Skip to main content

Effects of dietary lipid-coated zinc on the antioxidant defense system in the small intestine and liver of piglets

Abstract

The purpose of the study was to investigate the effects of lipid-coated ZnO (LCZ) and the level of LCZ compared with ordinary zinc oxide (ZnO) on antioxidant defense system in the intestine and liver of piglets. A total of forty piglets (n=8) were fed a diet supplemented with 100 ppm Zn with ZnO (ZnO-1), 2,500 ppm Zn with ZnO (ZnO-2), 100 ppm Zn as LCZ (LCZ-1), 200 ppm Zn as LCZ (LCZ-2), or 400 ppm Zn as LCZ (LCZ-3) for 14-d, respectively. The LCZ-3 group resulted in higher (P<0.05) mRNA expressions and activities of CuZn-superoxide dismutase (SOD), glutathione peroxidase (GPX), catalase (CAT), and glutathione S-transferase (GST) in jejunal mucosa compared with the ZnO-1 and LCZ-1 groups, while no difference was observed in the mRNA level of antioxidant genes between the ZnO-1 and ZnO-2 groups. Within the LCZ groups, the LCZ level linearly and quadratically (P<0.01) increased antioxidant enzymes in the jejunum. The maximum response of jejunal antioxidant enzymes to Zn supplementation was achieved by 400 ppm of LCZ. Hepatic mRNA expression of antioxidant enzymes was unaffected by Zn source and level, while hepatic SOD and GST activities were greater (P<0.05) in the LCZ-3 group than in the ZnO-1 group. No difference was observed in lipid peroxidation of the jejunum and liver and the total antioxidant power of plasma among groups. In conclusion, a supplementation with 400 ppm of LCZ resulted in a maximum increase in antioxidant enzymes, indicating that LCZ may affect antioxidant defense system more profoundly than ZnO.

References

  1. Prasad AS. Zinc: an antioxidant and anti-inflammatory agent: role of zinc in degenerative disorders of aging. J Trace Elem Med Biol 2014; 28(4): 364–371.

    Article  CAS  Google Scholar 

  2. Wang MQ, Tao WJ, Ye SS, Du YJ, Wang C, Shen SX. Effects of dietary pharmacological zinc on growth, liver metallothionein, Cu, Zn-SOD concentration and serum parameters in piglets. J Anim Vet Adv 2012; 11(9): 1390–1394.

    Article  Google Scholar 

  3. Prasad AS, Kucuk O. Zinc in cancer prevention. Cancer Metastasis Rev 2002; 21(3-4): 291–295.

    Article  CAS  Google Scholar 

  4. Sahin K, Sahin N, Kucuk O, Hayirli A, Prasad AS. Role of dietary zinc in heat-stressed poultry: a review. Poult Sci 2009; 88(10): 2176–2183.

    Article  CAS  Google Scholar 

  5. Tupe RS, Tupe SG, Tarwadi KV, Agte VV. Effect of different dietary zinc levels on hepatic antioxidant and micronutrients indices under oxidative stress conditions. Metabolism 2010; 59(11): 1603–1611.

    Article  CAS  Google Scholar 

  6. Bun SD, Guo YM, Guo FC, Ji FJ, Cao H. Influence of organic zinc supplementation on the antioxidant status and immune responses of broilers challenged with Eimeria tenella. Poult Sci 2011; 90(6): 1220–1226.

    Article  CAS  Google Scholar 

  7. Barman S, Srinivasan K. Attenuation of oxidative stress and cardioprotective effects of zinc supplementation in experimental diabetic rats. Br J Nutr 2017; 117(3): 335–350.

    Article  CAS  Google Scholar 

  8. Oteiza PL, Olin KL, Fraga CG, Keen CL. Oxidant defense systems in testes from zinc-deficient rats. Proc Soc Exp Biol Med 1996; 213(1): 85–91.

    Article  CAS  Google Scholar 

  9. Jemai H, Messaoudi I, Chaouch A, Kerkeni A. Protective effect of zinc supplementation on blood antioxidant defense system in rats exposed to cadmium. J Trace Elem Med Biol 2007; 21(4): 269–273.

