Abstract
This review provides a comprehensive overview of the current state of probiotic research, covering a wide range of topics, including strain identification, functional characterization, preclinical and clinical evaluations, mechanisms of action, therapeutic applications, manufacturing considerations, and future directions. The screening process for potential probiotics involves phenotypic and genomic analysis to identify strains with health-promoting properties while excluding those with any factor that could be harmful to the host. In vitro assays for evaluating probiotic traits such as acid tolerance, bile metabolism, adhesion properties, and antimicrobial effects are described. The review highlights promising findings from in vivo studies on probiotic mitigation of inflammatory bowel diseases, chemotherapy-induced mucositis, dysbiosis, obesity, diabetes, and bone health, primarily through immunomodulation and modulation of the local microbiota in human and animal models. Clinical studies demonstrating beneficial modulation of metabolic diseases and human central nervous system function are also presented. Manufacturing processes significantly impact the growth, viability, and properties of probiotics, and the composition of the product matrix and supplementation with prebiotics or other strains can modify their effects. The lack of regulatory oversight raises concerns about the quality, safety, and labeling accuracy of commercial probiotics, particularly for vulnerable populations. Advancements in multi-omics approaches, especially probiogenomics, will provide a deeper understanding of the mechanisms behind probiotic functionality, allowing for personalized and targeted probiotic therapies. However, it is crucial to simultaneously focus on improving manufacturing practices, implementing quality control standards, and establishing regulatory oversight to ensure the safety and efficacy of probiotic products in the face of increasing therapeutic applications.
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References
Turroni F (2009) Bifidobacteria: from ecology to genomics. Frontiers in Bioscience Volume:4673. https://doi.org/10.2741/3559
Food and Agriculture Organization, World Health Organization (2002) Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food. London
Morelli L (2000) In vitro selection of probiotic lactobacilli: a critical appraisal. Curr Issues Intest Microbiol 1:59–67
de Melo Pereira GV, de Oliveira CB, Magalhães Júnior AI et al (2018) How to select a probiotic? A review and update of methods and criteria. Biotechnol Adv 36:2060–2076. https://doi.org/10.1016/j.biotechadv.2018.09.003
Morelli L, Capurso L (2012) FAO/WHO guidelines on probiotics. J Clin Gastroenterol 46:S1–S2. https://doi.org/10.1097/MCG.0b013e318269fdd5
Abraham BP, Quigley EMM (2017) Probiotics in inflammatory bowel disease. Gastroenterol Clin North Am 46:769–782. https://doi.org/10.1016/j.gtc.2017.08.003
Le Barz M, Daniel N, Varin TV et al (2019) In vivo screening of multiple bacterial strains identifies Lactobacillus rhamnosus Lb102 and Bifidobacterium animalis ssp. lactis Bf141 as probiotics that improve metabolic disorders in a mouse model of obesity. FASEB J 33:4921–4935. https://doi.org/10.1096/fj.201801672R
Pereira DIA, Gibson GR (2002) Cholesterol assimilation by lactic acid bacteria and bifidobacteria isolated from the human gut. Appl Environ Microbiol 68:4689–4693. https://doi.org/10.1128/AEM.68.9.4689-4693.2002
Lin M-Y, Chang F-J (2000) Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Dig Dis Sci 45:1617–1622. https://doi.org/10.1023/A:1005577330695
Thirabunyanon M, Boonprasom P, Niamsup P (2009) Probiotic potential of lactic acid bacteria isolated from fermented dairy milks on antiproliferation of colon cancer cells. Biotechnol Lett 31:571–576. https://doi.org/10.1007/s10529-008-9902-3
Kim S-K, Guevarra RB, Kim Y-T et al (2019) Role of probiotics in human gut microbiome-associated diseases. J Microbiol Biotechnol 29:1335–1340. https://doi.org/10.4014/jmb.1906.06064
