RADIATION RESEARCH 174, 889–894 (2010)0033-7587/10 $15.00
g 2010 by Radiation Research Society.
All rights of reproduction in any form reserved.
DOI: 10.1667/RR1884.1

Epidemiological Studies of Cataract Risk at Low to Moderate Radiation
Doses: (Not) Seeing is Believing
Roy E. Shore,a,1 Kazuo Neriishib and Eiji NakashimacaChief of Research, b Department of Clinical Studies, and c Department of Statistics, Radiation Effects Research Foundation,
Hiroshima and Nagasaki, Japan

posterior subcapsular (PSC) region. Radiation damage
by both direct and oxidative mechanisms causes DNA
breaks, aberrant cell migration and complex biochemicalalterations that result in aberrant crystalline protein
folding and dysregulation of lens cell morphology (1–3).
Historically, PSC opacification was thought to be thesignature lesion of radiation damage to the lens,
although more recent data suggest that radiationinduced opacities can be found in the lens cortex as well.
Cataract was one of the earliest radiation-associatedpathologies found after Roentgen discovered X rays;
Chalupecky reported an experiment showing radiationinduced cataract only 1 year later, and Treutler reported
on a cataract in an X-ray worker within 10 years (4, 5).
However, cataract was long thought to result from only
high doses of radiation to the lens of the eye. This wascompatible with the data from early cyclotron workers
with cataract after substantial neutron doses (6, 7) andwith early Japanese A-bomb studies that reported excess
cataracts among those who received over 2–3 Gy (8, 9).
A number of other, more recent high lens-dose studies
have continued to report substantial cataract excesses[e.g. refs. (10, 11)].
Induction of cataracts in humans has been viewed as adeterministic effect that had a dose threshold and forwhich the severity increased and the latency decreased as
the radiation dose increased above that threshold. This
viewpoint was particularly strengthened by a seminal
paper by Merriam and Focht in 1957 (12) that showed
all the aforementioned features in a series of persons
who had received medical radiation therapy. They
concluded that the latent period between exposure andcataract manifestation was strongly inversely correlatedwith dose and that there was no cataract induction
below 2 Gy. However, inspection of the Merriam andFocht paper shows that the observation periods after
irradiation were mostly quite short (average of 8 years)
and that they studied only 20 individuals who had
estimated lens doses under 2 Gy, a rather limited basis
for establishing a prudent protection policy. Anotherinfluential paper was based on an early systematic
ophthalmological study of A-bomb survivors by Nefzger

Shore, R. E., Neriishi, J. and Nakashima, E. EpidemiologicalStudies of Cataract Risk at Low to Moderate Radiation Doses:(Not) Seeing is Believing. Radiat. Res. 174, 889–894 (2010).
The prevailing belief for some decades has been that humanradiation-related cataract occurs only after relatively high doses;
for instance, the ICRP estimates that brief exposures of at least
0.5–2 Sv are required to cause detectable lens opacities and 5 Sv
for vision-impairing cataracts. For protracted exposures, the
ICRP estimates the corresponding dose thresholds as 5 Sv and
8 Sv, respectively. However, several studies, especially in the last
decade, indicate that radiation-associated opacities occur atmuch lower doses. Several studies suggest that medical orenvironmental radiation exposure to the lens confers risk of
opacities at doses well under 1 Sv. Among Japanese A-bomb
survivors, risks for cataracts necessitating lens surgery were seenat doses under 1 Gy. The confidence interval on the A-bomb dosethreshold for cataract surgery prevalence indicated that the data
are compatible with a dose threshold ranging from none up to
only 0.8 Gy, similar to the dose threshold for minor opacities
seen among Chernobyl clean-up workers with primarily
protracted exposures. Findings from various studies indicatethat radiation risk estimates are probably not due to confounding by other cataract risk factors and that risk is seen after bothchildhood and adult exposures. The recent data are instigating
reassessments of guidelines by various radiation protection
bodies regarding permissible levels of radiation to the eye.
Among the future epidemiological research directions, the mostimportant research need is for adequate studies of visionimpairing cataract after protracted radiation exposure. g 2010 byRadiation Research Society

INTRODUCTION

The lens of the eye is a unique organ in that it is nonvascular and has no loss of cells over the lifetime, whichmeans there is no mechanism for the removal ofdamaged cells. Cataractogenic radiation damage occurs
at the ‘‘germinative zones’’ at the anterior surface where
dividing cells form a clear crystalline-protein fiber that
migrates toward the posterior pole of the lens, the1 Address for correspondence: RERF, 5-2 Hijiyama Park, Minamiku, Hiroshima 732-0815, Japan; e-mail: shore@rerf.or.jp.

