J. Radiat. Res.

, 49, 83–91 (2008) Lecture Note

Cancer Risks and Low-Level Radiation in U. S. Shipyard Workers

Genevieve M. MATANOSKI*, James A. TONASCIA, Adolfo CORREA-VILLASEÑOR,

Katherine C. YATES, Nancy FINK, Elizabeth ELLIOTT,
Bruce SANDERS and Deborah LANTRY

US nuclear workers/Cancer mortality/Low dose radiation/Epidemiology.

The risks for four cancers, leukemia, lymphopoietic cancers (LHC), lung cancer and mesothelioma,
were studied in workers from shipyards involved in nuclear powered ship overhauls. The population rep-
resented a sample of all workers based on radiation dose at study termination. The final sample included
28,000 workers with ≥ 5.0 mSv, 10,462 workers with < 5.0 mSv and 33,353 non-nuclear workers. Nuclear
workers had lower mortality rates for leukemia and LHC than US white males but higher rates of lung
cancer and a significant five-fold excess of mesothelioma. Dose-dependent analyses of risks in the high
exposure group indicated that for each cancer the risk increased at exposures above 10.0 mSv. An internal
comparison of workers with 50.0 mSv exposures to workers with exposures of 5.0–9.9 mSv indicated
relative risks for leukemia of 2.41 (95% CI: 0.5, 23.8), for LHC, 2.94 (95% CI: 1.0,12.0), for lung cancer,
1.26 (95% CI: 0.9, 1.9) and for mesothelioma, 1.61 (95% CI: 0.4, 9.7) for the higher exposure group.
Except for LHC, these risks are not significant. However, the increasing risk with increasing exposure for
these cancers, some of which are known to be related to radiation, suggests that low-level protracted expo-
sures to gamma rays may be associated with these cancers. Other agents such as asbestos, which are com-
mon to shipyard work, may play a role especially in the risk of mesothelioma. Future follow up of the
population would identify bounds on radiation risks for this population for comparison with similar risks
estimated from other populations.

from estimated exposures at a single point in time based on

INTRODUCTION
The Japanese Atomic Bomb survivors have provided most
of the current knowledge concerning the risks from exposure
to external radiation.1–3) Risks from fractionated long-term
radiation exposures have been studied in underground ura-
nium miners, but these exposures are limited to alpha
particle radiation with lung cancer as the primary health out-
come.4–7) For the Japanese population risks are determined
*Corresponding author: Phone: +1-410-223-1866,
Fax: +1-410-223-1867,
E-mail: gmatanos@jhsph.edu
Department of Epidemiology, Johns Hopkins Bloomberg School of Public
Health, 111 Market Place, Suite 850, Baltimore, MD 21202-6709, U.S.A..
This paper was presented on October 15, 2003, at the International Sympo-
sium “Health Effects of Low Dose Radiation on Cancer Risk” organized by
Low Dose Radiation Research Center, Central Research Institute of Electric
Power Industry, Tokyo.
Lecture notes were assembled by K. Ishida, K. Sakai, and H. Tanooka and
the paper rewritten by the author.
The study described in this document has been reviewed and approved by
the Committee on the Review of Use of Data from Human Subjects of the
Johns Hopkins School of Public Heath.
doi:10.1269/jrr.06082
location of individuals in relation to the radiation source. For
the uranium miners, risks are derived only from estimated
exposures based on time spent in the mines. Scientists have
questioned whether cumulative doses of gamma radiation
based on one or a few high exposures versus multiple low
exposures over extended time periods as occur in occupa-
tions are equivalent in terms of cancer risks. Recent research
has suggested that perhaps low doses of radiation may act
on cells in a different way than high dose exposure.8–12) In
addition, if doses based on low versus high dose rate expo-
sure are not equivalent, then examining the risks associated
with different external radiation exposure scenarios in pop-
ulations other than the Japanese would be important.
Approximately 30 years ago, the Department of Energy
with the cooperation of the Navy undertook a study of ship-
yard workers in eight Navy and private shipyards that were
involved in overhaul of nuclear vessels. The National Insti-
tute of Occupational Safety and Health (NIOSH) also under-
took a study of one of these yards. The initial NIOSH report
showed no risk of leukemia associated with radiation
exposures13) but a longer follow up has indicated that radia-
tion exposures are associated with an increased risk of leu-
kemia mortality.14)