Kiousi DE, Rathosi M, Tsifintaris M et al (2021) Pro-biomics: omics technologies to unravel the role of probiotics in health and disease. Adv Nutr 12:1802–1820. https://doi.org/10.1093/advances/nmab014
Ouwehand AC, Kirjavainen PV, Shortt C, Salminen S (1999) Probiotics: mechanisms and established effects. Int Dairy J 9:43–52. https://doi.org/10.1016/S0958-6946(99)00043-6
Borriello SP, Hammes WP, Holzapfel W et al (2003) Safety of probiotics that contain lactobacilli or bifidobacteria. Clin Infect Dis 36:775–780. https://doi.org/10.1086/368080
Riaz Rajoka MS, Mehwish HM, Siddiq M et al (2017) Identification, characterization, and probiotic potential of Lactobacillus rhamnosus isolated from human milk. LWT 84:271–280. https://doi.org/10.1016/j.lwt.2017.05.055
Jara S, Sánchez M, Vera R et al (2011) The inhibitory activity of Lactobacillus spp. isolated from breast milk on gastrointestinal pathogenic bacteria of nosocomial origin. Anaerobe 17:474–477. https://doi.org/10.1016/j.anaerobe.2011.07.008
Olivares M, Diaz-Ropero MP, Martin R et al (2006) Antimicrobial potential of four Lactobacillus strains isolated from breast milk. J Appl Microbiol 101:72–79. https://doi.org/10.1111/j.1365-2672.2006.02981.x
Damaceno QS, Gallotti B, Reis IMM et al (2021) Isolation and identification of potential probiotic bacteria from human milk. Probiotics Antimicrob Proteins. https://doi.org/10.1007/s12602-021-09866-5
Lyons KE, Ryan CA, Dempsey EM et al (2020) Breast milk, a source of beneficial microbes and associated benefits for infant health. Nutrients 12:1039. https://doi.org/10.3390/nu12041039
Shokryazdan P, Sieo CC, Kalavathy R et al (2014) Probiotic potential of Lactobacillus strains with antimicrobial activity against some human pathogenic strains. Biomed Res Int 2014:1–16. https://doi.org/10.1155/2014/927268
Martı́n R, Langa S, Reviriego C et al (2004) The commensal microflora of human milk: new perspectives for food bacteriotherapy and probiotics Trends Food Sci Technol 15 121 127 https://doi.org/10.1016/j.tifs.2003.09.010
Shokryazdan P, Faseleh Jahromi M, Liang JB, Ho YW (2017) Probiotics: from isolation to application. J Am Coll Nutr 36:666–676. https://doi.org/10.1080/07315724.2017.1337529
Reuben RC, Roy PC, Sarkar SL et al (2020) Characterization and evaluation of lactic acid bacteria from indigenous raw milk for potential probiotic properties. J Dairy Sci 103:1223–1237. https://doi.org/10.3168/jds.2019-17092
Naqqash T, Wazir N, Aslam K et al (2022) First report on the probiotic potential of Mammaliicoccus sciuri isolated from raw goat milk. Biosci Microbiota Food Health 41:2021–022. https://doi.org/10.12938/bmfh.2021-022
Coelho-Rocha ND, de Jesus LCL, Barroso FAL et al (2023) Evaluation of probiotic properties of novel Brazilian Lactiplantibacillus plantarum strains. Probiotics Antimicrob Proteins 15:160–174. https://doi.org/10.1007/s12602-022-09978-6
Dehghani Champiri I, Bamzadeh Z, Rahimi E, Rouhi L (2023) Lacticaseibacillus paracasei LB12, a potential probiotic isolated from traditional Iranian fermented milk (Doogh). Curr Microbiol 80:333. https://doi.org/10.1007/s00284-023-03376-z
Mokoena MP, Mutanda T, Olaniran AO (2016) Perspectives on the probiotic potential of lactic acid bacteria from African traditional fermented foods and beverages. Food Nutr Res 60:29630. https://doi.org/10.3402/fnr.v60.29630
Tchamani Piame L, Kaktcham PM, Foko Kouam EM et al (2022) Technological characterisation and probiotic traits of yeasts isolated from Sha’a, a Cameroonian maize-based traditional fermented beverage. Heliyon 8:e10850. https://doi.org/10.1016/j.heliyon.2022.e10850
Duangjitch Y, Kantachote D, Ongsakul M et al (2008) Selection of probiotic lactic acid bacteria isolated from fermented plant beverages. Pak J Biol Sci 11:652–655. https://doi.org/10.3923/pjbs.2008.652.655
Pumriw S, Luang-In V, Samappito W (2021) Screening of probiotic lactic acid bacteria isolated from fermented Pak-Sian for use as a starter culture. Curr Microbiol 78:2695–2707. https://doi.org/10.1007/s00284-021-02521-w
