Sustainability, Security and Safety in the Feed-to-Fish Chain: Focus on Toxic Contamination
The paper discusses the issue of feed ingredients in aquaculture as a telling example of implementation of a sustainable food safety strategy, aimed at protecting the health of next generation, under the One Health paradigm. Finfish and fishery products are a main nutrition security component as a valuable source of animal protein, particularly in developing countries. In addition, they are a critical source of essential oligo-nutrients, such as polyunsaturated fatty acids (PUFAs) and iodine. Production and consumption of fish has greatly increased in the last decade, mostly due to the growth of aquaculture. While the demand for aquaculture products continues to increase, there is the need to address consumers' concerns related to the nutritional quality and safety. In fact, both wild and farmed finfish can represent a significant source of exposure to contaminants for the consumer: noticeably, caught and farmed fish have a comparable content of nutrients and contaminants. Aquaculture feeds made of fish meal and fish oil are the main vehicle for transfer of environmental pollutants to farmed fish. The main fish contaminants (e.g., methylmercury, PCBs, PBDE) can bioaccumulate and affect development in humans. Feed ingredients as well fish species have a different liability to contamination depending, e.g., on the lipophilicity of the specific chemicals. Up-to-date risk-benefit assessments show that high intake of fish may lead to an undesirable intake of pollutants which is not sufficiently balanced by the concurrent intake of protective nutrients, such as PUFA. The use of vegetable-based feed ingredients in aquaculture has been explored from the standpoints of economic sustainability and fish productivity to a greater extent than from those of food safety and nutritional value. Available data show that vegetable oils can significantly modulate the lipid profile in fish flesh, depending on the oil and fish species. The use of vegetable ingredients can drastically reduce the accumulation of the main contaminants in fish; likewise the presence of other “unconventional” contaminants (e.g. PAHs) and the nutritional value of fish flesh could deserve more attention in the assessment of novel aquaculture feeds.
Sustainability, Security and Safety in the Feed-to-Fish Chain: Focus on Toxic Contamination, International Journal of Nutrition and Food Sciences. Special Issue: Human and Animal Exposures to Food and Feed Contaminants.
Vol. 4, No. 2-2,
2015, pp. 6-24.
Frazzoli C., Petrini C., Mantovani A. (2009). Sustainable development and next generation’s health: a long-term perspective about the consequences of today's activities for food safety. Annali Istituto Superiore Sanita. 45(1):65-75.
World Food Summit (1996), http://www.who.int/trade/glossary/story028/en/
Frazzoli C., Mantovani A. (2010). Toxicants Exposures as Novel Zoonoses: Reflections on Sustainable Development, Food Safety and Veterinary Public Health. Zoonoses Public Health. 7-8: e136-e142.
Commission of the European Communities (2000). White Paper on Food Safety. Brussels, 12 January 2000, COM (1999) 719 final.
La Rocca C., Mantovani A. (2006). From environment to food: the case of PCB. Annali Istituto Superiore Sanità. 42(4):410-6.
Mantovani A., Maranghi F., Purificato I., Macrì A. (2006) Assessment of feed additives and contaminants: an essential component of food safety. Annali Ististuto Superiore Sanità. 42(4):427-32.
Mantovani A., Frazzoli C. (2010). Risk assessment of contaminants in animal feed. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources. 5(46): 1-14.
Mantovani A (2012). Chemical risk assessment of animal feed. In: Animal feed contamination: Effects on livestock and food safety (ed. by Johanna Fink-Gremmels). Woodhead Publishing Series in Food Science, Technology and Nutrition, 215: 449-63.
EFSA (2005). Opinion of the Scientific Panel on Additives and Products or Substances used in Animal Feed on the request from the Commission on the use of iodine in feedingstuffs. The EFSA Journal, 168, 1- 42.
EFSA (2008). Consequences for the consumer of the use of vitamin A in animal nutrition. Scientific Opinion of the Panel on Additives and Products or Substances used in Animal Feed. The EFSA Journal, 873, 1-81.
EFSA (2009). Scientific Opinion on the use of cobalt compounds as additives in animal nutrition. The EFSA Journal, 7(12):1383.
EFSA (2014). Scientific Opinion on the potential reduction of the currently authorized maximum zinc content in complete feed. The EFSA Journal, 12(5):3668.
FAO (2012). The state of world fisheries and aquaculture.
EFSA ( 2005). Opinion of the Scientific Panel on contaminants in the food chain [CONTAM] related to the safety assessment of wild and farmed fish. The EFSA Journal, 236, 1-118.
EFSA (2014). Scientific Opinion on health benefits of seafood (fish and shellfish) consumption in relation to health risks associated with exposure to methylmercury. The EFSA Journal, 12 (7): 3761.
EFSA (2014). Scientific Opinion on Dietary Reference Values for iodine. The EFSA Journal, 12 (5): 3660.
EFSA (2014). Scientific Opinion on Dietary Reference Values for selenium. The EFSA Journal, 12 (10): 3846.
EFSA (2012). Scientific Opinion on the Tolerable Upper Intake Level of vitamin D. The EFSA Journal, 10 (7): 2813.
FAO. The International Network of Food Data System. Food Composition Tables – Europe (http://www.fao.org/infoods/tables_europe_en.stm
EFSA 2009. Scientific Opinion on the use of cobalt compounds as additives in animal Nutrition. EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP). The EFSA Journal, 2009; 7 (12):1383.
FAO 2010. The State of World Fisheries and Aquaculture, 197p.
