Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-27T12:28:57.311Z Has data issue: false hasContentIssue false
  • English
  • Français

Biochemical hepatic alterations and body lipid composition in the herbivorous grass carp (Ctenopharyngodon idella) fed high-fat diets

Published online by Cambridge University Press:  08 March 2007

Zhen-Yu Du ,
Pierre Clouet ,
Wen-Hui Zheng ,
Pascal Degrace ,
Li-Xia Tian  and
Yong-Jian Liu
Zhen-Yu Du
Affiliation:
Institute of Aquatic Economic Animals, School of Life Sciences, Sun Yat-sen University, 510275 Guangzhou, China UPRES Lipides et Nutrition EA2422, Université de Bourgogne, 21000 Dijon, France
Pierre Clouet
Affiliation:
UPRES Lipides et Nutrition EA2422, Université de Bourgogne, 21000 Dijon, France
Wen-Hui Zheng
Affiliation:
The Research Centre of Molecular Medicine, Medicine School, Sun Yat-sen University, 510089 Guangzhou, China
Pascal Degrace
Affiliation:
UPRES Lipides et Nutrition EA2422, Université de Bourgogne, 21000 Dijon, France
Li-Xia Tian
Affiliation:
Institute of Aquatic Economic Animals, School of Life Sciences, Sun Yat-sen University, 510275 Guangzhou, China
Yong-Jian Liu*
Affiliation:
Institute of Aquatic Economic Animals, School of Life Sciences, Sun Yat-sen University, 510275 Guangzhou, China
*
*Corresponding author: Professor Yong-Jian Liu, fax +86 20 84115896, email duzhenyu@263.net
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

High-fat diets may have favourable effects on growth of some carnivorous fish because of the protein-sparing effect of lipids, but high-fat diets also exert some negative impacts on flesh quality. The goal of the study was therefore to determine the effects of fat-enriched diets in juvenile grass carp (Ctenopharyngodon idella) as a typical herbivorous fish on growth and possible lipid metabolism alterations. Three isonitrogenous diets containing 2, 6 or 10% of a mixture of lard, maize oil and fish oil (1:1:1, by weight) were applied to fish for 8 weeks in a recirculation system. Data show that feeding diets with increasing lipid levels resulted in lowered feed intake, decreased growth and feed efficiency, and increased mesenteric fat tissue weight. Concomitantly, alteration of lipoprotein synthesis and greater level of lipid peroxidation were apparent in blood. In liver, muscle and mesenteric fat tissue, the percentages of α-linolenic acid and DHA were significantly increased or tended to increase with higher dietary lipid levels. Biochemical activity measurements performed on liver showed that, with the increase in dietary lipid level, there was a decrease in both mitochondrial and peroxisomal fatty acid oxidation capacities, which might contribute, at least in part, to the specific accumulation of α-linolenic acid and DHA into cells more active in membrane building. On the whole, grass carp have difficulty in energetically utilising excess dietary fat, especially when enriched in n−3 PUFA that are susceptible to peroxidation.

