• This record comes from PubMed

Defined Pig Microbiota Mixture as Promising Strategy against Salmonellosis in Gnotobiotic Piglets

. 2024 Jun 13 ; 14 (12) : . [epub] 20240613

Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic

Document type Journal Article

Grant support
21-15621S Czech Science Foundation

Probiotics are a potential strategy for salmonellosis control. A defined pig microbiota (DPM) mixture of nine bacterial strains previously exhibited probiotic and anti-Salmonella properties in vitro. Therefore, we evaluated its gut colonization ability and protection effect against S. typhimurium LT2-induced infection in the gnotobiotic piglet model. The DPM mixture successfully colonized the piglet gut and was stable and safe until the end of the experiment. The colon was inhabited by about 9 log CFU g-1 with a significant representation of bifidobacteria and lactobacilli compared to ileal levels around 7-8 log CFU g-1. Spore-forming clostridia and bacilli seemed to inhabit the environment only temporarily. The bacterial consortium contributed to the colonization of the gut at an entire length. The amplicon profile analysis supported the cultivation trend with a considerable representation of lactobacilli with bacilli in the ileum and bifidobacteria with clostridia in the colon. Although there was no significant Salmonella-positive elimination, it seems that the administered bacteria conferred the protection of infected piglets because of the slowed delayed infection manifestation without translocations of Salmonella cells to the blood circulation. Due to its colonization stability and potential protective anti-Salmonella traits, the DPM mixture has promising potential in pig production applications. However, advanced immunological tests are needed.

See more in PubMed

Jandhyala S.M., Talukdar R., Subramanyam C., Vuyyuru H., Sasikala M., Reddy D.N. Role of the normal gut microbiota. World J. Gastroenterol. 2015;21:8787. doi: 10.3748/wjg.v21.i29.8787. PubMed DOI PMC

Sonnenburg J.L., Xu J., Leip D.D., Chen C.-H., Westover B.P., Weatherford J., Buhler J.D., Gordon J.I. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science. 2005;307:1955–1959. doi: 10.1126/science.1109051. PubMed DOI

Pant A., Maiti T.K., Mahajan D., Das B. Human gut microbiota and drug metabolism. Microb. Ecol. 2023;86:97–111. doi: 10.1007/s00248-022-02081-x. PubMed DOI PMC

Gensollen T., Iyer S.S., Kasper D.L., Blumberg R.S. How colonization by microbiota in early life shapes the immune system. Science. 2016;352:539–544. doi: 10.1126/science.aad9378. PubMed DOI PMC

Enav H., Bäckhed F., Ley R.E. The developing infant gut microbiome: A strain-level view. Cell Host Microbe. 2022;30:627–638. doi: 10.1016/j.chom.2022.04.009. PubMed DOI

Rothschild D., Weissbrod O., Barkan E., Kurilshikov A., Korem T., Zeevi D., Costea P.I., Godneva A., Kalka I.N., Bar N. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018;555:210–215. doi: 10.1038/nature25973. PubMed DOI

Wilkins L.J., Monga M., Miller A.W. Defining dysbiosis for a cluster of chronic diseases. Sci. Rep. 2019;9:12918. doi: 10.1038/s41598-019-49452-y. PubMed DOI PMC

Karin M., Lawrence T., Nizet V. Innate immunity gone awry: Linking microbial infections to chronic inflammation and cancer. Cell. 2006;124:823–835. doi: 10.1016/j.cell.2006.02.016. PubMed DOI

Zeng M.Y., Inohara N., Nuñez G. Mechanisms of inflammation-driven bacterial dysbiosis in the gut. Mucosal Immunol. 2017;10:18–26. doi: 10.1038/mi.2016.75. PubMed DOI PMC

Stecher B., Robbiani R., Walker A.W., Westendorf A.M., Barthel M., Kremer M., Chaffron S., Macpherson A.J., Buer J., Parkhill J. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 2007;5:e244. PubMed PMC