889

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SHORE, NERIISHI AND NAKASHIMATABLE 1ICRP Guidelines on Minimal Lens Doses forCataract Induction (15, 16)

End point

Brief
exposures (Sv)

Detectable opacities
Visual impairment

0.5–2
5

Fractionatedor protacted Annual dose
exposures (Sv)rate (Sv)
5
.8

.0.1
.0.15

et al. (13). They described an excess of ‘‘axial opacities’’
in their highest dose group, which they indicated wasapproximately 2 Gy or greater. A later reanalysis basedon the improved DS86 dosimetry system estimated thec-radiation threshold dose as 1.4 Gy (14). Those papers
were highly influential as a basis for the recommendations of radiation protection groups such as the ICRP
and NCRP (15–17).
The current guidelines of the ICRP regarding
radiation protection against cataracts are shown in
Table 1. For brief exposures, the dose threshold wasconsidered to be 0.5–2 Sv for minor opacities but 5 Sv
for cataracts that cause visual impairment. For protracted or fractionated exposures the corresponding
dose thresholds were thought to be 5 and 8 Sv,
respectively. The guidelines for an annual dose rate
were based on an assumption of dose limits whensubstantial exposures were received over many years.
PRINCIPAL DATA PROMPTING A RE-EVALUATIONOF CATARACT RISK GUIDELINES

The present summary will focus primarily on lowLET radiation, although there are a small number ofstudies of high-LET radiation in the literature (6, 18,19). There is now a body of data suggesting that theguidelines for allowable lens dose might not be
sufficiently conservative. Another recent review reachingsimilar conclusions was published by Ainsbury et al. (3).
In a 1968 report, a blinded ophthalmological screening study of 234 New York City children given X-ray
treatment for scalp ringworm and 232 without X-ray
treatment indicated a significant, but imprecise, increased age-adjusted odds ratio (OR) of 5.9 [95%confidence interval (CI): 1.4–24] in minor opacities at
an early age after an eye dose of about 0.5 Gy (20).
A Swedish cohort of 484 treated with radium plaquesin infancy for skin hemangiomas received .0 to 8.4 Gy(mean, 0.4 Gy; 10% received .1 Gy) of c radiation to
the lens. An ophthalmological screening at a mean ageof 46 years showed dose-related risks of minor lens
opacities for both PSC (OR1Gy 5 1.50, CI: 1.1–2.1) andcortical opacities (OR1Gy 5 1.35, CI: 1.1–1.7) (21).
Persons exposed to c radiation for up to 15 years fromliving in radiocontaminated buildings in Taiwan were
given ophthalmological examinations (22). No radiation
effect was observed among the 53 examined at ages

