Risk-based consumption advice for farmed Atlantic and wild Pacific Salmon contaminated with dioxins and dioxin-like compounds.
We reported recently that several organic contaminants occurred at elevated concentrations in farmed Atlantic salmon compared with concentrations of the same contaminants in wild Pacific salmon [Hites et al. Science 303:226-229 (2004)]. We also found that polychlorinated biphenyls (PCBs), toxaphene toxaphene: see insecticides. , dieldrin dieldrin: see insecticides. , dioxins, and polybrominated diphenyl ethers Polybrominated diphenyl ethers or PBDE, are a flame retardant sub-family of the brominated flame retardant group. They have been used in a wide array of household products, including fabrics, furniture, and electronics. occurred at higher concentrations in European farm-raised salmon than in farmed salmon from North and South America. Health risks (based on a quantitative cancer risk assessment) associated with consumption of farmed salmon contaminated with PCBs, toxaphene, and dieldrin were higher than risks associated with exposure to the same contaminants in wild salmon. Here we present information on cancer and noncancer health risks of exposure to dioxins in farmed and wild salmon. The analysis is based on a tolerable intake level for dioxin-like compounds established by the World Health Organization and on risk estimates for human exposure to dioxins developed by the U.S. Environmental Protection Agency Environmental Protection Agency (EPA), independent agency of the U.S. government, with headquarters in Washington, D.C. It was established in 1970 to reduce and control air and water pollution, noise pollution, and radiation and to ensure the safe handling and . Consumption of farmed salmon at relatively low frequencies results in elevated exposure to dioxins and dioxin-like compounds with commensurate elevation in estimates of health risk. Key words: dioxins, risk-based consumption advice, salmon. doi:10.1289/ehp.7626 available via http://dx.doi.org/[Online 9 February 2005]
Between 1987 and 1999, salmon consumption increased annually at a rate of 14% in the European Union and 23% in the United States (Charron 1999). Currently, more than half the salmon sold globally is farm raised, primarily in northern Europe, Chile, Canada, and the United States. The annual global production of farmed salmon (predominantly Atlantic salmon) has risen from 27,000 to > 1 million metric tons during the past two decades [Food and Agriculture Organization of the United Nations Noun 1. Food and Agriculture Organization of the United Nations - the United Nations agency concerned with the international organization of food and agriculture
FAO, Food and Agriculture Organization (FAO FAO,
n See Food and Agriculture Organization. ) 2004].
The health benefits, primarily in terms of prevention of sudden cardiac death Sudden Cardiac Death Definition
Sudden cardiac death (SCD) is an unexpected death due to heart problems, which occurs within one hour from the start of any cardiac-related symptoms. SCD is sometimes called cardiac arrest. , of eating fish such as salmon have been well documented (Daviglus et al. 2002; Harper and Jacobson 2001); however, both farmed and wild salmon have been shown to accumulate a variety of toxic pollutants, some of which may counteract the beneficial effects of the omega-3 fatty acids This is a list of omega-3 fatty acids.
Common name Lipid name Chemical name
α-Linolenic acid (ALA) 18:3 (n-3) octadeca-9,12,15-trienoic acid
Stearidonic acid 18:4 (n-3) octadeca-6,9,12,15-tetraenoic acid present in fish and may increase risk of other diseases (Hires et al. 2004a, 2004b). One such pollutant is dioxin, which has been associated with numerous adverse health effects.
The most potent dioxin congener congener /con·ge·ner/ (kon´je-ner) something closely related to another thing, as a member of the same genus, a muscle having the same function as another, or a chemical compound closely related to another in composition and exerting , 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), is classified by the International Agency for Research on Cancer The International Agency for Research on Cancer (IARC, or CIRC in its French acronym) is an intergovernmental agency forming part of the World Health Organisation of the United Nations.
Its main offices are in Lyon, France. as a group I carcinogen carcinogen: see cancer.
Agent that can cause cancer. Exposure to one or more carcinogens, including certain chemicals, radiation, and certain viruses, can initiate cancer under conditions not completely understood. (known to cause cancer in humans), a classification that was reconfirmed recently (Steenland et al. 2004). The U.S. Environmental Protection Agency (EPA EPA eicosapentaenoic acid.
n.pr See acid, eicosapentaenoic.
n. ) has classified TCDD as "carcinogenic carcinogenic
having a capacity for carcinogenesis. to humans," and the agency has characterized complex mixtures of dioxins as likely human carcinogens Carcinogens
Substances in the environment that cause cancer, presumably by inducing mutations, with prolonged exposure.
Mentioned in: Colon Cancer, Rectal Cancer (U.S. EPA 2002). TCDD increases the risk of all cancers (Crump et al. 2002), including soft-tissue sarcomas Sarcomas Definition
A sarcoma is a bone tumor that contains cancer (malignant) cells. A benign bone tumor is an abnormal growth of noncancerous cells.
A primary bone tumor originates in or near a bone. (Kang et al. 1987), lung and liver cancers (Steenland et al. 2004), and breast cancer (Warner et al. 2002).
Complex mixtures of dioxins [hereafter "dioxin" refers to dioxin-like compounds (DLCs) as defined below] also elicit a variety of noncancer effects. Dioxin is an immunosuppressive Immunosuppressive
Any agent that suppresses the immune response of an individual.
Mentioned in: Antirheumatic Drugs, Graft-vs.-Host Disease, Immunosuppressant Drugs
1. pertaining to or inducing immunosuppression.
