Advertisement

Fish Physiology and Biochemistry

, Volume 45, Issue 1, pp 43–61 | Cite as

The effects of ethoxyquin and Angelica sinensis extracts on lipid oxidation in fish feeds and growth, digestive and absorptive capacities and antioxidant status in juvenile red carp (Cyprinus carpio var. xingguonensis): a comparative study

  • HuaTao LiEmail author
  • SiYi Tang
  • WenHao Du
  • Jun Jiang
  • PeiYuan Peng
  • Ping Yuan
  • YiHong Liao
  • Jiao Long
  • SiShun Zhou
Article
  • 133 Downloads

Abstract

Firstly, a linoleic and linolenic acid emulsion and fish feeds were incubated with graded levels of ethoxyquin (EQ) and petroleum ether extract, ethyl acetate extract (EAE), ethanol extract and aqueous extract of Angelica sinensis. The results showed that EQ and extracts of Angelica sinensis (EAs) inhibited lipid oxidation in material above. Of all of the examined EAs, EAE showed the strongest protective effects against the lipid oxidation. Moreover, EAE at high concentrations showed a stronger inhibitory effect on lipid oxidation than that of EQ. Next, 7 experimental diets that respectively supplemented 0.0, 0.2, 0.8 and 3.2 g kg−1 of EQ and EAE were fed to 280 juvenile red carp (Cyprinus carpio var. xingguonensis) with seven treatment groups for 30 days. The results indicated that dietary EAE improved growth performance in carp. Moreover, dietary EAE increased the activities of trypsin, lipase, alpha-amylase, alkaline phosphatase, glutamate-oxaloacetate transaminase and glutamate-pyruvate transaminase (GPT) and decreased plasma ammonia content in carp. Meanwhile, dietary EAE reduced the levels of malondialdehyde and raised the activities of anti-superoxide anion, anti-hydroxyl radical, superoxide dismutase, catalase, glutathione peroxidase and glutathione reductase and the content of reduced glutathione in the hepatopancreas and intestine of carp. However, with the exception of GPT, dietary EQ got the opposite results to dietary EAE in carp. These results revealed that dietary EAE improved the digestive, absorptive and antioxidant capacities in fish. However, dietary EQ inhibited the digestive, absorptive and antioxidant capacities in fish. So, EAE could be used as a natural antioxidant for replacing EQ in fish feeds.

Keywords

Ethoxyquin Angelica sinensis Lipid oxidation Digestion Absorption Antioxidant 

Notes

Acknowledgements

The authors wish to thank the personnel of these teams for their kind assistance.

Funding information

This research was financially supported by the Scientific Research Fund of Sichuan Provincial Education Department (16ZB0302), the Doctoral Research Fund of Neijiang Normal University (14B07) and the Science and Technology Commission Foundation of Sichuan Province, China (2015JY0067).

Compliance with ethical standards

All the procedures described above were approved by the Institutional Animal Care and Use Committee of Neijiang Normal University in accordance with the Institutional Ethics Committee of the Chinese Institute of Chemical Biology guidelines.

Conflict of interest

The authors declare that there is no conflict of interest.

