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2 mice following consumption of Great Lakes coho salmon (Oncorhynchus kisutch)
C h e m o s p h e r e , V o l . 1 7 , NOo2, P r i n t e d in G r e a t B r i t a i n
pp
405-420,
1988
0045-6535/88 $ 3 . 0 0 + .OO P e r g a m o n J o u r n a l s Ltd.
BIOACCUMULATION OF HALOGENATEDAROMATIC
HYDROCARBONS
IN C57BI/6 AND DBA/2 MICE FOLLOWING CONSUMPTION OF GREAT LAKES COHO SALMON (ONCORHYNCHUS KISUTCH)
Glenn B. Cleland*, Barry G. Oliver and Ronald A. Sonstegard *Department of Pathology, McMaster University, Hamilton, Ontario, L8N 3Z5 Canada (GBC); National Water Research Institute, Canada Centre for Inland waters, Burlington, Ontario, L7R 4A6, Canada (BGO); Department of Comparative Medicine, School of Veterinary Medicine, Tufts University, Grafton, MA, 01536, USA (RAS).
ABSTRACT A gradation of polychlorinated biphenyl isomer and congener levels were found in coho salmon from Lakes Erie, Michigan and Ontario. A similar bioaccumulation pattern was observed in mouse livers following consumption of Great Lakes fish and, in general, the levels were higher in C57BI/6 than in DBA/2 mice. INTRODUCTION Halogenated
aromatic
hydrocarbons
(HAHs)
have
been
shown
to
bioaccumulate
and
bioconcentrate in fish via both dietary exposure (Borgmann and Whittle, 1983) and gill exchange (Oliver and Niimi, 1983).
One of the most significant human chronic exposures to HAHs involves
the consumption of fish from contaminated lakes and streams by 1982).
Great Lakes salmon
consumers reportedly eat 24 to
sport fishermen (Cordle et al.,
25 ib of fish per year, with
upper
limits reaching 180 ib and one reported annual consumption of 260 ib (Cordle et al., 1982). In mice and rats, the toxicity
responses to HAHs are believed to be determined by the
gene locus which codes for a cytosolic receptor (Poland and Knutson, 1982; Okey, 1983).
Ah
Poland
and Knutson (1982) have suggested that HAH toxicity may be mediated through the Ah receptor and that the
initial event
is the stereoscopic
C57BI/6 (B/6) strain of mouse
recognition and
has been shown to be
binding by this
receptor.
Ah+ and therefore more susceptible to
The HAH
toxicity whereas the DBA/2 (D/2) strain of mouse has been shown to be Ah- and consequently more resistant to
HAH exposure
(Poland and
Knutson,
1982;
Silkworth and
Grabstein, 1982;
Okey,
1983). This study was designed to provide comprehensive baseline determinations of polychlorinated biphenyl (PCB) isomers and pollutants)
congeners (as well as several other
the levels of organochlorine
in coho salmon from three of the Great Lakes and from the Pacific Ocean.
dietary exposure to
these fish, the
subsequent levels and
Following
bioaccumulation patterns of
these
pollutants were examined and compared in liver tissues of C57BI/6 (Ah+) and DBA/2 (Ah-) mice.
405
406
MATERIALS AND METHODS
MICE: Three week
old
weanling male
Laboratory (Bar Harbor, Me.).
C57BI/6 and
Mice were
DBA/2
mice were
housed five-to-a cage
obtained from
the
Jackson
on a twelve hour daily
light
cycle and fed control or fish-supplemented diets and water ad libitum for four months. DIETS: Adult coho salmon (Oncorhynchus kisutch) were obtained during the 1982, fall spawning runs from Lake Ontario (Credit River, Streetsville, Ont.), Lake Erie (Walnut Lake Michigan
(Platte River,
Alaskan Seafoods
Honor, Mi.)
Inc., Kodiak,
Al.
and Pacific
Fish were
Creek, Fairview, Pa.),
Ocean coho salmon
beheaded, eviscerated
were obtained
and minced
from
in a
meat
grinder. Powdered rodent chow (Purina No. 5001) was supplemented with 33% (based on the dry wt of fish). No. 40060), i0 mg/kg of minerals,
(Teklad No. 170710),
thiamine (Swiss) to ensure nutritional quality. fish.
Diets were mixed
-20°C.
pooled coho salmon mince
Mouse diets were fortified with I0 mg/kg of vitamins,
Control mice were fed rodent
4.5% corn oil (Mazola), and I00 mg/kg of
All additives were
in a commercial food mixer
(Teklad
based on the dry weight of
(Hobart), pelletized and stored frozen
pellets (Purina No. 5001).
Mice were fed ad libitum
at for
four months. HALOGENATEDAROMATIC Ten, fifteen preparation.
HYDROCARBON ANALYSIS OF COHO SALMON ANDMOUSE TISSUES:
gram
samples were
taken
at random
from
each
pooled coho
salmon
mince
The samples from each coho salmon source were pooled, and total lipid levels were
determined by the were extracted
chloroformmethanol extraction method
and analyzed
by gas
of Bligh and
chromatography (GC)
to determine
Dyer (1959). a profile
Specimens of the
HAH
liver) tissues were ground in Na2SO 4 and soxhlet extracted
for
contaminants by the method described by Oliver and Nicol (1982). The coho salmon (or mouse 24 hours
with
hexane/acetone
distilled water to remove the Snyder condensor.
The bulk
(41:59).
The samples
then extracted
acetone, and evaporated to approximately lipid was removed
minute with 3 ml of high purity H2SO 4 in a passage through a 2.5
were
cm layer of
by shaking the
with 1
litre
30 ml using a 3
of
stage
extract for approximately
one
stoppered flask, and then the hexane layer dried by
Na2SO 4 in a
filter funnel.
Following re-evaporation,
the
extracts were further purified by passage through a H2SO4/silica gel column. The analyses utilized
dual capillary
chromatograph equipped with
columns (30m, OVl
electron capture detectors.
and SE54) on
The carrier
a Varian 3700
gas was helium
gas
(linear
velocity 30 cm/s) and the temperature program was 50°C to 250°C at l°/min. A total
of
91
chlorinated compounds gamma-chlordane
were
including
(pp-DDE),
2,2-bis-(p-chlorophenyl)-l,l-dichloroethane
-2,2,2-trichloroethane (mirex),
(pp-DDT),
Hexachlorobenzene
2,2-bis-(p-chlorophenyl)-l, (pp-DDD),
dodecachlorooctahydro-
gamma-hexachlorocyclohexane
as octachlorostyrene
(g-Cl),
measured.
pesticides,
seven
l,l-bis-(p-chlorophenyl)
1,3,4-metheno-2H-cyclobutopentalene
(lindane) and alpha-hexachlorocyclohexane
(OCS) and 82 individual PCB congeners were quantified.
compounds were used for instrument calibration.
(HCB),
l-dichloroethylene
The other isomers
(a-BHC), as well For PCBs, 53 pure
were tentatively identified
from the chromatograms and retention indices of Safe et al.
(1983) and Mullin et al. (1984) by
running Aroclor
same
1260,
1254,
and 1016
mixtures
with the
column (SE54)
at
the
same
407
temperature program rate. by
using
the
Aroclors
composition data of
Detector as
response factors (RFs) for unavailable isomers were
secondary
Mullin (1985).
standards
The
and
employing
total PCBs in
Aroclor
weight
found
percentage
Environmental Protection Agency
standard Aroclors 1242, 1248, 1016, 1254, and 1260 determined by
(EPA)
stmm~ing the concentrations of
individual congeners, agreed with the reference value to better than +/- 10%. The approximate compotmd
detection limits for the
material in the sample extracts
mouse livers, based
detected at a signal to
for di- and trichlorobiphenyls, 0.2 to .05 ng/g for the pesticides.
Control
mouse
chow
specimens were
on the amount
noise ratio of 5:1, were: ca. i
of ng/g
other PCBs and 0.i to 0.2 ng/g for the
concentrated
by 20-fold
to
provide
more
sensitive detection. The PCB isomer and congener numbering system of Ballschmiter and
Zell (1980) was used for
brevity.
RESULTS GAS CHROMATOGRAPHIC ANALYSIS OF HALOGENATED AROMATIC HYDROCARBON CONTENT OF COHO SALMON USED AS DIETARY SUPPLEMENTS FOR LABORATORY ANIMALS: Gas chromatographic analysis of the coho salmon used as dietary supplements for laboratory animals indicated that Pacific Ocean
coho salmon contained a total PCB content of 20 ng/g
Lake Ontario coho salmon contained 2900 ng/g (Table i). Michigan, the
greatest proportion
heptachlorobiphenyls (7-CB)
of the
PCBs were pentachlorobiphenyls
and hexachlorobiphenyls
and
In coho salmon from Lakes Ontario and
(6-CB).
greatest proportion of PCBs were 7-CB followed by 5-CB and Ocean contained mostly 5-CB followed by 6-CB and 7-CB.
In
6-CB.
(5-CB) followed
Lake Erie
coho salmon
by the
Coho salmon from the Pacific
This profile was also reflected in the
total percent chlorination of the PCBs which is similar in all four coho salmon groups (56.7% 59.1%). Isomeric analysis
of
the
PCB
content of
coho
salmon
used as
diet
supplements
for
laboratory animals (Table 2) revealed that the Lake Ontario coho salmon contained higher levels of all isomers seen in
other fish groups.
The
following PCB congeners were analyzed but
detected in either the coho salmon used as diets or the four month exposure:
#4, #6, #7, #8, #15+18,
not
in B/6 or D/2 mouse liver tissue following #16, #17, #19, #22, #24, #25, #26,
#28+31,
#32, #36+45, #46, #53 and #136. Hexachlorobenzene was detected in coho salmon from the Pacific Ocean (2.8 ng/g), Lake Erie (1.3 ng/g), Lake Michigan (2.5 ng/g) and Lake Ontario (9.1 ng/g).
Coho salmon from the Pacific
Ocean were the only specimens which contained detectable levels of a-BHC (8 ng/g). not detected in any of the fish (150 ng/g).
The
pesticides
distribution of low levels in
Lindane was
examined and mirex was found only in salmon from Lake pp-DDE
and
pp-DDT
followed
a pattern
similar
to
Ontario the
Pacific Ocean eoho salmon followed by increasing levels in
salmon from Lakes Erie, Michigan and Ontario.
PCB coho
Lake Erie coho salmon contained higher levels of
pp-DDD than Lake Michigan coho salmon, but both were less
than levels detected in Lake Ontario
coho salmon (27 ng/g). Analysis of control
Purina mouse
chow revealed very
low levels of
PCBs (0.4 ng/g)
and
pesticide residues (Table I). The total percentage of body
lipid was greatest in tissue from Pacific Ocean coho
(4.2%) and least (1.6%) in Lake Erie eoho salmon (Table I).
salmon
408
EFFECT OF DIETARY
EXPOSURE TO
HALOGENATED AROMATIC HYDROCARBON
CONTAMINATED COHO SALMON
FOR
FOUR MONTHS ON ORGANOCHLORINE LEVELS IN C57BI/6 AND DBA/2 MOUSE LIVER TISSUE:
Following a four month dietary exposure to coho salmon, soxhlet C57BI/6 and DBA/2 mice were analyzed by gas chromatography for (2-CB) were not
found in
trichlorobiphenyls were found in
either B/6 or
(3-CB) were
B/6 mice
D/2 mouse
not found in
which were fed
extracted liver tissue of
HAH content.
livers (Table 3,
coho salmon tissue
coho salmon
4, 5
Although
(Table i), detectable
from the Pacific
Michigan (18 ng/g), Lake Ontario (9.6 ng/g; Table 3), and
Dichlorobiphenyls and 6).
levels
ocean (6.3 ng/g),
Lake
in D/2 mice which consumed Lake Erie
coho salmon (22.0 ng/g, Table 5). Tetrachlorobiphenyls
(4-CB) occurred in liver
extracts of B/6 mice in all dietary
with the highest levels in the Lake Michigan (19 ng/g) fed mice (Table 3).
groups
and Lake Ontario (31 ng/g) coho salmon-
The 4-CB isomers were also detected in D/2 mice which were fed salmon from
all of the Great Lakes
with the highest levels occurring
Ontario (46 ng/g) groups (Table
5).
It was interesting to note that the 4-CB
pattern in mice did not follow the distribution in the tissue levels of 2.0 ng/g
in the Lake Erie (14 ng/g) and
Lake
bioaccumulation
dietary coho salmon (Table i) which had
(Lake Erie), 130 ng/g (Lake Michigan), and 260 ng/g (Lake
Ontario).
