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3 Biotech

, 9:291 | Cite as

Zinc-enriched probiotics enhanced growth performance, antioxidant status, immune function, gene expression, and morphological characteristics of Wistar rats raised under high ambient temperature

  • Rahmani Mohammad Malyar
  • Hu Li
  • Hamdard Enayatullah
  • Lili Hou
  • Rawan Ahmad Farid
  • Dandan Liu
  • Javaid Akhter Bhat
  • Jinfeng Miao
  • Fang Gan
  • Kehe Huang
  • Xingxiang ChenEmail author
Original Article

Abstract

The present study was conducted to evaluate the effects of zinc-enriched probiotics (ZnP) on growth performance, antioxidant status, immune function, related gene expression, and morphological characteristics of Wistar rats raised under high heat stress condition during summer. 36, 6-week-old male Wistar rats were randomly divided into three groups; fed with basal diet (control), basal diet with probiotics (P), and basal diet with zinc-enriched probiotics supplementation (ZnP, 100 mg/L), for 40 consecutive days. Blood samples were collected through intracardiac method on the last day of experiment and tissues were collected from liver, heart, and kidneys. The results revealed that both P and ZnP significantly (P < 0.05) enhanced growth performance. However, ZnP remarkably increased glutathione content, glutathione peroxidase, and superoxide dismutase activities but reduced malondialdehyde level in serum of the Wistar rats. The concentration of IL-2, IL-6, and IFN-γ was significantly (P < 0.05) increased with treatments of P and ZnP compared to control group while IL-10 was significantly (P < 0.05) decreased. Additionally, the expression of SOD1, SOD2, MT1, and MT2 genes was significantly (P < 0.05) up-regulated with the treatment of ZnP, but Hsp90 and Hsp70 heat shock genes were significantly (P < 0.05) down-regulated with the treatment of P and ZnP, respectively. Hematoxylin and Eosin staining showed that both P and ZnP supplementation treatments induced changes in villus height and intestinal wall thickness. In conclusion, zinc-enriched probiotics supplementation can improve the growth performance of Wistar rats under high ambient temperature through enhancing antioxidant status, immune function, related genes expression, and intestinal morphological characteristics. This product may serves as a potential nutritive supplement for Wistar rats under high heat stress conditions.

Keywords

Zinc-enriched probiotics Heat stress Antioxidant status Immune function Heat shock protein Wistar rats 

Notes

Authors’ contributions

RMM conceived and designed experiments and wrote the manuscript. GF and HLi designed the structure of this manuscript. JM, XXC, and KH gave some valuable advices about structure of manuscript. RMM, HE, DL, and JKB analyzed the data and revised the manuscript. RAF complied information; RMM and HL performed the experiments. All authors read and approved the final manuscript.

Funding

This project is funded by the National Key R & D Program (2017YFD0501000), National Natural Science Foundation of China (31811530300), MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Project of National Center for International Research on Animal Gut Nutrition and supported by the Priority Academic Program Development of Jiangsu Higher Education Institutions (Jiangsu, China).

