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OCR for page 242
c
Radiogenic Cancer at Specific Sites
LEUKEMIA
The induction of leukemia by ionizing radiation has been well docu-
mented in humans and laboratory animals. The types of leukemia induced
and their rates of induction vary markedly, depending on the species, strain,
age at irradiation, sex, and physiological state of the exposed individuals.
They also depend on the dose, dose rate, anatomical distribution, and
LET of the radiation, among other variables. The early literature has been
summarized elsewhere (NRC80, UN77, UN82, UN86, UNDO.
Human Data
The most extensive human data on the dose-incidence relationship
come from studies of the Japanese atomic-bomb survivors and patients
treated with x rays for ankylosing spondylitis. In the atomic-bomb survivors
of the Life Span Study Cohort, a total of 202 deaths from leukemia were
recorded for the period from 1950 to 1985, during which there were an esti-
mated 2,185,335 person-years of follow-up. Analyzed in terms of absorbed
dose to the bone marrow as estimated with the new DS86 dosimetry, the
dose response for Nagasaki rises less steeply than for Hiroshima, especially
in the dose range below 0.5 Gy, but the difference between the two cities
is smaller with the DS86 dosimetry than with the T65D dosimetry and is
no longer significant (Sham. For the combined data, the rate of mortality
is significantly elevated at 0.4 Gy and above but not at lesser doses. At
bone marrow doses of 3-4 Gy, the estimated dose-response curve pecks and
242
OCR for page 243
RADIOGENIC CANCER AT SPECIFIC SITES
~ 1 5
o
cn
[,J 1 0
o
a)
Q
An
I
LD
LL
y
0 1 2
243
~(32)t(18)~(21) 1 (10) 1 (10) 1 (6) 1
i:
5
0( it.
/
-
-
-
~0
Number of cases in the
( ) I indicated dose interval
3 4 5 6
MARROW DOSE EQUIVALENT (Sv)
7 8 9
FIGURE 5-1 Cumulative leukemia mortality in Hiroshima and Nagasaki as a function of
the estimated dose equivalent to the bone marrow under DS86. By 1985, there were 51
cases in the O Sv category and 31 cases in the 0.01-0.1 Sv stratum.
turns downward (Figure 5-1~. As noted below, this pattern is characteristic
of the leukemia response in other irradiated populations. The saturation
of the leukemia response at high doses has been attributed to the reduced
survival of potentially transformed myeloblasts in the range above 3-4 Gy
(Unapt.
Based on a simple linear dose-response model, which in the opinion of
RERF analysts fit the LSS data for leukemia mortality as well as a linear-
quadratic model and better than a simple quadratic model, the excess
relative risk per Sievert was estimated to range from 4.24 to 5.21, and the
number of excess deaths per 104 person-year-Sv was estimated to range
from 2.40 for a neutron RBE of 20 to 2.95 for an RBE of 1 (Sham.
The excess mortality from leukemia reached a peak within 10 years after
irradiation and has persisted at a diminished level (Figure 5-2~. No excess
cases of chronic lymphocytic leukemia have been observed (Pr87a).
Among 14,106 patients who were followed for up to 48 years after a
single course of x-ray therapy for ankylosing spondylitis, 39 deaths from
leukemia were recorded versus a total of 12.29 expected cases (ratio of
observed to expected deaths, 3.17) (Damp. The excess deaths became
detectable within two years after irradiation, reached a peak within the first
5 years, and declined thereafter; however, the excess death rate remained
significantly elevated (relative risk, 1.87) for more than 15 years, after which
it appeared to persist with little change (Damp. The relative risk did not
vary significantly with age at the time of treatment, but it was higher in
males (3.43) than in females (1.79~. The relative risk also varied with the
hematologic type of the disease, being higher for those with acute myeloid
l
OCR for page 244
244 EFFECTS OF EXPOSURE TO LOW LE~LS OF lONIZI`VG MOTION
25
10
ID
t
CD
s
y
En
111
>
111
llJ
En
ILL
1
4 ~
\
\
..
- 54-~-
573
All Cancers Except
Leukemia (+4.8%/year)
0.5 1 1 1 1 1 1 1 1
_ 26
_ Leukemia
T ~-0.7%/year,
18
.,
22
1
~'
1
856
26
-
_ _
942
:]
922
1950- 1955- 1959- 1963- 1967- 1971- 1975- 1979
1954 1958 1962 1966 1970 1974 1978 1982
INTERVAL OF FOLLOW-UP
FIGURE 5-2 Relative risk of mortality from leukemia and all cancers other than leukemia
in A-bomb survivors, 1950-1982, in relation to time after inadiation. The number of deaths
in each interval of follow-up and 99~o confidence intervals are indicated (Pr874.