The 4-CB which bioaceumulated to the highest level in B/6 mice which consumed Lake Michigan and Lake Ontario coho salmon was
PCB #47+75 (Table 4).
mice which consumed Lake Ontario isomers #61, #66, and
Isomer #47+75 also bioaccumulated in
coho salmon as did isomers
#70 were also
#61, #66 and #70 (Table 6).
primarily responsible for
D/2 PCB
the 4-CB content in Lake
Erie
salmon-fed D/2 mice (Table 6). Pentachlorobiphenyl
(5-CB)
isomers were detected
dietary groups (Table 3), as well as in all levels in B/6 mice
followed a similar
with the lowest levels in the Lakes Erie (68 ng/g)
Ocean coho salmon
5-CB isomers which accounted
3).
the Lake Erie salmon consumers
it's co-migrating
coho salmon, 120
5-CB
in both B/6
congener #129
lowest
and 6).
It
Michigan and 210 ng/g
it was not detected in
in Lake Ontario
either B/6 or D/2 mice (Tables 4 and
was 57 coho 6).
consumption of coho salmon from Lakes
Erie and (12.3 ng/g), Michigan (23.8 ng/g) and Ontario (136.0 which were fed coho salmon
#86,
parallel
For example, PCB isomer #i01 was found at levels of ng/g in Lake
Lake
The individual
and D/2 mice included (Tables 4
in fed
Ontario
had 84 ng/g and the
liver tissue (Table 5).
In contrast, isomer #118 was found in B/6 mice following also detected in D/2 mice
in the Lake
bioaccumulation pattern of 5-CB isomers in mice did not
that seen in the dietary coho salmon. salmon tissue (Table 2), yet
and the highest
all
salmon
In DBA/2 mice the 5-CB levels were also
for the bioaccumulation
#126 with
interesting to note that the ng/g in Lake Erie
The
levels in dietary coho
and the highest levels in B/6 mice
diet group (2.9 ng/g)
salmon-fed group (560 ng/g), however
#118 and
mice from
Pacific Ocean salmon-fed B/6 mice (15 ng/g), intermediate levels and Lake Michigan (120 ng/g)
Michigan coho salmon-fed D/2 mice had 35 ng/g in their
#99, #105,
tissue of B/6
D/2 mice which were fed fish (Table 5).
distribution pattern to
Lake Ontario coho salmon (290 ng/g; Table in the Pacific
in liver
ng/g, Table 4).
Isomer ~I18 was
from Lakes Erie (20.5 ng/g) or
Michigan
(9.3 ng/g) and especially Lake Ontario (220.0 ng/g, Table 6). Hexachlorobiphenyls
(6-CB) were detected at similar levels in liver extracts from both B/6
and D/2 strains of mice within most dietary groups (Tables 3 and 5). the 6-CBs which accounted
primarily for the bioaeeumulation
In both B/6 and D/2 mice,
were isomers #138, #146 and
#153
409
(Tables 4 and 6). The heptachlorobiphenyl detected in
B/6 and
D/2
(7-CB)
mice in
isomers accounted all dietary
salmon-fed mice had
the highest 7-CB
ng/g, Table 5) mice.
However, it
for
50% or
groups (Tables
levels in both B/6
more
3 and
of the
5).
(2500 ng/g, Table
was interesting to note that
total
The Lake
PCBs
Ontario
3) and D/2
(1900
B/6 mice which were fed
Lake
Erie coho salmon had 7-CB levels of 1200 ng/g (Table 3), whereas similarly fed D/2 mice had 250 ng/g (Table 5).
The 7-CB isomer #180 was in the highest concentration in both B/6 and D/2 mice
(Tables 4 and 6).
This isomer reached levels of
(Table 4).
7-CBs which
Other
isomers #170, #178, #183 and
accounted for
#187.
537.5 ng/g in Lake Erie salmon-fed B/6
the bioaccumulation
The isomer #189
(3.4 ng/g) Lake Ontario salmon-fed mice
in B/6 and
mice
D/2 mice
were
was found in both B/6 (7.9 ng/g) and
D/2
(Tables 4 and 6), although it was not detected in
the
dietary fish (Table 2). Most octachlorobiphenyl
(8-CB) isomers were detected at similar levels in B/6 and D/2 mice
which were fed coho salmon from Lakes Michigan and Ontario. was found at
23.0 ng/g
in B/6 mice
Ontario salmon (Tables 4 and 6).
In
and 4.4 ng/g
An exception was isomer #198 which
in D/2 mice
following consumption of
Lake
B/6 mice which were fed Lake Erie coho salmon diets,
8-CB isomers #194, #196 (and eo-eluting isomer #203) and #201
the
reached levels of 12.5, 20.3 and
19.0 ng/g respectively in B/6 mice (Table 4), and 6.6, 9.8, and 8.5 ng/g in D/2 mice (Table 6). The nonachlorobiphenyls Great Lakes coho salmon isomer (#209)
(9-CBs) reached similar levels in both strains of mice within each
dietary group (Tables 3 and
was found
Ontario coho salmon-fed
to an
5).
appreciable level in
groups (Tables 3
and 5).
The sole decachlorobiphenyl
both strains
Isomer
of mice only
#209 was not
(10-CB)
in the
Lake
detected in the
body
tissue of Lake Ontario salmon (Table i). The C57BI/6
mice which
burden of 4000 ng/g (Table
were fed
Lake Ontario
3) and DBA/2 mice fed
total PCB
liver
the same diet had a similar total PCB
salmon bioaccumulated a
liver
level of 3500 ng/g (Table 5), while the total PCB level in the dietary Lake Ontario coho salmon was 2900 ng/g (Table ng/g (Table i).
i).
Coho
salmon from Lake Michigan contained
Lake Michigan salmon-consuming
(Table 3) while D/2 mouse livers had liver contained a total PCB
B/6 mice accumulated
530 ng/g (Table 5).
a total PCB level of
860
930 ng/g of total
PCBs
Lake Erie coho salmon-fed B/6
mouse
concentration of 1500 ng/g (Table 3) and D/2 liver contained
only
480 ng/g (Table 5), while body tissue from Lake Erie coho salmon had 500 ng/g (Table i). noteworthy that the PCB congeners found in liver tissue of
It is
B/6 mice which were fed coho salmon
from Lake Ontario were always present in equal or greater concentration than those found in the livers of other B/6 dietary
groups, with the possible exception
of congener #32 (Table 4
and
6). Hexachlorobenzene
(HCB) was found in liver tissue of mice at
levels which were similar to
those detected in dietary coho salmon (Table i), except in Lake Ontario coho salmon-fed B/6 and D/2 mice where the HCB levels reached 20.3 and 15.0 ng/g respectively (Tables 3 and 5). other pesticides examined, a-BHC, lindane,
g-Cl and pp-DDT were not
which were fed Great Lakes coho salmon (Tables 3 and 5). diet in which mirex was detected (Table i). liver tissues of both
However,
Of the
detected in livers of mice
Lake Ontario coho salmon was the only
detectable levels of mirex were found in
mouse strains following dietary consumption
of coho salmon from any
the Great Lakes examined, with
the highest concentrations occurring in B/6 (700 ng/g) and
(490
fed Lake
ng/g)
mice
which
were
Ontario
salmon
(Tables
3
and
5).
The
of D/2
highest
410
levels of OCS were
found in B/6
from Lake
(Tables 3
Ontario
(24 ng/g) and D/2 (34
and
distribution pattern in livers of
5).
The
pp-DDE was
the two mouse strains.
from Lake Erie, the pp-DDE levels in B/6 in Lake Michigan coho
ng/g) mice which consumed coho
pesticide
found in
an
salmon
interesting
In mice which were fed coho
salmon
mice were 1.9 ng/g, and in D/2 mice 58 ng/g,
salmon-fed mice, the
B/6 strain had 48 ng/g
while in the Lake Ontario salmon-fed mice, the B/6 strain
whereas
and the D/2 had 2.1
ng/g,
had 240 ng/g and the D/2 had similar
280.0 ng/g level of pp-DDE (Tables 3 and 5). DISCUSSION A gradation of PCB concentrations the Great Lakes. Erie and
was found in the body tissue of adult coho salmon
from
The lowest level occurred in salmon from the Pacific Ocean, followed by Lakes
Michigan
with the
analysis of the PCB
highest concentration
in
body burdens similarly indicated
the highest levels of all
isomers and congeners and the
other chemicals studied. total organochlorine
Lake Ontario
The
coho salmon.
Isomeric
that Lake Ontario coho salmon
contained
highest levels of all but one of
PCB congener analysis confirms and expands a report of
levels
in
Lake
Ontario
salmon
(Sonstegard
and
Leatherland,
Similarly, Villeneuve et al. (1981) fed Sprague-Dawley rats diets containing
the
elevated 1978).
5.8% Lake Ontario
salmon and found liver PCB levels of 0.93+/-0.18 ppm following a 28 day exposure. The total PCB levels in exposure to coho
salmon,
liver tissue of B/6 and
in
which consumed diets
of Pacific
Ontario coho
bioaccumulated the
salmon
D/2 mice following a four month
general, reflected the pattern salmon had very highest
observed in the
low levels
while mice which
PCB levels.
fish.
dietary The
mice
were fed
Lake
This observation
appears
to
correlate with the total PCB levels to which the mice were exposed via the dietary fish. The relative
accumulation of
(BAF) which, in this case,
chemicals can fish.
Lake Ontario salmon, the following penta- (0.01-1.2, 0.37); hexa4.0).
factor
Although there was a large variation in the
PCB's.
For example,
in the B/6 mice which were
ranges and means were observed:
(0.02-2.9,
This observation
1.3); heptawas also
tetra- (0.05-0.62, the changes
in the
to fed
0.16);
(1.4-6.2, 2.8); octa- (2.6-3.3,
reflected by
by BAF
PCB's showing that PCB structure was important, the BAF tended
increase with the chlorine content of the
nona- (3.4-4.6,
the bioaccumulation
is defined as the chemical concentration in mouse liver divided
the chemical concentration in the diet within an isomeric class of
be estimated by
3.0); percent
chlorine of the total PCBs which were higher in the mice than in the diet fish (Tables i, 3 and 5). It has been suggested that, in general, are those which induce
the PCB congeners
mixed function oxidase
potentially toxic congeners is shown
these fish
percentage of toxics were similar (ca.
Similarly, the highest levels of total toxic PCB's were observed in
mouse livers following consumption was higher than in
these toxic PCB congeners.
A list of
Although the gradation pattern of toxic PCB's observed
in Grat Lakes salmon followed the total PCB levels, the
strains of mice
1983).
together with their total concentrations in dietary
and mouse livers in Tables i, 3 and 5. 20%) in all fish examined.
which tend to be the most toxic
enzymes (Safe et al.,
of Lake Ontario
coho salmon.
dietary fish, indicating
This observation
agrees with the
The percent toxics in
both
an enhanced biomagnification findings of Safe (1982),
also suggested a preferential bioaccumulation of toxic PCB congeners in human breast milk.
of
which
411
Of the nine pesticide HAHs reached similar coho salmon.
examined, hexachlorobenzene (HCB) and octachlorostyrene
concentrations in
both mouse
strains following consumption
Mirex bioaccumulated to levels which, in D/2
were 4.6-fold higher than levels to find mirex
in liver
in other
(OCS) Ontario
mice were 3.2-fold, and in B/6 mice
in their Lake Ontario coho salmon diets.
extracts of mice
of Lake
dietary groups than
It was
interesting
Lake Ontario
salmon.
Mirex has been utilized by companies other than Hooker Chemical Co., and traces of it have been reported in the literature in al., 1983). mice.
These results
areas other than the Niagara
River and Lake Ontario (Aspila
reflect the efficiency of bioaccumulation
Following consumption of coho salmon from Lake Erie,
of mirex by B/6 and
et D/2
D/2 mice had 30-fold higher levels
of pp-DDE than B/6 mice, however the levels were reversed in B/6 mice which had 23-fold greater levels of pp-DDE than D/2 mice which consumed Lake Michigan
coho salmon.
which consumed Lake Ontario salmon had similar levels of pp-DDE.
Mice of both strains
The diets of fish from Lakes
Erie or Michigan may contain substances which are blocking receptors
in B/6 or D/2 mice or are
acting synergistically or antagonistically to affect pp-DDE metabolism in these mouse strains. Dietary consumption of Great Lakes coho salmon has been identified as a significant source of chronic exposure to HAHs in
man (Cordle et al., 1982).
