Fish Physiology and Biochemistry

, Volume 43, Issue 6, pp 1733–1745 | Cite as

Effect of dietary betaine on growth performance, antioxidant capacity and lipid metabolism in blunt snout bream fed a high-fat diet

  • Jean-Jacques Yao Adjoumani
  • Kaizhou Wang
  • Man Zhou
  • Wenbin Liu
  • Dingdong Zhang
Article
  • 182 Downloads

Abstract

An 8-week feeding experiment was conducted to determine the effect of dietary betaine levels on the growth performance, antioxidant capacity, and lipid metabolism in high-fat diet-fed blunt snout bream (Megalobrama amblycephala) with initial body weight 4.3 ± 0.1 g [mean ± SEM]. Five practical diets were formulated to contain normal-fat diet (NFD), high-fat diet (HFD), and high-fat diet with betaine addition (HFB) at difference levels (0.6, 1.2, 1.8%), respectively. The results showed that the highest final body weight (FBW), weight gain ratio (WGR), specific growth rate (SGR), condition factor (CF), and feed intake (FI) (P < 0.05) were obtained in fish fed 1.2% betaine supplementation, whereas feed conversion ratio (FCR) was significantly lower in the same group compared to others. Hepatosomatic index (HSI) and abdominal fat rate (AFR) were significantly high in fat group compared to the lowest in NDF and 1.2% betaine supplementation, while VSI and survival rate (SR) were not affected by dietary betaine supplementation. Significantly higher (P < 0.05), plasma total cholesterol (TC), triglycerides (TG), low-density lipoprotein (LDL), aspartate transaminase (AST), alanine transaminase (ALT), cortisol, and lower high-density lipoprotein (HDL) content were observed in HFD but were improved when supplemented with 1.2% betaine. In addition, increase in superoxide dismutase (SOD), catalase (CAT), and reduced glutathione (GSH) in 1.2% betaine inclusion could reverse the increasing malondialdehyde (MDA) level induced by HFD. Based on the second-order polynomial analysis, the optimum growth of blunt snout bream was observed in fish fed HFD supplemented with 1.2% betaine. HFD upregulated fatty acid synthase messenger RNA (mRNA) expression and downregulated carnitine palmitoyltransferase 1, peroxisome proliferator-activated receptor α, and microsomal triglyceride transfer protein mRNA expression; nevertheless, 1.2% betaine supplementation significantly reversed these HFD-induced effects, implying suppression of fatty acid synthesis, β-oxidation, and lipid transport. This present study indicated that inclusion of betaine (1.2%) can significantly improve growth performance and antioxidant defenses, as well as reduce fatty acid synthesis and enhance mitochondrial β-oxidation and lipid transportation in high-fat diet-fed blunt snout bream, thus effectively alleviating fat accumulation in the liver by changing lipid metabolism.

Keywords

Betaine Megalobrama amblycephala Growth performance Lipid metabolism Antioxidant capacity Gene 

Notes

Acknowledgements

This work was supported by the China Agriculture Research System (grant number CARS-46-20).

