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Immunomodulatory Activity of Probiotics in Models of Bacterial Infections

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Abstract

As resistance to conventional antibiotics among bacteria continues to increase, researchers are increasingly focusing on alternative strategies for preventing and treating bacterial infections, one of which is microbiota modulation. The objective of this review is to analyze the scientific literature on the immunomodulatory effects of probiotics in bacterial infections. This is an integrative review of the literature based on systematic steps, with searches performed in the databases Medline, PubMed, Scopus, Embase, and ScienceDirect. The most prevalent bacterial genera used to evaluate infectious processes were Salmonella, Escherichia, Klebsiella, and Streptococcus. Lactobacillus was the most commonly used probiotic genus, with Lactobacillus delbrueckii subsp. bulgaricus is the most frequently used species. In most studies, prophylactic treatment with concentrations of probiotics equal to or greater than 8 log CFU/mL was chosen. However, there was considerable heterogeneity in terms of effective treatment duration, indicating that the results cannot be generalized across all studies. This review found that probiotics interact with the immune system through different mechanisms and have a positive effect on preventing different types of bacterial infections.

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References

  1. World Health Organization (2015) Global action plan on antimicrobial resistance. https://www.who.int/publications/i/item/9789241509763. Accessed 15 Dec 2022

  2. CENTERS FOR DISEASE CONTROL AND, PREVENTION et al (2019) Antibiotic resistance threats in the United States, 2019. Atlanta, GA: US Department of Health and Human Services, CDC. https://www.cdc.gov/drugresistance/pdf/threats-report/2019-ar-threats-report-508.pdf. Accessed 03 Dec 2022

  3. O’Neil J (2016) Tackling drug-resistant infections globally: final report and recommendations. https://amr-review.org/sites/default/files/160518_Final paper_with cover.pdf. Accessed 01 Feb 2023

  4. O’Neil J (2014) Review on antibiotic resistance. Antimicrobial Resistance: tackling a crisis for the health and wealth of nations.Heal. Wealth Nations, p1–16. https://amr-review.org/sites/default/files/AMR Review Paper - Tackling a crisis for the health and wealth of nations_1.pdf. Accessed 01 Feb 2023

  5. Murray CJL et al (2022) Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet 399(10325):629–655. https://doi.org/10.1016/S0140-6736(21)02724-0

    Article  CAS  Google Scholar 

  6. Hauser AR, Mecsas J, Moir DT (2016) Beyond antibiotics: new therapeutic approaches for bacterial infections. Clin Infect Dis 63(1):89–95. https://doi.org/10.1093/cid/ciw200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Derwa Y, Gracie DJ, Hamlin PJ, Ford AC (2017) Systematic review with meta-analysis: the efficacy of probiotics in inflammatory bowel disease. Aliment Pharmacol Ther 46:389–400. https://doi.org/10.1111/apt.14203

    Article  CAS  PubMed  Google Scholar 

  8. Szajewska H, Kolodziej M, Gieruszczak-Bialek D, Skorka A, Ruszczynski M, Shamir R (2019) Systematic review with meta-analysis: Lactobacillus rhamnosus GG for treating acute gastroenteritis in children-a 2019 update. Aliment Pharmacol Ther 49:1376–1384

    Article  PubMed  Google Scholar 

  9. Davani-davari D et al (2019) Prebiotics: definition, types, sources, mechanisms, and clinical applications. Foods v 8(3):92

    Article  CAS  Google Scholar 

  10. FAO/WHO. Food and Agricultural Organization of the United Nations and World Health Organization (2002) Joint FAO/WHO working group report on drafting guidelines for the evaluation of probiotics in food. Food and Agricultural Organization of the United Nations

  11. Hill C et al (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. https://doi.org/10.1038/nrgastro.2014.66

    Article  PubMed  Google Scholar 

  12. Cuevas-González PF, Liceaga AM, Aguilar-Toalá JE (2020) Postbiotics and paraprobiotics: from concepts to applications. Int Food Res J 136:109502. https://doi.org/10.1016/j.foodres.2020.109502