Keywords

Grass carpHigh-fat dietsLipid compositionβ-Oxidation
Type
Research Article
Information
British Journal of Nutrition , Volume 95 , Issue 5 , May 2006 , pp. 905 - 915
Copyright
Copyright © The Nutrition Society 2006

References

Aebi, HCatalase. In Methods of Enzymatic Analysis [Bergmeyer, HU] New York: Academic Press 1974 673–684Google ScholarPubMed
Arranz-Pena, ML, Tasende-Mata, J & Martin-Gil, FJComparison f two homogeneous assays with a precipitation method and an ultracentrifugation method for the measurement of HDL-cholesterol.Clin Chem 1998 44 2499–2505CrossRefGoogle Scholar
Arzel, J, Martinez López, FX, Métailler, R, Stéphan, G, Viau, M, Gandemer, G & Guillaume, JEffect of dietary lipid on growth performance and body composition of brown trout (Salmo trutta) reared in seawater. Aquaculture 1994 123 361–375CrossRefGoogle Scholar
Austreng, EFat and protein in diets for salmonid fishes. VI.Digestibility and feed utilization by rainbow trout (Salmo gairdneri Richardson) fed diets containing different levels of fat. Sci Rep Agric Univ Norway 1979 58 1–12Google Scholar
Austreng, E & Krogdahl, AFood quality of cultured salmonids can be influenced. Feedstuff 1987 59 12–14Google Scholar
Bachorik, PS & Ross, JWNational cholesterol education program recommendations for measurement of low-density lipoprotein cholesterol. Clin Chem 1995 41 1414–1420CrossRefGoogle ScholarPubMed
Bancroft, JD & Stevens, ATheory and Practice of Histopathological Techniques. Edinburgh: Churchill Livingstone 1977Google Scholar
Beamish, FWH & Medland, TEProtein sparing effects in large rainbow trout, Salmo gairdneri. Aquaculture 1986 55 35–42CrossRefGoogle Scholar
Bell, JG, McEvoy, JTocher, DR, McGhee, F, Campbell, PJ & Sargent, JRReplacement of fish oil with rapeseed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid compositions and hepatocyte fatty acid metabolism. J Nutr 2001 131 1535–1543CrossRefGoogle ScholarPubMed
Berge, GM & Storebakken, TEffect of dietary fat level on weight gain, digestibility, and fillet composition of Atlantic halibut. Aquaculture 1991 99 331–338CrossRefGoogle Scholar
Bilinski, E & Jonas, EEEffects of coenzyme A and carnitine on fatty acid oxidation by rainbow trout mitochondria. J Fish Res Board Can 1970 27 857–864CrossRefGoogle Scholar
Bligh, EC & Dyer, WJA rapid method of total lipid extraction and purification. Can J Biochem Physiol 1959 37 911–927CrossRefGoogle ScholarPubMed
Bremer, JThe effect of fasting on the activity of liver carnitine palmitoyltransferase and its inhibition by malonyl-CoA. Biochim Biophys Acta 1981 665 628–631CrossRefGoogle ScholarPubMed
Cacerez-Martinez, C, Cadena-Roa, M & Metailler, RNutritional requirements of turbot (Scophthalmus maximus): I. A preliminary study of protein and lipid utilization. J World Maricult Soc 1984 15 191–202CrossRefGoogle Scholar
Chen, SH, Li, SF, Liu, ZS, Qiu, QF & Lin, LKApplication of Nuclear Technology in Biology, Guangzhou, China: Zhongshan University Press 1992 61Google Scholar
Cho, CY, Kaushik, SJEffects of protein intake on metabolizable and net energy values of fish diets. In Nutrition and Feeding in Fish. Proceedings of International Symposium on Fish Feeding and Nutrition. [CB, Cowey, AM, Mackie and JG, Bell] London: Academic Press 1985 95–117Google Scholar
Cho, CY & Kaushik, SJNutritional energetics in fish: energy and protein utilization in rainbow trout (Salmo gairdneri). World Rev Nutr Diet 1990 61 132–172CrossRefGoogle ScholarPubMed