References

  1. Akshayamanai SMH, Prakash P (2016) Effect of betaine hydrochloride as feed attractant on growth, survival and feed utilization of common carp (Cyprinus carpio). J Aquaculture Marine Biol 4(3):00083. doi: 10.15406/jamb.2016.04.00083 Google Scholar
  2. Aksnes A, Mundheim H, Toppe J, Albrektsen S (2008) The effect of dietary hydroxyproline supplementation on salmon (Salmo salar L.) fed high plant protein diets. Aquaculture 275(1–4):242–249CrossRefGoogle Scholar
  3. Alirezaei M, Jelodar G, Niknam P, Ghayemi Z, Nazifi S (2011) Betaine prevents ethanol-induced oxidative stress and reduces total homocysteine in the rat, cerebellum. J Physiol Biochem 67(4):605–612CrossRefPubMedGoogle Scholar
  4. Allen Davis D, Arnold CR (2000) Replacement of fish meal in practical diets for the Pacific white shrimp, Litopenaeus vannamei. Aquaculture 185(3–4):291–298CrossRefGoogle Scholar
  5. And, G.W., Davis, D.A. 2005. Interrelationship among methionine, choline, and betaine in channel catfish Ictalurus punctutus. J World Aquacult Soc, 36(3), 337–345Google Scholar
  6. AOAC (1990) AOAC Official Methods of Analysis. 15th edition, Association of Official Analytical Chemists, ArlingtonGoogle Scholar
  7. Bolla S, Nicolaisen O, Amin A (2011) Liver alterations induced by long term feeding on commercial diets in Atlantic halibut (Hippoglossus hippoglossus L.) females. Histological and biochemical aspects. Aquaculture 312(1–4):117–125CrossRefGoogle Scholar
  8. Cañavate JP, Prieto A, Zerolo R, Sole M, Sarasquete C, Fernández-Díaz C (2007) Effects of light intensity and addition of carotene rich Dunaliella salina live cells on growth and antioxidant activity of Solea senegalensis Kaup (1858) larval and metamorphic stages. J Fish Biol 71(3):781–794CrossRefGoogle Scholar
  9. Chen Q-Q, Liu W-B, Zhou M, Dai Y-J, Xu C, Tian H-Y, Xu W-N (2016) Effects of berberine on the growth and immune performance in response to ammonia stress and high-fat dietary in blunt snout bream Megalobrama amblycephala. Fish Shellfish Immunol 55:165–172CrossRefPubMedGoogle Scholar
  10. Du ZY, Clouet P, Zheng WH, Degrace P, Tian LX, Liu YJ (2006) Biochemical hepatic alterations and body lipid composition in the herbivorous grass carp (Ctenopharyngodon idella) fed high-fat diets. Br J Nutr 95(5):905–915CrossRefPubMedGoogle Scholar
  11. Esteve-Garcia E, Mack S (2000) The effect of dl-methionine and betaine on growth performance and carcass characteristics in broilers. Anim Feed Sci Technol 87(1–2):85–93CrossRefGoogle Scholar
  12. Fange R, Grove DS (1979) Digestion in Fish Physiology, vol VIII. Acad. Press, NY. pp 162–260Google Scholar
  13. Ferré P (2004) The biology of peroxisome proliferator-activated receptors. Diabetes 53(1):43–50CrossRefGoogle Scholar
  14. Ganesan B, Buddhan S, Anandan R, Sivakumar R, Anbinezhilan R (2010) Antioxidant defense of betaine against isoprenaline-induced myocardial infarction in rats. Mol Biol Rep 37(3):1319CrossRefPubMedGoogle Scholar
  15. Ganesan B, Rajesh R, Anandan R, Dhandapani N (2007a) Biochemical studies on the protective effect of betaine on mitochondrial function in experimentally induced myocardial infarction in rats. J Health Sci 53(6):671–681CrossRefGoogle Scholar
  16. Ganesan B, Rajesh R, Anandan R, Dhandapani N (2007b) Protective effect of betaine on changes in the levels of protein, glycoproteins and amino acids in isoprenaline-induced myocardial infarction in rats. Afr J Biochem Res 1:117–123Google Scholar
  17. Genc MA, Tekelioglu N, Yilmaz E, Hunt AO, Yanar Y (2006) Effect of dietary betaine on growth performance and body composition of Oreochromis aureus reared in fresh and sea watera comparative study. J Animal Veterinary Advances 5(12)Google Scholar
  18. Goh Y, Tamura T (1980) Olfactory and gustatory responses to amino acids in two marine teleosts—red sea bream and mullet. Comparative Biochemistry & Physiology Part C Comparative Pharmacology 66(2):217–224CrossRefGoogle Scholar
  19. Gui D, Liu W, Shao X, Xu W (2010) Effects of different dietary levels of cottonseed meal protein hydrolysate on growth, digestibility, body composition and serum biochemical indices in crucian carp (Carassius auratus gibelio). Anim Feed Sci Technol 156(3–4):112–120CrossRefGoogle Scholar