Azat R, Liu Y, Li W et al (2016) Probiotic properties of lactic acid bacteria isolated from traditionally fermented Xinjiang cheese. Journal of Zhejiang University-SCIENCE B 17:597–609. https://doi.org/10.1631/jzus.B1500250
Talib N, Mohamad NE, Yeap SK, Hussin Y, Aziz MN et al (2019) Isolation and characterization of Lactobacillus spp. from kefir samples in Malaysia. Molecules 24:2606. https://doi.org/10.3390/molecules24142606
Ochman H, Lerat E, Daubin V (2005) Examining bacterial species under the specter of gene transfer and exchange. Proc Natl Acad Sci 102:6595–6599. https://doi.org/10.1073/pnas.0502035102
Miller JM, Rhoden DL (1991) Preliminary evaluation of Biolog, a carbon source utilization method for bacterial identification. J Clin Microbiol 29:1143–1147. https://doi.org/10.1128/jcm.29.6.1143-1147.1991
Aldridge C, Jones PW, Gibson S et al (1977) Automated microbiological detection/identification system. J Clin Microbiol 6:406–413. https://doi.org/10.1128/jcm.6.4.406-413.1977
Dingle TC, Butler-Wu SM (2013) MALDI-TOF mass spectrometry for microorganism identification. Clin Lab Med 33:589–609. https://doi.org/10.1016/j.cll.2013.03.001
van Veen SQ, Claas ECJ, Kuijper EJ (2010) High-throughput Identification of bacteria and yeast by matrix-assisted laser desorption ionization-time of flight mass spectrometry in conventional medical microbiology laboratories. J Clin Microbiol 48:900–907. https://doi.org/10.1128/JCM.02071-09
Bille E, Dauphin B, Leto J et al (2012) MALDI-TOF MS Andromas strategy for the routine identification of bacteria, mycobacteria, yeasts, Aspergillus spp. and positive blood cultures. Clin Microbiol Infect 18:1117–1125. https://doi.org/10.1111/j.1469-0691.2011.03688.x
Sogawa K, Watanabe M, Sato K et al (2011) Use of the MALDI BioTyper system with MALDI–TOF mass spectrometry for rapid identification of microorganisms. Anal Bioanal Chem 400:1905–1911. https://doi.org/10.1007/s00216-011-4877-7
Angelakis E, Million M, Henry M, Raoult D (2011) Rapid and accurate bacterial identification in probiotics and yoghurts by MALDI-TOF mass spectrometry. J Food Sci 76:M568–M572. https://doi.org/10.1111/j.1750-3841.2011.02369.x
Kizerwetter-Swida M, Binek M (2005) Selection of potentially probiotic Lactobacillus strains towards their inhibitory activity against poultry enteropathogenic bacteria. Pol J Microbiol 54:287–294
Petti CA, Polage CR, Schreckenberger P (2005) The role of 16S rRNA gene sequencing in identification of microorganisms misidentified by conventional methods. J Clin Microbiol 43:6123–6125. https://doi.org/10.1128/JCM.43.12.6123-6125.2005
Maiden MCJ, Bygraves JA, Feil E et al (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci 95:3140–3145. https://doi.org/10.1073/pnas.95.6.3140
Setubal JC (2021) Metagenome-assembled genomes: concepts, analogies, and challenges. Biophys Rev 13:905–909. https://doi.org/10.1007/s12551-021-00865-y
Johnson JS, Spakowicz DJ, Hong B-Y et al (2019) Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat Commun 10:5029. https://doi.org/10.1038/s41467-019-13036-1
Siekaniec G, Roux E, Lemane T et al (2021) Identification of isolated or mixed strains from long reads: a challenge met on Streptococcus thermophilus using a MinION sequencer. Microb Genom 7:. https://doi.org/10.1099/mgen.0.000654
Hill C, Guarner F, Reid G et al (2014) The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11:506–514. https://doi.org/10.1038/nrgastro.2014.66
De Filippis F, Esposito A, Ercolini D (2022) Outlook on next-generation probiotics from the human gut. Cell Mol Life Sci 79:76. https://doi.org/10.1007/s00018-021-04080-6
FDA (2016) Early clinical trials with live biotherapeutic products: chemistry, manufacturing, and control information. Rockville
Lugli GA, Longhi G, Alessandri G et al (2022) The probiotic identity card: a novel “probiogenomics” approach to investigate probiotic supplements. Front Microbiol 12:. https://doi.org/10.3389/fmicb.2021.790881