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84 G. M. Matanoski et al.
BACKGROUND
The nuclear workers in shipyards differ from many radi-
ation-exposed workers in that their jobs are not directly
related to working with a radiation source as do radiological
technicians for example. They are exposed incidentally to
radioactive materials when carrying out tasks related to their
trades because the materials they handle have become radio-
active. For example, plumbers working on pipes and other
materials that receive coolant water from the reactor are
exposed. Other workers performing the same job in other parts
of the ship remote from the reactor have little or no exposure.
The source of exposure for shipyard workers is from neu-
tron-activated corrosion products in the coolant system. The
major effective radiation exposure is to cobalt-60 (half-life
5.3 years), which decays with 1 low energy beta emission
and 2 high energy gamma rays. The dosimetry database of
the Navy also includes as part of the monitoring program, a
small number of radiographers and medical personnel who
may have had different radiation exposures.
A second important characteristic of the shipyard popula-
tion is that individual exposures have been measured from
the first overhaul. Members of the radiation safety program
continuously monitor workers for compliance with both
wearing and positioning of badges or dosimeters. Therefore,
this shipyard population has measured exposures for each
individual for the entire period of overhauls.
In summary, radiation exposure among shipyard workers is
associated with specific trades and areas worked within the
ship during overhaul. This exposure occurs at varying low
dose levels over time and a comprehensive monitoring pro-
gram provides dosimetry data for all individuals. Thus, this
population provides a unique opportunity to study low dose
exposure to gamma radiation over a prolonged period of time.
The current article includes the early analysis of the mor-
tality of workers through January 1, 1982. These preliminary
Table 1. Population for Study
≥ 5.0 mSv
Initial Population
Study Population
Stratified Random Sample
Person-years of follow-up*
Median age at entry to follow-up
Median year at entry to follow-up
* Unconfirmed deaths omitted from analysis.
Includes data from seven shipyards only.
J. Radiat. Res., Vol. 49, No. 1 (2008); http://jrr.jstage.jst.go.jp
reported results completed in the late 1980s include data
from only seven shipyards and for only four selected cancers
that were examined in detail. These cancers were selected
because of their suspected association with radiation and
asbestos exposure. The results summarize the data reported
to the U.S. Department of Energy in the early 1990s.
METHODS AND POPULATION
Study population
The initial population represented all employees in eight
shipyards and consisted of about 800,000 workers, 700,000
of whom were non-nuclear workers, as seen in Table 1. The
roster of workers was established from all records of
employees in each shipyard. Most workers in the non-
nuclear group were excluded because they had completed
employment before the start of nuclear overhauls, which
represented the beginning of potential radiation exposure for
most jobs. Radiation exposed workers were defined as all
workers certified to work in areas having potential exposure
to radioactivity at some time from the start of the nuclear
ship overhauls and who had an employment record and a
dosimetry record on the radiation database. Since women
and African-Americans represented a very small number of
the population of nuclear workers, their data were excluded
from analysis. Follow up of all workers in one shipyard was
not complete at the time of analysis and so all data for that
yard were omitted from the preliminary analysis. Non-nuclear
workers considered comparable to the nuclear workers were
defined as all persons employed at any time during overhauls
of nuclear vessels in each shipyard who were not considered
certified to work in areas with potential radiation. Since this
population of 77,000 nuclear and 117,000 non-nuclear
workers represented a large group, follow up was limited to
a stratified random sample of the group. The final sample
included all nuclear workers with lifetime exposures in the
shipyard of 5.0 mSv or more at the time of death or end of
Nuclear Workers Non-nuclear
< 5.0 mSv
35,079 71,772 692,612
28,060 49,449 117,718
28,000 10,462 33,353
356,091 139,746 425,070
34.3 33.6 33.4
1968.1 1967.0 1967.3
 Cancer Mortality in Shipyard Workers
follow up on January 1982 (28,000), about 20% of nuclear
workers with lifetime exposures below that dose (10,462),
and about 30% of non-nuclear workers (33,353). Additional
exclusions included military personnel and workers with
employment for less than 1 year.13)
Exposure assessment
Nuclear ship overhauls began at different times in each of
the eight shipyards from 1957 through 1967 but similar radi-
ation monitoring programs were started in each shipyard
with initial overhaul. The monitoring techniques to deter-
mine exposures of individuals differed during the period of
follow up. Exposures were measured initially using film
badges with open and closed windows to record both beta
and gamma radiation. However, the population rarely
received recordable beta radiation. The badges were read