2. agent, and the immune system appears to be one of the systems most sensitive to its effects (Birnbaum and Tuomisto 2000). Highly exposed residents of Seveso, Italy, showed a significant and dose-dependent reduction of plasma IgG levels (Baccarelli et al. 2002). Dutch children exposed perinatally to dioxin showed decreased allergies but altered lymphocytes and thrombocytes thrombocytes (throm´bosīts),
n.pl See platelets. (Ten Tusscher et al. 2003) and had lower antibody levels to mumps and measles at preschool age and higher incidence of recurrent middle-ear infections and chicken pox chicken pox or varicella (vâr'əsĕl`ə), infectious disease usually occurring in childhood. It is believed to be caused by the same herpesvirus that produces shingles. (Weisglas-Kuperus et al. 2000). Van Den Heuvel et al. (2002) have shown that Flemish adolescents exposed to polychlorinated biphenyls (PCBs) and dioxins are more susceptible to infectious diseases.
Dioxin also alters behavior in laboratory animals (Hojo et al. 2002) and humans (Vreugdenhil et al. 2002). Perinatally exposed monkeys showed decrements in ability to learn discrimination tasks (Schantz and Bowman 1989), and U.S. Air Force Ranch Hand Veterans with high exposure demonstrated reduced memory function (Barrett et al. 2001). Dioxins have been shown to increase risk of cardiovascular disease in laboratory animals (Lind et al. 2004), most likely secondary to causing an elevation of serum lipids (Calvert and Wille 1996). Dioxin exposure has also been shown to be associated with an increased risk of diabetes in Vietnam Ranch Hand Veterans (Michalek et al. 1999) and among individuals living near a dioxin-contaminated Superfund site (Cranmer et al. 2000). Dioxin alters other endocrine functions, causing endometriosis endometriosis (ĕn'dəmē'trē-ō`sĭs), a condition in which small pieces of the endometrium (the lining of the uterus) migrate to other places in the pelvic area. in monkeys (Rier and Foster 2002) and possibly in humans (Eskenazi et al. 2002). Dioxin is an antiestrogen and, as such, impairs prostate development (Roman and Peterson 1998), spermatogenesis, and reproductive capability in rodents (Mably et al. 1992). In human studies, Vreugdenhil et al. (2002) showed that higher prenatal dioxin levels were associated with more feminized play behavior in both boys and girls boys and girls
mercurialisannua. . High paternal exposure to dioxin alters the sex ratio of offspring, with significantly more girls than boys being born (Mocarelli et al. 2000; Ryan et al. 2002). Thus, although much attention has been focused on cancer as an end point of TCDD exposure, a number of other diseases of equal or perhaps greater public health importance are associated with exposure to complex mixtures of DLCs.
In previous studies (Hites et al. 2004a, 2004b), we reported that concentrations of dioxins, PCBs, polybrominated diphenyl ethers, and pesticides, including toxaphene and dieldrin, among other contaminants, are significantly higher in farm-raised salmon than in wild Pacific salmon and that salmon raised on European farms have significantly higher contaminant contaminant /con·tam·i·nant/ (kon-tam´in-int) something that causes contamination.
something that causes contamination. concentrations than do those raised on North and South American farms. Human cancer risks associated with consumption of farmed salmon contaminated with PCBs, toxaphene, and dieldrin are higher than cancer risks associated with consumption of similar quantities of wild salmon. As a result, risk-based consumption advice for farmed salmon is more stringent than consumption advice for wild salmon (Hites et al. 2004a).
Here we present risk-based consumption information for farmed and wild salmon contaminated with dioxins, furans, and dioxin-like PCBs (DLCs). We developed consumption levels based on the tolerable daily intake (TDI TDI - Transport Driver Interface ) of the World Health Organization (WHO 1998), which assesses dioxin health risks via a toxicity equivalency (TEQ TEQ Toxicity Equivalent
TEQ Time Domain Equalizer
TEQ Teacher Education Quarterly
TEQ Terra Est Quaestuosa (web-based game, Spanish: Lland is Profitable)
TEQ The Evil Quakkers (gaming clan) ) approach that characterizes dioxins and DLCs as 17 2,3,7,8-substituted polychlorinated dibenzodioxins (PCDDs) and polychlorinated dibenzofurans (PCDFs), and the 12 non-ortho and mono-ortho PCBs. Risk-based consumption advice was also developed via the methods of the U.S. EPA (2002).
Materials and Methods
Sample collection and preparation methods have been previously described in detail (Hites et al. 2004a). DLCs were measured in farmed and wild salmon collected from around the world. Atlantic salmon were purchased through wholesalers from farms in the world's eight major farming regions or as fillets from supermarkets in 16 North American and European cities. Five wild species of Pacific salmon (chum, Oncorhyncus ket; coho coho
or silver salmon
Species (Oncorhynchus kisutch) of salmon prized for food and sport that ranges from the Bering Sea to Japan and the Salinas River of Monterey Bay, Cal. It weighs about 10 lbs (4. , Oncorhyncus kisutch; chinook Chinook, indigenous people of North America
Chinook (shĭnk`, chĭ–), Native American tribe of the Penutian linguistic stock. , Oncorhyncus tshawytscha; pink, Oncorhyncus gorbuscha; sockeye, Oncorhyncus nerka) were also collected and analyzed. We did not analyze wild Atlantic salmon because few are available commercially, nor did we analyze farmed Pacific salmon because they are not raised in any substantial amounts (FAO 2004; Kocik and Brown 2002).