Lupp C., Robertson M.L., Wickham M.E., Sekirov I., Champion O.L., Gaynor E.C., Finlay B.B. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe. 2007;2:119–129. doi: 10.1016/j.chom.2007.06.010. PubMed DOI

Baldelli V., Scaldaferri F., Putignani L., Del Chierico F. The role of Enterobacteriaceae in gut microbiota dysbiosis in inflammatory bowel diseases. Microorganisms. 2021;9:697. doi: 10.3390/microorganisms9040697. PubMed DOI PMC

Swart A.N., Evers E.G., Simons R.L.L., Swanenburg M. Modeling of Salmonella contamination in the pig slaughterhouse. Risk Anal. 2016;36:498–515. doi: 10.1111/risa.12514. PubMed DOI

Correia-Gomes C., Leonard F., Graham D. Description of control programmes for Salmonella in pigs in Europe. Progress to date? J. Food Saf. 2021;41:e12916. doi: 10.1111/jfs.12916. DOI

Smith R.P., May H.E., Burow E., Meester M., Tobias T.J., Sassu E.-L., Pavoni E., Di Bartolo I., Prigge C., Wasyl D. Assessing pig farm biosecurity measures for the control of Salmonella on European farms. Epidemiol. Infect. 2023;151:e130. doi: 10.1017/S0950268823001115. PubMed DOI PMC

Bhunia A.K. Foodborne Microbial Pathogens: Mechanisms and Pathogenesis. Springer; Berlin/Heidelberg, Germany: 2018. pp. 271–287. DOI

Campos J., Mourão J., Peixe L., Antunes P. Non-typhoidal Salmonella in the pig production chain: A comprehensive analysis of its impact on human health. Pathogens. 2019;8:19. doi: 10.3390/pathogens8010019. PubMed DOI PMC

Casanova-Higes A., Marín-Alcalá C.M., Andrés-Barranco S., Cebollada-Solanas A., Alvarez J., Mainar-Jaime R.C. Weaned piglets: Another factor to be considered for the control of Salmonella infection in breeding pig farms. Vet. Res. 2019;50:45. doi: 10.1186/s13567-019-0666-7. PubMed DOI PMC

Gresse R., Chaucheyras-Durand F., Fleury M.A., Van de Wiele T., Forano E., Blanquet-Diot S. Gut microbiota dysbiosis in postweaning piglets: Understanding the keys to health. Trends Microbiol. 2017;25:851–873. doi: 10.1016/j.tim.2017.05.004. PubMed DOI

Callaway T.R., Morrow J.L., Edrington T.S., Genovese K.J., Dowd S., Carroll J., Dailey J.W., Harvey R.B., Poole T.L., Anderson R.C. Social stress increases fecal shedding of Salmonella typhimurium by early weaned piglets. Curr. Issues Intest. Microbiol. 2006;7:65–72. PubMed

Pereira W.A., Franco S.M., Reis I.L., Mendonça C.M.N., Piazentin A.C.M., Azevedo P.O.S., Marcos L.P., De Martinis E.C.P., Gierus M., Oliveira R.P.S. Beneficial effects of probiotics on the pig production cycle: An overview of clinical impacts and performance. Vet. Microbiol. 2022;269:109431. doi: 10.1016/j.vetmic.2022.109431. PubMed DOI

Zhang Y., Zhang Y., Liu F., Mao Y., Zhang Y., Zeng H., Ren S., Guo L., Chen Z., Hrabchenko N. Mechanisms and applications of probiotics in prevention and treatment of swine diseases. Porc. Health Manag. 2023;9:5. doi: 10.1186/s40813-022-00295-6. PubMed DOI PMC

Nair M.S., Amalaradjou M.A., Venkitanarayanan K. Antivirulence properties of probiotics in combating microbial pathogenesis. Adv. Appl. Microbiol. 2017;98:1–29. PubMed

