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Dietary Probiotic Bacillus licheniformis H2 Enhanced Growth Performance, Morphology of Small Intestine and Liver, and Antioxidant Capacity of Broiler Chickens Against Clostridium perfringens–Induced Subclinical Necrotic Enteritis

  • Ying Zhao
  • Dong Zeng
  • Hesong Wang
  • Xiaodan Qing
  • Ning Sun
  • Jinge Xin
  • Min Luo
  • Abdul Khalique
  • Kangcheng Pan
  • Gang Shu
  • Bo Jing
  • Xueqin NiEmail author
Article
  • 93 Downloads

Abstract

The reduction in the use of antibiotics in the poultry industry has considerably increased the appearance of Clostridium perfringens (CP)induced subclinical necrotic enteritis (SNE), forcing researchers to search alternatives to antibiotic growth promoters (AGP) like probiotics. This study aimed to investigate the effect and the underlying potential mechanism of dietary supplementation of Bacillus licheniformis H2 to prevent SNE. A total of 180 1-day-old male broiler chickens (Ross 308) were randomly divided into three groups, with six replicates in each group and ten broilers per pen: (a) basal diet in negative control group(NC group); (b) basal diet + SNE infection(coccidiosis vaccine + CP) (SNE group); (c) basal diet + SNE infection + H2 pre-treatment(BL group). Growth performance, morphology of small intestine and liver, and antioxidant capacity of the serum, ileum, and liver were assessed in all three groups. The results showed that H2 significantly suppressed (P < 0.05) the negative effects on growth performance induced by SNE, including loss of body weight gain, decrease of feed intake, and raise of feed conversion ratio among the different treatments at 28 days. The addition of H2 also increased (P < 0.05) the villus height: crypt depth ratio as well as villus height in the ileum. Chicks fed with H2 diet had lower malondialdehyde (MDA) concentration in the ileum in BL group than that in SNE group (P < 0.05). Moreover, compared with other treatment groups, dietary H2 improved the activities of antioxidant enzymes in the ileum, serum, and liver (P < 0.05). H2 may also prevent SNE by significantly increasing the protein content (P < 0.05) of Bcl-2 in the liver. Dietary supplementation of H2 could effectively prevent the appearance of CP-induced SNE and improve the growth performance of broiler chickens damaged by SNE, of which the mechanism may be related to intestinal development, antioxidant capacity, and apoptosis which were improved by H2.

Keywords

Broilers Subclinical necrotic enteritis Bacillus licheniformis H2 Growth performance Antioxidant capacity 

Abbreviations

NE

necrotic enteritis

SNE

subclinical necrotic enteritis

H2

Bacillus licheniformis H2

CP

Clostridium perfringens

AGP

antibiotic growth promoters

BWG

body weight gain

FI

feed intake

FCR

feed conversion ratio

T-AOC

total antioxidation capacity

CAT

activities of catalase

SOD

superoxide dismutase

GSH-Px

glutathione peroxidase

IHR

inhibition of hydroxy radical

MDA

malondialdehyde

Notes

Authors’ Contributions

All authors contributed to the design of the experiments. YZ, XQ, HW, and NS performed the experiments. YZ drafted the manuscript. All authors read and approved the final manuscript.

Funding Information

This study was supported by the International Cooperative Project of Science and Technology Bureau of Sichuan Province (2018HH0103).

Compliance with Ethical Standards

Ethical Approval

All animal experiment procedures were conducted in accordance with the guidelines of the Animal Welfare Act and all procedures and protocols were approved by the Institutional Animal Care and Use Committee of the Sichuan Agricultural University (approval number: SYXKchuan2014-187; approval date: January 29, 2014).

Competing Interest

The authors declare that they have no competing interest.