monthly. The minimum detectable effective dose was esti-
mated to be 0.1 mSv. In 1973 to 1974, all shipyards convert-
ed to thermal luminescent dosimeters (TLDs) that were read
daily. The new procedure led to a reduction in all annual
doses due to the limitation of measuring low doses in the
minimum detection range when cumulated doses are frac-
tionated into daily rather than monthly readings. The actual
recorded radiation exposure for each worker was used to
represent the effective dose of cobalt 60 without adjustment
for differences in potential detection level with different
devices, differing procedures over time or other potential
sources of exposure to radiation such as medical x-rays. The
radiation records were obtained from a database available
from the Navy. The information was validated on a random
sample of individual records using the workers medical
records where dose was recorded independently. The effec-
tive dose was used to define the samples and, thus, was used
in the analysis for consistency in reviewing all cancers.
Organ doses will be considered for any future analysis.
The yards require constant monitoring of each worker for
compliance in wearing dosimeters. They also conduct con-
tinuous air monitoring programs to detect air releases of
radiation. Routine surveillance procedures include external
and internal reviews to validate the accuracy of dosimeter
measurements using standard exposures.15) The annual and
cumulative measurements of radiation exposures from mon-
itoring were available for each nuclear worker from the start
of overhaul to end of follow up on January 1, 1982.
Study sample
The study sample was selected to be similar in distribu-
tion to the characteristics of the ≥ 5.0 mSv group in regard
to birth year, hire year, total duration worked, duration of
pre-nuclear work and job hazard index. Simultaneous adjust-
ment for these time factors during the sample selection
resulted in a carefully balanced population in regard to time
of exposures. The job hazard index was not intended to con-
trol for specific shipyard exposures but was used as a strat-
J. Radiat. Res., Vol. 49, No. 1 (2008); http://jrr.jstage.jst.go.jp
85
ification variable to control for general industrial exposures
among the three exposure groups. The hazard index score
was developed for each job through a unique procedure that
ranked all jobs based on the overall exposure to hazardous
substances for that job. A team of industrial hygienists with
experience in the shipyard environment were polled until
they reached a consensus agreement on the hazard score for
each job. For example, the jobs that represented three or
more percent of the workers and were included in the high
rank level were welder, painter and pipefitter. In this scheme
a job hazard index is not determined from a single agent but
from many possible hazardous agents. This stratification
variable was required for the entire population of nuclear
and non-nuclear workers for purposes of sampling. The only
job records that could be abstracted efficiently in order to
assign a hazard score from such a large number of records
(about 200,000) was the last job held. Thus, each individual
was ranked based on his last job. Since most shipyard jobs
represent skilled trades, this classification procedure was
deemed appropriate since most workers remain in one trade
throughout their shipyard employment. Pre-nuclear work
periods represented the time employed prior to the start of
dosimetry records for individual nuclear workers. In order to
balance the groups for the duration worked before starting
nuclear work, a pseudo pre-nuclear period was developed for
each non-nuclear worker by creating a subgroup of these
workers that were similar to the ≥ 5.0 mSv subgroup for the
other four variables. Then the non-nuclear workers were
assigned a pseudo pre-nuclear work variable, which repre-
sented a duration of “pre-nuclear” work that was the same
or greater than the distribution of that variable in the com-
parable nuclear reference group. Since 40 percent of nuclear
workers were recruited into the radiation program after five
or more years of employment, inclusion of the “pseudo pre-
nuclear work” time variable assured that the non-nuclear
worker group had the same long employment prior to radi-
ation start as did the nuclear workers. This avoided any
“survival bias” that might occur in nuclear workers related
to the fact that they were actively working at recruitment
into radiation work.
As seen in Table 2, the three exposure categories were not
similar based on the five strata characteristics before selec-
tion of the sample. Non-nuclear workers had increased pro-
portions in the older and younger age groups, more recent
years of hire, jobs with lower hazard indices and shorter
durations worked. After random selection of the samples
from the nuclear worker group at < 5.0 mSv and the non-
nuclear workers, all three groups were similar in all charac-
teristics (Table 3).
Although jobs were not directly compared in the three
groups, all nuclear compared to non-nuclear workers initial-
ly did have some differences in the distribution of jobs based
on last job title. Jobs were divided into 49 occupational title
codes as well as 21 “prefix” codes, the latter representing a
86 G. M. Matanoski et al.