Clouet, P, Niot, I & Bézard, JPathway of alpha-linolenic acid through the mitochondrial outer membrane in the rat liver and influence on the rate of oxidation Biochem J 1989 263 867–873CrossRefGoogle ScholarPubMed
Demar, JC, Ma, K, Chang, L, Bell, JM & Rapoport, SIAlphalinolenic acid does not contribute appreciably to docosahexaenoic acid within brain phospholipids of adult rats fed a diet enriched in docosahexaenoic acid. J Neurochem 2005 94 1063–1076CrossRefGoogle Scholar
Dias, J, Alvarez, MJ, Diez, A, Arzel, J, Corraze, G, Bautista, JM & Kaushik, SJRegulation of hepatic lipogenesis by dietary protein/energy in juvenile Eruopean seabass (Dicentrarchuslabrax). Aquaculture 1998 161 169–186CrossRefGoogle Scholar
Dos Santos, J, Burkow, IC & Jobling, MPatterns of growth and lipid deposition in cod, Gadus morhua L., fed natural prey and fishbased feeds. Aquaculture 1993 110 173–189CrossRefGoogle Scholar
Du, ZY, Liu, YJ, Tian, LX, Wang, JT, Wang, Y & Liang, GYEffect of dietary lipid level on growth, feed utilization and body composition by juvenile grass carp (Ctenopharyngodon idella). Aquacult Nutr 2005 11 139–146CrossRefGoogle Scholar
Forman, BM, Chen, J & Evans, RMHypolipidemic drugs, polyunsaturated fatty acids and eicosanoids are ligands for PPAR alpha and delta. Proc Natl Acad Sci U S A 1997 94 4312–4317CrossRefGoogle ScholarPubMed
Frøyland, L, Lie, ø & Berge, RKMitochondrial and peroxisomal β-oxidation capacities in various tissues from Atlantic salmon Salmo salar. Aquacult Nutr 2000 6 85–89CrossRefGoogle Scholar
Garling, DL & Wilson, RPEffect of dietary carbohydrate to lipid ratio on growth and body composition of fingerling channel catfish. Prog Fish Cult 1977 39 43–47CrossRefGoogle Scholar
Gavino, GR & Gavino, VCRat liver outer mitochondrial carnitine palmitoyltransferase activity towards long-chain polyunsaturated fatty acids and their CoA esters. Lipids 1991 26 266–270CrossRefGoogle ScholarPubMed
Gaye-Siessegger, J, Focken, U, Abel, H & Becker, KDietary lipid content influences the activity of lipogenic enzymes in the liver and whole body delta 13C values of Nile tilapia, Oreochromis niloticus(L). Isotopes Environ Health Stud 2004 40 181–190CrossRefGoogle Scholar
Gjedrem, TFlesh quality improvement in fish through breeding. Aquacult Int 1997 5 197–206CrossRefGoogle Scholar
Gordon, T, Castelli, WP, Hjortland, MC, Kannel, WB & Dawber, TRHigh density lipoprotein as a protective factor against coronary heart disease. Am J Med 1977 62 707–714CrossRefGoogle ScholarPubMed
Gray, JIMeasurement of lipid oxidation: a review. J Am Oil Chem Soc 1977 55 539–546CrossRefGoogle Scholar
Hagve, TA & Christophersen, BOEvidence for peroxisomal retroconversion of adrenic acid (22:4(n−6)) and docosahexaenoic acids (22:6(n−3)) in isolated liver cells. Biochim Biophys Acta 1986 875 165–173CrossRefGoogle Scholar
Halliwell, B & Gutteridge, JMCFree Radicals in Biology and Medicine, 3rd ed., Oxford: Clarendon Press 1999 936Google Scholar
Henderson, RJFatty acid metabolism in freshwater fish with particular reference to polyunsaturated fatty acids. Arch Anim Nutr 1996 49 5–22Google ScholarPubMed
Henderson, RJ & Tocher, DRThe lipid composition and biochemistry of freshwater fish. Prog Lipid Res 1987 26 281–347CrossRefGoogle ScholarPubMed