OCR for page 245
RADIOGENIC CANCER AT SPECIFIC SITES
TABLE 5-1 Observed, as Compared with Expected,
Numbers of Deaths from Leukemia in Persons Treated with
Spinal Irradiation for Ankylosing Spondylitisa
Number of Deaths
Type of Leukemia Observed
-
Expected
Myeloid leukemia
Acute 17 4.34 3.92
Chronic 3 2.05 1.46
Unspecified 4 0.71 5.63
All types 24 7.10 3.38
Lymphatic leukemia
Acute 2 0.93 2.15
Chronic 2 z.38 0.84
Unspecified 3 0.38 7.89
All types 7 3.69 1.89
Unspecified leukemia 3 0.28 10.71
All types 36 11.29 3.19
Ratio of
Observed/Expected
a From Darby et al. (Dated.
b Observed and expected deaths from leukemia occurring more than one year
after first treatment at ages less than 85 years by age at first treatment and by
type of leukemia as recorded on the death certificate. Retreated patients were
included for 12 months following treatment.
245
leukemia than for those with other types of leukemia. It was not elevated
for those with chronic lymphatic leukemia Amble 5-1~.
Analyzed in relation to the average dose to the bone marrow, which was
estimated to be 3.21 Gy, the excess relative risk amounted to O.98/Gy, or 0.45
additional cases of leukemia per 104 PYGy (Smirk. The smaller magnitude
of the risk per Gy in patients with anlylosing spondylitis, compared with
that in atomic-bomb survivors, may be ascribable to the younger average
age of atomic-bomb survivors at the time of exposure and to the fact
that they received instantaneous whole-bady irradiation, whereas in the
patients with anlylosing spondylitis only a portion of the active marrow
was irradiated and the dose was received in fractionated exposures that
usually totaled more than 5 Gy within a given treatment field (Leafy.
Murrhead and Darby have proposed different models of leukemia risk for
the spondylitics and the A-bomb survivors. They proposed a relative risk
model for the spondylitics and an absolute risk model for the atomic-bomb
survivors (Mush.
In an international case-control study of 30,000 women treated with
fractionated doses of radiation for carcinoma of the uterine cervix, the
risk was estimated to be increased by about 70%/Gy, corresponding to
an excess of 0~48 cases of leukemial104 PYGy (Bo87' Bosh. As in the
OCR for page 246
246 EFFECTS OF EXPOSURE TO LOW LEVELS OF IONIZING EDITION
Observed Data
2.8
2.6
2.4
Y 2.2
G
lo
>
g
tar
2.0
1.8
1.6
1.4
1.2
1.0
Off
-
Quadratic Exponential
Linear Exponential (A w)
Linear-Exponential (d)
Linear
~-
, .,
L l I i I l l l l l
0 2 4 6 8 10 12 14 16 18
AVERAGE BONE MARROW DOSE (Gy)
FIGURE 5-3 Relative risk of acute leukemia and chronic myeloid leukemia in women
treated with radiation for carcinoma of the uterine cervix, as influenced by the average
dose to the bone marrow. A better fit was obtained with a linear exponential model (~W)
which considered the weighted dose to each marrow component as opposed to the average
dose over all compartments (d) (Bomb.
A-bomb survivors mentioned previously, the excess cases were confined to
leukemias other than those of the chronic lymphatic type. The relative risk
was maximal within the first 5 years after irradiation, was larger in women
who were irradiated when they were under age 45 than in those who were
irradiated when they were over age 45, and reached a peak at an average
bone marrow dose of 2.5-5.0 Gy, above which it decreased (Figure 5-3~.
The data conformed to a linear-exponential model in which the total risk
equaled the sum of incremental risks to individually irradiated masses of
marrow. The latter risks, in turn, were taken to increase linearly with the
mass exposed and inversely with the total mass of marrow in the body; they
were also taken to increase curvilinearly in a manner consistent with the
dose-dependent killing of marrow cells (Bomb. In view of the decreased
risk- per Gy at high doses, it is not surprising that the average risk per
Gy in the women of this series was appreciably lower than that which has
been observed in women treated with smaller doses of ~ rave for h~.nian
gynecologic disorders (Bomb.
