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Low-Dose-Rate Epidemiology of High Background Radiation AreasAuthor(s): John D. Boice Jr, Jolyon H. Hendry, Nori Nakamura, Ohtsura Niwa, Seiichi Nakamura, andKazuo YoshidaSource: Radiation Research, 173(6):849-854. 2010.Published By: Radiation Research SocietyDOI: http://dx.doi.org/10.1667/RR2161.1URL: http://www.bioone.org/doi/full/10.1667/RR2161.1

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MEETING REPORT

Low-Dose-Rate Epidemiology of High Background Radiation Areas

John D. Boice, Jr.,a,1,3 Jolyon H. Hendry,b,1 Nori Nakamura,c,1 Ohtsura Niwa,d,2 Seiichi Nakamurae,2

and Kazuo Yoshidaf,2

a Vanderbilt University, Nashville, Tennessee and International Epidemiology Institute, Rockville, Maryland; b Gray Institute forRadiation Oncology and Biology, University of Oxford, United Kingdom; c Radiation Effects Research Foundation, Hiroshima, Japan; d NationalInstitute of Radiological Sciences, Chiba, Japan; e Health Research Foundation, Kyoto, Japan; and f Central Research Institute of Electric Power

Industry, Tokyo, Japan

A small workshop entitled International ReviewMeeting on Low Dose Rate Radioepidemiology of HighBackground Radiation Areas was held at the OhtemachiBuilding, Tokyo, January 15–16, 2010. The workshopwas organized and funded by the Health ResearchFoundation (HRF), Central Research Institute ofElectric Power Industry (CRIEPI), and the KansaiAtomic Conference. The Organizing Committee consistedof a member each from HRF and CRIEPI plus onemember affiliated with both HRF and CRIEPI and theNational Institute of Radiological Sciences. Participantswere chosen for their acknowledged expertise in epidemi-ology, physical dosimetry, biological dosimetry andradiation biology. The impetus for holding the workshopwas to review the extensive past and ongoing research onthe health effects associated with living in areas of highlevels of natural background radiation, consider theimportance and uniqueness of such research, and makerecommendations on future research endeavors.

In contrast to the large body of knowledge that hasaccumulated on lung cancer risk associated withdomestic indoor radon exposure (1), the epidemiologicalstudies conducted in areas of high background radiationthroughout the world have received less attention, inpart because of limitations associated with sample size,dosimetry, dose range and potential confounders (2).Recent studies in India and China, discussed during theworkshop, have addressed each of these deficiencies.

The lifetime population exposures of interest in thehigh background radiation areas are to terrestrial c raysfrom decaying radionuclides in the environment. Theunique aspect of such research is not that humanpopulations are exposed to low doses of radiation, butrather that the exposure is at a low dose rate and the

cumulative lifetime dose can reach appreciable levels, i.e..500 mGy, for which health effects, if present, should bedetectable. Animal studies consistently show that low doserates result in lower numbers of excess cancers than if thesame total dose were delivered briefly in time. The humanobservations, such as occupational studies of workers (3)or environmental studies of the Techa River population(4), are not as clear regarding whether low-dose-rateexposures result in lower radiation risks than seen amongJapanese atomic bomb survivors exposed briefly to cradiation and some neutrons (5). The possibilities forimproving and expanding low-dose-rate data obtainedfrom epidemiological studies gains special importancetoday with the proliferating use of radiation in medicine(CT scans and PET imaging), in airports (personnelwhole-body scanning), and in occupational and environ-mental circumstances with the possible expansion in theuse of nuclear power to generate electricity (6).

On the first day, the epidemiological studies ofpopulations with low-dose/low-dose-rate exposure to highbackground radiation were discussed, with special em-phasis on those in Kerala, India. Subsequent discussionsfocused on the current status of physical dosimetry andbiological dosimetry. The second day involved a criticalreview of the research program concluding with recom-mendation for future considerations.