All samples were shipped to the analytical laboratory (AXYS Analytical, Sidney, British Columbia Sidney is a town located at the northern end of the Saanich Peninsula, on Vancouver Island in the Canadian province of British Columbia. It has a population of approximately 11,300. , Canada) fresh or frozen on ice or gel packs. Fish were thawed and inspected by a fisheries biologist to verify species. Each fish was weighed and its length measured; then it was filleted to give two skin-on fillets. We analyzed skin-on fillets because most salmon are sold at retail outlets with the skin on. In each case, the fillets from three fish were ground and reground together to make a homogeneous composite.
We used U.S. EPA methods (U.S. EPA 1994, 1999) to measure dioxin and dioxin-like PCB PCB: see polychlorinated biphenyl.
in full polychlorinated biphenyl
Any of a class of highly stable organic compounds prepared by the reaction of chlorine with biphenyl, a two-ring compound. congeners (Hites et al. 2004a). All methods were based on gas chromatographic chro·mat·o·graph
An instrument that produces a chromatogram.
tr.v. chro·mat·o·graphed, chro·mat·o·graph·ing, chro·mat·o·graphs
To separate and analyze by chromatography. high-resolution mass spectrometry with isotopically labeled internal standards. Chlorinated chlorinated /chlo·ri·nat·ed/ (klor´i-nat?ed) treated or charged with chlorine.
charged with chlorine.
some, e.g. dibenzo-p-dioxins and dibenzofurans were measured using U.S. EPA Method 1613 (U.S. EPA 1994), which was calibrated cal·i·brate
tr.v. cal·i·brat·ed, cal·i·brat·ing, cal·i·brates
1. To check, adjust, or determine by comparison with a standard (the graduations of a quantitative measuring instrument): with an extra standard that was one-fifth the concentration of the method requirement. Dioxin concentrations were reported as TEQs assuming nondetects were zero and using WHO TEQ factors. Dioxin-like PCB congeners were quantitated using U.S. EPA Method 1668A (U.S. EPA 1999); this technique is an isotope-dilution, congener-specific method for the 12 dioxin-like congeners and an internal standard method for the remaining 197 congeners. Dioxin-like PCB concentrations were reported as TEQs assuming nondetects were zero. The reported DLC (1) (Data Link Control) See data link and OSI.
(2) (Data Link Control) The data link layer protocol (layer 2) that is used in IBM's SNA networking. See SNA, data link protocol and Microsoft DLC. results are the sum of the chlorinated dioxin/furan TEQ and the dioxin-like PCB TEQ, the latter always being the major contributor to the total.
Analyses were conducted in accordance with AXYS's accredited accredited
recognition by an appropriate authority that the performance of a particular institution has satisfied a prestated set of criteria.
cattle herds which have achieved a low level of reactors to, e.g. quality assurance/ quality control program as described by Hires et al (2004a). All blank measurements were near or below detection limits (typically < 0.02 pg/g for dioxins/furans, < 0.2 pg/g for dioxin-like PCBs); hence, blank values were not subtracted from the sample measurements. Certified reference samples were analyzed periodically to demonstrate analytical accuracy.
We present DLC-associated health risks by developing fish consumption rates for farmed and wild salmon that limit DLC intake to one of two levels--the lower range of the WHO TDI or a 20% increment above the average (65 pg TEQ/day) U.S. adult DLC daily intake (20% selected arbitrarily). We also assessed cancer risk associated with DLC exposure by using the U.S. EPA's draft cancer slope factor for dioxins of 1 x [10.sup.-3]/pg TEQ/kg/day (U.S. EPA 2002).
The WHO (1998) developed a TDI for DLCs from all sources of 1-4 pg TEQ/kg body weight (bw) per day (hereafter, pg TEQ/kg/day). The TDI was derived from LOAELs (lowest observed adverse effect levels) for a variety of adverse responses in experimental animals that occur in a relatively narrow dose range (WHO 1998). Long-term human daily intakes of 14-37 pg/kg/day associated with the LOAELs were adjusted by an uncertainty factor of 10 to establish the TEQ-based TDI of 1-4 pg TEQ/kg/day. The WHO (1998) consultation stressed that the upper range of the TDI (4 pg TEQ/kg/day) "should be considered a maximal tolerable intake on a provisional basis and that the ultimate goal is to reduce human intake levels below 1 pg TEQ/kg bw/day." The U.S. Agency for Toxic Substances and Disease Registry The United States Agency for Toxic Substances and Disease Registry, (ATSDR) is an agency for the U.S. Department of Health and Human Services that is directed by a congressional mandate to perform specific functions concerning the effect on public health of hazardous (ATSDR ATSDR Agency for Toxic Substances & Disease Registry 1998) has also established a minimal risk level for DLCs of 1 pg TEQ/kg/day.