Hill C., Guarner F., Reid G., Gibson G.R., Merenstein D.J., Pot B., Morelli L., Canani R.B., Flint H.J., Salminen S. 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. 2014;11:506–514. doi: 10.1038/nrgastro.2014.66. PubMed DOI

Rabetafika H.N., Razafindralambo A., Ebenso B., Razafindralambo H.L. Probiotics as Antibiotic Alternatives for Human and Animal Applications. Encyclopedia. 2023;3:561–581. doi: 10.3390/encyclopedia3020040. DOI

Barba-Vidal E., Martín-Orúe S.M., Castillejos L. Practical aspects of the use of probiotics in pig production: A review. Livest. Sci. 2019;223:84–96. doi: 10.1016/j.livsci.2019.02.017. DOI

Lekagul A., Tangcharoensathien V., Yeung S. Patterns of antibiotic use in global pig production: A systematic review. Vet. Anim. Sci. 2019;7:100058. doi: 10.1016/j.vas.2019.100058. PubMed DOI PMC

Barton M.D. Impact of antibiotic use in the swine industry. Curr. Opin. Microbiol. 2014;19:9–15. doi: 10.1016/j.mib.2014.05.017. PubMed DOI

Yang H., Paruch L., Chen X., Van Eerde A., Skomedal H., Wang Y., Liu D., Liu Clarke J. Antibiotic application and resistance in swine production in China: Current situation and future perspectives. Front. Vet. Sci. 2019;6:136. doi: 10.3389/fvets.2019.00136. PubMed DOI PMC

Liao S.F., Nyachoti M. Using probiotics to improve swine gut health and nutrient utilization. Anim. Nutr. 2017;3:331–343. doi: 10.1016/j.aninu.2017.06.007. PubMed DOI PMC

Lambo M.T., Chang X., Liu D. The recent trend in the use of multistrain probiotics in livestock production: An overview. Animals. 2021;11:2805. doi: 10.3390/ani11102805. PubMed DOI PMC

Valeriano V.D.V., Balolong M.P., Kang D.K. Probiotic roles of Lactobacillus sp. in swine: Insights from gut microbiota. J. Appl. Microbiol. 2017;122:554–567. doi: 10.1111/jam.13364. PubMed DOI

Barba-Vidal E., Castillejos L., Roll V.F.B., Cifuentes-Orjuela G., Moreno Muñoz J.A., Martín-Orúe S.M. The probiotic combination of Bifidobacterium longum subsp. infantis CECT 7210 and Bifidobacterium animalis subsp. lactis BPL6 reduces pathogen loads and improves gut health of weaned piglets orally challenged with Salmonella typhimurium. Front. Microbiol. 2017;8:1570. PubMed PMC

Lan R., Kim I. Enterococcus faecium supplementation in sows during gestation and lactation improves the performance of sucking piglets. Vet. Med. Sci. 2020;6:92–99. doi: 10.1002/vms3.215. PubMed DOI PMC

Luise D., Bosi P., Raff L., Amatucci L., Virdis S., Trevisi P. Bacillus spp. probiotic strains as a potential tool for limiting the use of antibiotics, and improving the growth and health of pigs and chickens. Front. Microbiol. 2022;13:801827. PubMed PMC

Cao G., Tao F., Hu Y., Li Z., Zhang Y., Deng B. Positive effects of a Clostridium butyricum-based compound probiotic on growth performance, immune responses, intestinal morphology, hypothalamic neurotransmitters, and colonic microbiota in weaned piglets. Food Funct. 2019;10:2926–2934. doi: 10.1039/C8FO02370K. PubMed DOI

García G.R., Dogi C.A., Poloni V.L., Fochesato A.S., De Moreno de Leblanc A., Cossalter A.M., Payros D., Oswald I.P., Cavaglieri L.R. Beneficial effects of Saccharomyces cerevisiae RC016 in weaned piglets: In vivo and ex vivo analysis. Benef. Microbes. 2019;10:33–42. doi: 10.3920/BM2018.0023. PubMed DOI

