United States
Environmental Protection
Agency
Office of
Radiation Programs
Washington, D.C. 20460
EPA 520/1-84-020
December 1984
Radiation
&EPA Frequencies of Chromosomal
Aberrations and Sister
Chromatid Exchanges in the
Benthic Worm
arenaceodentata Exposed to
Ionizing Radiation

-------
EPA 520/1-84-020
UCRL-53524
FREQUENCIES OF CHROMOSOMAL ABERRATIONS
AND SISTER CHROMATID EXCHANGES IN
THE BENTHIC WORM Neanthes arenaceodenta ta
EXPOSED TO IONIZING RADIATION
BY
Florence L. Harrison
David W. Rice, Jr.
Dan H. Moore
Lawrence Livermore National Laboratory
Livermore, California 94550
December 1984
This report was prepared as an account of contract work sponsored by the
United States Environmental Protection Agency under Interagency Agreement
No. AD-89-F00070 with Lawrence Livermore National Laboratory.
Project Officer
Marilyn E. Varela
Office of Radiation Programs
U.S. Environmental Protection Agency
Washington, D.C. 20460

-------
FOREWORD
In response to the mandate of Public Law 92-532, The Marine
Protection, Research and Sanctuaries Act of 1972, as amended, the
Environmental Protection Agency (EPA) has developed a program to
promulgate regulations and criteria to control the ocean disposal
of low-level radioactive wastes. The EPA seeks to understand the
mechanisms for biological response of marine organisms to the low
levels of radioactivity which may arise from the release of these
wastes as a result of ocean disposal practices. Such information
will play an important role in determining the adequacy of environ-
mental assessments provided to EPA in support of any disposal permit
application. Although packaging of low-level radioactive wastes
designed to prevent release during radiodecay is required by EPA, some
release of radioactive material into the deep sea environment may occur
if a package deteriorates. Therefore, methods for evaluating the
impact on biota are being evaluated.
Mortality and phenotypic responses are not anticipated at the
expected low environmental levels which might occur if material were
released from the low-level waste packages, and traditional bioassay
systems are unsuitable for assessing sublethal effects in the marine
environment. Therefore, the purpose of the study reported here is to
assess the feasibility of using a cytogenetic (chromosome study)
approach, and to compare the usefulness of two cytogenetic endpoints,
i.e., chromosomal aberrations and sister chromatid exchanges, as mea-
sures of low-level radiation effects on a marine organism, Neanthes
arenaceodentata~
This report characterizes the dose response of arenaceodentata
using the chromosomal aberration endpoint. This report also presents
the results of extending the range of doses, previously examined by the
Office of Radiation Programs, for which sister chromatid exchange has
been studied.
The results of this research may be useful Agency-wide because
large numbers of pollutants are mutagenic. Fundamental cytogenetic
endpoints, such as chromosomal aberration and sister chromatid
exchange, could ultimately be used to compare the risks of several
pollutant classes.
The Agency invites all readers of this report to send any comments
or suggestions to Mr. David E. Janes, Director, Analysis and Support
Division, Office of Radiation Programs (ANR-461), U.S. Environmental
Protection Agency, Washington, D.C. 20460.
Sheldon Meyers, Acting Director
Office of Radiation Programs
iii

-------
DISCLAIMER
This document was prepared as an account of work sponsored by an agency of the L'nited States Government.
Neither the United States Government nor the University of California nor any of their employees, makes
any warranty, express or implied, or assumes any legal liability or responsibility for the accuracy, com-
pleteness, or usefulness of any information, apparatus, product, or process disclosed, or represents that its
use would not infringe privately owned rights. Reference herein to any specific commercial products, process,
or service by trade name, trademark, manufacturer, or otherwise, does not necessarily constitute or imply its
endorsement, recommendation, or favoring by the l 'nited States Government or the U niversity of California.
The views and opinions of authors expressed herein do not necessarily state or reflect those of the United
States Government thereof, and shall not be used for advertising or product endorsement purposes.
iv

-------
CONTENTS
Foreword 		iii
Abstract		1
Introduction 		2
Methods 		6
Worm Culture and Handling 		6
Irradiation		8
Cytogenetic Preparation and Scoring of Worm Chromosomes		8
Quality Assurance		12
Results 		13
Chromosomal Aberrations		13
Sister Chromatid Exchanges 		16
Discussion 		24
Chromosomal Aberrations		24
Sister Chromatid Exchanges 		25
Feasibility of Cytogenetic Methodology 		26
Mechanisms of Chromosomal Aberration and Sister Chromatid Exchange
Formation 		29
Conclusions 		30
Appendix A. Quality Assurance		31
Appendix B. Effects of Cell-Cycle Time on Sister Chromatid
Exchange Frequency		45
References		52
v

-------
FREQUENCIES OF CHROMOSOMAL ABERRATIONS AND SISTER CHROMATID
EXCHANGES IN THE BENTHIC WORM
Neanthes arenaceodentata EXPOSED TO IONIZING RADIATION
ABSTRACT
Traditional bioassays are unsuitable for assessing sublethal effects from ocean
disposal of low-level radioactive waste because mortality and phenotypic responses are
not anticipated. We compared the usefulness of chromosomal aberration and sister
chromatid exchange (SCE) induction as measures of low-level radiation effects in a
sediment-dwelling marine worm, Neanthes arenaceodentata. The SCEs, in contrast to
chromosomal aberrations, do not alter the overall chromosome morphology and in
mammalian cells appear to be a more sensitive indicator of DNA alterations caused by
environmental mutagens.
Newly hatched larvae were exposed to two radiation-exposure regimes of either
x rays at a high dose rate of 0.7 Gy (70 rad)/min for as long as 5.5 min or to ^Co gamma
rays at a low dose rate of from 4.8 X 10~^ to 1.2 X 10~* Gy (0.0048 to 12 rad)/h for 24 h.
After irradiation, the larvae were exposed to 3 X 10~^M^ bromodeoxyuridine (BrdUrd) for
28 h (x-ray-irradiated larvae) or for 54 h (^Co-irradiated larvae). Larval cells were
examined for the proportion of cells in first, second, and third or greater division.
Frequencies of chromosomal aberrations and SCEs were determined in first and second
division cells, respectively.
Results from x-ray irradiation indicated that dose-related increases occur in
chromosome and chromatid deletions, but a dose of >2 Gy (>200 rad) was required to
observe a significant increase. Worm larvae receiving ^Co irradiation showed elevated
SCE frequencies with a significant increase at 0.6 Gy (60 rad).
We suggest that both SCEs and chromosomal aberrations may be useful for measuring
effects on genetic material induced by radiation. However, more detailed studies on
these responses and the factors affecting them are needed before either can be used to
quantify the effects of the chronic exposure to low-level radiation that is received under
field conditions.
1

-------
INTRODUCTION
Since the onset of the nuclear age, radioactive wastes have been disposed on land and
in the ocean. In addition, the testing of nuclear weapons has contributed measurable
quantities of radionuclides to the oceans. In the U.S., low-level solid radioactive wastes
were disposed in the coastal areas of both the Atlantic and Pacific Oceans (Joseph et al.,
1971). Although these practices were discontinued by 1970, little effort was made until
recently to determine the subsequent fate and distribution of radionuclides in these
wastes. Information now available indicates that some man-made radionuclides from
ocean disposal are present in bottom sediments but that there is little or no accumulation
by organisms in man's food chain (Dyer, 1976; Noshkin et al., 1978).
Several countries have continued to dispose of radioactive wastes in the ocean. The
use of oceanic waters for radioactive waste disposal is being considered currently in the
U.S. because of special problems presented by land disposal of radioactive particulate
waste (Meyer, 1979). Some opposition to oceanic disposal of nuclear waste has been based
on fear of irreparable consequences to ocean ecosystems and on the continuing lack of
empirical scientific data documenting the effects. This lack of data can be attributed in
part to the absence of appropriate bioassays. Traditional bioassays that use mortality and
phenotypic responses as end points are unsuitable for assessing the sublethal effects that
may be expected from oceanic disposal of low-level radioactive waste.
The U.S. Marine Protection Research and Sanctuaries Act as amended requires that
the Environmental Protection Agency (EPA) Administrator, in reviewing requests for
permits, determine that ocean "dumping will not unreasonably degrade or endanger human
health, welfare, or amenities, or the marine environment, ecological systems, or economic
potentialities" (Marine Protection, Research, and Sanctuaries Act, 1972). This act
requires the EPA to establish regulations and criteria to implement a permit program.
One possible criterion would utilize a bioassay technique that requires a methodology for
detecting the response of marine organisms to low levels of chronic irradiation. With such
methodology, post-disposal monitoring could verify the assumptions regarding doses to
marine organisms and evaluate ultimately the impact of radiation on the organisms. Such
a monitoring scheme could theoretically serve as an early-warning system.
Deleterious effects of radiation on organisms are well documented (Templeton et al.,
1976; U.S. National Academy of Science (NAS), 1980). Increased cell death and mutations
have been related to increased radiation dose. Changes in genetic material include base
damage, single-strand breaks, double-strand breaks, hydrogen-bond rupture, and
cross-linking between DNA and proteins (Yu, 1976). Some lesions can be detected by
2

-------
examining ceils in metaphase for chromosomal aberrations and sister chromatid exchanges
(SCEs). The yield of chromosomal aberrations in cells exposed to radiation (Blaylock and
Trabelka, 1978) is much better documented than that for SCEs (Kato, 1979).
The chromosomal aberrations are caused by the breakage of chromosomes followed
by either the subsequent rejoining of the broken ends to form new combinations or the
failure of broken ends to rejoin. They are identified by changes in chromosomal structure
that include deletions, translocations, and rings (Archer et al., 1981). It is well
established that a substantial part of the changes in DNA induced by ionizing radiation
consists of single- and double-strand breaks in the phospho-diester backbone of the DNA
molecule. However, according to Evans (1977), all chromosomal aberrations do not result
from one, two, or three specific lesions, but are caused by either a variety of changes in
the DNA that lead to helix disruption, helix distortion, or interference with the normal
replication process of the cell.
The SCEs represent the interchange of DNA replication products at apparently
homologous loci (Latt et al., 1981). This exchange, which does not alter the overall
chromosome morphology, was demonstrated first by autoradiographic techniques using
tritiated thymidine (Taylor, 1958). Currently, these exchanges are distinguished by
exposing cells to 5-bromodeoxyuridine (BrdUrd) for two rounds of replication and a
combined staining with fluorochrome plus Giemsa (FPG) (Perry and Wolff, 1974). Data on
SCE frequency in cells exposed to some physical and chemical agents indicate that in
mammalian cell systems, SCEs are a sensitive indicator of DNA alterations caused by
environmental mutagens and carcinogens.
The effects of ionizing radiation on the frequencies of SCEs have been studied in a
number of cell systems exposed to either beta rays, beta plus x rays, x rays, or gamma
rays (Table 1). Ionizing radiation resulted generally in increases in the baseline frequency
of SCEs. However, for equivalent doses there was a greater increase in frequency of
chromosomal aberrations than of SCEs. Very few data from these experiments are
applicable to whole-animal, in vivo irradiation. Increases in SCEs were found following in
vivo radiation of mice with x rays (Nakanishi and Schneider, 1979). In this study, as in the
majority of those listed in Table 1, dose rates much greater than those expected at
oceanic disposal sites were used.
Studies are required to further characterize the incidence of chromosomal
aberrations and SCEs in organisms that have been irradiated with the doses and the
long-term exposure regimes expected at radioactive waste-disposal sites. Nereidae
worms are indigenous to marine disposal sites used by the U.S. in the past, and it is
expected that they would be present in any future designated areas as well. Because they
live in the benthos and do not migrate, they are well suited to studies of radionuclides and
other contaminants that sorb to sediments.
3