Castro-López C, García HS, Guadalupe Martínez-Ávila GC et al (2021) Genomics-based approaches to identify and predict the health-promoting and safety activities of promising probiotic strains – a probiogenomics review. Trends Food Sci Technol 108:148–163. https://doi.org/10.1016/j.tifs.2020.12.017
Ventura M, Turroni F, van Sinderen D (2012) Probiogenomics as a tool to obtain genetic insights into adaptation of probiotic bacteria to the human gut. Bioengineered 3:73–79. https://doi.org/10.4161/bbug.18540
Ventura M, O’Flaherty S, Claesson MJ et al (2009) Genome-scale analyses of health-promoting bacteria: probiogenomics. Nat Rev Microbiol 7:61–71. https://doi.org/10.1038/nrmicro2047
Carvalho RDO, Guédon E, Aburjaile FF, Azevedo V (2022) Editorial: probiogenomics of classic and next-generation probiotics. Front Microbiol 13:. https://doi.org/10.3389/fmicb.2022.982642
Chin C-S, Alexander DH, Marks P et al (2013) Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 10:563–569. https://doi.org/10.1038/nmeth.2474
Salvetti E, O’Toole PW (2017) The genomic basis of lactobacilli as health-promoting organisms. Microbiol Spectr 5:. https://doi.org/10.1128/microbiolspec.BAD-0011-2016
Gueimonde M, Collado MC (2012) Metagenomics and probiotics. Clin Microbiol Infect 18:32–34. https://doi.org/10.1111/j.1469-0691.2012.03873.x
Bottacini F, van Sinderen D, Ventura M (2017) Omics of bifidobacteria: research and insights into their health-promoting activities. Biochemical Journal 474:4137–4152. https://doi.org/10.1042/BCJ20160756
Zmora N, Zilberman-Schapira G, Suez J et al (2018) Personalized gut mucosal colonization resistance to empiric probiotics is associated with unique host and microbiome features. Cell 174:1388-1405.e21. https://doi.org/10.1016/j.cell.2018.08.041
Johnson BR, Klaenhammer TR (2014) Impact of genomics on the field of probiotic research: historical perspectives to modern paradigms. Antonie Van Leeuwenhoek 106:141–156. https://doi.org/10.1007/s10482-014-0171-y
Garrigues C, Johansen E, Crittenden R (2013) Pangenomics – an avenue to improved industrial starter cultures and probiotics. Curr Opin Biotechnol 24:187–191. https://doi.org/10.1016/j.copbio.2012.08.009
Remus DM, Kleerebezem M, Bron PA (2011) An intimate tête-à-tête — how probiotic lactobacilli communicate with the host. Eur J Pharmacol 668:S33–S42. https://doi.org/10.1016/j.ejphar.2011.07.012
Hao Q, Lu Z, Dong BR et al (2011) Probiotics for preventing acute upper respiratory tract infections. In: Dong BR (ed) Cochrane Database of Systematic Reviews. John Wiley & Sons, Ltd, Chichester, UK
Ruiz L, Hidalgo C, Blanco-Míguez A et al (2016) Tackling probiotic and gut microbiota functionality through proteomics. J Proteomics 147:28–39. https://doi.org/10.1016/j.jprot.2016.03.023
Botthoulath V, Upaichit A, Thumarat U (2018) Identification and in vitro assessment of potential probiotic characteristics and antibacterial effects of Lactobacillus plantarum subsp. plantarum SKI19, a bacteriocinogenic strain isolated from Thai fermented pork sausage. J Food Sci Technol 55:2774–2785. https://doi.org/10.1007/s13197-018-3201-3
Kazou M, Alexandraki V, Blom J et al (2018) Comparative genomics of Lactobacillus acidipiscis ACA-DC 1533 isolated from traditional Greek kopanisti cheese against species within the Lactobacillus salivarius clade. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.01244
Fontana A, Falasconi I, Molinari P et al (2019) Genomic comparison of Lactobacillus helveticus strains highlights probiotic potential. Front Microbiol 10:. https://doi.org/10.3389/fmicb.2019.01380
Sanders ME, Akkermans LMA, Haller D et al (2010) Safety assessment of probiotics for human use. Gut Microbes 1:164–185. https://doi.org/10.4161/gmic.1.3.12127
Sorokulova IB, Pinchuk IV, Denayrolles M et al (2008) The safety of two Bacillus probiotic strains for human use. Dig Dis Sci 53:954–963. https://doi.org/10.1007/s10620-007-9959-1
Collins JK, Thornton G, Sullivan GO (1998) Selection of probiotic strains for human applications. Int Dairy J 8:487–490. https://doi.org/10.1016/S0958-6946(98)00073-9