Lake Michigan fish consumption
also been correlated with PCB levels in human maternal serum Schwartz et al., 1983).
and milk (Wichkizer et al., 1981;
Lake Michigan coho salmon-eating lactating mothers has been shown
have total PCB levels of 980.9 ng/g in their milk (Schwartz et al., 1983). also shown that lactating canadian women in the Ottawa region,
has
to
Recent surveys have
who do not eat freshwater fish,
have up to 29 ng/g of total PCBs and up to 39 ng/g of pp-DDE in their milk (Mes et al., 1984). It is apparent that man is being chronically exposed to the HAH congeners present in Great Lakes coho
salmon.
Furthermore,
the HAH
approaching those reported in this study. animals have been established.
levels in
humans
who eat
Great Lakes
fish
are
Comparative congener analysis of fish and laboratory
The bioaccumulation patterns in
the two strains of mice
will
provide reference points for future congener analysis in fish eating
humans and may aid in the
establishment of the
These
valuable in
the
(as yet
ongoing
unknown) Ah receptor
evaluation
of
the
status of
health
man.
risks associated
baselines will
with
this
route
be of
environmental exposure.
ACKNOWLEDGEMENT
These studies were supported in part by a grant from Research Council of Canada (RAS).
the National Science and Engineering
412
TABLE 1 GAS CHROMATOGRAPHIC ANALYSIS OF HALOGENATED AROMATIC HYDROCARBON LEVELS IN COHO SALMON TISSUE AND AS DIETARY SUPPLEMENTS FOR LABORATORY ANIMALS HALOGENATED AROMATIC HYDROCARBON CONTENT
COMPOUND 2-CB 3-CB 4-CB
(ng/g)
CONTROL CHOW
PACIFIC COHO
L. ERIE COHO
L. MICHIGAN COHO
L. ONTARIO COHO
ND ND ND
ND ND ND
ND ND 2.0 (0.4%)
ND ND 130 (15.1%)
ND ND 260 (9.3%)
5-CB
0.21 (52.5%)
ii. (56.8%)
170 (32.7%)
350 (40.8%)
920 (33.7%)
6-CB
0.03 (7.5%)
4.6 (23.1%)
130 (25.3%)
140 (16.3%)
670 (23.1%)
7-CB
0.05 (5.0%)
4.0 (20.1%)
190 (38.3%)
220 (25.9%)
890 (30.9%)
8-CB
0.14 (35.0%)
ND
16 (3.3%)
17 (1.9%)
76 (2.6%)
9-CB
ND
ND
ND
ND
9.7% (0.3%)
10-CB
ND
ND
ND
ND
Total PCB's % C1
0.4 59.5%
Total Toxic* PCB's Percent Toxic
PCB's
ND 0%
20 57.1% 4.0 2.0%
500 59.1%
860 56.7%
i00
170
20.0%
19.8%
HCB a-HCB Lindane Mirex OCS g-CL pp-DDE pp-DDD pp-DDT
ND ND ND ND ND 0.2 0.i ND 0.i
2.8 8.0 ND ND ND ND i0 2.7 6.6
1.3 ND ND ND 3.4 5.9 79 15 12
2.5 ND ND ND ND 15 240 9.3 37
Percent Lipid
4.3
4.2
1.6
2.0
( = toxic PCB's #81, 105, 118, 126, 128, 138, 156, 157, 158, 166, 170 and 189) (ND = not detected)
ND
2900 57.8% 630 21.7% 9.1 ND ND 150 27 12 670 27 61 2.6
413 TABLE 2
GAS CHROMATOGRAPHIC PCB CONGENER ANALYSIS OF COHO SALMON USED AS DIETARY SUPPLEMENTS FOR LABORATORY ANIMALS
PCB CONGENER CONTENT (ng/g) CONGENER
# # # # # # # # # # # # # # # # # # # # # # #
32 4O 42 44 47+74 49 52 61 64 66 70 71 78+109 81 82 84 86 87+112 91 92 95 97 99
# # # # # # # # # # # # # # # # # # # # # # #
i01 105 ii0 118 126+129 128 130 138 141 143 144 146 151 153 156 157 158+186 166 167 170 171+202 172 174 177 178 180 183 185 187 189 192 194 195
# # # # # # # # #
CONTROL CHOW
ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND 0.03 0.15 ND 0.03 ND ND hiD ND 0.01 ND ND ND ND ND 0.03 ND ND ND ND ND ND ND ND ND hiD ND ND ND ND 0.01 ND ND ND ND
PACIFIC COHO
ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND i0 1.3 ND ND ND 2.7 ND ND ND ND ND ND ND 4.6 ND ND ND ND ND ND ND ND ND hiD ND ND ND ND 1.3 ND ND ND ND
L. ERIE COHO
ND ND ND ND hiD ND ND 2 ND ND ND ND ND ND ND ND 4.6 9.2 ND ND 16 ND 18 57 7.2 32 16 hiD 8.6 ND 51 17 ND 22 6.6 ii 50 4.6 ND 2.6 ND ND 13 6.6 ND i0 8.6 Ii 53 12 ND 32 ND ND 5.9 ND
L. MICHIGAN COHO
ND ND ND ND ii ND 25 9.3 21 28 23 3.3 ND 9.3 ND ND 12 17 ND ND 21 18 42 120 17 55 40 ND 14 6.6 66 15 8 21 19 12 52 8 ND 5.3 ND ND ii 8.6 ND 6 6.6 13 56 9.3 ND 32 ND ND 5.3 ND
L. ONTARIO COHO
ND 1.8 ND 19 16 21 36 15 25 67 48 6.1 9.7 13 14 18 45 55 26 16 54 53 130 210 42 140 140 14 38 18 260 67 12 85 73 4O 240 22 16 21 16 17 52 19 21 33 35 44 240 51 7.9 130 ND 12 19 5.5
414
TABLE 2 (continued) GAS CHROMATOGRAPHIC PCB CONGENER ANALYSIS OF COHO SALMON USED AS DIETARY SUPPLEMENTS FOR LABORATORY ANIMALS PCB CONGENER CONTENT (ng/g) CONGENER # # # # # # # #
CONTROL CHOW
196+203 198 201 205 206 207 208 209
PACIFIC COHO
ND 0.14 ND hid ND ND ND ND
ND ND ND ND ND ND ND ND
L. ERIE COHO
L. MICHIGAN COHO
4.6 ND 5.9 ND ND ND ND ND
6.0 ND 5.3 ND ND ND ND ND
L. ONTARIO COHO 28 ND 23.0 ND 6.1 ND 3.6 ND
(ND : not detected)
TABLE 3 GAS CHROMATOGRAPHIC ANALYSIS OF HALOGENATEDAROMATIC HYDROCARBON LEVELS IN C57BI/6 MOUSE LIVER TISSUE AFTER A FOUR MONTH DIETARY EXPOSURE TO COHO SALMON HALOGENATEDAROMATIC HYDROCARBON CONTENT (ng/g) CONTROL CHOW
PACIFIC COHO
2-CB
ND
ND
3-CB
ND
COMPOUND
6.3+/-2.5 (8.1%)
L. ERIE COHO ND ND
L. MICHIGAN COHO
L. ONTARIO COHO
ND
ND
18+/-1.0 1.9%)
9.6+/-9.6 (0.1%)
4-CB
0.7+/-0.3 (1.9%)
1.6+/-0.8 (2.5%)
4.0+/-0.8 (0.3%)
19+/-4.8 1.9%)
31+/-13 (0.6%)
5-CB
4.2+/-2.8 (9.8%)
15+/-3.6 (18.6%)
68+/-3.0 (4.4%)
120+/-4.0 13.5%)
290+/-110 (6.6%)
6-CB
2.6+/-1.5 (6.5%)
5.7+/-1.2 (7.1%)
160+/-2.6 (10.9%)
120+/-5.9 12.1%)
860+/-150 (21.9%)
7-CB
40+/-4.2 (80.6%)
49+/-6.8 (64.5%)
1200+/-94 (79.6%)
590+/-40 52.2%)
2500+/-430 (63.1%)
8-CB
2.1+/-1.6 (1.3%)
0.2+/-0.2 (0.2%)
64+/-1.6 (4.2%)
44+/-1.5 4.8%)
240+/-42 (6.2%)
9-CB
ND
ND
8.8+/-0.2 (O.6%)
8.2+/0.9 0.9%)
42+/-8.9 (1.0%)
10-CB
ND
ND
0.2+/-0.2 (0.0%)
0.7+/-0.2 0.1%)
12+/-3.8 (0.3%)
TOTAL PCB'S % Cl
50+/-5.9 61.5
78+/-13 59.0
1500+/-100 62.2
930+/-42 60.7
4000+/-740 61.5
TOTAL TOXI C PCB's
17+/-2.1
30+/-5.2
560+/-44
350+/-33
1200+/-230
c o n t ' d .....