-------
Table 1. Irradiation conditions used in previous studies examining the frequencies of
sister chromatid exchanges in cells exposed to different kinds of radiation.
Cell system
Radiation
source
Total
dose
Dose
rate
Reference
Kangaroo rat
cells (Pt-Kl)
Chinese hamster
cells (D-6)
Chinese hamster
cells (CHEF-125)
Chinese hamster
cells (CHEF-125)
Chinese hamster
cells (CHO)
Chinese hamster
cells (CHO)
Syrian hamster
embryo cells
3(3H)a
B(3H)
3(3H)
or
3(3H)
plus
x ray
g(3H)
plus
x ray
x ray
x ray
Human lymphocytes x ray
(normal & ataxia
telangiectasia)
Chinese hamster x ray
cells (CHO)
Live mice	x ray
Human lymphocytes x ray
x ray
Mouse C3H/10T-1/2 x ray
cells
Mouse 10T-1/2 x ray
cells
Syrian hamster x ray
embryo ceils
8-38 rad
8-38 rad
27-3560 rad
380-700 rad
25-200 rad
^80 <5c 400 rad
175 rad
50-80 rad
0.3-1.4 rad/h Gibson and
Prescott (1972)
0.3-1.4 rad/h Kato (1974)
200 rad
100-400 rad
300 R
300 R
50-400 R
200-500 R
0.8-99 rad/h
11-19 rad/h
50 rad/min
^3-14 rad/h
60 rad/min
50 rad/min
50-100 rad 100 rad/min
50 rad/min
100-600 rad 450 rad/min
200-1500 rad
32 R/min
32 R/min
80 R/min
126 R/min
Marin and
Prescott(1964)
Gatti et
al. (1974)
Perry and
Evans (1975)
Yu (1976)
Galloway (1977)
Livingston and
Dethlefsen (1979)
Nakanishi and
Schneider (1979)
Morgan and
Crossen (1980)
Geard et al.
(1981)
Geard et al.
(1981)
Nagasawa and
Little (1981)
Popescu et al.
(1981)
4

-------
Table 1. (Continued)
Cell system
Radiation
source
Total
dose
Dose
rate
Reference
Chinese hamster
ceils (V79)
x ray
50-800 R
100 R/min
Renault et al.
(1982)
Chinese hamster
ovary cells
x ray
300 R
__b
Morgan et aJ.
(1983)
Human lymphocytes
y(60Co)
50-150 R
300 R/min
Solomon and
Bobrow (1975)
Human lymphocytes y(^Co)
25-200 R
125 R/min
Abramovsky
et al. (1978)
Human lymphocytes y(^Co)
150-300 R
50 R/min
Littlefield
et al. (1979)
a We estimated total doses and dose rates for 3(^H) radiation from autoradiographic film
grain-count data provided by the investigators. To calculate the 8-radiation dose to a cell
nucleus from	incorporated into DNA, we assumed that there was 1.08 rad/
disintegration (Goodheart, 1961) and that 14 disintegrations were required to produce one
grain count (Marin and Prescott, 1964).
b Dose rate not specified.
Pesch and Pesch (1980a) proposed that the marine polychaete Neanthes
arenaceodentata be used as an in vivo cytogenetic model for marine genetic toxicology.
jN. arenaceodentata is very suitable for cytogenetic studies because it has 18 large
chromosomes. This is in contrast to many invertebrates and fishes that have large
numbers of small chromosomes. The effects of ionizing radiation on this species were
60
assessed by quantifying the number of chromosomal aberrations induced by Co
radiation; at a dose rate of 7.5 R/h and a total dose of 180 R, an increase in chromosomal
aberrations was found (Pesch et al, 1981). Also, a preliminary study on N.
arenaceodentata was performed to determine the usefulness of SCE induction as a
measure of low-level radiation effects (Harrison and Rice, 1981). Larvae exposed to ^ฎCo
radiation at intermediate total doses of 10 to 60 R had SCE frequencies about two times
that of the control larvae, but those exposed to higher total doses of 170 to 309 R had
SCE frequencies that approximated those of the control larvae.
Our objective was to assess the feasibility of a cytogenetic approach to detect
alterations from radiation in the genetic material of a marine organism. We evaluated
the responses to irradiation by using the classical cytogenetic approach of quantifying the
frequency of chromosomal aberrations, and by using the more recently developed
technique of quantifying the frequency of SCEs. The responses of N. arenaceodentata to
5

-------
radiation delivered at high dose rates (x rays) and low dose rates (^Co) are evaluated as
well as those to a known mutagen, mitomycin C (MMC). Results from these experiments
will be used to determine what additional studies are required before cytogenetic changes
in nereidae worms can be used to detect radiation effects at radioactive waste disposal
sites. After establishing a dose-response relationship, we propose to validate assumptions
regarding doses expected to be received by organisms in the field from potential disposal
operations.
METHODS
WORM CULTURE AND HANDLING
Neanthes arenaceodentata were cultured following methods recommended by
Dr. Donald Reish of the California State University at Long Beach (Reish, 1974). Mated
pairs of adult worms were obtained from Dr. Reish and shipped through the U.S. mail in
inflated plastic bags containing approximately 100 mL of seawater. The worms were
shipped in the tubes they had constructed from the algae they were fed. Because shipping
time seldom exceeded 3 d, worm mortality was low; only a single death occurred during all
shipments.
On arrival at Lawrence Livermore National Laboratory (LLNL), each mated pair of
adult worms was placed in a 4-L glass beaker. The adult worms that produced larvae used
in experiments 1 through 6 were maintained using semistatic culture conditions; the water
was aerated continuously and three-fourths of the volume in the beakers was exchanged
weekly. Thereafter, adult worms were reared in 2-L beakers using flow-through
conditions; flow rate through the beaker was 100 mL/min. Adult worms were maintained
for 20 to 30 d in our laboratory before larvae were harvested. The mean culture
temperature was 19.4 ฑ 1.4ฐC. The adult worms were fed frozen Enteromorpha sp. ad
libitum and uneaten food was removed weekly.
The life cycle of this species is well known (Fig. 1) (Reish, 1957). Female worms die
after laying eggs and the embryos are brooded by the surviving male. Hatching occurs 8
to 10 d following egg deposition. We harvested larvae 1 to 3 d after they hatched (3 to 5
setiger stage) by removing the intact worm tube containing the adult male and larvae
from the beaker and gently aspirating the larvae from the walls of the tube with a
Jarge-bore plastic pipette. Harvested larvae were washed two times with seawater passed
through a 0.45-Mm- pore size Millipore filter.
6

-------

Figure 1. Life cycle Neanthes arenaceodentata (3 to mo at 20 to 22ฐC).
n

-------
The cleanliness of the glass and plastic ware was found to be an important factor in
the success of experiments. Some disposable plastic ware is sterilized with ethylene
oxide, which has been shown to increase SCEs in hospital workers (Garry et al., 1979).
Because some larvae appeared to be sensitized by laboratory ware that was not rinsed or
that contained residues of laboratory detergent, all containers used in the assay were
rinsed 20 times in hot tap water and then air dried.
IRRADIATION
Larvae were irradiated with x rays generated in a 40-keV x-ray machine and
delivered at 0.7 Gy (70 rad)/min for as long as 5.5 min and then examined for
chromosomal aberration induction. The doses ranged from 0.08 to 3.8 Gy (8 to 380 rad)
(Table 2). A 28-h BrdUrd exposure time was used to obtain the high proportion of
first-division cells required for chromosomal aberration scoring. The irradiation was
conducted in plastic 100- X 20-mm Petri dishes containing 10 mL of seawater (Fig. 2).
Three thermoluminescent dosimeters (TLDs) were placed in the water along with the
worms to determine the x-ray dose delivered.
Larvae were exposed to ^CO for 24 h and total doses delivered were different
(Table 3). Some larvae were examined for SCEs and chromosomal aberrations and others
just for SCEs. All irradiations were conducted in our low-level radiation facility equipped
with a 4.4 X 10^ Bq (1.25 Ci) 60Co source. A 54-h BrdUrd exposure was used to obtain
the high proportion of second-division cells required for scoring SCEs. For each exposure,
50 to 75 worm larvae harvested from 1 to 3 broods were placed in a cylindrical plastic
chamber (2.5-cm diam) containing 30 mL of filtered seawater. A Plexiglas sheet
(5 X 7 X 0.6 cm) was placed in front of each exposure chamber to ensure electron
equilibrium (Fig. 2). Different dose rates and total doses were obtained by varying the
distance between the chamber and the source. Delivered dose was determined from three
TLDs placed behind each exposure chamber.
Two groups of control worms were tested during each experiment. Neither group was
irradiated but one was treated with 5 X 10~^MMC, a drug known to increase the
frequency of SCEs, and served as a positive control. Both controls were maintained in the
exposure facility during the irradiation of the other groups of worms.
CYTOGENETIC PREPARATION AND SCORING OF WORM CHROMOSOMES
Immediately following irradiation for experiments 1 to 3, each treatment group of
worm larvae was transferred under amber light to 100- X 20-mm plastic culture dishes; a
large-bore plastic pipette was used to make the transfer. Each dish contained 30 mL of
8

-------
Table 2. The x-ray doses delivered to Neanthes arenaceodentata larvae.
X-ray dose (Gy)a
Experiment 0.08 0.24 0.37 0.48 1.0	1.7 2.2 2.6	3.8
1	X	X
2	X	X	X
3	X
4	XX
5	XX
6	X
7	X
8	X
9	X
10	X
11	X
12	X	X	X	X
a Dose rate was 0.7 Gy /min. One gray (Gy) is equivalent to 100 rads.
3	X 10"5M BrdUrd in filtered seawater. The same procedure was followed in experiments
4	to 30, except 50 mL of seawater in 100-mL glass beakers were used. Nonirradiated
control groups were also transferred to the same concentration of BrdUrd or to BrdUrd
plus 5 X 10~^M MMC. The BrdUrd and MMC exposures were carried out in the dark, and
colchicine (final concentration of 0.4 mg/mL) was added to the seawater 4 h before the
termination of the BrdUrd exposure. Colchicine is a microtubule disruptor that results in
the accumulation of cells in metaphase.
We generally followed the method of harvest of larvae and preparation of larval
tissue developed by Pesch and Pesch (1980b). Larvae were transferred to 15-mL conical
plastic tubes, the seawater decanted, and 10 mL of 0.075M potassium chloride added.
After 12 min, this solution was decanted and the larvae were fixed in three changes of
methanol plus acetic acid (3:1). The first fixative change was performed after 5 min, and
the remaining changes after 15 min each. Fixed larvae (50 to 75) were placed in a
depression of a ceramic spot dish and mashed twice with broad-tipped forceps. Next,
1 mL of 60% acetic acid was added, and the mixture was mashed continuously for an
9

-------
2.5 cm
1.25-Ci
60Co
24-h exposure
(4.8 X 10-5 to 1.2 X 10_1 Gy/h)
40-kev
X ray

$
Hh
6-mm
Plexiglass
toฐฐo
Ma o<=>
0
D
D
^Triplicate
thermoluminescent
dosimeters (TLDs)
~ 15-s
to
5-min
exposure
0.7 Gy/min
5 mm
-Triplicate TLDs
Figure 2. Exposing larvae to x rays and *>GCo irradiation.
additional minute. Two drops of the worm tissues suspended in acetic acid were deposited
on the end of a clean microscope slide held at 45ฐC. Using a disposable plastic pipette,
we made 10 to 15 successive transfers of the original drops of tissue suspension to clean
areas of the slide. This process resulted in the deposition of cells in a series of rings along
the length of the slide. The slides were dried at 45ฐC before staining. Generally, 4 slides
could be made from the macerated tissues of 50 to 75 worm larvae. The best spreading of
chromosomes was ensured by preparing the slides within 1 h of the start of fixation.
Differential staining of the sister chromatids was accomplished essentially according
to the procedure described by Minkler et al. (1978) (Fig. 3). Preparations were first
stained for 10 min in 5-Mg/mL Hoechst 33258 solution (Aldrich Chemical Company, Inc.,
Milwaukee, WI) in 0.9% sodium chloride (pH 6). Hoechst-stained slides were rinsed for
10

-------
Table 3. The 6ฎCo doses delivered to Neanthes arenaceodentata larvae.
60co dose (Gy)a
Experiment
0.001
0.01
0.1
0.3
0.6
1.7
3.0
13



X
X
X
X
14



X
X
X
X
15


X
X
X


16



X



17



X
X


18



X
X


19



X
X


20b




X


21b



X
X


22	X
23	X
24	X
25	X
26	X
27	X
a One gray (Gy) is equivalent to 100 rads.
b Scored for both chromosomal aberrations and sister chromatid exchanges.
5 min in distilled water and air dried for at least 20 min. They were next placed in a
shallow, clear plastic tray and covered with 0.067M^ phosphate buffer (pH 6.8) to a depth
of 5 mm. Slides were then exposed to UV light in an M-99 printer (400-W General Electric
mercury lamp from Colight, Inc., Minneapolis, MN) for 45 min. They then were
transferred to 10% Giemsa stain in 0.067iM phosphate buffer (pH 6.8) for 6 to 10 min, air
dried, and mounted with Permount (Fisher Scientific Company, Fairlawn, NJ). Worm
tissue fixation, slide preparation, and staining were all carried out under amber light.
Slides were scored by scanning the entire slide using a Zeiss Universal microscope
(Carl Zeiss, Inc., Oberkochen, West Germany) equipped with a 10X objective, 63X
objective, 1.25X optovar, and 12.5X oculars.
The proportions of metaphases identified as first, second, and third divisions after the
beginning of BrdUrd exposure were recorded. First- and second-division metaphases were
examined for the number of chromosomal aberrations and SCEs per metaphase,
11