EFSA (2005) Opinion of the scientific committee on a request from EFSA related to a generic approach to the safety assessment by EFSA of microorganisms used in food/feed and the production of food/feed additives. EFSA J 3:226. https://doi.org/10.2903/j.efsa.2005.226
Dunne C, O’Mahony L, Murphy L et al (2001) In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. Am J Clin Nutr 73:386s–392s. https://doi.org/10.1093/ajcn/73.2.386s
Pradhan D, Mallappa RH, Grover S (2020) Comprehensive approaches for assessing the safety of probiotic bacteria. Food Control 108:106872. https://doi.org/10.1016/j.foodcont.2019.106872
Sharma A, Lee S, Park Y-S (2020) Molecular typing tools for identifying and characterizing lactic acid bacteria: a review. Food Sci Biotechnol 29:1301–1318. https://doi.org/10.1007/s10068-020-00802-x
Li T, Teng D, Mao R et al (2020) A critical review of antibiotic resistance in probiotic bacteria. Food Res Int 136:109571. https://doi.org/10.1016/j.foodres.2020.109571
Wiles TJ, Guillemin K (2019) The other side of the coin: what beneficial microbes can teach us about pathogenic potential. J Mol Biol 431:2946–2956. https://doi.org/10.1016/j.jmb.2019.05.001
Sanders ME, Merenstein DJ, Ouwehand AC et al (2016) Probiotic use in at-risk populations. J Am Pharm Assoc 56:680–686. https://doi.org/10.1016/j.japh.2016.07.001
Koutsoumanis K, Allende A, Alvarez‐Ordóñez A et al (2021) Update of the list of QPS‐recommended biological agents intentionally added to food or feed as notified to EFSA 14: suitability of taxonomic units notified to EFSA until March 2021. EFSA Journal 19:. https://doi.org/10.2903/j.efsa.2021.6689
Abriouel H, Lerma LL, Casado Muñoz M del C et al (2015) The controversial nature of the Weissella genus: technological and functional aspects versus whole genome analysis-based pathogenic potential for their application in food and health. Front Microbiol 6:. https://doi.org/10.3389/fmicb.2015.01197
Li B, Zhan M, Evivie SE et al (2018) Evaluating the safety of potential probiotic Enterococcus durans KLDS6.0930 using whole genome sequencing and oral toxicity study. Front Microbiol 9:. https://doi.org/10.3389/fmicb.2018.01943
Cosentino S, Voldby Larsen M, Møller Aarestrup F, Lund O (2013) PathogenFinder - distinguishing friend from foe using bacterial whole genome sequence data. PLoS ONE 8:e77302. https://doi.org/10.1371/journal.pone.0077302
Joensen KG, Scheutz F, Lund O et al (2014) Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol 52:1501–1510. https://doi.org/10.1128/JCM.03617-13
Kim M, Ku S, Kim S et al (2018) Safety evaluations of Bifidobacterium bifidum BGN4 and Bifidobacterium longum BORI. Int J Mol Sci 19:1422. https://doi.org/10.3390/ijms19051422
Leplae R, Lima-Mendez G, Toussaint A (2010) ACLAME: a classification of mobile genetic elements, update 2010. Nucleic Acids Res 38:D57–D61. https://doi.org/10.1093/nar/gkp938
Mahillon J, Chandler M (1998) Insertion sequences. microbiology and molecular biology reviews 62:725–774. https://doi.org/10.1128/MMBR.62.3.725-774.1998
Jarocki P, Komoń-Janczara E, Podleśny M et al (2019) Genomic and proteomic characterization of bacteriophage BH1 spontaneously released from probiotic Lactobacillus rhamnosus Pen. Viruses 11:1163. https://doi.org/10.3390/v11121163
Liu C-J, Wang R, Gong F-M et al (2015) Complete genome sequences and comparative genome analysis of Lactobacillus plantarum strain 5–2 isolated from fermented soybean. Genomics 106:404–411. https://doi.org/10.1016/j.ygeno.2015.07.007
Philippe H, Douady CJ (2003) Horizontal gene transfer and phylogenetics. Curr Opin Microbiol 6:498–505. https://doi.org/10.1016/j.mib.2003.09.008
Abriouel H, Pérez Montoro B, Casado Muñoz MDC et al (2017) In silico genomic insights into aspects of food safety and defense mechanisms of a potentially probiotic Lactobacillus pentosus MP-10 isolated from brines of naturally fermented Aloreña green table olives. PLoS One 12:e0176801. https://doi.org/10.1371/journal.pone.0176801
