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Microencapsulate Probiotics (MP) Promote Growth Performance and Inhibit Inflammatory Response in Broilers Challenged with Salmonella typhimurium

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Abstract

Antibiotic-resistant bacteria are prevalent in husbandry around the world due to the abuse of antibiotic growth promoters (AGPs); therefore, it is necessary to find alternatives to AGPs in animal feed. Among all the candidates, probiotics are promising alternatives to AGPs against Salmonella infection. The anti-Salmonella effects of three probiotic strains, namely, Lactobacillus crispatus 7–4, Lactobacillus johnsonii 3–1, and Pediococcus acidilactici 20–1, have been demonstrated in our previous study. In this study, we further obtained the alginate beads containing compound probiotics, namely, microencapsulate probiotics (MP), and evaluated its regulatory effect on the health of broilers. We incubated free and microencapsulate probiotics in simulated gastric and intestinal juice for 2 h, and the results showed that compared to free probiotics, encapsulation increased tolerance of compound probiotics in the simulated gastrointestinal condition. We observed that the application of probiotics, especially MP, conferred protective effects against Salmonella typhimurium (S.Tm) infection in broilers. Compared to the S.Tm group, the MP could promote the growth performance (p < 0.05) and reduce the S.Tm load in intestine and liver (p < 0.05). In detail, MP pretreatment could modulate the cecal microflora and upregulate the relative abundance of Lactobacillus and Enterobacteriaceae. Besides, MP could reduce the inflammation injury of the intestine and liver, reduce the pro-inflammatory cytokines (IL-6, TNF-α, IL-1β) expression, and induce of anti-inflammatory cytokine (IL-10) expression. Furthermore, MP could inhibit NLRP3 pathway in ileum, thereby attenuating S.Tm-induced inflammation. In conclusion, MP could be a new feeding supplementation strategy to substitute AGPs in poultry feeding.

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Data Availability

All data generated or analyzed during this study are included in this published article.

Abbreviations

ADG:

Average daily gain

ADFI:

Average daily feed intake

AGPs:

Antibiotic growth promoters

ALT:

Alanine aminotransferase

AST:

Aspartate aminotransferase

CFU:

Colony forming units

CP:

Compound probiotics

FCR:

Feed conversion ratio

MP:

Microencapsulate probiotics

SEM:

Scanning electron microscopy

S.Tm :

Salmonella typhimurium

References

  1. Ferrari RG, Rosario DKA, Cunha-Neto A, Mano SB, Figueiredo EES, Conte-Junior CA (2019) Worldwide epidemiology of Salmonella serovars in animal-based foods: a meta-analysis. Appl Environ Microbiol. https://doi.org/10.1128/aem.00591-19

    Article  PubMed  PubMed Central  Google Scholar 

  2. Grassl GA, Valdez Y, Bergstrom KS, Vallance BA, Finlay BB (2008) Chronic enteric salmonella infection in mice leads to severe and persistent intestinal fibrosis. Gastroenterology 134(3):768–780. https://doi.org/10.1053/j.gastro.2007.12.043

    Article  CAS  PubMed  Google Scholar 

  3. Wang WW, Jia HJ, Zhang HJ, Wang J, Lv HY, Wu SG, Qi GH (2019) Supplemental plant extracts from Flos lonicerae in combination with Baikal skullcap attenuate intestinal disruption and modulate gut microbiota in laying hens challenged by Salmonella pullorum. Front Microbiol 10:1681. https://doi.org/10.3389/fmicb.2019.01681

    Article  PubMed  PubMed Central  Google Scholar 

  4. Gut AM, Vasiljevic T, Yeager T, Donkor ON (2018) Salmonella infection - prevention and treatment by antibiotics and probiotic yeasts: a review. Microbiology (Reading) 164(11):1327–1344. https://doi.org/10.1099/mic.0.000709