McFarland L.V. Efficacy of single-strain probiotics versus multi-strain mixtures: Systematic review of strain and disease specificity. Dig. Dis. Sci. 2021;66:694–704. doi: 10.1007/s10620-020-06244-z. PubMed DOI

Vinderola G., Gueimonde M., Gomez-Gallego C., Delfederico L., Salminen S. Correlation between in vitro and in vivo assays in selection of probiotics from traditional species of bacteria. Trends Food Sci. Technol. 2017;68:83–90. doi: 10.1016/j.tifs.2017.08.005. DOI

Papadimitriou K., Zoumpopoulou G., Foligné B., Alexandraki V., Kazou M., Pot B., Tsakalidou E. Discovering probiotic microorganisms: In vitro, in vivo, genetic and omics approaches. Front. Microbiol. 2015;6:58. doi: 10.3389/fmicb.2015.00058. PubMed DOI PMC

Horvathova K., Modrackova N., Splichal I., Splichalova A., Amin A., Ingribelli E., Killer J., Doskocil I., Pechar R., Kodesova T. Defined Pig Microbiota with a Potential Protective Effect against Infection with Salmonella typhimurium. Microorganisms. 2023;11:1007. doi: 10.3390/microorganisms11041007. PubMed DOI PMC

Splichalova A., Slavikova V., Splichalova Z., Splichal I. Preterm life in sterile conditions: A study on preterm, germ-free piglets. Front. Immunol. 2018;9:220. doi: 10.3389/fimmu.2018.00220. PubMed DOI PMC

Splichalova A., Jenistova V., Splichalova Z., Splichal I. Colonization of preterm gnotobiotic piglets with probiotic Lactobacillus rhamnosus GG and its interference with Salmonella typhimurium. Clin. Exp. Immunol. 2019;195:381–394. doi: 10.1111/cei.13236. PubMed DOI PMC

Trebichavský I., Dlabac V., Reháková Z., Zahradnícková M., Splichal I. Cellular changes and cytokine expression in the ilea of gnotobiotic piglets resulting from peroral Salmonella typhimurium challenge. Infect. Immun. 1997;65:5244–5249. doi: 10.1128/iai.65.12.5244-5249.1997. PubMed DOI PMC

Splichal I., Donovan S.M., Splichalova Z., Neuzil Bunesova V., Vlkova E., Jenistova V., Killer J., Svejstil R., Skrivanova E., Splichalova A. Colonization of germ-free piglets with commensal Lactobacillus amylovorus, Lactobacillus mucosae, and probiotic E. coli Nissle 1917 and their interference with Salmonella typhimurium. Microorganisms. 2019;7:273. doi: 10.3390/microorganisms7080273. PubMed DOI PMC

Modrackova N., Stovicek A., Burtscher J., Bolechova P., Killer J., Domig K.J., Neuzil-Bunesova V. The bifidobacterial distribution in the microbiome of captive primates reflects parvorder and feed specialization of the host. Sci. Rep. 2021;11:1–13. PubMed PMC

Hungate R.E., Macy J. The roll-tube method for cultivation of strict anaerobes. Bull. Ecol. Res. Comm. 1973;17:123–126.

Rada V., Petr J. A new selective medium for the isolation of glucose non-fermenting bifidobacteria from hen caeca. J. Microbiol. Methods. 2000;43:127–132. doi: 10.1016/S0167-7012(00)00205-0. PubMed DOI

Vlková E., Salmonová H., Bunešová V., Geigerová M., Rada V., Musilová Š. A new medium containing mupirocin, acetic acid, and norfloxacin for the selective cultivation of bifidobacteria. Anaerobe. 2015;34:27–33. doi: 10.1016/j.anaerobe.2015.04.001. PubMed DOI

Caporaso J.G., Lauber C.L., Walters W.A., Berg-Lyons D., Lozupone C.A., Turnbaugh P.J., Fierer N., Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA. 2011;108:4516–4522. doi: 10.1073/pnas.1000080107. PubMed DOI PMC