Arthur J.R., Bondad-Reantaso M.G., Campbell M.L., Hewitt C.L., Phillips M.J. and Subasinghe R.P. (2009). Understanding and applying risk analysis in aquaculture: a manual for decision-makers. FAO Fisheries and Aquaculture Technical 519/1, pp. 113.
Brander K. M. (2007). Global fish production and climate change. Proceedings of the National Academy of Sciences, 104(50), 19709–19714.
Bostock J., Murray F., Muir J., Telfer T., Lane A., Papanikos N. and Papegeorgiou P. (2009). European Aquaculture Competitiveness: Limitations and Possible Strategie. EU Parliament, Policy Department B: Structural and Cohesion Policies, Bruxelles, p. 136.
Barazi-Yeroulanos L. (2010). Regional synthesis of the Mediterranean marine finfish aquaculture sector and development of a strategy for marketing and promotion of Mediterranean aquaculture (MedAquaMarket). Studies and Review. General Fisheries Commission for the Mediterranean No. 88, pp. 198.
European Environment Agency - EEA, 2010.
ISMEA (2009). Il settore ittico in Italia - Check-up 2010, Roma, pp. 50.
EFSA (2009). Scientific Opinion on Arsenic in Food. The EFSA Journal 2009; 7(10):1351.
Gasull M., Bosch de Basea M., Puigdomènech E., Pumarega J., Porta M. (2011). Empirical analyses of the influence of diet on human concentrations of persistent organic pollutants: a systematic review of all studies conducted in Spain. Environment International, 37(7), 1226-35.
Mckeown D., 2006. Fish Consumption Benefits and Risks for Women in Childbearing Years and Young Children.
Maranghi F., Mantovani A. (2012). Targeted toxicological testing to investigate the role of endocrine disrupters in puberty disorders. Reproductive Toxicology, 33(3):290-6; 1.
Fucic A., Mantovani A. (2014). Puberty dysregulation and increased risk of disease in adult life: possible modes of action. Reproductive Toxicology, 44C:15-22.
Tacon A.G., Metian M. (2009). Fishing for feed or fishing for food: increasing global competition for small pelagic forage fish. Ambio 38 (6), 294-302.
Freire C., Ramos R., Lopez-Espinosa M.J., Dıez S., Vioque J., and Ballester F., Fernandez M.F. (2010). Hair mercury levels, fish consumption, and cognitive development in preschool children from Granada, Spain. Environmental Research Letters , 110, 96–104.
Ramon R., Murcia M., Aguinagalde X., Amurrio A., Llop S., Ibarluzea J., Lertxundi A., Alvarez-Pedrerol M., Casas M., Vioque J., Sunyer J., Tardon A., Martinez-Arguelles B., Ballester F. (2011). Prenatal mercury exposure in a multicenter cohort study in Spain. Environmental International, 37, 597–604.
EFSA (2008). Mercury as undesirable substance in animal feed. Scientific opinion of the Panel on Contaminants in the Food Chain. The EFSA Journal 654, 1-76.
Díez S. (2009). Human health effects of methylmercury exposure. Reviews of Environmental Contamination and Toxicology, 198, 111-32.
EFSA (2012). Scientific Opinion on the risk for public health related to the presence of mercury and methylmercury in food. The EFSA Journal, 10(12):2985.
Ceccatelli S., Daré E., Moors M. (2010). Methylmercury-induced neurotoxicity and apoptosis. Chemico-Biological Interactions, 188(2), 301-8.
Murata K., Yoshida M., Sakamoto M., Iwai-Shimada M., Yaginuma-Sakurai K., Tatsuta N., Iwata T., Karita K., Nakai K. (2011). Recent evidence from epidemiological studies on methylmercury toxicity. Nihon Eiseigaku Zasshi, 66(4), 682-95.
Debes F., Budtz-Jorgensen E., Weihe P., White R., Grandjean P. (2006). Impact of prenatal methylmercury exposure on neurobehavioral function at age 14 years. Neurotoxicology and Teratology, 28, 536-47.
Choi A.L., Cordier S., Weihe P., Grandjean P.(2008). Negative Confounding in the Evaluation of Toxicity: The Case of Methylmercury in Fish and Seafood. Critical Reviews in Toxicology, 38, 877–893.
Cheuk D.K., and Wong V. (2006). Attention-deficit hyperactivity disorder and blood mercury level: a case–control study in Chinese children. Neuropediatrics. 37, 234–40.
Davidson P.W., Myers G.J., Cox C., Wilding G.E., Shamlaye C.F., Huang L.S., Cenichiari E., Sloane-Reeves J., Palumbo D., Clarkson T.W. (2006). Methylmercury and neurodevelopment: longitudinal analysis of the Seychelles child development cohort. Neurotoxicology and Teratology, 28, 529-35.
Mozaffarian D., Rimm E.B.(2006). Fish intake, contaminants and human health-Evaluating the risks and the benefits. JAMA, 296 (15), 1885–1899.
Salonen J.T., Seppanen K., Lakka T.A., Salonen R., and Kaplan G.A. (2000). Mercury accumulation and accelerated progression of carotid atherosclerosis: a population-based prospective 4-year follow-up study in men in eastern Finland. Atherosclerosis, 148, 265–273.
Virtanen J.K., Voutilainen S., Rissanen T.H., Mursu J., Tuomainen T.P., Korhonen M.J.,Volkonen V.P., Sepp¨anen 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, 228–233.
Virtanen, J.K., Rissanen, T.H., Voutilainen, S., Tuomainen, T.P. (2007). Mercury as a risk factor for cardiovascular diseases. J Nutr Biochem 18, 75-85.