    Article  CAS  Google Scholar 

  13. Rizzardini G et al (2012) Evaluation of the immune benefits of two probiotic strains Bifidobacterium animalis ssp. lactis, BB-12® and Lactobacillus paracasei ssp. paracasei, L. casei 431® in an influenza vaccination model: a randomisez, double-blind, placebo-controlled study. Br J Nutr 107(6):876–884. https://doi.org/10.1017/S000711451100420X

    Article  CAS  PubMed  Google Scholar 

  14. Chifiriuc MC et al (2010) Patterns of colonization and immune response elicited from interactions between enteropathogenic bacteria, epithelial cells and probiotic fractions. Int J Biotechnol Mol Biol Res 1(4):47–57

    Google Scholar 

  15. Kemgang TS et al (2016) Fermented milk with probiotic Lactobacillus rhamnosus S1K3 (MTCC5957) protects mice from Salmonella by enhancing immune and nonimmune protection mechanisms at the intestinal mucosal level. J Nutr Biochem 30:62–73. https://doi.org/10.1016/j.jnutbio.2015.11.018

    Article  CAS  PubMed  Google Scholar 

  16. Bermudez-Brito M et al (2012) Probiotic mechanisms of action. Ann Nutr Metab 61(2):160–174

    Article  CAS  PubMed  Google Scholar 

  17. Ukena SN et al (2007) Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. PLoS ONE 2(12):e1308. https://doi.org/10.1371/journal.pone.0001308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mennigen R et al (2009) Probiotic mixture VSL# 3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am J Physiol Gastrointest Liver Physiol. https://doi.org/10.1152/ajpgi.90534.2008

    Article  PubMed  Google Scholar 

  19. Madsen K et al (2001) Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterol 121(3):580–591. https://doi.org/10.1053/gast.2001.27224

    Article  CAS  Google Scholar 

  20. Arpaia N et al (2013) Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504:451–455. https://doi.org/10.1038/nature12726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Smith PM et al (2013) The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341:569–573. https://doi.org/10.1126/science.1241165

    Article  CAS  PubMed  Google Scholar 

  22. Menard O et al (2008) Gnotobiotic mouse immune response induced by Bifidobacterium sp. strains isolated from infants. Appl Environ Microbiol 74(3):660–666. https://doi.org/10.1128/AEM.01261-07

    Article  CAS  PubMed  Google Scholar 

  23. Shanahan F (2010) Probiotics in perspective. Gastroenterol 139(6):1808–1812

    Article  Google Scholar 

  24. Otutumi LK, Góis MB, Garcia ERM, Loddi MM (2012) Variations on the Efficacy of Probiotics in Poultry. In: RIGOBELO, C. Probiotics in animals. InTech. 203–230

  25. Sterlin D et al (2020) Human IgA binds a diverse array of commensal bacteria. J Exp Med 217(3). https://doi.org/10.1084/jem.20181635

  26. Mestecky J et al (2005) Mucosal immunoglobulins. Mucosal immunology, 3rd edn. Academic Press, Burlington, MA, pp 153–181

    Chapter  Google Scholar 

  27. Pabst O (2012) New concepts in the generation and functions of IgA. Nat Rev Immunol 12(12):821–832. https://doi.org/10.1038/nri3322

    Article  CAS  PubMed  Google Scholar 

  28. Whittemore R, Knafl K (2005) The integrative review: updated methodology. J Adv Nurs 52(5):546–553. https://doi.org/10.1111/j.1365-2648.2005.03621.x

    Article  PubMed  Google Scholar 

  29. Santos C, Pimenta C, Nobre M (2007) A estratégia PICO para a construção da pergunta de pesquisa e busca de evidências. Rev Latino-Am Enfermagem 15(3):2–5. https://doi.org/10.1590/S0104-11692007000300023

    Article  Google Scholar 

  30. Ouzzani M et al (2016) Rayyan—a web and mobile app for systematic reviews. Syst Rev 5(1):1–10. https://doi.org/10.1186/s13643-016-0384-4

    Article  Google Scholar 

  31. Page MJ et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Syst Rev 10(1):1–11. https://doi.org/10.1016/j.ijsu.2021.105906

    Article  Google Scholar 

  32. Sarkis-Onofre R et al (2021) How to properly use the PRISMA Statement. Syst Rev 10(1):1–3. https://doi.org/10.1186/s13643-021-01671-z