    Article  CAS  PubMed  Google Scholar 

  5. He T, Long S, Mahfuz S, Wu D, Wang X, Wei X, Piao X (2019) Effects of Probiotics as antibiotics substitutes on growth performance, serum biochemical parameters, intestinal morphology, and barrier function of broilers. Animals (Basel). https://doi.org/10.3390/ani9110985

    Article  PubMed  PubMed Central  Google Scholar 

  6. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506–514. https://doi.org/10.1038/nrgastro.2014.66

    Article  PubMed  Google Scholar 

  7. Fuller R (1992) Probiotics: The scientific basis. Springer Dordrecht. https://doi.org/10.1007/978-94-011-2364-8

  8. Wang L, Zhang H, Rehman MU, Mehmood K, Jiang X, Iqbal M, Tong X, Gao X, Li J (2018) Antibacterial activity of Lactobacillus plantarum isolated from Tibetan yaks. Microb Pathog 115:293–298. https://doi.org/10.1016/j.micpath.2017.12.077

    Article  PubMed  Google Scholar 

  9. Xu X, Peng Q, Zhang Y, Tian D, Zhang P, Huang Y, Ma L, Dia VP, Qiao Y, Shi B (2020) Antibacterial potential of a novel Lactobacillus casei strain isolated from Chinese northeast sauerkraut and the antibiofilm activity of its exopolysaccharides. Food Funct 11(5):4697–4706. https://doi.org/10.1039/d0fo00905a

    Article  CAS  PubMed  Google Scholar 

  10. Pagnini C, Saeed R, Bamias G, Arseneau KO, Pizarro TT, Cominelli F (2010) Probiotics promote gut health through stimulation of epithelial innate immunity. Proc Natl Acad Sci U S A 107(1):454–459. https://doi.org/10.1073/pnas.0910307107

    Article  PubMed  Google Scholar 

  11. Castanon JI (2007) History of the use of antibiotic as growth promoters in European poultry feeds. Poult Sci 86(11):2466–2471. https://doi.org/10.3382/ps.2007-00249

    Article  CAS  PubMed  Google Scholar 

  12. Cox LA Jr, Ricci PF (2008) Causal regulations vs. political will: why human zoonotic infections increase despite precautionary bans on animal antibiotics. Environ Int 34(4):459–475. https://doi.org/10.1016/j.envint.2007.10.010

    Article  PubMed  Google Scholar 

  13. Timmerman HM, Koning CJ, Mulder L, Rombouts FM, Beynen AC (2004) Monostrain, multistrain and multispecies probiotics–a comparison of functionality and efficacy. Int J Food Microbiol 96(3):219–233. https://doi.org/10.1016/j.ijfoodmicro.2004.05.012

    Article  CAS  PubMed  Google Scholar 

  14. Homayouni A, Azizi A, Ehsani MR, Yarmand MS, Razavi SH (2008) Effect of microencapsulation and resistant starch on the probiotic survival and sensory properties of synbiotic ice cream. Food Chem 111(1):50–55. https://doi.org/10.1016/j.foodchem.2008.03.036

    Article  CAS  Google Scholar 

  15. Wang M, Wang C, Gao F, Guo M (2018) Effects of polymerised whey protein-based microencapsulation on survivability of Lactobacillus acidophilus LA-5 and physiochemical properties of yoghurt. J Microencapsul 35(5):504–512. https://doi.org/10.1080/02652048.2018.1538266

    Article  CAS  PubMed  Google Scholar 

  16. Bilenler T, Karabulut I, Candogan K (2017) Effects of encapsulated starter cultures on microbial and physicochemical properties of traditionally produced and heat treated sausages (sucuks). LWT 75:425–433. https://doi.org/10.1016/j.lwt.2016.09.003

    Article  CAS  Google Scholar 

  17. Qin X-S, Gao Q-Y, Luo Z-G (2021) Enhancing the storage and gastrointestinal passage viability of probiotic powder (Lactobacillus plantarum) through encapsulation with pickering high internal phase emulsions stabilized with WPI-EGCG covalent conjugate nanoparticles. Food Hydrocoll 116:106658. https://doi.org/10.1016/j.foodhyd.2021.106658