References

  1. 1.
    Parish WE (1961) Necrotic enteritis in the fowl (Gallus gallus domesticus). I. Histopathology of the disease and isolation of a strain of Clostridium welchii. J Comp Pathol 71:377–393.  https://doi.org/10.1016/S0368-1742(61)80043-X CrossRefPubMedGoogle Scholar
  2. 2.
    Timbermont L, Haesebrouck F, Ducatelle R, Van Immerseel F (2011) Necrotic enteritis in broilers: an updated review on the pathogenesis. Avian Pathol 40(4):341–347.  https://doi.org/10.1080/03079457.2011.590967 CrossRefPubMedGoogle Scholar
  3. 3.
    Prescott JF, Smyth JA, Shojadoost B, Vince A (2016) Experimental reproduction of necrotic enteritis in chickens: a review. Avian Pathol 45(3):317–322.  https://doi.org/10.1080/03079457.2016.1141345 CrossRefPubMedGoogle Scholar
  4. 4.
    Zahoor I, Ghayas A, Basheer A (2018) Genetics and genomics of susceptibility and immune response to necrotic enteritis in chicken: a review. Mol Biol Rep 45(1):31–37.  https://doi.org/10.1007/s11033-017-4138-8 CrossRefPubMedGoogle Scholar
  5. 5.
    Keyburn AL, Yan XX, Bannam TL, Van Immerseel F, Rood JI, Moore RJ (2010) Association between avian necrotic enteritis and Clostridium perfringens strains expressing NetB toxin. Vet Res 41(2):21.  https://doi.org/10.1051/vetres/2009069 CrossRefPubMedGoogle Scholar
  6. 6.
    Johansson A, Aspán A, Kaldhusdal M, Engström BE (2010) Genetic diversity and prevalence of netB in Clostridium perfringens isolated from a broiler flock affected by mild necrotic enteritis. Vet Microbiol 144(1-2):87–92.  https://doi.org/10.1016/j.vetmic.2009.12.017 CrossRefPubMedGoogle Scholar
  7. 7.
    Van Immerseel F, De Buck J, Pasmans F, Huyghebaert G, Haesebrouck F, Ducatelle R (2004) Clostridium perfringens in poultry: an emerging threat for animal and public health. Avian Pathol 33(4):537–549.  https://doi.org/10.1080/03079450400013162 CrossRefPubMedGoogle Scholar
  8. 8.
    Xue GD, Wu SB, Choct M, Swick RA (2017) The role of supplemental glycine in establishing a subclinical necrotic enteritis challenge model in broiler chickens. Anim Nutr 3(3):266–270.  https://doi.org/10.1016/j.aninu.2017.05.004 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Prescott JF, Parreira VR, Mehdizadeh Gohari I, Lepp D, Gong J (2016) The pathogenesis of necrotic enteritis in chickens: what we know and what we need to know: a review. Avian Pathol 45(3):288–294.  https://doi.org/10.1080/03079457.2016.1139688 CrossRefPubMedGoogle Scholar
  10. 10.
    Fasina YO, Newman MM, Stough JM, Liles MR (2016) Effect of Clostridium perfringens infection and antibiotic administration on microbiota in the small intestine of broiler chickens. Poult Sci 95(2):247–260.  https://doi.org/10.3382/ps/pev329 CrossRefPubMedGoogle Scholar
  11. 11.
    Vidanarachchi JK, Mikkelsen LL, Constantinoiu CC, Choct M, Iji PA (2013) Natural plant extracts and prebiotic compounds as alternatives to antibiotics in broiler chicken diets in a necrotic enteritis challenge model. Anim Prod Sci 53(12):1247–1259.  https://doi.org/10.1071/AN12374 CrossRefGoogle Scholar
  12. 12.
    Van Immerseel F, Rood JI, Moore RJ, Titball RW (2009) Rethinking our understanding of the pathogenesis of necrotic enteritis in chickens. Trends Microbiol 17(1):32–36.  https://doi.org/10.1016/j.tim.2008.09.005 CrossRefPubMedGoogle Scholar
  13. 13.