1. The current status of high background radiation areaepidemiology was presented by Dr. Suminori Akiba. Thesession was chaired by Dr. Ohtsura Niwa

Comprehensive epidemiological studies in areas ofhigh background radiation have been ongoing since the1972 in Yangjiang, China (7–10) and since 1990 inKerala, India (10, 11). The elevated levels of naturalbackground radiation are due to monazite sands with ahigh content of radioactive thorium. The China HighBackground Radiation Study is well designed and iscarefully conducted and analyzed. Variations in dosedepend on village location, type of dwelling, ventilation

1 Review Committee.

3 Address for correspondence: Vanderbilt University, Nashville,TN and International Epidemiology Institute, Rockville, MD; e-mail:john.boice@gmail.com.

2 Organizing Committee.

RADIATION RESEARCH 173, 849–854 (2010)0033-7587/10 $15.00g 2010 by Radiation Research Society.All rights of reproduction in any form reserved.DOI: 10.1667/RR2161.1

849

and occupancy. Approximately 90,000 residents havebeen continuously exposed to external c-ray doses of theorder of 4 mGy/year. The dose rate in the control areas(35,000 residents) is of the order of 1 mGy/year. To datethere has been little evidence of radiation-induced healtheffects, although increased frequencies of unstablechromosome aberrations in circulating lymphocyteshave been detected.

The largest and most comprehensive study of highbackground radiation is being conducted in Kerala, India.The coastal belt of Karunagappally, Kerala containsthorium-containing monazite sand with median outdoorradiation levels of 4 mGy/year and in certain locations ashigh as 70 mGy/year. A cohort of nearly 400,000 residentsin Karunagappally was established by the regional cancercenter in Trivandrum, Kerala between 1990–1997, andinterviews were conducted to obtain individual informa-tion on cancer risk factors such as tobacco use, pregnancyhistory, education and socioeconomic status. Measure-ments of radiation levels in homes were conducted,occupancy factors were obtained from interviews, andbiological dosimetry was conducted to validate cumula-tive dose estimation. The population has a low rate ofilliteracy and a low rate of infant mortality. Medicalradiation for scanning and imaging is infrequent, there arefew environmental pollutants, and the primary occupationis fishing. Similar to the China high background radiationstudy, increases in unstable chromosome aberrations incirculating lymphocytes were detected, but no significantincreases in cancer or leukemia have been detected to date.

An initial subcohort of nearly 70,000 residents of 6 ofthe 12 available panchayats (administrative areas) wasfollowed for up to 15 years (10.5 years average), andcancer incidence was determined through the regionalcancer registry that has existed since 1990 and isdescribed in IARC’s Cancer in Five Continents with ahigh level of diagnoses based on histopathology orcytology (11). Cumulative external radiation dose foreach individual was estimated based on outdoor andindoor dosimetry of each household, taking into accountsex- and age-specific house occupancy factors. By theend of 2005, 736,586 person-years of observation wereaccumulated and 1,379 cancer cases and 30 leukemiacases were identified. The excess relative risk (ERR) ofcancer excluding leukemia per Gy was estimated to be20.13 (95% Cl: 20.58, 0.46). In site-specific analysis, nocancer site or leukemia was significantly related tocumulative radiation dose. For leukemia excludingchronic lymphocytic leukemia (CLL), the ERR per Gywas imprecise due to small numbers: 3.72 (95% CI ,0.0,337). The range of external cumulative doses was broadwith 12% of the population estimated to have received.200 mGy at the time of last follow-up (mean 161 mGy).Migration, personal habits, socioeconomic status, ageand sex were all taken into account in the analyses.Figure 1 is based on data from Nair et al. (9) on the

relative risk of all cancers excluding leukemia and 95%CI over categories of cumulative dose. The numbers ofincident cancers in each of the five dose categories are282, 371, 463, 211 and 22, respectively.