    Article  Google Scholar 

  33. Cordeiro MA et al (2019) Fermented whey dairy beverage offers protection against Salmonella enterica ssp. enterica serovar Typhimurium infection in mice. J Dairy Sci 102(8):6756–6765. https://doi.org/10.3168/jds.2019-16340

    Article  CAS  PubMed  Google Scholar 

  34. Dowdell P et al (2020) Probiotic activity of Enterococcus faecium and Lactococcus lactis isolated from thai fermented sausages and their protective effect against Clostridium difficile. Probiotics & Antimicro Prot 12(2):641–648. https://doi.org/10.1007/s12602-019-09536-7

    Article  CAS  Google Scholar 

  35. Jain S, Yadav H, Sinha PR (2009) Probiotic dahi containing Lactobacillus casei protects against Salmonella enteritidis infection and modulates the immune response in mice. J Med Food 12(3):576–583. https://doi.org/10.1089/jmf.2008.0246

    Article  CAS  PubMed  Google Scholar 

  36. Medici M et al (2005) Effect of fermented milk containing probiotic bacteria in the prevention of an enteroinvasive Escherichia coli infection in mice. J Dairy Res 72(2):243–249. https://doi.org/10.1017/S0022029905000750

    Article  CAS  PubMed  Google Scholar 

  37. Villena J et al (2006) Yoghurt accelerates the recovery of defense mechanisms against Streptococcus pneumoniae in protein-malnourished mice. Br J Nutr 95(3):591–602. https://doi.org/10.1079/BJN20051663

    Article  CAS  PubMed  Google Scholar 

  38. Alvarez S et al (2001) Effect of Lactobacillus casei and yogurt administration on prevention of Pseudomonas aeruginosa infection in young mice. J Food Prot 64(11):1768–1774. https://doi.org/10.4315/0362-028X-64.11.1768

    Article  CAS  PubMed  Google Scholar 

  39. Tejada-Simon MV et al (1999) Ingestion of yogurt containing Lactobacillus acidophilus and Bifidobacterium to potentiate immunoglobulin A responses to cholera toxin in mice. J Dairy Sci 82(4):649–660. https://doi.org/10.3168/jds.S0022-0302(99)75281-1

    Article  CAS  PubMed  Google Scholar 

  40. Montijo-Prieto S et al (2015) A Lactobacillus plantarum strain isolated from kefir protects against intestinal infection with Yersinia enterocolitica O9 and modulates immunity in mice. Res Microbiol 166(8):626–632. https://doi.org/10.1016/j.resmic.2015.07.010

    Article  CAS  PubMed  Google Scholar 

  41. Kamaladevi A, Balamurugan K (2016) Lactobacillus casei triggers a TLR mediated RACK-1 dependent p38 MAPK pathway in Caenorhabditis elegans to resist Klebsiella pneumoniae infection. Food Funct 7(7):3211–3223. https://doi.org/10.1016/j.resmic.2015.07.010

    Article  CAS  PubMed  Google Scholar 

  42. Tsai Y, Cheng P, Pan T (2010) Immunomodulating activity of Lactobacillus paracasei subsp. paracasei NTU 101 in enterohemorrhagic Escherichia coli O157H7-infected mice. J Agric Food Chem 58(21):11265–11272. https://doi.org/10.1021/jf103011z

    Article  CAS  PubMed  Google Scholar 

  43. Vieira AT et al (2016) Control of Klebsiella pneumoniae pulmonary infection and immunomodulation by oral treatment with the commensal probiotic Bifidobacterium longum 51A. Microbes Infect 18(3):180–189. https://doi.org/10.1016/j.micinf.2015.10.008

    Article  PubMed  Google Scholar 

  44. Cooney MA et al (2014) A murine oral model for Mycobacterium avium subsp. paratuberculosis infection and immunomodulation with Lactobacillus casei ATCC 334. Front. Cell Infect Microbiol 4:11. https://doi.org/10.3389/fcimb.2014.00011