    Shojadoost B, Vince AR, Prescott JF (2012) The successful experimental induction of necrotic enteritis in chickens by Clostridium perfringens: a critical review. Vet Res 43:74–12.  https://doi.org/10.1186/1297-9716-43-74 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Hofacre CL, Smith JA, Mathis GF (2018) An optimist’s view on limiting necrotic enteritis and maintaining broiler gut health and performance in today's marketing, food safety, and regulatory climate. Poult Sci 97(6):1929–1933.  https://doi.org/10.3382/ps/pey082 CrossRefPubMedGoogle Scholar
  15. 15.
    Rodrigues I, Svihus B, Bedford MR, Gous R, Choct M (2018) Intermittent lighting improves resilience of broilers during the peak phase of sub-clinical necrotic enteritis infection. Poult Sci 97(2):438–446.  https://doi.org/10.3382/ps/pex315 CrossRefPubMedGoogle Scholar
  16. 16.
    Alagawany M, Abd El-Hack ME, Farag MR, Sachan S, Karthik K, Dhama K (2018) The use of probiotics as eco-friendly alternatives for antibiotics in poultry nutrition. Environ Sci Pollut Res Int 25(11):10611–10618.  https://doi.org/10.1007/s11356-018-1687-x CrossRefPubMedGoogle Scholar
  17. 17.
    Plaza-Diaz J, Gomez-Llorente C, Fontana L, Gil A (2014) Modulation of immunity and inflammatory gene expression in the gut, in inflammatory diseases of the gut and in the liver by probiotics. World J Gastroenterol 20(42):15632–15649.  https://doi.org/10.3748/wjg.v20.i42.15632 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Vieco-Saiz N, Belguesmia Y, Raspoet R, Auclair E, Gancel F, Kempf I, Drider D (2019) Benefits and inputs from Lactic Acid Bacteria and their bacteriocins as alternatives to antibiotic growth promoters during food-animal production. Front Microbiol 10:57.  https://doi.org/10.3389/fmicb.2019.00057 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Patterson JA, Burkholder KM (2003) Application of prebiotics and probiotics in poultry production. Poult Sci 82(4):627–631.  https://doi.org/10.1093/ps/82.4.627 CrossRefPubMedGoogle Scholar
  20. 20.
    Mishra C, Lambert J (1996) Production of anti-microbial substances by probiotics. Asia Pac J Clin Nutr 5(1):20–24PubMedGoogle Scholar
  21. 21.
    Markowiak P, Śliżewska K (2017) Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients 9(9):1021.  https://doi.org/10.3390/nu9091021 CrossRefPubMedCentralGoogle Scholar
  22. 22.
    Sun X, Jia Z (2018) Microbiome modulates intestinal homeostasis against inflammatory diseases. Vet Immunol Immunopathol 205:97–105.  https://doi.org/10.1016/j.vetimm.2018.10.014 CrossRefPubMedGoogle Scholar
  23. 23.
    Caly DL, D'Inca R, Auclair E, Drider D (2015) Alternatives to antibiotics to prevent necrotic enteritis in broiler chickens: a microbiologist’s perspective. Front Microbiol 6:1336.  https://doi.org/10.3389/fmicb.2015.01336 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Bai WK, Zhang FJ, He TJ, Su PW, Ying XZ, Zhang LL, Wang T (2016) Dietary probiotic Bacillus subtilis strain fmbj increases antioxidant capacity and oxidative stability of chicken breast meat during storage. PLoS One 11(12):e0167339.  https://doi.org/10.1371/journal.pone.0167339 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Mishra B, Jha R (2019) Oxidative stress in the poultry gut: potential challenges and interventions. Front Vet Sci 6:60.  https://doi.org/10.3389/fvets.2019.00060 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Li Z, Wang W, Lv Z, Liu D, Guo Y (2017) Bacillus subtilis and yeast cell wall improve the intestinal health of broilers challenged by Clostridium perfringens. Br Poult Sci 58(6):635–643.  https://doi.org/10.1080/00071668.2017.1370697 CrossRefPubMedGoogle Scholar
  27. 27.