The initial subcohort was extended and preliminaryanalyses were presented on the larger population of allresidents in the 12 panchayats with similar but moreprecise results. Additional follow-up through 2008 isplanned that will increase the number of incident cancersand, because the population is continually exposed tohigh background radiation, will increase the cumulativedoses. It is being considered whether to conduct focusedscreening studies to evaluate thyroid nodular disease,cataract formation, autoimmune thyroid disease andcytogenetic markers of exposure. More research onchildhood leukemia and childhood cancer is planned,including possible expansion of the childhood exposurecohort to include neighboring high background radiationareas where over 36,000 newborns have been studiedcomprehensively for malformations after characterizationof individual radiation doses (12). Because of the relativelyhigh cumulative doses, molecular studies might beconsidered to confirm and extend recent studies of uniqueindicators of heritable mutational effects in mitochondrialDNA and on the Y chromosome (13, 14). The possibleassociation between high background radiation and non-cancer mortality, e.g., ischemic heart disease, can beevaluated. Opportunities to combine data with the Chinahigh background radiation study in Yangjiang for certaincancer sites should be pursued.

2. The current status of physical dosimetry of highbackground radiation was presented by Naoto Fujinami

Elevated background radiation levels in some areas ofthe world can result from monazite sand deposits, whichhave high levels of thorium, such as Guarapari in Brazil,

FIG. 1. Risks of all cancers except leukemia in the current Keralacohort by estimated cumulative dose (9).

850 MEETING REPORT

Yangjiang in China, and the states of Kerala andMadras in India. Some high background radiation areasare due to volcanic soils such as Mineas Gerais in Brazil,and others are caused by 226Ra in hot springs such as inRamsar and Mahallat in Iran (10).

Radiological surveys were conducted in Iran, China,India and Brazil to assess individual external doses ofinhabitants (10). Individual doses were estimated withelectronic personal dosimeters (EPDs), optically stimu-lated luminescence dosimeters (OSLDs) and/or thermo-luminescence dosimeters (TLDs). Radiation dose rateswere measured at 1 m above the ground and at theEarth’s surface using NaI(Tl) scintillation survey meters.A sample of residents in the high background radiationareas wore personal dosimeters for a day or up to severalmonths. In general, good correlations were foundbetween the direct personal measurements of exposureand those obtained by indirect methods based onambient measurements and adjustments for occupancyfactors obtained from interviews in several surveys.

In the Yangjiang area of Guangdong Province, China,radiation dose levels were found to vary significantly byhouse. Personal dosimeters could be used to estimateindividual dose, but it would be impractical to placepersonal dosimeters on the entire population of nearly90,000 residents. Thus an indirect method was appliedfor estimating individual doses from ambient radiationdose rates obtained by environmental surveys andoccupancy factors obtained by personal interviews. Tovalidate the estimation methodology, personal dosime-ters were worn by selected families and the measuredcumulative doses compared with the estimated values.There was good correlation between the estimated dosevalues and the personal dosimetry measurements,adding some assurance that the individual dose valuesestimated for each of the study subjects were reasonablyvalid and reproducible. The annual external dosesranged from 1 to about 5 mGy in the high backgroundradiation area contrasted with 0.5 to about 1 mGy in thecontrol area of Enping.

Ramsar, Iran is 160 km northwest of Tehran and nearthe Caspian Sea, and high population exposures are dueto 226Ra deposited in soil from water flowing from hotsprings (10). Based on ambient air measurements andpersonal dosimetry studies, annual personal doses fromexternal c radiation were estimated to be 6 mGy onaverage for a sample of the population, with estimatesabove 20 mGy for a small number of inhabitants ofsome high-exposure residential areas. Living 50 years inthese areas might result in a cumulative external dose ofthe order of 300 mGy on average and much higher for asmall subset of the population. The correlations betweenpersonnel monitors and estimates based on physicalmeasurements and occupancy factors were not as goodas those in China. Outdoor dose rates varied largely andirregularly, particularly in the vicinity of the 226Ra-

containing hot springs. Indoor dose rates varied amongrooms in the same house, largely because of the non-uniform distribution of travertine contained in buildingmaterial. Travertine is a terrestrial sedimentary rockformed by the precipitation of carbonate minerals fromthe geothermally heated springs. Thus individual dosesbased only on ambient measurements and occupancyfactors, i.e., the indirect method, were not judged to beaccurate. Thus for any health study, including cytoge-netic evaluations, a direct method applying personaldosimeters would be required for accurate individualdose assessments. Such assessments might be feasiblegiven the relatively small size of the exposed population,only about 2000 exposed residents; however, this samplesize would seem inadequate for an epidemiologicalcohort study. Nonetheless, focused screening studies ofthyroid disease or even lens opacities among long-termresidents might be informative, coupled with detailedindividual dose assessments and perhaps cytogeneticevaluations of chromosome aberrations.