415
PERCENT TOXIC PCB's
34
38
37
38
30
HCB a-BHC Lindane Mirex OCS g-Cl pp-DDE pp-DDD pp-DDT
1.3+/-0.9 ND ND ND ND ND 1.8+/-0.2 ND ND
2.6+/-0.1 0.8+/-0.1 ND 1.1+/-0.4 ND ND 2.8+/-0.4 0.7+/-0.1 ND
2.3+/-0.1 ND ND 4.8+/-0.1 2.9+/-0.1 ND 1.9+/-0.1 ND k~
2.3+/-0.3 ND ND 5.7+/-0.2 0.2+/-0.2 ND 47.8+/-6.2 1.7+/-0.3 ND
20+/-2.7 ND hid 700+/-140 24.0+/-8.1 ND 235.0+/-49.7 ND ND
( = toxic PCB's #81, 105, 118, 126, 128, 138, 156, 157, 158, 166, 170, and 189) (ND = not detected; n = 4; mean +/- SEM)
TABLE 4
GAS CHROMATOGRAPHIC PCB CONGENER ANALYSIS OF C57BI/6 MOUSE LIVER TISSUE AFTER A FOUR MONTH DIETARY EXPOSURE TO COHO SALMON PCB CONGENER CONTENT (ng/g) CONGENER
CONTROL CHOW
PACIFIC COHO
L. ERIE COHO
L. MICHIGAN COHO
L. ONTARIO COHO
# # # # # # # # # # # # # # # # # # # # # # #
ND ND ND ND 0.7+/-0.3 ND ND ND ND ND ND ND ND ND ND
6.3+/-2.5 ND ND ND i. i+/-0.5 ND ND 0. i+/-0.1 ND ND ND ND ND 0.4+/-0.4 ND
ND ND ND ND 2.0+/-0.4 ND ND 0.2+/-0.2 ND ND 1.9+/-0.7 ND ND ND ND
17.6+/-9.5 ND ND ND 7.6+/-3.1 ND ND 0.8+/-0.2 ND 3.1+/-0.6 2.4+/-0.6 ND ND 4.6+/-0.5 ND
8.0+/-8.0 ND i. 5+/-i. 5 ND i0.0+/-7.3 i. 4+/-1.4 i. 7+/-1.7 3.7+/-1.3 i. 2+/-1.2 3.3+/-3.3 7.3+/-2.9 ND ND 0.7+/-0.7 ND ND 45.0+/-6.9 0.7+/-0.7 i. i+/-i. 1 ND 2.2+/-2.2 ND 57.5+/-57.5
32 40 42 44 47+75 49 52 61 64 66 70 71 78+109 81 82 84
86 87+112 91 92 95 97 99
ND
2.9+/-0.2 ND ND ND ND ND 0.6+/-0.6
(ND = not detected) (n = 4; mean +/- SEM)
ND
6.4+/-1.0 ND ND ND ND ND 6.7+/-1.1
ND
14.0+/-1.5 ND 0.6+/-0.2 ND ND ND 30.0+/-0.9
ND
35.5+/-5.3 0.5+/-0.5 i. I+/-0.4 ND ND ND 40.8+/-13.6
416
TABLE 4 (continued) GAS CHROMATOGRAPHIC PCB CONGENER ANALYSIS OF C57BI/6 MOUSE LIVER TISSUE AFTER A FOUR MONTH DIETARY EXPOSURE TO COHO SALMON PCB CONGENER CONTENT (ng/g) CONGENER
CONTROL CHOW
PACIFIC COHO
L. ERIE COHO
L. MICHIGAN COHO
L. ONTARIO COHO
# # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # #
ND ND ND 0.5+/-0.5 ND 0.7+/-0.3 i. 0+/-0.3 14.9+/-1.3 ND ND 0.2+/-0.2 ND ND 2.4+/-0.6 0.3+/-0.3 ND ND ND ND i. i+/-0.6 ND ND ND ND ND 13.6+/-1.5 ND ND 0.7+/-0.4 ND
ND 0.6+/-i. 7 0.5+/-0.5 0.6+/-0.6 ND i. i+/-0.1 0.9+/-0.3 27.0+/-3.4 ND ND 0.2+/-0.2 i. 0+/-0.3 ND 4.4+/-0.8 0.3+/-0.3 ND ND ND ND i. 0+/-0.6 ND ND ND ND ND 17.3+/-2.3 0.5+/-0.3 ND 1.6+/-0.3 ND
ND 6.3+/-1.7 ND 12.3+/-1.0 ND 9.0+/-0.4 ND 477.5+/-42.5 ND ND 0.7+/-0.2 34.5+/-0.6 ND 106.3+/-3.8 10.9+/-1.7 2.8+/-0.1 ND 4. I+/-0.2 3.8+/-0.1 41.3+/-0.6 ND 13.8+/-0.6 ND 9.3+/-3.1 58.3+/-1.4 537.5+/-47.7 24.8+/-1.1 ND 53.5+/-1.8 i. i+/-0.0
i. 0+/-i. 0 17.0+/-4.5 ND 23.8+/-2.3 ND 12.0+/-i. 3 Ii. i+/-i. 7 255.0+/-22.5 i. 0+/-0.4 ND ND 27.0+/-2.4 ND 75.3+/-3.1 10.7+/-0.5 2.7+/-0.1
i. 2+/-1.2 90.0+/-25.0 ND 136.0+/-38.3 16.8+/-16.8 54.5+/-8.5 13.8+/-2.1 752.0+/-129.4 i. 6+/-1.6 i. i+/-i. 1 5.0+/-5.0 167.5+/-25.9 ND 527.5+/-79.6 38.5+/-16.4 19.0+/-3.0 ii. 9+/-2.7 23.5+/-3.9 29.5+/-4.9 129.8+/-20.7 ND 63.8+/-10.3 ND 56.0+/-19.0 272.5+/-44.6 760.0+/-154.8 107.0+/-16.5 ND 312.5+/-51.7 7.9+/-2.9 22.5+/-5.0 53.8+/-9.4 17.8+/-2.9 73.0+/-12.2 23.0+/-4.8 74.8+/-12.5 ND 28.0+/-6.3 ND 12.3+/-1.9 ii. 5+/-3.9
101 105 ii0 118 126 128 130 138 141 143 144 146 151 153 156 157 158+186 166 167 170 171+202 172 174 177 178 180 183 185 187 189 192 194 195 196+203 198 201 205 206 207 208 209
ND
ND ND 0.6+/-0.2 ND ND ND ND ND ND ND
(ND = not detected) (n = 4; mean +/- SEM)
ND
2.9+/-0.3
ND ND 0.2+/-0.2 ND ND ND ND ND ND ND
12.5+/-0.3 5.7+/-0.2 20.3+/-1.1 6.2+/-0.4 19.3+/-0.3 ND 5.6+/-0.2 ND 3.2+/-0.2 0.3+/-0.3
0.5+/-0.1 2.7+/-0.1 3.4+/-0.3 24.3+/-1.9 ND 9. i+/-0.2 ND 3.8+/-2.2 32.0+/-2.3 195.0+/-11.9 15.8+/-1.1 ND 36.8+/-1.9 0.7+/-0.2 ND
9.5+/-0.1 3.3+/-0.3 14.5+/-0.5 3.7+/-0.3 13.0+/-0.4 ND 5.3+/-0.4 ND 2.7+/-0.4 0.7+/-0.2
417
TABLE 5 GAS CHROMATOGRAPHIC ANALYSIS OF HALOGENATEDAROMATIC HYDROCARBON LEVELS IN DBA/2 MOUSE LIVER TISSUE AFTER A FOUR MONTH DIETARY EXPOSURE TO COHO SALMON HALOGENATEDAROMATIC CONTROL CHOW
PACIFIC COHO
2-CB
ND
ND
3-CB
ND
4-CB
ND
5-CB
ND
COMPOUND
1.5+/-1.5 (6.3%) ND
HYDROCARBON LEVEL (ng/g) L. ERIE COHO ND 22+/-8.0 (4.8%)
L. MICHIGAN COHO
L. ONTARIO COHO
ND
ND
ND
0.8+/-0.7 0.O%)
14+/-3.6 (2.7%)
3.1+/-0.7 (0.6%)
46+/-15 1.2%)
2.9+/-1.1 (16.0%)
84+/-14 (17.1%)
35+/-6.7 (6.5%)
560+/-92 16.2%)
6-CB
1.1+/-0.4 (19.1%)
4.8+/-1.2 (29.8%)
90+/-11 (18.4%)
120+/-5.9 (22.7%)
770+/-130 22.2%)
7-CB
4.2+/-0.6 (80.9%)
7.3+/-0.8 (46.0%)
250+/-34 (50.0%)
320+/-17 (61.7%)
1900+/-330 54.0%)
8-CB
ND
0.03+/-0.02 (1.9%)
28+/-4.5 (5.7%)
38+/-2.2 (7.3%)
180+/-28 5.2%)
9-CB
ND
ND
6.2+/-0.8 (1.3%)
5.9+/-0.3 (1.1%)
33+/-6.0 1.0%)
10-CB
ND
ND
0.6+/-0.3 (0.1%)
0.9+/-0.1 (0.2%)
10+/-3.4 0.3%)
5.3+/-0.9
17+/-2.3
480+/-64
530+/-31
3500+/-600
59.0
59.5
61.1
60.6
2.0+/-0.3
3.9+/-0.5
160+/-22
150+/-11
1100+/-190
38
23
33
28
31
0.4+/-0.1 ND ND ND ND ND i. 0+/-0.1 0.4+/-0.1 ND
2.3+/-0.4 0.8+/-0.1 ND ND ND ND 2.9+/-0.4 0.6+/-0.1 ND
2.2+/-0.2 ND ND 7. i+/-I. 1 0.8+/-0.1 ND 58+/-8.6 i. 5+/-0.2 ND
2.4+/-0.3 ND ND 3. i+/-0.2 2.8+/-0.3 ND 2. i+/-0.3 0.2+/-0.1 ND
15+/-2.5 ND ND 490+/-75 34+/-4.9 ND 280+/-45 i. 7+/-1.7 ND
TOTAL PCB' s % Cl TOTAL TOXIC PCB' s PERCENT TOXIC PCB' s HCB a-HCB Lindane Mi rex OCS g-Cl pp-DDE pp-DDD pp-DDT
62.1
( = toxic PCB's #81, 105, 118, 126, 128, 138, 156, 157, 158, 166, 170 and 189) (ND = not detected; n = 4; mean +/- SEM)
418 TABLE 6 GAS CHROMATOGRAPHIC PCB CONGENER ANALYSIS OF DBA/2 MOUSE LIVER TISSUE AFTER A FOUR MONTH DIETARY EXPOSURE TO COHO SALMON PCB CONGENER CONTENT (ng/g) CONGENER
# # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # #
CONTROL CHOW
PACIFIC COHO
L. ERIE COHO
L. MICHIGAN COHO
L. ONTARIO COHO
22.0+/-8.0 ND ND ND ND i. 3+/-0.7 ND 0.7+/-0.7 ND 2.2+/-0.4 ND 5.4+/-1.3 2.2+/-0.3 ND ND 1.8+/-0.3 ND
ND ND ND ND ND ND ND ND ND 0.5+/-0.1 ND ND 1.6+/-0.3 ND ND ND ND
ND ND 3.5+/-2.0 ND ND 8.3+/-3.8 i. 9+/-0.7 3.2+/-1.8 ND 15.3+/-11.9 1.1+/-0.6 12.8+/-7.4 6.4+/-2.4 1.4+/-0.8 hiD 2.4+/-1.5 ND I. 8+/-1.8 33.0+/-5.4 i. 9+/-1.1 3. i+/-i. 7 ND i. 6+/-1.6 1.1+/-0.7 200.0+/-29.2
32 40 42 44 46 47+75 49 52 53 61 64 66 70 71 78+109 81 82
ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND
1.5+/-1.5 ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND
84
ND
ND
86 87+112 91 92 95 97 99 i01 105 ii0 118 126+129 128 130 138 141 143 144 146 151 153 156 157 158+186 166 167 170 171+202 172 174 177 178 180 183 185 187 189 192 194 195 196+203 198
ND ND ND ND ND ND ND ND ND ND ND ND 0.4+/-0.1 ND 1.7+/-0.2 ND ND ND ND ND 1.1+/-0.4 ND ND ND ND ND ND ND ND ND ND ND 1.7+/-0.1 ND ND 0.5+/-0.2 ND ND ND ND ND ND
ND ND ND ND ND ND 2.8+/-1.2 ND ND ND ND ND 0.6+/-0.0 ND
3.3+/-0.4 ND ND ND 0.2+/-0.2 ND 3.0+/-0.4 ND ND ND ND ND ND ND ND ND ND ND 2.3+/-0.3 ND ND i. 2+/-0.2 ND ND ND ND ND ND
ND
6.6+/-1.4 0.9+/-0.5 i. i+/-0.2 ND ND ND 39.3+/-5.1 ND 15+/-2.6 0.7+/-0.1 20.5+/-1.8 ND 9.6+/-1/1 2.8+/-0.4 83.0+/-11.1 0.7+/-0.4 0.5+/-0.2 ND 17.5+/-2.1 ND 57.8+/-8.3 8.6+/-0.9 2.3+/-0.4 4.7+/-0.6 1.7+/-0.2 2.9+/-0.8 15.5+/-4.1 ND 5.9+/-0.9 3.3+/-0.5 ND 14.8+/-2.3 69.0+/-10.4 11.1+/-1.5 ND 28.5+/-3.9 1.4+/-0.3 ND 6.6+/-1.1 1.9+/-0.1 9.8+/-1.6 1.1+/-0.4
ND
0.8+/-0.3 ND 0.5+/-0.2 ND ND ND 16.0+/-5.6 ND 4.5+/-0.8 ND 9.3+/-1.1 ND 6.9+/-0.7 1.5+/-1.1 93.8+/-5.8 ND ND 7.5+/-0.1 20.0+/-1.8 ND 76.8+/-3.1 6.6+/-2.4 2.1+/-0.1 4.4+/-0.3 1.8+/-0.1 3.6+/-0.1 21.3+/-1.8 ND 8.4+/-0.5 ND 9.4+/-0.6 27.3+/-1.4 104.0+/-5.6 14.8+/-0.8 ND 41.0+/-i. 7 0.9+/-0.1 4.5+/-0.2 9.3+/-0.6 2.7+/-0.3 12.0+/-0.8 1.9+/-0.0
ND 120.0+/-49.0 i. 5+/-0.5 220.0+/-33.9 16.0+/-9.7 51.5+/-6.9 10.8+/-3.6 565.0+/-99.2 I. 6+/-0.8 i. 9+/-1.1 7.0+/-4.0 142.0+/-21.5 0.3+/-0.3 512.0+/-96.8 46.8+/-7.9 17.5+/-3.1 30.8+/-5.6 ii. 5+/-2.9 34.3+/-5.8 112.5+/-18.8 ND 41.8+/-6.9 0.3+/-0.2 52.0+/-15.0 148.8+/-22.4 557.5+/-107.5 91.8+/-12.9 ND 280.0+/-51.1 3.4+/-1.9 18.3+/-4.2 44.8+/-6.5 12.0+/-I. 9 60.0+/-8.3 4.4+/-2.6
419
TABLE 6 (continued) GAS CHROMATOGRAPHIC PCB CONGENER ANALYSIS OF DBA/2 MOUSE LIVER TISSUE AFTER A FOUR MONTH DIETARY EXPOSURE TO COHO SALMON PCB CONGENER CONTENT (ng/g) CONGENER
CONTROL CHOW
# 201 205 # 206 # 207 # 208 # 209
ND ND ND ND ND ND
PACIFIC COHO
L. ERIE COHO
L. MICHIGAN COHO
L. ONTARIO COHO
0.2+/-0.1 ND ND ND ND ND
8.5+/-1.2 ND 3.8+/-0.6 0.4+/-0.2 2.0+/-0.1 0.6+/-0.3
12.3+/-0.6 ND 3.9+/-0.2 ND 1.9+/-0.1 0.9+/-0.1
54.5+/-8.1 i. 9+/-1.1 20.1+/-2.9 3.9+/-2.2 9.2+/-1.4 i0.3+/-3.4
(ND = not detected) (n = 4; mean +/- SEM)
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0045-6535/88 $ 3 . 0 0 + .OO P e r g a m o n J o u r n a l s Ltd.