FAO/WHO (Food and Agriculture Organization of the United Nations/World Health Organization), (2011). Safety evaluation of certain food additives and contaminants. Methylmercury. WHO Food Additives Series, 63, 605-684.
Munthe J., Wängberg I., Rognerud S., Fjeld E., Verta M., Porvari P. and Meili M. (2007). Mercury in Nordic ecosystems IVL Swedish Environmental Research Institute Ltd. IVL Report B1761. Available from http://www.norden.org/en/nordic-council-of-ministers/councils-of-ministers/nordic-council-of ministers-for-the-environment-mr-m/institutes-co-operative-bodies-and-working-groups/working groups/working-group-for-aquatic-ecosystem-aeg/mercury-in-nordic-ecosystems.).
Ciardullo S., Aureli F., Coni E., Guandalini E., Iosi F., Raggi A., Rufo G. and Cubadda F. (2008). Bioaccumulation Potential of Dietary Arsenic, Cadmium, Lead, Mercury, and Selenium in Organs and Tissues of Rainbow Trout (Oncorhyncus mykiss) as a Function of Fish Growth. Journal of Agricultural and Food Chemistry, 56(7):2442-51.
EFSA (2008). Mercury as undesirable substance in animal feed. Scientific opinion of the Panel on Contaminants in the Food Chain. The EFSA Journal, 654, 1-76
Måge A., Julshamn, K., Hemre G.-I. and Lunestad B.T. (2005). Årsrapport 2004. Overvåkningsprogram for fôrvarer til fiskog akvatiske dyr. http://www.mattilsynet.no.
Måge A., Julshamn K., Hemre G.-I. and Lunestad B.T. (2006). Årsrapport 2005. Overvåkningsprogram for fôrvarer til fiskog akvatiske dyr. http://www.mattilsynet.no
Måge A., Julshamn K., Hemre G.-I. and Lunestad B.T. (2007). Årsrapport 2006. Overvåkningsprogram for fôrvarer til fisk og akvatiske dyr. http://www.nifes.no
EFSA (2010). Results of the monitoring of dioxin levels in food and feed. The EFSA Journal, 8(3), 1385.
Shibamoto T., Yasuhara A., Katami T. (2007). Dioxin formation from waste incineration. Reviews of Environmental Contamination and Toxicology, 190, 1-41.
Pizzin G., Bentley S. (2006). Diossine, Furani PCB e alimenti di origine animale: Stato dell’arte. Ann. Fac. Medic. Vet. di Parma 26, 247 – 264.
EFSA (2011). Scientific Opinion on the risk to public health related to the presence of high levels of dioxins and dioxin-like PCBs in liver from sheep and deer. The EFSA Journal, 9(7), 2297.
Larsen J.C. (2006). Risk assessments of polychlorinated dibenzo- p-dioxins, polychlorinated dibenzofurans, and dioxin-like polychlorinated biphenyls in food. Molecular Nutrition & Food Research, 50(10), 885-96.
Connor K.T., Aylward L.L. (2006). Human response to dioxin: aryl hydrocarbon receptor (AhR) molecular structure, function, and dose-response data for enzyme induction indicate an impaired human AhR. Journal of Toxicology and Environmental Health, 9(2), 147-71.
Denison M.S., Pandini A., Nagy S.R., Baldwin E.P., and Bonati L. (2002). Ligand binding and activation of the Ah receptor. Chemico-Biological Interactions, 141, 3-24.
EC (European Commission) (2000). Opinion of the Scientific Committee on animal nutrition SCAN on the dioxin contamination of feeding stuffs and their contribution to the contamination of food of animal origin. http://europa.eu.int/comm/food/fs/sc/scan/outcome.en.html
Lu H., Crawford R.B., Suarez-Martinez J.E., Kaplan B.L., Kaminski N.E. (2010). Induction of the aryl hydrocarbon receptor-responsive genes and modulation of the immunoglobulin M response by 2,3,7,8-tetrachlorodibenzo-p-dioxin in primary human B cells. Toxicological Sciences, 118(1), 86-97.
Cok I., Donmez M.K., Satiroğlu M.H., Aydinuraz B., Henkelmann B., Shen H., Kotalik J., Schramm K.W. (2008). Concentrations of polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), and dioxin-like PCBs in adipose tissue of infertile men. Archives of Environmental Contamination and Toxicology, 55(1), 143-52.
Darras V.M. (2008). Endocrine disrupting polyhalogenated organic pollutants interfere with thyroid hormone signalling in the developing brain. Cerebellum 7(1), 26-37.
Zoeller R.T. (2007). Environmental chemicals impacting the thyroid: targets and consequences. Thyroid, 17(9), 811-7.
Belpomme D., Irigaray P., Hardell L., Clapp R., Montagnier L., Epstein S., Sasco A.J. (2007). The multitude and diversity of environmental carcinogens. Environmental Research, 105, 414–429.
EFSA (2011). Scientific Opinion on the risk to public health related to the presence of high levels of dioxins and dioxin-like PCBs in liver from sheep and deer. The EFSA Journal, 9(7), 2297.
Karl H., Ruoff U., Blüthgen A. (2003). Transfer of PCDDs and PCDFs into the edible parts of farmed rainbow trout, Oncorhynchus mykiss (Walbaum), via feed. Aquaculture Research, 34: 1009-1014.
Isosaari P., Kiviranta H., Lie O., Lundebye A.-K., Ritchie G., Vartiainen T. (2004). Accumulation and distribution of polychlorinated dibenzo-p-dioxin, dibenzofuran, andpolychlorinated biphenyl congeners in Atlantic salmon (Salmo Salar). Environmental Toxicology and Chemistry, 23 (7): 1672-1679.