Table 2. Characteristics of Study Population by Sampling Table 3. Characteristics of Random Sample by Strata, Birth-
Strata, Birthyear, Year of Hire, Job Hazard Index, Duration of year, Year of Hire, Job Hazard Index, Duration of Pre-Nuclear
Pre-nuclear Work and Total Duration Worked* Work and Total Duration Worked
NW ≥ 5.0 NW < 5.0 NNW NW ≥ 5.0 NW < 5.0 NNW
(N = 28,542) (N = 49,635) (N = 119,179) (N = 28,542) (N = 10,462) (N = 33,353)
Variable No. % No. % No. % Variable No. % No. % No. %
Birthyear Birthyear
<1920 5240 18 11967 24 26984 23 <1920 5240 18% 1920 18% 5861 18%
1920–1929 6298 22 9702 20 16658 14 1920–1929 6298 22% 2307 22% 7195 22%
1930–1939 6486 23 9959 20 15979 13 1930–1939 6486 23% 2382 23% 7802 23%
1940–1949 8345 29 13994 28 30958 26 1940–1949 8345 29% 3059 29% 9932 30%
1950+ 2173 8 4013 8 28600 24 1950+ 2173 8% 794 8% 2563 8%

Year of Hire Year of Hire

<1950 5435 19 11185 23 21627 18 <1950 5435 19% 1976 19% 5860 18%
1950–1959 5977 21 9771 20 11294 10 1950–1959 5977 21% 2152 21% 6221 19%
1960–1969 12048 42 20078 41 36079 30 1960–1969 12048 42% 4462 43% 15035 45%
1970+ 5082 18 8601 17 50179 42 1970+ 5082 18% 1872 18% 6237 19%

Job Hazard Index Job Hazard Index

Missing 1440 5 2152 4 3940 3 Missing 1440 5% 547 5% 1727 5%
Low 5038 18 13601 27 26238 22 Low 5038 18% 1929 18% 7534 23%
Medium 13047 46 23585 48 59452 50 Medium 13047 46% 4783 46% 14918 45%
High 9017 32 10297 21 29549 25 High 9017 32% 3203 31% 9174 28%

Duration of Pre-Nuclear Work Duration of Pre-Nuclear Work

0- years 10685 37 16413 33 N/A N/A 0- years 10685 37% 3874 37% 12871 37%
2- years 6326 22 10447 21 N/A N/A 2- years 6326 22% 2308 22% 7313 22%
5- years 4348 15 7293 15 N/A N/A 5- years 4348 15% 1565 15% 5003 15%
10- years 4272 15 6763 14 N/A N/A 10- years 4272 15% 1238 12% 4633 14%
20+ years 2911 10 8719 18 N/A N/A 20+ years 2911 10% 1477 14% 3533 11%

Total Duration Worked Total Duration Worked

0- years 870 3 2709 5 13531 11 0- years 870 3% 537 4% 2145 6%
2- years 2822 10 8923 18 38350 32 2- years 2822 10% 1991 19% 7561 23%
5- years 5554 19 10318 21 26367 22 5- years 5554 19% 2089 20% 7702 23%
10- years 8716 31 11454 23 15572 13 10- years 8716 31% 2650 26% 7428 22%
20+ years 10580 37 16231 33 25359 21 20+ years 10580 37% 3195 31% 8517 26%
*Includes data from eight shipyards

skill or responsibility level (e.g. foreman). The differences in of “prefix” codes indicates that, in general, the nuclear work-
the distribution of jobs between nuclear and non-nuclear ers have a higher percentage of foremen, inspectors and
workers were small and would have been partially controlled planners among these titles compared to non-nuclear work-
by the stratification on the hazard index (Table 4). A review ers whereas the latter group have more “worker” and “help-

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 Cancer Mortality in Shipyard Workers 87