Milani C., Hevia A., Foroni E., Duranti S., Turroni F., Lugli G.A., Sanchez B., Martin R., Gueimonde M., van Sinderen D. Assessing the fecal microbiota: An optimized ion torrent 16S rRNA gene-based analysis protocol. PLoS ONE. 2013;8:e68739. doi: 10.1371/journal.pone.0068739. PubMed DOI PMC

Mekadim C., Skalnikova H.K., Cizkova J., Cizkova V., Palanova A., Horak V., Mrazek J. Dysbiosis of skin microbiome and gut microbiome in melanoma progression. BMC Microbiol. 2022;22:63. doi: 10.1186/s12866-022-02458-5. PubMed DOI PMC

Bolyen E., Rideout J.R., Dillon M.R., Bokulich N.A., Abnet C.C., Al-Ghalith G.A., Alexander H., Alm E.J., Arumugam M., Asnicar F. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 2019;37:852–857. doi: 10.1038/s41587-019-0209-9. PubMed DOI PMC

Callahan B.J., McMurdie P.J., Rosen M.J., Han A.W., Johnson A.J.A., Holmes S.P. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods. 2016;13:581–583. doi: 10.1038/nmeth.3869. PubMed DOI PMC

Rognes T., Flouri T., Nichols B., Quince C., Mahé F. VSEARCH: A versatile open source tool for metagenomics. PeerJ. 2016;4:e2584. doi: 10.7717/peerj.2584. PubMed DOI PMC

Segata N., Izard J., Waldron L., Gevers D., Miropolsky L., Garrett W.S., Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12:R60. doi: 10.1186/gb-2011-12-6-r60. PubMed DOI PMC

Fouhse J.M., Zijlstra R.T., Willing B.P. The role of gut microbiota in the health and disease of pigs. Anim. Front. 2016;6:30–36. doi: 10.2527/af.2016-0031. DOI

Ríos-Covián D., Ruas-Madiedo P., Margolles A., Gueimonde M., De Los Reyes-gavilán C.G., Salazar N. Intestinal short chain fatty acids and their link with diet and human health. Front. Microbiol. 2016;7:185. PubMed PMC

Mamo G. Anaerobes as sources of bioactive compounds and health promoting tools. Anaerobes Biotechnol. 2016:433–464. doi: 10.1007/10_2016_6. PubMed DOI

Pickard J.M., Zeng M.Y., Caruso R., Núñez G. Gut microbiota: Role in pathogen colonization, immune responses, and inflammatory disease. Immunol. Rev. 2017;279:70–89. doi: 10.1111/imr.12567. PubMed DOI PMC

Wampach L., Heintz-Buschart A., Fritz J.V., Ramiro-Garcia J., Habier J., Herold M., Narayanasamy S., Kaysen A., Hogan A.H., Bindl L. Birth mode is associated with earliest strain-conferred gut microbiome functions and immunostimulatory potential. Nat. Commun. 2018;9:5091. doi: 10.1038/s41467-018-07631-x. PubMed DOI PMC

Chen X., Xu J., Ren E., Su Y., Zhu W. Co-occurrence of early gut colonization in neonatal piglets with microbiota in the maternal and surrounding delivery environments. Anaerobe. 2018;49:30–40. doi: 10.1016/j.anaerobe.2017.12.002. PubMed DOI

Stevens M.P., Kingsley R.A. Salmonella pathogenesis and host-adaptation in farmed animals. Curr. Opin. Microbiol. 2021;63:52–58. doi: 10.1016/j.mib.2021.05.013. PubMed DOI

Bescucci D.M., Moote P.E., Ortega Polo R., Uwiera R.R.E., Inglis G.D. Salmonella enterica serovar Typhimurium temporally modulates the enteric microbiota and host responses to overcome colonization resistance in swine. Appl. Environ. Microbiol. 2020;86:e01569-20. PubMed PMC