The U.S. EPA (2002) used a "margin-of-exposure" approach to assess the health risks of exposure to DLCs. The U.S. EPA also suggested that the average DLC intake in U.S. adults is approximately 65 pg TEQ/day, and this intake level and associated body burden are within a factor of 100, and in some cases within a factor of 10, of human no observable adverse effect levels (NOAELs) and related end points. As a result, the U.S. EPA has not proposed a reference dose for dioxins in its reassessment. Rather, the U.S. EPA (2002) suggests that evaluation of incremental exposures associated with specific sources of DLCs relative to background may be appropriate. To that end, we assessed the incremental exposure to DLCs above background associated with consumption of farmed and wild salmon as a function of contaminant concentration in salmon tissues and meal frequency. Meal frequencies were chosen to limit DLC intake to 20% above the background intake. Choice of an incremental increase of 20% greater than background was not intended to imply acceptable or unacceptable exposure levels; rather, the increment was chosen arbitrarily to compare health-based consumption rates for farmed and wild salmon.
All risk-based fish consumption rates were developed assuming an average meal size of 227 g (0.5 lb), consistent with U.S. EPA (2004) risk assessment methods for contaminants in fish, and an adult body weight of 70 kg. Risk-based meal consumption rates are based on average DLC concentrations for fish from each farming region, city, and species of wild Pacific salmon as reported by Hites et al. (2004a).
Location-specific, risk-based meal consumption rates for farmed and wild salmon are presented in Figure 1. To limit DLC intake to the lower end of the WHO TDI (1 pg TEQ/kg/day), most farmed salmon must be consumed at rates of < 10 meals/month. For salmon from northern European farms, meal frequencies are generally < 4 meals/month. These consumption rates assume that DLC exposure is from farmed salmon only and does not account for myriad other DLC exposure routes [Institute of Medicine (IOM IOM
See: Index and Option Market ) 2003]; thus, total human DLC exposure at the consumption rates shown in Figure 1 is likely higher than 1 pg TEQ/kg/day. In contrast, most wild Pacific salmon can be consumed at very high rates, in many cases > 1 meal/day, to limit DLC exposure to 1 pg TEQ/kg/day.
[FIGURE 1 OMITTED]
Consumption rates are directly related to contaminant concentrations in the tissues of farmed and wild salmon. DLC concentrations are significantly and considerably higher in farmed salmon than in wild salmon, and in salmon from European farms than in salmon from North and South American farms (Hites et al. 2004a). DLCs are present in other foods, but the levels in farmed salmon (~ 2 pg TEQ/g for the average of all farmed salmon) are greater than reported in any other food in the Food and Drug Administration (FDA FDA
Food and Drug Administration
n.pr See Food and Drug Administration.
n.pr the abbreviation for the Food and Drug Administration. ) Total Diet Survey, including meats, poultry, and dairy products (IOM 2003, Appendix Table B-2).
Consumption of salmon at rates that limit DLC intake to 1 pg TEQ/kg/day results in a 100% incremental increase over background (65 pg TEQ/day) DLC intake for an adult weighing 70 kg. Restriction of DLC intake to an incremental increase of 20% greater than background requires a substantial reduction in meal frequency of farmed and wild salmon (Figure 1). Meal frequencies are lowest for salmon with the highest DLC concentrations, such as those from European farms. For example, meal frequencies for farmed salmon from Scotland, the Faroe Islands, and Norway, as well as farmed salmon sold in European markets, is < 1 meal/month. Only wild Pacific salmon can be consumed at rates of [greater than or equal to] 4 meals/month (1 meal/week), with consumption rates for the least contaminated wild salmon > 16 meals/month (4 meals/week).
Application of the U.S. EPA draft cancer slope factor (U.S. EPA 2002) for DLCs in tissues of farmed and wild salmon results in upper-bound cancer risks as high as 1 x [10.sup.-3] (1 in 1,000) when fish are consumed at rates that result in DLC intake of 1 pg TEQ/kg/day; that is, cancer risks of 1 x [10.sup.-3] result from consumption of most farmed salmon at a meal frequency of greater than twice per week. When salmon are consumed at meal frequencies that limit DLC intake to 20% above background exposure (Figure 1), cancer risk declines to 2 x [10.sup.-4]. To achieve a cancer risk of 1 x [10.sup.-5] (the middle of the U.S. EPA's acceptable risk range; U.S. EPA 2000), consumption of farmed Atlantic salmon must be effectively eliminated and consumption of wild salmon must be restricted generally to less than one meal per month.
Many farmed Atlantic salmon contain dioxin concentrations that, when consumed at modest rates, pose elevated cancer and noncancer health risks. However, dioxin and DLCs are just one suite of many organic and inorganic contaminants and contaminant classes in the tissues of farmed salmon (Foran et al. 2004; Hites et al. 2004a, 2004b), and the cumulative health risk of exposure to these compounds via consumption of farmed salmon is likely even higher. As we have shown here, modest consumption of farmed salmon contaminated with DLCs raises human exposure levels above the lower end of the WHO TDI, and considerably above background intake levels for adults in the United States.
Although both farmed and wild salmon are sold commercially within and outside the United States, the FDA has not established a tolerance or other administrative level of DLCs for commercially sold fish or for other foods. However, the FDA has used 1 ppt ppt
1. parts per thousand
2. parts per trillion as a level of concern for dioxins in chicken, eggs, and catfish (FDA 2004). The European Commission Scientific Committee on Food (2000) established a temporary tolerable intake of 7 pg TEQ/kg/week for DLCs (effectively the lower end of the WHO TDI), which results in advice to restrict salmon consumption identical to TDI-based consumption restrictions in Figure 1.