~d ~ ~ _ ^ ~ ~ ^
one Incidence of leukemia has been observed to be elevated similarly
in patients treated with radiation for cancers of other sites (Bo84, Cu84,
Waged. An association between previous diagnostic irradiation and adult
OCR for page 247
RADIOGENIC CANCER AT SPECIFIC SITES
247
onset myeloid or monocytic leukemia has been suggested by three case-
control studies (St62, Gu64, Gimpy; however, the data in the first and largest
of the three studies (St62) have since been reinterpreted to argue against
a causal relationship on the grounds that "the 'extra' examinations all
happened within 5 years of the onset" of symptoms of leukemia (Steal. No
association between previous diagnostic irradiation and adult-onset myeloid
or monocytic leukemia was observed in a fourth case-control study (Light.
On the basis of extrapolation from the leukemogenic effects of irradiation
in atomic-bomb survivors and other relatively heavily irradiated groups, it
has been estimated that about 1% of all leukemia cases in the general
population may be attributable to diagnostic radiography (Every.
The risk has not been confined to acutely irradiated populations, such
as those mentioned above. Early cohorts of radiologists in the United
States (Le63, Ma84), the United Kingdom (Co58), and the People's Re-
public of China (WaS8), who were exposed to x rays occupationally in the
days preceding modern safety standards, also have shown an increased inci-
dence of acute leukemia and chronic granulocytic leukemia. These diseases
have, likewise, been observed to occur with increased frequency in patients
previously injected with radium-224 or Thorotrast (NRC80~. Because of
uncertainty about the doses to the bone marrow in the occupationally and
internally irradiated populations, it is not clear how their risks per unit dose
compare with those in the more acutely irradiated populations described
above.
An excess number of cases of leukemia have been observed in children
who were exposed to diagnostic x-irradiation in utero; the excess is larger
per unit dose than that in children who were irradiated during postnatal
life. The magnitude of the excess and the extent to which it may signify
an unusually high susceptibility of the embryo and fetus are discussed in
Chapter 6 of this report. Reports of an increased incidence of leukemia
in children residing in the vicinity of nuclear installations in the United
Kingdom are reviewed in Chapter 7.
Committee Analysis
For purposes of risk estimation, the Committee's analysis was restricted
to the total mortality from leukemias of all hematologic types combined,
excluding chronic lymphogytic leukemia. Modeling in terms of the various
types of leukemia was not possible because of limitations in the available
data. The different types vary markedly in the age distributions of their
occurrence in the general population and in their relative frequencies with
time after irradiation, depending on age at the time of exposure. To this
extent, the Committee's risk model for leukemia is a gross simplification.
For both the Life Span Study (LSS) and the Ankylosing Spondylitis
OCR for page 248
248 EFFECTS OF EXPOSURE TO LOW LEVELS OF IONIZING MOTION
(ASS) data, essentially comparable fits could be obtained using either
additive or relative risk models, although somewhat different modifying
effects were required in the two models and the relative risk model was
consistently more parsimonious. It must be remembered that follow-up of
the LSS cohort did not begin until five years after exposure, by which time
the peak in the excess rate had already occurred in the ASS data. Despite
this and other differences between the two studies, the modifying effects are
reasonably consistent. The preferred model from the ASS data is a relative
risk model with a decreasing effect in time after exposure. However, the
addition of an effect of age at exposure significantly improves the fit of the
LSS data. The magnitude of this effect and also the effect of time after
exposure depends on whether exposure occurred before or after age 20.
The ASS cohort did not include individuals younger than 20 years of age
at exposure, so the age factor could not be tested in that data set.
Dose-response in the LSS data was significantly improved by the addi-
tion of a quadratic term in dose. (Here, the linear term includes both the
gamma and neutron components, the latter weighted by the assumed RBE
of 20; the quadratic component includes only the gamma component.) The
"cross-over dose" (the dose at which the linear and quadratic contributions
are equal) was estimated to be about 0.9 Gy. However, ratios of log likeli-
hood estimates are biased and for these data the uncertainty is very large
(see Annex 4F). Similarly, the "dose rate effectiveness factor" (DREF, the
ratio of the fitted slopes of the pure linear and the linear~uadratic models)
is estimated as 2 but again with a very large uncertainty.
The final preferred model for leukemia mortality used in the risk
projections is given by equation 4-3 reproduced below.
/(d) = ID + ~3d2
~ _ J exit < 15) + ,B2I(15 < T < 25~] if E ~ 20
9 ~ exp~3I(T ~ 25) + 341(25 20
Thy model is plotted as a function of attained age in Figure 5-4 and excess
risk as a function of time after exposure for males is shown in Figure 5-5.