Hillestad, M, Johnsen, F, Austreng, E & Asgard, TLong-term effects of dietary fat level and feeding rate on growth, feed utilization and carcass quality of Atlantic salmon. Aquacult Nutr 1998 4 89–97Google Scholar
Hong, DD, Takahashi, Y, Kushiro, M & Ide, TDivergent effects of eicosapentaenoic and docosahexaenoic acid ethyl esters, and fish oil on hepatic fatty acid oxidation in the rat. Biochim Biophys Acta 2003 1635 29–36CrossRefGoogle ScholarPubMed
Jacobs, NJ & Vandemark, PJThe purification and properties of the alpha-glycerophosphate-oxidizing enzyme of Streptococcus faecalis. Arch Biochem Biophys 1960 88 250–255CrossRefGoogle ScholarPubMed
Johnsen, F, Hillestad, M & Austreng, EHigh energy diets for Atlantic salmon. Effects on pollution. In Fish Nutrition in Practice. Proceedings of the International Symposium on Fish Nutrition and Feeding, [Kaushik, SJ and Luquet, P] Paris: INRA 1993 391–401Google Scholar
Kaushik, SJ & Medale, FEnergy requirements, utilization and dietary supply to salmonids. Aquaculture 1994 124 81–97CrossRefGoogle Scholar
Kissileff, HR & van Itallie, TBPhysiology of the control of food intake. Ann Rev Nutr 1982 2 371–418CrossRefGoogle ScholarPubMed
Koditschek, LK & Umbreit, WWAlpha-glycerophosphate oxidase in Streptococcus faecium. J Bacteriol 1969 98 1063–1068CrossRefGoogle ScholarPubMed
Latruffe, N & Vamecq, JPeroxisome proliferators and peroxisomal proliferators activated receptor (PPARs) as regulators of lipid metabolism. Biochimie 1997 79 81–94CrossRefGoogle ScholarPubMed
Lee, DJ & Putnam, GBThe response of rainbow trout to varying protein/energy ratios in a test diet. J Nutr 1973 103 916–922CrossRefGoogle Scholar
Lee, SM, Jeon, IG & Lee, JYEffects of digestible protein and lipid levels in practical diets on growth, protein utilization and body composition of juvenile rockfish (Sebastes schlegeli). Aquaculture 2002 211 227–239CrossRefGoogle Scholar
Lie, ö, Lied, E & Lambertsen, GFeed optimization in Atlantic cod (Gadus morhua ): fat versus protein content in the feed. Aquaculture 1988 69 333–341CrossRefGoogle Scholar
Lin, DGrass carp, Ctenopharyngodon idella.In Handbook of Nutrient Requirements of Finfish, [Wilson, RP] Boca Raton, FL: CRC Press 1991 89–96Google Scholar
Lin, D, Mao, Y & Cai, FNutritional lipid liver disease of grass carp, Ctenopharyngodon idellus. Chin J Oceanol Limnol 1990 8 363–373Google Scholar
Luzzana, U, Serrini, G, Moretti, VM, Gianesini, C & Valfreá, FEffect of expanded feed with high fish oil content on growth and fatty acid composition of rainbow trout. Aquacult Int 1994 2 239–248CrossRefGoogle Scholar
Madsen, L, Frøyland, L, Dyroy, E, Helland, K & Berge, RKDocosahexaenoic and eicosapentaenoic acids are differently metabolized in rat liver during mitochondria and peroxisome proliferation. J Lipid Res 1998 39 583–593CrossRefGoogle ScholarPubMed
Mannaerts, GP, Debeer, LJ, Thomas, J & De Schepper, PJMitochondrial and peroxisomal fatty acid oxidation in liver homogenates and isolated hepatocytes from control and clofibrate-treated rats. J Biol Chem 1979 254 4585–4595CrossRefGoogle ScholarPubMed
Martino, RC, Cyrino, JEP, Portz, L & Trugo, LCEffect of dietary lipid level on nutritional performance of the surubim, Pseudoplatystoma coruscans. Aquaculture 2002 209 209–218CrossRefGoogle Scholar
Murai, T, Takeuchi, T, Watanabe, T & Nose, TEffects of dietary protein and lipid levels on performance and carcass composition of fingerling carp. Bull Jpn Soc Sci Fish 1985 51 605–608CrossRefGoogle Scholar