Tarrah A, Pakroo S, Corich V, Giacomini A (2020) Whole-genome sequence and comparative genome analysis of Lactobacillus paracasei DTA93, a promising probiotic lactic acid bacterium. Arch Microbiol 202:1997–2003. https://doi.org/10.1007/s00203-020-01883-2
Pei Z, Sadiq FA, Han X et al (2021) Comprehensive scanning of prophages in Lactobacillus : distribution, diversity, antibiotic resistance genes, and linkages with CRISPR-Cas systems. mSystems 6:. https://doi.org/10.1128/mSystems.01211-20
Pei Z, Sadiq FA, Han X et al (2020) Identification, characterization, and phylogenetic analysis of eight new inducible prophages in Lactobacillus. Virus Res 286:198003. https://doi.org/10.1016/j.virusres.2020.198003
Gueimonde M, Sánchez B, G. de los Reyes-Gavilán C, Margolles A (2013) Antibiotic resistance in probiotic bacteria. Front Microbiol 4:. https://doi.org/10.3389/fmicb.2013.00202
Ouoba LII, Lei V, Jensen LB (2008) Resistance of potential probiotic lactic acid bacteria and bifidobacteria of African and European origin to antimicrobials: determination and transferability of the resistance genes to other bacteria. Int J Food Microbiol 121:217–224. https://doi.org/10.1016/j.ijfoodmicro.2007.11.018
Ammor MS, Flórez AB, van Hoek AHAM et al (2008) Molecular characterization of intrinsic and acquired antibiotic resistance in lactic acid bacteria and bifidobacteria. Microb Physiol 14:6–15. https://doi.org/10.1159/000106077
Bennedsen M, Stuer-Lauridsen B, Danielsen M, Johansen E (2011) Screening for antimicrobial resistance genes and virulence factors via genome sequencing. Appl Environ Microbiol 77:2785–2787. https://doi.org/10.1128/AEM.02493-10
EFSA (2012) Guidance on the assessment of bacterial susceptibility to antimicrobials of human and veterinary importance. EFSA Journal 10:. https://doi.org/10.2903/j.efsa.2012.2740
EFSA Panel on Additives and Products or Substances used in Animal Feed (FEEDAP), Rychen G, Aquilina G et al (2018) Guidance on the characterisation of microorganisms used as feed additives or as production organisms. EFSA J 16:e05206. https://doi.org/10.2903/j.efsa.2018.5206
McInnes RS, McCallum GE, Lamberte LE, van Schaik W (2020) Horizontal transfer of antibiotic resistance genes in the human gut microbiome. Curr Opin Microbiol 53:35–43. https://doi.org/10.1016/j.mib.2020.02.002
Ruiz-Capillas C, Herrero A (2019) Impact of biogenic amines on food quality and safety. Foods 8:62. https://doi.org/10.3390/foods8020062
Wójcik W, Łukasiewicz M, Puppel K (2021) Biogenic amines: formation, action and toxicity – a review. J Sci Food Agric 101:2634–2640. https://doi.org/10.1002/jsfa.10928
Bover-Cid S, Holzapfel WH (1999) Improved screening procedure for biogenic amine production by lactic acid bacteria. Int J Food Microbiol 53:33–41. https://doi.org/10.1016/S0168-1605(99)00152-X
Li B, Jin D, Etareri Evivie S et al (2017) Safety assessment of Lactobacillus helveticus KLDS1.8701 based on whole genome sequencing and oral toxicity studies. Toxins (Basel) 9:301. https://doi.org/10.3390/toxins9100301
Ku S, Yang S, Lee HH et al (2020) Biosafety assessment of Bifidobacterium animalis subsp. lactis AD011 used for human consumption as a probiotic microorganism. Food Control 117:106985. https://doi.org/10.1016/j.foodcont.2019.106985
Saroj DB, Gupta AK (2020) Genome based safety assessment for Bacillus coagulans strain LBSC (DSM 17654) for probiotic application. Int J Food Microbiol 318:108523. https://doi.org/10.1016/j.ijfoodmicro.2020.108523
Grondin JA, Kwon YH, Far PM et al (2020) Mucins in intestinal mucosal defense and inflammation: learning from clinical and experimental studies. Front Immunol 11:. https://doi.org/10.3389/fimmu.2020.02054
Tailford LE, Crost EH, Kavanaugh D, Juge N (2015) Mucin glycan foraging in the human gut microbiome. Front Genet 6:. https://doi.org/10.3389/fgene.2015.00081
Pechar R, Rada V, Parafati L et al (2014) Mupirocin-mucin agar for selective enumeration of Bifidobacterium bifidum. Int J Food Microbiol 191:32–35. https://doi.org/10.1016/j.ijfoodmicro.2014.08.032