BIOACCUMULATION OF HALOGENATEDAROMATIC
HYDROCARBONS
IN C57BI/6 AND DBA/2 MICE FOLLOWING CONSUMPTION OF GREAT LAKES COHO SALMON (ONCORHYNCHUS KISUTCH)
Glenn B. Cleland*, Barry G. Oliver and Ronald A. Sonstegard *Department of Pathology, McMaster University, Hamilton, Ontario, L8N 3Z5 Canada (GBC); National Water Research Institute, Canada Centre for Inland waters, Burlington, Ontario, L7R 4A6, Canada (BGO); Department of Comparative Medicine, School of Veterinary Medicine, Tufts University, Grafton, MA, 01536, USA (RAS).
ABSTRACT A gradation of polychlorinated biphenyl isomer and congener levels were found in coho salmon from Lakes Erie, Michigan and Ontario. A similar bioaccumulation pattern was observed in mouse livers following consumption of Great Lakes fish and, in general, the levels were higher in C57BI/6 than in DBA/2 mice. INTRODUCTION Halogenated
aromatic
hydrocarbons
(HAHs)
have
been
shown
to
bioaccumulate
and
bioconcentrate in fish via both dietary exposure (Borgmann and Whittle, 1983) and gill exchange (Oliver and Niimi, 1983).
One of the most significant human chronic exposures to HAHs involves
the consumption of fish from contaminated lakes and streams by 1982).
Great Lakes salmon
consumers reportedly eat 24 to
sport fishermen (Cordle et al.,
25 ib of fish per year, with
upper
limits reaching 180 ib and one reported annual consumption of 260 ib (Cordle et al., 1982). In mice and rats, the toxicity
responses to HAHs are believed to be determined by the
gene locus which codes for a cytosolic receptor (Poland and Knutson, 1982; Okey, 1983).
Ah
Poland
and Knutson (1982) have suggested that HAH toxicity may be mediated through the Ah receptor and that the
initial event
is the stereoscopic
C57BI/6 (B/6) strain of mouse
recognition and
has been shown to be
binding by this
receptor.
Ah+ and therefore more susceptible to
The HAH
toxicity whereas the DBA/2 (D/2) strain of mouse has been shown to be Ah- and consequently more resistant to
HAH exposure
(Poland and
Knutson,
1982;
Silkworth and
Grabstein, 1982;
Okey,
1983). This study was designed to provide comprehensive baseline determinations of polychlorinated biphenyl (PCB) isomers and pollutants)
congeners (as well as several other
the levels of organochlorine
in coho salmon from three of the Great Lakes and from the Pacific Ocean.
dietary exposure to
these fish, the
subsequent levels and
Following
bioaccumulation patterns of
these
pollutants were examined and compared in liver tissues of C57BI/6 (Ah+) and DBA/2 (Ah-) mice.
405
406
MATERIALS AND METHODS
MICE: Three week
old
weanling male
Laboratory (Bar Harbor, Me.).
C57BI/6 and
Mice were
DBA/2
mice were
housed five-to-a cage
obtained from
the
Jackson
on a twelve hour daily
light
cycle and fed control or fish-supplemented diets and water ad libitum for four months. DIETS: Adult coho salmon (Oncorhynchus kisutch) were obtained during the 1982, fall spawning runs from Lake Ontario (Credit River, Streetsville, Ont.), Lake Erie (Walnut Lake Michigan
(Platte River,
Alaskan Seafoods
Honor, Mi.)
Inc., Kodiak,
Al.
and Pacific
Fish were
Creek, Fairview, Pa.),
Ocean coho salmon
beheaded, eviscerated
were obtained
and minced
from
in a
meat
grinder. Powdered rodent chow (Purina No. 5001) was supplemented with 33% (based on the dry wt of fish). No. 40060), i0 mg/kg of minerals,
(Teklad No. 170710),
thiamine (Swiss) to ensure nutritional quality. fish.
Diets were mixed
-20°C.
pooled coho salmon mince
Mouse diets were fortified with I0 mg/kg of vitamins,
Control mice were fed rodent
4.5% corn oil (Mazola), and I00 mg/kg of
All additives were
in a commercial food mixer
(Teklad
based on the dry weight of
(Hobart), pelletized and stored frozen
pellets (Purina No. 5001).
Mice were fed ad libitum
at for
four months. HALOGENATEDAROMATIC Ten, fifteen preparation.
HYDROCARBON ANALYSIS OF COHO SALMON ANDMOUSE TISSUES:
gram
samples were
taken
at random
from
each
pooled coho
salmon
mince
The samples from each coho salmon source were pooled, and total lipid levels were
determined by the were extracted
chloroformmethanol extraction method
and analyzed
by gas
of Bligh and
chromatography (GC)
to determine
Dyer (1959). a profile
Specimens of the
HAH
liver) tissues were ground in Na2SO 4 and soxhlet extracted
for
contaminants by the method described by Oliver and Nicol (1982). The coho salmon (or mouse 24 hours
with
hexane/acetone
distilled water to remove the Snyder condensor.
The bulk
(41:59).
The samples
then extracted
acetone, and evaporated to approximately lipid was removed
minute with 3 ml of high purity H2SO 4 in a passage through a 2.5
were
cm layer of
by shaking the
with 1
litre
30 ml using a 3
of
stage
extract for approximately
one
stoppered flask, and then the hexane layer dried by
Na2SO 4 in a
filter funnel.
Following re-evaporation,
the
extracts were further purified by passage through a H2SO4/silica gel column. The analyses utilized
dual capillary
chromatograph equipped with
columns (30m, OVl
electron capture detectors.
and SE54) on
The carrier
a Varian 3700
gas was helium
gas
(linear
velocity 30 cm/s) and the temperature program was 50°C to 250°C at l°/min. A total
of
91
chlorinated compounds gamma-chlordane
were
including
(pp-DDE),
2,2-bis-(p-chlorophenyl)-l,l-dichloroethane
-2,2,2-trichloroethane (mirex),
(pp-DDT),
Hexachlorobenzene
2,2-bis-(p-chlorophenyl)-l, (pp-DDD),
dodecachlorooctahydro-
gamma-hexachlorocyclohexane
as octachlorostyrene
(g-Cl),
measured.
pesticides,
seven
l,l-bis-(p-chlorophenyl)
1,3,4-metheno-2H-cyclobutopentalene
(lindane) and alpha-hexachlorocyclohexane
(OCS) and 82 individual PCB congeners were quantified.
compounds were used for instrument calibration.
(HCB),
l-dichloroethylene
The other isomers
(a-BHC), as well For PCBs, 53 pure
were tentatively identified
from the chromatograms and retention indices of Safe et al.
(1983) and Mullin et al. (1984) by
running Aroclor
same
1260,
1254,
and 1016
mixtures
with the
column (SE54)
at
the
same
407
temperature program rate. by
using
the
Aroclors
composition data of
Detector as
response factors (RFs) for unavailable isomers were
secondary
Mullin (1985).
standards
The
and
employing
total PCBs in
Aroclor
weight
found
percentage
Environmental Protection Agency
standard Aroclors 1242, 1248, 1016, 1254, and 1260 determined by
(EPA)
stmm~ing the concentrations of
individual congeners, agreed with the reference value to better than +/- 10%. The approximate compotmd
detection limits for the
material in the sample extracts
mouse livers, based
detected at a signal to
for di- and trichlorobiphenyls, 0.2 to .05 ng/g for the pesticides.
Control
mouse
chow
specimens were
on the amount
noise ratio of 5:1, were: ca. i
of ng/g
other PCBs and 0.i to 0.2 ng/g for the
concentrated
by 20-fold
to
provide
more
sensitive detection. The PCB isomer and congener numbering system of Ballschmiter and
Zell (1980) was used for
brevity.
RESULTS GAS CHROMATOGRAPHIC ANALYSIS OF HALOGENATED AROMATIC HYDROCARBON CONTENT OF COHO SALMON USED AS DIETARY SUPPLEMENTS FOR LABORATORY ANIMALS: Gas chromatographic analysis of the coho salmon used as dietary supplements for laboratory animals indicated that Pacific Ocean
coho salmon contained a total PCB content of 20 ng/g
Lake Ontario coho salmon contained 2900 ng/g (Table i). Michigan, the
greatest proportion
heptachlorobiphenyls (7-CB)
of the
PCBs were pentachlorobiphenyls
and hexachlorobiphenyls
and
In coho salmon from Lakes Ontario and
(6-CB).
greatest proportion of PCBs were 7-CB followed by 5-CB and Ocean contained mostly 5-CB followed by 6-CB and 7-CB.
In
6-CB.
(5-CB) followed
Lake Erie
coho salmon
by the
Coho salmon from the Pacific
This profile was also reflected in the
total percent chlorination of the PCBs which is similar in all four coho salmon groups (56.7% 59.1%). Isomeric analysis
of
the
PCB
content of
coho
salmon
used as
diet
supplements
for
laboratory animals (Table 2) revealed that the Lake Ontario coho salmon contained higher levels of all isomers seen in
other fish groups.
The
following PCB congeners were analyzed but
detected in either the coho salmon used as diets or the four month exposure:
#4, #6, #7, #8, #15+18,
not
in B/6 or D/2 mouse liver tissue following #16, #17, #19, #22, #24, #25, #26,
#28+31,
#32, #36+45, #46, #53 and #136. Hexachlorobenzene was detected in coho salmon from the Pacific Ocean (2.8 ng/g), Lake Erie (1.3 ng/g), Lake Michigan (2.5 ng/g) and Lake Ontario (9.1 ng/g).
Coho salmon from the Pacific
Ocean were the only specimens which contained detectable levels of a-BHC (8 ng/g). not detected in any of the fish (150 ng/g).
The
pesticides
distribution of low levels in
Lindane was
examined and mirex was found only in salmon from Lake pp-DDE
and
pp-DDT
followed
a pattern
similar
to
Ontario the
Pacific Ocean eoho salmon followed by increasing levels in
salmon from Lakes Erie, Michigan and Ontario.
PCB coho
Lake Erie coho salmon contained higher levels of
pp-DDD than Lake Michigan coho salmon, but both were less
than levels detected in Lake Ontario
coho salmon (27 ng/g). Analysis of control
Purina mouse
chow revealed very
low levels of
PCBs (0.4 ng/g)
and
pesticide residues (Table I). The total percentage of body
lipid was greatest in tissue from Pacific Ocean coho
(4.2%) and least (1.6%) in Lake Erie eoho salmon (Table I).
salmon
408
EFFECT OF DIETARY
EXPOSURE TO
HALOGENATED AROMATIC HYDROCARBON
CONTAMINATED COHO SALMON
FOR
FOUR MONTHS ON ORGANOCHLORINE LEVELS IN C57BI/6 AND DBA/2 MOUSE LIVER TISSUE:
Following a four month dietary exposure to coho salmon, soxhlet C57BI/6 and DBA/2 mice were analyzed by gas chromatography for (2-CB) were not
found in
trichlorobiphenyls were found in
either B/6 or
(3-CB) were
B/6 mice
D/2 mouse
not found in
which were fed
extracted liver tissue of
HAH content.
livers (Table 3,
coho salmon tissue
coho salmon
4, 5
Although
(Table i), detectable
from the Pacific
Michigan (18 ng/g), Lake Ontario (9.6 ng/g; Table 3), and
Dichlorobiphenyls and 6).
levels
ocean (6.3 ng/g),
Lake
in D/2 mice which consumed Lake Erie
coho salmon (22.0 ng/g, Table 5). Tetrachlorobiphenyls
(4-CB) occurred in liver
extracts of B/6 mice in all dietary
with the highest levels in the Lake Michigan (19 ng/g) fed mice (Table 3).
groups
and Lake Ontario (31 ng/g) coho salmon-
The 4-CB isomers were also detected in D/2 mice which were fed salmon from
all of the Great Lakes
with the highest levels occurring
Ontario (46 ng/g) groups (Table
5).
It was interesting to note that the 4-CB
pattern in mice did not follow the distribution in the tissue levels of 2.0 ng/g
in the Lake Erie (14 ng/g) and
Lake
bioaccumulation
dietary coho salmon (Table i) which had
(Lake Erie), 130 ng/g (Lake Michigan), and 260 ng/g (Lake
Ontario).
