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
- 93 Downloads
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.
KeywordsBroilers Subclinical necrotic enteritis Bacillus licheniformis H2 Growth performance Antioxidant capacity
subclinical necrotic enteritis
Bacillus licheniformis H2
antibiotic growth promoters
body weight gain
feed conversion ratio
total antioxidation capacity
activities of catalase
inhibition of hydroxy radical
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.
This study was supported by the International Cooperative Project of Science and Technology Bureau of Sichuan Province (2018HH0103).
Compliance with Ethical Standards
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).
The authors declare that they have no competing interest.
- 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
- 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.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
- 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
- 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
- 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.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
- 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
- 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
- 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.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.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.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
- 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
- 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
- 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
- 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.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
- 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
- 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
- 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
- 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