    Wang H, Ni X, Qing X, Zeng D, Luo M, Liu L, Li G, Pan K, Jing B (2017) Live probiotic Lactobacillus johnsonii BS15 promotes growth performance and lowers fat deposition by improving lipid metabolism, intestinal development, and gut microflora in broilers. Front Microbiol 8:1073.  https://doi.org/10.3389/fmicb.2017.01073 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Wang H, Ni X, Qing X, Liu L, Lai J, Khalique A, Li G, Pan K, Jing B, Zeng D (2017) Probiotic enhanced intestinal immunity in broilers against subclinical necrotic enteritis. Front Immunol 8:1592.  https://doi.org/10.3389/fimmu.2017.01592 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Qing X, Zeng D, Wang H, Ni X, Lai J, Liu L, Khalique A, Pan K, Jing B (2018) Analysis of hepatic transcriptome demonstrates altered lipid metabolism following Lactobacillus johnsonii BS15 prevention in chickens with subclinical necrotic enteritis. Lipids Health Dis 17(1):93.  https://doi.org/10.1186/s12944-018-0741-5 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Zhou M, Zeng D, Ni X, Tu T, Yin Z, Pan K, Jing B (2016) Effects of Bacillus licheniformis on the growth performance and expression of lipid metabolism-related genes in broiler chickens challenged with Clostridium perfringens-induced necrotic enteritis[J]. Lipids Health Dis 15:48.  https://doi.org/10.1186/s12944-016-0219-2 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Xu S, Lin Y, Zeng D, Zhou M, Zeng Y, Wang H, Zhou Y, Zhu H, Pan K, Jing B, Ni X (2018) Bacillus licheniformis normalize the ileum microbiota of chickens infected with necrotic enteritis. Sci Rep 8(1):1744.  https://doi.org/10.1038/s41598-018-20059-z CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Lin Y, Xu S, Zeng D, Ni X, Zhou M, Zeng Y, Wang H, Zhou Y, Zhu H, Pan K, Li G (2017) Disruption in the cecal microbiota of chickens challenged with Clostridium perfringens and other factors was alleviated by Bacillus licheniformis supplementation. PLoS One 12(8):e0182426.  https://doi.org/10.1371/journal.pone.0182426 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Smyth JA (2016) Pathology and diagnosis of necrotic enteritis: is it clear-cut? Avian Pathol 45(3):282–287.  https://doi.org/10.1080/03079457.2016.1158780 CrossRefPubMedGoogle Scholar
  34. 34.
    Huang T, Gao B, Chen WL, Xiang R, Yuan MG, Xu ZH, Peng XY (2018) Temporal effects of high fishmeal diet on gut microbiota and immune response in Clostridium perfringens-challenged chickens. Front Microbiol 9:2754.  https://doi.org/10.3389/fmicb.2018.02754 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Løvland A, Kaldhusdal M (1999) Liver lesions seen at slaughter as an indicator of necrotic enteritis in broiler flocks. FEMS Immunol Med Microbiol 24(3):345–351.  https://doi.org/10.1111/j.1574-695X.1999.tb01304.x CrossRefPubMedGoogle Scholar
  36. 36.
    Awad WA, Ghareeb K, Abdel-Raheem S, Böhm J (2009) Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult Sci 88(1):49–56.  https://doi.org/10.3382/ps.2008-00244 CrossRefPubMedGoogle Scholar
  37. 37.
    Musa BB, Duan Y, Khawar H, Sun Q, Ren Z, Elsiddig Mohamed MA, Abbasi IHR, Yang X (2019) Bacillus subtilis B21 and Bacillus licheniformis B26 improve intestinal health and performance of broiler chickens with Clostridium perfringens-induced necrotic enteritis. J Anim Physiol Anim Nutr (Berl) 103(4):1039–1049.  https://doi.org/10.1111/jpn.13082 CrossRefGoogle Scholar
  38. 38.
    Gobi N, Vaseeharan B, Chen JC, Rekha R, Vijayakumar S, Anjugam M, Iswarya A (2018) Dietary supplementation of probiotic Bacillus licheniformis Dahb1 improves growth performance, mucus and serum immune parameters, antioxidant enzyme activity as well as resistance against Aeromonas hydrophila in tilapia Oreochromis mossambicus. Fish Shellfish Immunol 74:501–508.  https://doi.org/10.1016/j.fsi.2017.12.066 CrossRefPubMedGoogle Scholar