Lundebye A.-K., Bernttsen M.H.G., Lie O., Ritchi e G., Isosaari P., Kiviranta H., Vartiainen T. (2004). Dietary uptake of dioxins (PCDD/PC DFs) and dioxin-like PCBs in Atlantic salmon (Salmo Salar). Aquaculture Nutrition, 10: 199-207.
Isosaari P., Vartiainen T., Hallikainen A., Ruohonen K. (2002). Feeding trial on rainbow trout: comparison of dry fish feed and Baltic herring as a source of PCDD/Fs and PCBs. Chemosphere, 48 (8): 795-804.
La Rocca C., Mantovani A. (2006). From environment to food: the case of PCB. Annali Istituto Superiore Sanità, 42(4):410-6.
Glauert H.P., Tharappel J.C., Lu Z., Stemm D., Banerjee S., Chan L.S., Lee E.Y., Lehmler H.J., Robertson L.W., Spear B.T. (2008). Role of Oxidative Stress in the Promoting Activities of PCBs. Environmental Toxicology and Pharmacology, 25(2), 247-250.
Tharappel J.C., Lehmler H.J., Srinivasan C., Robertson L.W., Spear B.T., Glauert H.P. (2008). Effect of antioxidant phytochemicals on the hepatic tumor promoting activity of 3,3',4,4'-tetrachlorobiphenyl (PCB-77). Food and Chemical Toxicology, 46(11), 3467-74.
Chevrier J., Eskenazi B., Bradman A., Fenster L., Barr D.B. (2007). Associations between prenatal exposure to polychlorinated biphenyls and neonatal thyroid-stimulating hormone levels in a Mexican-American population, Salinas Valley, California. Environmental Health Perspectives, 115(10), 1490-6.
Chevrier J., Eskenazi B., Holland N., Bradman A., Barr D.B. (2008). Effects of exposure to polychlorinated biphenyls and organochlorine pesticides on thyroid function during pregnancy. American Journal of Epidemiology, 168(3), 298-310.
Winneke G., Walkowiak J., and Lilienthal H. (2002). PCB-induced neurodevelopmental toxicity in human infants and its potential mediation by endocrine dysfunction. Toxicology, 181-182, 161-165.
Dórea G.J. (2008) Persistent, bioaccumulative and toxic substances in fish: Human health considerations. Science of the Total Environment, 400 (1-3), 93-114.
Wolff MS, Camann D, Gammon M, Stellman SD. Proposed PCB congener groupings for epidemiological studies. Environmental Health Perspectives, 1997, 105: 13–4.
Tait S., La Rocca C., Mantovani A. (2011). Exposure of human fetal penile cells to different PCB mixtures: transcriptome analysis points to diverse modes of interference on external genitalia programming. Reproductive Toxicology, 32(1), 1-14.
Hamers T, Kamstra JH, Cenijn PH, Pencikova K, Palkova L, Simeckova P, Vondracek J, Andersson PL, Stenberg M, Machala M. (2011). In vitro toxicity profiling of ultrapure non-dioxin-like polychlorinated biphenyl congeners and their relative toxic contribution to PCB mixtures in humans. Toxicological Sciences,121(1):88-100.
Fattore E., Fanelli R., Dellatte E., Turrini A., di Domenico A. (2008). Assessment of the dietary exposure to non-dioxin-like PCBs of the Italian general population. Chemosphere, 73(1 Suppl), S278-83.
Arnich N., Tard A., Leblanc J.C., Le Bizec B., Narbonne J.F., Maximilien R. (2009). Dietary intake of non-dioxin-like PCBs (NDL-PCBs) in France, impactof maximum levels in some foodstuffs. Regulatory Toxicology and Pharmacology., 54(3), 287-93.
Salgovicová D., Pavlovicová D. (2007). Exposure of the population of the Slovak Republic to dietary polychlorinated biphenyls. Food and Chemical Toxicology, 45(9), 1641-9.
Sirot V., Tard A., Venisseau A., Brosseaud A., Marchand P., Le Bizec B., Leblanc J.C. (2012). Dietary exposure to polychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans and polychlorinated biphenyls of the French population: Results of the second French Total Diet Study. Chemosphere, 88(4), 492-500.
Fromme H., Shahin N., Boehmer S., Albrecht M., Parlar H., Liebl B., Mayer R., Bolte G. (2009). [Dietary intake of non-dioxin-like polychlorinated biphenyls (PCB) in Bavaria, Germany. Results from the Integrated Exposure Assessment Survey (INES)], Gesundheitswesen, 71(5), 275-80.
ICAR- Imprégnation et Consommation Alimentaire de produits de Rivière – PCB (2011). Etude Nationale d’impregnation aux Polyclorobiphenyles (PCB) des consommateurs de poissons d’eau dolce. Anses/InVS Rapport d’étude scientifique (n° 2008-SA-0416).
EFSA (2011). Scientific Opinion on Polybrominated Diphenyl Ethers (PBDEs) in Food. EFSA Panel on Contaminants in the Food Chain (CONTAM). The EFSA Journal, 9(5), 2156.
Kim T.H., Lee Y.J., Lee E., Kim M.S., Kwack S.J., Kim K.B., Chung K.K., Kang T.S., Han S.Y., Lee J., Lee B.M., Kim H.S. (2009). Effects of gestational exposure to decabromodiphenyl ether on reproductive parameters, thyroid hormone levels, and neuronal development in Sprague-Dawley rats offspring. Journal of Toxicology and Environmental Health, 72(21-22), 1296-303.