The 4-CB which bioaceumulated to the highest level in B/6 mice which consumed Lake Michigan and Lake Ontario coho salmon was
PCB #47+75 (Table 4).
mice which consumed Lake Ontario isomers #61, #66, and
Isomer #47+75 also bioaccumulated in
coho salmon as did isomers
#70 were also
#61, #66 and #70 (Table 6).
primarily responsible for
D/2 PCB
the 4-CB content in Lake
Erie
salmon-fed D/2 mice (Table 6). Pentachlorobiphenyl
(5-CB)
isomers were detected
dietary groups (Table 3), as well as in all levels in B/6 mice
followed a similar
with the lowest levels in the Lakes Erie (68 ng/g)
Ocean coho salmon
5-CB isomers which accounted
3).
the Lake Erie salmon consumers
it's co-migrating
coho salmon, 120
5-CB
in both B/6
congener #129
lowest
and 6).
It
Michigan and 210 ng/g
it was not detected in
in Lake Ontario
either B/6 or D/2 mice (Tables 4 and
was 57 coho 6).
consumption of coho salmon from Lakes
Erie and (12.3 ng/g), Michigan (23.8 ng/g) and Ontario (136.0 which were fed coho salmon
#86,
parallel
For example, PCB isomer #i01 was found at levels of ng/g in Lake
Lake
The individual
and D/2 mice included (Tables 4
in fed
Ontario
had 84 ng/g and the
liver tissue (Table 5).
In contrast, isomer #118 was found in B/6 mice following also detected in D/2 mice
in the Lake
bioaccumulation pattern of 5-CB isomers in mice did not
that seen in the dietary coho salmon. salmon tissue (Table 2), yet
and the highest
all
salmon
In DBA/2 mice the 5-CB levels were also
for the bioaccumulation
#126 with
interesting to note that the ng/g in Lake Erie
The
levels in dietary coho
and the highest levels in B/6 mice
diet group (2.9 ng/g)
salmon-fed group (560 ng/g), however
#118 and
mice from
Pacific Ocean salmon-fed B/6 mice (15 ng/g), intermediate levels and Lake Michigan (120 ng/g)
Michigan coho salmon-fed D/2 mice had 35 ng/g in their
#99, #105,
tissue of B/6
D/2 mice which were fed fish (Table 5).
distribution pattern to
Lake Ontario coho salmon (290 ng/g; Table in the Pacific
in liver
ng/g, Table 4).
Isomer ~I18 was
from Lakes Erie (20.5 ng/g) or
Michigan
(9.3 ng/g) and especially Lake Ontario (220.0 ng/g, Table 6). Hexachlorobiphenyls
(6-CB) were detected at similar levels in liver extracts from both B/6
and D/2 strains of mice within most dietary groups (Tables 3 and 5). the 6-CBs which accounted
primarily for the bioaeeumulation
In both B/6 and D/2 mice,
were isomers #138, #146 and
#153
409
(Tables 4 and 6). The heptachlorobiphenyl detected in
B/6 and
D/2
(7-CB)
mice in
isomers accounted all dietary
salmon-fed mice had
the highest 7-CB
ng/g, Table 5) mice.
However, it
for
50% or
groups (Tables
levels in both B/6
more
3 and
of the
5).
(2500 ng/g, Table
was interesting to note that
total
The Lake
PCBs
Ontario
3) and D/2
(1900
B/6 mice which were fed
Lake
Erie coho salmon had 7-CB levels of 1200 ng/g (Table 3), whereas similarly fed D/2 mice had 250 ng/g (Table 5).
The 7-CB isomer #180 was in the highest concentration in both B/6 and D/2 mice
(Tables 4 and 6).
This isomer reached levels of
(Table 4).
7-CBs which
Other
isomers #170, #178, #183 and
accounted for
#187.
537.5 ng/g in Lake Erie salmon-fed B/6
the bioaccumulation
The isomer #189
(3.4 ng/g) Lake Ontario salmon-fed mice
in B/6 and
mice
D/2 mice
were
was found in both B/6 (7.9 ng/g) and
D/2
(Tables 4 and 6), although it was not detected in
the
dietary fish (Table 2). Most octachlorobiphenyl
(8-CB) isomers were detected at similar levels in B/6 and D/2 mice
which were fed coho salmon from Lakes Michigan and Ontario. was found at
23.0 ng/g
in B/6 mice
Ontario salmon (Tables 4 and 6).
In
and 4.4 ng/g
An exception was isomer #198 which
in D/2 mice
following consumption of
Lake
B/6 mice which were fed Lake Erie coho salmon diets,
8-CB isomers #194, #196 (and eo-eluting isomer #203) and #201
the
reached levels of 12.5, 20.3 and
19.0 ng/g respectively in B/6 mice (Table 4), and 6.6, 9.8, and 8.5 ng/g in D/2 mice (Table 6). The nonachlorobiphenyls Great Lakes coho salmon isomer (#209)
(9-CBs) reached similar levels in both strains of mice within each
dietary group (Tables 3 and
was found
Ontario coho salmon-fed
to an
5).
appreciable level in
groups (Tables 3
and 5).
The sole decachlorobiphenyl
both strains
Isomer
of mice only
#209 was not
(10-CB)
in the
Lake
detected in the
body
tissue of Lake Ontario salmon (Table i). The C57BI/6
mice which
burden of 4000 ng/g (Table
were fed
Lake Ontario
3) and DBA/2 mice fed
total PCB
liver
the same diet had a similar total PCB
salmon bioaccumulated a
liver
level of 3500 ng/g (Table 5), while the total PCB level in the dietary Lake Ontario coho salmon was 2900 ng/g (Table ng/g (Table i).
i).
Coho
salmon from Lake Michigan contained
Lake Michigan salmon-consuming
(Table 3) while D/2 mouse livers had liver contained a total PCB
B/6 mice accumulated
530 ng/g (Table 5).
a total PCB level of
860
930 ng/g of total
PCBs
Lake Erie coho salmon-fed B/6
mouse
concentration of 1500 ng/g (Table 3) and D/2 liver contained
only
480 ng/g (Table 5), while body tissue from Lake Erie coho salmon had 500 ng/g (Table i). noteworthy that the PCB congeners found in liver tissue of
It is
B/6 mice which were fed coho salmon
from Lake Ontario were always present in equal or greater concentration than those found in the livers of other B/6 dietary
groups, with the possible exception
of congener #32 (Table 4
and
6). Hexachlorobenzene
(HCB) was found in liver tissue of mice at
levels which were similar to
those detected in dietary coho salmon (Table i), except in Lake Ontario coho salmon-fed B/6 and D/2 mice where the HCB levels reached 20.3 and 15.0 ng/g respectively (Tables 3 and 5). other pesticides examined, a-BHC, lindane,
g-Cl and pp-DDT were not
which were fed Great Lakes coho salmon (Tables 3 and 5). diet in which mirex was detected (Table i). liver tissues of both
However,
Of the
detected in livers of mice
Lake Ontario coho salmon was the only
detectable levels of mirex were found in
mouse strains following dietary consumption
of coho salmon from any
the Great Lakes examined, with
the highest concentrations occurring in B/6 (700 ng/g) and
(490
fed Lake
ng/g)
mice
which
were
Ontario
salmon
(Tables
3
and
5).
The
of D/2
highest
410
levels of OCS were
found in B/6
from Lake
(Tables 3
Ontario
(24 ng/g) and D/2 (34
and
distribution pattern in livers of
5).
The
pp-DDE was
the two mouse strains.
from Lake Erie, the pp-DDE levels in B/6 in Lake Michigan coho
ng/g) mice which consumed coho
pesticide
found in
an
salmon
interesting
In mice which were fed coho
salmon
mice were 1.9 ng/g, and in D/2 mice 58 ng/g,
salmon-fed mice, the
B/6 strain had 48 ng/g
while in the Lake Ontario salmon-fed mice, the B/6 strain
whereas
and the D/2 had 2.1
ng/g,
had 240 ng/g and the D/2 had similar
280.0 ng/g level of pp-DDE (Tables 3 and 5). DISCUSSION A gradation of PCB concentrations the Great Lakes. Erie and
was found in the body tissue of adult coho salmon
from
The lowest level occurred in salmon from the Pacific Ocean, followed by Lakes
Michigan
with the
analysis of the PCB
highest concentration
in
body burdens similarly indicated
the highest levels of all
isomers and congeners and the
other chemicals studied. total organochlorine
Lake Ontario
The
coho salmon.
Isomeric
that Lake Ontario coho salmon
contained
highest levels of all but one of
PCB congener analysis confirms and expands a report of
levels
in
Lake
Ontario
salmon
(Sonstegard
and
Leatherland,
Similarly, Villeneuve et al. (1981) fed Sprague-Dawley rats diets containing
the
elevated 1978).
5.8% Lake Ontario
salmon and found liver PCB levels of 0.93+/-0.18 ppm following a 28 day exposure. The total PCB levels in exposure to coho
salmon,
liver tissue of B/6 and
in
which consumed diets
of Pacific
Ontario coho
bioaccumulated the
salmon
D/2 mice following a four month
general, reflected the pattern salmon had very highest
observed in the
low levels
while mice which
PCB levels.
fish.
dietary The
mice
were fed
Lake
This observation
appears
to
correlate with the total PCB levels to which the mice were exposed via the dietary fish. The relative
accumulation of
(BAF) which, in this case,
chemicals can fish.
Lake Ontario salmon, the following penta- (0.01-1.2, 0.37); hexa4.0).
factor
Although there was a large variation in the
PCB's.
For example,
in the B/6 mice which were
ranges and means were observed:
(0.02-2.9,
This observation
1.3); heptawas also
tetra- (0.05-0.62, the changes
in the
to fed
0.16);
(1.4-6.2, 2.8); octa- (2.6-3.3,
reflected by
by BAF
PCB's showing that PCB structure was important, the BAF tended
increase with the chlorine content of the
nona- (3.4-4.6,
the bioaccumulation
is defined as the chemical concentration in mouse liver divided
the chemical concentration in the diet within an isomeric class of
be estimated by
3.0); percent
chlorine of the total PCBs which were higher in the mice than in the diet fish (Tables i, 3 and 5). It has been suggested that, in general, are those which induce
the PCB congeners
mixed function oxidase
potentially toxic congeners is shown
these fish
percentage of toxics were similar (ca.
Similarly, the highest levels of total toxic PCB's were observed in
mouse livers following consumption was higher than in
these toxic PCB congeners.
A list of
Although the gradation pattern of toxic PCB's observed
in Grat Lakes salmon followed the total PCB levels, the
strains of mice
1983).
together with their total concentrations in dietary
and mouse livers in Tables i, 3 and 5. 20%) in all fish examined.
which tend to be the most toxic
enzymes (Safe et al.,
of Lake Ontario
coho salmon.
dietary fish, indicating
This observation
agrees with the
The percent toxics in
both
an enhanced biomagnification findings of Safe (1982),
also suggested a preferential bioaccumulation of toxic PCB congeners in human breast milk.
of
which
411
Of the nine pesticide HAHs reached similar coho salmon.
examined, hexachlorobenzene (HCB) and octachlorostyrene
concentrations in
both mouse
strains following consumption
Mirex bioaccumulated to levels which, in D/2
were 4.6-fold higher than levels to find mirex
in liver
in other
(OCS) Ontario
mice were 3.2-fold, and in B/6 mice
in their Lake Ontario coho salmon diets.
extracts of mice
of Lake
dietary groups than
It was
interesting
Lake Ontario
salmon.
Mirex has been utilized by companies other than Hooker Chemical Co., and traces of it have been reported in the literature in al., 1983). mice.
These results
areas other than the Niagara
River and Lake Ontario (Aspila
reflect the efficiency of bioaccumulation
Following consumption of coho salmon from Lake Erie,
of mirex by B/6 and
et D/2
D/2 mice had 30-fold higher levels
of pp-DDE than B/6 mice, however the levels were reversed in B/6 mice which had 23-fold greater levels of pp-DDE than D/2 mice which consumed Lake Michigan
coho salmon.
which consumed Lake Ontario salmon had similar levels of pp-DDE.
Mice of both strains
The diets of fish from Lakes
Erie or Michigan may contain substances which are blocking receptors
in B/6 or D/2 mice or are
acting synergistically or antagonistically to affect pp-DDE metabolism in these mouse strains. Dietary consumption of Great Lakes coho salmon has been identified as a significant source of chronic exposure to HAHs in
man (Cordle et al., 1982).