    Article  CAS  Google Scholar 

  10. Katouli M, Melin L, Jensen-Waern M, Wallgren P, Möllby R. The effect of zinc oxide supplementation on the stability of the intestinal flora with special reference to composition of coliforms in weaned pigs. J Appl Microbiol 1999; 87(4): 564–573.

    Article  CAS  Google Scholar 

  11. Hill GM, Mahan DC, Carter SD, Cromwell GL, Ewan RC, Harrold RL, Lewis AJ, Miller PS, Shurson GC, Veum TL. Effect of pharmacological concentrations of zinc oxide with or without the inclusion of an antibacterial agent on nursery pig performance. J Anim Sci 2001; 79: 934–941.

    Article  CAS  Google Scholar 

  12. Hedemann MS, Jensen BB, Poulsen HD. Influence of dietary zinc and copper on digestive enzyme activity and intestinal morphology in weaned pigs. J Anim Sci 2006; 84(12): 3310–3320.

    Article  CAS  Google Scholar 

  13. Zhou X, Li Y, Li Z, Cao Y, Wang F, Li C. Effect of dietary zinc on morphological characteristics and apoptosis related gene expression in the small intestine of Bama miniature pigs. Acta Histochem 2017; 119(3): 235–243.

    Article  CAS  Google Scholar 

  14. Pluske JR, Pethick DW, Hopwood DE, Hampson DJ. Nutritional influences on some major enteric bacterial diseases of pig. Nutr Res Rev 2002; 15(2): 333–371.

    Article  CAS  Google Scholar 

  15. Hill GM. Minerals and mineral utilization in swine. In: Sustainable Swine Nutrition (Chiba LI, ed), John Wiley & Sons, Inc., Oxford, 2013; pp 173–195.

    Google Scholar 

  16. Pekas JC. Zinc 65 metabolism: gastrointestinal secretion by the pig. Am J Physiol 1996; 211(2): 407–413.

    Article  Google Scholar 

  17. Jang I, Kwon CH, Ha DM, Jung DY, Kang SY, Park MJ, Han JH, Park BC, Lee CY. Effects of a lipid-encapsulated zinc oxide supplement on growth performance and intestinal morphology and digestive enzyme activities in weanling pigs. J Anim Sci Technol 2014; 56: 29.

    Article  Google Scholar 

  18. Kwon CH, Lee CY, Han SY, Kim SJ, Park BC, Jang I, Han JH. Effects of dietary supplementation of lipid-encapsulated zinc oxide on colibacillosis, growth and intestinal morphology in weaned piglets challenged with enterotoxigenic Escherichia coli. Anim Sci J 2014; 85(8): 805–813.

    Article  CAS  Google Scholar 

  19. Park BC, Jung DY, Kang SY, Ko YH, Ha DM, Kwon CH, Park MJ, Han JH, Jang I, Lee CY. Effects of dietary supplementation of a zinc oxide product encapsulated with lipid on growth performance, intestinal morphology, and digestive enzyme activities in weanling pigs. Anim Feed Sci Technol 2015; 200: 112–117.

    Article  CAS  Google Scholar 

  20. Song YM, Kim MH, Kim HN, Jang I, Han JH, Fontamillas GA, Lee CY, Park BC. Effects of dietary supplementation of lipid-coated zinc oxide on intestinal mucosal morphology and expression of the genes associated with growth and immune function in weanling pigs. Asian-Australas J Anim Sci 2018; 31(3): 403–409.

    Article  CAS  Google Scholar 

  21. Grüngreiff K, Reinhold D, Wedemeyer H. The role of zinc in liver cirrhosis. Ann Hepatol 2016; 15(1): 7–16.

    Article  Google Scholar 

  22. Xia T, Lai W, Han M, Han M, Ma X, Zhang L. Dietary ZnO nanoparticles alters intestinal microbiota and inflammation response in weaned piglets. Oncotarget 2017; 8(39): 64878–64891.

    Article  Google Scholar 

  23. Xu Z, Squires EJ, Bray TM. Effects of dietary zinc deficiency on the hepatic microsomal cytochrome P450 2B in rats. Can J Physiol Pharmacol 1994; 72(3): 211–216.

    Article  CAS  Google Scholar 

  24. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 2001; 25(4): 402–408.

    Article  CAS  Google Scholar 

  25. Kupfer D, Levin E. Monooxygenase drug metabolizing activity in CaCl2-aggregated hepatic microsomes from rat liver. Biochem Biophys Res Commun 1972; 47(3): 611–618.