Koutsoumanis K, Allende A, Alvarez‐Ordóñez A et al (2020) Scientific opinion on the update of the list of QPS‐recommended biological agents intentionally added to food or feed as notified to EFSA (2017–2019). EFSA Journal 18:. https://doi.org/10.2903/j.efsa.2020.5966
Koutsoumanis K, Allende A, Alvarez‐Ordóñez A et al (2021) Update of the list of QPS‐recommended biological agents intentionally added to food or feed as notified to EFSA 13: suitability of taxonomic units notified to EFSA until September 2020. EFSA Journal 19:. https://doi.org/10.2903/j.efsa.2021.6377
Flint HJ, Scott KP, Duncan SH et al (2012) Microbial degradation of complex carbohydrates in the gut. Gut Microbes 3:289–306. https://doi.org/10.4161/gmic.19897
C Slattery PD Cotter W. O’Toole P 2019 Analysis of health benefits conferred by Lactobacillus species from kefir Nutrients 11 1252 https://doi.org/10.3390/nu11061252
Kim J, Muhammad N, Jhun BH, Yoo J-W (2016) Probiotic delivery systems: a brief overview. J Pharm Investig 46:377–386. https://doi.org/10.1007/s40005-016-0259-7
Abushelaibi A, Al-Mahadin S, El-Tarabily K et al (2017) Characterization of potential probiotic lactic acid bacteria isolated from camel milk. LWT Food Sci Technol 79:316–325. https://doi.org/10.1016/j.lwt.2017.01.041
Ruiz-Moyano S, Martín A, Benito MJ et al (2008) Screening of lactic acid bacteria and bifidobacteria for potential probiotic use in Iberian dry fermented sausages. Meat Sci 80:715–721. https://doi.org/10.1016/j.meatsci.2008.03.011
Kailasapathy K, Chin J (2000) Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol Cell Biol 78:80–88. https://doi.org/10.1046/j.1440-1711.2000.00886.x
Kim EJ, Kang YI, Bang T Il et al (2016) Characterization of Lactobacillus reuteri BCLR-42 and Lactobacillus plantarum BCLP-51 as novel dog probiotics with innate immune enhancing properties. Korean J Vet Res 56:75–84. https://doi.org/10.14405/kjvr.2016.56.2.75
Vera-Pingitore E, Jimenez ME, Dallagnol A et al (2016) Screening and characterization of potential probiotic and starter bacteria for plant fermentations. LWT Food Sci Technol 71:288–294. https://doi.org/10.1016/j.lwt.2016.03.046
Ruiz-Moyano S, Gonçalves dos Santos MTP, Galván AI et al (2019) Screening of autochthonous lactic acid bacteria strains from artisanal soft cheese: probiotic characteristics and prebiotic metabolism. LWT 114:108388. https://doi.org/10.1016/j.lwt.2019.108388
Lee J, Yang W, Hostetler A et al (2016) Characterization of the anti-inflammatory Lactobacillus reuteri BM36301 and its probiotic benefits on aged mice. BMC Microbiol 16:69. https://doi.org/10.1186/s12866-016-0686-7
Song M, Yun B, Moon J-H et al (2015) Characterization of selected Lactobacillus strains for use as probiotics. Korean J Food Sci Anim Resour 35:551–556. https://doi.org/10.5851/kosfa.2015.35.4.551
Sanz Y (2007) Ecological and functional implications of the acid-adaptation ability of Bifidobacterium: a way of selecting improved probiotic strains. Int Dairy J 17:1284–1289. https://doi.org/10.1016/j.idairyj.2007.01.016
Rabah H, Ménard O, Gaucher F et al (2018) Cheese matrix protects the immunomodulatory surface protein SlpB of Propionibacterium freudenreichii during in vitro digestion. Food Res Int 106:712–721. https://doi.org/10.1016/j.foodres.2018.01.035
Minekus M, Alminger M, Alvito P et al (2014) A standardised static in vitro digestion method suitable for food – an international consensus. Food Funct 5:1113–1124. https://doi.org/10.1039/C3FO60702J
Ménard O, Cattenoz T, Guillemin H et al (2014) Validation of a new in vitro dynamic system to simulate infant digestion. Food Chem 145:1039–1045. https://doi.org/10.1016/j.foodchem.2013.09.036
da Silva TF, de Glória R, A, de Sousa TJ et al (2023) Comprehensive probiogenomics analysis of the commensal Escherichia coli CEC15 as a potential probiotic strain. BMC Microbiol 23:364. https://doi.org/10.1186/s12866-023-03112-4
Brodkorb A, Egger L, Alminger M et al (2019) INFOGEST static in vitro simulation of gastrointestinal food digestion. Nat Protoc 14:991–1014. https://doi.org/10.1038/s41596-018-0119-1
