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A low dietary intake of cod protein is sufficient to increase growth, improve serum and tissue fatty acid compositions, and lower serum postprandial glucose and fasting non-esterified fatty acid concentrations in obese Zucker fa/fa rats

Abstract

Purpose

Studies in rats suggest that fish proteins may improve lipid and glucose regulation and could thus be a potential tool in the treatment of obesity-related comorbidities. To date, all published rat studies on dietary fish protein have been designed with 50 or 100 % of dietary proteins from fish. As it is not common, nor advised, to consume fish as the only protein source in a healthy diet, mechanistic studies on the effects of diets with low dose fish proteins are needed. Here, we investigate whether a low dose of cod protein would affect glucose homeostasis and lipid metabolism in obese Zucker fa/fa rats.

Methods

Twelve male obese Zucker fa/fa rats consumed diets where cod proteins accounted for 25 % of the total protein intake with the remaining 75 % from casein (COD) or 100 % of protein as casein (CAS) for 4 weeks.

Results

Rats fed COD achieved a higher body weight without affecting adiposity and thigh muscle mass after 4 weeks, but liver weight and hepatic cholesterol level were higher than in CAS-fed rats. Fasting serum level of non-esterified fatty acids and 2 h postprandial glucose level were lower in COD than in CAS. The fatty acid metabolism was beneficially affected by the COD diet, with e.g., higher ratio of n-3/n-6 PUFAs in serum, liver and adipose tissue when compared to CAS.

Conclusions

A low intake of cod protein (25 % of protein intake) was sufficient to beneficially affect lipid metabolism and postprandial glucose regulation in obese fa/fa rats.

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References

  1. World Health organisation (2012) Obesity and overweight. Fact sheet. http://www.who.int/mediacentre/factsheets/fs311/en/

  2. Wilding JP (2007) Treatment strategies for obesity. Obes Rev 8(Suppl 1):137–144

    Article  Google Scholar 

  3. Westerterp-Plantenga MS, Nieuwenhuizen A, Tome D et al (2009) Dietary protein, weight loss, and weight maintenance. Annu Rev Nutr 29:21–41

    CAS  Article  Google Scholar 

  4. Dyson PA (2010) The therapeutics of lifestyle management on obesity. Diabetes Obes Metab 12:941–946

    CAS  Article  Google Scholar 

  5. Krauss RM, Eckel RH, Howard B et al (2000) AHA Dietary Guidelines: revision 2000: a statement for healthcare professionals from the Nutrition Committee of the American Heart Association. Circulation 102:2284–2299

    CAS  Article  Google Scholar 

  6. Iritani N, Narita R, Fujita T et al (1985) Effects of dietary fish protein, soybean protein and casein on cholesterol turnover in rats. J Nutr Sci Vitaminol 31:385–392

    CAS  Article  Google Scholar 

  7. Demonty I, Deshaies Y, Jacques H (1998) Dietary proteins modulate the effects of fish oil on triglyceridemia in the rat. Lipids 33:913–921

    CAS  Article  Google Scholar 

  8. Zhang X, Beynen AC (1993) Influence of dietary fish proteins on plasma and liver cholesterol concentrations in rats. Br J Nutr 69:767–777

    CAS  Article  Google Scholar 

  9. Lavigne C, Marette A, Jacques H (2000) Cod and soy proteins compared with casein improve glucose tolerance and insulin sensitivity in rats. Am J Physiol Endocrinol Metab 278:E491–E500

    CAS  Google Scholar 

  10. Lavigne C, Tremblay F, Asselin G et al (2001) Prevention of skeletal muscle insulin resistance by dietary cod protein in high fat-fed rats. Am J Physiol Endocrinol Metab 281:E62–E71

    CAS  Google Scholar 

  11. Ait-Yahia D, Madani S, Savelli JL et al (2003) Dietary fish protein lowers blood pressure and alters tissue polyunsaturated fatty acid composition in spontaneously hypertensive rats. Nutrition 19:342–346

    CAS  Article  Google Scholar 

  12. Shukla A, Bettzieche A, Hirche F et al (2006) Dietary fish protein alters blood lipid concentrations and hepatic genes involved in cholesterol homeostasis in the rat model. Br J Nutr 96:674–682

    CAS  Google Scholar 

  13. Kato M, Ogawa H, Kishida T et al (2009) The mechanism of the cholesterol-lowering effect of water-insoluble fish protein in ovariectomised rats. Br J Nutr 102:816–824

    CAS  Article  Google Scholar 

  14. Liaset B, Madsen L, Hao Q et al (2009) Fish protein hydrolysate elevates plasma bile acids and reduces visceral adipose tissue mass in rats. Biochim Biophys Acta 1791:254–262

    CAS  Article  Google Scholar 

  15. Pilon G, Ruzzin J, Rioux LE et al (2011) Differential effects of various fish proteins in altering body weight, adiposity, inflammatory status, and insulin sensitivity in high-fat-fed rats. Metabolism 60:1122–1130