-------
Figure 3. Metaphase chromosomes from irradiated iarvae of Neanthes arenaceodentata
stained to visuaiize sister chromatid exchanges.
respectively. The number of chromosomes scored was recorded for aJi metaphases
examined. Data for chromosomal aberrations were recorded only for cells that had 17 or
18 chromosomes that could be scored; data for SCEs were recorded for those that had 15
to 18 chromosomes that could be scored.
QUALITY ASSURANCE
All slides were scored blind, and four people performed the scoring. The results of
the comparative scoring of experiments are summarized in Appendix A. In addition to a
control population that received no irradiation, a positive control was run using larvae
that received no irradiation but were exposed to a concentration of 5 X 10 MMC for
54 h before they were harvested.
12

-------
RESULTS
CHROMOSOMAL ABERRATIONS
Almost all chromosomal aberrations induced by x rays in cells of _N. arenaceodentata
larvae were chromosome and chromatid deletions and gaps. An aberration was classified
as a deletion when the fragment was displaced and when all undisplaced fragments were
separated by a non-staining region equal to or greater than one chromatid width. If the
non-staining region was less than a chromatid width or did not extend across the
chromatid and was not displaced, it was scored as a gap. However, only data on
chromosome and chromatid deletions are included because the scoring of gaps is
subjective and not generally reported in the literature.
The frequency of chromosome and chromatid deletions in cells that received no
irradiation was low (Table 4). The mean chromosome and chromatid deletion per cell for
the 14 control (zero dose) experiments was 0.06, and the individual means from the
experiments ranged from 0.00 to 0.22. Differences in the frequencies of chromosome and
chromatid deletions reported by different scorers and for different slides were tested for
homogeneity of binomial proportions using Cochran's test (Snedecor and Cochran, 1967).
There was excellent agreement between scorers when the same slides were scored
independently; all differences were easily accounted for by binomial sampling variability.
There was also good agreement in frequencies reported for different slides within the
same experiment, with differences not exceeding those expected from binomial sampling.
In contrast to these results, there was significant heterogeneity among the chromosome
and chromatid deletion rates from different experiments (p = 0.0016 based on Cochran's
test for homogeneous binomial proportions, Snedecor and Cochran, 1967, p. 240).
The frequency of chromosome and chromatid deletions was determined also in cells
exposed to x rays (Table 5, Fig. 4). Weighted (by the number of cells scored) least-squares
linear regression was used to determine if there was a linear relationship between dose
and chromosome and chromatid deletion rate. The regression is highly significant
(F = 76.6 with 1 and 14 degrees of freedom, p < 0.01), and the estimated slope is 0.094
chromosome and chromatid deletion per ceil per gray of radiation (standard
error = 0.017). However, a prediction based on the least-squares best-fit line is not very
reliable because of the extreme heterogeneity of the responses at each dose level.
Nevertheless, it appears that doses above 2.0 Gy lead to increased frequencies of
chromosome and chromatid deletions.
In the experimental cells scored, the number of chromosome and chromatid deletions
per individual cell ranged from one to greater than four. The percentage of the total
chromosome and chromatid deletions that occurred singly (one per cell) and multiply
13

-------
Table 4. Mean frequency per cell of chromosome and chromatid deletions in cells from
Neanthes arenaceodentata larvae that received no radiation. Larvae were harvested
after a 28-h exposure to BrdUrd.
Experiment
Number of scorers3
Cells scored'3
Deletions
Deletion



scored*3
per cell
1
3
74
0
0.00
2
3
33
0
0.00
3
3
62
2
0.032
4
3
28
6
0.21
5
1
30
1
0.033
6
3
64
5
0.078
7
3
50
3
0.060
8
2
51
11
0.22
9
1
9
0
0.00
10
3
11
2
0.18
11
2
41
2
0.049
12
1
89
5
0.056
20
1
16
1
0.062
21
3
95
1
0.010
a Four scorers were available for the experiments.
b For slides scored by more than one person for an individual experiment, the number of
cells and chromosome and chromatid deletions scored were averaged.
(more than one per cell) was compared to the total dose delivered (Table 6). The fraction
of the total chromosome and chromatid deletions scored that occurred as more than one
chromosome and chromatid deletion per cell did not appear to be dose related.
Limited data are available on the frequencies of chromosome and chromatid deletions
induced in worm larvae exposed to low dose rates of ^Co (Table 7). All larvae were held
in BrdUrd for 28 h after exposure to the different total doses. Over the range tested, no
significant increases in chromosome and chromatid deletions were found.
14

-------
Table 5. Mean frequency per cell of chromosome and chromatid deletions in cells from
Neanthes arenaceodentata larvae exposed to x rays at 0.7 Gy (70 rad)/min. Larvae were
harvested after a 28-h exposure to BrdUrd that followed the irradiation.
Dose (Gy)
Experiment
Number of
scorers3
Cells scored*3
Deletions
scored*3
Deletion
per cell
0.08
2
1
41
2
0.049
0.18
5
1
30
2
0.067
0.19
4
1
54
2
0.037
0.22
10
1
29
3
0.10
0.24
2
1
40
8
0.20
0.37
5
1
109
4
0.037
0.45
4
2
22
1
0.045
0.47
2
2
28
2
0.071
0.48
1
2
112
12
0.11
0.88
6
2
66
5
0.076
0.88
12
2
95
7
0.074
1.0
1
2
57
10
0.18
1.6
8
3
12
2
0.17
1.7
12
3
52
7
0.13
2.0
7
3
21
12
0.57
2.2
8
3
61
16
0.26
2.5
3
3
48
36
0.75
2.6
12
2
51
11
0.22
3.6
11
3
34
12
0.35
3.8
12
2
56
14
0.25
a Four scorers were available for the experiments.
13 For slides scored by more than one person for an individual experiment, the number of
cells and chromosome and chromatid deletions scored were averaged.
SISTER CHROMATID EXCHANGES
The frequency of SCEs in cells from worm larvae exposed to BrdUrd for 54 h, but not
to radiation, was determined in 18 different experiments. The mean SCE frequency per
chromosome for the individual experiments ranged from 0.096 to 0.38 (Table 8). These
experiments were performed over 17 mo, and occasionally, larvae were harvested after
15

-------
0.8
8
ฃ
ง
I
w
ฆo
| 0.4
o
o
E
0
1	0.2
c
re
0)
2
X-ray dose (Gy)
Figure 4. Mean frequencies per cell of chromosome and chromatid deletions in cells from
Neanthes arenaceodentata larvae exposed to x rays at 0.7 Gy (70 rad)/min. Larvae were
harvested after a 28-h exposure to BrdUrd that followed the radiation. The regression
was highly significant (p< 0.01) and the estimated slope of the regression line is
0.094- chromosome and chromatid deletion per gray (standard error = 0.017).
varying BrdUrd exposure times (including 54 h). Before the SCE frequency data on control
cells were pooled to compile control baseline values for SCE frequencies, the effect of
cell-cycle time on SCE frequency was assessed. Using data from larvae harvested at
times ranging from 28 to 66 h, we determined that the cell-cycle time was about 28 h and
had little effect on SCE frequency (Appendix B).
An analysis of individual results (not shown) revealed that at zero dose, the
experiment-to-experiment variability was large compared with that between scorers and
slides. The standard deviation from scorer to scorer was 0.033, from slide to slide it was
0.037, and from experiment to experiment it was 0.056.
Cellular SCEs tended to follow a skewed distribution with medians consistently lower
than mean SCEs because of the presence of variable numbers of high-frequency cells
(HFCs) (Fig. 5). The HFC is defined by pooling all SCEs from the controls (1059 cells
from 18 experiments) and finding, in our case, the 90th percentile of this pooled
distribution. To have 95% confidence that the estimated percentile will, in fact, contain
16

-------
Table 6. Percentage of total chromosome and chromatid deletions occurring singly or
multiply in cells of Neanthes arenaceodentata larvae exposed to x rays at 0.7 Gy
(70 rad)/min. Larvae were harvested after a 28-h exposure to BrdUrd that followed the
irradiation.
Dose
(Gy)
Cells
scored
Number of
deletions

Occurance of deletions per cell (%)
1 del.
2 dels.
3 dels.
>_ 4 dels.
Control
643
39
63
21
16
0
0.08
41
2
100
0
0
0
0.18 to 0.24
153
15
60
40
0
0
0.37
109
4
100
0
0
0
0.45 to 0.48
164
15
60
13
0
27
0.88 to 1.0
228
22
60
24
0
16
1.6 to 1.7
62
9
57
0
0
43
2.0 to 2.2
82
28
63
15
22
0
2.5 to 2.6
99
47
42
20
38
0
3.6 to 3.8
90
26
56
25
0
19
90% of the ceils, we used the nonparametric procedure described by Walsh (1962) and
found the kth-largest SCE value from the pooled sample, where k is given by
k = 1059(1.0 - 0.90) + 0.5 - 1.645 / 1059(0.90)(0.10)
where 1059 is our sample size and 0.90 is the percentile expressed as a fraction. (The
1.645 comes from the 95th percentile of the standard normal distribution.) The
90th-largest SCE frequency in our sample is 0.44 SCE per chromosome. Thus, we define
an HFC as a cell with more than 0.44 SCE per chromosome.
There is clearly variability in the number of HFCs in our control samples.
Fortunately, the means of the SCEs are reasonably normally distributed with an overall
mean (weighted by number of cells scored) of 0.19 SCE per chromosome and a weighted
standard deviation of the means of 0.056. Normality of the means was tested using
Filliben's order statistic correlation test; a value of 0.988 was obtained, which is well
above the 5% critical value of 0.938 (Filliben, 1975).
Worm larvae exposed to different doses of ^Co and then examined for SCE induction
after a 54-h exposure to BrdUrd had mean frequencies of SCEs that varied with the total
17

-------
Table 7. Frequency of chromosome and chromatid deletions in cells from Neanthes
arenaceodentata larvae exposed to ^Co for 24 h. Larvae were harvested after a 28-h
exposure to BrdUrd that followed the irradiation.
Experiment
Dose (Gy)a
Cells scored
Deletion
per cell
19
0.6
12
0.072
20
0.6
2
0.045
21
0.6
5
0.072



0.054b
19
0.3
11
0.035
21
0.3
11
0.027



0.030b
19
Control
18
0.022
20
Control
1
0.054
21
Control
12
0.033



0.028b
a One gray (Gy) is equivalent to 100 rads.
b Mean weighted by the number of cells scored.
dose (Table 9). Analysis of results from individual experiments conducted at comparable
doses revealed again that there was significant variability from experiment to
experiment. This was caused mainly by significantly high proportions of HFCs in a few of
the experiments.
The frequency of SCEs in cells from larvae receiving 0.6 Gy of ^Co radiation is
clearly different from those not receiving radiation (Fig. 6). The frequency distribution is
similar to that of larvae exposed to MMC; both groups are characterized by having
increased incidences of HFCs.
A least-squares linear regression of mean SCE on radiation dose was performed
(Fig. 7). When weighted (by number of cells scored) linear regression is performed for all
doses, the slope of the best-fit line is not significantly different from zero. This is caused
by the low responses at the two highest doses. When these data pairs are omitted, a
significant (p = 0.025) slope results (0.241 + 0.008 increase in SCE per chromosome per
gray). Again, the best-fit line is not very useful for predicting responses because of the
large experiment-to-experiment variability. However, the significant regression indicates
that over this range of radiation there is a general rise in SCE frequency with increased
radiation dose. A significant increase in SCE frequency occurred at 0.6 but not at 0.3 Gy
18