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

References

  1. Altan Ö, Pabuçcuoğlu A, Altan A, Konyalioglu S, Bayraktar Ö (2003) Effect of heat stress on oxidative stress, lipid peroxidation and some stress parameters in broilers. Br Poult Sci 44:545–550.  https://doi.org/10.1080/00071660310001618334 CrossRefPubMedGoogle Scholar
  2. Atakisi O, Atakisi E, Kart A (2009) Effects of dietary zinc and l-arginine supplementation on total antioxidants capacity, lipid peroxidation, nitric oxide, egg weight, and blood biochemical values in Japanase quails. Biol Trace Elem Res 132(1–3):136–143CrossRefGoogle Scholar
  3. Babinska I, Rotkiewicz T, Otrocka-Domagala I (2005) The effect of Lactobacillus acidophilus and Bifidobacterium spp. administration on the morphology of the gastrointestinal tract, liver and pancreas in piglets. Polish J Vet Sci 8(1):29–35Google Scholar
  4. Bernabucci U, Lacetera N, Baumgard LH, Rhoads RP, Ronchi B, Nardone A (2010) Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal 4(7):1167–1183.  https://doi.org/10.1017/s175173111000090x CrossRefPubMedGoogle Scholar
  5. Buzadžić B, Korać B, Lazić T, Obradović D (2002) Effect of supplementation with Cu and Zn on antioxidant enzyme activity in the rat tissues. Food Res Int 35(2–3):217–220CrossRefGoogle Scholar
  6. Carlson M, Boren C, Wu C, Huntington C, Bollinger D, Veum T (2004a) Evaluation of various inclusion rates of organic zinc either as polysaccharide or proteinate complex on the growth performance, plasma, and excretion of nursery pigs. J Anim Sci 82(5):1359–1366CrossRefGoogle Scholar
  7. Carlson MS, Boren CA, Wu C, Huntington CE, Bollinger DW, Veum TL (2004b) Evaluation of various inclusion rates of organic zinc either as polysaccharide or proteinate complex on the growth performance, plasma, and excretion of nursery pigs. J Anim Sci 82(5):1359–1366.  https://doi.org/10.2527/2004.8251359x CrossRefPubMedGoogle Scholar
  8. Cho JH, Liu SD, Yun W, Kim KS, Kim IH (2018) Effect of supplemented microencapsulated zinc oxide and organic acids and pure botanicals on growth performance, nutrient digestibility, blood profiles, feces microflora, and zinc level of feces in weanling pigs. Can J Anim Sci 99(1):66–73.  https://doi.org/10.1139/cjas-2017-0114 CrossRefGoogle Scholar
  9. Wood CM, Farrell AP, Brauner CJ (2011) Contents of Homeostasis and Toxicology of Essential Metals, Volume 31A. Fish physiology, vol 31A. Academic Press, pp ix–xiii.  https://doi.org/10.1016/S1546-5098(11)31037-0
  10. Council NR (1995) Nutrient requirements of laboratory animals, 4th edn. The National Academies Press, Washington, DC.  https://doi.org/10.17226/4758 CrossRefGoogle Scholar
  11. De Rensis F, Scaramuzzi RJ (2003) Heat stress and seasonal effects on reproduction in the dairy cow—a review. Theriogenology 60(6):1139–1151CrossRefGoogle Scholar
  12. Dong G, Chen H, Qi M, Dou Y, Wang Q (2014) Balance between metallothionein and metal response element binding transcription factor 1 is mediated by zinc ions. Mol Med Rep 11:1582–1586.  https://doi.org/10.3892/mmr.2014.2969 CrossRefPubMedGoogle Scholar
  13. Flanagan SW, Moseley PL, Buettner GR (1998) Increased flux of free radicals in cells subjected to hyperthermia: detection by electron paramagnetic resonance spin trapping. FEBS Lett 431(2):285–286.  https://doi.org/10.1016/S0014-5793(98)00779-0 CrossRefPubMedGoogle Scholar
  14. Fridovich I (1978) The biology of oxygen radicals. Science 201(4359):875–880.  https://doi.org/10.1126/science.210504 CrossRefPubMedGoogle Scholar
