Effect of Bacillus subtilis on the microarchitectural development of the immune system in Salmonella-challenged broiler chickens


Sikandar A, Zaneb H, Nasir A, Rehman A, Kashif M, Shah M, Luqman Z, Din S, Iqbal MF, Khan I, Irshad I (2022): Effect of Bacillus subtilis on the microarchitectural development of the immune system in Salmonella-challenged broiler chickens. Vet Med-Czech 67, 28–37.

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The effect of Bacillus subtilis on the immune responses and morphometry of the immune organs was evaluated in broilers challenged with S. gallinarum.  For this purpose, Salmonella-free birds (n = 240) were split into four groups with six replicates of ten birds each. Groups included an NC (negative control, non-infected + non-medicated), a PC-S (positive control, Salmonella-infected + non-medicated), an AT-S (Salmonella-infected + medicated with enrofloxacin), and a BS-S (Salmonella-infected + B. subtilis (2.0 × 1010 cfu/g; 0.1 g/kg) group. On day 21, the thickness of the thymus cortex and medulla, germinal centre area of the spleen, bursal follicular length and bursal follicular area increased (P < 0.05) in the BS-S when compared to the NC and PC-S groups. On day 35, the BS-S group exhibited a higher (P < 0.05) antibody titre against the Newcastle disease virus (NDV), and cortex of the thymus was thicker (P < 0.05) compared to the other groups. A decrease in the thymus medulla thickness, germinal area of the spleen and bursal follicular number were noted in the PC-S group when compared to the other treatment groups. In conclusion, the prophylactic use of B. subtilis type probiotics alleviated the stress resulting from a Salmonella gallinarum infection and improved the immune organs development and function in infected broilers.