  20. Habte-Tsion HM, Liu B, Ge XP, Xie J, Xu P, Mingchun R (2013) Effects of dietary protein levels on the growth performance, muscle composition, blood composition and digestive enzymes activities of Wuchang bream, Megalobrama amblycephala fry.Nanjing, Nanjing Agricultural University,M.Sc.degree Thesis, p. 83Google Scholar
  21. Hassan RA, Ebeid TA, El-Lateif AIA, Ismail NB (2011) Effect of dietary betaine supplementation on growth, carcass and immunity of New Zealand white rabbits under high ambient temperature. Livest Sci 135(2):103–109CrossRefGoogle Scholar
  22. He S, Zhao S, Dai S, Liu D, Bokhari SG (2015) Effects of dietary betaine on growth performance, fat deposition and serum lipids in broilers subjected to chronic heat stress. Anim Sci J 86(10):897–903CrossRefPubMedGoogle Scholar
  23. Huang QC, Xu ZR, Han XY, Li WF (2008) Effect of dietary betaine supplementation on lipogenic enzyme activities and fatty acid synthase mRNA expression in finishing pigs. Anim Feed Sci Technol 140(3):365–375CrossRefGoogle Scholar
  24. Jobling M (2001) Nutrient partitioning and the influence of feed composition on body composition. In: Houlihan D, Boujard T, Joblin M (eds) Food intake in fish. 2001:354–376Google Scholar
  25. Jones DP, Eklöw L, Thor H, Orrenius S (1981) Metabolism of hydrogen peroxide in isolated hepatocytes: relative contributions of catalase and glutathione peroxidase in decomposition of endogenously generated H2O2. Arch Biochem Biophys 210(2):505–516CrossRefPubMedGoogle Scholar
  26. Junnila M, Rahko T, Sukura A, Lindberg LA (2000) Reduction of carbon tetrachloride-induced hepatotoxic effects by oral administration of betaine in male Han-Wistar rats: a morphometric histological study. Vet Pathol 37(3):231–238CrossRefPubMedGoogle Scholar
  27. Kang X, Zhong W, Liu J, Song Z, Mcclain CJ, Kang YJ, Z.Z. (2009) Zinc supplementation reverses alcohol-induced steatosis in mice through reactivating hepatocyte nuclear factor-4α and peroxisome proliferator-activated receptor-α. Hepatology 50(4):1241CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kasper CS, White MR, Brown PB (2002) Betaine can replace choline in diets for juvenile Nile tilapia, Oreochromis niloticus. Aquaculture 205(1–2):119–126CrossRefGoogle Scholar
  29. Kohen R, Nyska A (2002) Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol Pathol 30(6):620CrossRefPubMedGoogle Scholar
  30. Kolkovski S, Arieli A, Tandler A (1997) Visual and chemical cues stimulate microdiet ingestion in sea bream larvae. Aquac Int 5(6):527–536CrossRefGoogle Scholar
  31. Korman SH, Waterham HR, Gutman A, Jakobs C, Wanders RJA (2005) Novel metabolic and molecular findings in hepatic carnitine palmitoyltransferase I deficiency. Mol Genet Metab 86(3):337–343CrossRefPubMedGoogle Scholar
  32. Li X, Jiang Y, Liu W, Ge X (2012a) Protein-sparing effect of dietary lipid in practical diets for blunt snout bream (Megalobrama amblycephala) fingerlings: effects on digestive and metabolic responses. Fish Physiol Biochem 38(2):529–541CrossRefPubMedGoogle Scholar
  33. Li XF, Liu WB, Lu KL, Xu WN, Wang Y (2012b) Dietary carbohydrate/lipid ratios affect stress, oxidative status and non-specific immune responses of fingerling blunt snout bream, Megalobrama amblycephala. Fish Shellfish Immunol 33(2):316–323CrossRefPubMedGoogle Scholar
  34. Lu KL, Xu WN, Li JY, Li XF, Huang GQ, Liu WB (2013) Alterations of liver histology and blood biochemistry in blunt snout bream, (Megalobrama amblycephala) fed high-fat diets. Fish Sci 79(4):661–671CrossRefGoogle Scholar
  35. Lu KL, Xu WN, Liu WB, Wang LN, Zhang CN, Li XF (2014a) Association of mitochondrial dysfunction with oxidative stress and immune suppression in blunt snout bream (Megalobrama amblycephala) fed a high-fat diet. J Aquat Anim Health 26(2):100–112CrossRefPubMedGoogle Scholar
  36. Lu KL, Xu WN, Wang LN, Zhang DD, Zhang CN, Liu WB (2014b) Hepatic β-oxidation and regulation of carnitine palmitoyltransferase (CPT) I in blunt snout bream (Megalobrama amblycephala) fed a high fat diet. PLoS One 9(3):e93135CrossRefPubMedPubMedCentralGoogle Scholar