    CAS  Article  Google Scholar 

  16. Madani Z, Louchami K, Sener A et al (2012) Dietary sardine protein lowers insulin resistance, leptin and TNF-alpha and beneficially affects adipose tissue oxidative stress in rats with fructose-induced metabolic syndrome. Int J Mol Med 29:311–318

    CAS  Google Scholar 

  17. Gudbrandsen OA, Wergedahl H, Liaset B et al (2005) Dietary proteins with high isoflavone content or low methionine–glycine and lysine–arginine ratios are hypocholesterolaemic and lower the plasma homocysteine level in male Zucker fa/fa rats. Br J Nutr 94:321–330

    CAS  Article  Google Scholar 

  18. Hurley C, Galibois I, Jacques H (1995) Fasting and postprandial lipid and glucose metabolism are modulated by dietary proteins and carbohydrates: role of plasma insulin concentrations. J Nutr Biochem 6:540–546

    CAS  Article  Google Scholar 

  19. Wergedahl H, Liaset B, Gudbrandsen OA et al (2004) Fish protein hydrolysate reduces plasma total cholesterol, increases the proportion of HDL cholesterol, and lowers acyl-CoA:cholesterol acyltransferase activity in liver of zucker rats. J Nutr 134:1320–1327

    CAS  Google Scholar 

  20. Hosomi R, Fukunaga K, Arai H et al (2009) Effects of dietary fish protein on serum and liver lipid concentrations in rats and the expression of hepatic genes involved in lipid metabolism. J Agric Food Chem 57:9256–9262

    CAS  Article  Google Scholar 

  21. Hosomi R, Fukunaga K, Arai H et al (2011) Fish protein decreases serum cholesterol in rats by inhibition of cholesterol and bile acid absorption. J Food Sci 76:H116–H121

    CAS  Article  Google Scholar 

  22. Hosomi R, Fukunaga K, Arai H et al (2013) Effect of combination of dietary fish protein and fish oil on lipid metabolism in rats. J Food Sci Technol 50:266–274

    CAS  Article  Google Scholar 

  23. Wergedahl H, Gudbrandsen OA, Rost TH et al (2009) Combination of fish oil and fish protein hydrolysate reduces the plasma cholesterol level with a concurrent increase in hepatic cholesterol level in high-fat-fed Wistar rats. Nutrition. 25:98–104

    CAS  Article  Google Scholar 

  24. de Artinano AA, Castro MM (2009) Experimental rat models to study the metabolic syndrome. Br J Nutr 102:1246–1253

    Article  Google Scholar 

  25. Picchi A, Gao X, Belmadani S et al (2006) Tumor necrosis factor-alpha induces endothelial dysfunction in the prediabetic metabolic syndrome. Circ Res 99:69–77

    CAS  Article  Google Scholar 

  26. Hotamisligil GS, Shargill NS, Spiegelman BM (1993) Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science 259:87–91

    CAS  Article  Google Scholar 

  27. Kromann N, Green A (1980) Epidemiological studies in the Upernavik district, Greenland. Incidence of some chronic diseases 1950–1974. Acta Med Scand 208:401–406

    CAS  Article  Google Scholar 

  28. Feskens EJ, Bowles CH, Kromhout D (1991) Inverse association between fish intake and risk of glucose intolerance in normoglycemic elderly men and women. Diabetes Care 14:935–941

    CAS  Article  Google Scholar 

  29. Kris-Etherton PM, Harris WS, Appel LJ (2002) Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106:2747–2757

    Article  Google Scholar 

  30. The Norwegian Directorate of Health (2014) Recommendations regarding diet, nutrition and physical activity [Anbefalinger om kosthold, ernæring og fysisk aktivitet], p 28. http://www.helsedirektoratet.no/publikasjoner/anbefalinger-om-kosthold-ernering-og-fysisk-aktivitet/Sider/default.aspx

  31. Fulgoni VL 3rd (2008) Current protein intake in America: analysis of the National Health and Nutrition Examination Survey, 2003–2004. Am J Clin Nutr 87:1554S–1557S

    CAS  Google Scholar 

  32. Totland TH (2012) Norkost 3, National dietary survey conducted among adults in Norway aged 18–70 years [En landsomfattende kostholdsundersøkelse blant menn og kvinner i Norge i alderen 18-70 år, 2010-11]. The Norwegian Directorate of Health, Oslo, p 67. http://www.helsedirektoratet.no/publikasjoner/norkost-3-en-landsomfattende-kostholdsundersokelse-blant-menn-og-kvinner-i-norge-i-alderen-18-70-ar/Sider/default.aspx

  33. Vikoren LA, Nygard OK, Lied E et al (2013) A randomised study on the effects of fish protein supplement on glucose tolerance, lipids and body composition in overweight adults. Br J Nutr 109:648–657

    CAS  Article  Google Scholar 

  34. Reeves PG, Nielsen FH, Fahey GC Jr (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123:1939–1951

    CAS  Google Scholar 

  35. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    CAS  Article  Google Scholar 

  36. Suckling KE, Benson GM, Bond B et al (1991) Cholesterol lowering and bile acid excretion in the hamster with cholestyramine treatment. Atherosclerosis 89:183–190