  39. 39.
    Jia P, Cui K, Ma T, Wan F, Wang W, Yang D, Wang Y, Guo B, Zhao L, Diao Q (2018) Influence of dietary supplementation with Bacillus licheniformis and Saccharomyces cerevisiae as alternatives to monensin on growth performance, antioxidant, immunity, ruminal fermentation and microbial diversity of fattening lambs. Sci Rep 8(1):16712–16710.  https://doi.org/10.1038/s41598-018-35081-4 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Zhou M, Zeng D, Ni X, Tu T, Yin Z, Pan K, Jing B (2016) Effects of Bacillus licheniformis on the growth performance and expression of lipid metabolism-related genes in broiler chickens challenged with Clostridium perfringens-induced necrotic enteritis. Lipids Health Dis 15:48–10.  https://doi.org/10.1186/s12944-016-0219-2 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Mingmongkolchai S, Panbangred W (2018) Bacillus probiotics: an alternative to antibiotics for livestock production. J Appl Microbiol 124(6):1334–1346.  https://doi.org/10.1111/jam.13690 CrossRefPubMedGoogle Scholar
  42. 42.
    Zhang ZF, Kim IH (2014) Effects of multistrain probiotics on growth performance, apparent ileal nutrient digestibility, blood characteristics, cecal microbial shedding, and excreta odor contents in broilers. Poult Sci 93(2):364–370.  https://doi.org/10.3382/ps.2013-03314 CrossRefPubMedGoogle Scholar
  43. 43.
    Jayaraman S, Das PP, Saini PC, Roy B, Chatterjee PN (2017) Use of Bacillus Subtilis PB6 as a potential antibiotic growth promoter replacement in improving performance of broiler birds. Poult Sci 96(8):2614–2622.  https://doi.org/10.3382/ps/pex079 CrossRefPubMedGoogle Scholar
  44. 44.
    Bortoluzzi C, Serpa Vieira B, de Paula Dorigam JC, Menconi A, Sokale A, Doranalli K, Applegate TJ (2009) Bacillus subtilis DSM 32315 supplementation attenuates the effects of Clostridium perfringens challenge on the growth performance and intestinal microbiota of broiler chickens. Microorganisms 7(3):E71.  https://doi.org/10.3390/microorganisms7030071 CrossRefGoogle Scholar
  45. 45.
    Bai K, Huang Q, Zhang J, He J, Zhang L, Wang T (2017) Supplemental effects of probiotic Bacillus subtilis fmbJ on growth performance, antioxidant capacity, and meat quality of broiler chickens. Poult Sci 96(1):74–82.  https://doi.org/10.3382/ps/pew246 CrossRefPubMedGoogle Scholar
  46. 46.
    Mountzouris KC, Tsirtsikos P, Kalamara E, Nitsch S, Schatzmayr G, Fegeros K (2007) Evaluation of the efficacy of a probiotic containing Lactobacillus, Bifidobacterium, Enterococcus, and Pediococcus strains in promoting broiler performance and modulating cecal microflora composition and metabolic activities. Poult Sci 86(2):309–317.  https://doi.org/10.1093/ps/86.2.309 CrossRefPubMedGoogle Scholar
  47. 47.
    Yang CM, Cao GT, Ferket PR, Liu TT, Zhou L, Zhang L, Xiao YP, Chen AG (2012) Effects of probiotic, Clostridium butyricum, on growth performance, immune function, and cecal microflora in broiler chickens. Poult Sci 91(9):2121–2129.  https://doi.org/10.3382/ps.2011-02131 CrossRefPubMedGoogle Scholar
  48. 48.
    Wang X, Farnell YZ, Peebles ED, Kiess AS, Wamsley KG, 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
  49. 49.
    Zhang L, Bai K, Zhang J, Xu W, Huang Q, Wang T (2017) Dietary effects of Bacillus subtilis fmbj on the antioxidant capacity of broilers at an early age. Poult Sci 96(10):3564–3573.  https://doi.org/10.3382/ps/pex172 CrossRefPubMedGoogle Scholar
  50. 50.