-------
Table 8. Mean and median sister chromatid exchanges per chromosome (SCEs/C) in cells
from Neanthes arenaceodentata larvae that were not irradiated (control). Larvae were
harvested after a 5k-h exposure to BrdUrd.
Cells	Mean	Standard	Median Percent
Experiment scored	SCEs/C	deviation	SCEs/C HFCsa
13
2k
0.096
0.08
0.09k
0
Ik
18
0.20
0.22
O.Ik
16.7
15b
21
0.27
0.22
0.20
14.3
16
33
0.13
0.10
0.13
0
17
65
0.22
0.15
0.18
4.6
18
52
0.30
0.20
0.25
26.9
19
kO
0.18
0.19
0.13
7.5
20
9
0.19
0.15
0.18
11.1
21
12
0.13
0.09
0.11
0
22
32
0.17
0.14
0.12
3.1
23
52
0.12
0.10
0.089
0
2k
21
0.22
0.25
0.17
9.5
25
2k
0.26
0.2k
0.17
20.8
26
67
0.15
0.12
0.11
1.5
27
73
0.18
0.13
0.17
4.1
28
20
0.38
0.51
0.17
20
29
22
0.18
0.17
0.17
9.1
30
18
0.17
0.32
0.063
11.1
a Percentage of high-frequency cells (HFCs) (cells with more than O.kk SCE per
chromosome),
k Larvae harvested after a 48-h exposure to BrdUrd.
(Bonferroni t-test adjusted for seven multiple comparisons; p = 0.0003) (Miller, 1966). The
absence of a significant difference from control at 0.3 Gy may be a false negative. A
difference may have been detected if the sample were larger.
19

-------
0	0.2	0.4	0.6	0.8	1.0	1.2	1.4	1.6	1.8	2.0
SCE per chromosome
Figure 5. The SCE frequency distribution in Neanthes arenaceodentata larvae that were not irradiated (control). Larvae
were harvested after a 5^-h exposure to BrdUrcH

-------
Table 9. Mean and median sister chromatid exchanges per chromosome (SCEs/C) in cells
from Neanthes arenaceodentata larvae irradiated with 60Co. Larvae were harvested
after a 54-h exposure to BrdUrd that followed the irradiation.
Dose	Mean Standard Median Cells	Percent
(Gy)a	Experiment	SCEs/C deviation SCEs/C scored HFCs*5
0.001
0.001
0.001
0.001
22
23
24
25
0.22
0.17
0.16
0.17
0.22
0.13
0.15
0.14
0.17
0.13
0.11
0.12
81
42
29
10
12
2.4
6.3
0
0.01
26
0.17
0.14
0.17
152
5.3
0.1
0.1
15
27
0.42
0.17
0.34
0.19
0.44
0.12
25
140
32
5.7
0.3
0.3
0.3
0.3
0.3
0.3
0.3
0.3
13
14
15
16
17
18
19
21
0.55
0.16
0.34
0.12
0.23
0.30
0.17
0.20
0.49
0.18
0.31
0.11
0.23
0.27
0.22
0.22
0.47
0.11
0.19
0.11
0.12
0.26
0.13
0.12
24
15
25
49
19
12
32
22
50
13
32
2
10
25
3.1
14
0.6
0.6
0.6
0.6
0.6
0.6
0.6
0.6
13
14
15
17
18
19
20
21
0.41
0.20
0.47
0.37
0.32
0.15
0.46
0.25
0.54
0.28
0.39
0.22
0.36
0.09
0.60
0.22
0.13
0.06
0.33
0.39
0.22
0.12
0.24
0.20
25
22
32
11
17
23
15
6
24
18
41
36
24
0
33
17
21

-------
Table 9. (Continued)
Dose
(Gy)a
Experiment
Mean
SCEs/C
Standard
deviation
Median
SCEs/C
Cells
scored
Percent
HFCsb
1.7
13
0.24
0.21
0.16
10
10
1.7
14
0.15
0.12
0.13
13
0
3.0
13
0.24
0.40
0.17
23
4.3
3.0
14
0.18
0.27
0.17
31
6.5
a One gray (Gy) is equivalent to 100 rads.
b Percentage of high-frequency cells (HFCs) (cells with more than 0.44 SCE per
chromosome).
22

-------
30
20
10
1
o
o
15
K)
V*>
I	10
s
*-
0	5
1	0
2	30
20
10
-i	1	r
i	1	r
~	Mean	90% 95%
Li I
- - ij INI,ฆ!! |i'^	,	f*
-i	1 r
ฆ llllJil a nil. i.i ฆฆ ฆ . ฆ i . ... i..
IlL Ji
0.6-GyฎฐCo
in. I I ฆฆฆlli ซL I ฆ ฆ ฆ ฆ I ฆ	a
Mitomycin C
Control

~i	1	r
_ฆ	ฆ
0.2 0.4 0.6 0.8 1.0 12 1.4 1.6 1.8 2.0
SCE per chromosome
Figure 6. The SCE frequency distributions in Neanthes arenaceodentata larvae that received 0.6 Gy (60 rad) of 60co
radiation, were treated with 5 X 10"'mitomycin C, or received no irradiation. Larvae were harvested after a 5k-h
exposure to BrdUrd that followed the treatment.

-------
0.6
O
o
| 0.4
O
0
0
1
2
60Co dose (Gy)
3
4
Figure 7. The mean SCE per chromosome in cells from Neanthes arenaceodentata larvae
that had been irradiated with ^Co. Larvae were harvested after a 54-h exposure to
BrdUrd that followed the radiation. The solid line shows the regression of all mean SCE
per chromosome on dose and the slope is not significantly different from zero. The dotted
line shows the regression of mean SCE per chromosome on dose for doses < I Gy and the
slope is significant (P = 0.025) and is 0.241 + 0.008 increase in SCE per chromosome per
gray.
CHROMOSOMAL ABERRATIONS
The induction of chromosomal aberrations by irradiation has been demonstrated both
in vivo and in vitro in many mammals and in mammalian cell systems (Gebhart, 1981).
Although the response to radiation was dose related in mammalian systems, the rate of
induction differed with the test system and the cell-cycle at the time of irradiation. In
the worm larvae, we found that the response was dose related also. The chromosomal
aberrations that we quantified, chromosome and chromatid deletions, are one-break
aberrations that are considered to be induced linearly with dose. However, our studies on
the background levels of chromosomal aberration induction indicate that in worm larvae,
as in mammalian systems, the incidence of chromosomal aberrations is low. Neither the
incidence of true point (intragenic) mutations, which are base-pair changes or frame shifts
DISCUSSION
24

-------
in DNA, nor gross chromosomal (polygenic) mutations, which are brought about by the
breakage of chromosomes, is easily quantified at low radiation doses. This is because very
few of these incidents are found and it is difficult to get a significant increase over
background values unless large numbers of cells are scored.
SISTER CHROMATID EXCHANGES
The induction of SCEs is a sensitive indicator of changes due to mutagenic
chemicals. However, the data available on mammalian cells indicate that the response is
more sensitive to chemicals than to ionizing radiation. Our results for worm larvae show
that a response that was significantly different from controls was obtained at lower doses,
using the SCE frequency, than by using the chromosomal aberration frequency as an
endpoint. However, the SCE response to doses M*7 Gy (170 rad) was not related to dose;
the frequency of SCEs appeared to plateau or decline.
A plateau in the SCE induction rate in mammals was found for beta-radiation doses
(Gibson and Prescott, 1972). More recently, however, Nagasawa and Little (1981)
reported a dose-related response in SCE frequencies in the density-inhibited plateau phase
of cultures of mouse 10T-1/2 cells irradiated with x rays, but commented that the
relationship of the induction of SCE to total dose was more complex and very different
from that for the production of chromosomal aberrations. They reported that the
dose-response curve for SCEs increased linearly up to 100 rad (1 Gy), then declined with
increasing doses. At the doses on the exponential portion of the survival curve (> 200 rad,
or 2 Gy), the frequency of induced SCEs declined rapidly. For 400 rad (4 Gy), the SCE
frequency was only 20 to 30% higher than the baseline (spontaneous frequency) compared
to the twofold increase induced by 100 rad (1 Gy).
Furthermore, the induction of SCE was also related to the repair interval; there was a
rise in SCE with repair intervals up to 4 h, followed by a decline at later times. They
noted also that the mean frequencies of SCEs and their distribution among cells showed
little change during repair periods in the sublethal dose range (50 to 100 rad, or 0.5 to
1 Gy), but did change during the repair period at the higher doses to greater numbers of
cells with high frequencies of SCEs. These investigators propose that these phenomena
occur as a result of the kinetics of repair and of cell survival.
The existence of a plateau or a decline at high doses in SCE induction may limit the
range of doses over which SCEs in NJ. arenaceodentata could be used as an indicator of in
vivo environmental exposure to radiation. However, this would not be expected to be a
problem at the doses expected at low-level waste disposal sites.
25

-------
Factors that may affect SCE incidence in benthic worms include the following:
•	cell-cycle stage at the time of irradiation,
•	length of time induced SCEs are retained in cells, and
•	life-history stage at the time of irradiation.
Some of these were shown to be important in mammalian cell culture systems and may
also be important in our in vivo worm bioassay.
From data on synchronously dividing cultures of mammalian cells, it is known that
the induction of SCEs and chromosomal aberrations by x rays is dependent on the
cell-cycle stage during irradiation. For SCE induction, S is the most sensitive cell-cycle
stage (Yu, 1976; Morgan and Crossen, 1980). For chromosomal aberration induction, is
the most sensitive stage (Carrano, 1975; Yu, 1976). Because N. arenaceodentata larvae
represent a nonsynchronously dividing complex population of cells and our irradiations
were during several cell-cycle stages, the role that changes in radiosensitivity during
cell-cycle or for differentially responsive subpopulations of cells might play in our
observed SCE frequencies is unclear.
Another factor to be considered is the length of time that induced SCEs are retained
in the cells. In vivo irradiated mice that received BrdUrd 26 h after irradiation still
showed an increased SCE incidence (Nakanishi and Schneider, 1979). Experiments to
examine changes in SCE incidence with time following the irradiation of worms would
provide data relevant to possible influences conservation of SCEs might have on SCE
incidence.
A final factor is the effect of life-history stage on observed SCE frequencies. Worm
larvae contain populations of rapidly dividing cells, whereas adult worms may contain
primarily slowly dividing cells. Nondividing human lymphocytes exposed to x rays showed
no increase in SCE incidence (Galloway, 1977; Littlefield et al., 1979; Morgan and Crossen,
1980), while similar populations of cells induced to divide and then irradiated showed
significant increases in SCE frequencies (Galloway, 1977; Morgan and Crossen, 1980). If
measurements of SCE frequency in chronically exposed animals are conducted on adult
rather than larvae worms, then dose response for adults must be established.
FEASIBILITY OF CYTOGENETIC METHODOLOGY
The feasibility of using cytogenetic endpoints to measure low-level radiation effects
required (1) identification of an appropriate cytogenetic model and (2) obtaining a
response with the model organism that is related to the dose delivered. Our results
indicate that N. arenaceodentata is a good cytogenetics model. Both chromosome and
26

-------
chromatid deletions and SCEs are induced by ionizing radiation delivered in vivo to jN.
arenaceodentata. The induction of chromosome and chromatid deletions by x rays
delivered at 0.7 Gy (70 rad)/min was dose related, but doses >2 Gy (200 rad) were required
to get a response that was significantly different from background levels. The induction
of SCEs by ^Co delivered at total doses of <,0.6 Gy (60 rad) appeared to be dose related,
but at higher doses it was not; only the frequency of SCEs induced by 0.6 Gy (60 rad) was
significantly different from that of controls.
If variability in cytogenetic response is so high that a large amount of data is
required to establish a difference between control animals and those at a radioactive
dump site, this method will not be cost effective. Therefore, we made a concerted effort
to identify variability sources in the bioassay as well as to understand the process of
induction of chromosomal aberrations and SCEs. We investigated factors that could
potentially alter their frequency and concentrated our efforts on SCE induction, because a
response that was significantly different from controls was obtained at a lower dose for
SCEs than for chromosomal aberrations.
Some of the factors we investigated were:
•	baseline SCE frequency per chromosome,
•	cell-cycle time in larvae,
•	effect of cell-cycle time on SCE induction,
•	among and between experiment variability, and
•	between scorer variability.
The results on SCE were analyzed using standard statistical procedures as well as methods
developed by LLNL personnel for application to SCE distribution.
Our data show that there is great variability in the baseline SCE frequency in worm
larvae; the greatest variability was between experiments. Variability was reported also in
mammalian systems (Carrano and Moore, 1982). Some of the variability in an unexposed
reference population can be attributed to differences in incorporation of BrdUrd used to
visualize the SCEs, to differences in the cell's repair capacities, and to other unknown
inherent differences (Carrano et al., 1980). Increased sensitivity of our bioassay could be
obtained by reducing the high variability in background SCE frequencies.
At the Windscale radioactive waste disposal site in the Irish Sea, the maximum
possible dose rate is estimated to be about k5 mrem/h (^4.5 X 10"^ Gy/h) (Woodhead,
1980). The lowest dose rate used in our study that gave a response statistically greater
-2	60
than that of the control was the induction of SCEs by 2.5 X 10 Gy (2.5 rad)/h of Co
for a total dose of 0.6 Gy (60 rad). Although a small increase in mean SCE frequency was
observed at a dose rate of 5 X 10"^ Gy (0.05 rad)/h of 60Co and a total dose of 0.01 Gy
27

