Environmental Toxicology and Chemistry, Vol. 23, No. 9, pp. 2108–2110, 2004
? 2004 SETAC
Printed in the USA
0730-7268/04 $12.00 ? .00
A SURVEY OF METALS IN TISSUES OF FARMED ATLANTIC AND WILD
JEFFERY A. FORAN,*† RONALD A. HITES,‡ DAVID O. CARPENTER,§ M. COREEN HAMILTON,?
AMY MATHEWS-AMOS,# and STEVEN J. SCHWAGER††
†Midwest Center for Environmental Science and Public Policy, Milwaukee, Wisconsin 53202, USA
‡School of Public and Environmental Affairs, Indiana University, Bloomington, Indiana 47405, USA
§School of Public Health and Institute for Health and the Environment, University at Albany, Rensselaer, New York 12144, USA
?Axys Analytical Services, P.O. Box 2219, 2045 Mills Road, Sidney, British Columbia V8L3S8, Canada
#Turnstone Consulting, P.O. Box 3283, Shepherdstown, West Virginia 25443, USA
††Department of Biological Statistics and Computational Biology, 434 Warren Hall, Cornell University, Ithaca, New York 14853, USA
(Received 12 February 2003; Accepted 13 March 2004)
Abstract—Contamination of fish tissues with organic and inorganic contaminants has been a pervasive environmental and public
health problem. The present study reports the concentrations of nine metals in tissues of farmed Atlantic salmon (Salmo salar) and
two species of wild-caught salmon (chum [Oncorhynchus keta] and coho [O. kisutch]) analyzed as part of a global survey of
contaminants in these fish. Of the nine metals, organic arsenic was significantly higher in farmed than in wild salmon, whereas
cobalt, copper, and cadmium were significantly higher in wild salmon. None of the contaminants exceeded federal standards or
Keywords—MetalsFarmed salmonWild salmon
The occurrence of persistent and bioaccumulative chemi-
cals in tissues of fish and other freshwater and marine organ-
isms is an issue of global significance. In the United States,
contaminants in tissues of sport-caught fish have resulted in
fish consumption advisories issued by 48 of 50 states. In 2002,
such advisories totaled 2,800, with the majority triggered by
mercury and polychlorinated biphenyls [1–7]. Mercury con-
tamination in tissues of commercially sold fish [8,9] has also
triggered a consumption advisory by the U.S. Food and Drug
Administration (U.S. FDA). As a result, the U.S. FDA has
warned women and children to reduce or eliminate consump-
tion of swordfish, tilefish, shark, and mackerel (www.cfsan.
fda.gov/?dms/admehg.html). Unlike organic contaminants,
however, most metals other than mercury have been monitored
rarely and detected infrequently in fish tissues.
Salmon is a very popular fish for human consumption and
a healthy source of protein and omega-3 polyunsaturated fatty
acids [10,11]. During the last several years, consumption of
commercially sold salmon (i.e., salmon purchased in stores
and restaurants as opposed to those caught by sport anglers)
has grown rapidly. Year-round availability and lower price are
responsible for salmon’s increased popularity and are the result
of a practice commonly referred to as fish farming or aqua-
culture. Today, farmed salmon comprise the majority ofsalmon
consumed from commercial markets  (also available at
www.fao.org/fi/statist/statist.asp). Despite this increased pop-
ularity, minimal attention has been paid to contaminants in
commercially sold farmed or wild salmon.
We conducted, to our knowledge, the first comprehensive,
global analysis of more than 40 contaminants in farmed and
wild salmon to quantify contaminant levels in salmon tissues
* To whom correspondence may be addressed (firstname.lastname@example.org).
and to determine whether contaminants pose risks to the health
of individuals who consume commercially sold salmon. The
present study was conducted in two phases: Phase 1, in which
we analyzed organic contaminants and metals in tissues of 120
farmed and 57 wild salmon, and phase 2, reported elsewhere
, in which we performed a health-based analysis of organic
contaminants in tissues of more than 700 samples of farmed
and wild salmon.