Abudabos AM, Ali MH, Nassan MA, Saleh AA. Ameliorative effect of Bacillus subtilis on growth performance and intestinal architecture in broiler infected with Salmonella. Animals. 2019 Apr 23;9(4):190. https://doi.org/10.3390/ani9040190
Ben Y, Fu C, Hu M, Liu L, Wong MH, Zheng C. Human health risk assessment of antibiotic resistance associated with antibiotic residues in the environment: A review. Environ Res. 2019 Feb;169:483-93. https://doi.org/10.1016/j.envres.2018.11.040
Campbell TW, Ellis CK. Avian and exotic animal hematology and cytology. Hoboken: John Wiley & Sons; 2013. 694 p.
de Oliveira JE, van der Hoeven-Hangoor E, van de Linde IB, Montijn RC, van der Vossen JM. In ovo inoculation of chicken embryos with probiotic bacteria and its effect on posthatch Salmonella susceptibility. Poult Sci. 2014 Apr;93(4):818-29. https://doi.org/10.3382/ps.2013-03409
Dobson A, Cotter PD, Ross RP, Hill C. Bacteriocin production: A probiotic trait? Appl Environ Microbiol. 2012 Jan;78(1):1-6.  https://doi.org/10.1128/AEM.05576-11
Famularo G, Moretti S, Marcellini S, De Simone C. Stimulation of immunity by probiotics. In: Fuller R, editor. Probiotics 2. Applications and practical aspects. Dord-recht: Springer-Science + Business Media, B.V.; 1997. p. 133-61.
Gadde U, Oh ST, Lee YS, Davis E, Zimmerman N, Rehberger T, Lillehoj HS. The effects of direct-fed microbial supplementation, as an alternative to antibiotics, on growth performance, intestinal immune status, and epithelial barrier gene expression in broiler chickens. Probiotics Antimicrob Proteins. 2017 Dec;9(4):397-405. https://doi.org/10.1007/s12602-017-9275-9
Geng T, Guan X, Smith EJ. Screening for genes involved in antibody response to sheep red blood cells in the chicken, Gallus gallus. Poult Sci. 2015 Sep;94(9):2099-107. https://doi.org/10.3382/ps/pev224
Ghanima MMA, Abd El-Hack ME, Othman SI, Taha AE, Allam AA, Eid Abdel-Moneim AM. Impact of different rearing systems on growth, carcass traits, oxidative stress biomarkers, and humoral immunity of broilers exposed to heat stress. Poult Sci. 2020 Jun;99(6):3070-8. https://doi.org/10.1016/j.psj.2020.03.011
Gill HS, Rutherfurd KJ, Cross ML. Dietary probiotic supplementation enhances natural killer cell activity in the elderly: An investigation of age-related immunological changes. J Clin Immunol. 2001 Jul;21(4):264-71.
Guo M, Wu F, Hao G, Qi Q, Li R, Li N, Wei L, Chai T. Bacillus subtilis improves immunity and disease resistance in rabbits. Front Immunol. 2017 Mar 29;8:354. https://doi.org/10.3389/fimmu.2017.00354
Haghighi HR, Gong J, Gyles CL, Hayes MA, Zhou H, Sanei B, Chambers JR, Sharif S. Probiotics stimulate production of natural antibodies in chickens. Clin Vaccine Immunol. 2006 Sep;13(9):975-80. https://doi.org/10.1128/CVI.00161-06
Haley P, Perry R, Ennulat D, Frame S, Johnson C, Lapointe JM, Nyska A, Snyder P, Walker D, Walter G; STP Immunotoxicology Working Group. STP position paper: Best practice guideline for the routine pathology evaluation of the immune system. Toxicol Pathol. 2005;33(3):404-7. https://doi.org/10.1080/01926230590934304
Kabploy K, Bunyapraphatsara N, Morales NP, Paraksa N. Effect of antibiotic growth promoters on anti-oxidative and anti-inflammatory activities in broiler chickens. Thai J Vet Med. 2016;46(1):89-95.
Khalique A, Zeng D, Shoaib M, Wang H, Qing X, Rajput DS, Pan K, Ni X. Probiotics mitigating subclinical necrotic enteritis (SNE) as potential alternatives to antibiotics in poultry. AMB Express. 2020 Mar 14;10(1):50. https://doi.org/10.1186/s13568-020-00989-6
Madej JP, Stefaniak T, Bednarczyk M. Effect of in ovo-delivered prebiotics and synbiotics on lymphoid-organs’ morphology in chickens. Poult Sci. 2015 Jun;94(6):1209-19. https://doi.org/10.3382/ps/pev076
Molnar AK, Podmaniczky B, Kurti P, Tenk I, Glavits R, Virag G, Szabo Z. Effect of different concentrations of Bacillus subtilis on growth performance, carcase quality, gut microflora and immune response of broiler chickens. Br Poult Sci. 2011 Dec;52(6):658-65. https://doi.org/10.1080/00071668.2011.636029
Nair DVT, Anup KJ. Salmonella in poultry meat production. Food safety in poultry meat production. Cham: Springer; 2019. p. 1-24.
Schat KA, Skinner MA. Avian immunosuppressive diseases and immunoevasion. In: Schat KA, Kaspers B, Kaiser P, editors. Avian immunology. Amsterdam: Elsevier/Academic Press; 2014. p. 275-97.
Sikandar A, Zaneb H, Nasir A, Adil M, Ali HM, Muhammad N, Rehman T, Rehman A, Rehman HF. Effects of Bacillus subtilis on performance, immune system and gut in Salmonella-challenged broilers. S Afr J Anim Sci. 2020 Oct 1;50(5):654-62. https://doi.org/10.4314/sajas.v50i5.2
Sikandar A, Zaneb H, Younus M, Masood S, Aslam A, Khattak F, Ashraf S, Yousaf MS, Rehman H. Effect of sodium butyrate on performance, immune status, microarchitecture of small intestinal mucosa and lymphoid organs in broiler chickens. Asian-Australas J Anim Sci. 2017 May;30(5):690-9. https://doi.org/10.5713/ajas.16.0824
Slawinska A, Siwek M, Bednarczyk M. Synbiotics injected in ovo regulate immune-related gene expression signatures in chicken. Am J Vet Res. 2014 Nov;75(11):997-1003.  https://doi.org/10.2460/ajvr.75.11.997
Teo AY, Tan HM. Evaluation of the performance and intestinal gut microflora of broilers fed on corn-soy diets supplemented with Bacillus subtilis PB6 (CloSTAT). J Appl Poult Res. 2007 Oct 1;16(3):296-303. https://doi.org/10.1093/japr/16.3.296
Wagner RD, Johnson SJ. Probiotic bacteria prevent Salmonella – Induced suppression of lymphoproliferation in mice by an immunomodulatory mechanism. BMC Microbiol. 2017 Mar 29;17(1):77. https://doi.org/10.1186/s12866-017-0990-x
Withers DR, Davison TF, Young JR. Diversified bursal medullary B-cells survive and expand independently after depletion following neonatal infectious bursal disease virus infection. Immunology. 2006 Apr;117(4):558-65. https://doi.org/10.1111/j.1365-2567.2006.02332.x
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