    Article  CAS  Google Scholar 

  45. Deng Q et al (2015) Intravaginal lactic acid bacteria modulated local and systemic immune responses and lowered the incidence of uterine infections in periparturient dairy cows. PLoS ONE 10(4):e0124167. https://doi.org/10.1371/journal.pone.0124167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Johnson-Henry KC et al (2005) Amelioration of the effects of Citrobacter rodentium infection in mice by pre-treatment with probiotics. J Infect Dis 191(12):2106–2117. https://doi.org/10.1086/430318

    Article  PubMed  Google Scholar 

  47. Mao J et al (2020) Lactobacillus rhamnosus GG attenuates lipopolysaccharide-induced inflammation and barrier dysfunction by regulating MAPK/NF-κB signaling and modulating metabolome in the piglet intestine. J Nutr 150(5):1313–1323. https://doi.org/10.1093/jn/nxaa009

    Article  PubMed  Google Scholar 

  48. Noto Llana M et al (2013) Consumption of Lactobacillus casei fermented milk prevents Salmonella reactive arthritis by modulating IL-23/IL-17 expression. PLoS ONE 8(12):e82588. https://doi.org/10.1371/journal.pone.0082588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Salva S, Villena J, Alvarez S (2010) Immunomodulatory activity of Lactobacillus rhamnosus strains isolated from goat milk: impact on intestinal and respiratory infections. Int J Food Microbiol 141(1–2):82–89. https://doi.org/10.1016/j.ijfoodmicro.2010.03.013

    Article  CAS  PubMed  Google Scholar 

  50. Sharma R et al (2014) Improvement in Th1/Th2 immune homeostasis, antioxidative status and resistance to pathogenic E. coli on consumption of probiotic Lactobacillus rhamnosus fermented milk in aging mice. Age 36(4):1–17

    Article  CAS  Google Scholar 

  51. Silva AM et al (2004) Effect of Bifidobacterium longum ingestion on experimental salmonellosis in mice. J Appl Microbiol 97(1):29–37. https://doi.org/10.1111/j.1365-2672.2004.02265.x

    Article  CAS  PubMed  Google Scholar 

  52. Wilson AS et al (2020) Diet and the human gut microbiome: an international review. Dig Dis Sci 65(3):723–740. https://doi.org/10.1007/s10620-020-06112-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Illikoud N et al (2022) Dairy starters and fermented dairy products modulate gut mucosal immunity. Immunol Lett. https://doi.org/10.1016/j.imlet.2022.11.002

    Article  PubMed  Google Scholar 

  54. Ha E, Zemel MB (2003) Functional properties of whey, whey components, and essential amino acids: mechanisms underlying health benefits for active people. J Nutr Biochem 14(5):251–258. https://doi.org/10.1016/S0955-2863(03)00030-5

    Article  CAS  PubMed  Google Scholar 

  55. Ume ROOBAB et al (2020) Sources, formulations, advanced delivery and health benefits of probiotics. Curr Opin Food Sci v 32:17–28

    Article  Google Scholar 

  56. Aspri M, Papademas P, Tsaltas D (2020) Review on non-dairy probiotics and their use in non-dairy based products. Fermentation 6(1):30. https://doi.org/10.3390/fermentation6010030

    Article  CAS  Google Scholar 

  57. Kumar D et al (2022) Functional fermented probiotics, Prebiotics, and Synbiotics from Non-Dairy Products: a perspective from Nutraceutical. Mol Nutr Food Res 66(14):2101059. https://doi.org/10.1002/mnfr.202101059

    Article  CAS  Google Scholar 

  58. Francisco GUARNER et al (2008) World Gastroenterology Organisation Practice Guideline: Probiotics and Prebiotics-May 2008: guideline. South Afr Gastroenterol Rev v 6(2):14–25

    Google Scholar 

  59. BRASIL, Resolução (2002) n. 2, de 7 de janeiro de Aprova o Regulamento Técnico de Substâncias Bioativas e Probióticos Isolados com Alegação de Propriedades Funcional e ou de Saúde. Diário Oficial da União, Poder Executivo, de 9 de janeiro de 2002. https://www.saude.rj.gov.br/comum/code/MostrarArquivo.php?C=MjI1Mw%2 C%2 C Accessed 10 Jan 2023

