Chronic consumption of farmed salmon containing persistent organic pollutants causes insulin resistance and obesity in mice
Mohammad Madani Ibrahim, Even Fjære, Erik-Jan Lock, Danielle Naville, Heidi Amlund, Emmanuelle Meugnier, Brigitte Le Magueresse Battistoni, Livar Frøyland, Lise Madsen, Niels Jessen, Sten Lund, Hubert Vidal, Jérôme Ruzzin, Mohammad Madani Ibrahim, Even Fjære, Erik-Jan Lock, Danielle Naville, Heidi Amlund, Emmanuelle Meugnier, Brigitte Le Magueresse Battistoni, Livar Frøyland, Lise Madsen, Niels Jessen, Sten Lund, Hubert Vidal, Jérôme Ruzzin
Abstract
Background: Dietary interventions are critical in the prevention of metabolic diseases. Yet, the effects of fatty fish consumption on type 2 diabetes remain unclear. The aim of this study was to investigate whether a diet containing farmed salmon prevents or contributes to insulin resistance in mice.
Methodology/principal findings: Adult male C57BL/6J mice were fed control diet (C), a very high-fat diet without or with farmed Atlantic salmon fillet (VHF and VHF/S, respectively), and Western diet without or with farmed Atlantic salmon fillet (WD and WD/S, respectively). Other mice were fed VHF containing farmed salmon fillet with reduced concentrations of persistent organic pollutants (VHF/S(-POPs)). We assessed body weight gain, fat mass, insulin sensitivity, glucose tolerance, ex vivo muscle glucose uptake, performed histology and immunohistochemistry analysis, and investigated gene and protein expression. In comparison with animals fed VHF and WD, consumption of both VHF/S and WD/S exaggerated insulin resistance, visceral obesity, and glucose intolerance. In addition, the ability of insulin to stimulate Akt phosphorylation and muscle glucose uptake was impaired in mice fed farmed salmon. Relative to VHF/S-fed mice, animals fed VHF/S(-POPs) had less body burdens of POPs, accumulated less visceral fat, and had reduced mRNA levels of TNFα as well as macrophage infiltration in adipose tissue. VHF/S(-POPs)-fed mice further exhibited better insulin sensitivity and glucose tolerance than mice fed VHF/S.
Conclusions/significance: Our data indicate that intake of farmed salmon fillet contributes to several metabolic disorders linked to type 2 diabetes and obesity, and suggest a role of POPs in these deleterious effects. Overall, these findings may participate to improve nutritional strategies for the prevention and therapy of insulin resistance.
Conflict of interest statement
Competing Interests: The authors have declared that no competing interests exist.
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References
- Ford ES, Giles WH, Mokdad AH. Increasing prevalance of the metabolic syndrome among U.S adults. Diabetes Care. 2004;27:2444–2449.
- OECD/EU. 2010. Health at a glance: Europe 2010. Available from , accessed 01 February 2011.
- WHO. Geneva, Switzerland: 2005. Chronic diseases: a vital investment.
- Sacks FM, Bray GA, Carey VJ, Smith SR, Ryan DH, et al. Comparison of Weight-Loss Diets with Different Compositions of Fat, Protein, and Carbohydrates. N Eng J Med. 2009;360:859–873.
- Mann JI. Diet and risk of coronary heart disease and type 2 diabetes. Lancet. 2002;360:783–789.
- Daviglus ML, Stamler J, Orencia AJ, Dyer AR, Liu K, et al. Fish consumption and the 30-year risk of fatal myocardial infarction. N Eng J Med. 1997;336:1046–1053.
- Dyerberg J, Bang HO, Stoffersen E, Moncada S, Vane JR. Eicosapentanoic Acid and Prevention of Thrombosis and Atherosclerosis. Lancet. 1978;2:117–119.
- Storlien LH, Kraegen EW, Chisholm DJ, Ford GL, Bruce DG, et al. Fish Oil Prevents Insulin Resistance Induced by High-Fat Feeding in Rats. Science. 1987;237:885–888.
- Ouellet V, Marois J, Weisnagel SJ, Jacques H. Dietary cod protein improves insulin sensitivity in insulin-resistant men and women. Diabetes Care. 2007;30:2816–2821.
- Lavigne C, Tremblay F, Asselin G, Jacques H, Marette A. Prevention of skeletal muscle insulin resistance by dietary cod protein in high fat-fed rats. Am J Physio Endocrinol Metab. 2001;281:E62–E71.
- Storlien LH, Jenkins AB, Chisholm DJ, Pascoe WS, Khouri S, et al. Influence of Dietary-Fat Composition on Development of Insulin Resistance in Rats - Relationship to Muscle Triglyceride and Omega-3-Fatty-Acids in Muscle Phospholipid. Diabetes. 1991;40:280–289.