Here, we report the results of metals analysis in farmed
Atlantic and wild Pacific salmon conducted during phase 1 of
this study. We also provide a comparison of contaminant con-
centrations with federal regulatory or guidance levels to de-
termine whether metal concentrations in salmon tissue pose a
risk to the health of individuals who consume commercially
MATERIALS AND METHODS
All fish sampled in the present study were farmed or wild
salmon. Farmed Atlantic salmon (Salmo salar) werepurchased
from commercial suppliers in the United States and Canada
and were selected to include salmon farmed in British Colum-
bia (Canada), Chile, Maine (USA), and Norway. Each of three
suppliers provided 10 fish from each region for a total of 120
farmed salmon. For comparison, six batches of 10 wild Pacific
salmon were collected from suppliers in Alaska (USA), British
Columbia, and Washington (USA) for a total of 57 wild salmon
(three fish from one batch had thawed during shipping and
were rejected on receipt). Wild fish included chum (Oncor-
hynchus keta) and coho (O. kisutch). The viscera from all fish
were removed before they were shipped, and the heads and
gills were left on the fish.
All samples came to the analytical laboratory (Axys An-
alytical, Sidney, BC, Canada) fresh or frozen on ice or gel-
Metals in farmed and wild salmon
Environ. Toxicol. Chem. 23, 2004 2109
Fig. 1. Wet-weight concentrations of nine metals in farmed (black
bars) and wild (white bars) salmon. Error bars show one standard
error about the mean. **Significance at the 0.01 level, *Significance
at the 0.05 level. ND ? not detected above the detection limit.
packs. The fish were thawed and inspected by a fisheries bi-
ologist to verify species. Each fish was weighed, and its length
was measured. Ten whole fish from each supplier/region were
ground and reground together to make a homogenous com-
Analyses were conducted by Frontier Geosciences (Seattle,
WA, USA). Arsenic, tin, copper, cobalt, strontium, cadmium,
lead, and uranium were measured as follows: Approximately
0.5 g of the homogenized fish tissue was digested in 10 ml of
concentrated nitric acid for 5 h and then diluted to 40 ml with
reagent water. Metals were quantified by argon inductively
coupled plasma–mass spectrometry on a ELAN 6000 instru-
ment (Perkin-Elmer, Norwalk, CT, USA). Scandium was used
as the internal standard for cobalt and copper; indium as the
internal standard for arsenic, strontium, and tin; and platinum
as the internal standard for lead and uranium. The arsenic ion
at m/z 75 was corrected for a small interference from the plasma
caused by ArCl. Total inorganic arsenic was quantified using
hydride generation, cryogenic trapping, gas chromatography,
and atomic absorption spectrometry at a sample pH ? 2.
For mercury analysis, approximately 0.5 g of the fish tissue
was digested in 10 ml of 25% KOH/methanol for 2 h at 60?C
and then diluted to 40 ml with methanol. A 10-ml aliquot of
the original digestate was diluted with 30 ml of 50% 0.2 N
BrCl to oxidize all the mercury to Hg2?. Total mercury was
determined by SnCl2reduction and dual gold amalgamation
using cold-vapor atomic fluorescence spectrometry (CVAFS).
Methyl mercury was then determined on a separate aliquot of
the digestate using aqueous-phase ethylation purging onto Car-
botrap (Supelco, Bellafonte, PA, USA), isothermal gas chro-
matographic separation, and CVAFS. Calibration standards
were National Institute of Science and Technology (NIST; Gai-
thersburg, MD, USA) certified or traceable to NIST-certified
materials. Methyl mercury standards were made from pure
powder and calibrated for methyl mercury (equal to total mer-
cury minus ionic mercury) against National Bureau of Stan-
dards-3133 and cross-verified by analysis of Dogfish Muscle
Certified Reference Material for Trace Metals (DORM-2; Na-
tional Research Council of Canada, Ottawa, ON, Canada). The
majority of the mercury in muscle tissue is methylated. Mea-
surements for total mercury and methyl mercury gave similar
results for each sample; thus, these were considered to be
duplicate measurements and were averaged.
