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Mercury, selenium and fish oils in marine food webs and implications for human health

Published online by Cambridge University Press:  08 September 2015

Matthew O. Gribble*
Affiliation:
Department of Preventive Medicine, University of Southern California Keck School of Medicine, Los Angeles, CA, USA
Roxanne Karimi
Affiliation:
School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, USA
Beth J. Feingold
Affiliation:
Department of Environmental Health Sciences, University at Albany School of Public Health, State University of New York, Rensselaer, NY, USA
Jennifer F. Nyland
Affiliation:
Department of Pathology, Microbiology and Immunology, University of South Carolina School of Medicine, Columbia, SC, USA
Todd M. O'Hara
Affiliation:
Department of Veterinary Medicine, College of Natural Science and Mathematics, University of Alaska Fairbanks, Fairbanks, AK, USA
Michail I. Gladyshev
Affiliation:
Institute of Biophysics of Siberian Branch of Russian Academy of Sciences, Akademgorodok, Krasnoyarsk, Russia Siberian Federal University, Krasnoyarsk, Russia
Celia Y. Chen
Affiliation:
Department of Biological Sciences – Dartmouth College, Hanover, NH, USA
*
Correspondence should be addressed to: M.O. Gribble, Department of Preventive Medicine, University of Southern California, 2001 N. Soto Street, Los Angeles, CA 90032, USA. email: [email protected]
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Abstract

Humans who eat fish are exposed to mixtures of healthful nutrients and harmful contaminants that are influenced by environmental and ecological factors. Marine fisheries are composed of a multitude of species with varying life histories, and harvested in oceans, coastal waters and estuaries where environmental and ecological conditions determine fish exposure to both nutrients and contaminants. Many of these nutrients and contaminants are thought to influence similar health outcomes (i.e., neurological, cardiovascular, immunological systems). Therefore, our understanding of the risks and benefits of consuming seafood require balanced assessments of contaminants and nutrients found in fish and shellfish. In this paper, we review some of the reported benefits of fish consumption with a focus on the potential hazards of mercury exposure, and compare the environmental variability of fish oils, selenium and mercury in fish. A major scientific gap identified is that fish tissue concentrations are rarely measured for both contaminants and nutrients across a range of species and geographic regions. Interpreting the implications of seafood for human health will require a better understanding of these multiple exposures, particularly as environmental conditions in the oceans change.

Type
Research Article
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015

The world's oceans support marine fisheries for commercial, recreational and subsistence uses, and thus are directly linked to human health through fish consumption (i.e. Bergé & Barnathan, Reference Bergé and Barnathan2005; Kite-Powell et al., Reference Kite-Powell, Fleming, Backer, Faustman, Hoagland, Tsuchiya, Younglove, Wilcox and Gast2008; Halpern et al., Reference Halpern, Longo, Hardy, McLeod, Samhouri, Katona, Kleisner, Lester, O'Leary, Ranelletti, Rosenberg, Scarborough, Selig, Best, Brumbaugh, Chapin, Crowder, Daly, Doney Scott, Elfes, Fogarty, Gaines, Jacobsen, Karrer, Leslie Heather, Neeley, Pauly, Polasky, Ris, St. Martin, Stone, Sumaila and Zeller2012; Moore et al., Reference Moore, Depledge, Fleming, Hess, Lees, Leonard, Madsen, Owen, Pirlet, Seys, Vasconcelos and Viarengo2013; Tacon & Metian, Reference Tacon and Metian2013). Fish comprise an important source of animal protein for much of the world's human population, and in the next decade, total production from wild fisheries and aquaculture is expected to exceed production of beef, pork or poultry (FAO/WHO, 2011). In 2010, fish accounted for 16.7% of the world's intake of animal protein, and the world fish food supply grew 3.2% per year from 1961–2012, nearly doubling from an average of 9.9 kg per capita to 19.2 kg per capita (FAO, 2014, pp. 3–4).

The ability of the global population to obtain healthful marine-derived food is dependent on well-managed ecosystems. A broad interdisciplinary approach is needed to understand the connections between the marine environment and human health (Kite-Powell et al., Reference Kite-Powell, Fleming, Backer, Faustman, Hoagland, Tsuchiya, Younglove, Wilcox and Gast2008; Moore et al., Reference Moore, Depledge, Fleming, Hess, Lees, Leonard, Madsen, Owen, Pirlet, Seys, Vasconcelos and Viarengo2013), particularly for evaluating the risks and benefits of consuming seafood. This necessarily requires expertise from marine science as well as public health and biomedical science. This paper is authored by an interdisciplinary group comprising marine and human health scientists who have shared their expertise to synthesize current knowledge on the benefits and risks of consuming marine organisms as routes of human exposure to combinations of fish oils, selenium and the global contaminant mercury, particularly its highly bioavailable and toxic form, methylmercury. Other potential compounds of interest in marine organisms, including organohalogens, natural toxins, arsenicals, trace essential elements and vitamins are beyond the scope of this review; however, introductions to such topics are available elsewhere (Jeandel & Minster, Reference Jeandel and Minster1987; Edmonds & Francesconi, Reference Edmonds and Francesconi1993; Neff, Reference Neff1997; Garthwaite, Reference Garthwaite2000; Lail et al., Reference Lail, Skrabal, Kieber, Bouillon and Wright2007; Guglielmo et al., Reference Guglielmo, Lammel and Maier-Reimer2009; Shaw & Kannan, Reference Shaw and Kannan2009; Yogui & Sericano, Reference Yogui and Sericano2009; Dickey & Plakas, Reference Dickey and Plakas2010; Buck et al., Reference Buck, Franklin, Berger, Conder, Cousins, de Voogt, Jensen, Kannan, Mabury and van Leeuwen2011; Cusick & Sayler, Reference Cusick and Sayler2013; Prego-Faraldo et al., Reference Prego-Faraldo, Valdiglesias, Méndez and Eirín-López2013; Skjånes et al., Reference Skjånes, Rebours and Lindblad2013; Ahrens & Bundschuh, Reference Ahrens and Bundschuh2014; Alonso et al., Reference Alonso, Azevedo, Torres, Dorneles, Eljarrat, Barceló, Lailson-Brito and Malm2014; Sañudo-Wilhelmy et al., Reference Sañudo-Wilhelmy, Gómez-Consarnau, Suffridge and Webb2014). This review provides a limited overview of select dimensions of marine seafood chemical content, and demonstrates the multidisciplinary issues at the interface of Oceans and Human Health (OHH). It does not set out to provide a comprehensive review of seafood content or the overall health implications of seafood consumption. The collaboration of the co-authors of this paper, hailing from diverse disciplinary backgrounds including veterinary medicine, toxicology, immunology, epidemiology, ecology, toxicology and geography, also exemplifies the goals of the OHH initiative which includes the sharing of insights and priorities across research communities (European Marine Board, 2013).

HEALTH BENEFITS OF FISH CONSUMPTION

Fish and shellfish contain protein, long-chain omega-3 fatty acids, vitamins, minerals and trace elements such as calcium and magnesium (Tacon & Metian, Reference Tacon and Metian2013). Seafood has the highest concentration of long-chain omega-3 polyunsaturated fatty acids (PUFAs), including eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), of any foods (Tacon & Metian, Reference Tacon and Metian2013). EPA and DHA show beneficial associations with cardiovascular phenotypes including blood pressure (Campbell et al., Reference Campbell, Dickinson, Critchley, Ford and Bradburn2013), vascular endothelial function (Xin et al., Reference Xin, Wei and Li2012), arterial stiffness (Pase et al., Reference Pase, Grima and Sarris2011) and heart rate variability (Xin et al., Reference Xin, Wei and Li2013). Fish or fish oil intake is also associated with decreased weight and waist circumference (Bender et al., Reference Bender, Portmann, Heg, Hofmann, Zwahlen and Egger2014). Possible impacts of EPA and DHA on cholesterol in humans are unclear. Among persons with diabetes, fish oil supplementation may be associated with lower triglycerides and lower levels of very low density lipoprotein (VLDL) cholesterol, but with higher levels of low density lipoprotein (LDL) cholesterol (Hartweg et al., Reference Hartweg, Perera, Montori, Dinneen, Neil and Farmer2008). In dialysis patients, there are also associations of fish oil supplements with lower triglycerides, but also higher high density lipoprotein (HDL) cholesterol, and no association with LDL cholesterol (Zhu et al., Reference Zhu, Dong, Du, Zhang, Chen, Hu and Hu2014). However, the relationship of EPA and DHA to hard cardiovascular endpoints is less clear. A pooled meta-analysis of 68,680 fish oil supplement clinical trial participants, many of whom (more than half of the trials) had pre-existing cardiovascular disease and were being followed for a second event, did not show evidence for lower risk of mortality (from any cause), cardiac death, myocardial infarction or stroke (Rizos et al., Reference Rizos, Ntzani, Bika, Kostapanos and Elisaf2012). In contrast, many observational studies report a decrease in cardiovascular disease and all-cause mortality with higher fish oil intake (Wang et al., Reference Wang, Harris, Chung, Lichtenstein, Balk, Kupelnick, Jordan and Lau2006). The discrepancy between the clinical trial and the observational study results may reflect differences in study populations, or may suggest that another nutrient in fish (or an interacting cofactor in fish) is responsible for some of the cardiovascular benefits attributed to fish oils.

In addition to their possible relevance for cardiometabolic diseases, EPA and DHA fatty acids also may be associated with many other health outcomes. For example, observational studies suggest a lower risk of breast cancer with higher exposure (Zheng et al., Reference Zheng, Hu, Zhao, Yang and Li2013). DHA is essential for ophthalmological and neurological development (Uauy et al., Reference Uauy, Hoffman, Peirano, Birch and Birch2001; Janssen & Kiliaan, Reference Janssen and Kiliaan2014) and fish oil supplements may be associated with cognitive development among infants (Jiao et al., Reference Jiao, Li, Chu, Zeng, Yang and Zhu2014). Among women who previously had delivered a pre-term baby, fish oil supplements appeared to be associated with longer latency and greater weight at birth of the child but did not appear to be associated with differences in risk of another pre-term birth (Saccone & Berghella, Reference Saccone and Berghella2015).

Selenium, present in marine biota including fish and mussels (Outzen et al., Reference Outzen, Tjønneland, Larsen, Andersen, Christensen, Overvad and Olsen2015), has biological effects that are dose-dependent: at low doses, selenium is an essential nutrient used in selenoproteins such as glutathione peroxidase (Barceloux, Reference Barceloux1999), but at higher doses, selenium might be toxic to a range of animals including humans (Barceloux, Reference Barceloux1999; Hoffman, Reference Hoffman2002; Lemly, Reference Lemly2002; Adams et al., Reference Adams, Brix, Edwards, Tear, DeForest and Fairbrother2003; Ackerman & Eagles-Smith, Reference Ackerman and Eagles-Smith2009; Rigby et al., Reference Rigby, Deng, Grieb, Teh and Hung2010; Hladun et al., Reference Hladun, Kaftanoglu, Parker, Tran and Trumble2013; Thomas & Janz, Reference Thomas and Janz2014), although the dose-response of selenium toxicity differs across animal species (Ackerman & Eagles-Smith, Reference Ackerman and Eagles-Smith2009). In humans, the health effects of selenium (total selenium and selenium species) are controversial, with ongoing research into possible elevations or decreases in risk of various health outcomes according to selenium intake (Sabino et al., Reference Sabino, Stranges and Strazzullo2013). A recent Cochrane review (a comprehensive review in medical sciences that aims to summarize published and unpublished data on a topic) of selenium and cancer prevention found heterogeneous studies furnishing no overall evidence that selenium reduces cancer risk (Vinceti et al., Reference Vinceti, Dennert, Crespi, Zwahlen, Brinkman, Zeegers, Horneber, D'Amico and Del Giovane2014).

HAZARDS OF MERCURY

Although seafood provides important nutritional benefits, there may also be hazards from contaminants such as mercury. Neurological impacts of high methylmercury exposure were described in mass poisoning events in Minamata Bay, Japan (Harada, Reference Harada1995) from consumption of seafood contaminated by effluent from a chlor-alkali facility. ‘Minamata disease’ was characterized by deficits in sensation, vision, hearing, coordination (ataxia) and other problems associated with neurological function (Eto et al., Reference Eto, Takizawa, Akagi, Haraguchi, Asano, Takahata and Tokunaga1999; Uchino et al., Reference Uchino, Hirano, Satoh, Arimura, Nakagawa and Wakamiya2005). Children who had high in utero exposures suffered many neurotoxic effects including cerebral palsy, mental retardation, sensorimotor dysfunction and low birth weight (Chapman & Chan, Reference Chapman and Chan2000; Karagas et al., Reference Karagas, Choi, Oken, Horvat, Schoeny, Kamai, Cowell, Grandjean and Korrick2012). At lower doses, the neurological effects of methylmercury are less clear (Axelrad et al., Reference Axelrad, Bellinger, Ryan and Woodruff2007; Karagas et al., Reference Karagas, Choi, Oken, Horvat, Schoeny, Kamai, Cowell, Grandjean and Korrick2012).

Neurodevelopmental toxicity of mercury

Methylmercury neurotoxicity from consumption of seafood has been the focus of birth cohorts in the Faroe Islands, Seychelles and elsewhere (Table 1). In the Faroe Islands, where much of the mercury was acquired from consumption of marine mammals contaminated by organochlorines, there was an inverse association between mercury in cord blood and children's performance on developmental tests (Grandjean et al., Reference Grandjean, Weihe, Burse, Needham, Storr-Hansen, Heinzow, Debes, Murata, Simonsen, Ellefsen, Budtz-Jørgensen, Keiding and White2001, Reference Grandjean, Weihe, Debes, Choi and Budtz-Jørgensen2014). However, in the Seychelles, where much of the mercury was from fish, overall associations between foetal exposure to mercury and neurodevelopmental impairments were generally not observed (Carocci et al., Reference Carocci, Rovito, Sinicropi and Genchi2014). However, at 9 years of age there appeared to be possible differences in fine motor function at higher levels of mercury exposure (Davidson et al., Reference Davidson, Myers, Weiss, Shamleye and Cox2006; van Wijngaarden et al., Reference van Wijngaarden, Beck, Shamlaye, Cernichiari, Davidson, Myers and Clarkson2006; Mergler et al., Reference Mergler, Anderson, Chan, Mahaffey, Murray, Sakamoto and Stern2007), and evidence for interactions between fatty acids and mercury for cognitive processes (Strain et al., Reference Strain, McAfee, van Wijngaarden, Thurston, Mulhern, McSorley, Watson, Love, Smith, Yost, Harrington, Shamlaye, Henderson, Myers and Davidson2015). Emerging research suggests that genetic polymorphisms and epigenetic processes may account for some of the inter-individual variations of health effects given exposures (reviewed in Basu et al., Reference Basu, Goodrich and Head2014). A recent systematic review examined the associations between exposure to methylmercury from seafood consumption and developmental neurotoxicity from 164 studies in 43 countries and found that mercury might be impacting the health of Arctic and riverine populations near gold mining sites, and might also be relevant for public health in highly populated coastal regions (Sheehan et al., Reference Sheehan, Burke, Navas-Acien, Breysse, McGready and Fox2014).