22–65 years. The reported 61 examinees at ages 3–
20 years, with an estimated dose range of 1–1200 mGy(mean ,170 mGy), showed a dose–response association(OR1Gy 5 1.18, CI: 1.02–1.36) for subclinical lesions
described as ‘‘focal lens defects.’’ An average 4.7-year
update of those originally examined before age 20
showed a further dose-related increase in the size andnumber of focal lens defects (23)Studies of opacities among NASA astronauts haveused a radiation exposure database that includes lensdoses from diagnostic X rays, trapped radiation andgalactic cosmic rays (GCR). The first report ofscreenings for opacities indicated that astronauts withrelatively higher lens doses (.8 mSv, average 45 mSv)
had a higher incidence and earlier appearance of lens
opacities than those with lower doses (,8 mSv) (24).
This was recently updated and extended by Chylack etal. (25). They compared lens opacity prevalence in 171
astronauts who had flown in space with 53 astronauts
who had not flown in space, 95 military aircrew and 99
military non-aircrew. The digitized Nidek EAS 1000 lensimages were graded by computer software for nuclear,cortical and PSC lens opacities. Adjustment was made in
the analysis for individual sunlight-exposure scores,
demographics, medical history items, smoking, genderand age. They reported that cortical opacity frequency
was significantly higher in exposed astronauts than in
the comparison groups. The number and size of PSC
opacities was greater among the astronauts who had
flown compared to those who had not. No association
was found between space radiation exposure and nuclear
opacities. These results suggest increased cortical and
PSC cataract risks at relatively low radiation doses,
although dose units were not reported (25).
An occupational study of 8,600 Chernobyl clean-up
workers reported statistically significant dose–response
relationships for several opacity end points based on two
blinded ophthalmological examinations administered
2 years apart (26). A dose reconstruction was performed
to estimate both c-ray and b-particle doses to the eyelens with some account taken of dose uncertainties (27).
The median dose was 123 mGy, and 95% had estimateddoses ,500 mGy. Significant dose–response associations were seen for most of the categories (28) of nonnuclear type cataracts: Stage 1 PSC cataracts (OR1Gy 5
1.42, CI: 1.01, 2.00), Stage 1 posterior cortical cataracts(OR1Gy 5 1.51, CI: 1.09, 2.10), and all (Stage 1–5) nonnuclear cataracts (OR1Gy 5 1.65, CI: 1.18, 2.30) (26). For
Stage 2–5 non-nuclear cataracts, the association was
only suggestive (OR1Gy 5 1.82, CI: 0.82, 3.72). As
expected, no association was seen for nuclear cataracts(OR1Gy 5 1.07, CI: 0.56, 2.04). An analysis by age at thetime of work at Chernobyl showed a higher radiation
risk among those who were younger at exposure (Shore,
unpublished, 2009). The analyses were able to adjust fora number of other risk factors for cataract (e.g., age,

CATARACT RISK AT LOW TO MODERATE RADIATION DOSES

smoking, diabetes), but the results should be temperedby the fact that there were substantial uncertainties in
estimated lens doses for individuals.
Several recent studies of cataract frequency in relation
to radiation dose among A-bomb survivors have been
conducted in the Adult Health Study (AHS), which
provides biennial clinical examinations to a fixedsubcohort of survivors. An ophthalmological screening
study (29) was conducted of 873 AHS participants,
including as many as possible of those under age 14 at
exposure and those who had participated in an earlier
cataract screening study (30). Using a standardized
opacity scoring system (31), the investigators foundstatistically significant dose–response associations forposterior subcapsular opacities, with an OR1Gy 5 1.41
(CI: 1.21, 1.64), and for cortical opacities, with an OR1Gy
5 1.29 (CI: 1.12, 1.49). Since the lenses were photographed, it was possible to conduct blinded rescoring of
the lens photographs by a single ophthalmologist for
better standardization; this led to risk estimates virtually
identical to those indicated by the original scoring (32).
In addition, they found greater radiation risk for PSC
opacities among those exposed at younger ages. A dosethreshold analysis of those data gave a best estimate of
0.6 Gy (CI: ,0, 1.2) for cortical opacities and 0.7 Gy(CI: ,0, 2.8) for PSC opacities. The investigators did
not observe a statistically significant excess (P . 0.2)
among those who were exposed in utero, but thestatistical power for that observation was quite limited.
Since a major question regarding radiation cataract
induction pertains to the risk and dose threshold forcataracts that cause visual impairment, a second AHS
study examined the prevalence of cataract surgeries
among 3,761 study subjects 55–57 years after thebombings, in which 479 surgical-cataract cases were
documented (33). The study subjects were primarily 0–
35 years old at exposure. The analysis examined theassociation with radiation dose, after adjusting for city,
gender, age at exposure (and age at risk), and history of
diabetes. A linear model provided a good fit to the data,
which was not materially improved by adding a quadratic
term. The radiation risk estimate for lens removal surgery
was an OR1Gy 5 1.39 (CI: 1.24, 1.55). There was no
indication that age at exposure modified the magnitude of
the radiation effect. A key finding was that the dosethreshold analysis showed a best dose-threshold estimateof 0.1 Gy (CI: ,0, 0.8 Gy), i.e., the data were compatible
with no dose threshold or a threshold up to 0.8 Gy but nothigher. A subsequent unpublished analysis of the somewhat enlarged data set (645 persons with surgicallyremoved cataracts among 3,994 examined) yielded a risk
estimate very similar to the others reported (Fig. 1) and abest dose-threshold estimate of 0 Gy (CI: ,0, 0.7)
(Neriishi and Nakashima, unpublished, 2008).
Currently, a cataract-surgery incidence study is being
conducted for 1986–2005, the interval in which cataract