-------
(1.2 rad), no significant increase in the number of HFCs was found. The time over which
the doses were delivered in our system was 24 h; in natural systems it may be over the life
span of the organism. Greater sensitivity of our bioassay could be obtained by increasing
the duration of the exposure to the low dose rates.
A reliable method for determining the exposure of irradiated people to ionizing
radiation has been developed using peripheral lymphocytes. Because these cells are
long-lived and nondividing, aberrations can persist rather than be converted to lethal
events as a result of genetic imbalance in cell division. These ceils have been shown to
act as an integrating dosimeter for ionizing radiation.
The feasibility of using chromosomal aberrations in environmental monitoring appears
to be related to the availability of an integrating dosimeter. We have identified several
systems in worms comparable to that of the lymphocytes in mammals. One of these
would be to utilize the changes that occur during regeneration. In adult organisms, the
rate of division of somatic cells is generally low. However, it is well documented that at
the site of regeneration there is increased rate of division. We propose that adult worms
be exposed to radiation, regeneration be induced by excising part of the worm, and then
the cells of the blastema be examined for increased incidence of chromosomal aberrations
in somatic cells that have been stimulated to divide. This system would be amenable to
field studies because regeneration could be induced in animals recovered from nuclear
waste-disposal sites.
Another possibility would be to utilize the changes that occur during oogenesis. In
nereidae worms, primary oocytes undergo maturation in the coelom, the mature gametes
are released into seawater upon rupture of the body wall, and then are fertilized. The
maturing oocytes may serve as an integrating system. The frequency of chromosomal
aberrations could be examined either during meiosis or the first mitotic division after
fertilization. This system would be amenable to field studies only in those situations
where sexually mature adults were available from the field.
A third possibility would be to utilize blood cells of worms in tests similar to those
that have been developed for human lymphocytes. This system could be used in the study
of those sites that have worms of sufficient size for blood sampling.
The use of SCE frequency in tissues as an integrating dosimeter for chronic exposure
of mammalian cells has not yet been established. For those chemical mutagens that are
S-dependent, DNA repair can potentially remove adducts before the cells enter S phase,
and result in increased variability of response. S-dependency means that the substance
must be present during replicative DNA synthesis, or the lesions it produces in the
chromatin require DNA synthesis to be translated into a structural change. Because the
28

-------
induction of SCEs by radiation is also S-dependent, such increased variability can be
expected also. We still, however, suggest considering the use of SCE induction in cells as
a dosimeter while searching for an integrating system for chromosomal aberrations.
MECHANISMS OF CHROMOSOMAL ABERRATION AND SISTER
CHROMATID EXCHANGE FORMATION
Much effort has been directed toward understanding the mechanisms of chromosomal
aberration and SCE formation and their relationships in genetic material (Gebhart, 1981;
Carrano and Moore, 1982). It has been shown that chemicals attach to DNA and produce
a variety of lesions that can vary from chemical to chemical (Wolff, 1982). With several
chemicals, both SCEs and aberrations increase linearly with the dose. Thus, for a given
chemical, the ratio of SCEs to aberrations is constant over a large dose range (Carrano et
al., 1978; 1980). Because this ratio changes for each chemical, it may indicate that of the
multitude of lesions produced for a given chemical, some could lead to SCEs and others to
aberrations, or that the lesions that lead to the induction of aberrations are a subset of
those that produce SCEs (Carrano and Thompson, 1982). Wolff (1982) states that in any
case, the induction of SCEs shows that DNA is being affected and that SCEs are an
indicator of damage.
According to Wolff (1982),
Most geneticists agree that induced mutations are detrimental and,
therefore, that any general increase in the mutation rate will also be
detrimental. The reasons for this are both empirical and theoretical.
For instance, radiation-induced mutations in plants, fruit flies, or any
other system that is favorable for genetic analysis usually lead to
reduced fitness, i.e., are lethal or semilethal. This makes theoretical
sense because all living organisms are the result of eons of evolution
and have been selected to fit their particular ecological niche;
mutations, which are random changes in the genetic constitution of the
organisms, can upset the balance brought about by natural selection.
There is, however, a problem in determining exactly how detrimental
the effects of mutations will be and how much damage really will be
done, especially after low doses.
Because of the uncertainties in our ability to predict the consequences of changes in
chromosomes induced by low levels of irradiation, the presence of the changes should be
used currently only to signal potential problems in a population. As more data on
radiation effects at low dose levels become available, we may be able to relate changes in
chromosomes to those in populations and, in turn, to those in communities.
29

-------
CONCLUSIONS
Nereidae worms, because of their karyotype and life style, are a good cytogenetic
model for studying radiation effects on benthic organisms. We used _N. arenaceodentata
larvae to characterize the rates of induction of chromosome and chromatid deletions and
SCEs from exposure to ionizing radiation.
The induction of chromosome and chromatid deletions by x rays delivered at 0.7 Gy
(70 rad)/min was dose related, but doses >2 Gy (200 rad) were required to obtain a
response that was significantly different from background. At present we have data from
organisms that were exposed for a maximum period of only 24 h. Because under field
conditions organisms would be exposed to radiation over their entire lifetime, further
studies are required to characterize the effects of chronic exposure. Also, before this
bioassay can be applied to conditions that exist at low-level, radioactive-waste disposal
sites, increased sensitivity is required. We suggest that increased sensitivity of the
response in the worm be achieved by identifying a long-lived cell system, similar to that
of the lymphocytes in mammals, that can be used as a integrating dosimeter for
chromosomal aberrations.
The induction of SCEs by *^Co delivered at total doses of 0.001 to 0.6 Gy (0.1 to
60 rad) appeared to be dose related, but at higher doses it was not. A response that was
significantly different from controls was obtained at 0.6 Gy (60 rad). This dose is
considerably lower than that needed to obtain a significant difference for chromosome
and chromatid deletion frequencies, but higher than that required to monitor most
radioactive-waste disposal sites. Also, the dose over which SCE induction may be used as
an indicator of environmental exposure is limited because of the decline in the dose
response at higher doses. Consequently, this bioassay could be applied only to field
situations where no doses higher than 0.6 Gy (60 rad) are expected, unless factors
producing the decline at high doses are identified. Further, we suggest that the required
increased sensitivity of this response be obtained by either decreasing the variability in
the response at low dose levels or by identifying a cell system that can be used as an
integrating dosimeter for SCEs.
30

-------
APPENDIX A.
QUALITY ASSURANCE
Most of the slides that were scored for chromosomal aberrations (specifically,
chromosome and chromatid deletions) and SCEs were examined by more than one person.
The results of the multiple scoring of chromosome and chromatid deletions are presented
in Table A1 and those of SCEs in Table A2.
31

-------
Table Al. Chromosomal and chromatid deletions (Del) detected by different individuals
scoring the same slide.
Experiment		Scorer 1	 	Scorer 2	Scorer 3


Cells

Del/
Cells

Del/
Cells

Del/

Slide
scored
Del
cell
scored
Del
cell
scored
Del
cell





Control larvae




1
a
28
1
0.036
24
0
0
24
0
0

b
21
0
0
21
0
0
21
0
0

c
28
0
0
—
—
—
—
—
—
2
a
14
0
0
15
0
0
15
0
0

b
9
0
0
14
0
0
14
0
0

c
6
0
0
—
—
—
—
—
—
3
a
40
1
0.025
43
3
0.070
43
2
0.047

b
20
0
0
—
—
ซ
—
—
—
4
a
13
2
0.15
14
2
0.14
14
2
0.14

b
3
0
0
3
0
0
3
0
0

c
12
6
0.50
10
3
0.30
—
—
—
5
a
11
0
0
12
0
0
11
0
0

b
7
1
0.14
—
—
—
—
—
—

c
12
0
0
—
—
—
—
—
—
6
a
19
1
0.053
25
1
0.040
25
1
0.040

b
25
1
0.040
30
1
0.033
16
0
0

c
17
3
0.12
—
—
—
—
—
—
7
a
17
2
0.12
19
2
0.10
10
1
0.056

b
22
1
0.045
24
1
0.042
23
1
0.043

c
12
0
0
--
—
—
—
—
—
S
a
32
5
0.16
38
7
0.18
37
6
0.16

b
15
5
0.33
15
5
0.33
—
	
—

-------
Table Al. (Continued)
Experiment		Scorer 1	 	Scorer 2	Scorer 3	
Cells	Del/ Cells	Del/ Cells	Del/
Slide scored Del cell scored Del cell scored Del cell
9
a
5
0
0
—
—
ซ
—
—
—

b
3
0
0
—
—
ซ
—
--
—

c
1
0
0
—
—
ซ
—
—
—
10
a
12
1
0.0S3
12
2
0.17
10
2
0.20
11
a
19
1
0.053
30
2
0.067
—
—


b
17
0
0
—
—
—
—
—
—
12
a
34
3
0.088
34
3
0.088
—
—


b
24
1
0.042
—
—
—
—
—
—

c
31
1
0.032
—
—
—
—
—
—
20
a
6
0
0
—
—
—
—
—
—

b
10
1
0
—
~
—
—
~
—
21
a
46
1
0
49
1
0.20
27
1
0.21

b
27
0
0
27
0
0
21
0
0

c
21
1
0.022
21
0
0
47
0
0
	Larvae irradiated with x rays
3.6 to 3.8 Gya
11
a
10
1
0.10
15
2
0.13
15
2
0.13

b
7
4
0.57
7
4
0.57
7
4
0.57

c
13
4 .
0.31
15
7
0.47
—
—
—
12
a
15
4
0.27
22
4
0.23
—
—
—

b
20
3
0.15
32
11
0.34
—
—
~

c
12
3
0.25


—
	
—
—
33

-------
Table Al. (Continued)
Experiment		Scorer 1	 	Scorer 2	Scorer 3	
Cells	Del/ Cells	Del/ Cells	Del/
Slide scored Del cell scored Del cell scored Del cell
2.5 to 2.6 Gy
3
a
27
30
1.11
28
25
0.89
28
19
0.68

b
7
2
0.29
7
4
0.57
7
3 •
0.43

c
12
5
0.42
14
11
0.71
13
8
0.62
12
a
22
3
0.14
20
4
0.20
—

b
16
3
0.19
16
4
0.25
—

c
18
4
0.22
10
2
0.20
—
2.0 to 2.2 Gy
7
a
10
5
0.50
1
0
0
7
2
0.29

b
3
1
0.33
6
6
1
8
3
0.38

c
15
7
0.47
3
5
r.67
9
9
1
8
a
13
0
0
4
4
1
6
0
0

b
4
1
0.25
1
0
0
5
1
0.20

c
22
1
0.045
14
0
0
17
2
0.12
d
10
0
0
5
0
0
4
1
0.25
e
15
5
0.33
15
7
0.47
14
4
0.29
f
13
6
0.46
8
13
1.62
11
5
0.46
1.6 to 1.7 Gy
8
a
2
0
0
6
1
0.17
4
1
0.25

b
3
0
0
1
0
0
0
0
0

c
7
1
0.14
7
1
0.14
7
1
0.14
12
a
18
7
0.39
18
7
0.39
16
5
0.31

b
16
0
0
22
0
0
23
0
0

c
19
1
0.053
14
1
0.071
12
0
0
34

-------
Table Al. (Continued)
Experiment


Scorer 1


Scorer 2


Scorer 3



Cells

Del/
Cells

Del/
Cells

Del/
Slide
scored
Del
cell
scored
Del
cell
scored
Del
cell
0.88 to 1.0 Gy










1
a
12
2
0.17
12
3
0.25
12
3
0.25

b
28
4
0.14
27
4
0.15
—
—
—

c
19
3
0.16
15
3
0.20
—
—
—
6
a
25
3
0.12
24
1
0.042




b
16
0
0
15
2
0.13
15
2
0.13

c
24
1
0.042
30
3
0.10
—
—
—
12
a
26
1
0.038
28
1
0.036
28
1
0.036

b
30
1
0.033
49
6
0.14
—
~
—

c
29
3
0.10
28
2
0.071
ซ
—
—
0.45 to 0.48 Gy










1
a
31
3
0.097
31
7
0.21
30
5
0.17

b
30
5
0.17
28
4
0.14
--
--
—

c
47
2
0.043
56
4
0.07
—
—
—
2
a
4
0
0
4
0
0
4
0
0

b
10
0
0
10
0
0
~
—
—

c
15
2
0.13
14
1
0.071
—
—
—
4
a
8
0
0



	
	