Dingemans M.M., van den Berg M., Westerink R.H. (2011). Neurotoxicity of brominated flame retardants: (in)direct effects of parent and hydroxylated polybrominated diphenyl ethers on the (developing) nervous system. Environmental Health Perspectives, 119(7), 900-7.
Banasik M., Suchecka D. (2011). Neurotoxicity of PBDEs on the developing nervous system. Environmental Health Perspectives, 119(8), A331-2.
Dunnick J.K., Nyska A. (2009). Characterization of liver toxicity in F344/N rats and B6C3F1 mice after exposure to a flame retardant containing lower molecular weight polybrominated diphenyl ethers. Experimental and Toxicologic Pathology, 61(1), 1-12.
Chevrier J., Harley K.G., Bradman A., Sjödin A., Eskenazi B. (2011). Prenatal exposure to polybrominated diphenyl ether flame retardants and neonatal thyroid-stimulating hormone levels in the CHAMACOS study. American Journal of Epidemiology, 174(10), 1166-74.
Gill U., Chu I., Ryan J.J., Feeley M. (2004). Polybrominated diphenyl ethers: human tissue levels and toxicology. Reviews of Environmental Contamination and Toxicology, 183, 55-97.
Leblanc J.C., Volatier J.L., Sirot V. and Bemrah-Aouachria N. (2006). CALIPSO, Fish and seafood consumption study and biomarker of exposure to trace elements, pollutants and omega 3. The General Directorate for Foods of France’s Ministry of Agriculture and Fisheries, AFSSA, the French Food Safety Agency and the French Institute for Agronomy Research INRA. Available from ).
van Leeuwen S.P. and de Boer J. (2008). Brominated flame retardants in fish and shellfish - levels and contribution of fish consumption to dietary exposure of Dutch citizens to HBCD. Molecular Nutrition & Food Research, 52, 194-203.
Domingo J.L., Marti-Cid R., Castell V. and Llobet J.M. (2008). Human exposure to PBDEs through the diet in Catalonia, Spain: temporal trend. A review of recent literature on dietary PBDE intake. Toxicology, 248, 25-32; Voorspoels S, Covaci A, Neels H and Schepens P, 2007. Dietary PBDE intake: a market-basket study in Belgium. Environment International, 33, 93-97.
Mariussen E., Fjeld E., Breivik K., Steinnes E., Borgen A., Kjellberg G. and Schlabach M., (2008). Elevated levels of polybrominated diphenylethers (PBDEs) in fish from Lake Mjosa, Norway. Science of the Total Environment, 390, 132-141.
Bethune C., Julshamn K., Lundebye A.K. (2005). A preliminary comparison of polybrominated diphenyl ethers (PBDEs) to lipid content and levels of polychlorinated biphenyls (PCBs) and dioxins (PCDD/Fs) in farmed Atlantic salmon (Salmo salar). International Journal of Food Science & Technology, 40:143-148.
Eriksson P., Fischer C., Wallin M., Jakobsson E. and Fredriksson A. (2006). Impaired behaviour, learning and memory, in adult mice neonatally exposed to hexabromocyclododecane (HBCDD). Environmental Toxicology and Pharmacology, 21, 317-322.
van der Ven L., Verhoef A., van de Kuil T., Slob W., Leonards P.E.G., Visser T.J., Hamers T., Herlin M., Håkansson H., Olausson H., Piersma A.H. and Vos J.G. (2006). A 28-day oral dose toxicity study enhanced to detect endocrine effects of hexabromocyclododecane in Wistar rats. Toxicological Sciences, 94, 281-292.
Ema M., Fujii S., Hirata-Koizumi and Matsumoto M. (2008). Two-generation reproductive toxicity study of the flame retardant hexabromocyclododecane in rats. Reproductive Toxicology, 25, 335-351.
EFSA (2008). Perfluorooctane sulfonate (PFOS), perfluorooctanoic acid (PFOA) and their salts. Scientific Opinion of the Panel on Contaminants in the Food chain. The EFSA Journal, 653, 1-131).
Prevedouros K., Cousins I.T., Buck R.C., Korzeniowsk, S.H.(2006). Sources, fate and transport of perfluorocarboxylates. Environmental Science & Technology, 40, 32-44.
EFSA (2012). Perfluoroalkylated substances in food: occurrence and dietary exposure. European Food Safety Authority. EFSA Journal, 10(6):2743.
Lau C., Anitole K., Hodes C., Lai D., Pfahles-Hutchens A., and Seed J. (2007). Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicological Sciences, 99, 366-394.
Zhang H., Shi Z, Liu Y,Wei Y. Dai J. (2008). Lipid homeostasis and oxidative stress in the liver of male rats exposed to perfluorododecanoic acid. Toxicology and Applied Pharmacology, 227, 16–25.
Shi Z., Ding L., Zhang H., Feng Y., Xu M., Dai J. (2009) Chronic exposure to perfluorododecanoic acid disrupts testicular steroidogenesis and the expression of related genes in male rats. Toxicology Letters, 188:192–200.
Peden-Adams M.M., Stuckey J.E., Gaworecki K.M., Berger-Ritchie J., Bryant K., Jodice P.G., Scott T.R., Ferrario J.B., Guan B., Vigo C., Boone J.S., McGuinn W.D., DeWitt J.C., Keil D.E. (2009). Developmental toxicity in white leghorn chickens following in ovo exposure to perfluorooctane sulfonate (PFOS). Reproductive Toxicology, 27:307–318.