Table 1. Major cohort studies examining early-life methylmercury (MeHg) and total mercury (Hg) exposure and neurodevelopment in children. IQR, inter-quartile range (25th to 75th percentile).

IQR, inter-quartile range (25th and 75th percentiles of distribution).

Immune toxicity of mercury

Data are limited regarding whether mercury from fish affects the immune system, although studies have been conducted in human populations and in toxicological experiments. In cross-sectional studies in Amazonian Brazil, elevated mercury exposures were associated with increased levels of auto-antibodies in gold miners highly exposed to elemental mercury but also possibly exposed to some methylmercury (Silva et al., Reference Silva, Nyland, Gorman, Perisse, Ventura, Santos, de Souza, Burek, Rose and Silbergeld2004; Gardner et al., Reference Gardner, Nyland, Silva, Ventura, deSouza and Silbergeld2010a). A cross-sectional, nationally representative survey of adults in the USA, showed that hair and blood mercury (thought to largely reflect methylmercury exposures) but not urine mercury (thought to largely reflect inorganic exposures) were associated with having anti-nucleolar auto-antibodies (Somers et al., Reference Somers, Ganser, Warren, Basu, Wang, Zick and Park2015). In in vitro toxicological experiments with sufficiently high doses of mercury (3.6 to 36 μM) to induce cell death within 24 h, exposure of human immune cells in vitro to methylmercury prevented B cell proliferation, and these suppressive effects were more severe if mercury exposure occurred prior to immune cell activation (Shenker et al., Reference Shenker, Berthold, Rooney, Vitale, DeBolt and Shapiro1993). In T cells, proliferation was suppressed and apoptosis induced following mercury exposure in vitro, although these effects were examined in mixed culture systems (Shenker et al., Reference Shenker, Berthold, Decker, Mayro, Rooney, Vitale and Shapiro1992; Shenker et al., Reference Shenker, Guo and Shapiro1998). In mixed cultures of peripheral blood mononuclear cells stimulated with lipopolysaccharide, which stimulates macrophages, subcytotoxic concentrations of methylmercury increased production of pro-inflammatory cytokines TNF-α and IL-1β (Gardner et al., Reference Gardner, Nyland, Evans, Wang, Doyle, Crainiceanu and Silbergeld2009, Reference Gardner, Nyland and Silbergeld2010b). Thus, stimulatory effects of methylmercury were observed at doses closer to the typical in vivo human exposure range, generally less than 200 nM (Mahaffey, Reference Mahaffey2004; Mahaffey et al., Reference Mahaffey, Clickner and Jeffries2009), while higher doses were inhibitory. In the more environmentally relevant administered dose studies, effects were primarily observed when cells were stimulated, suggesting that immune activation state at least partially determines the sensitivity to toxic effects on the immune system. If mercury does affect inflammation, then inflammatory mechanisms could impact other organ systems including the cardiovascular system.

Cardiovascular toxicity of mercury

Mercury's potential impacts on the cardiovascular system are a growing area of research (Roman et al., Reference Roman, Walsh, Coull, Dewailly, Guallar, Hattis, Mariën, Schwartz, Stern, Virtanen and Rice2011). Mercury's relationship to fatal heart attacks was recently cited as the potentially most expensive and therefore the most important uncertainty in the cost-benefit analysis for economic benefit of mercury pollution reductions to the USA (Rice et al., Reference Rice, Hammitt and Evans2010). Myocardial infarction and mortality risks from mercury have been evaluated in several recent studies. A cross-sectional survey in a nationally representative sample of South Koreans found a higher odds of previous myocardial infarction with higher levels of blood mercury (Kim et al., Reference Kim, Kim, Yang and Lee2014). A case-control study of 1408 men found that toenail mercury was associated with higher odds of myocardial infarction after accounting for levels of the heart-protective fatty acid DHA (Guallar et al., Reference Guallar, Sanz-Gallardo, van't Veer, Bode, Aro, Gómez-Aracena, Kark, Riemersma, Martín-Moreno and Kok2002). In contrast, a pooled convenience sample drawn from the Health Professionals Follow-up Study and Nurses’ Health Study in the USA (6045 adults) found non-significant, but potentially protective associations between toenail mercury and risk of myocardial infarction, stroke and coronary heart disease (Mozaffarian et al., Reference Mozaffarian, Shi, Morris, Spiegelman, Grandjean, Siscovick, Willett and Rimm2011). This result is acknowledged by the authors to likely reflect the cardio-protective benefits of fish oils, rather than being an accurate portrait of mercury's cardiovascular impact per se. A Swedish cohort also found lower risk of first myocardial infarction with higher erythrocyte mercury, even after controlling for a plasma biomarker of fish oils (Hallgren et al., Reference Hallgren, Hallmans, Jansson, Marklund, Huhtasaari, Schütz, Strömberg, Vessby and Skerfving2001). In contrast, a large cohort study of 1871 elderly men in Finland found strong positive associations of hair mercury levels with acute coronary events, death, and with cause-specific mortality related to congestive heart failure and cardiovascular disease (Virtanen et al., Reference Virtanen, Voutilainen, Rissanen, Mursu, Tuomainen, Korhonen, Valkonen, Seppänen, Laukkanen and Salonen2005). Additional research is needed to clarify whether mercury is causally associated with fatal cardiovascular disease, and to tease apart the reasons for the apparently discrepant findings in the existing literature. It is likely that there are differing distributions of interacting and confounding variables (i.e. other dietary nutrients, or genetics) across these study populations. Data on geographic variation in joint distributions of nutrients and contaminants in seafood would provide important context for interpreting the human health literature.

CONCENTRATIONS OF EPA + DHA

Variability up to 128-fold has been documented in EPA and DHA levels across fish species (Gladyshev et al., Reference Gladyshev, Sushchik and Makhutova2013). EPA and DHA contents in aquatic animals depend on both taxonomic and ecological factors (Makhutova et al., Reference Makhutova, Sushchik, Gladyshev, Ageev, Pryanichnikova and Kalachova2011; Gladyshev et al., Reference Gladyshev, Lepskaya, Sushchik, Makhutova, Kalachova, Malyshevskaya and Markevich2012b; Lau et al., Reference Lau, Vrede, Pickova and Goedkoop2012); other factors such as an anthropogenic pollution (Gladyshev et al., Reference Gladyshev, Anishchenko, Sushchnik, Kalacheva, Gribovskaya and Ageev2012a) may also be important. Research on the possible impacts of fish health status on fish fatty acid content is limited, but suggests the relationships may be complex and organism-specific. In a recent experiment with cultured puffer fish (Fugu rubripes) with or without Trichodina infection, flat fish (Paralichthys olivaceus) with or without streptococcus infection, yellowtail (Seriola quinqueradiata) with or without jaundice, and amberjack (Seriola purpurascens) with or without Photobacterium damselae sp. piscicida, there was not a significant difference by fish disease status in the overall fish fatty acid composition in fish livers; however, liver DHA was significantly higher in the diseased fish than healthy fish for flat fish, yellowtail and amberjack (Tanaka et al., Reference Tanaka, Shigeta, Sugiura, Hatate and Matsushita2014). There is also growing interest in how oxidative stress in fish may affect fish lipids (Tanaka & Nakamura, Reference Tanaka and Nakamura2012; Tanaka et al., Reference Tanaka, Shigeta, Sugiura, Hatate and Matsushita2014).

One objective for our review is to summarize data on EPA and DHA across fish populations. To identify EPA and DHA content of diverse marine fish species, including anadromous fish, we queried Web of Science, Core Collection on 2 October 2014 for ‘fatty acid AND content AND fish AND marine’ (Table 2). Unfortunately, most studies report EPA and DHA as per cent of total fatty acids, and do not provide quantitative information on contents of these PUFA in mass units per fish portion (Gladyshev et al., Reference Gladyshev, Sushchik, Gubanenko, Demirchieva and Kalachova2007, Reference Gladyshev, Lepskaya, Sushchik, Makhutova, Kalachova, Malyshevskaya and Markevich2012b; Huynh & Kitts, Reference Huynh and Kitts2009). In this manuscript, we review data from 10 studies reporting direct measurements of EPA and DHA contents in wild fish biomass obtained using internal standards in chromatography (using capillary columns) over two recent decades. These had slightly different methodologies. For small fish, less than 35 cm (e.g. sardine or capelin), the fish were analysed whole (Huynh & Kitts, Reference Huynh and Kitts2009). Larger fish species (e.g. salmon) were sampled by dissecting muscle tissue (filets without skin), usually under dorsal fin (e.g. Gladyshev et al., Reference Gladyshev, Sushchik, Gubanenko, Demirchieva and Kalachova2006, Reference Gladyshev, Sushchik, Gubanenko, Demirchieva and Kalachova2007, Reference Gladyshev, Lepskaya, Sushchik, Makhutova, Kalachova, Malyshevskaya and Markevich2012b; Huynh & Kitts, Reference Huynh and Kitts2009; Kitson et al., Reference Kitson, Patterson, Izadi and Stark2009; Abd Aziz et al., Reference Abd Aziz, Azlan, Ismail, Alinafiah and Razman2013; Sahari et al., Reference Sahari, Farahani, Soleimanian and Javadi2014). In some studies (Chuang et al., Reference Chuang, Bulbul, Wen, Glew and Ayaz2012) ventral muscles were sampled. In other studies both small and large fish were taken whole, e.g. ground and homogenized (Castro-Gonzalez et al., Reference Castro-Gonzalez, Maafs-Rodriguez, Silencio-Barrita, Galindo-Gomez and Perez-Gil2013). Some authors did not report the sampling in detail (Garcia-Moreno et al., Reference Garcia-Moreno, Perez-Galvez, Morales-Medina, Guadix and Guadix2013).

Table 2. Content of eicosapentaenoic (EPA) and docosahexaenoic (DHA) acids (mg g−1, wet weight) in various wild fish species, their types of habitat (H1: p, pelagic, bp, benthopelagic, d, demersal; H2: c, cold waters, t, temperate waters; w, warm waters) and size (cm). Orders and species are ranged by EPA + DHA content values.

The resulting data set includes 63 fish species across 11 orders (Table 2). Since PUFA contents in aquatic animals are known to depend on both phylogenetic and ecological factors (Makhutova et al., Reference Makhutova, Sushchik, Gladyshev, Ageev, Pryanichnikova and Kalachova2011; Gladyshev et al., Reference Gladyshev, Lepskaya, Sushchik, Makhutova, Kalachova, Malyshevskaya and Markevich2012b; Lau et al., Reference Lau, Vrede, Pickova and Goedkoop2012), fish species were organized by their EPA and DHA values within taxonomic orders. Putative effects of ecological (habitat) factors were taken into account by dividing the fish species into pelagic, benthopelagic and demersal, as well as by category of water temperature of their habitat, i.e. cold-water, temperate and warm-water (tropical) species. Common size of the fish species was used as a proxy of their trophic level, although this is an imperfect surrogate.

Values of EPA + DHA concentration in the 63 fish species varied from 25.60 mg g−1 (sardine Sardinops sagax, order Clupeiformes) to 0.04 mg g−1 (spotted weakfish Cynoscion nebulosus, order Perciformes) (Table 2). Clupeiformes had the highest median and maximum values of EPA + DHA contents, followed by Salmoniformes, while Perciformes, Scorpaeniformes and Gadiformes and miscellaneous had nearly similar median values (Figure 1). Nevertheless, ranges of values for EPA + DHA content of all orders overlapped in minimum values (Figure 1, Table 2). Thus, all orders, including Clupeiformes, have species with comparatively low content of EPA and DHA.

Fig. 1. Contents of eicosapentaenoic acid (EPA) + docosahexaenoic acid (DHA) in fish orders: minimum, maximum and median values and quartiles. Number of species, N: order Clupeiformes, N = 9; order Salmoniformes, N = 3; order Perciformes, N = 36; order Scorpaeniformes, N = 3; order Gadiformes, N = 4; miscellaneous (orders Osmeriformes, Pleuronectiformes, Siluriformes, Mugiliformes, Beloniformes and Myliobatiformes), N = 8.

Interpretation of these results may be complicated by measurement error introduced by differing methods used for fish sampling and analysis, but some broad patterns in the data are interesting. Analysis of published EPA + DHA values found no statistically significant effect of type of habitat (pelagic, benthopelagic and demersal), or temperature of habitat, or their interaction on the PUFA content in fish. To visualize the results of ANOVA, a two-dimensional graph of the PUFA content in the groups of species was created (Figure 2). Since EPA + DHA contents in benthopelagic species overlapped completely with those of pelagic and demersal species, they were not included in the depicted groups. In addition, there were only six cold water species amongst pelagic, benthopelagic and demersal, which were joined in one group. The graph illustrates that EPA and DHA values of all the groups, pelagic temperate water, pelagic warm water, demersal temperate water, demersal warm water and cold water species, overlapped nearly completely.

Fig. 2. Areas of eicosapentaenoic acid (EPA) vs docosahexaenoic acid (DHA) A levels in fish species from diverse habitats: pelagic warm water species (number of species, N = 17, violet), pelagic temperate water species (N = 10, black), demersal warm water species (N = 15, green), demersal temperate water species (N = 10, blue) and cold water species (N = 6, red).