__

b
15
1
0.067
14
1
0.071
—
—
—
0.37 Gy










5
a
37
1
0.027
—
—

—
—
—

b
44
3
0.068
—
--
—
--
—
35

-------
Table Al. (Continued)
Experiment		Scorer 1	 	Scorer 2	Scorer 3	
Cells	Del/ Cells	Del/ Cells	Del/
Slide scored Del ceil scored Del cell scored Del cell
0.18 to 0.24 Gy





2
a
17
4
0.24
— — — — — 	

b
12
2
0.17
-

c
11
2
0.18
-
4
a
17
2
0.12
_ 	 — — 	 __

b
16
0
0
-

c
21
0
0
_
5
a
7
1
0.14
— — — 	 — —

b
23
1
0.043
-
10
a
4
0
0


b
14
0
0


c
11
3
0.27
—
0.08 Gy





2
a
19
2
0.105
— — __ — —

b
14
0
0
-

c
8
0
0
— — — —
a One gray (Gy) is equivalent to 100 rads.
36

-------
Table A2. Mean SCE frequencies determined by different individuals scoring the same slide.
Experiment		Scorer 1		Scorer 2	 	Scorer 3	
Cells Mean	Cells Mean	Cells Mean
Slide scored SCEs SDa scored SCEs SD scored SCEs SD
Control larvae
13 a 16	0.10 0.083 15
b 8	0.083 0.084 10
0.15 0.10 —
0.14 0.10 --
14 a 6	0.18 0.14 6
b 5	0.14 0.089 --
c 7	0.23 0.21 --
0.20 0.31 —
15 a 7	0.38 0.30 --
b 11	0.22 0.14 14
0.22 0.14 14
0.22 0.14
16
17
0.13 0.077 20
0.11 0.089 20
0.12 0.085
13
0.16 0.12
17
a
b
c
d
19
16
15
24
0.28
0.36
0.23
0.17
0.24	13
0.33	13
0.14	-
0.077	-
0.30 0.25 13
0.22 0.12 12
0.32
0.24
0.24
0.13
18
a
b
c
d
e
8
7
16
14
8
0.34
0.32
0.30
0.24
0.32
0.35
0.24
0.22
0.15
0.20
0.32 0.26 7
0.32 0.26
19
a
b
19
28
0.-16
0.13
0.12 —
0.12 21
0.20 0.24
20
a
b
1
9
0.059
0.20
1
0.16 8
0.11 — 1
0.20 0.16 8
0.11
0.20
0.16
37

-------
Table A2. (Continued)
Experiment		Scorer 1	 	Scorer 2	 	Scorer 3	
Ceils Mean	Cells Mean	Cells Mean
Slide scored SCEs SDa scored SCEs SD scored SCEs SD
21
a
12
0.11
0.097
7
0.13
0.09
—
—

b
6
0.12
0.072
5
0.12
0.10
5
0.14
22
a
17
0.19
0.16
—
—
__
—
—

b
4
0.06
0.051
—
—
—
--
—

c
11
0.17
0.12
~
—
--
--
—
23
a
9
0.11
0.12
	
—
—
	
	

b
18
0.10
0.12
--
—
—
—
—

c
13
0.17
0.09
—
~
—
~
~

d
12
0.08
0.074
—
—
~
--
—
24
a
3
0.14
0.08
—
—
—
—
—

b
10
0.20
0.18
—
—
—
--
—

c
8
0.28
0.36
—
—
—
—
—
25
a
6
0.28
0.24
—
	
—
—
	

b
14
0.25
0.24
--
—
—
—
--

c
4
0.25
0.28
--
—
—
~
—
26
a
22
0.14
0.093
—
--
—
—
—

b
24
0.18
0.14
—
—
—
~
—

c
13
0.09
0.092
—
—
—
—
—

d
8
0.16
0.10

—
—
—
—
27
a
42
0.18
0.11
32
0.17
0.10
--
—

b
13
0.18
0.12
13
0.18
o.ll
13
0.18

c
10
0.20
0.13
11
0.25
0.20
—
—

d
9
0.15
0.070
14
0.177
0.088
~
—

e
3
0.11
0.10
3
0.15
0.11
—
—
28
a
15
0.46
0.57
—

	
—
—

b
5
0.12
0.094
—

—
—
~
0.099
0.14
38

-------
Table A2. (Continued)
Experiment		Scorer 1	 	Scorer 2	 	Scorer 3

Slide
Cells
scored
Mean
SCEs
SDa
Cells
scored
Mean
SCEs
SD
Cells
scored
Mean
SCEs
SD
29
a
b
15
7
0.18
0.20
0.20
0.12
—
—
—
ซ
—
—
30
a
b
11
7
0.077
0.31
0.059
0.49
—
—
—
—
—
—



Larvae irradiated with ^
Co




n c
Gy










13
a
23
0.235
0.401
—
~
—
—
—
—
14
a
b
21
10
0.183
0.195
0.148
0.227
—
--
—
—
—
—
Gy










13
a
5
0.26
0.12
4
0.28
0.16
4
0.28
0.14

b
12
0.65
0.79
6
0.16
0.16
6
0.22
0.26
14
a
14
0.17
0.18
6
0.12
0.12
6
0.12
0.12

b
12
0.12
0.10
7
0.17
0.12
8
0.21
0.20
Gy










13
a
19
0.43
0.45
12
0.24
0.34
20
0.39
0.46

b
10
0.48
0.82
13
0.26
0.33
5
0.62
1.21
14
a
4
0.20
0.029
4
0.078
0.097
3
0.037
0.064

b
10
0.36
0.38
6
0.068
0.058
8
0.32
0.38

c
13
0.22
0.28
11
0.14
0.24
10
0.15
0.22
15
a
16
0.50
0.34
13
0.40
0.27
12
0.40
0.28

b
17
0.62
0.60
20
0.52
0.44
18
0.48
0.40
39

-------
Table A2. (Continued)
Experiment		Scorer 1	 	Scorer 2	 	Scorer 3	
Cells Mean	Cells Mean	Cells Mean
Slide scored SCEs SDa scored SCEs SD scored SCEs SD
17	a
b
18	a
b
19	a
b
20	a
b
21	a
b
0.3 Gy
13	a
b
14	a
b
15	a
16	a
b
17	a
b
18	a
b
4	0.46	0.089
10	0.30	0.27
12	0.32	0.22
9	0.22	0.32
13	0.12	0.078
13	0.14	0.099
7	0.67	0.52
7	0.37	0.64
3	0.17	0.14
2	0.46	0.34
11	0.97	1.59
15	0.53	0.41
11	0.22	0.14
11	0.26	0.29
23	0.45	0.38
13	0.14	0.13
26	0.14	0.13
10	0.19	0.15
11	0.46	0.41
5	0.23	0.10
5	0.54	0.34
5	0.40	0.13
7	0.34	0.27
12	0.28	0.20
6	0.36	0.56
11	0.16	0.076
12	0.15	0.10
8	0.54	0.52
7	0.35	0.70
4	0.13	0.10
3	0.41	0.29
9	0.84	0.32
15	0.51	0.13
11	0.16	0.16
6	0.10	0.22
25	0.34	0.31
24	0.074	0.067
25	0.14	0.10
11	0.16	0.12
9	0.30	0.24
5	0.22	0.094
6	0.26	0.22
4	0.42	0.070
7	0.40	0.28
9	0.29	0.18
8	0.35	0.50
11	0.16	0.092
6	0.44	0.27
7	0.38	0.68
4	0.13	0.10
2	0.47	0.25
19	0.55	0.94
6	0.48	0.32
10	0.16	0.16
5	0.13	0.24
22	0.34	0.32
24	0.081	0.014
25	0.16	0.13
8	0.15	0.12
8	0.32	0.30
4	0.18	0.099
7	0.36	0.34
40

-------
Table A2. (Continued)
Experiment		Scorer 1	 	Scorer 2	 	Scorer 3	
Cells Mean	Cells Mean	Cells Mean
Slide scored SCEs SDa scored SCEs SD scored SCEs SD
19
a
15
0.23
0.30
23
0.J 3
0.096
22
0.18
0.25

b
12
0.16
0.20
10
0.12
0.10
8
0.10
0.099
21
a
12
0.20
0.17
14
0.19
0.24
12
0.16
0.25

b
10
0.22
0.16
8
0.23
0.18
8
0.24
0.20
Gy










15
a
25
0.42
0.34
—
--
—
--
~
—
27
a
29
0.30
0.30
28
0.16
0.18
22
0.17
0.18

b
18
0.281
0.22
18
0.24
0.22
18
0.24
0.23

c
10
0.30
0.48
14
0.22
0.45
12
0.22
0.42

d
10
0.12
0.10
13
0.14
0.092
11
0.10
0.08

e
6
0.30
0.33
14
0.22
0.20
14
0.22
0.21

f
18
0.13
0.10
22
0.12
0.10
20
0.12
0.11

g
16
0.093
0.073
22
0.12
0.083
—
—
~

h
2
0.056
0.000
11
0.15
0.075
10
0.15
0.094

i
6
0.17
0.17
12
0.19
0.14
11
0.18
0.15
1 Gy










26
a
26
0.19
0.14
—
--
—
—
—
—

b
27
0.2 0
0.15
—
—
--
--
—
—

c
13
0.21
0.20
—
—
—
—
—
—

d
11
0.18
0.14
—
—
—
—
—
__

e
14
0.17
0.13
--
—
~

—
—

f
21
0.18
0.13
—
—
—
—
—
—

g
14
0.11
0.097
~
--
—
—
—
—

h
14
0.16
0.10
ซ
—
—
—
—


i
12
0.10
0.10
	
—
	
—
	
__
41

-------
Table A2. (Continued)
Experiment		Scorer 1			Scorer 2	 	Scorer 3	
Ceils Mean	Cells Mean	Cells Mean
Slide scored SCEs SDa	scored SCEs SD	scored SCEs SD
0.001 Gy
22
a
9
0.16
0.09

b
17
0.16
0.23

c
12
0.37
0.27

d
14
0.19
0.22

e
17
0.22
0.22

f
12
0.21
0.14
23
a
17
0.21
0.17

b
10
0.14
0.087

c
13
0.14
0.079

d
2
0.17
0.16
24
a
11
0.083
0.040

b
8
0.22
0.19

c
10
0.18
0.17
25
a
4
0.15
0.15

b
4
0.18
0.18

c
2
0.20
0.12



Larvae
treated
13
a
14
0.51
0.56
14
a
11
0.25
0.23

b
6
0.45
0.36

c
7
0.37
0.32
15
a
20
0.78
0.46
0.38 0.55
16 0.62 0.41
42

-------
Table A2. (Continued)
Experiment		Scorer 1	 	Scorer 2	 	Scorer 3	
Cells Mean	Cells Mean	Cells Mean
Slide scored SCEs SDa scored SCEs SD scored SCEs SD
17
a
16
0.31
0.23
14
0.29
0.12
—

b
13
0.48
0.38
--
—
—
—
18
a
10
0.44
0.40
9
0.42
0.36
	 __

b
5
0.16
0.063
—
—
—
~
19
a
11
0.30
0.18
12
0.25
0.077
	 __

b
10
0.21
0.11
—
--
—
—
20
a
1
0.067
ซ...
1
0.000
— 	
	 	

b
4
0.17
0.13
—
—
—
—
21
a
8
0.36
0.17
8
0.35
0.21
	 	

b
7
0.19
0.17
~
—
~
~
22
a
4
0.38
0.30
	
__
—m.
	 __

b
14
0.19
0.16
—
ซ
__
"

c
7
0.29
0.24
—
—
—
—
23
a
3
0.15
0.12
ป
—
	 __
	 	

b
14
0.34
0.19

--
~
—
24
a
10
0.14
0.097
—
—
— 	
— __

b
10
0.27
0.29
~
—
—
—

c
3
0.075
0.031
—
~
~
—
25
a
8
0.29
0.19
—
__
__ --
—

b
2
0.063
0.006
—
—
—
—

c
6
0.087
0;08I

__
—

43

-------
Table A2. (Continued)
Experiment
Slide

Scorer 1

Scorer 2

Scorer 3
Cells
scored
Mean
SCEs
SDa
Cells Mean
scored SCEs
SD
Cells Mean
scored SCEs SD
26
a
25
0.32
0.28
_



b
17
0.21
0.18
—
--
—

c
21
0.18
0.13
—
~
—

d
8
0.23
0.10
11 0.28
0.14
—
27
a
9
0.33
0.32
7 0.24
0.22
—
a Standard deviation.
b Cells harvested at 48 h; all others harvested at 54 h..
c One gray (Gy) is equivalent to 100 rads.
44