Our assessment of contaminants in farmed and wild salmon (Foran et al. 2004; Hites et al. 2004a, 2004b) has been criticized for not including potential contaminant reductions, and commensurate reduction in health risks, that may result from proper fish preparation and cooking procedures. This issue is complex and has been examined in salmon from the Great Lakes as well as in other species (Salama et al. 1998; Skea et al. 1979; Voiland et al. 1991; Zabik et al. 1995, 1996; Zabik and Zabik 1999). These studies demonstrate that removal of skin (and associated fat, lateral line, and belly flap) and some cooking methods do, in some cases, reduce contaminant levels in fish. However, the amount of contaminant reduction is highly variable within species, among species, and among contaminants.
Most of these studies suffer from small sample sizes, questionable data analyses, inconsistent analytical techniques, inconsistent data presentation, and variability in initial and postintervention contaminant concentrations within and among species, preparation techniques, and cooking techniques. Deficiencies in study design and variability in contaminant reductions preclude development of a useful quantitative correction factor for the effects of preparation and cooking on contaminant burden. As a result, reductions in exposure and risk associated with reduction in contaminant concentrations from preparation and cooking cannot be evaluated quantitatively; thus, we have not incorporated the effects of cooking and preparation in our risk assessments.
Despite these limitations, it may be prudent public health practice to prepare and cook fish in ways that reduce fatty components of fish tissue. However, consumers will accrue benefits, if any, offish off·ish
Inclined to be distant and reserved; aloof.
off preparation and cooking methods only if they are aware of and use the proper methods. An extensive education program in the Great Lakes basin The Great Lakes Basin consists of the Great Lakes and the surrounding lands of the states of Illinois, Indiana, Michigan, Minnesota, New York, Ohio, Pennsylvania, and Wisconsin in the United States, and the provinces of Ontario and Quebec in Canada, whose direct runoff and was designed to influence fish preparation, cooking, and consumption behavior with the goal of reducing human exposure to contaminants in the tissues of Great Lakes sport fish. This program was based on dissemination of consumption, cleaning, and cooking advice regionally--primarily via written material (e.g., brochures distributed with fishing licenses)--and locally through more intensive initiatives such as communication with consumer groups and health care professionals. The results of these programs are not compelling. Tilden et al. (1997) surveyed > 8,300 residents of the Great Lakes basin to determine their consumption behaviors (for Great Lakes sport fish) and their awareness and use of preparation, cooking, and consumption advice. Despite extensive education efforts, slightly fewer than half of Great Lakes fish consumers were aware of the advice, and awareness was significantly lower in females (39%) and in races other than "white" (22%). Even fewer changed behavior as a result of the advice.
The IOM (2003) and the American Heart Association American Heart Association (AHA),
n.pr a national voluntary health agency that has the goal of increasing public and medical awareness of cardiovascular diseases and stroke, and thereby reducing the number of associated deaths and disabilities. (2005) recommend frequent consumption of fish (at least 2 meals/week) to attain the benefits associated with intake of the omega-3 fatty acids. Consumption of omega-3 fatty acids is important for cardiac health in individuals of ages where they are vulnerable to heart attacks. However, health risks of cancer and a variety of noncancer health effects resulting from consumption of DLCs and other contaminants may outweigh the benefits of consumption of certain types of seafood The following is a partial list of types of seafood. Seafood includes fish, shellfish, and roe.
The list includes markings which summarize the assessment of Monterey Bay Aquarium about how well managed the world's supply of that seafood source is, as of 2004:
1. The act of taking food and drink into the body by the mouth.
2. of omega-3 fatty acids by choosing fish, including most wild salmon, that have lower concentrations of DLCs or by eating other foods, such as various nuts, oils, and vegetables that are high in these healthy fats.
Our work also supports the IOM recommendation to "interrupt the cycle of DLCs through forage, animal feed, and food-producing animals" (IOM 2003). The feed of farmed salmon appears to be the source of DLCs and many other organic contaminants to these fish (Hites et al 2004a). Changes in the composition of feed that result in reduction of organic contaminant concentrations should result in commensurate contaminant reductions in the edible tissues of farmed salmon. We have also supported labeling that identifies all salmon as farmed or wild and that identifies the country of origin so consumers can reduce exposure to DLCs and other contaminants by making informed choices about the fish they choose to purchase and consume.
It is apparent that consumption advice for DLC-contaminated fish varies considerably when based on risk assessment or exposure reduction methods of different national and international agencies. To some degree this reflects scientific uncertainty as well as the economic forces that influence consumption advisories and other risk and exposure reduction methods. However, divergent consumption recommendations that result from inconsistent risk assessment and exposure reduction methods exacerbate consumer confusion. These considerations point to the urgent need for methods that are consistent among national and international agencies to develop consumption advice for contaminated fish as well as other foods.
American Heart Association. 2005. Dietary Guidelines. Dallas, TX:American Heart Association. Available: http://www. americanheart.org/presenter.jhtml?identifier=1330 [accessed 18 January 2005].
ATSDR. 1998. Toxicological Profile for Chlorinated Dibenzo-p-dioxins. Washington, DC:Agency for Toxic Substances and Disease Registry.
Baccarelli A, Mocarelli P, Patterson DG, Bonzini M, Pesatori AD, Caporaso N, et al. 2002. Immunologic effects of dioxin: new results from Seveso and comparison with other studies. Environ Health Perspect 110:1169-1173.
Barrett OH, Morris RD, Akhtar FZ, Michalek JE. 2001. Serum dioxin and cognitive functioning among veterans of Operation Ranch Hand Operation Ranch Hand was a U.S. Military operation during part of the Vietnam War, lasting from 1962 until 1971.