This analysis of available data did not identify a strong predictor for EPA and DHA contents in fish. Temperature, for example, had limited impact: the contents of EPA + DHA in three pelagic planktivorous Clupeiformes with nearly identical sizes: sardine Sardinops sagax from temperate waters, shad Hilsa macrura from warm waters and herring Clupea harengus from cold waters were all similar (Table 2). Moths et al. (Reference Moths, Dellinger, Holub, Ripley, McGraw and Kinnunen2013) analysed freshwater fish from the Great Lakes as well as 99 other species from freshwater and marine systems documented in seven other studies. As in this study, Moths et al. (Reference Moths, Dellinger, Holub, Ripley, McGraw and Kinnunen2013) found that for marine systems, there was no relationship between latitude and omega-3 fatty acid composition of fish. However, in temperate climates, marine fish had higher omega-3/6 ratios than freshwater fish and for freshwater fish alone, there were higher omega-3 fatty acids in temperate fish as compared with tropical fish. While this study was based on relatively few datasets and many different species, it suggests some interesting patterns. For marine zooplankton, Kattner & Hagen (Reference Kattner, Hagen, Arts, Kainz and Brett2009) did not find significant differences in latitudinal distribution of EPA and DHA levels. Since zooplankton are the main food of these three planktivorous fish species from different latitudes, Kattner & Hagen's (Reference Kattner, Hagen, Arts, Kainz and Brett2009) findings for zooplankton are consistent with those for the planktivorous fish. Thus, more specific characteristics of diverse aquatic ecosystems, such as levels of primary production of PUFA and the efficiency of their transfer through trophic chains (Gladyshev et al., Reference Gladyshev, Sushchik, Anishchenko, Makhutova, Kolmakov, Kalachova, Kolmakova and Dubovskaya2011), are likely to be contributing factors for EPA and DHA content of given fish species. In these large meta-analyses, many environmental and fish specific variables may obscure the potential effects of individual environmental factors such as temperature or trophic level, or pharmacokinetic compartment differences of lipids across fish tissues. More research directed to effects of fish phylogenetics, ecological niche, type of habitat, food quality and other possible determinants is needed to be able to predict EPA and DHA contents, particularly in marine fish.

Studies of fish from field sampling, particularly with heterogeneous methodology, are not conducive to investigating the mechanistic sources of difference between populations living in different environmental settings. In contrast to the analysis of metadata for fish fatty acids above, experimental laboratory studies suggest that fatty acid concentrations in plankton and fish may be influenced in part by the food and temperature environments to which they are exposed. Numerous studies have shown that EPA and PUFAs increase in cells grown at lower temperatures and saturated fatty acids decrease (Thompson et al., Reference Thompson, Guo, Harrison and Whyte1992; Jiang & Gao, Reference Jiang and Gao2004; Fuschino et al., Reference Fuschino, Guschina, Dobson, Yan, Harwood and Arts2011; Teoh et al., Reference Teoh, Phang and Chu2013). In addition, some fish either naturally occurring or cultured have higher concentrations of fatty acids when grown in colder temperatures. Fish need to adjust membrane fluidity for metabolic function in fluctuating temperatures (homeoviscous adaptation) and they do this by changing the concentrations and composition of individual fatty acids and sterols in cell membranes (Sinensky, Reference Sinensky1974; Snyder et al., Reference Snyder, Schregel and Wei2012). Several experimental studies show differences in fatty acid concentrations in fish exposed to different temperatures. Experiments with juvenile Atlantic salmon at two temperatures (14 and 19°C) found that n-3, n-5 and total fatty acids were higher in fish raised in colder water (Arts et al., Reference Arts, Palmer, Skiftesvik, Jokinen and Browman2012). Another study on cultured Atlantic salmon found that the temperature effect was dependent on the type of oil in their food; temperature effects were more pronounced in fish fed copepod oil diets than fish oil diets (Bogevik et al., Reference Bogevik, Henderson, Mundheim, Olsen and Tocher2011). Another study found the digestibility of the lipids in Atlantic salmon to increase with increasing rearing temperatures suggesting that while colder temperatures may favour higher fatty acid concentrations, they may be less digestible than at warmer temperatures (Huguet et al., Reference Huguet, Norambuena, Emery, Hermon and Turchini2015). Laurel et al. (Reference Laurel, Copeman and Parrish2012) found that lower temperatures also favoured increases in unsaturated fatty acids in newly hatched Pacific cod larvae but relative amounts of essential fatty acids did not change with temperature. Similarly, n-3 and n-6 fatty acids decreased with increased temperatures in eggs and larvae of the marine fish, Inimicus japonicas (Wen et al., Reference Wen, Huang, Chen and Feng2013). Thus, there are a range of experimental studies supporting the role of temperature and potentially diet determining fatty acid composition in aquatic plankton and fish. They suggest that colder temperatures result in higher amounts and differing quality of fatty acids. However, the disparity between patterns observed in experimental and field-based studies should be further investigated.

VARIABILITY IN FISH MERCURY CONCENTRATIONS

One of the major challenges in managing human exposure to mercury from fish consumption is that fish mercury concentrations are highly variable. Numerous studies have measured broad differences in mercury content across different finfish and shellfish taxa (Sunderland, Reference Sunderland2007; Karimi et al., Reference Karimi, Fitzgerald and Fisher2012). A recent review estimated that mercury content within a given taxon can also be highly variable, ranging from 0.3–2.4 orders of magnitude, depending on the taxon (Karimi et al., Reference Karimi, Fitzgerald and Fisher2012). This variability poses a challenge to estimating mercury exposure from seafood consumption, and makes it difficult to quantify the risk associated with consuming specific fish taxa.

Numerous studies have shown that body size, age, trophic level and food source of fish are related to concentrations of methylmercury and the per cent of total mercury that is methylmercury (Chen et al., Reference Chen, Dionne, Mayes, Ward, Sturup and Jackson2009; Piraino & Taylor, Reference Piraino and Taylor2009). Across species, body size can be more strongly correlated with mercury concentration than trophic level (Karimi et al., Reference Karimi, Frisk and Fisher2013). In general, larger fish across and within species have higher concentrations of methylmercury because larger fish eat higher trophic level prey and are older and have had a longer time to accumulate mercury (Cossa et al., Reference Cossa, Harmelin-Vivien, Mellon-Duval, Loizeau, Averty, Crochet, Chou and Cadiou2012; Storelli and Barone, Reference Storelli and Barone2013). However, some studies have found that mercury concentration is more strongly correlated with age than length or weight (Braune, Reference Braune1987; Burger & Gochfeld, Reference Burger and Gochfeld2011). For example, the size of Bluefin tuna is not related to mercury concentration (Burger & Gochfeld, Reference Burger and Gochfeld2011) and Atlantic herring in the Arctic show relationships at 3–5 years of age but a decrease at 1–2 years of age due to growth dilution (Braune, Reference Braune1987). While there are clear positive relationships between total mercury and fish size and fish age, there is still variability in total mercury concentrations that is not explained by those two variables as well as the presence of interspecific and intraspecific variability (Tremain & Adams, Reference Tremain and Adams2012). Some of this unexplained variability likely comes from the food source and geographic range of the fish. Fish that have more pelagic than benthic food sources appear to bioaccumulate higher concentrations of mercury (Power et al., Reference Power, Klein, Guiguer and Kwan2002; Chen et al., Reference Chen, Dionne, Mayes, Ward, Sturup and Jackson2009; Karimi et al., Reference Karimi, Frisk and Fisher2013). Not surprisingly, fish that are exposed to higher water and sediment concentrations also have higher tissue concentrations of mercury (Lowery & Garrett, Reference Lowery and Garrett2005; Chen et al., Reference Chen, Dionne, Mayes, Ward, Sturup and Jackson2009; Gehrke et al., Reference Gehrke, Blum and Marvin-DiPasquale2011; Taylor et al., Reference Taylor, Linehan, Murray and Prell2012; Chen et al., Reference Chen, Lai, Chen, Hsu, Hung and Chen2014). However, levels of mercury may vary between similar species in a small geographic area and by tissue within a fish (Bank et al., Reference Bank, Chesney, Shine, Maage and Senn2007). A recent study also suggests increases in methylmercury bioaccumulation in fish experiencing warmer temperatures (Dijkstra et al., Reference Dijkstra, Buckman, Ward, Evans, Dionne and Chen2013). Overall, these studies show that fish size, age, trophic level, food source and geographic region each influence fish mercury content, with no strict rules for which of these factors explains the largest portion of mercury variability. While agencies such as the Food and Drug Administration (FDA) in the USA monitor mercury in marine fish consumed by humans, they do not report fish sizes or geographic location, both of which are extremely important when looking at mercury bioaccumulation.

SELENIUM AND MERCURY CONCENTRATIONS IN FISH

There is a long-running interest in nutrient-toxicant interactions between mercury and selenium (Ganther et al., Reference Ganther, Goudie, Sunde, Kopicky, Wagner, Oh and Hoekstra1972). Although recent evidence suggests possible synergistic interactions between mercury and selenium for fish development (Penglase et al., Reference Penglase, Hamre and Ellingsen2014), the weight of evidence suggests antagonistic interactions in which selenium mediates mercury toxicokinetics (reviewed in Peterson et al., Reference Peterson, Ralston, Whanger, Oldfield and Mosher2009). Selenomethionine increases mercury elimination in zebrafish (Danio rerio) (Yamashita et al., Reference Yamashita, Yamashita, Suzuki, Kani, Mizusawa, Imamura, Takemoto, Hara, Hossain, Yabu and Touhata2013; Amlund et al., Reference Amlund, Lundebye, Boyle and Ellingsen2015), shrimp (Bjerregaard & Christensen, Reference Bjerregaard and Christensen2012) and goldfish (Carassius auratus) (Bjerregaard et al., Reference Bjerregaard, Fjordside, Hansen and Petrova2012); selenite, and seleno-cysteine also increased mercury elimination in goldfish and shrimp. In humans, dietary organic selenium can increase mercury elimination (Li et al., Reference Li, Dong, Chen, Li, Gao, Qu, Wang, Fu, Zhao and Chai2012). Ralston and colleagues report that selenium not only ameliorates the toxic effects of methylmercury by sequestering methylmercury and reducing its bioavailability to organisms, but mercury and selenium may also have physiologically important interactions mediated by other mechanisms (Ralston et al., Reference Ralston, Blackwell and Raymond2007; Ralston & Raymond, Reference Ralston and Raymond2010). Based on rat data, Ralston (Reference Ralston2008) suggests that where the selenium to mercury molar ratio exceeds 1:1, there is adequate selenium to counter mercury toxicity. However, this has not been clearly demonstrated in humans. In recent trout (Salmo trutta) studies in a Norwegian lake, the selenium to mercury molar ratio was a better predictor of trout metallothionein levels than was either selenium or mercury (Sørmo et al., Reference Sørmo, Ciesielski, Øverjordet, Lierhagen, Eggen, Berg and Jenssen2011). However, human studies and clinical trials for selenium demonstrate mixed and inconclusive results for cardiovascular effects of methylmercury and selenium (Mozaffarian, Reference Mozaffarian2009). It has been suggested that mercury cardiovascular toxicity may be modified by selenium intake (Cooper et al., Reference Cooper, Rader and Ralston2007; Khan & Wang, Reference Khan and Wang2009; Mozaffarian, Reference Mozaffarian2009). This might arise through selenium impacts on mercury kinetics (Huang et al., Reference Huang, Strathe, Fadel, Johnson, Lin, Liu and Hung2013) or through impacts on oxidative stress mediators of mercury toxicity (Kaneko & Ralston, Reference Kaneko and Ralston2007; Ralston et al., Reference Ralston, Blackwell and Raymond2007; Farina et al., Reference Farina, Aschner and Rocha2011; Alkazemi et al., Reference Alkazemi, Egeland, Roberts Ii, Chan and Kubow2013; Drescher et al., Reference Drescher, Dewailly, Diorio, Ouellet, Sidi, Abdous, Valera and Ayotte2014), although evidence for the oxidative stress mediation hypotheses is ambiguous (Belanger et al., Reference Belanger, Mirault, Dewailly, Berthiaume and Julien2008). Selenium-mercury interactions may also be relevant for neurodevelopmental outcomes (Choi et al., Reference Choi, Budtz-Jørgensen, Jørgensen, Steuerwald, Debes, Weihe and Grandjean2007).

In recent years due to the interest in selenium to mercury molar ratios, a number of studies have assessed mercury and selenium concentrations and the selenium to mercury molar ratios for a variety of fish species from field samples as well as fish purchased from supermarkets (Burger et al., Reference Burger, Stern and Gochfeld2005, Reference Burger, Gochfeld and Fote2013; Burger & Gochfeld, Reference Burger and Gochfeld2011, Reference Burger and Gochfeld2012; Gochfeld et al., Reference Gochfeld, Burger, Jeitner, Donio and Pittfield2012; Karimi et al., Reference Karimi, Frisk and Fisher2013, Reference Karimi, Fisher and Meliker2014). The relationship between body size and selenium to mercury molar ratios vary with species, tissues and geographic location. Selenium to mercury molar ratios decreased with size of fish for yellowfin tuna and windowpane flounder in Delaware Bay and a wide variety of species in the Aleutians (Burger & Gochfeld, Reference Burger and Gochfeld2011, Reference Burger and Gochfeld2012). Some individuals of most of the 15 species studied in the Aleutians had ratios less than 1.0, where older, larger, higher trophic level fish had the lowest ratios. This was the result of mercury concentrations increasing with fish size but selenium concentrations not increasing with size. While selenium to mercury molar ratios were negatively correlated with fish length for bluefish, the ratios were lower for white muscle tissue, the portion of the fish that humans consume. In a study of 19 species off the coast of New Jersey (USA), (Burger & Gochfeld, Reference Burger and Gochfeld2011) mercury and selenium were positively related for five species and negatively related for two species, and across all species, selenium had no consistent relationship with length. However, for most species tested across all of these studies, the ratios were greater than 1.0, although 20% of the striped bass caught by trawling off the New Jersey coast had molar ratios of less than 1.0 (Gochfeld et al., Reference Gochfeld, Burger, Jeitner, Donio and Pittfield2012).