891

FIG. 1. Prevalence of surgically removed cataracts (n 5 645
persons) by dose among 3,994 A-bomb survivors in the Adult HealthStudy, 2000–2002. Adjusted for age, gender, city and history of
diabetes.

surgery was systematically recorded in the medical
records of AHS participants. The value of an incidence
study is that it minimizes the potential biases that might
have occurred in the prevalence studies described above;it also permits a better assessment of age- and timerelated variables. Preliminary analyses, after potentiallyadjusting for a large variety of cataract risk factors,
show a risk estimate and a dose-threshold estimate very
similar to the prevalence data.
LOW-DOSE STUDIES

Although the low-dose studies generally had insufficient statistical power to make major contributions to arisk assessment, they may give indications of whether therisk at those doses is generally compatible with the risk
estimates derived from higher-dose studies. An ophthalmological screening study of Ukrainian children exposed downwind of the Chernobyl accident, comparedwith those upwind, showed an excess of posterior
subcapsular opacities (OR 5 2.8, CI: 1.3, 6.1) in the
downwinders with estimated Chernobyl doses of around
30 mGy (34). However, because of the voluntary
screening-participation process and the fact that theophthalmologists could not be blinded as to exposure
status (which was defined by screening location),
potential biases due to self-selection or differential
screening sensitivity cannot be ruled out.
A low-dose occupational study of 35,700 U.S.
radiologic technologists did not observe a statisticallysignificant dose–response trend for self-reports of either
total cataracts (ERR1Gy 5 2.0, CI: 20.7, 5.7) or
surgically removed cataracts (ERR1Gy 5 1.5, CI: 23.4,
6.4) (35). The mean estimated dose was 28 mGy, and thehighest dose group was ,60 mGy. However, the excess

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SHORE, NERIISHI AND NAKASHIMA

risk for total cataracts in the highest dose group wasnearly statistically significant (OR 5 1.18, CI: 0.99, 1.40).
The authors also found that self-reports of the number ofdiagnostic X rays to the head or neck were associated withthe risk of total cataracts but not surgically removed
cataracts. Another study, involving an ophthalmologicalexamination of Chinese radiation workers and an
unexposed comparison group, suggested a higher risk
among the radiation workers (36), but insufficient study
details are available to fully evaluate the results.
Two studies have retrospectively assessed whether
patients with CT scans to the head are at elevated risk
for cataracts, but the studies have yielded mixed results.
An initial report suggested an association with posterior
subcapsular opacities (OR 5 1.5, CI: 1.1, 2.0) (37), but asecond study of approximately the same size did not(OR 5 0.9, CI: 0.6, 1.3) (38).
STATUS OF RISK ASSESSMENT