-------
APPENDIX B.
EFFECTS OF CELL-CYCLE TIME
ON SISTER CHROMATID EXCHANGE FREQUENCY
Control larvae were exposed to 3 X 10~^M BrdUrd for 28, 36, 42, 48, 54, 60, and
66 h. In a given experiment, either single or multiple harvest times were used (Table Bl).
The cells of N. arenaceodentata may not all divide at the same rate. If some cells are
dividing more rapidly than others, they will be found at a given division (first, second, or
third) at an earlier time than those that are dividing more slowly. That is, second division
cells harvested at 28 h represent a faster dividing population of cells than those harvested
at later times. The proportion of cells observed in first, second, or third division varied
with the BrdUrd harvest time (Fig. Bl). The percent of cells in first division is high at
28 h and low at 66 h; the converse is true for cells in third division.
The number of cells scored and the mean and median SCE frequency obtained for
each experiment at differing harvest times were compiled (Table B2, Fig. B2). Because
the number of cells scored for each experiment was different, we used the Kruskal-Wallis
(K-W) nonparametric test (Conover, 1971) to compare the means of each experiment to
the number of cells scored. No significant bias of the mean by the number of cells scored
was found; p was 0.80 (Table B3). Next, the significance of differences in mean and
median SCE frequencies at different BrdUrd harvest times was examined using the K-W
test. The probability that all of the data from different BrdUrd harvest times were drawn
from a homogeneous pool was 0.43 for means and 0.39 for medians. This is in agreement
with the cell culture literature (Leonard and Decat, 1979; Giulotto et al., 1980).
45

-------
Table Bl. Times at which cells were harvested after initiation of the BrdUrd exposure.
Experiment
Harvest time (h)


28 36 42 48
54
60 66
1
X


2
X


3
X


4
X


5
X


6
X


7
X


8
X


9
X


11
X


12
X


13

X

14

X

15
X


16
X X
X
X x
17

X

18

X

19

X

20
X
X

21
X
X

22

X

23

X

24

X

25

X

26

X

27

X

28
X X
X

29
XXX
X
X
30

X


-------
100
100
g 50
28	36 .42	48	54
BrdUrd exposure time (h)
60
66
72
Figure Bl. Percent (a) first, (b) second, and (c) third division ceiis observed in control
Neanthes arenaceodentata larvae at differing times following initiation of BrdUrd
exposure.
47

-------
Table B2. Mean and median sister chromatid exchanges per chromosome (SCEs/C)
observed in control cell populations harvested at differing times following initiation of
BrdUrd exposure. The fraction of cells in first, second, and third division for each
experiment harvest time is also given.
BrdUrd	Fraction of cells in
harvest	Cells	Mean Median	specific division
time(h) Experiment scored3 SCEs/C SCEs/C First Second Third N*5
28
1
3
0.30
0.24
0.97
0.03
0
174

2
11
0.37
0.28
0.66
0.33
0.01
169

3
7
0.28
0.29
0.83
0.17
0
408

4
34
0.24
0.22
0.59
0.39
0.02
568

5
19
0.16
0.17
0.47
0.44
0.09
182

6
48
0.24
0.17
0.57
0.42
0.01
282

7
6
0.18
0.17
0.85
0.15
0
163

8
3
0.45
0.44
0.85
0.15
0
137

9
17
0.12
0.12
0.42
0.47
0.11
126

11
2
0.51
0.51
0.75
0.25
0
206

12
8
0.18
0.13
0.80
0.20
0
82

20
20
0.31
0.23
0.60
0.39
0.01
82

21
23
0.11
0.07
0.94
0.04
0.01
163

c
201
0.22
0.17
0.72
0.26
0.20
	





+ 0.18
+ 0.15
+ 0.04

36
29
23
0.22
0.18
0.64
0.34
0.02
126

c
23
0.22
0.18
0.64
0.34
0.02
--
42
16
39
0.56
0.11
0.45
0.55
0.01
207

28
28
0.24
0.17
0.58
0.37
0.05
148

29
17
0.20
0.18
0.55
0.44
0.01
107

c
84
0.19
0.16
0.53
0.45
0.02
—
+ 0.07 + 0.09 + 0.02
48

-------
Table B2. (Continued).
BrdUrd	Fraction of cells in
harvest	Cells	Mean Median	specific division	
time(h) Experiment scored3 SCEs/C SCEs/C First Second Third N*5
48
15
21
0.27
0.20
0.28
0.44
0.28
307

16
26
0.12
0.11
0.38
0.60
0.02
100

28
22
0.30
0.21
0.39
0.54
0.08
13

29
21
0.35
0.27
0.32
0.60
0.09
111

c
90
0.25
0.18
0.34
0.55
0.12
—




+ 0.05
+ 0.08
+ 0.11


54
13
24
0.10
0.09
0.19
0.58
0.23
218

14
18
0.20
0.14
0.42
0.50
0.08
208

16
33
0.13
0.13
0.35
0.62
0.03
146

17
65
0.22
0.18
0.35
0.61
0.04
685

18
52
0.30
0.25
0.37
0.55
0.08
883

19
40
0.18
0.13
0.39
0.56
0.06
205

20
9
0.19
0.18
0.44
0.47
0.08
727

21
12
0.13
0.12
0.60
0.39
0.01
117

22
32
0.17
0.12
0.35
0.61
0.04
137

23
52
0.12
0.09
0.35
0.63
0.02
210

24
21
0.22
0.17
0.43
0.48
0.09
148

25
24
0.26
0.27
0.48
0.48
0.04
118

26
67
0.50
0.11
0.53
0.44
0.03
359

27
73
0.19
0.17
0.32
0.62
0.06
293

28
20
0.38
0.17
0.29
0.53
0.19
70

29
22
0.19
0.17
0.21
0.74
0.05
87

30
18
0.17
0.06
0.25
0.65
0.10
83

__c
582
0.19
0.14
0.37
0.56
0.07
	





+ 0.11
+ 0.09
+ 0.06

49

-------
Table B2. (Continued).
BrdUrd
harvest	Cells	Mean Median
time(h) Experiment scored3 SCEs/C SCEs/C
Fraction of cells in
specific division
First
Second
Third
Nb
60
16
29
25
33
0.16
0.17
0.17
0.15
0.26
0.25
0.57
0.66
0.17
0.09
81
m
58
0.17
0.16
+ 0.01
0.26
+ 0.06
0.62
+ 0.06
0.13
66
16
c
21
21
0.13
0.134
0.11
0.11
0.16
0.16
0.71
0.71
0.13
0.13
85
a Data from experiments with less than 10 cells scored were pooled and treated as a
single experiment with n = 29, mean = 0.269, and median = 0.222.
b N, total number of cells examined.
c Values for this BrdUrd harvest time.
50

-------
42	48	54
BrdUrd exposure time (h)
Figure B2. Mean SCE frequencies observed in Neanthes arenaceodentata larvae control
cells harvested at differing times following initiation of 3 X lO^JM BrdUrd exposure.
Table B3. Distribution of the means of sister chromatid exchanges per chromosome
(SCEs/C) in control cells in relation to the number of cells scored.
Cells
scored	Mean SCEs/C
0-10
0.18
0.18
0.19
0.28
0.30
0.45
0.51
—
—
11-20
0.12
0.13
0.16
0.17
0.20
0.20
0.31
0.37
0.38
21-30
0.096
0.11
0.11
0.13
0.16
0.19
0.22
0.22
0.24

0.26
0.27
0.30
0.35
—
--

—
—
31-40
0.31
0.16
0.17
0.17
0.18
0.24
—
—
—
41-50
0.24
—
—
—
—
—
—
—
—
51-60
0.12
0.30
—
—
—
—
—
—
—
61-70
0.15
0.22
—
—
—
—
—
—
--
>71
0.18








51

-------
REFERENCES
Abramovsky, I., G. Vorsanger, and K. Hirschhorn (1978), "Sister-Chromatid Exchange
Induced by X Ray of Human Lymphocytes and the Effect of L-Cysteine," Mutat. Res. 50,
93-100.
Archer, P. G., A. V. Carrano, M. Bender, R. J. Preston, A. D. Bloom, and J. G. Brewen
(1981), "Guidelines for Cytogenetic Studies in Mutagen-Exposed Human Populations,
Report of Panel 1," Guidelines for Studies of Human Populations Exposed to Mutagenic
and Reproductive Hazards, A. D. Bloom and N. W. Paul, Eds. (March of Dimes Birth
Defects Foundation) pp. 1-35.
Blaylock, B. G., and T. R. Trabelka (1978), "Evaluating the Effects of Ionizing Radiation
on Aquatic Organisms," Adv. Radiat. Biol. 7, 103-152.
Carrano, A. V. (1975), "Induction of Chromosomal Aberrations in Human Lymphocytes by
X Rays and Fission Neutrons: Dependence on Cell-Cycle Stage," Radiat. Res. 63, 403-421.
Carrano, A. V., J. L. Minkler, D. G. Stetka, and D. H. Moore (1980), "Variation in the
Baseline Sister Chromatid Exchange Frequency in Human Lymphocytes," Environ.
Mutagen. 2, 325-337.
Carrano, A. V., and D. H. Moore (1982), "The Rationale and Methodology for Quantifying
Sister Chromatid Exchange in Humans," Mutagenicity; New Horizons in Genetic
Toxicology (Academic Press, Inc., New York), pp. 267-304.
Carrano, A. V., and L. H. Thompson (1982), "Sister Chromatid Exchange and Gene
Mutation," Cytogenet. Cell Genet. 33, 57-61.
Carrano, A. V., L. H. Thompson, P. A. Lindl, and 3. L. Minkler (1978), "Sister Chromatid
Exchanges as an Indicator of Mutagenesis," Nature 271, 551-553.
Conover, W. J. (1971), Practical Nonparametric Statistics (John Wiley 6c Sons, Inc., New
York).
52

-------
Dyer, R. S. (1976), "Environmental Surveys of Two Deepsea Radioactive Waste Disposal
Sites Using Submersibles," International Symposium on the Management of Radioactive
Wastes from the Nuclear Fuel Cycle (International Atomic Energy Agency, Vienna,
Austria, IAEA-Su-207/65), pp. 22-26.
Evans, H. 3. (1977), "Molecular Mechanisms in the Induction of Chromosome Aberrations,"
Progress in Genetic Toxicology, D. Scott, B. A. Bridges, and F. H. Sobels, Eds. (Elsevier,
North-Holland Biomedical Press, New York).
Filliben, 3. 3. (1975), "The Probability Plot Correlation Coefficient Test for Normality,"
Technometrics 17, 111-117.
Galloway, S. M. (1977), "Ataxia Telangiectasia: The Effects of Chemical Mutagens and
X Rays on Sister Chromatid Exchanges in Blood Lymphocytes," Mutat. Res. 45, 343-349.
Garry, V. F., 3. Hozier, D. 3acobs, R. L. Wade, and D. G. Gray (1979), "Ethylene Oxide:
Evidence of Human Chromosomal Effects," Environ. Mutagen. 1_, 375-382.
Gatti, M., S. Pimpinelli, and G. Olivieri (1974), "The Frequency and Distribution of
Iso-Labelling in Chinese Hamster Chromosomes after Exposure to X Rays," Mutat. Res.
23, 229-238.
Geard, C. R., M. Rutledge-Freeman, R. C. Miller, and C. Borek (1981), "Antipain and
Radiation Effects on Oncogenic Transformation and Sister Chromatid Exchanges in Syrian
Hamster Embryo and Mouse C3H/10T-1/2 Cells," Carcinogenesis 12, 1229-1233.
Gebhart, E. (1981), "Sister Chromatid Exchange (SCE) and Structural Aberration in
Mutagenicity Testing," Hum. Genet. 58, 235-254.
Gibson, D. A., and D. M. Prescott (1972), "Induction of Sister Chromatid Exchanges in
Chromosomes of Rat Kangaroo Cells by Tritium Incorporated into DNA," Exptl. Cell Res.
74, 397-402.
Giulotto, E., A. Mottura, R. Giorgi, L. de Carli, and F. Nuzzo (1980), "Frequencies of
Sister Chromatid Exchanges in Relation to Cell Kinetics in Lymphocyte Cultures," Mutat.
Res. 70, 343-350.
53