In general, studies of selenium to mercury molar ratios have found that mercury concentrations were positively related to fish length and trophic level but selenium concentrations were not, and selenium to mercury molar ratios are more strongly related to mercury content than selenium content (Karimi et al., Reference Karimi, Frisk and Fisher2013). This reflects the fact that mercury more strongly accumulates in the body, and biomagnifies through the food chain compared with selenium (Karimi et al., Reference Karimi, Frisk and Fisher2013). These findings are consistent with lower efflux (loss) rates of methylmercury than selenium, because lower efflux rates lead to greater bioaccumulation over time as body size increases (Karimi et al., Reference Karimi, Fisher and Folt2010). However, bivalves (e.g. clams, mussels and oysters) are known to be relatively efficient selenium accumulators (Stewart et al., Reference Stewart, Luoma, Schlekat, Doblin and Hieb2004; Presser & Luoma, Reference Presser and Luoma2010), and have higher selenium concentrations than finfish (Karimi et al., Reference Karimi, Frisk and Fisher2013). It also appears that the mean selenium to mercury molar ratio declines with mean size of fish species and with individual fish size within a species. Both suggest that larger, predatory fish as well as the largest individuals of many species have lower selenium to mercury molar ratios and may not provide selenium protection against mercury toxicity for human seafood consumers (although selenium may be available in their diet from other sources). Moreover, smaller fish of a given species may provide greater protective benefits suggesting that those age classes that reside in more estuarine and coastal environments may present lower human health hazards (Burger et al., Reference Burger, Gochfeld and Fote2013). However, the variability of selenium to mercury molar ratios found within and across species makes it difficult to use this ratio in risk assessment, risk management and risk communication at the present time. Most governmental organizations that develop fish consumption advisories do not have the data on both mercury and selenium levels in individual fish which are necessary to determine the selenium to mercury molar ratio variation within and across species. It is difficult for risk assessors to develop advisories that are protective without an estimate of this variability.

FISH THAT OPTIMIZE POTENTIAL BENEFITS VS RISKS

Recent research is beginning to address the need to quantify the overall nutritional and toxicological value of different types of fish and shellfish based on concentrations of multiple nutrients and contaminants in edible tissues. A recent study found unique, relative concentrations of mercury, omega-3 fatty acids, and selenium, or mercury-nutrient signatures, across seafood taxa (Figure 3, Karimi et al., Reference Karimi, Fisher and Meliker2014). Specifically, salmon and forage fish (herring, anchovies and sardines) are high in EPA and DHA compared with other seafood (Figure 3). In contrast, predatory fish have higher mercury concentrations than lower trophic level fish but nutrient concentrations do not appear to differ as strongly by trophic level. Karimi et al. (Reference Karimi, Fisher and Meliker2014) found that these distinct mercury–nutrient signatures were reflected in the blood of seafood consumers based on their consumption habits. Most notably, consumers with a salmon-dominated diet had a high percentage of omega-3 fatty acids in their blood compared with other seafood consumers. Consumers who tended to eat top-predator fish had higher mercury, but similar nutrient concentrations in blood compared with consumers of lower trophic level seafood. These results suggest that consuming lower trophic level seafood can minimize the risk of mercury exposure without reducing the benefits of nutrient intake, and more broadly, demonstrate the value of examining nutrient and mercury exposure patterns simultaneously. Such research efforts are valuable in summarizing the largest signals among otherwise complex patterns of multiple nutrients and contaminants, but there is a need for a deeper understanding of these multivariate patterns at higher levels of taxonomic resolution. In some cases, the seafood categories used in this study include multiple species that share market names in order to compare mercury–nutrient signatures between edible seafood and seafood consumers. For example, salmon includes Atlantic salmon and multiple species of Pacific salmon, and tuna steak includes bigeye and yellowfin tuna (Karimi et al., Reference Karimi, Fisher and Meliker2014). Future studies that examine the composition of individual fish of the same species would complement these broader analyses by examining nutrient-contaminant patterns at greater taxonomic resolution, and in relation to ecological and environmental factors. In addition, better information on the taxonomic identity of market fish and shellfish would improve estimates of co-exposure to nutrients and contaminants in seafood consumers.

Fig. 3. Canonical discriminant analyses testing for differences in mercury-nutrient signatures among seafood items (from Karimi et al., Reference Karimi, Fisher and Meliker2014, reprinted with permission). Circles indicate 95% confidence limits for means of each seafood group and indicate the degree of difference among groups. Mercury and nutrient vectors (inset) represent the underlying structure of the axes. The position of circles relative to the direction of vectors indicates correlations between seafood groups and the concentration gradient of mercury or nutrients. Vector length indicates the overall contribution of mercury or nutrients in discriminating among seafood groups. Vector direction indicates the correlation of mercury or nutrient with each axis (vectors parallel to an axis are highly correlated with that axis). Angles between vectors represent correlations among mercury and nutrient concentrations. EPA, eicosapentaenoic acid; DHA, docosahexaenoic acid; Hg, mercury; Se, selenium.

Advice describing both the types and amounts of seafood consumption, while complex, is necessary to better manage risks and benefits of seafood consumption (Oken et al., Reference Oken, Wright, Kleinman, Bellinger, Amarasiriwardena, Hu, Rich-Edwards and Gillman2005; Gerber et al., Reference Gerber, Karimi and Fitzgerald2012). Seafood risk communication also requires risks and benefits to be considered together for appropriate context (Kuntz et al., Reference Kuntz, Ricco, Hill and Anderko2010; Turyk et al., Reference Turyk, Bhavsar, Bowerman, Boysen, Clark, Diamond, Mergler, Pantazopoulos, Schantz and Carpenter2012; Laird et al., Reference Laird, Goncharov, Egeland and Chan2013). Many fish advisories consider multiple chemical contaminants but provide minimal discussion of fish nutrients, focused on omega-3 fatty acids (Scherer et al., Reference Scherer, Tsuchiya, Younglove, Burbacher and Faustman2008). Compared with mercury concentrations, there are fewer studies quantifying fatty acids and selenium in seafood (Karimi et al., Reference Karimi, Fisher and Meliker2014). Therefore, to inform risk assessment more research is needed quantifying the risks and benefits associated with specific seafood consumption habits, such as considering the recommended daily consumption of seafood nutrients relative to reference doses (i.e. hazard quotients) of seafood contaminants (i.e. Gladyshev et al., Reference Gladyshev, Sushchik, Anishchenko, Makhutova, Kalachova and Gribovskaya2009).

To conduct appropriate human health risk assessment for contaminants such as mercury requires an understanding of how mercury, fish oils and selenium co-exposures affect the human body. This work can be informed by studies from marine biology and fisheries science, coupled with epidemiological biomonitoring, anthropological and food science investigations into the role of culinary preparation and gut processing on mercury and nutrient bioavailability (Laird et al., Reference Laird, Shade, Gantner, Chan and Siciliano2009; Moses et al., Reference Moses, Whiting, Bratton, Taylor and O'Hara2009a, Reference Moses, Whiting, Muir, Wang and O'Harab; Costa et al., Reference Costa, Afonso, Bandarra, Gueifão, Castanheira, Carvalho, Cardoso and Nunes2013). Acknowledging the concerns about contaminant exposure from seafood and its health benefits, the Joint FAO/WHO Expert Consultation on the Risks and Benefits of Fish Consumption (2010) recommended that government entities ‘Develop, maintain and improve existing databases on specific nutrients and contaminants, particularly methylmercury and dioxins, in fish consumed in their region’ and ‘Develop and evaluate risk management and communication strategies that both minimize risks and maximize benefits from eating fish’ (FAO/WHO, 2010, p. 33). Nevertheless, their general conclusions acknowledge fish as an important food source with clear benefits for reducing heart disease mortality and supporting optimal neurodevelopment in children.

CONCLUSIONS

Our current ability to properly estimate the risks and benefits to humans of seafood consumption are hampered by the common approaches of separately studying either contaminants or nutrients in fish. To date there are few studies in which fish tissue concentrations have been measured for both contaminants and nutrients across a range of species and geographic regions, even for the restricted set of chemicals considered in this review. There is tremendous variability between and within fish species in their mercury, EPA and DHA concentrations, leading to different versions of the ‘fish intake’ exposure across participants in epidemiological studies (Greenland & Robins, Reference Greenland and Robins2009), complicating the interpretation of studies on seafood health implications. Better characterizing the extent of interspecies and intraspecies variation of chemicals in fish may help inform future human exposure studies by allowing for more explicit accounting of measurement error (Spiegelman et al., Reference Strain, McAfee, van Wijngaarden, Thurston, Mulhern, McSorley, Watson, Love, Smith, Yost, Harrington, Shamlaye, Henderson, Myers and Davidson1997; Murad & Freedman, Reference Murad and Freedman2007; Guo et al., Reference Guo, Little and McConnell2012; Pollack et al., Reference Pollack, Perkins, Mumford, Ye and Schisterman2013). Furthermore, statistical methods are improving for epidemiological studies to incorporate source (i.e. seafood) contaminant levels, intake frequencies, toxicokinetic processes and biomarkers for an integrated exposure assessment (Conti et al., Reference Conti, Cortessis, Molitor and Thomas2003; Bartell & Johnson, Reference Bartell and Johnson2011; Tan et al., Reference Tan, Sobus, Chang, Tornero-Velez, Goldsmith, Pleil and Dary2012; Shin et al., Reference Shin, Steenland, Ryan, Vieira and Bartell2014); or to consider complex interactions between multiple seafood contaminants (Lynch et al., Reference Lynch, Huang, Cox, Strain, Myers, Bonham, Shamlaye, Stokes-Riner, Wallace, Duffey, Clarkson and Davidson2011) Thus, additional research on the joint distribution of multiple chemicals in marine foods has potential to contribute directly to future epidemiological investigations. Bringing multiple stakeholders (i.e. fish consumers and marine scientists) together in a trans-disciplinary conversation with health scientists can also help target the science to relevant questions and improve on knowledge translation (Boote et al., Reference Boote, Telford and Cooper2002; Burger et al., Reference Burger, Gochfeld and Fote2013). Future assessments of the risks and benefits of fish consumption will require more detailed understanding of exposures to both fish contaminants and nutrients as well as the environmental and ecological drivers that control their chemical transformations, and flow through marine food webs. The processes affecting composition of marine fish may be altered by climate change impacts including but not limited to ocean warming and ocean acidification (Edwards & Richardson, Reference Edwards and Richardson2004; Halpern et al., Reference Halpern, Walbridge, Selkoe, Kappel, Micheli, D'Agrosa, Bruno, Casey, Ebert, Fox, Fujita, Heinemann, Lenihan, Madin, Perry, Selig, Spalding, Steneck and Watson2008; Kroeker et al., Reference Kroeker, Gambi and Micheli2012); fishing (Micheli et al., Reference Micheli, De Leo, Butner, Martone and Shester2014); emerging joint exposures such as pharmaceuticals and personal care products potentially changing xenobiotic kinetics for some other compounds (Smital et al., Reference Smital, Luckenbach, Sauerborn, Hamdoun, Vega and Epel2004; Epel et al., Reference Epel, Stevenson, MacManus-Spencer, Luckenbach, Hamdoun and Smital2008; Bosnjak et al., Reference Bosnjak, Uhlinger, Heim, Smital, Franekic-Colic, Coale, Epel and Hamdoun2009); and future changes in contaminant sources and inputs (UNEP, 2013). Together, these changes indicate a need for continued research on fish nutrients and contaminants in marine and medical science, as well as ongoing communication between these disciplines.

FINANCIAL SUPPORT

MOG was supported on a training grant from the National Institute for Environmental Health Sciences (T32ES013678-07). RK's contribution was supported by the Gelfond Fund for Mercury Research and Outreach. MIG was supported by  project No. 6.1089.214/K of the Siberian Federal University, carried out according to Federal Tasks of Ministry of Education and Science of Russian Federation, and by Russian Federal Tasks of Fundamental Research (project No. 51.1.1). CYC's contribution was supported by NIH grant numbers P42 ES007373 and 1R01ES021950 from the National Institute of Environmental Health Sciences.