Lake Michigan fish consumption
also been correlated with PCB levels in human maternal serum Schwartz et al., 1983).
and milk (Wichkizer et al., 1981;
Lake Michigan coho salmon-eating lactating mothers has been shown
have total PCB levels of 980.9 ng/g in their milk (Schwartz et al., 1983). also shown that lactating canadian women in the Ottawa region,
has
to
Recent surveys have
who do not eat freshwater fish,
have up to 29 ng/g of total PCBs and up to 39 ng/g of pp-DDE in their milk (Mes et al., 1984). It is apparent that man is being chronically exposed to the HAH congeners present in Great Lakes coho
salmon.
Furthermore,
the HAH
approaching those reported in this study. animals have been established.
levels in
humans
who eat
Great Lakes
fish
are
Comparative congener analysis of fish and laboratory
The bioaccumulation patterns in
the two strains of mice
will
provide reference points for future congener analysis in fish eating
humans and may aid in the
establishment of the
These
valuable in
the
(as yet
ongoing
unknown) Ah receptor
evaluation
of
the
status of
health
man.
risks associated
baselines will
with
this
route
be of
environmental exposure.
ACKNOWLEDGEMENT
These studies were supported in part by a grant from Research Council of Canada (RAS).
the National Science and Engineering
412
TABLE 1 GAS CHROMATOGRAPHIC ANALYSIS OF HALOGENATED AROMATIC HYDROCARBON LEVELS IN COHO SALMON TISSUE AND AS DIETARY SUPPLEMENTS FOR LABORATORY ANIMALS HALOGENATED AROMATIC HYDROCARBON CONTENT
COMPOUND 2-CB 3-CB 4-CB
(ng/g)
CONTROL CHOW
PACIFIC COHO
L. ERIE COHO
L. MICHIGAN COHO
L. ONTARIO COHO
ND ND ND
ND ND ND
ND ND 2.0 (0.4%)
ND ND 130 (15.1%)
ND ND 260 (9.3%)
5-CB
0.21 (52.5%)
ii. (56.8%)
170 (32.7%)
350 (40.8%)
920 (33.7%)
6-CB
0.03 (7.5%)
4.6 (23.1%)
130 (25.3%)
140 (16.3%)
670 (23.1%)
7-CB
0.05 (5.0%)
4.0 (20.1%)
190 (38.3%)
220 (25.9%)
890 (30.9%)
8-CB
0.14 (35.0%)
ND
16 (3.3%)
17 (1.9%)
76 (2.6%)
9-CB
ND
ND
ND
ND
9.7% (0.3%)
10-CB
ND
ND
ND
ND
Total PCB's % C1
0.4 59.5%
Total Toxic* PCB's Percent Toxic
PCB's
ND 0%
20 57.1% 4.0 2.0%
500 59.1%
860 56.7%
i00
170
20.0%
19.8%
HCB a-HCB Lindane Mirex OCS g-CL pp-DDE pp-DDD pp-DDT
ND ND ND ND ND 0.2 0.i ND 0.i
2.8 8.0 ND ND ND ND i0 2.7 6.6
1.3 ND ND ND 3.4 5.9 79 15 12
2.5 ND ND ND ND 15 240 9.3 37
Percent Lipid
4.3
4.2
1.6
2.0
( = toxic PCB's #81, 105, 118, 126, 128, 138, 156, 157, 158, 166, 170 and 189) (ND = not detected)
ND
2900 57.8% 630 21.7% 9.1 ND ND 150 27 12 670 27 61 2.6
413 TABLE 2
GAS CHROMATOGRAPHIC PCB CONGENER ANALYSIS OF COHO SALMON USED AS DIETARY SUPPLEMENTS FOR LABORATORY ANIMALS
PCB CONGENER CONTENT (ng/g) CONGENER
# # # # # # # # # # # # # # # # # # # # # # #
32 4O 42 44 47+74 49 52 61 64 66 70 71 78+109 81 82 84 86 87+112 91 92 95 97 99
# # # # # # # # # # # # # # # # # # # # # # #
i01 105 ii0 118 126+129 128 130 138 141 143 144 146 151 153 156 157 158+186 166 167 170 171+202 172 174 177 178 180 183 185 187 189 192 194 195
# # # # # # # # #
CONTROL CHOW
ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND 0.03 0.15 ND 0.03 ND ND hiD ND 0.01 ND ND ND ND ND 0.03 ND ND ND ND ND ND ND ND ND hiD ND ND ND ND 0.01 ND ND ND ND
PACIFIC COHO
ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND i0 1.3 ND ND ND 2.7 ND ND ND ND ND ND ND 4.6 ND ND ND ND ND ND ND ND ND hiD ND ND ND ND 1.3 ND ND ND ND
L. ERIE COHO
ND ND ND ND hiD ND ND 2 ND ND ND ND ND ND ND ND 4.6 9.2 ND ND 16 ND 18 57 7.2 32 16 hiD 8.6 ND 51 17 ND 22 6.6 ii 50 4.6 ND 2.6 ND ND 13 6.6 ND i0 8.6 Ii 53 12 ND 32 ND ND 5.9 ND
L. MICHIGAN COHO
ND ND ND ND ii ND 25 9.3 21 28 23 3.3 ND 9.3 ND ND 12 17 ND ND 21 18 42 120 17 55 40 ND 14 6.6 66 15 8 21 19 12 52 8 ND 5.3 ND ND ii 8.6 ND 6 6.6 13 56 9.3 ND 32 ND ND 5.3 ND
L. ONTARIO COHO
ND 1.8 ND 19 16 21 36 15 25 67 48 6.1 9.7 13 14 18 45 55 26 16 54 53 130 210 42 140 140 14 38 18 260 67 12 85 73 4O 240 22 16 21 16 17 52 19 21 33 35 44 240 51 7.9 130 ND 12 19 5.5
414
TABLE 2 (continued) GAS CHROMATOGRAPHIC PCB CONGENER ANALYSIS OF COHO SALMON USED AS DIETARY SUPPLEMENTS FOR LABORATORY ANIMALS PCB CONGENER CONTENT (ng/g) CONGENER # # # # # # # #
CONTROL CHOW
196+203 198 201 205 206 207 208 209
PACIFIC COHO
ND 0.14 ND hid ND ND ND ND
ND ND ND ND ND ND ND ND
L. ERIE COHO
L. MICHIGAN COHO
4.6 ND 5.9 ND ND ND ND ND
6.0 ND 5.3 ND ND ND ND ND
L. ONTARIO COHO 28 ND 23.0 ND 6.1 ND 3.6 ND
(ND : not detected)
TABLE 3 GAS CHROMATOGRAPHIC ANALYSIS OF HALOGENATEDAROMATIC HYDROCARBON LEVELS IN C57BI/6 MOUSE LIVER TISSUE AFTER A FOUR MONTH DIETARY EXPOSURE TO COHO SALMON HALOGENATEDAROMATIC HYDROCARBON CONTENT (ng/g) CONTROL CHOW
PACIFIC COHO
2-CB
ND
ND
3-CB
ND
COMPOUND
6.3+/-2.5 (8.1%)
L. ERIE COHO ND ND
L. MICHIGAN COHO
L. ONTARIO COHO
ND
ND
18+/-1.0 1.9%)
9.6+/-9.6 (0.1%)
4-CB
0.7+/-0.3 (1.9%)
1.6+/-0.8 (2.5%)
4.0+/-0.8 (0.3%)
19+/-4.8 1.9%)
31+/-13 (0.6%)
5-CB
4.2+/-2.8 (9.8%)
15+/-3.6 (18.6%)
68+/-3.0 (4.4%)
120+/-4.0 13.5%)
290+/-110 (6.6%)
6-CB
2.6+/-1.5 (6.5%)
5.7+/-1.2 (7.1%)
160+/-2.6 (10.9%)
120+/-5.9 12.1%)
860+/-150 (21.9%)
7-CB
40+/-4.2 (80.6%)
49+/-6.8 (64.5%)
1200+/-94 (79.6%)
590+/-40 52.2%)
2500+/-430 (63.1%)
8-CB
2.1+/-1.6 (1.3%)
0.2+/-0.2 (0.2%)
64+/-1.6 (4.2%)
44+/-1.5 4.8%)
240+/-42 (6.2%)
9-CB
ND
ND
8.8+/-0.2 (O.6%)
8.2+/0.9 0.9%)
42+/-8.9 (1.0%)
10-CB
ND
ND
0.2+/-0.2 (0.0%)
0.7+/-0.2 0.1%)
12+/-3.8 (0.3%)
TOTAL PCB'S % Cl
50+/-5.9 61.5
78+/-13 59.0
1500+/-100 62.2
930+/-42 60.7
4000+/-740 61.5
TOTAL TOXI C PCB's
17+/-2.1
30+/-5.2
560+/-44
350+/-33
1200+/-230
c o n t ' d .....
415
PERCENT TOXIC PCB's
34
38
37
38
30
HCB a-BHC Lindane Mirex OCS g-Cl pp-DDE pp-DDD pp-DDT
1.3+/-0.9 ND ND ND ND ND 1.8+/-0.2 ND ND
2.6+/-0.1 0.8+/-0.1 ND 1.1+/-0.4 ND ND 2.8+/-0.4 0.7+/-0.1 ND
2.3+/-0.1 ND ND 4.8+/-0.1 2.9+/-0.1 ND 1.9+/-0.1 ND k~
2.3+/-0.3 ND ND 5.7+/-0.2 0.2+/-0.2 ND 47.8+/-6.2 1.7+/-0.3 ND
20+/-2.7 ND hid 700+/-140 24.0+/-8.1 ND 235.0+/-49.7 ND ND
( = toxic PCB's #81, 105, 118, 126, 128, 138, 156, 157, 158, 166, 170, and 189) (ND = not detected; n = 4; mean +/- SEM)
TABLE 4
GAS CHROMATOGRAPHIC PCB CONGENER ANALYSIS OF C57BI/6 MOUSE LIVER TISSUE AFTER A FOUR MONTH DIETARY EXPOSURE TO COHO SALMON PCB CONGENER CONTENT (ng/g) CONGENER
CONTROL CHOW
PACIFIC COHO
L. ERIE COHO
L. MICHIGAN COHO
L. ONTARIO COHO
# # # # # # # # # # # # # # # # # # # # # # #
ND ND ND ND 0.7+/-0.3 ND ND ND ND ND ND ND ND ND ND
6.3+/-2.5 ND ND ND i. i+/-0.5 ND ND 0. i+/-0.1 ND ND ND ND ND 0.4+/-0.4 ND
ND ND ND ND 2.0+/-0.4 ND ND 0.2+/-0.2 ND ND 1.9+/-0.7 ND ND ND ND
17.6+/-9.5 ND ND ND 7.6+/-3.1 ND ND 0.8+/-0.2 ND 3.1+/-0.6 2.4+/-0.6 ND ND 4.6+/-0.5 ND
8.0+/-8.0 ND i. 5+/-i. 5 ND i0.0+/-7.3 i. 4+/-1.4 i. 7+/-1.7 3.7+/-1.3 i. 2+/-1.2 3.3+/-3.3 7.3+/-2.9 ND ND 0.7+/-0.7 ND ND 45.0+/-6.9 0.7+/-0.7 i. i+/-i. 1 ND 2.2+/-2.2 ND 57.5+/-57.5
32 40 42 44 47+75 49 52 61 64 66 70 71 78+109 81 82 84
86 87+112 91 92 95 97 99
ND
2.9+/-0.2 ND ND ND ND ND 0.6+/-0.6
(ND = not detected) (n = 4; mean +/- SEM)