Popa G.L., Papa M.I. Salmonella spp. infection-a continuous threat worldwide. Germs. 2021;11:88. doi: 10.18683/germs.2021.1244. PubMed DOI PMC

Marin C., Chinillac M.C., Cerdà-Cuéllar M., Montoro-Dasi L., Sevilla-Navarro S., Ayats T., Marco-Jimenez F., Vega S. Contamination of pig carcass with Salmonella enterica serovar Typhimurium monophasic variant 1, 4 [5], 12:i:-originates mainly in live animals. Sci. Total Environ. 2020;703:134609. doi: 10.1016/j.scitotenv.2019.134609. PubMed DOI

Roasto M., Bonardi S., Mäesaar M., Alban L., Gomes-Neves E., Vieira-Pinto M., Vågsholm I., Elias T., Lindegaard L.L., Blagojevic B. Salmonella enterica prevalence, serotype diversity, antimicrobial resistance and control in the European pork production chain. Trends Food Sci. Technol. 2022 doi: 10.1016/j.tifs.2022.12.007. DOI

Blagojevic B., Nesbakken T., Alvseike O., Vågsholm I., Antic D., Johler S., Houf K., Meemken D., Nastasijevic I., Pinto M.V. Drivers, opportunities, and challenges of the European risk-based meat safety assurance system. Food Control. 2021;124:107870. doi: 10.1016/j.foodcont.2021.107870. DOI

Low C.X., Tan L.T.-H., Ab Mutalib N.-S., Pusparajah P., Goh B.-H., Chan K.-G., Letchumanan V., Lee L.-H. Unveiling the impact of antibiotics and alternative methods for animal husbandry: A review. Antibiotics. 2021;10:578. doi: 10.3390/antibiotics10050578. PubMed DOI PMC

Monger X.C., Gilbert A.-A., Saucier L., Vincent A.T. Antibiotic resistance: From pig to meat. Antibiotics. 2021;10:1209. doi: 10.3390/antibiotics10101209. PubMed DOI PMC

Vt Nair D., Venkitanarayanan K., Kollanoor Johny A. Antibiotic-resistant Salmonella in the food supply and the potential role of antibiotic alternatives for control. Foods. 2018;7:167. doi: 10.3390/foods7100167. PubMed DOI PMC

Kwoji I.D., Aiyegoro O.A., Okpeku M., Adeleke M.A. Multi-strain probiotics: Synergy among isolates enhances biological activities. Biology. 2021;10:322. doi: 10.3390/biology10040322. PubMed DOI PMC

Shokryazdan P., Faseleh Jahromi M., Liang J.B., Ho Y.W. Probiotics: From isolation to application. J. Am. Coll. Nutr. 2017;36:666–676. doi: 10.1080/07315724.2017.1337529. PubMed DOI

Luo Y., Ren W., Smidt H., Wright A.-D.G., Yu B., Schyns G., McCormack U.M., Cowieson A.J., Yu J., He J. Dynamic distribution of gut microbiota in pigs at different growth stages: Composition and contribution. Microbiol. Spectr. 2022;10:e00688-21. doi: 10.1128/spectrum.00688-21. PubMed DOI PMC

Pechar R., Killer J., Mekadim C., Geigerová M., Rada V. Classification of culturable bifidobacterial population from colonic samples of wild pigs (Sus scrofa) based on three molecular genetic methods. Curr. Microbiol. 2017;74:1324–1331. doi: 10.1007/s00284-017-1320-0. PubMed DOI

Pechar R., Killer J., Salmonová H., Geigerová M., Švejstil R., Švec P., Sedláček I., Rada V., Benada O. Bifidobacterium apri sp. nov., a thermophilic actinobacterium isolated from the digestive tract of wild pigs (Sus scrofa) Int. J. Syst. Evol. Microbiol. 2017;67:2349–2356. doi: 10.1099/ijsem.0.001956. PubMed DOI