References

  1. Adam A, Crespy V, Levrat-Verny MA, Leenhardt F, Leuillet M, Demigne C, Remesy C (2002) The bioavailability of ferulic acid is governed primarily by the food matrix rather than its metabolism in intestine and liver in rats. J Nutr 132:1962–1968Google Scholar
  2. Anson NM, Berg R, Havenaar R, Bast A, Haenen GRMM (2009) Bioavailability of ferulic acid is determined by its bioaccessibility. J Cereal Sci 49:296–300Google Scholar
  3. Augustyniak A, Niezgoda A, Skolimowski J, Kontek R, Błaszczyk A (2012) Cytotoxicity and genotoxicity of ethoxyquin dimmers. Bromatol Chem Toksykol 45:228–234Google Scholar
  4. Berdikova Bohne VJ, Hamre K, Arukwe A (2006) Hepatic biotransformation and metabolite profile during a 2-week depuration period in Atlantic salmon fed graded levels of the synthetic antioxidant, ethoxyquin. Toxicol Sci 93:11–21Google Scholar
  5. Błaszczyk A, Augustyniak A, Skolimowski J (2013) Ethoxyquin: an antioxidant used in animal feed. Int J Food Sci Nutr 2013:1–12Google Scholar
  6. Błaszczyk A, Skolimowski J (2015) Cytotoxicity and genotoxicity of ethoxyquin used as an antioxidant. Food Rev Intl 31:222–235Google Scholar
  7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254Google Scholar
  8. Chen J, Zhou X, Feng L, Liu Y, Jiang J (2009) Effects of glutamine on hydrogen peroxide-induced oxidative damage in intestinal epithelial cells of Jian carp (Cyprinus carpio var. Jian). Aquaculture 288:285–289Google Scholar
  9. Chen YJ, Liu YJ, Tian LX, Niu J, Liang GY, Yang HJ, Yuan Y, Zhang YQ (2013) Effect of dietary vitamin E and selenium supplementation on growth, body composition, and antioxidant defense mechanism in juvenile largemouth bass (Micropterus salmoide) fed oxidized fish oil. Fish Physiol Biochem 39:593–604Google Scholar
  10. Correa LM, Kochhann D, Becker AG, Pavanato MA, Llesuy SF, Loro VL, Raabe A, Mesko MF, Flores EM, Dressler VL, Baldisserotto B (2008) Biochemistry, cytogenetics and bioaccumulation in silver catfish (Rhamdia quelen) exposed to different thorium concentrations. Aquat Toxicol 88:250–256Google Scholar
  11. Dabas A, Nagpure NS, Kumar R, Kushwaha B, Kumar P, Lakra WS (2012) Assessment of tissue-specific effect of cadmium on antioxidant defense system and lipid peroxidation in freshwater murrel, Channa punctatus. Fish Physiol Biochem 38:469–482Google Scholar
  12. Dalar A, Turker M, Zabaras D, Konczak I (2014) Phenolic composition, antioxidant and enzyme inhibitory activities of Eryngium bornmuelleri leaf. Plant Foods Hum Nutr 69:30–36Google Scholar
  13. Koning AJ (2002) The antioxidant ethoxyquin and its analogues: a review. Int J Food Prop 5:451–461Google Scholar
  14. EFSA (2015) Safety and efficacy of ethoxyquin (6-ethoxy-1,2-dihydro-2,2,4-trimethylquinoline) for all animal species. EFSA J 13:4272Google Scholar
  15. German JB (1999) Food processing and lipid oxidation. Adv Exp Med Biol 459:23–50Google Scholar
  16. Han YZ, Ren TJ, Jiang ZQ, Jiang BQ, Gao J, Koshio S, Komilus CF (2012) Effects of palm oil blended with oxidized fish oil on growth performances, hematology, and several immune parameters in juvenile Japanese sea bass, Lateolabrax japonicas. Fish Physiol Biochem 38:1785–1794Google Scholar
  17. Hernández A, García García B, Jordán MJ, Hernández MD (2014) Natural antioxidants in extruded fish feed: protection at different storage temperatures. Anim Feed Sci Technol 195:112–119Google Scholar