    CAS  Article  Google Scholar 

  37. Meier S, Mjos SA, Joensen H et al (2006) Validation of a one-step extraction/methylation method for determination of fatty acids and cholesterol in marine tissues. J Chromatogr A 1104:291–298

    CAS  Article  Google Scholar 

  38. Sciotto C, Mjos SA (2012) Trans isomers of EPA and DHA in omega-3 products on the European market. Lipids 47:659–667

    CAS  Article  Google Scholar 

  39. Wasta Z, Mjos SA (2013) A database of chromatographic properties and mass spectra of fatty acid methyl esters from omega-3 products. J Chromatogr A 1299:94–102

    CAS  Article  Google Scholar 

  40. Chavali SR, Zhong WW, Utsunomiya T et al (1997) Decreased production of interleukin-1-beta, prostaglandin-E2 and thromboxane-B2, and elevated levels of interleukin-6 and -10 are associated with increased survival during endotoxic shock in mice consuming diets enriched with sesame seed oil supplemented with Quil-A saponin. Int Arch Allergy Immunol 114:153–160

    CAS  Article  Google Scholar 

  41. Benevenga NJ, Gahl MJ, Crenshaw TD et al (1994) Protein and amino acid requirements for maintenance and amino acid requirements for growth of laboratory rats. J Nutr 124:451–453

    CAS  Google Scholar 

  42. McDonough FE, Steinke FH, Sarwar G et al (1990) In vivo rat assay for true protein digestibility: collaborative study. J Assoc Off Anal Chem 73:801–805

    CAS  Google Scholar 

  43. Aoyama Y, Hattori Y, Yoshida A et al (1979) Effect of deficiency in individual essential amino acids in diets on liver lipid content and serum triglyceride level of growing rats. Nutr Rep Int 20:669–675

    CAS  Google Scholar 

  44. Roden M, Price TB, Perseghin G et al (1996) Mechanism of free fatty acid-induced insulin resistance in humans. J Clin Invest 97:2859–2865

    CAS  Article  Google Scholar 

  45. Kritchevsky D, Tepper SA, Czarnecki SK et al (1982) Atherogenicity of animal and vegetable protein: influence of the lysine to arginine ratio. Atherosclerosis 41:429–431

    CAS  Article  Google Scholar 

  46. Spielmann J, Kluge H, Stangl GI et al (2009) Hypolipidaemic effects of potato protein and fish protein in pigs. J Anim Physiol Anim Nutr (Berl) 93:400–409

    CAS  Article  Google Scholar 

  47. Gao F, Kiesewetter D, Chang L et al (2009) Whole-body synthesis-secretion rates of long-chain n-3 PUFAs from circulating unesterified alpha-linolenic acid in unanesthetized rats. J Lipid Res 50:749–758

    CAS  Article  Google Scholar 

  48. Brenner RR (2003) Hormonal modulation of delta6 and delta5 desaturases: case of diabetes. Prostaglandins Leukot Essent Fatty Acids 68:151–162

    CAS  Article  Google Scholar 

  49. Dort J, Leblanc N, Maltais-Giguere J et al (2013) Beneficial effects of cod protein on inflammatory cell accumulation in rat skeletal muscle after injury are driven by its high levels of arginine, glycine, taurine and lysine. PLoS One 8:e77274

    CAS  Article  Google Scholar 

  50. Ouellet V, Weisnagel SJ, Marois J et al (2008) Dietary cod protein reduces plasma C-reactive protein in insulin-resistant men and women. J Nutr 138:2386–2391

    CAS  Article  Google Scholar 

  51. Pot GK, Geelen A, Majsak-Newman G et al (2010) Increased consumption of fatty and lean fish reduces serum C-reactive protein concentrations but not inflammation markers in feces and in colonic biopsies. J Nutr 140:371–376

    CAS  Article  Google Scholar 

  52. Grunfeld C, Verdier JA, Neese R et al (1988) Mechanisms by which tumor necrosis factor stimulates hepatic fatty acid synthesis in vivo. J Lipid Res 29:1327–1335

    CAS  Google Scholar 

  53. Wellen KE, Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Invest 115:1111–1119

    CAS  Article  Google Scholar 

  54. Farris EJ, Griffith JQ (1949) The rat in laboratory investigation. J. B. Lippincott Company, Philadelphia

    Google Scholar 

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Acknowledgments

The present research has been supported by funding from the Bergen Medical Research Foundation.

Conflict of interest

I.H. is a minor shareholder in Seagarden AS. The other authors declare no conflicts of interest.

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Correspondence to Oddrun Anita Gudbrandsen.

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Drotningsvik, A., Mjøs, S.A., Høgøy, I. et al. A low dietary intake of cod protein is sufficient to increase growth, improve serum and tissue fatty acid compositions, and lower serum postprandial glucose and fasting non-esterified fatty acid concentrations in obese Zucker fa/fa rats. Eur J Nutr 54, 1151–1160 (2015). https://doi.org/10.1007/s00394-014-0793-x

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  • DOI: https://doi.org/10.1007/s00394-014-0793-x

Keywords

  • Obesity
  • Fish protein
  • Insulin
  • Tumor necrosis factor-alpha
  • Inflammation