Quality assurance/quality control
All metal analyses were conducted in accordance with a
Frontier Geosciences–accredited quality-assurance/quality-
control program. The analysis batch of 18 samples also in-
cluded the following quality-assurance/quality-control sam-
ples: Four procedural blanks, two reference samples (DORM-
2 and the Dogfish Liver Certified Reference Material for Trace
Metals; National Research Council of Canada), a spiked ma-
trix, a spiked-matrix duplicate, and an analysis duplicate. The
sample results were reviewed and evaluated in relation to the
quality-assurance/quality-control samples worked up at the
same time. Reported results have been corrected for the in-
strument blanks and the preparation blanks. The estimated
method detection limits, calculated as threefold the standard
deviation of the preparation blanks, were as follows: cobalt
and arsenic, 0.03 mg/kg; copper and strontium, 0.01 mg/kg;
cadmium, 0.003 mg/kg; tin, 0.002 mg/kg; lead and uranium,
0.001 mg/kg; and mercury, 0.001 mg/kg. Results for reference
samples and spiked-matrix samples were in the range of 75
to 125% recovery. Duplicate analyses differed from each other
by less than 25%.
The primary objective of the present study was to compare
metal concentrations in wild and farmed salmon. Therefore,
we treated all farmed salmon as replicates and all wild salmon
as replicates, and we compared the averages of farmed and
wild measurements with a Student’s t test. The critical values
for these t statistics vary with the appropriate degrees of free-
dom specified by the Welch modified two-sample t test for
unequal variances . A t test could not be conducted for
cadmium, because all farmed fish samples were nondetects.
Therefore, a chi-square test of the numbers of observations
below and above the detection limit was conducted.
RESULTS AND DISCUSSION
Total arsenic concentrations (all values in mg/kg wet wt)
in the farmed fish were significantly higher than in the wild
fish (Fig. 1). However, inorganic arsenic was not detectable
(limit of detection, 4 ng/g wet wt) in these samples, indicating
that arsenic was present in fish tissues in the relativelynontoxic
organic form . Cobalt, copper, and cadmium were signif-
icantly higher in wild fish than in farmed fish. Differences
between farmed and wild salmon for the other metals were
not detected. No significant differences were found in metal
concentrations among farmed salmon from different regions,
nor were significant differences found between the two wild
salmon species with the exception of cadmium (p ? 0.025).
The concentration of mercury (total and methyl) in fish
tissues is generally correlated positively with size , where-
as concentrations of other metals in fish muscle are not [17,18].
Mercury concentrations in farmed and wild salmon in the pre-
sent study were not significantly different, even though wild
salmon were significantly longer than farmed salmon (p ?
0.001). No significant differences in length were found among
farmed fish from different regions or between the two wild
The U.S. FDA has established regulatory levels for mer-
cury, arsenic, cadmium, and lead in fish tissue  (also avail-
able at www.cfsan.fda.gov/?comm/haccp4.html), and U.S.
Environmental Protection Agency methods  allow devel-
opment of consumption advisories for arsenic, cadmium,meth-
2110 Download full-text
Environ. Toxicol. Chem. 23, 2004 J.A. Foran et al.
Table 1. The U.S. Food and Drug Administration (U.S. FDA) action/
tolerance levels  and the lowest contaminant concentration that
would trigger a consumption advisory using U.S. Environmental
Protection Agency (U.S. EPA) Methods 
U.S. FDA tolerance/
action level (mg/kg)
aAll arsenic detected in farm-raised and wild salmon from the present
study was organic. Levels of inorganic arsenic were less than de-
bU.S. FDA tolerance/action level. This level is for crustaceans.
cBased on cancer risk at the 1 ? 10?5risk level.
dBased on noncancer risk.
eNA ? not available.
yl mercury, and tin in fish (Table 1). Differences were found
in some metal concentrations between farmed andwildsalmon,
but concentrations of mercury, arsenic, cadmium, tin, and lead
did not exceed U.S. FDA regulatory or U.S. Environmental
Protection Agency guidance levels in any of the fish. Regu-
latory or guidance levels for strontium, uranium, cobalt, and
copper have not been developed.
Concentrations of organic contaminants, including poly-
chlorinated biphenyls, dioxin, and several organic pesticides,
are highly and significantly elevated in farmed compared with
wild salmon , likely as a result of the feed provided to
these fish [13,21]. However, the results of the present study
indicate that metals, unlike organic contaminants, do not show
a consistent pattern of elevation in farmed salmon and do not
occur in either farmed or wild salmon at levels that pose a
threat to human health.
Acknowledgement—This research was initiated and supported by the
Environment Division of the Pew Charitable Trusts. We thank B.
Knuth for valuable comments on the manuscript and S. Burrows for
assistance with sample collection. We thank P. Chapman and two
anonymous reviewers for valuable suggestions.