  18. Hong Y, Jiang WD, Kuang SY, Hu K, Tang L, Liu Y, Jiang J, Zhang YA, Zhou XQ, Feng L (2015) Growth, digestive and absorptive capacity and antioxidant status in intestine and hepatopancreas of sub-adult grass carp Ctenopharyngodonidella fed graded levels of dietary threonine. J Anim Sci Biotechnol 6:34Google Scholar
  19. Huang SH, Lin CM, Chiang BH (2008) Protective effects of Angelica sinensis extract on amyloid beta-peptide-induced neurotoxicity. Phytomedicine 15:710–721Google Scholar
  20. Jiang WD, Wu P, Kuang SY, Liu Y, Jiang J, Hu K, Li SH, Tang L, Feng L, Zhou XQ (2011) Myo-inositol prevents copper-induced oxidative damage and changes in antioxidant capacity in various organs and the enterocytes of juvenile Jian carp (Cyprinus carpio var. Jian). Aquat Toxicol 105:543–551Google Scholar
  21. Kaptaner B, Kankaya E, Doğan A, Çelik İ (2014) Histopathology and oxidative stress in the liver of Chalcalburnus tarichi living in lake Van, Turkey. Life Sci J 11:66–77Google Scholar
  22. Kaptaner B, Kankaya E, Ünal G (2009) Effects of 17α-ethynylestradiol on hepatosomatic index, plasma vitellogenin levels and liver glutathione-s-transferase activity in lake van fish (Chalcalburnus tarichi Pallas, 1811). Fresenius Environ Bull 18:2366–2372Google Scholar
  23. Kochhann D, Pavanato MA, Llesuy SF, Correa LM, Konzen Riffel AP, Loro VL, Mesko MF, Flores EM, Dressler VL, Baldisserotto B (2009) Bioaccumulation and oxidative stress parameters in silver catfish (Rhamdia quelen) exposed to different thorium concentrations. Chemosphere 77:384–391Google Scholar
  24. Laohabanjong R, Tantikitti C, Benjakul S, Supamattaya K, Boonyaratpalin M (2009) Lipid oxidation in fish meal stored under different conditions on growth, feed efficiency and hepatopancreatic cells of black tiger shrimp (Penaeus monodon). Aquaculture 286:283–289Google Scholar
  25. Lee HJ, Choi JS, Kim WH, Park SI, Song J (2015) Effect of excess iron on oxidative stress and gluconeogenesis through hepcidin during mitochondrial dysfunction. J Nutr Biochem 26:1414–1423Google Scholar
  26. Li HT, Zhou XQ, Gao P, Li QY, Li HS, Huang R, Wu M (2016a) Inhibition of lipid oxidation in foods and feeds and hydroxyl radical-treated fish erythrocytes: a comparative study of Ginkgo biloba leaves extracts and synthetic antioxidants. Anim Nutr 2:234–241Google Scholar
  27. Li HT, Zhou XQ, Wu M, Deng ML, Wang C, Hou JJ, Mou PJ (2016b) The cytotoxicity and protective effects of Astragalus membranaceus extracts and butylated hydroxyanisole on hydroxyl radical-induced apoptosis in fish erythrocytes. Anim Nutr 2:376–382Google Scholar
  28. Li HT, Feng L, Jiang WD, Liu Y, Jiang J, Li SH, Zhou XQ (2013) Oxidative stress parameters and anti-apoptotic response to hydroxyl radicals in fish erythrocytes: protective effects of glutamine, alanine, citrulline and proline. Aquat Toxicol 126:169–179Google Scholar
  29. Li HT, Su DH, Shang T, Pan WG, Gao P (2008) Antioxidant activity of the essential oils and aqueous extracts obtained from five Chinese herbal medicines. Nat Prod Res Dev 20:974–982Google Scholar
  30. Li XY, Tang L, Hu K, Liu Y, Jiang WD, Jiang J, Wu P, Chen GF, Li SH, Kuang SY, Feng L, Zhou XQ (2014) Effect of dietary lysine on growth, intestinal enzymes activities and antioxidant status of sub-adult grass carp (Ctenopharyngodon idella). Fish Physiol Biochem 40:659–671Google Scholar
  31. Lin YH, Shiau SY (2009) Mutual sparing of dietary requirements for alpha-tocopherol and selenium in grouper, Epinephelus malabaricus. Aquaculture 294:242–245Google Scholar
  32. Lin Y, Zhou XQ (2006) Dietary glutamine supplementation improves structure and function of intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Aquaculture 256:389–394Google Scholar