Eriksen K.T., Raaschou-Nielsenb O., Sørensen M., Roursgaard M., Loft S., Møller P. (2010) Genotoxic potential of the perfluorinated chemicals PFOA, PFOS, PFBS, PFNA and PFHxA in human HepG2 cells. Mutation Research, 700:39–43.
Pinkas A., Slotkin T.A., Brick-Turin Y., Zee E.A. van der , Yanai Y. (2010) Neurobehavioral teratogenicity of perfluorinated alkyls in an avian model. Neurotoxicology and Teratology 32:182–186.
La Rocca C., Tait S., Guerranti C., Busani L., Ciardo F., Bergamasco B., Stecca L., Perra G., Mancini F.R., Marci R., Bordi G., Caserta D., Focardi S., Moscarini M., Mantovani A. (2014). Exposure to endocrine disrupters and nuclear receptors gene expression in infertile and fertile women from different Italian areas. International Journal of Environmental Research and Public Health, 11, 10146-10164.
Grandjean P., Andersen E.W., Budtz-Jørgensen E., Nielsen F., Mølbak K., Weihe P., Heilmann C. (2012). Serum vaccine antibody concentrations in children exposed to perfluorinated compounds. JAMA, 25;307(4):391-7.
Gruber L., Tentschert J. (2011). Migration of poly- and perfluorinated compounds from food contact materials into food. 3rd International Workshop on Anthropogenic Perfluorinated Compounds, June 15-17, Amsterdam, The Netherlands.
Trier X., Granby K., Christensen J.H. (2011) Polyfluorinated surfactants (PFS) in paper and board coatings for food packaging. Environmental Science and Pollution Research, 18:1108–1120.
D'Hollander W., de Voogt P., De Coen W., Bervoets L. (2010). Perfluorinated substances in human food and other sources of human exposure. Reviews of Environmental Contamination and Toxicology, 208:179-215.
Berger U., Glynn A., Holmström K.E., Berglund M., Ankarberg E.H., Törnkvist A. (2009) Fish consumption as a source of human exposure to perfluorinated alkyl substances in Sweden – Analysis of edible fish from Lake Vättern and the Baltic Sea. Chemosphere, 76:799–804.
Schuetze A., Heberer T., Effkemann S., Juergensen S. (2010) Occurrence and assessment of perfluorinated chemicals in wild fish from Northern Germany. Chemosphere, 78:647–652.
Suominen K., Hallikainen A., Ruokojärvi P., Airaksinen R., Koponen J., Rannikko R., Kiviranta H. (2011). Occurrence of PCDD/F, PCB, PBDE, PFAS, and organotin compounds in fish meal, fish oil and fish feed. Chemosphere, 85(3):300-6.
Goeritz I., Falk S., Stahl T., Schäfers C., Schlechtriem C. (2013). Biomagnification and tissue distribution of perfluoroalkyl substances (PFASs) in market-size rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Chemistry, 32(9):2078-88.
Felix Gru¨ n and Bruce Blumberg. Minireview: The Case for Obesogens. Molecular Endocrinology, 23: 1127–1134, 2009.
EFSA (2004). Opinion of the Scientific Panel on Contaminants in the Food Chain on a request from the Commission to assess the health risks to consumers associated with exposure to organotins in foodstuffs. The EFSA Journal, 102, 1-119.
Gru¨n F., Watanabe H., Zamanian Z., Maeda L., Arima K., Chubacha R., Gardiner D.M., Kanno J., Iguchi T., Blumberg B. (2006). Endocrine disrupting organotin compounds are potent inducers of adipogenesis in vertebrates. Molecular Endocrinology, 20:2141–2155.
Kirchner S., Kieu T., Chow C., Casey S., and Blumberg B. (2010). Prenatal Exposure to the Environmental Obesogen Tributyltin Predisposes Multipotent Stem Cells to Become Adipocytes. Molecular Endocrinology, 24: 526–539.
FAO/WHO (2010). Report of the Joint FAO/WHO Expert Consultation on the Risks and Benefits of Fish Consumption Rome, 25–29 January 2010. FAO Fisheries and Aquaculture Report. No. 979.
EFSA (2015). Statement on the benefits of fish/seafood consumption compared to the risks of methylmercury in fish/seafood. The EFSA Journal 2015;13(1):3982.
Karatela S., Paterson J., Schluter P.J., Anstiss R. (2011). Methylmercury exposure through seafood diet and health in New Zealand: Are seafood eating communities at a greater risk?. Australasian Epidemiologist, 18, 26 – 32.
Baldi F., Mantovani A. (2008) A new database for food safety: EDID (Endocrine disrupting chemicals - Diet Interaction Database). Annali Istituto Superiore Sanita, 44: 57-63.
Jayashankar S., Glover C.N., Folven K.I., Brattelid T., Hogstrand C., Lundebye A.K. (2012). Cerebral gene expression and neurobehavioural responses in mice pups exposed to methylmercury and docosahexaenoic acid through the maternal diet. Environmental Toxicology and Pharmacology, 33(1):26-38.
Maranghi F., Tassinari R., Moracci G., Altieri I., Rasinger J.D., Carroll T.S., Hogstrand C., Lundebye A.K., Mantovani A. (2013). Dietary exposure of juvenile female mice to polyhalogenated seafood contaminants (HBCD, BDE-47, PCB-153, TCDD): comparative assessment of effects in potential target tissues. Food and Chemical Toxicology, 56: 443-9.
Rasinger J.D., Carroll T.S., Lundebye A.K., Hogstrand C. (2014). Cross-omics gene and protein expression profiling in juvenile female mice highlights disruption of calcium and zinc signalling in the brain following dietary exposure to CB-153, BDE-47, HBCD or TCDD. Toxicology, 321:1-12.