    Article  CAS  Google Scholar 

  18. Yeung TW, Üçok EF, Tiani KA, McClements DJ, Sela DA (2016) Microencapsulation in alginate and chitosan microgels to enhance viability of Bifidobacterium longum for oral delivery. Front Microbiol 7:494. https://doi.org/10.3389/fmicb.2016.00494

    Article  PubMed  PubMed Central  Google Scholar 

  19. Sun J, Tan H (2013) Alginate-based biomaterials for regenerative medicine applications. Materials (Basel) 6(4):1285–1309. https://doi.org/10.3390/ma6041285

    Article  CAS  PubMed  Google Scholar 

  20. Dhamecha D, Movsas R, Sano U, Menon JU (2019) Applications of alginate microspheres in therapeutics delivery and cell culture: past, present and future. Int J Pharm 569:118627. https://doi.org/10.1016/j.ijpharm.2019.118627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ding C, Wu H, Cao X, Ma X, Gao X, Gao Z, Liu S, Fan W, Liu B, Song S (2021) Lactobacillus johnsonii 3–1 and Lactobacillus crispatus 7–4 promote the growth performance and ileum development and participate in lipid metabolism of broilers. Food Funct 12(24):12535–12549. https://doi.org/10.1039/d1fo03209g

    Article  CAS  PubMed  Google Scholar 

  22. Song H, Yu W, Gao M, Liu X, Ma X (2013) Microencapsulated probiotics using emulsification technique coupled with internal or external gelation process. Carbohydr Polym 96(1):181–189. https://doi.org/10.1016/j.carbpol.2013.03.068

    Article  CAS  PubMed  Google Scholar 

  23. Taub N, Nairz M, Hilber D, Hess MW, Weiss G, Huber LA (2012) The late endosomal adaptor p14 is a macrophage host-defense factor against Salmonella infection. J Cell Sci 125(Pt 11):2698–2708. https://doi.org/10.1242/jcs.100073

    Article  CAS  PubMed  Google Scholar 

  24. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR (2007) Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 104(34):13780–13785. https://doi.org/10.1073/pnas.0706625104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Metzler-Zebeli BU, Hooda S, Pieper R, Zijlstra RT, van Kessel AG, Mosenthin R, Gänzle MG (2010) Nonstarch polysaccharides modulate bacterial microbiota, pathways for butyrate production, and abundance of pathogenic Escherichia coli in the pig gastrointestinal tract. Appl Environ Microbiol 76(11):3692–3701. https://doi.org/10.1128/aem.00257-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Takahashi H, Saito R, Miya S, Tanaka Y, Miyamura N, Kuda T, Kimura B (2017) Development of quantitative real-time PCR for detection and enumeration of Enterobacteriaceae. Int J Food Microbiol 246:92–97. https://doi.org/10.1016/j.ijfoodmicro.2016.12.015

    Article  CAS  PubMed  Google Scholar 

  27. Penders J, Vink C, Driessen C, London N, Thijs C, Stobberingh EE (2005) Quantification of Bifidobacterium spp., Escherichia coli and Clostridium difficile in faecal samples of breast-fed and formula-fed infants by real-time PCR. FEMS Microbiol Lett 243(1):141–147. https://doi.org/10.1016/j.femsle.2004.11.052

    Article  CAS  PubMed  Google Scholar 

  28. Matsuki T, Watanabe K, Fujimoto J, Miyamoto Y, Takada T, Matsumoto K, Oyaizu H, Tanaka R (2002) Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol 68(11):5445–5451. https://doi.org/10.1128/aem.68.11.5445-5451.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  30. Organization WH (2016) Interventions for the control of non-typhoidal Salmonella spp. in beef and pork. Microbiol Risk Assess Ser (30). https://www.who.int/publications/i/item/9789241565240