It involved spraying an estimated 19 million US gallons of defoliants over rural areas of South Vietnam in an attempt to deprive the Viet Cong of . Neurotoxicology 22:491-502.
Birnbaurn LS, Tuomisto J. 2000. Non-carcinogenic effects of TCDD in animals. Food Addit Contam 17:275288.
Calvert GM, Wille KK. 1996. Evaluation of serum lipid concentrations among U.S. workers exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Arch Environ Health 51:100-108.
Charron B. 1999. An IntraFish.com Industry Report on Salmon Product Development--The Fish of the Future? Bergen, Norway:IntraFish. Available: http://www.intrafish.com/ intrafish-analysis/SPD_1999_45_eng [accessed 18 January 2065].
Cranmer M, Louie S, Kennedy RH, Kern PA, Fonseca VA 2000. Exposure to 2,3,7,8-tetrachiorodibenzo-p-dioxin is associated with hyperinsulinemia and insulin resistance. Toxicol Sci 56:431-436.
Crump KS, Canady R, Kogevinas M. 2002. Meta-analysis of dioxin cancer dose response for three occupational cohorts. Environ Health Perspect 111:681-687.
Daviglus M, Sheeshka J, Murkin E. 2002. Health benefits from eating fish. Comments Toxicol 8:345-374.
Eskenazi B, Mocarelli P, Warner M, Samuels S, Vercellini P, Olive D, at al. 2002. Serum dioxin concentrations and endomatriosis: a cohort study in Seveso, Italy. Environ Health Perspect 110:629-634.
European Commission Scientific Committee on Food. 2000. Opinion of the Scientific Committee on Food on the Risk Assessment of Dioxins and Bioxin-like PCBs in Food. SCF SCF Service Canadien des Forêts (Canadian Forest Service)
SCF Stem Cell Factor
SCF Scientific Committee on Food (European Commission)
SCF Service Canadien de la Faune .CS.CNTM/DIOXIN/8 Final. Brussels:European Commission, Health & Consumer Protection. Available: http://europa.eu.int/comm/food/fs/sc/scf/out90_en.pdf [cited 16 March 2005].
FAO. 2004. Fisheries Databases and Statistics. Rome:Food and Agriculture Organization of the United Nations. Available: http://www.fao.org/fi/statist/statist.asp [accessed 18 January 2005].
FDA. 2004. Questions and Answers about Dioxin. Washington, DC:Center for Food Safety and Applied Nutrition The Center for Food Safety and Applied Nutrition (CFSAN, pronounced sif'-san) is the branch of the Food and Drug Administration (FDA) which regulates food, dietary supplements, and cosmetics.
"Food" within the context of FDA is a very broad term with some limitations. , U.S. Food and Drug Administration. Available: http://www.cfsan. fda.gov/~lrd/dioxinqa.html#f1 [accessed 18 January 2005].
Foran JA, Hites RA, Carpenter DO, Hamilton MC, Mathews-Amos A, Schwager SJ. 2004. A survey of metals in farmed Atlantic and wild Pacific salmon. Environ Toxicol Chem 23(9):2108-2110.
Harper CR, Jacobson TA. 2061. The fats of life: the role of omega-3 fatty acids in the prevention of coronary heart disease coronary heart disease: see coronary artery disease.
coronary heart disease
or ischemic heart disease
Progressive reduction of blood supply to the heart muscle due to narrowing or blocking of a coronary artery (see atherosclerosis). . Arch Intern Med 161:2185-2192.
Hites RA, Foran JA, Carpenter DO, Hamilton MC, Knuth BA, Schwager SJ. 2004a. Global assessment of organic contaminants in farmed salmon. Science 303:220-229.
Hites RA, Foran JA, Schwager SJ, Knuth BA, Hamilton MC, Carpenter DO. 2004b. Global assessment of polybrominated diphenyl ethers in farmed and wild salmon. Environ Sci Technol 38(19):4945-4949.
Hojo R, Stern S, Zareba za·re·ba also za·ree·ba
1. An enclosure of bushes or stakes protecting a campsite or village in northeast Africa.
2. A campsite or village protected by such an enclosure. G, Markowski VP, Cox C, Kost JT, et al. 2602. Sexually dimorphic dimorphic
see dimorphic fungus. behavioral responses to prenatal dioxin exposure. Environ Health Perspect 110:247-254.
IOM [Institute of Medicine). 2003. Bioxins and Dioxin-like Compounds in the Food Supply. Strategies to Decrease Exposure. Washington, DC:National Academies Press.
Kang H, Enziger F, Breslini P, Feil M, Lee Y, Shepard B. 1987. Soft tissue sarcoma soft tissue sarcoma Oncology A sarcoma that arises in muscle, fat, fibrous tissue, blood vessels, or other supporting tissues. See Sarcoma.
Soft tissue sarcoma staging
I A and military service in Vietnam: a case-control study. J Natl Cancer Inst 79:693-699.
Kocik JF, Brown RW. 2662. From game fish to tame fish--Atlantic salmon in North America, 1798 to 1998. In: Sustaining North American Salmon: Perspectives across Regions and Disciplines [Lynch KD, Jones ML, Taylor WW, ads). Bethesda, MD:American Fisheries Society, 342.