Bell J.G., McGhee F., Campbell P.J. and Sargent J.R. (2003). Rapeseed oil as an alternative to marine fish oil in diets of post-smolt Atlantic salmon (Salmo salar): changes in flesh fatty acid composition and effectiveness of subsequent fish oil washout. Aquaculture, 218: 515–528.
Bell J.G., Henderson R.J., Tocher D.R., McGhee F., Dick J.R., Porter A., Smullen R.P. and Sargent J.R. (2002). Substituting Fish Oil with Crude Palm Oil in the Diet of Atlantic Salmon (Salmo salar) Affects Muscle Fatty Acid Composition and Hepatic Fatty Acid Metabolism. Nutrition Journal, 132, 2 222-230.
Torstensen B.E., Frøyland L, Ørnsrud R., Lie Ø. (2004). Tailoring of a cardioprotective muscle fatty acid composition of Atlantic salmon (< i> Salmo salar) fed vegetable oils. Food Chemistry, 87, 4, 567–580.
Kaushik S., Coves D., Dutto G., Blanc D. (2004). Almost total replacement of fish meal by plant protein sources in the diet of a marine teleost, the European seabass, Dicentrarchus labrax. Aquaculture, 230, 391–404.
Steffens W. (1989). Principles of fish nutrition, West Sussex, Ellis Horwood Ltd., 384 pp.
New M. (1996). Responsible use of aquaculture feeds. Aquaculture. Asia, 1: 3-12.
Cowey C.B. and Sargent J.R. (1979). Nutrition. In W.S. Hoar, D.J. Randall and J.R. Brett, eds. Fish physiology, Vol. 8, p. 1-69. New York, Academic Press.
New M.B. (1987). Feed and feeding of fish and shrimp. ADCP/Rep/87/26, UNDP/FAO, Rome, 275 pp.
NRC (National Research Council). (1983). Nutrient requirements of warmwater fishes and shellfishes, Washington DC, National Academy Press, 102 pp.
Takeuchi T., Watanabe T. and Ogino C. (1979). Availability of carbohydrate and lipid as dietary energy sources for carp. Bulletin of the Japanese Society of Scientific Fisheries, 45: 977-982.
Garling D.L. Jr. and Wilson R.P. (1977). Effect of dietary carbohydrate-to-lipid ratios on growth and body composition of fingerling channel catfish. Prog. Fish-Cult. 39: 43-47.
Luquet P. (1989). Practical considerations on the protein nutrition and feeding of tilapia. Aquatic Living Resources, 2: 99-104.
Tacon A.G.J. (1990). Standard methods for the nutrition and feeding of farmed fish and shrimp, Washington DC, Argent Laboratories Press, 454 pp.
Hepher B. (1990). Nutrition of pond fishes, Cambridge, Cambridge University Press, 388 pp.
Yiannikouris A., Connolly C., Powera R. and Lobinskic R. (2009). Characterization of metal–peptide complexes in feed supplements of essential trace elements. Metallomic,1, 235-248.
Morelli E., Marangi M.L., Fantozzi L. (2009). A phytochelatin-based bioassay in marine diatoms useful for the assessment of bioavailability of heavy metals released by polluted sediments. Environment International, 35, 3, 532–538.
Storebakken, Shearer and Roem (2000). Growth, uptake and retention of nitrogen and phosphorus, and absorption of other minerals in Atlantic salmon Salmo salar fed diets with fish meal and soy–protein concentrate as the main sources of protein. Aquaculture Nutrition, 6, 2, 103–108.
Francisa G., Makkarb H.P.S., Becker K. (2001). Antinutritional factors present in plant-derived alternate fish feed ingredients and their effects in fish. Aquaculture, 199, 3–4, 1: 197–227.
Wolfgang Mareta, Harold H. Sandstead. (2006). Zinc requirements and the risks and benefits of zinc supplementation. Journal of Trace Elements in Medicine and Biology, 20, 1:3–18.
Tacon A.G.J. (1997). Feeding tomorrow’s fish: keys for sustainability. In A. Tacon and B. Basurco, eds. Feeding tomorrow’s fish, p. 11-33. Proceedings of the workshop of the CIHEAM Network on Technology of Aquaculture in the Mediterranean (TECAM), jointly organized by CIHEAM, FAO and IEO Mazarron, Spain, 24-26 June 1996, CIHEAM, Apodo, Spain.
Kaushik, S.J. (2000). Applied nutrition for sustainable aquaculture development. In Book of Synopses, p. 155-158. NACA/FAO International Conference on Aquaculture in the Third Millennium, 20-25 February 2000.
Caballero M.J., Obach A., Rosenlund G., Montero D., Gisvold M. and Izquierdo M.S. (2002). Impact of different dietary lipid sources on growth, lipid digestibility, tissue fatty acid composition and histology of rainbow trout, Oncorhynchus mykiss. Aquaculture, 214: 253–271.
Bell G., Torstensen B. and Sargent J. (2005). Replacement of marine fish oils with vegetable oils in feeds for farmed salmon. Lipid Technology 17: 7-11.
Turchini G.M., Torstensen B.E. and Wing-Keong Ng (2009). Fish oil replacement in finfish nutrition. Reviews in Aquaculture, 1, 10–57.
Gatlin D.M.G., Barrows F.T., Brown P., Dabrowski K., Gaylord T.G., Hardy R.W., Herman E., Hu G., Krogdahl A., Nelson R., Overturf K., Rus, M., Sealey W., Skonberg D., Souza E.J., Stone D., Wilson R., Wurtele E. (2007). Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquaculture Research, 38: 551-579.