Crespo-Piazuelo D., Estellé J., Revilla M., Criado-Mesas L., Ramayo-Caldas Y., Óvilo C., Fernández A.I., Ballester M., Folch J.M. Characterization of bacterial microbiota compositions along the intestinal tract in pigs and their interactions and functions. Sci. Rep. 2018;8:12727. doi: 10.1038/s41598-018-30932-6. PubMed DOI PMC

Li X., Højberg O., Canibe N., Jensen B.B. Phylogenetic diversity of cultivable butyrate-producing bacteria from pig gut content and feces. J. Anim. Sci. 2016;94:377–381. doi: 10.2527/jas.2015-9868. PubMed DOI

Larsen N., Thorsen L., Kpikpi E.N., Stuer-Lauridsen B., Cantor M.D., Nielsen B., Brockmann E., Derkx P.M.F., Jespersen L. Characterization of Bacillus spp. strains for use as probiotic additives in pig feed. Appl. Microbiol. Biotechnol. 2014;98:1105–1118. doi: 10.1007/s00253-013-5343-6. PubMed DOI

Álvarez J., Real J.M.F., Guarner F., Gueimonde M., Rodríguez J.M., de Pipaon M.S., Sanz Y. Gut microbes and health. Gastroenterol. Hepatol. 2021;44:519–535. doi: 10.1016/j.gastrohep.2021.01.009. PubMed DOI

Colella M., Charitos I.A., Ballini A., Cafiero C., Topi S., Palmirotta R., Santacroce L. Microbiota revolution: How gut microbes regulate our lives. World J. Gastroenterol. 2023;29:4368. doi: 10.3748/wjg.v29.i28.4368. PubMed DOI PMC

Buddhasiri S., Sukjoi C., Kaewsakhorn T., Nambunmee K., Nakphaichit M., Nitisinprasert S., Thiennimitr P. Anti-inflammatory effect of probiotic Limosilactobacillus reuteri KUB-AC5 against Salmonella infection in a mouse colitis model. Front. Microbiol. 2021;12:716761. PubMed PMC

Lin Y., Xie Z., Li Z., Yuan C., Zhang C., Li Y., Xie K., Wang K. Assessment of the role and mechanism of Bifidobacterium animalis subsp. lactis isolated from neonates’ feces in protecting neonatal rats from Salmonella infection. Microb. Pathog. 2023;174:105935. PubMed

Tanner S.A., Chassard C., Rigozzi E., Lacroix C., Stevens M.J.A. Bifidobacterium thermophilum RBL67 impacts on growth and virulence gene expression of Salmonella enterica subsp. enterica serovar Typhimurium. BMC Microbiol. 2016;16:46. PubMed PMC

Shen J., Zhang J., Zhao Y., Lin Z., Ji L., Ma X. Tibetan pig-derived probiotic Lactobacillus amylovorus SLZX20-1 improved intestinal function via producing enzymes and regulating intestinal microflora. Front. Nutr. 2022;9:846991. doi: 10.3389/fnut.2022.846991. PubMed DOI PMC

Muyyarikkandy M.S., Amalaradjou M.A. Lactobacillus bulgaricus, Lactobacillus rhamnosus and Lactobacillus paracasei attenuate Salmonella enteritidis, Salmonella heidelberg and Salmonella typhimurium colonization and virulence gene expression in vitro. Int. J. Mol. Sci. 2017;18:2381. doi: 10.3390/ijms18112381. PubMed DOI PMC

Myhill L.J., Stolzenbach S., Mejer H., Krych L., Jakobsen S.R., Kot W., Skovgaard K., Canibe N., Nejsum P., Nielsen D.S. Parasite-probiotic interactions in the gut: Bacillus sp. and Enterococcus faecium regulate type-2 inflammatory responses and modify the gut microbiota of pigs during helminth infection. Front. Immunol. 2022;12:793260. doi: 10.3389/fimmu.2021.793260. PubMed DOI PMC

Ailioaie L.M., Litscher G. Probiotics, photobiomodulation, and disease management: Controversies and challenges. Int. J. Mol. Sci. 2021;22:4942. doi: 10.3390/ijms22094942. PubMed DOI PMC