  33. Ling J, Feng L, Liu Y, Jiang J, Jiang WD, Hu K, Li SH, Zhou XQ (2010) Effects of dietary iron levels on growth, body composition and intestinal enzymes activities of juvenile Jian carp (Cyprinus carpio var. Jian). Aquac Nutr 16:616–624Google Scholar
  34. Liu Y, Feng L, Jiang J, Liu Y, Zhou XQ (2009) Effects of dietary protein levels on the growth performance, digestive capacity and amino acid metabolism of juvenile Jian carp (Cyprinus carpio var. Jian). Aquac Res 40:1073–1082Google Scholar
  35. Liu ZF, Gao XQ, Yu JX, Qian XM, Xue GP, Zhang QY, Liu BL, Hong L (2017) Effects of different salinities on growth performance, survival, digestive enzyme activity, immune response, and muscle fatty acid composition in juvenile American shad (Alosa sapidissima). Fish Physiol Biochem 43:761–773Google Scholar
  36. Lundebye AK, Hove H, Mage A, Bohne VJ, Hamre K (2010) Levels of synthetic antioxidants (ethoxyquin, butylated hydroxytoluene and butylated hydroxyanisole) in fish feed and commercially farmed fish. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 27:1652–1657Google Scholar
  37. Maqsood S, Benjakul S (2010) Comparative studies of four different phenolic compounds on in vitro antioxidative activity and the preventive effect on lipid oxidation of fish oil emulsion and fish mince. Food Chem 119:123–132Google Scholar
  38. March BE (1992) Essential fatty acids in fish physiology. Can J Bhysiol Bharmacol 71:684–689Google Scholar
  39. Marco GJ (1968) A rapid method for evaluation of antioxidants. J Am Oil Chem Soc 45:594–598Google Scholar
  40. Matés JM, Sanchez-Jimenez FM (2000) Role of reactive oxygen species in apoptosis: implications for cancer therapy. Int J Biochem Cell Biol 32:157–170Google Scholar
  41. Morrissey PA, Sheehy PJA, Galvin K, Kerry JP, Buckley DJ (1998) Lipid stability in meat and meat products. Meat Sci 49:S73–S86Google Scholar
  42. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358Google Scholar
  43. Porter NA (1986) Mechanisms for the autoxidation of polyunsaturated lipids. Acc Chem Res 19:262–270Google Scholar
  44. Pratt DA, Tallman KA, Porter NA (2011) Free radical oxidation of polyunsaturated lipids: new mechanistic insights and the development of peroxyl radical clocks. Acc Chem Res 44:458–467Google Scholar
  45. Pretto A, Loro VL, Baldisserotto B, Pavanato MA, Moraes BS, Menezes C, Cattaneo R, Clasen B, Finamor IA, Dressler V (2010) Effects of water cadmium concentrations on bioaccumulation and various oxidative stress parameters in Rhamdia quelen. Arch Environ Contam Toxicol 60:309–318Google Scholar
  46. Reyes J, Hernández ME, Meléndez E, Gómez-Lojero C (1995) Inhibitory effect of the antioxidant ethoxyquin on electron transport in the mitochondrial respiratory chain. Biochem Pharmacol 49:283–289Google Scholar
  47. Rosen F, Roberts NR, Nichol CA (1959) Glucocorticosteroids and transaminase activity. I. increased activity of glutamic-pyruvic transaminase in four conditions associated with gluconeogenesis. J Bio Chem 234:476–480Google Scholar
  48. Sakihama Y, Cohen MF, Grace SC, Yamasaki H (2002) Plant phenolic antioxidant and prooxidant activities: phenolics induced oxidative damage mediated by metals in plants. Toxicology 177:67–80Google Scholar
  49. Saxena TB, Zachariassen KE, Jørgensen L (2000) Effects of ethoxyquin on the blood composition of turbot, Scophthalmus maximus L. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 127:1–9Google Scholar
  50. Sharma S, Vig AP (2014) Preliminary phytochemical screening and in vitro antioxidant activities of Parkinsonia aculeata Linn. Biomed Res Int 2014:1–8Google Scholar