Dias J., Conceicao L.E.C., Ribeiro A.R., Borges P., Valente L.M.P., Dinis M.T. (2009). Practical diet with low fish-derived protein is able to sustain growth performance in gilthead seabream (Sparus aurata) during the grow-out phase. Aquaculture, 293, 255–262.
Pereira T.G., Oliva-Teles A. (2003). Evaluation of corn gluten meal as a protein source in diets for gilthead sea bream (Sparus aurata L.) juveniles. Aquaculture Research. 34, 1111-1117.
Gómez-Requeni, P., Mingarro, M., Calduch-Giner, J.A., Médale, F., Martin, S.A.M., Houlihan, D.F., Kaushik, S., Pérez-Sánchez, J. (2004). Protein growth performance, amino acid utilization and somatotropic axis responsiveness to fish meal replacement by plant protein sources in gilthead sea bream (Sparus aurata). Aquaculture 232, 493-510.
Mantovani A., Frazzoli C., La Rocca C. (2009) Risk assessment of endocrine-active compounds in feeds. The Veterinary Journal,182, 392-401.
Ackman R. G. (1990) Canola fatty acids—an ideal mixture for health, nutrition and food use. Shahidi, F. eds. Canola and Rapeseed. 1990:81-98 Avi New York, NY.
Bell J. G., McEvoy J., Tocher D. R., McGhee F., Campbell P. J. & Sargent, J. R. (2001) Replacement of fish oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid compositions and hepatocyte fatty acid metabolism. Journal of Nutrition, 131:1535-1543.
Bell J. G., Henderson R. J., Tocher D. R., McGhee F., Dick J. R., Porter A., Smullen R. P. & Sargent, J. R. (2002) Substituting fish oil with crude palm oil in the diet of Atlantic salmon (Salmo salar) affects muscle fatty acid composition and hepatic fatty acid metabolism. Journal of Nutrition, 132:222-230.
Bell J.G., Tocher D.R., Henderson R.J., Dick J.R., and Crampton.V.O. (2003). Altered Fatty Acid Compositions in Atlantic Salmon (Salmo salar) Fed Diets Containing Linseed and Rapeseed Oils Can Be Partially Restored by a Subsequent Fish Oil Finishing Diet. Journal of Nutrition, 133, 9, 2793-2801.
Izquierdo M.S., Obach A., Arantzamendi L., Montero D., Robaina L. and Rosenlund G. (2003). Dietary lipid sources for seabream and seabass: growth performance, tissue composition and flesh quality Aqua. Nutr., 9: 397-407.
Masiha A., Ebrahimi E., Soofiani N.M., Kadivar M. (2013). Effect of Dietary Vegetable Oils on the Growth Performance and Fatty Acid Composition of Fingerlings of Rainbow Trout, Oncorhynchus mykiss. Food Science and Technology, 1(2): 21-29, 2013.
Benedito-Palos L., Navarro J.C., Sitjà-Bobadilla A., Bell J.G., Kaushik S. and Pérez-Sánchez J. (2008). High levels of vegetable oils in plant protein-rich diets fed to gilthead seabream (Sparus aurata L.): growth performance, muscle fatty acid profiles and histological alterations of target tissues. British Journal of Nutrition, 100 (5): 992-1003.
EFSA (2014). Scientific Opinion on the substantiation of a health claim related to DHA and contribution to normal brain development pursuant to Article 14 of Regulation (EC) No 1924/2006. EFSA Journal, 12(10):3840.
Huffman S.L.,. Harika R.K., Eilander A., Osendarp S.J.M. (2011). Essential fats: how do they affect growth and development of infants and young children in developing countries? A literature review. Maternal and Child Nutrition 7 (3), 44-65.
Genuis S.J. (2008). To sea or not to sea: Benefits and risks of gestational fish consumption.Reproductive Toxicology 26, 81–85.
Bell J.G., McGhee F., Dick J.R, Tocher D.R. (2005). Dioxin and dioxin-like polychlorinated biphenyls (PCBs) in Scottish farmed salmon (Salmo salar): effects of replacement of dietary marine fish oil with vegetable oils. Aquaculture 243, 1–4, 305–314.
Berntssen M.H.G., Lundebye A.K., Torstennsen B.E. (2005) Reducing the levels of dioxins and dioxin-like PCBs in farmed Atlantic salmon by substitution of fish oil with vegetable oil in the feed. Aquaculture Nutrition, 11, 3, 219–231.
Berntssen M.H.G, Julshamn K., Lundebye A.K. (2010). Chemical contaminants in aquafeeds and Atlantic salmon (Salmo salar) following the use of traditional- versus alternative feed ingredients. Chemosphere, 78, 6, 637–646.
EFSA (2008). Polycyclic Aromatic Hydrocarbons in Food. Scientific Opinion of the Panel on Contaminants in the Food Chain. The EFSA Journal, 724, 1-114.
Moret S., Dudine A., Conte L.S. (2000) Processing effects on the polyaromatic hydrocarbon content of rapeseed oil. Journal of the American Oil Chemists' Society, 77:1289–1292.
Midtbø LK1, Ibrahim MM, Myrmel LS, Aune UL, Alvheim AR, Liland NS, Torstensen BE, Rosenlund G, Liaset B, Brattelid T, Kristiansen K, Madsen L. Intake of farmed Atlantic salmon fed soybean oil increases insulin resistance and hepatic lipid accumulation in mice. PLoS One. 2013;8(1):e53094.