  15. Gan F, Ren F, Chen X, Lv C, Pan C, Ye G, Shi J, Shi X, Zhou H, Shituleni SA (2013) Effects of selenium-enriched probiotics on heat shock protein mRNA levels in piglet under heat stress conditions. J Agric Food Chem 61(10):2385–2391CrossRefGoogle Scholar
  16. Gan F, Chen X, Liao SF, Lv C, Ren F, Ye G, Pan C, Huang D, Shi J, Shi XJ (2014) Selenium-enriched probiotics improve antioxidant status, immune function, and selenoprotein gene expression of piglets raised under high ambient temperature. J Agric Food Chem 62(20):4502–4508CrossRefGoogle Scholar
  17. Gunal M, Yayli G, Kaya O, Karahan N, Sulak O (2006) The effects of antibiotic growth promoter, probiotic or organic acid supplementation on performance, intestinal microflora and tissue of broilers. Int J Poult Sci 5:149–155.  https://doi.org/10.3923/ijps.2006.149.155 CrossRefGoogle Scholar
  18. Hahn JD, Baker DH (1993) Growth and plasma zinc responses of young pigs fed pharmacologic levels of zinc. J Anim Sci 71(11):3020–3024.  https://doi.org/10.2527/1993.71113020x CrossRefPubMedGoogle Scholar
  19. Hall DM, Buettner GR, Matthes RD, Gisolfi CV (1994) Hyperthermia stimulates nitric oxide formation: electron paramagnetic resonance detection of NO-heme in blood. J Appl Physiol (Bethesda, Md: 1985) 77(2):548–553.  https://doi.org/10.1152/jappl.1994.77.2.548 CrossRefGoogle Scholar
  20. Hamid M, Liu D, Abdulrahim Y, Liu Y, Qian G, Khan A, Gan F, Huang K (2017) Amelioration of CCl4-induced liver injury in rats by selenizing Astragalus polysaccharides: role of proinflammatory cytokines, oxidative stress and hepatic stellate cells. Res Vet Sci 114:202–211.  https://doi.org/10.1016/j.rvsc.2017.05.002 CrossRefPubMedGoogle Scholar
  21. Jordan ER (2003) Effects of heat stress on reproduction. J Dairy Sci 86:E104–E114.  https://doi.org/10.3168/jds.S0022-0302(03)74043-0 CrossRefGoogle Scholar
  22. Kadzere C, Murphy M, Silanikove N, Maltz E (2002) Heat stress in lactating dairy cows: a review. Livest Prod Sci 77(1):59–91CrossRefGoogle Scholar
  23. Kambe T, Tsuji T, Hashimoto A, Itsumura N (2015) The physiological, biochemical, and molecular roles of zinc transporters in zinc homeostasis and metabolism. Physiol Rev 95(3):749–784.  https://doi.org/10.1152/physrev.00035.2014 CrossRefPubMedGoogle Scholar
  24. Khan J, Wan Saudi WS, Islam M (2013) Effect of zinc on chronic stress induced small intestinal changes in rats. Int Med J 20:29–33Google Scholar
  25. King L, Osati-Ashtiani F, Fraker PJI (1995a) Depletion of cells of the B lineage in the bone marrow of zinc-deficient mice. Immunology 85(1):69PubMedPubMedCentralGoogle Scholar
  26. King LE, Osati-Ashtiani F, Fraker PJ (1995b) Depletion of cells of the B lineage in the bone marrow of zinc-deficient mice. Immunology 85(1):69–73PubMedPubMedCentralGoogle Scholar
  27. Kirchner H, Rink L (2000) Zinc-altered immune function and cytokine production. J Nutr 130(5):1407S–1411S.  https://doi.org/10.1093/jn/130.5.1407S CrossRefPubMedGoogle Scholar
  28. Krishnan G, Bagath M, Pragna MKVP, Vidya MK, Aleena J, Archana PR, Sejian V, Bhatta R (2017) Mitigation of the heat stress impact in livestock reproduction. Theriogenology 8:8–9.  https://doi.org/10.5772/intechopen.69091 CrossRefGoogle Scholar
  29. Kumar BVS, Kumar A, Kataria M (2011) Effect of heat stress in tropical livestock and different strategies for its amelioration. J Stress Physiol Biochem 7(1):45–54Google Scholar
  30. Lessard M, Dupuis M, Gagnon N, Nadeau E, Matte J, Goulet J, Fairbrother JM (2009) Administration of Pediococcus acidilactici or Saccharomyces cerevisiae boulardii modulates development of porcine mucosal immunity and reduces intestinal bacterial translocation after Escherichia coli challenge. J Anim Sci 87(3):922–934CrossRefGoogle Scholar