-------
Goodheart, C. R. (1961), "Radiation Dose Calculation in Ceils Containing Intranuclear
Tritium," Radiat. Res. 15, 767.
Harrison, F. L., and D. W. Rice, 3r. (1981), Effects of Low ^Co Dose Rates on Sister
Chromatid Exchange Incidence in the Benthic Worm Neanthes arenaceodentata, Lawrence
Livermore National Laboratory, Livermore, CA, UCRL-53205.
Joseph, A. B., P. F. Gustafson, I. R. Russell, E. A. Schuert, H. L. Volchok, and A. Tamplin
(1971), "Sources of Radioactivity and their Characteristics," Radioactivity in the Marine
Environment (National Academy of Sciences, Washington, DC), pp. 6-41.
Kato, H. (1974), "Spontaneous Sister Chromatid Exchanges Detected by a BUdR-Labelling
Method," Nature 251, 70-72.
Kato, H. (1979), "Spontaneous and Induced Sister Chromatid Exchanges as Revealed by the
BUdR-Labelling Method," Int. Rev. Cytol. 49, 55-97.
Latt, S. A., J. Allen, S. Bloom, A. Carrano, E. Falke, D. Kram, E. Schneider, R. Schreck,
R. Tice, B. Whitfield, and S. Wolff (1981), "Sister Chromatid Exchanges— A Report of the
GENE-TOX Workshop," Mutat. Res. 83, 17-62.
Leonard, A., and G. Decat (1979), "Relation between Cell-Cycle and Yield of Aberrations
Observed in Irradiated Human Lymphocytes," Can. 3. Genet. Cytol. 21, 473-478.
Littlefield, L. G., S. P. Colyer, E. E. Joiner, and R. J. DuFrain (1979), "Sister Chromatid
Exchanges in Human Lymphocytes Exposed to Ionizing Radiation during Gq," Radiat. Res.
78, 514-521.
Livingston, G. K., and L. A. Dethlefsen (1979), "Effects of Hyperthermia and X-Irradiation
on Sister Chromatid Exchange (SCE) Frequency in Chinese Hamster Ovary (CHO) Cells,"
Radiat. Res. 77, 512-520.
Marin, G., and P. M. Prescott (1964), "The Frequency of Sister Chromatid Exchanges
3
following Exposure to Varying Doses of H -Thymidine or X Rays," J. Cell Biol. 21,
159-167.
54

-------
Marine Protection, Research, and Sanctuaries Act (1972), 33 U.S.C. Sees. 1401 et seq.
(Federal).
Meyer, G. L. (1979), "Problems and Issues in the Ground Disposal of Low-Level
Radioactive Waste," Management of Low-Level Radiation Waste, Vol. 2, M. Carter, A.
Moghissi, and B. Kahn, Eds. (Pergammon Press, New York).
Miller, R. G. (1966), Simultaneous Statistical Inference (McGraw-Hill, New York), p. 62.
Minkier, J., D. Stetka, Jr., and A. V. Carrano (1978), "An Ultraviolet Light Source for
Consistent Differential Staining of Sister Chromatids," Stain Technol. 53, 359-360.
Morgan, W. F., and P. E. Crossen (1980)," X-Irradiation and Sister Chromatid Exchange in
Cultured Human Lymphocytes," Environ. Mutagen. 2, 140-155.
Morgan, W. F., 3. L. Schwartz, J. P. Murnane, and S. Wolff (1983), Effect of
3-Aminobenzamide on Sister Chromatid Exchange Frequency in X-Irradiated Cells,
Laboratory of Radiobiology and Environmental Health and Department of Anatomy,
University of California, San Francisco, CA.
Nagasawa, H., and J. B. Little (1981), "Induction of Chromosome Aberrations and Sister
Chromatid Exchanges by X Rays in Density-Inhibited Cultures of Mouse 10T-1/2 Cells,"
Radiat. Res. 87, 538-551.
Nakanishi, Y., and E. L. Schneider (1979), "In vivo Sister-Chromatid Exchange: A Sensitive
Measure of DNA Damage," Mutat. Res. 60, 329-337.
National Academy of Sciences (1980), The Effects on Populations of Exposure to Low
Levels of Ionizing Radiation, National Academy of Sciences, Washington, DC.
Noshkin, V. E., K. M. Wong,- T. A. Jokela, R. J. Eagle, and J. L. Brunk (1978),
Radionuclides in the Marine Environment near the Farallon Islands, Lawrence Livermore
Laboratory, Livermore, CA, UCRL-52381.
55

-------
Perry, P., and H. 3. Evans (1975), "Cytological Detection of Mutagen-Carcinogen Exposure
by Sister Chromatid Exchange," Nature 258, 121-125.
Perry, P., and S. Wolff (1974), "New Giemsa Method for the Differential Staining of Sister
Chromatids," Nature 251, 156-158.
Pesch, G. G., and C. E. Pesch (1980a), "Neanthes arenaceodentata (Polychaeta: Annelida),
A Proposed Cytogenetic Model for Marine Genetic Toxicology," Can. 3. Fish. Aquatic Sci.
37, 1225-1228.
Pesch, G. G., and C. E. Pesch (1980b), "Chromosome Complement of the Marine Worm,
Neanthes arenaceodentata (Polychaeta; Annelida)," Can. 3. Fish. Aquatic Sci. 37, 286-288.
Pesch, G. G., 3. S. Young, and M. Varela (1981), Effects of Ionizing Radiation on the
Chromosomes of the Marine Worm, Neanthes arenaceodentata, Environmental Protection
Agency, Environmental Research Laboratory, Narragansett, RI, Contribution No. 198.
Popescu, N. C., S. C. Amsbaugh, and 3. A. DiPaolo (1981), "Relationship of
Carcinogen-Induced Sister Chromatid Exchange and Neoplastic Cell Transformation," Int.
3. Cancer 28, 71-77.
Reish, D. 3. (1957), "The Life History of the Polychaetous Annelid Neanthes caudata
(delle chiaje), Including a Summary of Development in the Family Nereidae," Pac. Sci. 11,
216-228.
Reish, D. 3. (1974), "The Establishment of Laboratory Colonies of Polychaetous Annelids,"
Thalassia 3ugosl. 10, 181-195.
Renault, G., A. Gentil, and I. Chouroulinkov (1982), "Kinetics of Induction of
Sister-Chromatid Exchanges by X Rays through Two Cell-Cycles," Mutat. Res. 94,
359-368.
Snedecor, G. W., and W. G. Cochran (1967), Statistical Methods (The Iowa State University
Press, Ames, Iowa), 6th ed.
56

-------
Solomon, E., and M. Bobrow (1975), "Sister Chromatid Exchanges— A Sensitive Assay of
Agents Damaging Human Chromosomes," Mutat. Res. 30, 273-278.
Taylor, J. H. (1958), "Sister Chromatid Exchanges in Tritium Labeled Chromosomes,"
Genetics 43, 515-529.
Templeton, W. L., M. Barnhard, B. G. Blaylock, C. Fisher, M. J. Holden, A. G. Klimov,
P. Metalli, R. Mukherjee, O. Ravera, L. Sztanyik, and F. Van Hoeck (1976), "Effects of
Ionizing Radiation on Populations and Ecosystems," Effects of Ionizing Radiation on
Aquatic Organisms and Ecosystems, International Atomic Energy Agency, Vienna, Austria,
Technical Document 1972.
Walsh, J. E. (1962), "Nonparametric Confidence Intervals and Tolerance Regions,"
Contribution to Order Statistics, A.E. Sarban and B.G. Greenberg, Eds. (Whey, New York).
Wolff, S. (1982), "Difficulties in Assessing the Human Health Effects of Mutagenic
Carcinogens by Cytogenetic Analyses," Cytogenet. Cell Genet. 33, 7-13.
Woodhead, D. S. (1980), "Marine Disposal of Radioactive Wastes," Helgol. Wiss.
Meeresunters. 33, 122-137.
Yu, L. (1976), Probing the Mechanism of Sister Chromatid Exchange Formation with the
Fluorescent plus Giemsa Technique, Ph.D. thesis, University of California, San Francisco,
CA.
PMB/adf
57

-------
TECHNICAL REPORT DATA
(Please read Instructions on the reverse before completing)
1. REPORT NO. 2.
EPA 520/1-84-020
3. RECIPIENT'S ACCESSION NO.
4. TITLE AND SUBTITLE
Frequencies of Chromosomal Aberrations and Sister
Chromatid Exchanges in the Benthic Worm Neanthes
arenaceodentata Exposed to Ionizing Radiation
5. REPORT DATE
6. PERFORMING ORGANIZATION CODE
/. author(s) piorence l> Harrison Dan H. Moore
David W. Rice, Jr.
8. PERFORMING ORGANIZATION REPORT NO.
UCRL-53524
9. PERFORMING ORGANIZATION NAME AND ADDRESS
Lawrence Livermore National Laboratory
Environmental Sciences Division
Livermore, California 94550
10. PROGRAM ELEMENT NO.
11. CONTRACT/GRANT NO.
IAG No. EPA-AD 89 F00070
12. SPONSORING AGENCY NAME AND ADDRESS
Office of Radiation Programs
U.S. Environmental Protection Agency
401 M St., S.W.
Washington, DC 20460
13. TYPE OF REPORT AND PERIOD COVERED
14. SPONSORING AGENCY CODE
ANR-461
15. SUPPLEMENTARY NOTES
16. abstract Traditional bioassays are unsuitable tor assessing sublethal effects from
ocean disposal of low-level radioactive waste because mortality and phenotypic
responses are not anticipated. We compared the usefulness of chromosomal aberration
(CA) and sister chromatid exchange (SCE) induction as measures of low-level radiation
effects in a sediment-dwelling marine worm, Neanthes arenaceodentata. The SCEs, in
contrast to CAs, do not alter the overall chromosome morphology and, in mammalian cells,
appear to be a more sensitive indicator of DNA alterations caused by environmental
mutagens.
Newly hatched larvae were exposed to two radiation exposure regimes of either
x rays at a high rate of 0.7 Gy (70 R)/min for as long as 5.5 min or to 60Co gamma rays
at a low rate of from 4.8 x 10~ to 1.2 x 10 Gy (0.005 to 12 R)/h for 24 h. After
irradiation, the larvae were exposed to 3 x 10 M bromodeoxyuridine (BrdUrd) for 28 h
(x-ray-irradiated larvae) or for 54 h (6 Co-irradiated larvae). Larval cells were
examined for the proportion of cells in first, second, and third or greater division.
Frequencies of CAs and SCEs were determined in first and second division cells,
respectively.
For x-ray irradiation, dose-related increases occur in chromosome and and chromatid
deletions, but a dose of >2 Gy (>200 R) was required to observe a significant increase.
LS.rvae receiving Co irradiation showed elevated SCE frequencies with significant
increases at 0.6 Gy (60 R).
17. KEY WORDS AND DOCUMENT ANALYSIS
a. DESCRIPTORS
b.IDENTIFIERS/OPEN ENDED TERMS
c. COS ATI Field/Group
1.	Radiation Effects
2.	Chromosomal Aberration
3.	Sister Chromatid Exchange
4.	Polychaete Worms


18. DISTRIBUTION STATEMENT
Unlimited Release
19. SECURITY CLASS (ThisReport)
Unclassified
21. NO. OF PAGES
20. SECURITY CLASS (This page)
Unclassified
22. PRICE
EPA Form 2220-1 (Rปป. 4-77) previous edition is obsolete

-------