  37. Luo Z, Tan XY, Liu XJ, Wen H (2011) Effect of dietary betaine levels on growth performance and hepatic intermediary metabolism of GIFT strain of Nile tilapia (Oreochromis niloticus) reared in freshwater. Aquac Nutr 17(4):361–367CrossRefGoogle Scholar
  38. Mackie AM, Mitchell AI (2006) Studies on the chemical nature of feeding stimulants for the juvenile European eel, Anguilla anguilla (L.) J Fish Biol 22(4):425–430CrossRefGoogle Scholar
  39. Mcdevitt RM, Mack S, Wallis IR (2000) Can betaine partially replace or enhance the effect of methionine by improving broiler growth and carcase characteristics? Br Poult Sci 41(4):473–480Google Scholar
  40. Mensinger AF, Walsh PJ, Hanlon RT (2005) Blood biochemistry of the oyster toadfish. J Aquat Anim Health 17(17):170–176CrossRefGoogle Scholar
  41. Miller JK, Brzezinska-Slebodzinska E, Madsen FC (1993) Oxidative stress, antioxidants, and animal function. J Dairy Sci 76(9):2812–2823CrossRefPubMedGoogle Scholar
  42. Ministry of Agriculture of the People’s Republic of China (2013) Chinese fishery statistical yearbook. Chinese Agricultural Press, Beijing (in Chinese)Google Scholar
  43. Moeckel GW, Shadman R, Fogel JM, Sadrzadeh SM (2002) Organic osmolytes betaine, sorbitol and inositol are potent inhibitors of erythrocyte membrane ATPases. Life Sci 71(20):2413CrossRefPubMedGoogle Scholar
  44. Moustaïd N, Jones BH, Taylor JW (1996) Insulin increases lipogenic enzyme activity in human adipocytes in primary culture. J Nutr 126(4):865–870PubMedGoogle Scholar
  45. Papatryphon E, Soares JH Jr (2000) Identification of feeding stimulants for striped bass, Morone saxatilis. Aquaculture 185(3–4):339–352CrossRefGoogle Scholar
  46. Parvez S, Raisuddin S (2005) Protein carbonyls: novel biomarkers of exposure to oxidative stress-inducing pesticides in freshwater fish Channa punctata (Bloch). Environ Toxicol Pharmacol 20(1):112–117CrossRefPubMedGoogle Scholar
  47. Patel VB, Mehta K (2015) Betaine in context. Food & Nutritional Components in Focus 2015(7):3–8CrossRefGoogle Scholar
  48. Quesada H, Bas JMD, Pajuelo D, Díaz S, Fernandezlarrea J, Pinent M, Arola L, Salvadó MJ, Bladé C (2009) Grape seed proanthocyanidins correct dyslipidemia associated with a high-fat diet in rats and repress genes controlling lipogenesis and VLDL assembling in liver. Int J Obes 33(9):1007–1012CrossRefGoogle Scholar
  49. Ronnestad I, Tonheim SK, Fyhn HJ, Rojasgarcia CR, Kamisaka Y, Koven W, Finn RN, Terjesen BF, Barr Y, Lec C (2003) The supply of amino acids during early feeding stages of marine fish larvae: a review of recent findings. Aquaculture 227(1–4):147–164CrossRefGoogle Scholar
  50. Rumsey GL (1991) Choline-betaine requirements of rainbow trout (Oncorhynchus mykiss). Aquaculture 95(1–2):107–116CrossRefGoogle Scholar
  51. Sargent J, Bell G, McEvoy L, Tocher D, Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177(1–4):191–199CrossRefGoogle Scholar
  52. Sheard NF, Zeisel SH (1989) Choline: an essential dietary nutrient? Nutrition 5(1):1–5Google Scholar
  53. Sies H (1992) Oxidative stress: oxidants and antioxidants. Cardiovasc Res 82(8):291Google Scholar
  54. Song Z, Deaciuc I, Zhou Z, Song M, Chen T, Hill D, Mcclain CJ (2007) Involvement of AMP-activated protein kinase in beneficial effects of betaine on high-sucrose diet-induced hepatic steatosis. Am J Physiol Gastrointest Liver Physiol 293(4):G894–G902CrossRefPubMedPubMedCentralGoogle Scholar
  55. Takeuchi-Yorimoto A, Noto T, Yamada A, Miyamae Y, Oishi Y, Matsumoto M (2013) Persistent fibrosis in the liver of choline-deficient and iron-supplemented l-amino acid-defined diet-induced nonalcoholic steatohepatitis rat due to continuing oxidative stress after choline supplementation. Toxicol Applied Pharmacol 268(3):264–277CrossRefGoogle Scholar
  56. Trevisan M, Browne R, Ram M, Muti P, Freudenheim J, Carosella AM, Armstrong D (2001) Correlates of markers of oxidative status in the general population. Am J Epidemiol 154(4):348–356CrossRefPubMedGoogle Scholar