The abrupt changes in risk with age at the time of irradiation that
are specified in the model reflect simplifying compromises in model fitting
and are not based on hypotheses concerning the biological mechanism
of age dependent changes in susceptibility. Insofar as different types of
leukemia vary in age distribution in the general population, their causative
mechanisms and temporal distributions in irradiated populations might be
expected to vary as well.
This leukemia model is based on LSS data, which do not include
information prior to five years post exposure. A number of fitted models
OCR for page 249
4.6
4.2
3.8
>`
3.4
So
a)
Q 3.0
An
~ 2.6
LIJ
>
-
LL
1.8
1.4
1.0
RADIOGENIC CANCER AT SPECIFIC SITES
0 10 20
249
Age at Exposure
5
15
25
45
60
30 40 50
AfrAINED AGE i
60 70 80
FIGURE 5-4 The relative risk of leukemia due to low LET radiation for both sexes by
attained age from age 7 to age 75 for exposure at various ages.
were tested but these produced rather varied and unreliable risk estimates
in extrapolations to this early, first 5-year period. Sources of data, other
than that from A-bomb survivors, provide some guidance on this point.
The cervical cancer study by Boice et al. (Bo87) indicates that excess
leukemia cases were observed only within the first five years post exposure.
On the other hand, the spondylitic cohort shows a mixture of excess cases
before and after five years post exposure (Damp. In that study, 14 cases
with 1.6 expected were observed in the first five years, and 25 cases with
10.7 expected after five years post exposure. One could then reasonably
argue that nearly one-half of the excess leukemias would be observed
within the first five years after exposure. The Committee chose to model
the 2- to S-year post-exposure period by extrapolating to two years the
excess relative risk observed for the S- to 10-year post-exposure period.
This method resulted in an approximately 15% increase in the lifetime
risks. The Committee's extrapolation procedure for the 2- to S-year post-
exposure period may lead to an underestimate of the actual risk, and this
should be kept in mind when interpreting the Committee's risk estimates
for leukemia.
OCR for page 250
250 EFFECTS OF EXPOSE TO LOW LEVELS OF IONIZING MOTION
16
14
-
>~
CD
~ 12 _
0 _
Q 10
-
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I
8
6
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co
llJ
X 4
2
_ ,
_~\
1'
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/
/\
~I
./ I
~1 ''
.~1
' 1
Age at Exposure
__ i
O1 1 1 1 1 1 1 1 1 1 1 1 ~ _
0 4 8 12 16 20 24 28 32 36 40
TIME AFTER EXPOSURE a
FIGURE 5-5 Excess leukemia deaths by time after exposure to low-LET radiation for
U.S. males at various ages of exposure.
Leukemia Studies in Animals
In mice, rats, dogs, swine, and other laboratory animals, a variety of
lymphoid and myeloid leukemias have been induced by irradiation (UN77,
UN86, NRC80~. In such animals, the dose-incidence relationship has been
observed to vary from one type of leukemia to another, but in no instance
does it conform to a simple, linear nonthreshold function. The most
extensively studied of the experimental leukemias are T-cell neoplasms that
arise in the mouse thymus. The induction of these growths is inhibited
drastically by shielding a portion of the hemopoietic marrow (UN77) and
may involve the activation of a latent leukemia virus (Red LV) (Yo86~.
The dose-incidence curve for the disease is of the threshold type in mice of
certain strains (UNTO. In the range of 0.5-1.0 Gy, the RBE of fast neutrons
for induction of these neoplasms has been observed to range from a value
of 1.0-2.0 with single or fractionated exposures to a value exceeding 10 with
continuous, duration-of-life irradiation (UN77, UN86 Fecal.