1. Tilden J, Hanrahan LP, Anderson H, Palit C, Olson J, MacKenzie
W. 1997. Health advisories for consumers of Great Lakes sport
fish: Is the message being received? Environ Health Perspect
2. U.S. Environmental Protection Agency. 2003. Fact sheet—Up-
date: National listing of fish and wildlife advisories. EPA-823-F-
03-003. Office of Water, Washington, DC.
3. Clark JR, DeVault D, Bowden RJ, Weishaar JA. 1984. Contam-
inant analysis of fillets from Great Lakes coho salmon, 1980. J
Gt Lakes Res 10:38–47.
4. DeVault DS, Hesselberg R, Rodgers PW, Feist TJ. 1996. Con-
taminant trends in lake trout and walleye from the Laurentian
Great Lakes. J Gt Lakes Res 22:884–895.
5. Smith DW. 2000. Analysis of rates of decline of PCBs in different
Lake Superior media. J Gt Lakes Res 26:152–163.
6. Capon CJ. 1984. Content and chemical form of mercury and
selenium in Lake Ontario salmon and trout. J Gt Lakes Res 10:
7. Rohrer TK, Forney JC, Hartig JH. 1982. Organochlorine and
heavy metal residues in standard fillets of coho and chinook salm-
on of the Great Lakes—1980. J Gt Lakes Res 8:623–634.
8. Johnson BL, Hicks HE, Jones DE, Cibulas W, Wargo A, DeRosa
CT. 1998. Public health implications of persistenttoxicsubstances
in the Great Lakes and St. Lawrence Basins. J Gt Lakes Res 24:
9. Davidson PW, Meyers GJ, Cox C, Axtell C, Shamlaye C, Sloane-
Reeves J, Cernichiari E, Needham L, Choi A, Wang Y, Berlin M,
Clarkson TW. 1998. Effects of prenatal and postnatal methyl mer-
cury exposure from fish consumption on neurodevelopment out-
comes at 66 months of age in the Seychelles child development
study. JAMA 280:701–707.
10. Hu FB, Bronner L, Willett WC, Stampfer MJ, Rexrode KM,
Albert CM, Hunter D, Manson JE. 2002. Fish and omega-3 fatty
acid intake and risk of coronary heart disease in women. JAMA
11. Terry P, Wolk A, Vainio H, Weiderpass E. 2002. Fatty fish con-
sumption lowers the risk of endometrial cancer: A nationwide
case-control study in Sweden. Cancer Epidemiol Biomark Prev
12. U.N. Food and Agriculture Organization. 2004. Fisheries global
information systems (FI-GIS). Rome, Italy.
13. Hites RA, Foran JA, Carpenter DO, Hamilton MC, Knuth BA,
Schwager SJ. 2004. Global assessment of contaminants in farmed
and wild salmon. Science 303:226–229.
14. Ott RL, Longnecker M. 2001. An Introduction to StatisticalMeth-
ods and Data Analysis, 5th ed. Duxbury, Pacific Grove, CA,
15. U.S. Environmental Protection Agency. 2003.Technicalsummary
of information available on the bioaccumulation of arsenic in
aquatic organisms. EPA-822-R-03-032. Office of Science and
Technology, Office of Water, Washington, DC.
16. Neumann RM. 1999. Bioaccumulation and biomagnification of
mercury in two warm-water fish communities. J Freshw Ecol 14:
17. Farkas A. 2003. Age- and size-specific patterns of heavy metals
in the organs of freshwater fish populating a low-contaminated
site. Water Res 37:959–964.
18. Cronin M, Davies IM, Newton A, Pirie JM, Topping G, Swan S.
1998. Trace metal concentrations in deep sea fish from the North
Atlantic. Mar Environ Res 45:225–238.
19. U.S. Food and Drug Administration. 2001. Fish and Fishery
Products Hazards and Controls Guide, 3rd ed. Washington, DC.
20. U.S. Environmental Protection Agency. 2000. National Guidance
for Assessing Chemical Contaminant D for Use in Fish Advi-
sories, Vol 2. Risk Assessment and Fish Consumption Limits,
3rd ed. EPA 823-B-00-008. Office of Science and Technology,
Office of Water, Washington, DC.
21. Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge
MCM, Clay J, Folke C, Lubchenco J, Mooney H, Troell M. 2000.
Effect of aquaculture on world fish supplies. Nature 405:1017–