  51. Shiau SY, Su SL (2005) Juvenile tilapia (Oreochromis niloticus × Oreochromis aureus) requires dietary myo-inositol for maximal growth. Aquaculture 243:273–277Google Scholar
  52. Shoveller AK, Stoll B, Ball RO, Burrin DG (2005) Nutritional and functional importance of intestinal sulfur amino acid metabolism. J Nutr 135:1609–1612Google Scholar
  53. Skaare JU, Henriksen T (1975) Free radical formation in the antioxidant ethoxyquin. J Sci Food Agric 26:1647–1654Google Scholar
  54. Suzuki A, Yamamoto M, Jokura H, Fujii A, Tokimitsu I, Hase T, Saito I (2007) Ferulic acid restores endothelium-dependent vasodilation in aortas of spontaneously hypertensive rats. Am J Hypertens 20:508–513Google Scholar
  55. Tang JF, Wu ZH, Jian JC, Lu YS, Tang YP (2009) Effects of Chinese herbal compound on growth and muscle composition in Tilapia. Siliao Gongye 30:19–21Google Scholar
  56. Vermerris W, Nicholson R (2006) Phenolic compound biochemistry Springer Families of phenolic compounds and means of classification: 1–34Google Scholar
  57. Wang J, Ai QH, Mai KS, Xu HG, Zuo RT, Xu W, Zhang WB, Zhang CX (2015) Effects of dietary ethoxyquin on growth, feed utilization and residue in the muscle of juvenile Japanese seabass, Lateolabrax japonicus. Aquac Res 46:2656–2664Google Scholar
  58. Wang J, Ai QH, Mai KS, Xu W, Xu HG, Zhang WB, Wang XJ, Liufu ZG (2010) Effects of dietary ethoxyquin on growth performance and body composition of large yellow croaker Pseudosciaena crocea. Aquaculture 306:80–84Google Scholar
  59. Wang JQ, Qi CX, Cheng AX, Yan YC, Li WK, Yan YL (2008) Effects of dietary Radix astragali, Radix polygoni multiflori and Fructus crataegi on growth and digestibility in juvenile yellow catfish (Pelteobagrus fulvidraco). Chin J Fish 21:34–41Google Scholar
  60. Wu YC, Hsieh CL (2011) Pharmacological effects of Radix Angelica Sinensis (Danggui) on cerebral infarction. Chin Med 6:32Google Scholar
  61. Xin YF, Zhou GL, Shen M, Chen YX, Liu SP, Chen GC, Chen H, You ZQ, Xuan YX (2007) Angelica sinensis: a novel adjunct to prevent doxorubicin-induced chronic cardiotoxicity. Basic Clin Pharmacol Toxicol 101:421–426Google Scholar
  62. Yeh TS, Huang CC, Chuang HL, Hsu MC (2014) Angelica sinensis improves exercise performance and protects against physical fatigue in trained mice. Molecules 19:3926–3939Google Scholar
  63. Yuan YV, Bone DE, Carrington MF (2005) Antioxidant activity of dulse (Palmaria palmata) extract evaluated in vitro. Food Chem 91:485–494Google Scholar
  64. Zhang L (2015) Free radical scavenging properties and anti-fatigue activities of Angelica sinensis polysaccharides. Adv Mater Res 1092-1093:1538–1542Google Scholar
  65. Zheng Q, Han C, Zhong Y, Wen R, Zhong M (2017) Effects of dietary supplementation with green tea waste on growth, digestive enzyme and lipid metabolism of juvenile hybrid tilapia, Oreochromis niloticus × O. aureus. Fish Physiol Biochem 43:361–371Google Scholar
  66. Zhou XQ, Zhao CR, Lin Y (2007) Compare the effect of diet supplementation with uncoated or coated lysine on juvenile Jian carp (Cyprinus carpio Var. Jian). Aquac Nutr 13:457–461Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Key Laboratory of Sichuan Province for Conservation and Utilization of Fishes Resources in the Upper Reaches of the Yangtze RiverNeijiang Normal UniversityNeijiangChina
  2. 2.College of Life ScienceNeijiang Normal UniversityNeijiangChina
  3. 3.Animal Nutrition InstituteSichuan Agricultural UniversityChengduChina

Personalised recommendations