References

REFERENCES

Abd Aziz, N., Azlan, A., Ismail, A., Alinafiah, S.M. and Razman, M.R. (2013) Quantitative determination of fatty acids in marine fish and shellfish from warm water of straits of Malacca for nutraceutical purposes. BioMed Research International. Article 284329.CrossRefGoogle ScholarPubMed
Ackerman, J.T. and Eagles-Smith, C.A. (2009) Selenium bioaccumulation and body condition in shorebirds and terns breeding in San Francisco Bay, California, USA. Environmental Toxicology and Chemistry 28, 21342141.CrossRefGoogle Scholar
Adams, W.J., Brix, K.V., Edwards, M., Tear, L.M., DeForest, D.K. and Fairbrother, A. (2003) Analysis of field and laboratory data to derive selenium toxicity thresholds for birds. Environmental Toxicology and Chemistry 22, 20202029.CrossRefGoogle ScholarPubMed
Ahrens, L. and Bundschuh, M. (2014) Fate and effects of poly- and perfluoroalkyl substances in the aquatic environment: a review. Environmental Toxicology and Chemistry 33, 19211929.CrossRefGoogle ScholarPubMed
Alkazemi, D., Egeland, G.M., Roberts Ii, L.J., Chan, H.M. and Kubow, S. (2013) New insights regarding tissue Se and Mercury interactions on oxidative stress from plasma IsoP and IsoF measures in the Canadian Inuit population. Journal of Lipid Research 54, 19721979.CrossRefGoogle ScholarPubMed
Alonso, M.B., Azevedo, A., Torres, J.P., Dorneles, P.R., Eljarrat, E., Barceló, D., Lailson-Brito, J. Jr. and Malm, O. (2014) Anthropogenic (PBDE) and naturally-produced (MeO-PBDE) brominated compounds in cetaceans – a review. Science of the Total Environment 481, 619634.CrossRefGoogle ScholarPubMed
Amlund, H., Lundebye, A.K., Boyle, D. and Ellingsen, S. (2015) Dietary selenomethionine influences the accumulation and depuration of dietary methylmercury in zebrafish (Danio rerio). Aquatic Toxicology 158, 211217.CrossRefGoogle ScholarPubMed
Arts, M.T., Palmer, M.E., Skiftesvik, A.B., Jokinen, I.E. and Browman, H.I. (2012) UVB radiation variably affects n-3 fatty acids but elevated temperature reduces n-3 fatty acids in juvenile Atlantic salmon (Salmo salar). Lipids 47, 11811192.CrossRefGoogle ScholarPubMed
Axelrad, D.A., Bellinger, D.C., Ryan, L.M. and Woodruff, T.J. (2007) Dose-response relationship of prenatal mercury exposure and IQ: an integrative analysis of epidemiologic data. Environmental Health Perspectives 115, 609615.CrossRefGoogle ScholarPubMed
Bank, M.S., Chesney, E., Shine, J.P., Maage, A. and Senn, D.B. (2007) Mercury bioaccumulation and trophic transfer in sympatric snapper species from the Gulf of Mexico. Ecological Applications 17, 21002110.CrossRefGoogle ScholarPubMed
Barceloux, D.G. (1999) Selenium. Journal of Toxicology – Clinical Toxicology 37, 145172.CrossRefGoogle ScholarPubMed
Bartell, S.M. and Johnson, W.O. (2011) Estimating equations for biomarker based exposure estimation under non-steady state conditions. Environmental Health 10, 57.CrossRefGoogle ScholarPubMed
Basu, N., Goodrich, J.M. and Head, J. (2014) Ecogenetics of mercury: from genetic polymorphisms and epigenetics to risk assessment and decision-making. Environmental Toxicology and Chemistry 33, 12481258.CrossRefGoogle ScholarPubMed
Belanger, M.C., Mirault, M.E., Dewailly, E., Berthiaume, L. and Julien, P. (2008) Environmental contaminants and redox status of coenzyme Q10 and vitamin E in Inuit from Nunavik. Metabolism: Clinical and Experimental 57, 927933.CrossRefGoogle ScholarPubMed
Bender, N., Portmann, M., Heg, Z., Hofmann, K., Zwahlen, M. and Egger, M. (2014) Fish or n3-PUFA intake and body composition: a systematic review and meta-analysis. Obesity Reviews 15, 657665.CrossRefGoogle ScholarPubMed
Bergé, J.P. and Barnathan, G. (2005) Fatty acids from lipids of marine organisms: molecular biodiversity, roles as biomarkers, biologically active compounds, and economical aspects. Advances in Biochemical Engineering and Biotechnology 96, 49125.Google ScholarPubMed
Bjerregaard, P. and Christensen, A. (2012) Selenium reduces the retention of Methyl mercury in the brown shrimp Crangon crangon. Environmental Science and Technology 46, 63246329.CrossRefGoogle ScholarPubMed
Bjerregaard, P., Fjordside, S., Hansen, M.G. and Petrova, M.B. (2012) Dietary selenium reduces retention of methyl mercury in freshwater fish. Environmental Science and Technology 45, 97939798.CrossRefGoogle Scholar
Bogevik, A.S., Henderson, R.J., Mundheim, H., Olsen, R.E. and Tocher, D.R. (2011) The effect of temperature and dietary fat level on tissue lipid composition in Atlantic salmon (Salmo salar) fed wax ester-rich oil from Calanus finmarchicus. Aquaculture Nutrition 17, e781e788.CrossRefGoogle Scholar
Boote, J., Telford, R. and Cooper, C. (2002) Consumer involvement in health research: a review and research agenda. Health Policy 61, 213236.CrossRefGoogle ScholarPubMed
Bosnjak, I., Uhlinger, K.R., Heim, W., Smital, T., Franekic-Colic, J., Coale, K., Epel, D. and Hamdoun, A. (2009) Multidrug efflux transporters limit accumulation of inorganic, but not organic, mercury in sea Urchin embryos. Environmental Science and Technology 43, 83748380.CrossRefGoogle Scholar
Braune, B.M. (1987) Mercury accumulation in relation to size and age of Atlantic herring (Clupea harengus harengus) from the southwestern Bay of Fundy, Canada. Archives of Environmental Contamination and Toxicology 16, 311320.CrossRefGoogle Scholar
Buck, R.C., Franklin, J., Berger, U., Conder, J.M., Cousins, I.T., de Voogt, P., Jensen, A.A., Kannan, K., Mabury, S.A. and van Leeuwen, S.P.J. (2011) Perfluoroalkyl and polyfluoroalkyl substances in the environment: terminology, classification and origins. Integrated Environmental Assessment and Management 7, 513541.CrossRefGoogle ScholarPubMed
Burger, J. and Gochfeld, M. (2011) Mercury and selenium in 19 species of saltwater fish from New Jersey as a function of species, size, and season. Science of the Total Environment 409, 14181429.CrossRefGoogle Scholar
Burger, J. and Gochfeld, M. (2012) Selenium and mercury molar ratios in saltwater fish from New Jersey: individual and species variability complicate use in human health fish consumption advisories. Environmental Research 114, 1223.CrossRefGoogle ScholarPubMed
Burger, J., Gochfeld, M. and Fote, T. (2013) Stakeholder participation in research design and decisions: scientists, fishers, and mercury in saltwater fish. Ecohealth 10, 2130.CrossRefGoogle ScholarPubMed
Burger, J., Stern, A.H. and Gochfeld, M. (2005) Mercury in commercial fish: optimizing individual choice to reduce risk. Environmental Health Perspectives 113, 266271.CrossRefGoogle ScholarPubMed
Campbell, F., Dickinson, H.O., Critchley, J.A., Ford, G.A. and Bradburn, M. (2013) A systematic review of fish-oil supplements for the prevention and treatment of hypertension. European Journal of Preventive Cardiology 20, 107120.CrossRefGoogle ScholarPubMed
Carocci, A., Rovito, N., Sinicropi, M.S. and Genchi, G. (2014) Mercury toxicity and neurodegenerative effects. Reviews of Environmental Contamination and Toxicology 229, 118.Google ScholarPubMed
Castro-Gonzalez, I., Maafs-Rodriguez, A.G., Silencio-Barrita, J.L., Galindo-Gomez, C. and Perez-Gil, F. (2013) Evaluation of the possible inclusion of certain fish species in chronic kidney disease diets based on their adverse and beneficial nutrient ratios. International Journal of Food Sciences and Nutrition 64, 8288.CrossRefGoogle ScholarPubMed
Chapman, L. and Chan, H.M. (2000) The influence of nutrition on methyl mercury intoxication. Environmental Health Perspectives 108(Suppl. 1), 2956.Google ScholarPubMed
Chen, C.Y., Dionne, M., Mayes, B.M., Ward, D.M., Sturup, S. and Jackson, B. P. (2009) Mercury bioavailability and bioaccumulation in estuarine food webs in the Gulf of Maine. Environmental Science and Technology 43, 18041810.CrossRefGoogle ScholarPubMed
Chen, C.Y., Lai, C.C., Chen, K.S., Hsu, C.C., Hung, C.C. and Chen, M.H. (2014) Total and organic mercury concentrations in the muscles of Pacific Albacore (Thunnus Alalunga) and Bigeye Tuna (Thunnus Obesus). Marine Pollution Bulletin 85, 606612.CrossRefGoogle ScholarPubMed
Choi, A.L., Budtz-Jørgensen, E., Jørgensen, P.J., Steuerwald, U., Debes, F., Weihe, P. and Grandjean, P. (2007) Selenium as a potential protective factor against mercury developmental neurotoxicity. Environmental Research 107, 4552.CrossRefGoogle ScholarPubMed
Chuang, L.-T., Bulbul, U., Wen, P.-C., Glew, R.H. and Ayaz, F.A. (2012) Fatty acid composition of 12 fish species from the Black Sea. Journal of Food Science 77, C512C518.Google Scholar
Conti, D.V., Cortessis, V., Molitor, J. and Thomas, D.C. (2003) Bayesian modeling of complex metabolic pathways. Human Heredity 56, 8393.CrossRefGoogle ScholarPubMed
Cooper, L.T., Rader, V. and Ralston, N.V. (2007) The roles of selenium and mercury in the pathogenesis of viral cardiomyopathy. Congestive Heart Failure 13, 193199.CrossRefGoogle ScholarPubMed
Cossa, D., Harmelin-Vivien, M., Mellon-Duval, C., Loizeau, V., Averty, B., Crochet, S., Chou, L. and Cadiou, J.F. (2012) Influences of bioavailability, trophic position, and growth on methylmercury in hakes (Merluccius merluccius) from Northwestern Mediterranean and Northeastern Atlantic. Environmental Science and Technology 46, 48854893.CrossRefGoogle ScholarPubMed
Costa, S., Afonso, C., Bandarra, N.M., Gueifão, S., Castanheira, I., Carvalho, M.L., Cardoso, C. and Nunes, M.L. (2013) The emerging farmed fish species meagre (Argyrosomus regius): how culinary treatment affects nutrients and contaminants concentration and associated benefit-risk balance. Food and Chemical Toxicology 60, 277286.CrossRefGoogle ScholarPubMed
Crump, K.S., Kjellstrom, T., Shipp, A.M., Silvers, A. and Stewart, A. (1998) Influence of prenatal mercury exposure upon scholastic and psychological test performance: benchmark analysis of a New Zealand cohort. Risk Analysis 18, 701713.CrossRefGoogle ScholarPubMed
Cusick, K.D., and Sayler, G.S. (2013) An overview on the marine neurotoxin, saxitoxin: genetics, molecular targets, methods of detection and ecological functions. Marine Drugs 11, 9911018.CrossRefGoogle ScholarPubMed
Davidson, P.W., Myers, G.J., Cox, C., Axtell, C., Shamlaye, C., Sloane-Reeves, J., Cernichiari, E., Needham, L., Choi, A., Wang, Y., Berlin, M. and Clarkson, T.W. (1998) Effects of prenatal and postnatal methylmercury exposure from fish consumption on neurodevelopment: outcomes at 66 months of age in the Seychelles Child Development Study. Journal of the American Medical Association 280, 701707.CrossRefGoogle ScholarPubMed
Davidson, P.W., Myers, G.J., Weiss, B., Shamleye, C.F. and Cox, C. (2006) Prenatal methyl mercury exposure from fish consumption and child development: a review of evidence and perspectives from the Seychelles Child Development Study. Neurotoxicology 27, 11061109.CrossRefGoogle ScholarPubMed
Davidson, P.W., Strain, J.J., Myers, G.J., Thurston, S.W., Bonham, M.P., Shamlaye, C.F., Stokes-Riner, A., Wallace, J.M., Robson, P.J., Duffy, E.M., Georger, L.A., Sloane-Reeves, J., Cernichiari, E., Canfield, R.L., Cox, C., Huang, L.S., Janciuras, J. and Clarkson, T.W. (2008) Neurodevelopmental effects of maternal nutritional status and exposure to methylmercury from eating fish during pregnancy. Neurotoxicology 29, 767775.CrossRefGoogle ScholarPubMed
Deroma, L., Parpinel, M., Tognin, V., Channoufi, L., Tratnik, J., Horvat, M., Valent, F. and Barbone, F. (2013) Neuropsychological assessment at school-age and prenatal low-level exposure to mercury through fish consumption in an Italian birth cohort living near a contaminated site. International Journal of Hygiene and Environmental Health 216, 486493.CrossRefGoogle Scholar
Dickey, R.W. and Plakas, S.M. (2010) Ciguatera; a public health perspective. Toxicon 56, 123136.CrossRefGoogle ScholarPubMed
Dijkstra, J.A., Buckman, K.L., Ward, D., Evans, D.W., Dionne, M. and Chen, C.Y. (2013) Experimental and natural warming elevates mercury concentrations in estuarine fish. PloS ONE 8, e58401.CrossRefGoogle ScholarPubMed
Drescher, O., Dewailly, E., Diorio, C., Ouellet, N., Sidi, E.A., Abdous, B., Valera, B. and Ayotte, P. (2014) Methylmercury exposure, PON1 gene variants and serum paraoxonase activity in Eastern James Bay Cree adults. Journal of Exposure Science and Environmental Epidemiology 24, 608614.CrossRefGoogle ScholarPubMed
Edmonds, J.S. and Francesconi, K.A. (1993) Arsenic in seafoods: human health aspects and regulations. Marine Pollution Bulletin 26, 665674.CrossRefGoogle Scholar
Edwards, M. and Richardson, A.J. (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430, 881884.CrossRefGoogle ScholarPubMed
Epel, D., Stevenson, C.N., MacManus-Spencer, L.A., Luckenbach, T., Hamdoun, A. and Smital, T. (2008) Efflux transporters: newly appreciated roles in protection against pollutants. Environmental Science and Technology 42, 39143920.CrossRefGoogle ScholarPubMed
Eto, K., Takizawa, Y., Akagi, H., Haraguchi, K., Asano, S., Takahata, N. and Tokunaga, H. (1999) Differential diagnosis between organic and inorganic mercury poisoning in human cases – the pathologic point of view. Toxicologic Pathology 27, 664671.CrossRefGoogle ScholarPubMed
European Marine Board (2013) Linking oceans & human health: a strategic research priority for Europe. Position Paper 19 of the European Marine Board, Ostend, Belgium.Google Scholar
FAO (2014) The State of World Fisheries and Aquaculture 2014: Opportunities and Challenges. Rome: Food and Agriculture Organization of the United Nations. E-ISBN 978-92-5-108276-8.Google Scholar
FAO/WHO (2011) FAO Fisheries and Aquaculture Report No. 978. Report of the Joint FAO/WHO Expert Consultation on the Risks and Benefits of Fish Consumption. Rome: Food and Agriculture Organization of the United Nations; Geneva: World Health Organization. 50 pp.Google Scholar
Farina, M., Aschner, M. and Rocha, J.B. (2011) Oxidative stress in methylmercury-induced neurotoxicity. Toxicology and Applied Pharmacology 256, 405417.CrossRefGoogle Scholar
Fuschino, J.R., Guschina, I.A., Dobson, G., Yan, N.D., Harwood, J.L. and Arts, M.T. (2011) Rising water temperatures alter lipid dynamics and reduce N-3 essential fatty acid concentration in Scendesmus obliguus (Chlorophyta). Journal of Phycology 47, 763774.CrossRefGoogle Scholar
Ganther, H.E., Goudie, C., Sunde, M.L., Kopicky, M.J., Wagner, P., Oh, S.H. and Hoekstra, W.G. (1972) Selenium relation to decreased toxicity of methylmercury added to diets containing tuna. Science 175, 11221124.CrossRefGoogle ScholarPubMed
Garcia-Moreno, P.J., Perez-Galvez, R., Morales-Medina, R., Guadix, A. and Guadix, E.M. (2013) Discarded species in the west Mediterranean sea as sources of omega-3 PUFA. European Journal of Lipid Science and Technology 115, 982989.CrossRefGoogle Scholar
Gardner, R.M., Nyland, J.F., Evans, S.L., Wang, S.B., Doyle, K.M., Crainiceanu, C.M. and Silbergeld, E.K. (2009) Mercury induces an unopposed inflammatory response in human peripheral blood mononuclear cells in vitro. Environmental Health Perspectives 117, 19321938.CrossRefGoogle ScholarPubMed
Gardner, R.M., Nyland, J.F., Silva, I.A., Ventura, A.M., deSouza, J.M., and Silbergeld, E.K. (2010a) Mercury exposure, serum antinuclear/ antinucleolar autoantibodies, and serum cytokine levels in mining populations in Amazonian Brazil: a cross-sectional study. Environmental Research 104, 345354.CrossRefGoogle Scholar
Gardner, R.M., Nyland, J.F. and Silbergeld, E.K. (2010b) Differential immunotoxic effects of inorganic and organic mercury species in vitro. Toxicology Letters 198, 182190.CrossRefGoogle ScholarPubMed
Garthwaite, I. (2000) Keeping shellfish safe to eat: a brief review of shellfish toxins, and methods for their detection. Trends in Food Science and Toxicology 11, 235244.CrossRefGoogle Scholar
Gehrke, G. E., Blum, J. D. and Marvin-DiPasquale, M. (2011) Sources of mercury to San Francisco Bay surface sediment as revealed by mercury stable isotopes. Geochimica et Cosmochimica Acta 75, 691705.CrossRefGoogle Scholar
Gerber, L.R., Karimi, R. and Fitzgerald, T.P. (2012) Sustaining seafood for public health. Frontiers in Ecology and the Environment 10, 487493.CrossRefGoogle Scholar
Gladyshev, M.I., Anishchenko, O.V., Sushchnik, N.N., Kalacheva, G.S., Gribovskaya, I.V. and Ageev, A.V. (2012a) Influence of anthropogenic pollution on content of essential polyunsaturated fatty acids in links of food chain of river ecosystem. Contemporary Problems of Ecology 5, 376385.CrossRefGoogle Scholar
Gladyshev, M.I., Lepskaya, E.V., Sushchik, N.N., Makhutova, O.N., Kalachova, G.S., Malyshevskaya, K.K. and Markevich, G.N. (2012b) Comparison of polyunsaturated fatty acids content in filets of anadromous and landlocked sockeye salmon Oncorhynchus nerka. Journal of Food Science 77, C1306C1310.CrossRefGoogle ScholarPubMed
Gladyshev, M.I., Sushchik, N.N., Anishchenko, O.V., Makhutova, O.N., Kalachova, G.S. and Gribovskaya, I.V. (2009) Benefit-risk ratio of food fish intake as the source of essential fatty acids vs. heavy metals: a case study of Siberian grayling from the Yenisei River. Food Chemistry 115, 545550.CrossRefGoogle Scholar