  60. Izumo T et al (2011) Influence of Lactobacillus pentosus S-PT84 ingestion on the mucosal immunity of healthy and Salmonella typhimurium-infected mice. Biosci Microflora 30(2):27–35. https://doi.org/10.12938/bifidus.30.27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Nauciel C, Espinasse-Maes F (1992) Role of gamma interferon and tumor necrosis factor alpha in resistance to Salmonella typhimurium infection. Infect Immun 60(2):450–454. https://doi.org/10.1128/iai.60.2.450-454.1992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Martinez MB, Trabulsi LR (2008) Enterobacteriaceae. In: Trabulsi LR, Alterthum F (eds) Editores. Microbiologia. Atheneu, São Paulo, pp 271–279

    Google Scholar 

  63. Nataro JP, Kaper JB (1998) Diarrheagenic Escherichia coli. Clin Microbiol Rev 11(1):142–201. https://doi.org/10.1128/CMR.11.1.142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Chang J, Park J, Kim S (2006) Dependence on p38 MAPK signaling in the up-regulation of TLR2, TLR4 and TLR9 gene expression in Trichomonas vaginalis‐treated HeLa cells. Immunol 118(2):164–170. https://doi.org/10.1111/j.1365-2567.2006.02347.x

    Article  CAS  Google Scholar 

  65. Quan CP et al (1997) Natural polyreactive secretory immunoglobulin a autoantibodies as a possible barrier to infection in humans. Infect Immun 65(10):3997–4004. https://doi.org/10.1128/iai.65.10.3997-4004.1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Mills KHG, Mcguirk P (2004) Antigen-specific regulatory T cells—their induction and role in infection. In: seminars in immunology. Acad Press 16:107–117. https://doi.org/10.1016/j.smim.2003.12.006

    Article  CAS  Google Scholar 

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Funding

This research was financially supported by Technical Cooperation Agreement to Support the Development of the Brazilian Semi-Arid Region - FAPEMA/CAPES - ACT-05691/21, ACT 01784-21 and to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) - Finance Code 001.

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Authors and Affiliations

  1. Graduate Program in Health and Technology, Center for Sciences of Imperatriz, Federal University of Maranhão, Maranhão, Brazil

    Tatielle Gomes Dias, Ana Lúcia Fernandes Pereira, Adriana Gomes Nogueira Ferreira, Marcelino Santos Neto, Richard Pereira Dutra, Aramys Silva Reis & Márcia Cristina Gonçalves Maciel

  2. Graduate Program in Biodiversity and Biotechnology, Federal University of Maranhão, São Luís, Maranhão, Brazil

    Liliane dos Santos Rodrigues

  3. Graduate Program in Health Sciences, Federal University of Maranhão, São Luís, Maranhão, Brazil

    Josivan Regis Farias & Rosane Nassar Meireles Guerra

  4. Department of Pathology, Federal University of Maranhão, São Luís, Maranhão, Brazil

    Rosane Nassar Meireles Guerra & Valério Monteiro-Neto

  5. Department of Cell Biology, University of Brasília, Brasília, Distrito Federal, Brazil

    Márcia Cristina Gonçalves Maciel

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Contributions

All authors contributed to the study conception and design. The authors confirm contribution to the paper as follows: TGD: Theme idea, bibliographic survey and article writing; LSR: Table and figure construction, complete review of the manuscript; JRF: Substantial contributions to the conception or design of the work; ALF: Review and correction of the content discussed in the introduction; AGNF: Review and methodology correction, as well as assistance in the implementation of tools to assist in search of bibliographic; MSN: Review and critical analysis of the discussion; RPD: Review and elaboration of the guiding question; ASR: Critical analysis of results and correction of figures and tables; RNMG: Critical analysis of writing and coherence of the text; VMN: categorization of studies that emphasized the immunomodulatory potential of probiotics; MCGM: Critical review for intellectual content and final approval of the version to be published.

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Correspondence to Márcia Cristina Gonçalves Maciel.

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Dias, T.G., Rodrigues, L.d.S., Farias, J.R. et al. Immunomodulatory Activity of Probiotics in Models of Bacterial Infections. Probiotics & Antimicro. Prot. 16, 862–874 (2024). https://doi.org/10.1007/s12602-023-10090-6

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