  31. Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Teillant A, Laxminarayan R (2015) Global trends in antimicrobial use in food animals. Proc Natl Acad Sci U S A 112(18):5649–5654. https://doi.org/10.1073/pnas.1503141112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Barton MD (2001) Antibiotic use in animal feed and its impact on human health. Nutr Res Rev 13(2):279–299. https://doi.org/10.1079/095442200108729106

  33. Union E (2006) Ban on antibiotics as growth promoters in animal feed enters into effect. Brussels. https://ec.europa.eu/commission/presscorner/detail/en/IP_05_1687

  34. Reuben RC, Sarkar SL, Ibnat H, Roy PC, Jahid IK (2022) Novel mono- and multi-strain probiotics supplementation modulates growth, intestinal microflora composition and haemato-biochemical parameters in broiler chickens. Vet Med Sci 8(2):668–680. https://doi.org/10.1002/vms3.709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Reuben RC, Sarkar SL, Ibnat H, Setu MAA, Roy PC, Jahid IK (2021) Novel multi-strain probiotics reduces Pasteurella multocida induced fowl cholera mortality in broilers. Sci Rep 11(1):8885. https://doi.org/10.1038/s41598-021-88299-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Motalebi Moghanjougi Z, Rezazadeh Bari M, Alizadeh Khaledabad M, Amiri S, Almasi H (2021) Microencapsulation of Lactobacillus acidophilus LA-5 and Bifidobacterium animalis BB-12 in pectin and sodium alginate: a comparative study on viability, stability, and structure. Food Sci Nutr 9(9):5103–5111. https://doi.org/10.1002/fsn3.2470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Zhang H, Yang C, Zhou W, Luan Q, Li W, Deng Q, Dong X, Tang H, Huang F (2018) A pH-responsive gel macrosphere based on sodium alginate and cellulose nanofiber for potential intestinal delivery of probiotics. ACS Sustain Chem Eng 6(11):13924–13931. https://doi.org/10.1021/acssuschemeng.8b02237

    Article  CAS  Google Scholar 

  38. Lee KY, Heo TR (2000) Survival of Bifidobacterium longum immobilized in calcium alginate beads in simulated gastric juices and bile salt solution. Appl Environ Microbiol 66(2):869–873. https://doi.org/10.1128/aem.66.2.869-873.2000

    Article  CAS  PubMed Central  Google Scholar 

  39. Pickard JM, Zeng MY, Caruso R, Núñez G (2017) Gut microbiota: role in pathogen colonization, immune responses, and inflammatory disease. Immunol Rev 279(1):70–89. https://doi.org/10.1111/imr.12567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Pei L, Liu J, Huang Z, Iqbal M, Shen Y (2021) Effects of lactic acid bacteria isolated from equine on Salmonella-infected gut mouse model. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-021-09841-0

    Article  PubMed  Google Scholar 

  41. Papizadeh M, Rohani M, Nahrevanian H, Javadi A, Pourshafie MR (2017) Probiotic characters of Bifidobacterium and Lactobacillus are a result of the ongoing gene acquisition and genome minimization evolutionary trends. Microb Pathog 111:118–131. https://doi.org/10.1016/j.micpath.2017.08.021

    Article  CAS  PubMed  Google Scholar 

  42. Xiao Y, Zhao J, Zhang H, Zhai Q, Chen W (2021) Mining genome traits that determine the different gut colonization potential of Lactobacillus and Bifidobacterium species. Microb Genom. https://doi.org/10.1099/mgen.0.000581

    Article  PubMed  PubMed Central  Google Scholar 

  43. Litvak Y, Byndloss MX, Tsolis RM, Bäumler AJ (2017) Dysbiotic proteobacteria expansion: a microbial signature of epithelial dysfunction. Curr Opin Microbiol 39:1–6. https://doi.org/10.1016/j.mib.2017.07.003