A radiological survey in Guarapari and Meaipe,Brazil was contrasted with previous surveys in the1960s of these areas with monazite sands (10). In thedowntown areas, dose-rate levels had decreased signif-icantly in the 1990s. In the less developed areas,including beaches and unpaved roads, the dose rateswere not markedly different over the 30-year periodbetween surveys. Clearly the natural radiation environ-ment was modified by the process of urbanization,which included paved streets, new structures anddifferent building materials for homes. No furtherdosimetry or health surveys are planned. The datasuggest, though, that the opportunity to effectively studyother areas of high background radiation may be lostunless efforts are made and resources are provided soonto study these uniquely exposed populations in otherparts of the world.

During 1990–1997 in Karunagappally, Kerala, India,house-to-house visits were conducted; indoor andoutdoor c-radiation levels were measured and personalinformation was obtained by interview. Measurementswere made on over 71,000 houses and individual doseswhere estimated for the nearly 400,000 inhabitants,accounting for age, gender, occupancy factor andambient measurements (11). A random sample of 200individuals were asked to wear optically stimulatedluminescence dosimeters (OSLDs), and measured doseswere compared with the estimated doses with very goodresults. Details of the approach to dosimetry as it appliesto epidemiological studies were published (11). Annualexternal dose levels ranged from ,1 mGy in the controlareas to .10 mGy in the highest exposure levels. Sincecumulative dose is directly related to length of exposure,as the population ages, their cumulative dose alsoincreases. As of last follow-up in 2003, 12% of thepopulation had cumulative external doses in excess of

MEETING REPORT 851

200 mGy and 7% had over 500 mGy. The meancumulative population dose was 161 mGy. Individualdoses are continually being reassessed and take intoaccount migration and population movement. In partic-ular, homes within one of the panchayats (Alappad) wereseverely damaged by the tsunami triggered by theSumatra-Andaman earthquake in December 2004. Resi-dents moved away and some returned but to new homes.

3. Current status of biological dosimetry of highbackground radiation areas was presented by ToshiyasuIwasaki and Seiji Kodama. The session was chaired by Dr.Isamu Hayata

Chromosome aberrations in peripheral lymphocytesare considered a sensitive and reliable indicator ofradiation exposure. Cytogenetic investigations wereperformed in high background radiation areas in the1980s that indicated differences in chromosomal aber-rations between residents of exposed and control areas(8). These surveys were extended in China and India (10,15). Unstable chromosome aberrations (dicentrics andrings) and stable chromosome aberrations (transloca-tions) were evaluated.

In China, blood samples were taken from a sample ofadults and children and individual external doses weremeasured with electric pocket dosimeters for 24 h and/orwith thermoluminescence dosimeters for 2 months. Age-dependent increases in chromosomal translocations werefound, but correlations between stable aberrations andindividual doses were not observed. Stable transloca-tions are also induced throughout life by otherclastogenic agents, so the underlying high backgroundradiation frequency, coupled with a relatively narrowrange of cumulative doses, would make it difficult toobserve differences caused by radiation had theyoccurred. On the other hand, the background rate forunstable aberrations is low, and a significant correlationwith dose was observed. Not only did dicentrics andrings increase with age (which is directly correlated withcumulative dose), but there was also a good correlationbetween estimated cumulative dose and increasedproportions of these unstable chromosome aberrations.These biodosimetry results were interpreted to supportthe validity of the physical dosimetry methods inestimating individual doses.

Preliminary results from cytogenetic studies in Keralawere also presented. Results were analyzed in theRegional Cancer Center in Trivandrum. Unstablechromosome aberrations were scored in at least 1000metaphases per individual blood sample. Similar to theChina high background studies, there was an excellentcorrelation with unstable aberration frequencies overestimated cumulative external doses ranging from as lowas 50 mGy to nearly 400 mGy. These cytogenetic studiesprovide some assurance that the estimated cumulative

doses based on physical measurements with adjustmentsfor age, gender and occupancy are reliable for use inepidemiological studies.