    Jayaraman S, Thangavel G, Kurian H, Mani R, Mukkalil R, Chirakkal H (2013) Bacillus subtilis PB6 improves intestinal health of broiler chickens challenged with Clostridium perfringens-induced necrotic enteritis. Poult Sci 92(2):370–374.  https://doi.org/10.3382/ps.2012-02528 CrossRefPubMedGoogle Scholar
  51. 51.
    Salim HM, Kang HK, Akter N, Kim DW, Kim JH, Kim MJ, Na JC, Jong HB, Choi HC, Suh OS, Kim WK (2013) Supplementation of direct-fed microbials as an alternative to antibiotic on growth performance, immune response, cecal microbial population, and ileal morphology of broiler chickens. Poult Sci 92(8):2084–2090.  https://doi.org/10.3382/ps.2012-02947 CrossRefPubMedGoogle Scholar
  52. 52.
    Song J, Xiao K, Ke YL, Jiao LF, Hu CH, Diao QY, Shi B, Zou XT (2014) Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress. Poult Sci 93(3):581–588.  https://doi.org/10.3382/ps.2013-03455 CrossRefPubMedGoogle Scholar
  53. 53.
    Mohammadagheri N, Najafi R, Najafi G (2016) Effects of dietary supplementation of organic acids and phytase on performance and intestinal histomorphology of broilers. Vet Res Forum 7(3):189–195PubMedPubMedCentralGoogle Scholar
  54. 54.
    Shah M, Zaneb H, Masood S, Khan RU, Mobashar M, Khan I, Din S, Khan MS, Rehman HU, Tinelli A (2019) Single or combined applications of zinc and multi-strain probiotic on intestinal histomorphology of broilers under cyclic heat stress. Probiotics Antimicrob Proteins 1–8.  https://doi.org/10.1007/s12602-019-09561-6
  55. 55.
    Bai K, Feng C, Jiang L, Zhang L, Zhang J, Zhang L, Wang T (2018) Dietary effects of Bacillus subtilis fmbj on growth performance, small intestinal morphology, and its antioxidant capacity of broilers. Poult Sci 97(7):2312–2321.  https://doi.org/10.3382/ps/pey116 CrossRefPubMedGoogle Scholar
  56. 56.
    Schieber M, Chandel NS (2014) ROS function in redox signaling and oxidative stress. Curr Biol 24(10):R453–R462.  https://doi.org/10.1016/j.cub.2014.03.034 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Wang Y, Wu Y, Wang Y, Xu H, Mei X, Yu D, Wang Y, Li W (2017) Antioxidant properties of probiotic bacteria. Nutrients 9(5):E521.  https://doi.org/10.3390/nu9050521 CrossRefPubMedGoogle Scholar
  58. 58.
    Zolotukhin PV, Prazdnova EV, Chistyakov VA (2018) Methods to assess the antioxidative properties of probiotics. Probiotics Antimicrob Proteins 10(3):589–599.  https://doi.org/10.1007/s12602-017-9375-6 CrossRefPubMedGoogle Scholar
  59. 59.
    Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24(5):981–990.  https://doi.org/10.1016/j.cellsig.2012.01.008 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Tian T, Wang Z, Zhang J (2017) Pathomechanisms of oxidative stress in inflammatory bowel disease and potential antioxidant therapies. Oxidative Med Cell Longev 2017:4535194.  https://doi.org/10.1155/2017/4535194 CrossRefGoogle Scholar
  61. 61.
    Rezaie A, Parker RD, Abdollahi M (2007) Oxidative stress and pathogenesis of inflammatory bowel disease: an epiphenomenon or the cause? Dig Dis Sci 52(9):2015–2021.  https://doi.org/10.1007/s10620-006-9622-2 CrossRefPubMedGoogle Scholar
  62. 62.
    Piechota-Polanczyk A, Fichna J (2014) Review article: the role of oxidative stress in pathogenesis and treatment of inflammatory bowel diseases. Naunyn Schmiedeberg's Arch Pharmacol 387(7):605–620.  https://doi.org/10.1007/s00210-014-0985-1 CrossRefGoogle Scholar
  63. 63.
    Lovasova E, Skardova I, Sesztakova E, Skarda J (2009) Necrotic enteritis and oxidative stress parameters in chickens. Indian Vet J 86(6):555–557.  https://doi.org/10.1103/PhysRevB.22.1123 CrossRefGoogle Scholar
