetheless, if public concerns about safety outweigh other priorities and resources are available, an update of the NCI study could very well provide reassurance and, as in the past, be deemed worth doing as providing a benefit to society.
Maureen Hatch (NCI) provided a marvelous finale to the NCRP 2013 Annual Meeting. She discussed effects on the public following nuclear reactor accidents and echoed previous speakers in noting that psychosocial outcomes will likely emerge as the most significant and widespread health effect—and one that until recently has not been well recognized (Bromet 2012). Risk perception plays a role and points to the importance of risk communication and radiation education (Table 3). Jimmy Buffett, in Volcano Lyrics, exemplified the problem in that despite the essential absence of population exposure in 1979 after the Three Mile Island Reactor accident, he “Don’t want to land in the Three Mile Island; Don’t want to see my skin aglow (no no no).” When I returned from visiting the damaged nuclear Fukushima Reactor in 2011, my wife told friends not “to get me angry,” alluding to the possibility that I would transform into something like the green Hulk as when Dr. Banner got mad. Perception and reality—will ever the twain be met? Hopefully we can do better with education, sound understanding, and start with the young generation.
Other than psychosocial disorders, thyroid cancer following exposures to children living near Chernobyl in 1986 is the only convincing late effect from the nuclear accident (UNSCEAR 2011). Over 5,000 thyroid cancers have been detected, but fortunately, fewer than 10 deaths have been reported. Problems in quantifying the risk following radioactive iodine exposures include the ecological nature of many studies, inadequate assessment of thyroid dose, effects of intense screening, and special surveillance of the heavily exposed and dietary deficiencies of stable iodine (IARC 2001). Perhaps the most methodologically sound study is the NCI-Ukraine study that addressed many of the deficiencies in prior studies (Brenner et al. 2011). The estimated excess relative risk at 1 Gy of 1.91 (relative risk of 2.91 at 1 Gy) following protracted exposure to radioiodines during childhood (131I has an 8 d half-life) can be contrasted with the excess relative risk at 1 Gy of 7.7 following acute exposure to external radiation (Ron et al. 1995). Although statistically compatible, the data suggest that radioactive iodines may be four times less effective than acute exposures to external radiation. This lower effectiveness is consistent with studies of thyroid nodularities after fallout from Semipalatinsk nuclear detonations, which concluded that internal exposures were three times less effective than external exposures (Land et al. 2008), and with the comprehensive studies of thyroid disorders following the Hanford 131I releases in the 1940s and 1950s, which found little evidence for a dose response for thyroid cancer, nodules, or thyroid hormone levels despite estimated mean thyroid doses of 0.17 Gy (maximum 2.8 Gy) (Davis et al. 2004).
An intriguing finding in several of the Chernobyl studies is the possible influence of dietary stable iodine on radiation-related thyroid cancer. The Ukraine-Russian-Belarus areas were inland, and diets deficient in iodine were not uncommon, resulting in endemic goiter. In one case-control study, the risk from the exposure to radioiodines appeared concentrated among children residing in severe iodine-deficient areas (i.e., where the radiation risk was three times higher than the risk observed in children residing in the areas of less severe iodine deficiency) (Cardis et al. 2005). The thyroid glands living in areas of iodine deficiency are likely more active and undergo more cellular proliferation and growth than in areas of iodine sufficiency, and it may be that this enhanced cellular activity is related to the enhanced risk observed. If the elevated radiation risk reflects an interaction with a dysfunctional thyroid gland, it would temper generalizations to other areas in the world with dietary iodine sufficiency (Boice 2005), such as around Fukushima where the diets have a surplus of stable iodine due to high fish and seaweed consumption. The child’s thyroid gland proliferates more rapidly than the adult gland, and it is thought that this rapid cell growth is the primary reason why radiation effects are so apparent after exposures in childhood and not among adults. Given the influence of stable iodine on subsequent risk of radiation-related thyroid cancer, there may be a need to reassess guidance on the use of potassium iodide during accident circumstances.
Table 6 and Table 7 provide snapshots of the Annual Meeting and ways forward into the 21st century. Radiation is in the public eye because of Fukushima, CT examinations, airport screenings, and possible terrorist attacks. Nuclear power may be on the resurgence due to concerns with greenhouse gases and projected growth in electrical demands. Because of the increasing uses of radiation, the increases in population exposures, and the increasing knowledge of radiation effects, constant vigilance is needed to keep up with the changing times. Psychosocial disorders associated with the inappropriate (but real) fear of radiation need to be recognized as a radiation detriment. Radiation risk communication, radiation education, and communication must improve at all levels: to members of the public, the media, other scientists, and radiation professionals (Table 3). Stakeholders must continue to be involved in all radiation protection initiatives (Table 2). Finally, we are at a crisis in that the baby boomer radiation professionals are depleting at a rapid rate, and there are few in the pipeline to fill the current and looming need. NCRP has initiated WARP—Where Are the Radiation Professionals? as an attempt to rejuvenate the pipeline before the trickle is at its last drop. Meetings were held in July 2013 with government agencies, military, private sector, universities, White House representatives, and societies to develop a coordinated and national action plan. Stay tuned, and please help! “If we don’t keep swimmin’ (Disney’s Nemo),” “we’ll sink (Dylan).”
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National Council on Radiation Protection and Measurements; radiation dosimetry; radiation epidemiology; radiation protection
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