Gladyshev, M.I., Sushchik, N.N., Anishchenko, O.V., Makhutova, O.N., Kolmakov, V.I., Kalachova, G.S., Kolmakova, A.A. and Dubovskaya, O.P. (2011) Efficiency of transfer of essential polyunsaturated fatty acids versus organic carbon from producers to consumers in a eutrophic reservoir. Oecologia 165, 521531.CrossRefGoogle Scholar
Gladyshev, M.I., Sushchik, N.N., Gubanenko, G.A., Demirchieva, S.M. and Kalachova, G.S. (2006) Effect of way of cooking on content of essential polyunsaturated fatty acids in muscle tissue of humpback salmon (Oncorhynchus gorbuscha). Food Chemistry 96, 446451.CrossRefGoogle Scholar
Gladyshev, M.I., Sushchik, N.N., Gubanenko, G.A., Demirchieva, S.M. and Kalachova, G.S. (2007) Effect of boiling and frying on the content of essential polyunsaturated fatty acids in muscle tissue of four fish species. Food Chemistry 101, 16941700.CrossRefGoogle Scholar
Gladyshev, M.I., Sushchik, N.N. and Makhutova, O.N. (2013) Production of EPA and DHA in aquatic ecosystems and their transfer to the land. Prostaglandins and Other Lipid Mediators 107, 117126.CrossRefGoogle ScholarPubMed
Gochfeld, M., Burger, J., Jeitner, C., Donio, M. and Pittfield, T. (2012) Seasonal, locational and size variations in mercury and selenium levels in striped bass (Morone saxatilis) from New Jersey. Environmental Research 112, 819.CrossRefGoogle ScholarPubMed
Grandjean, P., Weihe, P., Burse, V.W., Needham, L.L., Storr-Hansen, E., Heinzow, B., Debes, F., Murata, K., Simonsen, H., Ellefsen, P., Budtz-Jørgensen, E., Keiding, N. and White, R.F. (2001) Neurobehavioral deficits associated with PCB in 7-year-old children prenatally exposed to seafood neurotoxicants. Neurotoxicology and Teratology 23, 305317.CrossRefGoogle ScholarPubMed
Grandjean, P., Weihe, P., Debes, F., Choi, A.L. and Budtz-Jørgensen, E. (2014) Neurotoxicity from prenatal and postnatal exposure to methylmercury. Neurotoxicology and Teratology 43, 3944.CrossRefGoogle ScholarPubMed
Grandjean, P., Weihe, P., White, R.F., Debes, F., Araki, S., Murata, K., Sørensen, N., Dahl, D., Yokoyama, K. and Jørgensen, P.J. (1997) Cognitive deficit in 7-year-old children with prenatal exposure to methylmercury. Neurotoxicology and Teratology 19, 417428.CrossRefGoogle ScholarPubMed
Greenland, S. and Robins, J. (2009) Identifiability, exchangability and confounding revisited. Epidemiologic Perspectives and Innovations 6.CrossRefGoogle Scholar
Guallar, E., Sanz-Gallardo, M.I., van't Veer, P., Bode, P., Aro, A., Gómez-Aracena, J., Kark, J.D., Riemersma, R.A., Martín-Moreno, J.M., Kok, F.J. and the Heavy Metals and Myocardial Infarction Study Group (2002) Mercury, fish oils, and the risk of myocardial infarction. New England Journal of Medicine 347, 17471754.CrossRefGoogle ScholarPubMed
Guglielmo, F., Lammel, G. and Maier-Reimer, E. (2009) Global environmental cycling of gamma-HCH and DDT in the 1980s – a study using a coupled atmosphere and general ocean circulation model. Chemosphere 76, 15091517.CrossRefGoogle Scholar
Guo, Y., Little, R.J. and McConnell, D.S. (2012) On using summary statistics from an external calibration sample to correct for covariate measurement error. Epidemiology 23, 165174.CrossRefGoogle ScholarPubMed
Hallgren, C.G., Hallmans, G., Jansson, J.H., Marklund, S.L., Huhtasaari, F., Schütz, A., Strömberg, U., Vessby, B. and Skerfving, S. (2001) Markers of high fish intake are associated with decreased risk of a first myocardial infarction. British Journal of Nutrition 86, 397404.CrossRefGoogle ScholarPubMed
Halpern, B.S., Longo, C., Hardy, D., McLeod, K.L., Samhouri, J.F., Katona, S.K., Kleisner, K., Lester, S.E., O'Leary, J., Ranelletti, M., Rosenberg, A.A., Scarborough, C., Selig, E.R., Best, B.D., Brumbaugh, D.R., Chapin, F.S., Crowder, L.B., Daly, K.L., Doney Scott, C., Elfes, C., Fogarty, M.J., Gaines, S.D., Jacobsen, K.I., Karrer, L.B., Leslie Heather, M., Neeley, E., Pauly, D., Polasky, S., Ris, B., St. Martin, K., Stone, G.S., Sumaila, U.R. and Zeller, D. (2012) In index to assess the health and benefits of the global ocean. Nature 488, 615620.CrossRefGoogle ScholarPubMed
Halpern, B.S., Walbridge, S., Selkoe, K.A., Kappel, C.V., Micheli, F., D'Agrosa, C., Bruno, J.F., Casey, K.S., Ebert, C., Fox, H.E., Fujita, R., Heinemann, D., Lenihan, H.S., Madin, E.M.P., Perry, M.T., Selig, E.R., Spalding, M., Steneck, R. and Watson, R. (2008) A global map of human impacts on marine ecosystems. Science 321, 14461447.Google Scholar
Harada, M. (1995) Minamata disease: methylmercury poisoning in Japan caused by environmental pollution. Critical Reviews in Toxicology 25, 124.CrossRefGoogle ScholarPubMed
Hartweg, J., Perera, R., Montori, V., Dinneen, S., Neil, H.A. and Farmer, A. (2008) Omega-3 polyunsaturated fatty acids (PUFA) for type 2 diabetes mellitus. Cochrane Database of Systematic Reviews 1, CD003205.Google Scholar
Hladun, K.R., Kaftanoglu, O., Parker, D.R., Tran, K.D. and Trumble, J.T. (2013) Effects of selenium on development, survival, and accumulation in the honeybee (Aphis mellifera L.). Environmental Toxicology and Chemistry 23, 25842592.CrossRefGoogle Scholar
Hoffman, D.J. (2002) Role of selenium toxicity and oxidative stress in aquatic birds. Aquatic Toxicology 57, 1126.CrossRefGoogle ScholarPubMed
Huang, S.S., Strathe, A.B., Fadel, J.G., Johnson, M.L., Lin, P., Liu, T.Y. and Hung, S.S. (2013) The interactive effects of selenomethionine and methylmercury on their absorption, disposition, and elimination in juvenile white sturgeon. Aquatic Toxicology 126, 274282.CrossRefGoogle ScholarPubMed
Huguet, C.T., Norambuena, F., Emery, J.A., Hermon, K. and Turchini, G.M. (2015) Dietary n-6/n-3 LC-PUFA ratio, temperature and time interactions on nutrients and fatty acids digestibility in Atlantic salmon. Aquaculture 436, 160166.CrossRefGoogle Scholar
Huynh, M.D. and Kitts, D.D. (2009) Evaluating nutritional quality of pacific fish species from fatty acid signatures. Food Chemistry 114, 912918.CrossRefGoogle Scholar
Janssen, C.I. and Kiliaan, A.J. (2014) Long-chain polyunsaturated fatty acids (LCPUFA) from genesis to senescence: the influence of LCPUFA on neural development, aging, and neurodegeneration. Progress in Lipid Research 53, 117.CrossRefGoogle ScholarPubMed
Jeandel, C. and Minster, F. (1987) Chromium behavior in the oceans: global versus regional processes. Global Biogeochemical Cycles 1, 131154.CrossRefGoogle Scholar
Jiang, H. and Gao, K. (2004) Effects of lowering temperature during culture on the production of polyunsaturated fatty acids in the marine diatom Phaeodactylum tricornutum (Bacillariophyceae). Journal of Phycology 40, 651654.CrossRefGoogle Scholar
Jiao, J., Li, Q., Chu, J., Zeng, W., Yang, M. and Zhu, S. (2014) Effect of n-3 PUFA supplementation on cognitive function throughout the life span from infancy to old age: a systematic review and meta-analysis of randomized controlled trials. American Journal of Clinical Nutrition 100, 14221436.CrossRefGoogle ScholarPubMed
Kaneko, J.J. and Ralston, N.V.C. (2007) Selenium and mercury in pelagic fish in the central north pacific near Hawaii. Biological Trace Element Research 119, 242254.CrossRefGoogle ScholarPubMed
Karagas, M.R., Choi, A.L., Oken, E., Horvat, M., Schoeny, R., Kamai, E., Cowell, W., Grandjean, P. and Korrick, S. (2012) Evidence on the human health effects of low-level methylmercury exposure. Environmental Health Perspectives 120, 799806.CrossRefGoogle ScholarPubMed
Karimi, R., Fisher, N.S. and Folt, C.L. (2010) Multielement stoichiometry in aquatic invertebrates: when growth dilution matters. American Naturalist 176, 699709.CrossRefGoogle ScholarPubMed
Karimi, R., Fitzgerald, T.P. and Fisher, N.S. (2012) A quantitative synthesis of mercury in commercial seafood and implications for exposure in the United States. Environmental Health Perspectives 120, 15121519.CrossRefGoogle ScholarPubMed
Karimi, R., Frisk, M. and Fisher, N.S. (2013) Contrasting food web factor and body size relationships with Mercury and Se concentrations in marine biota. PloS ONE 9, e74695.CrossRefGoogle Scholar
Karimi, R., Fisher, N.S. and Meliker, J.R. (2014) Mercury-nutrient signatures in seafood and in the blood of avid seafood consumers. Science of the Total Environment 496, 636643.CrossRefGoogle ScholarPubMed
Kattner, G. and Hagen, W. (2009) Lipids in marine copepods: latitudinal characteristics and perspectives to global warming. In Arts, M.T., Kainz, M. and Brett, M.T. (eds) Lipids in aquatic ecosystems. New York, NY: Springer, pp. 147178.Google Scholar
Kjellström, T., Kennedy, P., Wallis, S. and Mantell, C. (1986) Physical and mental development of children with prenatal exposure to mercury from fish. Stage 1: Preliminary tests at age 4. Report 3030. Solna: National Swedish Environmental Board.Google Scholar
Kjellström, T., Kennedy, P., Wallis, S., Stewart, A., Friberg, L., Lind, B., Wutherspoon, T. and Mantell, C. (1989) Physical and mental development of children with prenatal exposure to mercury from fish. Stage 2: Interviews and psychological tests at age 6. Report 3642. Solna: National Swedish Environmental Board.Google Scholar
Kim, Y.N., Kim, Y.A., Yang, A.R. and Lee, B.H. (2014) Relationship between blood mercury level and risk of cardiovascular diseases: results from the Fourth Korea National Health and Nutrition Examination Survey (KHANES IV): 2008–2009. Preventive Nutrition and Food Science 19, 333342.CrossRefGoogle Scholar
Khan, M.A. and Wang, F. (2009) Mercury-selenium compounds and their toxicological significance: toward a molecular understanding of the mercury-selenium antagonism. Environmental Toxicology and Chemistry 28, 15671577.CrossRefGoogle Scholar
Kite-Powell, H.L., Fleming, L.E., Backer, L.C., Faustman, E.M., Hoagland, P., Tsuchiya, A., Younglove, L.R., Wilcox, B.A. and Gast, R.J. (2008) Linking the oceans to public health: current efforts and future directions. Environmental Health 7(Suppl. 2), S6.CrossRefGoogle ScholarPubMed
Kitson, A.P., Patterson, A.C., Izadi, H. and Stark, K.D. (2009) Pan-frying salmon in an eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) enriched margarine prevents EPA and DHA loss. Food Chemistry 114, 927932.CrossRefGoogle Scholar
Kroeker, K.J., Gambi, M.C. and Micheli, F. (2012) Ocean acidification causes ecosystem shifts via altered competitive interactions. Nature Climate Change 3, 156159.CrossRefGoogle Scholar
Kuntz, S.W., Ricco, J.A., Hill, W.G. and Anderko, L. (2010) Communicating methylmercury risks and fish consumption benefits to vulnerable childbearing populations. Journal of Obstetric, Gynecologic and Neonatal Nursing 39, 118126.CrossRefGoogle ScholarPubMed
Lail, E.M., Skrabal, S.A., Kieber, R.J., Bouillon, R.C. and Wright, J.L.C. (2007) The role of particles on the biogeochemical cycling of domoic acid and its isomers in natural water matricies. Harmful Algae 6, 651657.CrossRefGoogle Scholar
Laird, B.D., Goncharov, A.B., Egeland, G.M. and Chan, H.M. (2013) Dietary advice on Inuit traditional food use needs to balance benefits and risks of mercury, selenium, and n3 fatty acids. Journal of Nutrition 143, 923930.CrossRefGoogle ScholarPubMed
Laird, B.D., Shade, C., Gantner, N., Chan, H.M. and Siciliano, S.D. (2009) Bioaccessibility of mercury from traditional northern country foods measured using an in vitro gastrointestinal model is independent of mercury concentration. Science of the Total Environment 407, 60036008.CrossRefGoogle Scholar
Lau, D.C.P., Vrede, T., Pickova, J. and Goedkoop, W. (2012) Fatty acid composition of consumers in boreal lakes – variation across species, space and time. Freshwater Biology 57, 2438.CrossRefGoogle Scholar
Laurel, B.J., Copeman, L.A. and Parrish, C.C. (2012) Role of temperature on lipid/fatty acid composition on Pacific cod (Gadus macrocephalus) eggs and unfed larvae. Marine Biology 159, 20252034.CrossRefGoogle Scholar
Lemly, A.D. (2002) Symptoms and implications of selenium toxicity in fish: the Belews Lake case example. Aquatic Toxicology 57, 3949.CrossRefGoogle ScholarPubMed
Li, Y.F., Dong, Z., Chen, C., Li, B., Gao, Y., Qu, L., Wang, T., Fu, X., Zhao, Y. and Chai, Z. (2012) Organic selenium supplementation increases mercury excretion and decreases oxidative damage in long-term mercury-exposed residents from Wanshan, China. Environmental Science and Technology 46, 1131311318.CrossRefGoogle ScholarPubMed
Lowery, T. and Garrett, E.S. (2005) Synoptic survey of total mercury in recreational finfish of the Gulf of Mexico. NOAA Fisheries, Office of Sustainable Fisheries, National Seafood Inspection Laboratory.Google Scholar
Lynch, M.L., Huang, L.S., Cox, C., Strain, J.J., Myers, G.J., Bonham, M.P., Shamlaye, C.F., Stokes-Riner, A., Wallace, J.M., Duffey, E.M., Clarkson, T.W. and Davidson, P.W. (2011) Varying coefficient function models to explore interactions between maternal nutritional status and prenatal methylmercury toxicity in the Seychelles Child Development Nutrition Study. Environmental Research 111, 7580.CrossRefGoogle ScholarPubMed
Mahaffey, K.R. (2004) Fish and shellfish as dietary sources of methylmercury and the omega-3 fatty acids, eicosahexaenoic acid and docosahexaenoic acid: risks and benefits. Environmental Research 95, 414428.CrossRefGoogle ScholarPubMed
Mahaffey, K.R., Clickner, R.P. and Jeffries, R.A. (2009) Adult women's blood mercury concentrations vary regionally in the United States: association with patterns of fish consumption (NHANES 1999–2004). Environmental Health Perspectives 117, 4753.CrossRefGoogle ScholarPubMed
Makhutova, O.N., Sushchik, N.N., Gladyshev, M.I., Ageev, A.V., Pryanichnikova, E.G. and Kalachova, G.S. (2011) Is the fatty acid composition of freshwater zoobenthic invertebrates controlled by phylogenetic or trophic factors? Lipids 46, 709721.CrossRefGoogle ScholarPubMed
Mergler, D., Anderson, H.A., Chan, L.H., Mahaffey, K.R., Murray, M., Sakamoto, M., Stern, A.H. and the Panel on Health Risks and Toxicological Effects of Methylmercury (2007) Methylmercury exposure and health effects in humans: a worldwide concern. Ambio 36, 311.CrossRefGoogle ScholarPubMed
Micheli, F., De Leo, G., Butner, C., Martone, R.G. and Shester, G. (2014) A risk-based framework for assessing the cumulative impact of multiple fisheries. Biological Conservation 176, 224235.CrossRefGoogle Scholar
Moore, M.N., Depledge, M.H., Fleming, L., Hess, P., Lees, D., Leonard, P., Madsen, L., Owen, R., Pirlet, H., Seys, J., Vasconcelos, V., Viarengo, A. and the Marine Board-ESF Working Group on Oceans and Human Health (2013) Oceans and Human Health (OHH): a European perspective from the Marine Board of the European Science Foundation (Marine Board-ESF). Microbial Ecology 65, 889900.CrossRefGoogle ScholarPubMed
Moses, S.K., Whiting, A.V., Bratton, G.R., Taylor, R.J. and O'Hara, T.M. (2009a) Inorganic nutrients and contaminants in subsistence species of Alaska: linking wildlife and human health. International Journal of Circumpolar Health 68, 5374.CrossRefGoogle ScholarPubMed
Moses, S.K., Whiting, A.V., Muir, D.C., Wang, X. and O'Hara, T.M. (2009b) Organic nutrients and contaminants in subsistence species of Alaska: concentrations and relationship to food preparation method. International Journal of Circumpolar Health 68, 354371.CrossRefGoogle ScholarPubMed
Moths, M.D., Dellinger, J.A., Holub, B., Ripley, M.P., McGraw, J.E. and Kinnunen, R.E. (2013) Omega-3 fatty acids in fish from the Laurentian Great Lakes tribal fisheries. Human and Ecological Risk Assessment 19, 16281643.CrossRefGoogle Scholar
Mozaffarian, D. (2009) Fish, mercury, selenium and cardiovascular risk: current evidence and unanswered questions. International Journal of Environmental Research and Public Health 6, 18941916.CrossRefGoogle ScholarPubMed
Mozaffarian, D., Shi, P., Morris, J.S., Spiegelman, D., Grandjean, P., Siscovick, D.S., Willett, W.C. and Rimm, E.B. (2011) Mercury exposure and risk of cardiovascular disease in two U.S. cohorts. New England Journal of Medicine 364, 11161125.CrossRefGoogle ScholarPubMed
Murad, H. and Freedman, L.S. (2007) Estimating and testing interactions in linear regression models when explanatory variables are subject to classical measurement error. Statistics in Medicine 26, 42934310.CrossRefGoogle ScholarPubMed
Myers, G.J., Davidson, P.W., Cox, C., Shamlaye, C.F., Palumbo, D., Cernichiari, E., Sloane-Reeves, J., Wilding, G.E., Kost, J., Huang, L.S. and Clarkson, T.W. (2003) Prenatal methylmercury exposure from ocean fish consumption in the Seychelles child development study. Lancet 361, 16861692.CrossRefGoogle ScholarPubMed
Myers, G.J., Thurston, S.W., Pearson, A.T., Davidson, P.W., Cox, C., Shamlaye, C.F., Cernichiari, E. and Clarkson, T.W. (2009) Postnatal exposure to methyl mercury from fish consumption: a review and new data from the Seychelles Child Development Study. Neurotoxicology 30, 338349.CrossRefGoogle ScholarPubMed
Neff, J.M. (1997) Ecotoxicology of arsenic in the marine environment. Environmental Toxicology and Chemistry 16, 917927.Google Scholar