Table 4. Distribution of Selected Last Occupational Title outcomes were determined from underlying causes of death
Codes* for Workers in Four Shipyards Based on Radiation Sta- listed on death certificates with confirmation of the diag-
tus noses of selected cancers through review of hospital records
Non-nuclear and cancer registry databases. The cancers in the current
Nuclear Workers Workers analysis do not reflect the results of these hospital records
(N = 24130) (N = 125925) Significant searches. Since the U.S. data used for comparison consisted
of death certificate information only, the same data had to be
Job Title* N % N % at p < = 0.05
used for causes of death for the shipyard workers in order to
5 Electrician 1942 8 9087 7 NS be comparable. Hospital records were used only to verify the
8 Engineer 2418 10 8075 6 S accuracy of the death certificates. For these cancers this ver-
ification process confirmed that virtually all death certificate
23 Laborer 200 1 6120 5 S
results were accurate. The study team obtained death certif-
25 Machinist 3090 13 16215 13 NS icates on over 99 percent of the suspected deaths from the
30 Nuclear Engineer 989 4 1815 1 S four specific cancers.
35 Pipefitter 2777 12 7795 6 S
37 Rigger 1103 5 4874 4 NS
Analysis
Two independent analyses were performed on the data.
42 Shipfitter 1426 6 10394 8 S First, a categorical analysis was performed using three life-
47 Welder 1348 6 11306 9 S time cumulative dose groups defined as cumulative dose at
88 Administrative 323 1 4894 4 S death or study termination corrected by age and calendar
time to US white male rates. A second dose sensitive anal-
*Specific job titles are included if they represented four percent or
more of jobs for either nuclear or non-nuclear worker. ysis using the Life Table method16) was performed on work-
ers with lifetime exposures of 5.0 mSv or more. For this
analysis, the risk of cancer deaths for each individual at each
er” classifications. (Data are not shown.) As shown in Table dose they experienced at a specified age and calendar time
4, among the specific job titles that represent at least four period was compared to the risk in the 5–9 mSv reference
percent or more of the distribution of job titles of either population using the same adjustment methods. This time
nuclear or non-nuclear workers, three were significantly dependent analysis results in all individuals with high cumu-
higher in nuclear and four in non-nuclear workers with the lative doses adding person-years to all lower dose groups
remaining three jobs equally distributed in the two groups. included in the time dependent analysis although they would
The most important differences may be the higher propor- not have an event at the lower doses. The group with < 5
tion of pipefitters among nuclear workers and the higher mSv could not be used as a reference because that group was
proportion of shipfitters and welders among non-nuclear excluded from the time dependent analysis. Since the cate-
workers. Thus, even after balancing the populations by job gory of < 5.0 mSv was a sample of all workers with a final
hazard index, the nuclear workers could differ from non- dose of that level and since the multistrata sampling was
nuclear workers in regard to exposure to other agents com- complicated making it impossible to reconstruct the original
mon in shipyards. population from the sample, this group could not be includ-
ed as part of the dose, age and calendar time dependent
Follow up of population analysis. Adding person-years from the 5 mSv or more
Multiple data sources were searched to determine the vital population to a sample of the < 5 mSv group would have
status of each worker including Social Security Administra- inflated the person-years in the < 5 mSv exposure group and
tion files, Civil Service Administration files, Health Care artificially lowered the risk in this group. The risks were ana-
Financing Administration (HCFA) files, Virginia mortality lyzed with lagging for different exposure periods. This
files and the National Death Index. All of these files could adjustment excludes any radiation exposure during a speci-
determine whether a worker was deceased. In addition, fied “lag period” from the worker’s exposure for the person
Social Security, HCFA, and Civil Service Administration years or events accrued in that period. Thus, the cumulative
had separate files that could determine whether the enrollee person-years and any events occurring at any point in the
was alive. All shipyard workers who were current employees follow up are attributed to the cumulative radiation dose to
at any time during the final year of the study were classified that time minus any dose accrued during the lag period. The
as alive if there was no confirmation of a death from a death lag periods included no lag and 2, 5, 10, and 15 years. The
certificate. Vital status, either living or deceased, was deter- short lag period represented the time when first cases of leu-
mined on all but four percent of the workers. Follow up was kemia reportedly have appeared after exposures to a known
not complete for one shipyard at study termination and all leukemogen. The longer lag periods were included to repre-
data on those workers are excluded from the analysis. The sent possible latency periods of solid tumors. However, the

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88 G. M. Matanoski et al.

number of workers with 10 or more years of follow up was Table 6. Age-adjusted Leukemia Mortality by Radiation
limited since the median follow up period for all workers Group
was 13 years. Therefore, the analysis reported includes only External Comparison to US Male Population:
a lag of two years for leukemia and five years for all other
Non-nuclear
cancers as well as the analysis with no lag. Nuclear Workers Workers

RESULTS ≥ 5.0 mSv < 5.0 mSv

Deaths 21 4 29
Four cancer sites were selected for initial analyses SMR 0.91 0.42 0.97
because of their potential association with either radiation or
95% CI (0.56,1.39) (0.11,1.07) (0.65,1.39)
asbestos exposure: leukemia, lymphoma and hematopoetic
cancers, lung cancer and mesothelioma. For each cancer, the Internal Comparison:
upper portion of the Tables 5–9 represents the overall cate-
Workers No Lag Lag 2 years
gorical results by lifetime radiation exposure status and the
lower portion represents the calendar time, age and dose Relative Relative
dependent Life Table analysis of the complete 5.0 mSv or Nuclear ≥ 5.0 mSv Risk 95% CI Risk 95% CI
more population.
5.0-* 1.00 – 1.00 –
The all cause mortality ratios, as shown in Table 5, indi-
cate that the risk of death in shipyard workers is equal to or 10.0-* 2.63 (0.6,24.2) 3.05 (0.7,27.8)
lower than that of US white males. However, only in the two 50.0-* 2.41 (0.5,23.8) 2.29 (0.4,23.2)
nuclear categories are the risks significantly lower than the
Nuclear < 5.0 mSv 1.02 (0.2,11.3) 1.07 (0.2,11.9)
general population. The relative risks for all outcomes are
higher in both nuclear workers at < 5.0 mSv and non-nuclear Non-nuclear 2.37 (0.6,20.5) 2.54 (0.6,21.9)
workers than in the reference category of nuclear workers
*Dose dependent analysis (Reference 5.0–9.9 mSv)
with doses of 5.0 to 10.0 mSv . In the dose dependent anal- Adjusted for age and calendar time by indirect adjustment
ysis with a lag of five years, the risk increases with increas-
ing dose. This increase, even at the highest dose, is not

Table 5. Age-adjusted All Cause Mortality by Radiation Table 7. Age-adjusted Lymphatic and Hematopoietic Can-
Group cer Mortality by Radiation Group
External Comparison to US Male Population: External Comparison to US Male Population:

Non-nuclear Non-nuclear
Nuclear Workers Workers Nuclear Workers Workers

≥ 5.0 mSv < 5.0 mSv ≥ 5.0 mSv < 5.0 mSv
Deaths 2215 973 3745 Deaths 50 13 84
SMR 0.76 0.81 1.00 SMR 0.82 0.53 1.1
95% CI (0.73, 0.79) (0.76, 0.86) (0.97, 1.03) 95% CI (0.61, 1.08) (0.28, 0.91) (0.88, 1.37)

Internal Comparison: Internal Comparison:

Workers No Lag Lag 5 years Workers No Lag Lag 5 years
Relative Relative Relative Relative
Nuclear ≥ 5.0 mSv Risk 95% CI Risk 95% CI Nuclear ≥ 5.0 mSv Risk 95% CI Risk 95% CI
5.0-* 1.00 – 1.00 – 5.0-* 1.00 – 1.00 –
10.0-* 1.10 (0.89,1.23) 1.08 (0.96,1.22) 10.0-* 3.23 (1.1, 12.6) 5.84 (1.5, 50.8)
50.0-* 1.03 (0.91,1.16) 1.13 (0.99,1.30) 50.0-* 2.94 (1.0, 12.0) 5.37 (1.2, 48.7)

Nuclear < 5.0 mSv 1.13 (1.01,1.26) 1.15 (1.02,1.30) Nuclear < 5.0 mSv 1.71 (0.57, 7.2) 2.95 (0.6, 27.4)

Non-nuclear 1.39 (1.26,1.53) 1.39 (1.24,1.55) Non-nuclear 3.58 (1.3, 13.5) 5.63 (1.5, 47.5)
*Dose dependent analysis (Reference 5.0–9.9 mSv) *Dose dependent analysis (Reference 5.0–9.9 mSv)
Adjusted for age and calendar time by indirect adjustment Adjusted for age and calendar time by indirect adjustment

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 Cancer Mortality in Shipyard Workers 89

Table 8. Age-adjusted Lung Cancer Mortality by Radiation significant.

Group The leukemia risk by lifelong exposure category indicates
External Comparison to US Male Population: that the highest mortality ratio compared to U.S. white males
occurs in non-nuclear workers as seen in Table 6. Although
Non-nuclear
Nuclear Workers Workers
all ratios indicate risks below that of the general population
of US white males, comparison of the low and high radiation
≥ 5.0 mSv < 5.0 mSv exposure in categorical groups indicates a leukemia mortal-
Deaths 237 98 306 ity that is two times higher in the group with highest lifetime
SMR 1.07 1.11 1.15 exposures compared to the low exposure group. In the dose
dependent analysis shown in the lower portion of the table,
95% CI (0.94, 1.21) (0.90, 1.35) (1.02, 1.29)
there is a suggestion of an increase in risk with dose but the
Internal Comparison:
relative risks in each dose group are non-significant due to
small numbers. The risk of leukemia for workers with doses
Workers No Lag Lag 5 years
of 50 mSv or more is 2.41 (95% CI: 0.5, 23.8) times higher
Relative Relative than the reference category of 5.0–9.9 mSv. The numbers by
Nuclear ≥ 5.0 mSv Risk 95% CI Risk 95% CI cell type are too small for analyses. Myeloid leukemias rep-
5.0-* 1.00 – 1.00 –
resent 60 percent of all cases with identified types.
The overall mortality from lymphatic and hematopoetic
10.0-* 1.08 (0.8, 1.6) 1.05 (0.7, 1.6)
cancers (LHC) including leukemia shown in Table 6 indi-
50.0-* 1.26 (0.9, 1.9) 1.36 (0.9, 2.1) cates a significantly low LHC death rate for those exposed
at < 5.0 mSv compared to US white males with the pattern
Nuclear < 5.0 mSv 1.16 (0.8, 1.7) 1.25 (0.9, 1.9)
of SMRs by category that is similar to that for leukemia. The
Non-nuclear 1.21 (0.9, 1.7) 1.22 (0.9, 1.7) ratio for those in the ≥ 5.0 mSv category is higher than the
lowest radiation exposure group. In the dose dependent anal-
*Dose dependent analysis (Reference 5.0–9.9 mSv)
Adjusted for age and calendar time by indirect adjustment ysis, the relative risk at 50 mSv or more is significantly high-
er (RR = 2.94; 95% CI: 1.0, 12.0) than risks at 5.0 to 10.0
mSv. That difference is even more apparent when the expo-
sures in the last 5 years of follow up before a specific
Table 9. Age-adjusted Mesothelioma Mortality by Radiation calendar time or event (lag 5 years) are omitted (RR = 5.37;
Group 95% CI: 1.2, 48.7).
The lung cancer standardized mortality ratios using the
External Comparison to US Male Population:
comparison US population for the life long exposure cate-
Nuclear Workers Non-nuclear gories indicate little difference in ratio between the three
Workers
groups as shown in Table 8. All ratios are above 1.00 but
≥ 5.0 mSv < 5.0 mSv only non-nuclear workers have a significantly higher mortal-
Deaths 18 8 10 ity ratio from lung cancer compared to US white males. In
the dose dependent analysis, the risk of lung cancer mortal-
SMR 5.11 5.75 2.41
ity is about 30 percent higher for those receiving 50 mSv or
95% CI (3.03, 8.08) (2.48, 11.33) (1.16, 4.43) more exposure compared to 5.0 to 10.0 mSv (RR = 1.26;
95% CI: 0.9,1.9) and there is a suggested dose response for
Internal Comparison:
both lag-periods. For the 277 lung cancers with hospital
Workers No Lag Lag 5 years record reviews, data on morphology indicated 36 percent
Relative Relative had squamous cell carcinoma, 20 percent had adenocarcino-
Nuclear ≥ 5.0 mSv Risk 95% CI Risk 95% CI
ma, 15 percent had small cell carcinoma and 18 percent had
an undifferentiated cell type with smaller percentages of oth-
5.0-* 1.00 – 1.00 –
er cell types.
10.0-* 1.21 (0.3, 9.1) 1.24 (0.3, 7.2) Mesothelioma was examined because radiation workers’
50.0-* 1.61 (0.4, 9.7) 1.50 (0.3, 9.2) jobs may involve exposures both to asbestos and radiation.
The mortality from mesothelioma based on life long catego-
Nuclear < 5.0 mSv 1.45 (0.4, 8.5) 1.31 (0.3, 7.8) ries of radiation exposure indicate that shipyard workers in
Non-nuclear 0.61 (0.2, 3.4) 0.57 (0.1, 3.3)
all groups have 2.4 to 5.8 times higher mortality compared
to US white males and that SMRs are 2.1 to 2.4 times higher
*Dose dependent analysis (Reference 5.0 – 9.9 mSv)
in the radiation exposed groups compared to the non-
Adjusted for age and calendar time by indirect adjustment
exposed (Table 9). The dose dependent comparison of risks