    Article  CAS  PubMed  Google Scholar 

  44. Litvak Y, Mon KKZ, Nguyen H, Chanthavixay G, Liou M, Velazquez EM, Kutter L, Alcantara MA, Byndloss MX, Tiffany CR, Walker GT, Faber F, Zhu Y, Bronner DN, Byndloss AJ, Tsolis RM, Zhou H, Bäumler AJ (2019) Commensal Enterobacteriaceae protect against Salmonella colonization through oxygen competition. Cell Host Microbe 25(1):128-139.e125. https://doi.org/10.1016/j.chom.2018.12.003

    Article  CAS  PubMed  Google Scholar 

  45. Liu Y, Chen F, Odle J, Lin X, Jacobi SK, Zhu H, Wu Z, Hou Y (2012) Fish oil enhances intestinal integrity and inhibits TLR4 and NOD2 signaling pathways in weaned pigs after LPS challenge. J Nutr 142(11):2017–2024. https://doi.org/10.3945/jn.112.164947

    Article  CAS  PubMed  Google Scholar 

  46. Chen CY, Tsen HY, Lin CL, Yu B, Chen CS (2012) Oral administration of a combination of select lactic acid bacteria strains to reduce the Salmonella invasion and inflammation of broiler chicks. Poult Sci 91(9):2139–2147. https://doi.org/10.3382/ps.2012-02237

    Article  CAS  PubMed  Google Scholar 

  47. Abreu MT (2010) Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 10(2):131–144. https://doi.org/10.1038/nri2707

    Article  CAS  PubMed  Google Scholar 

  48. Zampiga M, Bertocchi M, Bosi P, Trevisi P, Meluzzi A, Sirri F (2019) Differences in productive performance and intestinal transcriptomic profile in two modern fast-growing chicken hybrids. J Anim Physiol Anim Nutr (Berl) 103(1):125–134. https://doi.org/10.1111/jpn.13015

    Article  CAS  PubMed  Google Scholar 

  49. Fries-Craft KA, Meyer MM, Lindblom SC, Kerr BJ, Bobeck EA (2021) Lipid source and peroxidation status alter immune cell recruitment in broiler chicken ileum. J Nutr 151(1):223–234. https://doi.org/10.1093/jn/nxaa356

    Article  PubMed  Google Scholar 

  50. Qu Y, Misaghi S, Newton K, Maltzman A, Izrael-Tomasevic A, Arnott D, Dixit VM (2016) NLRP3 recruitment by NLRC4 during Salmonella infection. J Exp Med 213(6):877–885. https://doi.org/10.1084/jem.20132234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to thank Jiangsu Yancheng Nature Reserve provides sampling opportunities; Yuting Wu, Shuo Zhang, Jiwen Liu, and Meihua Zhang for helping with the necropsy of experimental animals.

Funding

This work was supported by National Key R&D Program (2022YFC2105005), the Forestry Science and Technology Innovation and Promotion Project of Jiangsu Province (LYKJ [2021]40), the Project of Science and Technology Support Plan of Taizhou (SNY20210022), Jiangsu Agriculture Science and Technology Innovation Fund (JASTIF) (CX (21)3174), and the Priority Academic Program Development of Jiangsu Higher Education Institutions.

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Authors and Affiliations

  1. MOE Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, 210095, China

    Huixian Wu, Chenchen Ding, Xujie Ma, Zhangshan Gao, Shuhui Liu & Suquan Song

  2. Management Office of Dafeng, Milu National Nature Reserve, Yancheng, 224136, China

    Bin Liu

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  1. Huixian Wu
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Contributions

SS and WH designed the experiments. WH, DC, LB, and MX carried out animal experiment, data analysis, and drafted the manuscript. WH and MX did the cell culture. GZ and LS analyzed the qRT-PCR. WH and DC wrote the manuscript. SS and LB reviewed the manuscript.

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Correspondence to Suquan Song.

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Wu, H., Ding, C., Ma, X. et al. Microencapsulate Probiotics (MP) Promote Growth Performance and Inhibit Inflammatory Response in Broilers Challenged with Salmonella typhimurium. Probiotics & Antimicro. Prot. 16, 623–635 (2024). https://doi.org/10.1007/s12602-023-10074-6

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