The second day was spent discussing the strengths andweakness of the high background radiation studies, theirpotential for providing new knowledge on radiationeffects, and recommendations for future research. Thesession was chaired by Dr. John Boice. The other projectreviewers were Drs. Jolyon Hendry and Nori Naka-mura.

One of the committee members had published a recentreview of high background radiation studies (2), andanother member had been actively involved in priorstudies that included examinations, dose estimation andcytogenetic studies (8). All reviewers were impressed bythe extensive epidemiological work that was recentlycompleted, particularly in Kerala, and enthusiasticallysupported its continuation. These new and extendedevaluations of cancer risk in areas of chronic exposure toc radiation have the potential to provide important newinformation relevant not only to radiation protection(16) but also to public and scientific understanding ofthe level of risk after protracted exposures throughoutlife. Such knowledge is relevant to current exposuresfrom medical, environmental and occupational sources.Conceivably, accurate results could provide insights intothe dose and dose-rate effectiveness factor (DDREF)used in radiation protection and risk extrapolation thatallows for a possible reduction in the risk obtained athigh dose rates, i.e., atomic bomb survivor studies, forexposures at low doses and low dose rates (16–18).

Many of the recommendations found in the recentoverview of high background radiation studies (2)concerning what would be needed for high-qualitystudies have been or soon will be addressed in the newstudies from Kerala. The need was described for largenumbers, good dosimetry with a range of relatively highcumulative doses, accurate outcome (cancer) determina-tion, and control of confounding factors. Consideringthe success of studies of indoor radon (1), another typeof background radiation, Hendry et al. (2) wrote that‘‘the success of these studies is mainly due to the carefulorgan dose reconstruction (with relatively high doses tothe lung), and to the fact that large-scale collaborativestudies have been conducted to maximize the statisticalpower and to ensure the systematic collection ofinformation on potential confounding factors.’’ At thetime of that review article, it appeared that ‘‘recent stepstaken in China and India to establish cohorts for follow-up and to conduct nested case-control studies mayprovide useful information about risks in the future,provided that careful organ dose reconstruction ispossible and information is collected on potentialconfounding factors.’’

The present International Workshop confirmed thatthe potential for epidemiological studies of high

852 MEETING REPORT

background radiation areas to yield information onradiation risks is beginning to be realized. There arecareful individual external dose assessments, and notjust ecological values, that are based on physicalmeasurements in homes and on personal interviews foroccupancy factors. The estimated cumulative doses arevalidated with personal dosimeter measurements andcytogenetic studies. The studies are large and includenearly 400,000 subjects in India alone, which exceeds thestudy size of the Japanese atomic bomb survivors (5)and the Techa River cohort (4, 19) and is equivalent tothe size of the 15-country occupational study (3). TheKerala study to date is suggesting a lack of health risk incontrast to the other chronic radiation scenario analyses(Table 1). Potential confounders were systematicallycollected by interviews conducted prior to follow-up andcancer ascertainment. Cancer incidence and not mortalityis obtained from a regional cancer registry that began in1990. Over 70% of cancer diagnoses are confirmedhistologically. The population is literate, healthy andhomogeneous and includes men, women and children whoare being followed prospectively. There is little confound-ing influence at present related to increased medicalexposures, to CT scanning, or to environmental pollut-ants; the main industry is fishing. Finally, the cumulativedose levels are remarkably broad, and mean doses(161 mGy in Kerala) are higher and dose ranges broaderthan studies of occupational groups (19 mSv) or TechaRiver residents (40 mGy, primarily from internal intakesof radionuclides). Thus the statistical power to detecteffects should be more than adequate.