OCR for page 251
RADIOGENIC CANCER AT SPECIFIC SITES
251
Less thoroughly investigated are experimentally induced myeloid leu-
kemias, which have been observed in mice (Up70, Ma78, Hu87), dogs
(Fr73), and swine (Ho70) that were subjected to various regimens of
external or internal irradiation. The dose-incidence curve for myeloid
leukemia in mice rises with increasing dose of acute whole-body x or
gamma radiation, passes through a maximum at 2-3 Gy of x or gamma rays
(lower dose of neutrons), and decreases at higher doses (Figure 5-6~; in
the dose range below 1 Gy, the shape of the curve appears to vary among
strains (UN86, U187~. The downturn in the dose-incidence curse at doses
above 2-3 Gy is consistent with the reduction in numbers of potentially
transformed myelopoietic cells surviving such doses (Gr65, Ba78, Ro78,
Ma78, UNDO. In the low to intermediate dose range, the curve rises
more steeply with fast neutrons than with x rays or gamma rays (Up70,
Mo82, U187, Pr87a), and on fractionation or protraction, the incidence
per Gy decreases markedly with x or gamma irradiation but decreases less
markedly, if at all, with fast neutron irradiation (Figure 5-6~. As a result,
the neutron RBE increases with decreasing dose rate, from a value of 2-3
at dose rates exceeding 0.1 Gy/minute to a value as high as 16 at dose rates
of less than 0.01 Gy/minute (Upper. Various models have been fitted to the
observed dose-incidence data, all of which have included cell-killing terms
to account for the diminution of the response at intermediate to high dose
levels (UNTO. Although the data do not exclude a linear dose term in the
low to intermediate dose range, all models also include higher power dose
terms to account for the fact that the incidence per Gy of low-LET radiation
increases with increasing dose at high dose rates in the intermediate dose
range but is substantially reduced at low dose rates (UNDO. The induction
of myeloid leukemia, in contrast to induction of thymic lymphoma, is not
inhibited disproportionately by shielding part of the hemopoietic system
(Upon.
The incidence of myeloid leukemia per Gy has been observed to be
increased in mice in which granulocyte turnover is accelerated by injection
of turpentine and decreased in mice in which granulocyte turnover is
reduced by the elimination of microflora, implying that induction of the
disease is promoted by proliferation of granulocyte precursors (Upped.
Susceptibility to the induction of lymphoid and myeloid leukemias also
varies among mice of different strains and in relation to age at the time
of irradiation (UNTO. There is no evidence, however, that susceptibility
in mice is unusually high during prenatal life; on the contrary, the data
imply that it may be substantially reduced at that time of life (Up66,
Si81, UNDO. Whereas the incidence of lymphoid and myeloid leukemias
is typically increased by whole-body irradiation in most strains of mice,
depending on the conditions of irradiation, the incidence of reticulum cell
OCR for page 252
252 EFFECTS OF EXPOSURE TO LOW LEVELS OF IONIZING RADIATION
40
llJ
A
llJ
z 20
n
n
x
10
,,-''
I/
~ /~K'/
\
~6
in' \
-
-
-8
- 5
4 5
DOSE (Gy)
\4
1
6
FIGURE 5-6 Lifetime incidence of myeloid leukemia (in excess of control incidence) in
male mice of different strains, in relation to dose and dose rate of whole body neutron-, x-,
or y-irradiation. REM mice (U187~: acute neutron irradiation (curve 1~; acute y-irradiation
(curve 2~; CBA mice (Mo82, Mo83a, Mo83b). acute neutron irradiation (curve 3~; acute
x-irradiation (curve 4~; protracted -radiation (curve 5~. RF/[Jp mice (Upper: acute
neutron irradiation (curve 6~; protracted neutron irradiation (curve 7~; acute x-irradiation
(curve 8~; protracted y-irradiation (curve 9~.
neoplasms in such animals has usually been observed to decrease with
increasing dose (UN77, UNBID.
Summary
The risks of acute leukemia and of chronic myeloid leukemia are
increased by irradiation of hemopoietic cells, the magnitude of the increase
depending on the dose of radiation, its distribution in time and space, and
the age and sex of the exposed individuals, among other variables. The
mean latent period preceding the clinical onset of the leukemia also varies,
depending on the hematologic type of the disease as well as age at the
time of irradiation. The data do not suffice to define the dose-incidence
relationship precisely, but the dose-response curve for the total excess cases
of leukemia appears to increase in slope with increasing mean dose to the
marrow, to pass through a maximum in the dose range of 3-4 Gy, and to
decrease with a further increase in the dose.
OCR for page 341
RADIOGENIC CANCER AT SPECIFIC SITES
341
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II. Estimation of thyroid gland size, thyroid radiation dose, and predicted
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Ho88 Holm, L-E., K E. Wicklund, G. E. Lundell, J. D. Boice, N. ~ Bergman, G.
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OCR for page 342
342 EFFECTS OF EXPOSURE TO LOW LE~LS OF IONIZING EDITION
Ka85
Ke78
Ki78
Kl87
Kl82
Kn82
Ko86
Ku87
La87
La89
La80
La86
Le63
Le73
Le79
Le82
Le88
Li82
Li63
Kamiya, K., A. Inch, Y. Fujii, K Kanda, T. Kobayashi, and K Yokoro. 1985.
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Zo80
Representative terms from entire chapter:
breast cancer