Murata, Hβ-Oxidation of 22:6 acid in fish liver and dark muscle mitochondria. Bull Jpn Soc Sci Fish 1979 45 379–383CrossRefGoogle Scholar
Murata, H & Higashi, TStudies on the metabolism of fatty acid in fish: rate of fatty acid decrease based on β-oxidation in carp dark muscle mitochondria. Bull Jpn Soc Sci Fish 1979 45 211–217CrossRefGoogle Scholar
Nakamura, M, Taniguti, Y, Yamamoto, M, Hino, K & Manabe, MHomogeneous assays of serum LDL-cholesterol on an automatic analyzer. Clin Chem 1997 43 260>–S261Google Scholar
Nanton, DA, Lall, SP, Ross, NW & McNiven, MAEffect of dietary lipid level on fatty acid b-oxidation and lipid composition in various tissues of haddock, Melanogrammus aeglefinus L. Comp Biochem Physiol 2003 135B 95–108Google Scholar
Peres, H & Oliva-Teles, AInfluence of temperature on protein utilization in juvenile European sea bass (Dicentrarchus labrax). Aquaculture 1999a 170 337–348CrossRefGoogle Scholar
Peres, H & Oliva-Teles, AEffect of dietary lipid level on growth performance and feed utilization by European sea bass juvenile (Dicentrarchus labrax). Aquaculture 1999b 179 325–334CrossRefGoogle Scholar
Pullman, DL, Liesman, JS & Emery, RSA species comparison of liver slice synthesis and secretion of triacylglycerol from nonesterified fatty acids in media. J Anim Sci 1990 68 1395–1399CrossRefGoogle Scholar
Regost, C, Arzel, J, Cardinal, M, Robin, J, Laroche, M & Kaushik, SJDietary lipid level, hepatic lipogenesis and flesh quality in turbot (Psetta maxima). Aquaculture 2001 193 291–309CrossRefGoogle Scholar
Ren, B, Thelen, AP, Petters, JM, Gonzalez, FJ & Jump, DBPolyunsaturated fatty acid suppression of hepatic fatty acid synthase and S14 gene expresstion does not require peroxisome proliferator activated receptor α. J Biol Chem 1997 272 26827–26832CrossRefGoogle Scholar
Richmond, WPreparation and properties of a cholesterol oxidase from Nocardia sp. and its application to the enzymatic assay of total cholesterol in serum. Clin Chem 1973 19 1350–1356CrossRefGoogle Scholar
Roeschlau, P, Bernt, E & Gruber, WEnzymatic determination of total cholesterol in serum. Clin Chem Clin Biochem 1974 12 226Google ScholarPubMed
Rueda-Jasso, R, Conceicao, LEC, Dias, J, De Coen, W, Gomes, E, Rees, JF, Soares, F, Dinis, MT & Sorgeloos, PEffect of dietary non-protein energy levels on condition and oxidative status of Senegalese sole (Solea senegalensis) juveniles. Aquaculture 2004 231 417–433CrossRefGoogle Scholar
Ruyter, B, Andersen, ø, Dehli, A, Östlund, F, Gjøen, T & Thomassen, MSPeroxisome proliferator activated receptors in Atlantic salmon (Salmo salar): effects on PPAR transcription and acyl-CoA oxidase activity in hepatocytes by peroxisome proliferators and fatty acids. Biochim Biophys Acta 1997 1348 331–338CrossRefGoogle ScholarPubMed
Sargent, JR, Bell, JG, McEvoy, L, Tocher, DR & Estevez, A Recent developments in the essential fatty acid nutrition of fish. Aquaculture 1999 177 191–199CrossRefGoogle Scholar
Schwartz, MW, Baskin, DG, Kaiyala, KJ & Woods, SCModel for the regulation of energetic balance and adiposity by the central nervous system. Am J Clin Nutr 1999 69 584–596CrossRefGoogle Scholar
Silverstein, JT, Shearer, KS, Dickhoff, WW & Plisetskaya, EMRegulation and nutrient intake and energy balance in salmon. Aquaculture 1999 177 161–169CrossRefGoogle Scholar
Smith, PK, Krohn, RI, Hermanson, GT, Mallia, AK, Gartner, FH, Provenzano, MD, Fujimoto, EK, Goeke, NM, Olson, BJ & Klenk, DCMeasurement of protein using bicinchoninic acid. Anal Biochem 1985 150 76–85CrossRefGoogle ScholarPubMed