As with all epidemiological studies that are observa-tional in nature, there are limitations that must becontinually addressed. The populations appear stable atthe moment, but migration does occur, such as whatoccurred in some areas in Kerala after the tsunami in2004. Environmental radiation levels can change withredistribution of sands over the years or with urbaniza-tion so that periodic reassessment of ambient levels, atleast on a sample, is important. As the regions continue

to develop, increased exposure to medical X rays andother environmental factors may become important.Confounding factors such as tobacco use were deter-mined at interview in the 1990s and, although suchinformation is unique to occupational or environmentalstudies, re-interviewing a sample periodically should beconsidered. Occupancy factors may also change withtime. The large studies do not have large numbers ofchildren so ways to combine or enhance the childhood,populations should be considered, such as including the36,000 newborns in India who had been studied for birthdefects with family dose assessments (12). Additionalcytogenetic work should continue to confirm theestimates of high cumulative doses, and perhaps otherbiomarkers of cumulative dose (electron spin resonanceof tooth enamel or unrepaired DNA breaks detectedusing c-H2AX foci) might be considered. Given thestability of the populations, studies of possible genetic(heritable) effects could be considered such as confirm-ing and extending previous reports of mutations inmitochondrial DNA inherited from mothers (13) and inthe Y chromosome (14).

The numbers of individual cancers remain relativelysmall, so additional follow-up would provide moreuseful evaluations of site-specific risks such as leukemiaand cancers of the thyroid and breast, i.e., sites withparticular sensitivity to radiation effects (18, 19).Combining all cancers excluding leukemia has littlebiological rationale, but it is often done for radiationprotection purposes and as a general summary estimatethat radiation epidemiologists produce for comparisonswith other studies. Such ‘‘all cancers excluding leuke-mia’’ estimates are also related to background rates ofcancers, which can differ greatly across countries. InIndia and China, for example, cancers that have aninfectious etiology appear to be more prevalent than inother countries, which points to the value of individualsite-specific analyses. Finally, the extent of internalintakes of radionuclides and exposure to radon have notbeen fully evaluated.

TABLE 1Cancer Risks from Studies of Exposed Populations Contrasting Acute Exposures (atomic bomb) with

Low-Dose-Rate Exposures

Study populationSize ofcohort

Average cumulativedose (mGy)

Average years offollow-up

Number of solidcancers

ERR/Gy(90% CI)a

Techa River Cohort (4) (incidence) 17,433 40 25.6 1,836 1.00 (0.3, 1.9)15-Country Nuclear Workers Study (3)

(mortality) 407,391 19.4 12.7 4,770 0.97 (0.27, 1.80)NRRW 3rd (21) (incidence) 174,541 24.9 22.3 10,855 0.27 (0.06, 0.53)Yangjiang, China (9) (mortality) 80,640 ,100 mSv 15.5 677 20.11 (20.67, 0.69)Karunagappally, Kerala (11) (incidence) 385,103 161 10.5 1,379b 20.13 (20.58, 0.46)b,c

Atomic Bomb Survivors (5) (incidence) 105,427 ,230 26.2 17,448 0.47 (0.40, 0.54)

a The risk estimates are not strictly comparable because they include populations of different ages and sexes. The underlying background ratesof cancers differ appreciably.

b 69,958 residents in initial analysis.c 95% CI.

MEETING REPORT 853

CONCLUSION

Discussions at this workshop highlighted the uniqueopportunity to obtain quantitative information on thelong-term effects of radiation doses delivered overprotracted periods at a low rate but accumulating torelatively high dose levels. Populations residing in areasof high background radiation, particularly in India,represent a large and relatively unrecognized databasewhose value is just emerging. Lifetime doses can beestimated accurately for large numbers of individuals,cancer incidence can be determined, confounding factorscan be adjusted for in the analyses, the cumulative dosescan reach levels approaching 1 Gy with substantialnumbers exceeding 500 mGy, and the studies are largerand doses greater than current studies of occupationallyand environmentally exposed populations (18). Further,the annual dose rates of .4 mGy per year can becontrasted with actual occupational exposures today inthe U.S. nuclear industry, which are smaller and averageof the order of 2 mSv per year (20).

With the large increase in the use of diagnosticradiation, the potential increase in nuclear energyproduction, the use of X-ray scanners at airports forsecurity purposes, and so on, the world’s population willcontinue to be exposed to increased levels of radiationthroughout life (6). Large studies with good dosimetryof populations living in areas of high backgroundradiation have the potential to contribute much-neededdata on human health risks from exposures to radiationdelivered slowly throughout life.

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