Lind PM, Orberg J, Edlund UB, Sjoblom L, Lind L. 2604. The dioxin-like pollutant PCB 125 (3,3'4,4',5-pentachlorobiphenyl) affects risk factors for cardiovascular disease in female rats. Toxicol Lett 150:293-299.
Mably TA, Bjerke DL, Moore RW, Gendron-Fitzpatrick A, Paterson RE. 1992. In utero and lactational exposure of male rats to 2,3,7,8-tetrachlorodibenzo-p-dioxin. 3. Effects on spermatogenesis and reproductive capability. Toxicol Appl Pharmacol 114:118-126.
Michalek JE, Akhtar FZ, Kiel J. 1999. Serum dioxin, insulin, fasting glucose, and sex hormone-binding globulin globulin, any of a large family of proteins of a spherical or globular shape that are widely distributed throughout the plant and animal kingdoms. Many of them have been prepared in pure crystalline form. in veterans of Operation Ranch Hand. J Clin Endocrinol Metab 84:1540-1543.
Mocarelli P, Gerthoux PM, Ferrari E, Patterson DG, Kieszak S, Brambilla P, et al. 2000. Paternal concentrations of dioxin and sex ratio of offspring. Lancet 355:1838-1839.
Rier S, Foster WG. 2002. Environmental dioxins and endometriosis. Toxicol Sci 70:161-170.
Roman BL, Peterson RE. 1998. In utero and lactational exposure of the male rat to 2,3,67,8-tetrachlorodibenzo-p-dioxin impairs prostate development. 1. Effects on gone expression. Toxicol Appl Pharmacol 150:240-253.
Ryan JJ, Amirova Z, Carrier G. 2002. Sex ratios of children of Russian pesticide producers exposed to dioxin. Environ Health Perspect 110:A699-A701.
Salama, AA, Mohamed MAM, Dural dural /du·ral/ (dur´'l) pertaining to the dura mater.
pertaining to the dura mater.
see dural ossification. B, Potter TL, Levin RE. 1998. Polychlorinated biphenyl concentration in raw and cooked north Atlantic bluefish bluefish, voracious marine fish of the family Pomatomidae, resembling the pompano but more closely related to the sea basses. Bluefish are found in the warm waters of the Indian Ocean, the Mediterranean Sea, and the Atlantic. They average 30 in. fillets. J Agric Food Chem 46:1359-1362.
Schantz SL, Bowman RE. 1989. Learning in monkeys exposed perinatally to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Neurotoxicol Teratol 11:13-19.
Skea JC, Simonin HA, Harris EJ, Jackling S, Spagnoli J J, Symula J, et al. 1979. Reducing levels of mirex mirex
an effective organic pesticide used in ant control and as a fire retardant; it is, however, very persistent in tissue and now banned because of residue problems. , Aroclor 1254, and DDE (Dynamic Data Exchange) A message protocol in Windows that allows application programs to request and exchange data between them automatically.
DDE - Dynamic Data Exchange by trimming and cooking Lake Ontario brown trout and smallmouth bass. J Great Lakes Res 5(2):153-159.
Steenland K, Bertazzi P, Baccarelli A, Kogevinas M. 2004. Dioxin revisited: developments since the 1997 IARC classification of dioxin as a human carcinogen. Environ Health Perspect 112:1265-1268.
Ten Tusscher GW, Teerenberg PA, van Loveren H, Vos JG, van dam Borne AEGK, Westra M, et al. 2003. Persistent hematologic hematological, hematologic
pertaining to or emanating from blood cells.
total and differential white cell counts, hematocrit estimation, erythrocyte count. and immunologic disturbances in 8-year-old Dutch children associated with perinatal dioxin exposure. Environ Health Perspect 111:1519-1523.
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 105:1360-1365.
U.S. EPA. 1994. Method 1613. Tetra- through Octa-Chlorinated Dioxins and Furans by Isotype Dilution HRGC/HRMS. EPA 821-B-94-005. Washington, DC:U.S. Environmental Protection Agency.
U.S. EPA. 1999. Method 1668, Revision A: Chlorinated Biphenyl biphenyl /bi·phen·yl/ (-fen´il) diphenyl.
polychlorinated biphenyl (PCB) any of a group of chlorinated derivatives of biphenyl, used as heat-transfer agents and electrical insulators; they are Congeners in Water, Soil, Sediment, and Tissue by HRGC/HRMS. EPA 821-R-00-002. Washington, DC:U.S. Environmental Protection Agency.
U.S. EPA. 2060. Radiation Protection at EPA: The First 30 Years. EPA 402-B-00-001. Washington, DC:U.S. Environmental Protection Agency, Office of Radiation and Indoor Air.
U.S. EPA. 2002. Draft Dioxin Reassessment. Washington, DC:U.S. Environmental Protection Agency. Available: http://cfpub. epa.gov/ncaa/cfm/pa rt3.cfm?ActType=default [accessed 18 January 2005].
U.S. EPA. 2004. Guidance for Assessing Chemical Contaminant Data for Use in Fish Advisories. Washington, DC:U.S. Environmental Protection Agency. Available: http://www. epa.gov/waterscience/fish/guidance.html [accessed 18 January 2005].
Van Den Heuvel RL, Koppen G, Staessen JA, Hand ED, Verheyen G, Nawrot TS, et al. 2002. Immunologic biomarkers in relation to exposure markers of PCBs and dioxins in Flemish adolescents (Belgium). Environ Health Perspect 110:595-660.