  64. 64.
    Salami SA, Majoka Mohammed A, Saha S, Garber A (2015) Efficacy of dietary antioxidants on broiler oxidative stress, performance and meat quality: science and market. Avian Biol Res 8(2):65–78.  https://doi.org/10.3184/175815515X14291701859483 CrossRefGoogle Scholar
  65. 65.
    Gupta RK, Patel AK, Shah N, Chaudhary AK, Jha UK, Yadav UC, Gupta PK, Pakuwal U (2014) Oxidative stress and antioxidants in disease and cancer: a review. Asian Pac J Cancer Prev 15(11):4405–4409.  https://doi.org/10.7314/apjcp.2014.15.11.4405 CrossRefGoogle Scholar
  66. 66.
    Mishra V, Shah C, Mokashe N, Chavan R, Yadav H, Prajapati J (2015) Probiotics as potential antioxidants: A systematic review. J Agric Food Chem 63(14):3615–3626.  https://doi.org/10.1021/jf506326t CrossRefPubMedGoogle Scholar
  67. 67.
    Liao X, Wu R, Ma G, Zhao L, Zheng Z, Zhang R (2015) Effects of Clostridium butyricum on antioxidant properties, meat quality and fatty acid composition of broiler birds. Lipids Health Dis 14:36.  https://doi.org/10.1186/s12944-015-0035-0 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Gong L, Wang B, Mei X, Xu H, Qin Y, Li W, Zhou Y (2018) Effects of three probiotic Bacillus on growth performance, digestive enzyme activities, antioxidative capacity, serum immunity, and biochemical parameters in broilers. Anim Sci J 89(11):1561–1571.  https://doi.org/10.1111/asj.13089 CrossRefPubMedGoogle Scholar
  69. 69.
    Kupsco A, Schlenk D (2015) Oxidative stress, unfolded protein response, and apoptosis in developmental toxicity. Int Rev Cell Mol Biol 317:1–66.  https://doi.org/10.1016/bs.ircmb.2015.02.002 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Khailova L, Mount Patrick SK, Arganbright KM, Halpern MD, Kinouchi T, Dvorak B (2010) Bifidobacterium bifidum reduces apoptosis in the intestinal epithelium in necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 299(5):G1118–G1127.  https://doi.org/10.1152/ajpgi.00131.2010 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Paolella G, Mandato C, Pierri L, Poeta M, Di Stasi M, Vajro P (2014) Gut-liver axis and probiotics: their role in non-alcoholic fatty liver disease. World J Gastroenterol 20(42):15518–15531.  https://doi.org/10.3748/wjg.v20.i42.15518 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Wiest R, Albillos A, Trauner M, Bajaj JS, Jalan R (2017) Targeting the gut-liver axis in liver disease. J Hepatol 67(5):1084–1103.  https://doi.org/10.1016/j.jhep.2017.05.007 CrossRefPubMedGoogle Scholar
  73. 73.
    Haque TR, Barritt AS 4th (2016) Intestinal microbiota in liver disease. Best Pract Res Clin Gastroenterol 30(1):133–142.  https://doi.org/10.1016/j.bpg.2016.02.004 CrossRefPubMedGoogle Scholar
  74. 74.
    Konturek PC, Harsch IA, Konturek K, Schink M, Konturek T, Neurath MF, Zopf Y (2018) Gut-liver axis: how do gut bacteria influence the liver? Med Sci (Basel) 6(3):E79.  https://doi.org/10.3390/medsci6030079 CrossRefGoogle Scholar
  75. 75.
    Cramer TA, Kim HW, Chao Y, Wang W, Cheng HW, Kim YHB (2018) Effects of probiotic (Bacillus subtilis) supplementation on meat quality characteristics of breast muscle from broilers exposed to chronic heat stress. Poult Sci 97(9):3358–3368.  https://doi.org/10.3382/ps/pey176 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Animal Microecology Institute, College of VeterinarySichuan Agricultural UniversityChengduChina
  2. 2.Lab of Brain Connectivity, School of Life Science and TechnologyUniversity of Electronic Science and Technology of ChinaChengduChina

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