J. Radiat. Res., Vol. 49, No. 1 (2008); http://jrr.jstage.jst.go.jp

90 G. M. Matanoski et al.
suggests that the risk of mesothelioma increases with
increasing radiation in the ≥ 5.0 mSv group. The dose cate-
gory of 50.0 mSv or more has a RR = 1.6 (95% CI: 0.4, 9.7)
compared to the workers with 5.0 to 10.0 mSv exposures.
None of these observations are significantly different from
1.0 (or no excess risk) due to small numbers in each catego-
ry. The increases could be related to differences in asbestos
exposure that may be correlated with the radiation dose
although there is no apparent reason to suggest that this
should occur.
DISCUSSION
Workers involved with overhaul of nuclear powered ships
represent an occupational group exposed intermittently to
low-level gamma-ray exposure from cobalt 60 while per-
forming their usual jobs. The mortality analysis based on
lifetime radiation exposure shows that these nuclear workers
with cumulative exposures both below and above 5.0 mSv
have lower risks of leukemia, lung cancer and LHC than
non-nuclear workers. The radiation exposed workers are
selected into the program from the group of all shipyard
workers primarily on the basis of work performance since
one of the shipyard’s aims is to complete an overhaul of the
reactor area in the shortest time period possible to reduce the
total radiation exposure per overhaul. The workers also must
complete a physical exam, radiation training and certifica-
tion prior to being allowed to work in the potentially
exposed areas. Thus, selection bias may explain the overall
lower SMR of these cancers in nuclear versus non-nuclear
workers since healthier and more efficient workers may be
selected for radiation training and certification. Mesothelio-
ma risks that are known to be associated with asbestos
exposure actually show higher SMRs in nuclear versus non-
nuclear workers suggesting there may be differences in
exposure to confounding agents, especially asbestos, in
nuclear work. For example, Table 4 suggests a higher pro-
portion of pipefitters who have potential asbestos exposure
among nuclear compared to non-nuclear workers.
The dose dependent data analyses suggest that doses of
radiation of 10.0 mSv or more are associated with an
increased risk of leukemia, LHC, lung cancer and mesothe-
lioma compared to workers with doses of 5.0 to 10.0 mSv.
For each cancer the risks appear to increase with increased
dose but few values except for LHC show significant differ-
ences. However, the case numbers are small and only three
dose groups are analyzed which limits any use of trend anal-
ysis. The small number of deaths can be attributed to the fact
that overhauls began between 1957 and 1967 and recruitment
of workers ceased at the end of follow up in 1982 resulting in
only about 13 years as the median period of observation.
The population for study represented three groups that
were carefully balanced for several confounding time factors
such as age, year of hire and duration of pre-nuclear work
J. Radiat. Res., Vol. 49, No. 1 (2008); http://jrr.jstage.jst.go.jp
as well as a work exposure factor termed the hazard index.
However, that hazard factor was not meant to control for
specific exposures. Therefore, the increased risk of mesothe-
lioma and lung cancer could have been related to confound-
ing exposures to asbestos and for lung cancer, differences in
smoking by radiation exposure also could have played a role
in the observed risks. Unfortunately, the smoking habits of
all individuals in the study were not available. However, a
survey of one shipyard suggested no difference in the age-
adjusted rates of ever smokers in nuclear and non-nuclear
workers and a lower rate of current smokers in the nuclear
groups. Thus, if all shipyards were similar to the one sur-
veyed, smoking could have explained the difference in the
higher lung cancer risks in non-nuclear versus nuclear work-
ers. However, smoking differences are unlikely explanations
for the increased risks observed in the higher radiation
exposed group versus the lower dose reference groups.
The data on jobs of workers indicate a higher proportion
of pipefitter jobs in nuclear versus non-nuclear workers.