Guo P., Zhang K., Ma X., He P. Clostridium species as probiotics: Potentials and challenges. J. Anim. Sci. Biotechnol. 2020;11:24. doi: 10.1186/s40104-019-0402-1. PubMed DOI PMC

Mun D., Kyoung H., Kong M., Ryu S., Jang K.B., Baek J., Park K., II, Song M., Kim Y. Effects of Bacillus-based probiotics on growth performance, nutrient digestibility, and intestinal health of weaned pigs. J. Anim. Sci. Technol. 2021;63:1314. doi: 10.5187/jast.2021.e109. PubMed DOI PMC

He Y., Jinno C., Kim K., Wu Z., Tan B., Li X., Whelan R., Liu Y. Dietary Bacillus spp. enhanced growth and disease resistance of weaned pigs by modulating intestinal microbiota and systemic immunity. J. Anim. Sci. Biotechnol. 2020;11:101. doi: 10.1186/s40104-020-00498-3. PubMed DOI PMC

Soares M.B., Almada C.N., Pereira E.P.R., Ferreira B.M., Balthazar C.F., Khorshidian N., Rocha R.S., Xavier-Santos D., Cruz A.G., Ranadheera C.S. Sporeforming probiotic bacteria: Characteristics, health benefits, and technological aspects for their applications in foods and beverages. Trends Food Sci. Technol. 2023 doi: 10.1016/j.tifs.2023.06.029. DOI

Todorov S.D., Ivanova I.V., Popov I., Weeks R., Chikindas M.L. Bacillus spore-forming probiotics: Benefits with concerns? Crit. Rev. Microbiol. 2022;48:513–530. doi: 10.1080/1040841X.2021.1983517. PubMed DOI

Deng F., Chen Y., Sun T., Wu Y., Su Y., Liu C., Zhou J., Deng Y., Wen J. Antimicrobial resistance, virulence characteristics and genotypes of Bacillus spp. from probiotic products of diverse origins. Food Res. Int. 2021;139:109949. doi: 10.1016/j.foodres.2020.109949. PubMed DOI

Zhang C., Derrien M., Levenez F., Brazeilles R., Ballal S.A., Kim J., Degivry M.-C., Quéré G., Garault P., van Hylckama Vlieg J.E.T. Ecological robustness of the gut microbiota in response to ingestion of transient food-borne microbes. ISME J. 2016;10:2235–2245. doi: 10.1038/ismej.2016.13. PubMed DOI PMC

Chen D., Jin D., Huang S., Wu J., Xu M., Liu T., Dong W., Liu X., Wang S., Zhong W. Clostridium butyricum, a butyrate-producing probiotic, inhibits intestinal tumor development through modulating Wnt signaling and gut microbiota. Cancer Lett. 2020;469:456–467. doi: 10.1016/j.canlet.2019.11.019. PubMed DOI

Lefevre M., Racedo S.M., Denayrolles M., Ripert G., Desfougères T., Lobach A.R., Simon R., Pélerin F., Jüsten P., Urdaci M.C. Safety assessment of Bacillus subtilis CU1 for use as a probiotic in humans. Regul. Toxicol. Pharmacol. 2017;83:54–65. doi: 10.1016/j.yrtph.2016.11.010. PubMed DOI

Zeng Z., Zhang J., Li Y., Li K., Gong S., Li F., Wang P., Iqbal M., Kulyar M.F.-e.-A., Li J. Probiotic potential of bacillus licheniformis and bacillus pumilus isolated from Tibetan yaks, China. Probiotics Antimicrob. Proteins. 2022;14:579–594. doi: 10.1007/s12602-022-09939-z. PubMed DOI

Altun G.K., Erginkaya Z. Identification and characterization of Bacillus coagulans strains for probiotic activity and safety. LWT. 2021;151:112233. doi: 10.1016/j.lwt.2021.112233. DOI

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...