ND
6.4+/-1.0 ND ND ND ND ND 6.7+/-1.1
ND
14.0+/-1.5 ND 0.6+/-0.2 ND ND ND 30.0+/-0.9
ND
35.5+/-5.3 0.5+/-0.5 i. I+/-0.4 ND ND ND 40.8+/-13.6
416
TABLE 4 (continued) GAS CHROMATOGRAPHIC PCB CONGENER ANALYSIS OF C57BI/6 MOUSE LIVER TISSUE AFTER A FOUR MONTH DIETARY EXPOSURE TO COHO SALMON PCB CONGENER CONTENT (ng/g) CONGENER
CONTROL CHOW
PACIFIC COHO
L. ERIE COHO
L. MICHIGAN COHO
L. ONTARIO COHO
# # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # #
ND ND ND 0.5+/-0.5 ND 0.7+/-0.3 i. 0+/-0.3 14.9+/-1.3 ND ND 0.2+/-0.2 ND ND 2.4+/-0.6 0.3+/-0.3 ND ND ND ND i. i+/-0.6 ND ND ND ND ND 13.6+/-1.5 ND ND 0.7+/-0.4 ND
ND 0.6+/-i. 7 0.5+/-0.5 0.6+/-0.6 ND i. i+/-0.1 0.9+/-0.3 27.0+/-3.4 ND ND 0.2+/-0.2 i. 0+/-0.3 ND 4.4+/-0.8 0.3+/-0.3 ND ND ND ND i. 0+/-0.6 ND ND ND ND ND 17.3+/-2.3 0.5+/-0.3 ND 1.6+/-0.3 ND
ND 6.3+/-1.7 ND 12.3+/-1.0 ND 9.0+/-0.4 ND 477.5+/-42.5 ND ND 0.7+/-0.2 34.5+/-0.6 ND 106.3+/-3.8 10.9+/-1.7 2.8+/-0.1 ND 4. I+/-0.2 3.8+/-0.1 41.3+/-0.6 ND 13.8+/-0.6 ND 9.3+/-3.1 58.3+/-1.4 537.5+/-47.7 24.8+/-1.1 ND 53.5+/-1.8 i. i+/-0.0
i. 0+/-i. 0 17.0+/-4.5 ND 23.8+/-2.3 ND 12.0+/-i. 3 Ii. i+/-i. 7 255.0+/-22.5 i. 0+/-0.4 ND ND 27.0+/-2.4 ND 75.3+/-3.1 10.7+/-0.5 2.7+/-0.1
i. 2+/-1.2 90.0+/-25.0 ND 136.0+/-38.3 16.8+/-16.8 54.5+/-8.5 13.8+/-2.1 752.0+/-129.4 i. 6+/-1.6 i. i+/-i. 1 5.0+/-5.0 167.5+/-25.9 ND 527.5+/-79.6 38.5+/-16.4 19.0+/-3.0 ii. 9+/-2.7 23.5+/-3.9 29.5+/-4.9 129.8+/-20.7 ND 63.8+/-10.3 ND 56.0+/-19.0 272.5+/-44.6 760.0+/-154.8 107.0+/-16.5 ND 312.5+/-51.7 7.9+/-2.9 22.5+/-5.0 53.8+/-9.4 17.8+/-2.9 73.0+/-12.2 23.0+/-4.8 74.8+/-12.5 ND 28.0+/-6.3 ND 12.3+/-1.9 ii. 5+/-3.9
101 105 ii0 118 126 128 130 138 141 143 144 146 151 153 156 157 158+186 166 167 170 171+202 172 174 177 178 180 183 185 187 189 192 194 195 196+203 198 201 205 206 207 208 209
ND
ND ND 0.6+/-0.2 ND ND ND ND ND ND ND
(ND = not detected) (n = 4; mean +/- SEM)
ND
2.9+/-0.3
ND ND 0.2+/-0.2 ND ND ND ND ND ND ND
12.5+/-0.3 5.7+/-0.2 20.3+/-1.1 6.2+/-0.4 19.3+/-0.3 ND 5.6+/-0.2 ND 3.2+/-0.2 0.3+/-0.3
0.5+/-0.1 2.7+/-0.1 3.4+/-0.3 24.3+/-1.9 ND 9. i+/-0.2 ND 3.8+/-2.2 32.0+/-2.3 195.0+/-11.9 15.8+/-1.1 ND 36.8+/-1.9 0.7+/-0.2 ND
9.5+/-0.1 3.3+/-0.3 14.5+/-0.5 3.7+/-0.3 13.0+/-0.4 ND 5.3+/-0.4 ND 2.7+/-0.4 0.7+/-0.2
417
TABLE 5 GAS CHROMATOGRAPHIC ANALYSIS OF HALOGENATEDAROMATIC HYDROCARBON LEVELS IN DBA/2 MOUSE LIVER TISSUE AFTER A FOUR MONTH DIETARY EXPOSURE TO COHO SALMON HALOGENATEDAROMATIC CONTROL CHOW
PACIFIC COHO
2-CB
ND
ND
3-CB
ND
4-CB
ND
5-CB
ND
COMPOUND
1.5+/-1.5 (6.3%) ND
HYDROCARBON LEVEL (ng/g) L. ERIE COHO ND 22+/-8.0 (4.8%)
L. MICHIGAN COHO
L. ONTARIO COHO
ND
ND
ND
0.8+/-0.7 0.O%)
14+/-3.6 (2.7%)
3.1+/-0.7 (0.6%)
46+/-15 1.2%)
2.9+/-1.1 (16.0%)
84+/-14 (17.1%)
35+/-6.7 (6.5%)
560+/-92 16.2%)
6-CB
1.1+/-0.4 (19.1%)
4.8+/-1.2 (29.8%)
90+/-11 (18.4%)
120+/-5.9 (22.7%)
770+/-130 22.2%)
7-CB
4.2+/-0.6 (80.9%)
7.3+/-0.8 (46.0%)
250+/-34 (50.0%)
320+/-17 (61.7%)
1900+/-330 54.0%)
8-CB
ND
0.03+/-0.02 (1.9%)
28+/-4.5 (5.7%)
38+/-2.2 (7.3%)
180+/-28 5.2%)
9-CB
ND
ND
6.2+/-0.8 (1.3%)
5.9+/-0.3 (1.1%)
33+/-6.0 1.0%)
10-CB
ND
ND
0.6+/-0.3 (0.1%)
0.9+/-0.1 (0.2%)
10+/-3.4 0.3%)
5.3+/-0.9
17+/-2.3
480+/-64
530+/-31
3500+/-600
59.0
59.5
61.1
60.6
2.0+/-0.3
3.9+/-0.5
160+/-22
150+/-11
1100+/-190
38
23
33
28
31
0.4+/-0.1 ND ND ND ND ND i. 0+/-0.1 0.4+/-0.1 ND
2.3+/-0.4 0.8+/-0.1 ND ND ND ND 2.9+/-0.4 0.6+/-0.1 ND
2.2+/-0.2 ND ND 7. i+/-I. 1 0.8+/-0.1 ND 58+/-8.6 i. 5+/-0.2 ND
2.4+/-0.3 ND ND 3. i+/-0.2 2.8+/-0.3 ND 2. i+/-0.3 0.2+/-0.1 ND
15+/-2.5 ND ND 490+/-75 34+/-4.9 ND 280+/-45 i. 7+/-1.7 ND
TOTAL PCB' s % Cl TOTAL TOXIC PCB' s PERCENT TOXIC PCB' s HCB a-HCB Lindane Mi rex OCS g-Cl pp-DDE pp-DDD pp-DDT
62.1
( = toxic PCB's #81, 105, 118, 126, 128, 138, 156, 157, 158, 166, 170 and 189) (ND = not detected; n = 4; mean +/- SEM)
418 TABLE 6 GAS CHROMATOGRAPHIC PCB CONGENER ANALYSIS OF DBA/2 MOUSE LIVER TISSUE AFTER A FOUR MONTH DIETARY EXPOSURE TO COHO SALMON PCB CONGENER CONTENT (ng/g) CONGENER
# # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # # #
CONTROL CHOW
PACIFIC COHO
L. ERIE COHO
L. MICHIGAN COHO
L. ONTARIO COHO
22.0+/-8.0 ND ND ND ND i. 3+/-0.7 ND 0.7+/-0.7 ND 2.2+/-0.4 ND 5.4+/-1.3 2.2+/-0.3 ND ND 1.8+/-0.3 ND
ND ND ND ND ND ND ND ND ND 0.5+/-0.1 ND ND 1.6+/-0.3 ND ND ND ND
ND ND 3.5+/-2.0 ND ND 8.3+/-3.8 i. 9+/-0.7 3.2+/-1.8 ND 15.3+/-11.9 1.1+/-0.6 12.8+/-7.4 6.4+/-2.4 1.4+/-0.8 hiD 2.4+/-1.5 ND I. 8+/-1.8 33.0+/-5.4 i. 9+/-1.1 3. i+/-i. 7 ND i. 6+/-1.6 1.1+/-0.7 200.0+/-29.2
32 40 42 44 46 47+75 49 52 53 61 64 66 70 71 78+109 81 82
ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND
1.5+/-1.5 ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND ND
84
ND
ND
86 87+112 91 92 95 97 99 i01 105 ii0 118 126+129 128 130 138 141 143 144 146 151 153 156 157 158+186 166 167 170 171+202 172 174 177 178 180 183 185 187 189 192 194 195 196+203 198
ND ND ND ND ND ND ND ND ND ND ND ND 0.4+/-0.1 ND 1.7+/-0.2 ND ND ND ND ND 1.1+/-0.4 ND ND ND ND ND ND ND ND ND ND ND 1.7+/-0.1 ND ND 0.5+/-0.2 ND ND ND ND ND ND
ND ND ND ND ND ND 2.8+/-1.2 ND ND ND ND ND 0.6+/-0.0 ND
3.3+/-0.4 ND ND ND 0.2+/-0.2 ND 3.0+/-0.4 ND ND ND ND ND ND ND ND ND ND ND 2.3+/-0.3 ND ND i. 2+/-0.2 ND ND ND ND ND ND
ND
6.6+/-1.4 0.9+/-0.5 i. i+/-0.2 ND ND ND 39.3+/-5.1 ND 15+/-2.6 0.7+/-0.1 20.5+/-1.8 ND 9.6+/-1/1 2.8+/-0.4 83.0+/-11.1 0.7+/-0.4 0.5+/-0.2 ND 17.5+/-2.1 ND 57.8+/-8.3 8.6+/-0.9 2.3+/-0.4 4.7+/-0.6 1.7+/-0.2 2.9+/-0.8 15.5+/-4.1 ND 5.9+/-0.9 3.3+/-0.5 ND 14.8+/-2.3 69.0+/-10.4 11.1+/-1.5 ND 28.5+/-3.9 1.4+/-0.3 ND 6.6+/-1.1 1.9+/-0.1 9.8+/-1.6 1.1+/-0.4
ND
0.8+/-0.3 ND 0.5+/-0.2 ND ND ND 16.0+/-5.6 ND 4.5+/-0.8 ND 9.3+/-1.1 ND 6.9+/-0.7 1.5+/-1.1 93.8+/-5.8 ND ND 7.5+/-0.1 20.0+/-1.8 ND 76.8+/-3.1 6.6+/-2.4 2.1+/-0.1 4.4+/-0.3 1.8+/-0.1 3.6+/-0.1 21.3+/-1.8 ND 8.4+/-0.5 ND 9.4+/-0.6 27.3+/-1.4 104.0+/-5.6 14.8+/-0.8 ND 41.0+/-i. 7 0.9+/-0.1 4.5+/-0.2 9.3+/-0.6 2.7+/-0.3 12.0+/-0.8 1.9+/-0.0
ND 120.0+/-49.0 i. 5+/-0.5 220.0+/-33.9 16.0+/-9.7 51.5+/-6.9 10.8+/-3.6 565.0+/-99.2 I. 6+/-0.8 i. 9+/-1.1 7.0+/-4.0 142.0+/-21.5 0.3+/-0.3 512.0+/-96.8 46.8+/-7.9 17.5+/-3.1 30.8+/-5.6 ii. 5+/-2.9 34.3+/-5.8 112.5+/-18.8 ND 41.8+/-6.9 0.3+/-0.2 52.0+/-15.0 148.8+/-22.4 557.5+/-107.5 91.8+/-12.9 ND 280.0+/-51.1 3.4+/-1.9 18.3+/-4.2 44.8+/-6.5 12.0+/-I. 9 60.0+/-8.3 4.4+/-2.6
419
TABLE 6 (continued) GAS CHROMATOGRAPHIC PCB CONGENER ANALYSIS OF DBA/2 MOUSE LIVER TISSUE AFTER A FOUR MONTH DIETARY EXPOSURE TO COHO SALMON PCB CONGENER CONTENT (ng/g) CONGENER
CONTROL CHOW
# 201 205 # 206 # 207 # 208 # 209
ND ND ND ND ND ND
PACIFIC COHO
L. ERIE COHO
L. MICHIGAN COHO
L. ONTARIO COHO
0.2+/-0.1 ND ND ND ND ND
8.5+/-1.2 ND 3.8+/-0.6 0.4+/-0.2 2.0+/-0.1 0.6+/-0.3
12.3+/-0.6 ND 3.9+/-0.2 ND 1.9+/-0.1 0.9+/-0.1
54.5+/-8.1 i. 9+/-1.1 20.1+/-2.9 3.9+/-2.2 9.2+/-1.4 i0.3+/-3.4
(ND = not detected) (n = 4; mean +/- SEM)
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