Voiland MP, Gall KL, Lisk D J, MacNeill DB. 1991. Effectiveness of recommended fat-trimming procedures on the reduction of PCB and mirex levels in brown trout from Lake Ontario. J Great Lakes Res 17(4):454-460.
Vreugdenhil HJI HJI Hamilton-Jacobi-Isaacs (partial differential equation) , Slijper FME FME Formal Methods Europe
FME Faculty of Mechanical Engineering (Brno University of Technology, Czech Republic)
FME Feature Manipulation Engine
FME Facultat de Matemàtiques I Estadística , Mulder PGH PGH Pittsburgh
PGH Philippine General Hospital
PGH Proyecto Genoma Humano (Spanish)
PGH Philadelphia General Hospital
PGH Palace of the Golden Horses
PGH Patrol Gunboat (Hydrofoil) , Weisglas-Kuperus N. 2002. Effects of perinatal exposure to PCBs and dioxins on play behavior in Dutch children at school age. Environ Health Perspect 110:A593-A598.
Warner M, Eskenazi B, Morcarelli P, Gerthoux PM, Samuels S, Needham L, et al. 2002. Serum dioxin concentrations and breast cancer risk in the Seveso women's health study. Environ Health Perspect 110:625-628.
Weisglas-Kuperus N, Patandin S, Berbers GAM, Sas TCJ TCJ The Comics Journal
TCJ The Computer Journal
TCJ The Chiropractic Journal
TCJ Tanners Council of Japan
TCJ Travis County Jail
TCJ Tactical Communications Jamming , Mulder PGH, Sauer PJJ PJJ Portland Jazz Jams (podshow) , et al. 2000. Immunologic effects of background exposure to polychlorinated biphenyls and dioxins in Dutch preschool children. Environ Health Perspect 108:1203-1207.
WHO. 1998. Assessment of the Health Risk of Dioxins: Re-evaluation of the Tolerable Daily Intake (TOI Toi (tō`ī), in the Bible, king of Hamath, father of Joram (3.) ). Geneva Geneva, canton and city, Switzerland
Geneva (jənē`və), Fr. Genève, canton (1990 pop. 373,019), 109 sq mi (282 sq km), SW Switzerland, surrounding the southwest tip of the Lake of Geneva. :World Health Organization, European Centre for Environment and Health, and International Programme on Chemical Safety The International Programme on Chemical Safety (IPCS) is a collaboration between three United Nations bodies—the World Health Organization, the International Labour Organization and the United Nations Environment Programme. .
Zabik ME, Booren A, Zabik MJ, Welch R, Humphrey H. 1996. Pesticide residues, PCBs and PAHs in baked, charbroiled, salt boiled and smoked 6teat teat (tet) nipple (1).
1. See nipple.
2. The female breast; mamma.
3. A papilla. Lakes lake trout. Food Chem 55(3):231-239.
Zabik ME, Zabik MJ. 1999. Polychlorinated biphenyls, polybrominated biphenyls, and dioxin reduction during processing/cooking food. Adv Exp Med Biol 459:213-231.
Zabik ME, Zabik MJ, Booren AM, Nettles net·tle
1. Any of numerous plants of the genus Urtica, having toothed leaves, unisexual apetalous flowers, and stinging hairs that cause skin irritation on contact.
2. Any of various hairy, stinging, or prickly plants. M, Song JH, Welch R, et al. 1995. Pesticides and total polychlorinated biphenyls in Chinook salmon chinook salmon
or king salmon
Prized North Pacific food and sport fish (Oncorhynchus tshawytscha) of the salmon family. The average weight is about 22 lbs (10 kg), but individuals of 50–80 lbs (22–36 kg) are not unusual. and carp harvested from the Great Lakes: effects of skin-on and skin-off processing and selected cooking methods. J Agric Food Chem 43:993-1001.
Jeffery A. Foran, (1) David O. Carpenter, (2) M. Coreen Hamilton, (3) Barbara A. Knuth, (4) and Steven J. Schwager (5)
(1) Midwest Center for Environmental Science and Public Policy, Milwaukee, Wisconsin, USA; (2) Institute for Health and the Environment, University at Albany, Rensselaer, New York Rensselaer is a city in Rensselaer County, New York, U.S., located on the Hudson River, directly opposite Albany. As of the 2000 census, the city population was 7,761; in 1920, it was 10,832. , USA; (3) AXYS Analytical Services Ltd., Sidney, British Columbia, Canada; (4) Department of Natural Resources Many sub-national governments have a Department of Natural Resources or similarly-named organization:
For other places or objects named Ithaca, see Ithaca (disambiguation). , USA
Address correspondence to J.A. Foran, Midwest Center for Environmental Science and Public Policy, 1845 N. Farwell Ave., Suite 100, Milwaukee, WI 53202 USA. Telephone: (414) 271-7280. Fax: (414) 273-7293. E-mail: Jforan@mcespp.org
We thank A.M. Amos (Turnstone Consulting) for superb project management and S. Burrows for help obtaining the samples.
This research was initiated and supported by the Environmental Division of the Pew Charitable Trusts Pew Charitable Trusts, philanthropic foundation established (1948) by the children of Sun Oil Company founder Joseph N. Pew (1886–1963) of Philadelphia to provide funds for "general religious, charitable, scientific, literary, and educational purposes. .
The authors declare they have no competing financial interests.
Received 28 September 2004; accepted 9 February 2005.