- Ruzzin J, Turcotte S, Leblanc V, Lavigne C, Froyland L, et al. Dietary salmon protein improves insulin sensitivity in high-fat fed obese rats. Ann Nutr Metab. 2007;51:347 (abstract P689).
- Pilon G, Ruzzin J, Rioux LE, Lavigne C, White PJ, et al. Differential effects of various fish proteins in altering body weight, inflammatory status, and insulin sensitivity in high-fat-fed rats. Metab Clin Exp. 2011 doi: .
- van Woudenbergh GJ, van Ballegooijen AJ, Kuijsten A, Sijbrands EJG, van Rooij FJA, et al. Eating Fish and Risk of Type 2 Diabetes A population-based, prospective follow-up study. Diabetes Care. 2009;32:2021–2026.
- Kaushik M, Mozaffarian D, Spiegelman D, Manson JE, Willett WC, et al. Long-chain omega-3 fatty acids, fish intake, and the risk of type 2 diabetes mellitus. Am J Clin Nutr. 2009;90:613–620.
- Djousse L, Gaziano JM, Buring JE, Lee IM. Dietary omega-3 fatty acids and fish consumption and risk of type 2 diabetes. Am J Clin Nutr. 2011;93:143–150.
- Ruzzin J, Petersen R, Meugnier E, Madsen L, Lock EJ, et al. Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ Health Perspect. 2010;118:465–471.
- Hites RA, Foran JA, Carpenter DO, Hamilton MC, Knuth BA, et al. Global assessment of organic contaminants in farmed salmon. Science. 2004;303:226–229.
- Berntssen MHG, Olsvik PA, Torstensen BE, Julshamn K, Midtun T, et al. Reducing persistent organic pollutants while maintaining long chain omega-3 fatty acid in farmed Atlantic salmon using decontaminated fish oils for an entire production cycle. Chemosphere. 2010;81:242–252.
- Torstensen BE, Espe M, Sanden M, Stubhaug I, Waagbo R, et al. Novel production of Atlantic salmon (Salmo salar) protein based on combined replacement of fish meal and fish oil with plant meal and vegetable oil blends. Aquaculture. 2008;285:193–200.
- Jessen N, Buhl ES, Pold R, Schmitz O, Lund S. A novel insulin sensitizer (S15511) enhances insulin-stimulated glucose uptake in rat skeletal muscles. Horm Metab Res. 2008;40:269–275.
- Ruzzin J, Wagman AS, Jensen J. Glucocorticoid-induced insulin resistance in skeletal muscles: defects in insulin signalling and the effects of a selective glycogen synthase kinase-3 inhibitor. Diabetologia. 2005;48:2119–2130.
- Sargis RM, Johnson DN, Choudhury RA, Brady MJ. Environmental Endocrine Disruptors Promote Adipogenesis in the 3T3-L1 Cell Line through Glucocorticoid Receptor Activation. Obesity. 2010;18:1283–1288.
- Burcelin M, Crivelli V, Dacosta A, Roy-Tirelli A, Thorens B. Heterogeneous metabolic adaptation of C57BL/6J mice to high-fat diet. Am J Physio Endocrinol Metab. 2002;282:E834–E842.
- DeFronzo RA. From the Triumvirate to the Ominous Octet: A New Paradigm for the Treatment of Type 2 Diabetes Mellitus. Diabetes. 2009;58:773–795.
- Bonnard C, Durand A, Peyrol S, Chanseaume E, Chauvin MA, et al. Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest. 2008;118:789–800.
- Feskens EJM, Virtanen SM, Rasanen L, Tuomilehto J, Stengard J, et al. Dietary Factors Determining Diabetes and Impaired Glucose-Tolerance - a 20-Year Follow-up of the Finnish and Dutch Cohorts of the 7-Countries Study. Diabetes Care. 1995;18:1104–1112.
- Fasching P, Ratheiser K, Waldhausl W, Rohac M, Osterrode W, et al. Metabolic Effects of Fish-Oil Supplementation in Patients with Impaired Glucose-Tolerance. Diabetes. 1991;40:583–589.
- Toft I, Bonaa KH, Ingebretsen OC, Nordoy A, Jenssen T. Effects of N-3 Polyunsaturated Fatty-Acids on Glucose-Homeostasis and Blood-Pressure in Essential-Hypertension - a Randomized, Controlled Trial. Ann Int Med. 1995;123:911–918.
- Eritsland J, Seljeflot I, Abdelnoor M, Arnesen H, Torjesen PA. Long-Term Effects of N-3 Fatty-Acids on Serum-Lipids and Glycemic Control. Scan J Clin Lab Invest. 1994;54:273–280.