  57. Turan F, Akyurt I (2005) Effects of androstenedione, a phytoandrogen, on growth and body composition in the African catfish (Clarias gariepinus). Isr J Aquacult Bamidgeh 57(1):62–66Google Scholar
  58. Wang L, Zhang H, Zhou J, Liu Y, Yang Y (2014a) Betaine attenuates hepatic steatosis by reducing methylation of the MTTP promoter and elevating genomic methylation in mice fed a high-fat diet. J Nutr Biochem 25(3):329-36Google Scholar
  59. Wang L, Chen L, Tan Y, Wei J, Chang Y, Jin T, Zhu H (2012) Betaine supplement alleviates hepatic triglyceride accumulation of apolipoprotein E deficient mice via reducing methylation of peroxisomal proliferator-activated receptor alpha promoter. Lipids Health Dis 12(1):34CrossRefGoogle Scholar
  60. Wang LJ, Zhang HW, Zhou JY, Liu Y, Yang Y, Chen XL, Zhu CH, Zheng RD, Ling WH, Zhu HL (2014b) Betaine attenuates hepatic steatosis by reducing methylation of the MTTP promoter and elevating genomic methylation in mice fed a high-fat diet. J Nutr Biochem 25(3):329Google Scholar
  61. Wang YZ, Xu ZR, Chen ML (2000) Effect of betaine on carcass fat metabolism of meat duck. Chinese J Veterinaryence 20:409–413Google Scholar
  62. Wang YZ, Xu ZR, Feng J (2004) The effect of betaine and dl-methionine on growth performance and carcass characteristics in meat ducks. Anim Feed Sci Technol 116(1–2):151–159CrossRefGoogle Scholar
  63. Wang SH, Chen JC (2005) The protective effect of chitin and chitosan against vibrio alginolyticus, in white shrimp Litopenaeus vannamei[J]. Fish Shellfish Immunol 19(19):191–204CrossRefPubMedGoogle Scholar
  64. Wang Z, Yao T, Pini M, Zhou Z, Fantuzzi G, Song Z (2010) Betaine improved adipose tissue function in mice fed a high-fat diet: a mechanism for hepatoprotective effect of betaine in nonalcoholic fatty liver disease. Ajp Gastrointestinal & Liver Physiology 298(5):G634CrossRefGoogle Scholar
  65. Watanabe T (1982) Lipid nutrition in fish. Comparative Biochemistry & Physiology B Comparative Biochemistry 73(1):3–15CrossRefGoogle Scholar
  66. Wetterau JR, Aggerbeck LP, Bouma ME, Eisenberg C, Munck A, Hermier M, Schmitz J, Gay G, Rader DJ, Gregg RE (1992) Absence of microsomal triglyceride transfer protein in individuals with Abetalipoproteinemia. Science 258(258):999–1001CrossRefPubMedGoogle Scholar
  67. Xu L, Huang D, Hu Q, Wu J, Wang Y, Feng J (2015) Betaine alleviates hepatic lipid accumulation via enhancing hepatic lipid export and fatty acid oxidation in rats fed with a high-fat diet. Br J Nutr 113(6):1835–1843CrossRefPubMedGoogle Scholar
  68. Xue M, Cui Y (2001) Effect of several feeding stimulants on diet preference by juvenile gibel carp (Carassius auratus gibelio), fed diets with or without partial replacement of fish meal by meat and bone meal. Aquaculture 198(3–4):281–292CrossRefGoogle Scholar
  69. Yang H, Li F, Xiong X, Kong X, Zhang B, Yuan X, Fan J, Duan Y, Geng M, Li L (2012) Soy isoflavones modulate adipokines and myokines to regulate lipid metabolism in adipose tissue, skeletal muscle and liver of male Huanjiang mini-pigs. Mol Cell Endocrinol 365(1):44–51CrossRefPubMedGoogle Scholar
  70. Zhang XD, Zhu YF, Cai LS, TX W (2008) Effects of fasting on the meat quality and antioxidant defenses of market-size farmed large yellow croaker (Pseudosciaena crocea). Aquaculture 280:136–139CrossRefGoogle Scholar
  71. Zhou J, Li C, Wang L, Ji H, Zhu T (2015) Hepatoprotective effects of a Chinese herbal formulation, Yingchen decoction, on olaquindox-induced hepatopancreas injury in Jian carp (Cyprinus carpio var. Jian). Fish Physiol Biochem 41(1):153–163CrossRefPubMedGoogle Scholar
  72. Zhou Z, Ren Z, Zeng H, Yao B (2008) Apparent digestibility of various feedstuffs for bluntnose black bream Megalobrama amblycephala Yih. Aquac Nutr 14(2):153–165CrossRefGoogle Scholar
  73. Zou XT, Jian-Jun LU (2002) Effect of betaine on the regulation of the lipid metabolism in laying hen. J Integr Agric 1(9):1043–1049Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Key Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, College of Animal Science and TechnologyNanjing Agricultural UniversityNanjingPeople’s Republic of China

Personalised recommendations