  31. Li H-H, Jiang X-R, Wang W-J, Qiao J-Y (2018) Effects of Lactobacillus acidophilus and zinc oxide on the growth performance, jejunal morphology and immune function of weaned piglet following an Escherichia coli K88 challenge. Ital J Anim Sci 17(1):114–120.  https://doi.org/10.1080/1828051X.2017.1344573 CrossRefGoogle Scholar
  32. Lord-Fontaine S, Averill-Bates DA (2002) Heat shock inactivates cellular antioxidant defenses against hydrogen peroxide: protection by glucose. Free Radic Biol Med 32(8):752–765.  https://doi.org/10.1016/S0891-5849(02)00769-4 CrossRefPubMedGoogle Scholar
  33. Ma Y, Zhou G, Li Y, Zhu Y, Yu X, Zhao F, Li H, Xu X, Li C (2018) Intake of fish oil specifically modulates colonic Muc2 expression in middle-aged rats by suppressing the glycosylation process. Mol Nutr Food Res 62(4):8–9.  https://doi.org/10.1002/mnfr.201700661 CrossRefGoogle Scholar
  34. Matur E, Eraslan E (2012) The impact of probiotics on the gastrointestinal physiology. In: New Advances in the Basic and Clinical Gastroenterology. ISBN: 978-953-51-0521-3.  https://doi.org/10.5772/34067 Google Scholar
  35. Musa HH, Wu S, Zhu C, Seri H, Zhu GJ (2009) The potential benefits of probiotics in animal production and health. J Anim Vet Adv 8(2):313–321Google Scholar
  36. Pham-Huy LA, He H, Pham-Huy C (2008) Free radicals, antioxidants in disease and health. Int J Biomed Sci 4(2):89–96PubMedPubMedCentralGoogle Scholar
  37. Poulsen HD (1995) Zinc oxide for weanling piglets. Acta Agric Scand Sect A Anim Sci 45(3):159–167.  https://doi.org/10.1080/09064709509415847 CrossRefGoogle Scholar
  38. Ranaldi G, Caprini V, Sambuy Y, Perozzi G, Murgia C (2009) Intracellular zinc stores protect the intestinal epithelium from Ochratoxin A toxicity. Toxicol Vitro 23(8):1516–1521CrossRefGoogle Scholar
  39. Rao SVR, Prakash B, Raju MVLN, Panda AK, Kumari R, Reddy EPK (2016) Effect of supplementing organic forms of zinc, selenium and chromium on performance, anti-oxidant and immune responses in broiler chicken reared in tropical summer. Biol Trace Elem Res 172:511–520.  https://doi.org/10.1007/s12011-015-0587-x CrossRefPubMedGoogle Scholar
  40. Ren Z, Zhao Z, Wang Y, Huang K (2011a) Preparation of selenium/zinc-enriched probiotics and their effect on blood selenium and zinc concentrations, antioxidant capacities, and intestinal microflora in canine. Biol Trace Elem Res 141(1–3):170–183CrossRefGoogle Scholar
  41. Ren Z, Zhao Z, Wang Y, Huang K (2011b) Preparation of selenium/zinc-enriched probiotics and their effect on blood selenium and zinc concentrations, antioxidant capacities, and intestinal microflora in canine. Biol Trace Elem Res 141(1–3):170–183CrossRefGoogle Scholar
  42. Sahin K, Smith M, Onderci M, Sahin N, Gursu M, Kucuk O (2005) Supplementation of zinc from organic or inorganic source improves performance and antioxidant status of heat-distressed quail. Poult Sci 84(6):882–887CrossRefGoogle Scholar
  43. Stehlik-Tomas V, Gulan Zetić V, Stanzer D, Grba S, Vahčić N (2004) Zinc, copper and manganese enrichment in yeast saccharomyces cerevisiae. Food Technol Biotechnol 42:115–120Google Scholar
  44. Tapiero H, Tew KD (2003) Trace elements in human physiology and pathology: zinc and metallothioneins. Biomed Pharmacother 57(9):386–398CrossRefGoogle Scholar
  45. Thornalley PJ, Vašák M (1985) Possible role for metallothionein in protection against radiation-induced oxidative stress. Kinetics and mechanism of its reaction with superoxide and hydroxyl radicals. Biochem Biophys Acta 827(1):36–44PubMedGoogle Scholar