Since asbestos is one hazardous agent associated with pipe-
fitting work, one might expect higher rates of mesothelioma
in nuclear compared to non-nuclear workers and that is the
case (Table 9). However, although jobs may have differed
between nuclear and non-nuclear workers, it is less likely
that the jobs differed between workers at the various dose
levels. Therefore, the increases in risk by radiation dose,
even though not significant, suggest that radiation may be
playing a role. Further investigation of the joint effects of
asbestos and radiation on the risk of mesothelioma has been
completed on the total study population by one of the co-
investigators.17) The results suggest that each agent may
independently increase the risk of this cancer. Further adjust-
ment for possible confounding occupational exposures
should be included as part of future studies of this popula-
tion. Stratification on the general hazard index in the study
sample should not interfere with the ability to examine spe-
cific agents of interest.
The only results that conflict with this apparent dose
response effect from radiation are that for many of these
cancers, leukemia, lung cancer and LHC, the non-nuclear
workers have as high a risk as the highest radiation dose. As
suggested, a probable explanation for these findings is that
selection of workers for the radiation program may intro-
duce a bias that is reflected in inherently low risks of cancer
in nuclear versus non-nuclear workers at comparable ages.
This phenomenon, which might be termed an “enhanced
healthy worker effect”, results from a two step selection pro-
cess for nuclear workers. They must be selected to work in
shipyards at time of hire (the usual “healthy worker effect”)
and then they are selected again to become nuclear workers
based on health and work performance while employed.
Therefore, the analyses of nuclear workers by dose are the
most reliable assessment of the potential risks from low dose
radiation in this population. Unfortunately, the lowest dose
 Cancer Mortality in Shipyard Workers
of < 5.0 mSv is only analyzed as a category because the
sampling strategy was complicated and that group could not
be expanded to utilize in dose dependent analysis.
The consistency of the finding of an increased risk with
increasing dose for each cancer in the dose-dependent anal-
ysis is highly suggestive that radiation is associated with the
risk of these cancers. In addition, the LHC cancers, which
include leukemias and multiple myelomas as well as non-
Hodgkin lymphomas, are recognized or suspected to be
associated with an increased risk from radiation exposure.
These cancers show a significant and very high five to six-
fold excess risk in 50 mSv or more radiation-exposed work-
ers compared to those in the low dose reference group.
Therefore, these data on increasing risks from radiation
exposure for LHC support the findings from similar studies
in the literature. The consistency of the increase in risk with
dose for each cancer and the significantly high risk of LHC
associated with radiation doses of 10 mSv or more indicate
that the shipyard population, which was still very early in
follow up at the time of termination of the study, needs to
have additional follow up to determine the risks of leukemia,
LHC and solid tumors. These early data suggest the workers
may have a risk of some cancers from low dose radiation. A
precise estimate of risks from nuclear work in this popula-
tion could be obtained by examining the mortality for all
77,000 nuclear workers in the study population plus addi-
tional entrants into the program and extending the follow up
to more recent years. The additional data provided could
identify the boundaries of the estimates of risks from low-
level repeated doses of gamma radiation and these results
could be compared to risks derived from the Japanese Atom-
ic Bomb survivors who essentially had a single radiation
dose. Any future analyses also should adjust the radiation
risks for other job exposures.
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Lecture on October 15, 2003
Received on September 15, 2006
Accepted on July 24, 2007
J-STAGE Advance Publication Date: August 10, 2007