Stephan, G, Dreanno, C, Guillaume, J & Arzel, JIncidence of different amounts of proteins, lipids and carbohydrates in diets on the muscle lipid composition in the turbot (Scophthalmus maximus). Ichtyophysiol Acta 1996 19 11–30Google Scholar
Stephan, G, Guillaume, J & Lamour, FLipid peroxidation in turbot (Scophthalmus maximus) tissue: effect of dietary vitamin E and dietary n−6 or n−3 polyunsaturated fatty acids. Aquaculture 1995 130 251–268CrossRefGoogle Scholar
Stowell, SL & Gatlin III, DMEffects of dietary pantethine and lipid levels on growth and body composition of channel catfish (Ictalurus punctatus). Aquaculture 1992 108 177–188CrossRefGoogle Scholar
Takeuchi, TEssential fatty acid requirements in carp. Arch Tierernahr 1996 49 23–32CrossRefGoogle ScholarPubMed
Takeuchi, T, Watanabe, T & Ogino, CAvailability of carbohydrate and lipid as dietary energy sources for carp. Bull Jpn Soc Sci Fish 1979 45 977–982CrossRefGoogle Scholar
Vamecq, J, Vallee, L, De la Porte, PL, Fontaine, M, De Cramer, D, Van den Branden, C, Lafont, H, Grataroli, R & Nalbone, GEffect of various n−3/n−6 fatty acid ratio contents of high diets on rat liver and heart peroxisomal and mitochondrial βoxidation. Biochim Biophys Acta 1993 1170 151–156CrossRefGoogle Scholar
van den Branden, C, De Craemer, D, Pauwels, M & Vamecq, JPeroxisomes in mice fed a diet supplemented with low doses of fish oil. Lipids 1995 30 701–705CrossRefGoogle ScholarPubMed
Veerkamp, JH, Van Moerkerk, HT, Glatz, JF & Van Hinsbergh, VWIncomplete palmitate oxidation in cell-free systems of rat and human muscles. Biochim Biophys Acta 1983 753 399–410CrossRefGoogle ScholarPubMed
Wang, JT, Liu, YJ, Tian, LX, Mai, KS, Du, ZY, Wang, Y & Yang, HJEffect of dietary lipid level on growth performance, lipid deposition, hepatic lipogenesis in juvenile cobia (Rachycentron canadum). Aquaculture 2005 249 439–447CrossRefGoogle Scholar
Watanabe, TLipid nutrition in fish. Comp Biochem Physiol 1982 73B 3–15Google Scholar
Watanabe, T, Takeuchi, T & Ogino, CStudies on the sparing effect of lipids on dietary protein in rainbow trout (Salmo gairdneri). In Proceedings of World Symposium on Finfish Nutrition and Fishfeed Technology, [Halver, JE and Tiews, K] Berlin: Heenemann. 1979 113–125Google Scholar
Weatherup, RN, McCracken, KJ, Foy, R, Ride, D, McKendry, J, Maris, RJ & Hoey, R\ The effects of dietary fat content on performance and body composition of farmed rainbow trout Oncorhynchus mykiss. Aquaculture 1997 15 173–184CrossRefGoogle Scholar
Weissbach, H, Smith, TE, Daly, JW, Witkop, B & Udenfriend, SA rapid spectrophotometric assay of mono-amine oxidase based on the rate of disappearance of kynuramine. J Biol Chem 1960 235 1160–1163CrossRefGoogle ScholarPubMed
Winston, GW & Di Giulio, RTProoxidant and antioxidant mechanism in aquatic organisms. Aquat Toxicol 1991 19 137–161CrossRefGoogle Scholar
Xu, RP, Hung, SSO & German, JBWhite sturgeon tissue fatty acid compositions are affected by dietary lipids. J Nutr 1993 123 1685–1692CrossRefGoogle ScholarPubMed
Yu, SK, Olsen, CE & Marcussen, JMethods for the assay of 1,5-anhydro-D-fructose and α-1,4-glucanlyase. Carbohyd Res 1998 305 73–82CrossRefGoogle Scholar
Zheng, WH, Liu, YJ & Tian, LXA simple method for fatty acid analysis of fish liver. Chin J Health Lab Tech 2002 2 159Google Scholar