A preliminary question to be addressed is whether the
existing studies have been able to take into accountpossible bias or confounding by other risk factors for lens
opacities. A number of the main risk factors have been
evaluated in various studies, for example, age (all studies),
diabetes mellitus (21, 22, 25, 26, 29, 33–35), corticosteroid
use (21, 22, 26, 35), and smoking (25, 26, 29, 33, 35).
Ultraviolet-radiation exposure was grossly examined by a
few studies (22, 26, 33, 35), but only the astronaut study
had detailed data concerning it (25). In general, there islittle evidence to suggest that confounding factors havebeen a serious problem in the studies reported here.
While it clearly would be useful to have more
confirming data and studies with fewer limitations,
there nevertheless is enough information to maketentative weight-of-evidence judgments regarding several important issues. A first question is whether there is arisk for minor opacities at low to moderate doses to thelens. Several studies with doses primarily below 1 Gy
were positive (20–22) but did not specifically analyze
their data for a dose threshold. Two other studies havedirectly addressed this question. The Chernobyl cleanup worker study obtained dose-threshold estimates forstage 1 PSC and cortical opacities of about 0.35 Gy, withCI of about 0.2–0.65 (26). The A-bomb screening study
analyzed a range of opacity severities together, thoughmost were early opacities, and found estimated dosethresholds of 0.6–0.7 Gy for both PSC and cortical
opacities, though the wide CI encompassed both no
threshold and a rather high threshold (29). The
similarity in the dose-threshold results between the Abomb study with a single brief exposure and theChernobyl clean-up workers with fractionated/protracted exposures is notable. Ainsbury et al. (3) have also
pointed out that protraction of doses does not appear toaffect risk significantly. However, more data on thispoint are clearly needed, because the precision ofexisting studies is limited.
A secondary question about this end point is whether
radiation-associated minor opacities progress to become
vision-impairing cataracts. Most of the data on thisquestion are anecdotal, with a suggestion that a fractionof them progress and earlier high-dose studies suggestingthat the rate of progression may be dose-related (39).
As to the more consequential cataracts causing visual
impairment, there is no informative study available ofsuch risk after highly fractionated or protracted
exposure, which reflects an important gap in thescientific evidence. The A-bomb study, with a brief
exposure, has addressed vision-impairing cataracts byanalyzing the prevalence of cataract surgeries in theclinical AHS subcohort. The result, after adjusting forage and other variables, was a dose-threshold estimateof 0.1 Gy (CI: ,0, 0.8 Gy) (33). A preliminary analysis
of cataract surgery incidence in the AHS yielded asimilar dose-threshold upper bound (Nakashima and
Neriishi, unpublished, 2009). One uncertainty with the
A-bomb data comes from basing the analysis on aweighted Gy (c-ray z 10 3 neutron) dose metric; if thetrue neutron RBE for cataract were 20 or 30, this could
alter the estimated dose threshold but probably not
greatly since neutrons constitute only a small fraction of
the dose. Based largely on experimental data, the ICRP
has tentatively concluded that the RBE for neutron
induction of cataracts is in the range 2–20 (40).
Another question of import for radiation protection
purposes is the degree to which the risk of radiationassociated opacities is modified by age at exposure.
Several different studies reported that exposure at an
early age confers more risk per unit dose than exposure
at a later age (26, 30, 32, 41), although other human data
have not provided support for this (33). Most data sets,
however, have had only a limited age range, so arriving
at a broad-based answer is difficult.
Although PSC opacities have been considered theclassical sentinel effect of radiation on the lens, there are
now several studies showing radiation effects for cortical
opacities as well (21, 25, 26, 29). Various studies, however,
have found that nuclear cataracts are not associated withradiation exposure (21, 25, 26, 29), with one possible
exception being a study of airline pilots (42).
Ultimately one would like to ask what biologicalmechanisms mediate the development of radiation
cataracts. This question is beyond the scope of thisreview, but mention should be made that a lens tissuebank of extracted cataracts from A-bomb survivors has
been initiated at the RERF (K. Neriishi, principal
investigator) in anticipation of collaborations withvarious radiobiologists to study mechanistic questions.
Environmental co-exposures (e.g. smoking) or genetic
factors may affect susceptibility to cataract induction byradiation. For example, a study has shown that

CATARACT RISK AT LOW TO MODERATE RADIATION DOSES

haploinsufficiency of the mrad9 and atm genes confers
added susceptibility to radiation cataractogenesis inmice (43). It will be of interest to determine whether
heterozygous mutations in those or other human genes
are involved in radiation cataract susceptibility.
ACKNOWLEDGMENT
This work was supported by the RERF (Research Protocols 2-75
and 3-00), Hiroshima and Nagasaki, Japan, a private, nonprofit
foundation funded by Japan’s Ministry of Health, Labor and Welfare
and the U.S. Department of Energy, with the latter funding provided
partly through the U.S. National Academy of Sciences.
Received: June 4, 2009; accepted: August 21, 2009; published online:
August 30, 2010

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