Oken, E., Wright, R.O., Kleinman, K.P., Bellinger, D., Amarasiriwardena, C.J., Hu, H., Rich-Edwards, J.W. and Gillman, M.W. (2005) Maternal fish consumption, hair mercury, and infant cognition in a U.S. Cohort. Environmental Health Perspectives 113, 13761380.CrossRefGoogle Scholar
Outzen, M., Tjønneland, A., Larsen, E.H., Andersen, K.K., Christensen, J., Overvad, K. and Olsen, A. (2015) The effect on selenium concentrations of a randomized intervention with fish and mussels in a population with relatively low habitual dietary selenium intake. Nutrients 7, 608624.CrossRefGoogle Scholar
Pase, M.P., Grima, N.A. and Sarris, J. (2011) Do long-chain n-3 fatty acids reduce arterial stiffness? A meta-analysis of randomised controlled trials. British Journal of Nutrition 106, 974980.CrossRefGoogle ScholarPubMed
Penglase, S., Hamre, K. and Ellingsen, S. (2014) Selenium and mercury have a synergistic negative effect on fish reproduction. Aquatic Toxicology 149, 1624.CrossRefGoogle ScholarPubMed
Peterson, S.A., Ralston, N.V.C., Whanger, P.D., Oldfield, J.E. and Mosher, W.D. (2009) Selenium and mercury interactions with emphasis on fish tissue. Environmental Bioindicators 4, 318334.CrossRefGoogle Scholar
Piraino, M.P. and Taylor, D.L. (2009) Bioaccumulation and trophic transfer of mercury in striped bass (Morone saxatilis) and tautog (Tautoga onitis) in the Narragansett Bay (Rhode Island, USA). Marine Environmental Research 67, 117128.CrossRefGoogle ScholarPubMed
Pollack, A.Z., Perkins, N.J., Mumford, S.L., Ye, A. and Schisterman, E.F. (2013) Correlated biomarker measurement error: an important threat to inference in environmental epidemiology. American Journal of Epidemiology 117, 8492.CrossRefGoogle Scholar
Power, M., Klein, G.M., Guiguer, K. and Kwan, M.K.H. (2002) Mercury accumulation in the fish community of a sub-Arctic lake in relation to trophic position and carbon sources. Journal of Applied Ecology 39, 819830.CrossRefGoogle Scholar
Prego-Faraldo, M.V., Valdiglesias, V., Méndez, J. and Eirín-López, J. (2013) Okadaic acid meet and greet: an insight into detection methods, response strategies and genotoxic effects in marine invertebrates. Marine Drugs 11, 28292845.CrossRefGoogle ScholarPubMed
Presser, T.S. and Luoma, S.N. (2010) A methodology for ecosystem-scale modeling of selenium. Integrated Environmental Assessment and Management 6, 685710.CrossRefGoogle ScholarPubMed
Ralston, N.V.C. (2008) Selenium health benefit values as seafood safety criteria. Ecohealth 5, 442455.CrossRefGoogle ScholarPubMed
Ralston, N.V.C., Blackwell, J.L. and Raymond, L.J. (2007) Importance of molar ratios in selenium-dependent protection against methylmercury toxicity. Biological Trace Element Research 119, 255268.CrossRefGoogle ScholarPubMed
Ralston, N.V.C. and Raymond, L.J. (2010) Dietary selenium's protective effects against methylmercury toxicity. Toxicology 278, 112123.CrossRefGoogle ScholarPubMed
Rice, G.E., Hammitt, J.K. and Evans, J.S. (2010) A probabilistic characterization of the health benefits of reducing methyl mercury intake in the United States. Environmental Science and Technology 44, 52165224.CrossRefGoogle ScholarPubMed
Rigby, M.C., Deng, X., Grieb, T.M., Teh, S.J. and Hung, S.S. (2010) Effect threshold for selenium toxicity in juvenile spittail, Pogonichthys macrolepidotus A. Bulletin of Environmental Contamination and Toxicology 84, 7679.CrossRefGoogle Scholar
Rizos, E.C., Ntzani, E.E., Bika, E., Kostapanos, M.S. and Elisaf, M.S. (2012) Association between omega-3 fatty acid supplementation and risk of major cardiovascular disease events: a systematic review and meta-analysis. Journal of the American Medical Association 308, 10241033.CrossRefGoogle ScholarPubMed
Roman, H.A., Walsh, T.L., Coull, B.A., Dewailly, É., Guallar, E., Hattis, D., Mariën, K., Schwartz, J., Stern, A.H., Virtanen, J.K. and Rice, G. (2011) Evaluation of the cardiovascular effects of methylmercury exposures: current evidence supports development of a dose-response function for regulatory benefits analysis. Environmental Health Perspectives 119, 607614.CrossRefGoogle ScholarPubMed
Sabino, P., Stranges, S. and Strazzullo, P. (2013) Does selenium matter in cardiometabolic disorders? A short review of the evidence. Journal of Endocrinological Investigation 36(10 Suppl.), 2127.Google Scholar
Saccone, G. and Berghella, V. (2015) Omega-3 supplementation to prevent recurrent preterm birth: a systematic review and meta-analysis of randomized controlled trials. American Journal of Obstetrics and Gynecology 213, 135140.CrossRefGoogle Scholar
Sahari, M.A., Farahani, F., Soleimanian, Y. and Javadi, A. (2014) Effect of frozen storage on fatty acid composition of the different tissues of four scombrid and one dussumeriid species. Journal of Applied Ichthyology 30, 381391.CrossRefGoogle Scholar
Sañudo-Wilhelmy, S.A., Gómez-Consarnau, L., Suffridge, C. and Webb, E.A. (2014) The role of B vitamins in marine biogeochemistry. Annual Review of Marine Science 6, 339367.CrossRefGoogle ScholarPubMed
Scherer, A.C., Tsuchiya, A., Younglove, L.R., Burbacher, T.M. and Faustman, E.M. (2008) Comparative analysis of state fish consumption advisories targeting sensitive populations. Environmental Health Perspectives 116, 15981606.CrossRefGoogle ScholarPubMed
Shaw, S.D. and Kannan, K. (2009) Polybrominated diphenyl ethers in marine ecosystems of the American continents: foresight from current knowledge. Reviews on Environmental Health 24, 157229.CrossRefGoogle ScholarPubMed
Sheehan, M.C., Burke, T.A., Navas-Acien, A., Breysse, P.N., McGready, J. and Fox, M.A. (2014) Global methylmercury exposure from seafood consumption and risk of developmental neurotoxicity: a systematic review. Bulletin of the World Health Organization 92, 254269F.CrossRefGoogle ScholarPubMed
Shenker, B.J., Berthold, P., Decker, S., Mayro, J., Rooney, C., Vitale, L. and Shapiro, I.M. (1992) Immunotoxic effects of mercuric compounds on human lymphocytes and monocytes. II. Alterations in cell viability. Immunopharmacology and Immunotoxicology 14, 555577.CrossRefGoogle ScholarPubMed
Shenker, B.J., Berthold, P., Rooney, C., Vitale, L., DeBolt, K. and Shapiro, I.M. (1993) Immunotoxic effects of mercuric compounds on human lymphocytes and monocytes. III. Alterations in B-cell function and viability. Immunopharmacology and Immunotoxicology 15, 87112.CrossRefGoogle ScholarPubMed
Shenker, B.J., Guo, T.L. and Shapiro, I.M. (1998) Low-level methylmercury exposure causes human T-cells to undergo apoptosis: evidence of mitochondrial dysfunction. Environmental Research 77, 149159.CrossRefGoogle ScholarPubMed
Shin, H.M., Steenland, K., Ryan, P.B., Vieira, V.M. and Bartell, S.M. (2014) Biomarker-based calibration of retrospective exposure predictions of perfluorooctanoic acid. Environmental Science and Technology 48, 56365642.CrossRefGoogle ScholarPubMed
Silva, I.A., Nyland, J.F., Gorman, A., Perisse, A., Ventura, A.M., Santos, E.C.O., de Souza, J.M., Burek, C.L., Rose, N.R. and Silbergeld, E.K. (2004) Mercury exposure, malaria, and serum antinuclear/antinucleolar antibodies in Amazon populations in Brazil: a cross-sectional study. Environmental Health 3, 1122.CrossRefGoogle ScholarPubMed
Sinensky, M. (1974) Homoviscous adaptation – a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proceedings of the National Academy of Sciences USA 71, 522525.CrossRefGoogle Scholar
Skjånes, K., Rebours, C. and Lindblad, P. (2013) Potential for green microalgae to produce hydrogen, pharmaceuticals and other high-value products in a combined process. Critical Reviews in Biotechnology 33, 172215.CrossRefGoogle Scholar
Smital, T., Luckenbach, T., Sauerborn, R., Hamdoun, A.M., Vega, R.L. and Epel, D. (2004) Emerging contaminants – pesticides, PPCPs, microbial degradation products and natural substances as inhibitors of multixenobiotic defense in aquatic organisms. Mutation Research 552, 101117.CrossRefGoogle ScholarPubMed
Somers, E.C., Ganser, M.A., Warren, J.S., Basu, N., Wang, L., Zick, S.M. and Park, S.K. (2015) Mercury exposure and antinucleolar antibodies among females of reproductive age in the United States: NHANES. Environmental Health Perspectives. http://dx.doi.org/10.1289/ehp.1408751.CrossRefGoogle Scholar
Snyder, R.J., Schregel, W.D. and Wei, Y. (2012) Effects of thermal acclimation on tissue fatty acid composition of freshwater alewives (Alosa pseudoharengus). Fish Physiology and Biochemistry 38, 363373.CrossRefGoogle ScholarPubMed
Sørmo, E.G., Ciesielski, T.M., Øverjordet, I.B., Lierhagen, S., Eggen, G.S., Berg, T. and Jenssen, B.J. (2011) Selenium moderates mercury toxicity in free-ranging freshwater fish. Environmental Science and Technology 45, 65616566.CrossRefGoogle ScholarPubMed
Stewart, A.R., Luoma, S.N., Schlekat, C.E., Doblin, M.A. and Hieb, K.A. (2004) Food web pathway determines how selenium affects aquatic ecosystems: a San Francisco Bay case study. Environmental Science and Technology 38, 45194526.CrossRefGoogle ScholarPubMed
Storelli, M.M. and Barone, G. (2013) Toxic metals (Hg, Pb, and Cd) in commercially important demersal fish from Mediterranean Sea: contamination levels and dietary exposure assessment. Journal of Food Science 78, T362T366.CrossRefGoogle ScholarPubMed
Strain, J.J., McAfee, A., van Wijngaarden, E., Thurston, S.W., Mulhern, M. S., McSorley, E.M., Watson, G.E., Love, T.M., Smith, T.H., Yost, K., Harrington, D., Shamlaye, C.F., Henderson, J., Myers, G.J. and Davidson, P.W. (2015) Prenatal exposure to methyl mercury from fish consumption and polyunsaturated fatty acids: associations with child development at 20 mo of age in an observational study in the Republic of Seychelles. American Journal of Clinical Nutrition 101, 530537 doi: 10.3945/ajcn.114.100503.CrossRefGoogle Scholar
Strain, J.J., Yeates, A.J., van Wijngaarden, E., Thurston, S.W., Mulhern, M.S., McSorley, E.M., Watson, G.E., Love, T.M., Smith, T.H., Yost, K., Harrington, D., Shamlaye, C.F., Spiegelman, D., McDermott, A. and Rosner, B. (1997) Regression calibration method for correcting measurement-error bias in nutritional epidemiology. American Journal of Clinical Nutrition 65(4 Suppl.), 1179S1186S.Google Scholar
Sunderland, E. M. (2007) Mercury exposure from domestic and imported estuarine and marine fish in the US seafood market. Environmental Health Perspectives 115, 235242.CrossRefGoogle ScholarPubMed
Tacon, A.G.J. and Metian, M. (2013) Fish matters: importance of aquatic foods in human nutrition and global food supply. Reviews in Fisheries Science 21, 2238.CrossRefGoogle Scholar
Tan, Y.M., Sobus, J., Chang, D., Tornero-Velez, R., Goldsmith, M., Pleil, J. and Dary, C. (2012) Reconstructing human exposures using biomarkers and other “clues”. Journal of Toxicology and Environmental Health, Part B: Critical Reviews 15, 2228.CrossRefGoogle ScholarPubMed
Tanaka, R., and Nakamura, T. (2012) Effects of exhaustive exercise on lipid peroxide and hyroxy lipids in yellowtail Seriola quinqueradiata. North American Journal of Aquaculture 74, 164168.CrossRefGoogle Scholar
Tanaka, R., Shigeta, K., Sugiura, Y., Hatate, H. and Matsushita, T. (2014) Accumulation of hydroxyl lipids and 4-hydroxy-2-hexenal in live fish infected with fish diseases. Lipids 49, 385396.CrossRefGoogle ScholarPubMed
Tatsuta, N., Nakai, K., Murata, K., Suzuki, K., Iwai-Shimada, M., Kurokawa, N., Hosokawa, T. and Satoh, H. (2014) Impacts of prenatal exposures to polychlorinated biphenyls, methylmercury, and lead on intellectual ability of 42-month-old children in Japan. Environmental Research 133, 321326.CrossRefGoogle ScholarPubMed
Taylor, D.L., Linehan, J.C., Murray, D.W. and Prell, W.L. (2012) Indicators of sediment and biotic mercury contamination in a southern New England estuary. Marine Pollution Bulletin 64, 807819.CrossRefGoogle Scholar
Teoh, M.L., Phang, S.M. and Chu, W.L. (2013) Response of Antarctic, temperate, and tropical microalgae to temperature stress. Journal of Applied Phycology 25, 285297.CrossRefGoogle Scholar
Thomas, J.K. and Janz, D.M. (2014) In ovo exposure to selenomethionine via maternal transfer increases developmental toxicities and impairs swim performance in F1 generation zebrafish (Danio rerio). Aquatic Toxicology 152, 2029.CrossRefGoogle ScholarPubMed
Thompson, P.A., Guo, M., Harrison, P.J. and Whyte, J.C. (1992) Effect of variation in temperature. II. On the fatty acid composition of eight species of marine phytoplankton. Journal of Phycology 28, 488497.CrossRefGoogle Scholar
Tremain, D.M. and Adams, D.H. (2012) Mercury in groupers and sea basses from the Gulf of Mexico: relationships with size, age, and feeding ecology. Transactions of the American Fisheries Society 141, 12741286.CrossRefGoogle Scholar
Turyk, M.E., Bhavsar, S.P., Bowerman, W., Boysen, E., Clark, M., Diamond, M., Mergler, D., Pantazopoulos, P., Schantz, S. and Carpenter, D.O. (2012) Risks and benefits of consumption of Great Lakes fish. Environmental Health Perspectives 120, 1118.CrossRefGoogle ScholarPubMed
Uauy, R., Hoffman, D.R., Peirano, P., Birch, D.G. and Birch, E.E. (2001) Essential fatty acids in visual and brain development. Lipids 36, 885895.CrossRefGoogle ScholarPubMed
Uchino, M., Hirano, T., Satoh, H., Arimura, K., Nakagawa, M. and Wakamiya, J. (2005) The severity of Minamata disease declined in 25 years: temporal profile of the neurological findings analyzed by multiple logistic regression model. Tohoku Journal of Experimental Medicine 205, 5363.CrossRefGoogle ScholarPubMed
UNEP (2013) Technical background report for the global mercury assessment 2013. Odder: Narayana Press.Google Scholar
Valent, F., Mariuz, M., Bin, M., Little, D., Mazej, D., Tognin, V., Tratnik, J., McAfee, A.J., Mulhern, M.S., Parpinei, M., Carrozzi, M., Horvat, M., Tamburlini, G. and Barbone, F. (2013) Associations of prenatal mercury exposure from maternal fish consumption and polyunsaturated fatty acids with child neurodevelopment: a prospective cohort study in Italy. Journal of Epidemiology 23, 360370.CrossRefGoogle ScholarPubMed
van Wijngaarden, E., Beck, C., Shamlaye, C.F., Cernichiari, E., Davidson, P.W., Myers, G.J. and Clarkson, T.W. (2006) Benchmark concentrations for methyl mercury obtained from the 9-year follow-up of the Seychelles Child Development Study. Neurotoxicology 27, 702709.CrossRefGoogle ScholarPubMed
Vinceti, M., Dennert, G., Crespi, C.M., Zwahlen, M., Brinkman, M., Zeegers, M.P., Horneber, M., D'Amico, R. and Del Giovane, C. (2014) Selenium for preventing cancer. Cochrane Database of Systematic Reviews 3, CD005195.Google Scholar
Virtanen, J.K., Voutilainen, S., Rissanen, T.H., Mursu, J., Tuomainen, T.P., Korhonen, M.J., Valkonen, V.P., Seppänen, K., Laukkanen, J.A. and Salonen, J.T. (2005) Mercury, fish oils, and risk of acute coronary events and cardiovascular disease, coronary heart disease, and all-cause mortality in men in Eastern Finland. Arteriosclerosis, Thrombosis, and Vascular Biology 25, 228233.CrossRefGoogle ScholarPubMed
Xin, W., Wei, W. and Li, X. (2012) Effect of fish oil supplementation on fasting vascular endothelial function in humans: a meta-analysis of randomized controlled trials. PLoS ONE 7, e46028.CrossRefGoogle ScholarPubMed
Xin, W., Wei, W. and Li, X.Y. (2013) Short-term effects of fish-oil supplementation on heart rate variability in humans: a meta-analysis of randomized controlled trials. American Journal of Clinical Nutrition 97, 926935.CrossRefGoogle ScholarPubMed
Wang, C., Harris, W.S., Chung, M., Lichtenstein, A.H., Balk, E.M., Kupelnick, B., Jordan, H.S. and Lau, J. (2006) n-3 fatty acids from fish or fish oil supplements, but not alpha-linolenic acid, benefit cardiovascular disease outcomes in primary- and secondary-prevention studies: a systematic review. American Journal of Clinical Nutrition 84, 517.CrossRefGoogle Scholar
Wen, W., Huang, X., Chen, Q. and Feng, L. (2013) Temperature effects on early development and biochemical dynamics of the marine fish, Inimicus japonicus. Journal of Experimental Marine Biology 442, 2229.CrossRefGoogle Scholar
Yamashita, M., Yamashita, Y., Suzuki, T., Kani, Y., Mizusawa, N., Imamura, S., Takemoto, K., Hara, T., Hossain, M.A., Yabu, T. and Touhata, K. (2013) Selenoneine, a novel selenium-containing compound, mediates detoxification mechanisms against methylmercury accumulation and toxicity in zebrafish embryo. Marine Biotechnology 15, 559570.CrossRefGoogle ScholarPubMed
Yogui, G.T. and Sericano, J.L. (2009) Polybrominated diphenyl ether flame retardants in the U.S. marine environment – a review. Environment International 35, 655666.CrossRefGoogle ScholarPubMed
Zheng, J.S., Hu, X.J., Zhao, Y.M., Yang, J. and Li, D. (2013) Intake of fish and marine n-3 polyunsaturated fatty acids and risk of breast cancer: meta-analysis of data from 21 independent prospective cohort studies. British Medical Journal 346, f3706.CrossRefGoogle ScholarPubMed
Zhu, W., Dong, C., Du, H., Zhang, H., Chen, J., Hu, X. and Hu, F. (2014) Effect of fish oil on serum lipid profile in dialysis patients: a systematic review and meta-analysis of randomized controlled trials. Lipids in Health and Disease 13, 127.CrossRefGoogle ScholarPubMed
Figure 0