- Giacco R, Cuomo V, Vessby B, Uusitupa M, Hermansen K, et al. Fish oil insulin sensitivity, insulin secretion and glucose tolerance in healthy people: Is there any effect of fish oil supplementation in relation to the type of background diet and habitual dietary intake of n-6 and n-3 fatty acids? Nutr Metab Cardio Disease. 2007;17:572–580.
- Laaksonen DE, Lakka TA, Lakka HM, Nyyssonen K, Rissanen T, et al. Serum fatty acid composition predicts development of impaired fasting glycaemia and diabetes in middle-aged men. Diab Med. 2002;19:456–464.
- van Dam RM, Stampfer M, Willett WC, Hu FB, Rimm EB. Dietary fat and meat intake in relation to risk of type 2 diabetes in men. Diabetes Care. 2002;25:417–424.
- Woodman RJ, Mori TA, Burke V, Puddey IB, Watts GF, et al. Effects of purified eicosapentaenoic and docosahexaenoic acids on glycemic control, blood pressure, and serum lipids in type 2 diabetic patients with treated hypertension. Am J Clin Nutr. 2002;76:1007–1015.
- Hendra TJ, Britton ME, Roper DR, Wagainetwabwe D, Jeremy JY, et al. Effects of Fish Oil Supplements in Niddm Subjects - Controlled-Study. Diabetes Care. 1990;13:821–829.
- Borkman M, Chisholm DJ, Furler SM, Storlien LH, Kraegen EW, et al. Effects of Fish Oil Supplementation on Glucose and Lipid-Metabolism in Niddm. Diabetes. 1989;38:1314–1319.
- Vessby B, Karlstrom B, Boberg M, Lithell H, Berne C. Polyunsaturated Fatty-Acids May Impair Blood-Glucose Control in Type-2 Diabetic-Patients. Diab Med. 1992;9:126–133.
- Mostad IL, Bjerve KS, Bjorgaas MR, Lydersen S, Grill V. Effects of n-3 fatty acids in subjects with type 2 diabetes: reduction of insulin sensitivity and time-dependent alteration from carbohydrate to fat oxidation. Am J Clin Nutr. 2006;84:540–550.
- Glauber H, Wallace P, Griver K, Brechtel G. Adverse Metabolic Effect of Omega-3 Fatty-Acids in Non-Insulin-Dependent Diabetes-Mellitus. Ann Int Med. 1988;108:663–668.
- Meyer KA, Kushi LH, Jacobs DR, Folsom AR. Dietary fat and incidence of type 2 diabetes in older Iowa women. Diabetes Care. 2001;24:1528–1535.
- Grun F, Blumberg B. Endocrine disrupters as obesogens. Mol Cell Endo. 2009;304:19–29.
- Lim S, Ahn SY, Song IC, Chung MH, Jang HC, et al. Chronic Exposure to the Herbicide, Atrazine, Causes Mitochondrial Dysfunction and Insulin Resistance. Plos One. 2009;4
- Arsenescu V, Arsenescu RI, King V, Swanson H, Cassis LA. Polychlorinated biphenyl-77 induces adipocyte differentiation and proinflammatory adipokines and promotes obesity and atherosclerosis. Environ Health Perspect. 2008;116:761–768.
- Lee DH, Lee IK, Song K, Steffes M, Toscano W, et al. A strong dose-response relation between serum concentrations of persistent organic pollutants and diabetes: results from the National Health and Examination Survey 1999-2002. Diabetes Care. 2006;29:1638–1644.
- Carpenter D. Environmental contaminants as risk factors for developing diabetes. Rev Environ Health. 2008;23:59–74.
- Lee DH, Steffes MW, Sjodin A, Jones RS, Needham LL, et al. Low Dose of Some Persistent Organic Pollutants Predicts Type 2 Diabetes: A Nested Case-Control Study. Environ Health Perspect. 2010;118:1235–1242.
- Lee DH, Steffes MW, Sjodin A, Jones RS, Needham LL, et al. Low Dose Organochlorine Pesticides and Polychlorinated Biphenyls Predict Obesity, Dyslipidemia, and Insulin Resistance among People Free of Diabetes. Plos One. 2011;6
- Fisher BE. Most unwanted. Environ Health Perspect. 1999;107:A18–23.
- Lordo RA, Dinh KT, Schwemberger JG. Semivolatile organic compounds in adipose tissue: Estimated averages for the US population and selected subpopulations. Am J Public Health. 1996;86:1253–1259.
- Li QQ, Loganath A, Chong YS, Tan J, Obbard JP. Levels of persistent organic pollutant residues in human adipose and muscle tissues in Singapore. J Toxic Environ Health. 2006;69:1927–1937.
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