    Article  CAS  Google Scholar 

  26. Tappel AL. Glutathione peroxidase and hydroperoxides. Methods Enzymol 1978; 52: 506–513.

    Article  CAS  Google Scholar 

  27. Habig WH, Pabst MJ, Jakoby WB. Glutathione S-transferase: The first enzymatic step in mercapturic acid formation. J Biol Chem 1974; 249(22): 7130–7139.

    CAS  Google Scholar 

  28. Melega S, Canistro D, De Nicola GR, Lazzeri L, Sapone A, Paolini M. Protective effect of Tuscan black cabbage sprout extract against serum lipid increase and perturbations of liver antioxidant and detoxifying enzymes in rats fed a high-fat diet. Br J Nutr 2013; 110(6): 988–997.

    Article  CAS  Google Scholar 

  29. Bidlack WR, Tappel AL. Damage to microsomal membrane by lipid peroxidation. Lipids 1973; 8(4): 177–182.

    Article  CAS  Google Scholar 

  30. Song Y, Leonard SW, Traber MG, Ho E. Zinc deficiency affects DNA damage, oxidative stress, antioxidant defenses, and DNA repair in rats. J Nutr 2009; 139(9): 1626–1631.

    Article  CAS  Google Scholar 

  31. She Y, Huang Q, Li D, Piao X. Effects of proteinate complex zinc on growth performance, hepatic and splenic trace elements concentrations, antioxidative function and immune functions in weaned piglets. Asian-Australas J Anim Sci 2017; 30(8): 1160–1167.

    Article  CAS  Google Scholar 

  32. Nijhoff WA, Peters WH. Induction of rat hepatic and intestinal glutathione S-transferases by dietary butyrated hydroxyanisole. Biochem Pharmacol 1992; 44(3): 596–600.

    Article  CAS  Google Scholar 

  33. de Waziers I, Boisset M, Atteba S. Pre- and postweaning development of drug-metabolizing enzyme activities in small intestine and liver of rats. Drug Metab Dispos 1988; 16(2): 310–315.

    PubMed  Google Scholar 

  34. Yang W, Chen Y, Cheng Y, Wen C, Zhou Y. Effects of zinc bearing palygorskite supplementation on the growth performance, hepatic mineral content, and antioxidant status of broilers at early age. Asian-Australas J Anim Sci 2017; 30(7): 1006–1012.

    Article  CAS  Google Scholar 

  35. Uddin MG, Hossain MS, Rahman MA, Uddin AHMM, Bhuiyan MS. Elemental zinc is inversely associated with C-reactive protein and oxidative stress in chronic liver disease. Biol Trace Elem Res 2017; 178(2): 189–193.

    Article  CAS  Google Scholar 

  36. Fridovich I. Superoxide dismutase. Enzymology 1974; 41: 36–40.

    Google Scholar 

  37. Matés JM. Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology 2000; 153(1-3): 83–104.

    Article  Google Scholar 

  38. Miroñczuk-Chodakowska I, Witkowska AM, Zujko ME. Endogenous non-enzymatic antioxidants in the human body. Adv Med Sci 2018; 63(1): 68–78.

    Article  Google Scholar 

  39. Ruttkay-Nedecky B, Nejdl L, Gumulec J, Zitka O, Masarik M, Eckschlager T, Stiborova M, Adam V, Kizek R. The role of metallothionein in oxidative stress. Int J Mol Sci 2013; 14(3): 6044–6066.

    Article  CAS  Google Scholar 

  40. Tang ZG, Chen GY, Li LF, Wen C, Wang T, Zhou YM. Effect of zinc-bearing zeolite clinoptilolite on growth performance, zinc accumulation, and gene expression of zinc transporters in broilers. J Anim Sci 2015; 93(2): 620–626.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to In-Surk Jang.

Rights and permissions

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://doi.org/creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, HN., Jeon, DG., Lee, C.Y. et al. Effects of dietary lipid-coated zinc on the antioxidant defense system in the small intestine and liver of piglets. Lab Anim Res 34, 65–74 (2018). https://doi.org/10.5625/lar.2018.34.2.65

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.5625/lar.2018.34.2.65

Keywords