Table 1. Major cohort studies examining early-life methylmercury (MeHg) and total mercury (Hg) exposure and neurodevelopment in children. IQR, inter-quartile range (25th to 75th percentile).

Figure 1

Table 2. Content of eicosapentaenoic (EPA) and docosahexaenoic (DHA) acids (mg g−1, wet weight) in various wild fish species, their types of habitat (H1: p, pelagic, bp, benthopelagic, d, demersal; H2: c, cold waters, t, temperate waters; w, warm waters) and size (cm). Orders and species are ranged by EPA + DHA content values.

Figure 2

Fig. 1. Contents of eicosapentaenoic acid (EPA) + docosahexaenoic acid (DHA) in fish orders: minimum, maximum and median values and quartiles. Number of species, N: order Clupeiformes, N = 9; order Salmoniformes, N = 3; order Perciformes, N = 36; order Scorpaeniformes, N = 3; order Gadiformes, N = 4; miscellaneous (orders Osmeriformes, Pleuronectiformes, Siluriformes, Mugiliformes, Beloniformes and Myliobatiformes), N = 8.

Figure 3

Fig. 2. Areas of eicosapentaenoic acid (EPA) vs docosahexaenoic acid (DHA) A levels in fish species from diverse habitats: pelagic warm water species (number of species, N = 17, violet), pelagic temperate water species (N = 10, black), demersal warm water species (N = 15, green), demersal temperate water species (N = 10, blue) and cold water species (N = 6, red).

Figure 4

Fig. 3. Canonical discriminant analyses testing for differences in mercury-nutrient signatures among seafood items (from Karimi et al., 2014, reprinted with permission). Circles indicate 95% confidence limits for means of each seafood group and indicate the degree of difference among groups. Mercury and nutrient vectors (inset) represent the underlying structure of the axes. The position of circles relative to the direction of vectors indicates correlations between seafood groups and the concentration gradient of mercury or nutrients. Vector length indicates the overall contribution of mercury or nutrients in discriminating among seafood groups. Vector direction indicates the correlation of mercury or nutrient with each axis (vectors parallel to an axis are highly correlated with that axis). Angles between vectors represent correlations among mercury and nutrient concentrations. EPA, eicosapentaenoic acid; DHA, docosahexaenoic acid; Hg, mercury; Se, selenium.