  46. Tortuero F, Rioperez J, Fernandez E, Luisa Rodriguez M (1995) Response of piglets to oral administration of lactic acid bacteria. J Food Protect 58:1369–1374.  https://doi.org/10.4315/0362-028x-58.12.1369 CrossRefGoogle Scholar
  47. Wang A, Yi X, Yu H, Dong B, Qiao S (2009) Free radical scavenging activity of Lactobacillus fermentum in vitro and its antioxidative effect on growing–finishing pigs. J Appl Microbiol 107(4):1140–1148CrossRefGoogle Scholar
  48. Wang J, Ji H, Wang S, Zhang D, Liu H, Shan D, Wang Y (2012) Lactobacillus plantarum ZLP001: in vitro assessment of antioxidant capacity and effect on growth performance and antioxidant status in weaning piglets. Asian Aust J Anim Sci 25(8):1153CrossRefGoogle Scholar
  49. Wang X, Peebles ED, Morgan TW, Harkess RL, Zhai W (2015) Protein source and nutrient density in the diets of male broilers from 8 to 21 d of age: effects on small intestine morphology. Poult Sci 94(1):61–67.  https://doi.org/10.3382/ps/peu019 CrossRefPubMedGoogle Scholar
  50. Wang X, Farnell YZ, Peebles ED, Kiess AS, Wamsley KGS, Zhai W (2016) Effects of prebiotics, probiotics, and their combination on growth performance, small intestine morphology, and resident Lactobacillus of male broilers. Poult Sci 95(6):1332–1340.  https://doi.org/10.3382/ps/pew030 CrossRefPubMedGoogle Scholar
  51. Wolfenson D, Roth Z, Meidan R (2000) Impaired reproduction in heat-stressed cattle: basic and applied aspects. Anim Reprod Sci 60:535–547CrossRefGoogle Scholar
  52. Xiong W, Bai L, Muhammad R-U-H, Zou M, Sun Y (2012) Molecular cloning, characterization of copper/zinc superoxide dismutase and expression analysis of stress-responsive genes from Eisenia fetida against dietary zinc oxide. Comput Biochem Physiol C Toxicol Pharmacol 155(2):416–422.  https://doi.org/10.1016/j.cbpc.2011.11.004 CrossRefGoogle Scholar
  53. Zhang HJ, Xu L, Drake VJ, Xie L, Oberley LW, Kregel KC (2003) Heat-induced liver injury in old rats is associated with exaggerated oxidative stress and altered transcription factor activation. FASEB J Off Publ Fed Am Soc Exp Biol 17(15):2293–2295.  https://doi.org/10.1096/fj.03-0139fje CrossRefGoogle Scholar
  54. Zhang W, Azevedo MS, Wen K, Gonzalez A, Saif LJ, Li G, Yousef AE, Yuan LJV (2008) Probiotic Lactobacillus acidophilus enhances the immunogenicity of an oral rotavirus vaccine in gnotobiotic pigs. Vaccine 26(29–30):3655–3661CrossRefGoogle Scholar
  55. Zhao C-Y, Tan S-X, Xiao X-Y, Qiu X-S, Pan J-Q, Tang Z-X (2014) Effects of dietary zinc oxide nanoparticles on growth performance and antioxidative status in broilers. Biol Trace Elem Res 160(3):361–367CrossRefGoogle Scholar
  56. Zulkifli I, Abdullah N, Azrin NM, Ho YW (2000) Growth performance and immune response of two commercial broiler strains fed diets containing Lactobacillus cultures and oxytetracycline under heat stress conditions. Br Poult Sci 41(5):593–597CrossRefGoogle Scholar

Copyright information

© King Abdulaziz City for Science and Technology 2019

Authors and Affiliations

  • Rahmani Mohammad Malyar
    • 1
    • 2
  • Hu Li
    • 1
  • Hamdard Enayatullah
    • 4
  • Lili Hou
    • 1
  • Rawan Ahmad Farid
    • 2
  • Dandan Liu
    • 1
  • Javaid Akhter Bhat
    • 3
  • Jinfeng Miao
    • 1
  • Fang Gan
    • 1
  • Kehe Huang
    • 1
  • Xingxiang Chen
    • 1
    Email author
  1. 1.College of Veterinary MedicineNanjing Agricultural UniversityNanjingChina
  2. 2.Faculty of Veterinary ScienceNangarhar UniversityJalalabadAfghanistan
  3. 3.National Centre for Soybean ImprovementNanjing Agricultural UniversityNanjingChina
  4. 4.College of Animal Science and TechnologyAgricultural UniversityNanjingChina

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