Abuhelwa AY, Williams DB, Upton RN, Foster DJR (2017) Food, gastrointestinal pH, and models of oral drug absorption. Eur J Pharm Biopharm 112:234–248. https://doi.org/10.1016/j.ejpb.2016.11.034
Jia W, Xie G, Jia W (2018) Bile acid–microbiota crosstalk in gastrointestinal inflammation and carcinogenesis. Nat Rev Gastroenterol Hepatol 15:111–128. https://doi.org/10.1038/nrgastro.2017.119
Prete R, Long SL, Gallardo AL et al (2020) Beneficial bile acid metabolism from Lactobacillus plantarum of food origin. Sci Rep 10:1165. https://doi.org/10.1038/s41598-020-58069-5
Bustos AY, Font de Valdez G, Fadda S, Taranto MP (2018) New insights into bacterial bile resistance mechanisms: the role of bile salt hydrolase and its impact on human health. Food Res Int 112:250–262. https://doi.org/10.1016/j.foodres.2018.06.035
Sung JY, Shaffer EA, Costerton JW (1993) Antibacterial activity of bile salts against common biliary pathogens. Dig Dis Sci 38:2104–2112. https://doi.org/10.1007/BF01297092
Floch MH, Binder HJ, Filburn B, Gershengoren W (1972) The effect of bile acids on intestinal microflora. Am J Clin Nutr 25:1418–1426. https://doi.org/10.1093/ajcn/25.12.1418
Corzo G, Gilliland SE (1999) Bile salt hydrolase activity of three strains of Lactobacillus acidophilus. J Dairy Sci 82:472–480. https://doi.org/10.3168/jds.S0022-0302(99)75256-2
Klaver FA, van der Meer R (1993) The assumed assimilation of cholesterol by Lactobacilli and Bifidobacterium bifidum is due to their bile salt-deconjugating activity. Appl Environ Microbiol 59:1120–1124. https://doi.org/10.1128/aem.59.4.1120-1124.1993
Kishida T, Taguchi F, Feng L et al (1997) Analysis of bile acids in colon residual liquid or fecal material in patients with colorectal neoplasia and control subjects. J Gastroenterol 32:306–311. https://doi.org/10.1007/BF02934485
Bin Masalam MS, Bahieldin A, Alharbi MG et al (2018) Isolation, molecular characterization and probiotic potential of lactic acid bacteria in Saudi raw and fermented milk. Evidence-Based Complementary and Alternative Medicine 2018:1–12. https://doi.org/10.1155/2018/7970463
Begley M, Hill C, Gahan CGM (2006) Bile salt hydrolase activity in probiotics. Appl Environ Microbiol 72:1729–1738. https://doi.org/10.1128/AEM.72.3.1729-1738.2006
Horáčková Š, Plocková M, Demnerová K (2018) Importance of microbial defence systems to bile salts and mechanisms of serum cholesterol reduction. Biotechnol Adv 36:682–690. https://doi.org/10.1016/j.biotechadv.2017.12.005
Liong MT, Shah NP (2005) Acid and bile tolerance and cholesterol removal ability of lactobacilli strains. J Dairy Sci 88:55–66. https://doi.org/10.3168/jds.S0022-0302(05)72662-X
Saravanan C, Gopu V, Shetty PH (2015) Diversity and functional characterization of microflora isolated from traditional fermented food idli. J Food Sci Technol 52:7425–7432. https://doi.org/10.1007/s13197-015-1791-6
Kumari A, Angmo K, Monika BTC (2016) Probiotic attributes of indigenous Lactobacillus spp. isolated from traditional fermented foods and beverages of north-western Himalayas using in vitro screening and principal component analysis. J Food Sci Technol 53:2463–2475. https://doi.org/10.1007/s13197-016-2231-y
Awasti N, Tomar SK, Pophaly SD et al (2016) Probiotic and functional characterization of bifidobacteria of Indian human origin. J Appl Microbiol 120:1021–1032. https://doi.org/10.1111/jam.13086
Lee Y-K, Salminen S (1995) The coming of age of probiotics. Trends Food Sci Technol 6:241–245. https://doi.org/10.1016/S0924-2244(00)89085-8
Saxelin M (1997) Lactobacillus GG—a human probiotic strain with thorough clinical documentation. Food Rev Intl 13:293–313. https://doi.org/10.1080/87559129709541107
Ouwehand AC, Isolauri E, Kirjavainen PV, Salminen SJ (1999) Adhesion of four Bifidobacterium strains to human intestinal mucus from subjects in different age groups. FEMS Microbiol Lett 172:61–64. https://doi.org/10.1111/j.1574-6968.1999.tb13450.x
Haddaji N, Mahdhi AK, Krifi B et al (2015) Change in cell surface properties of Lactobacillus casei under heat shock treatment. FEMS Microbiol Lett 362:. https://doi.org/10.1093/femsle/fnv047
Van Tassell ML, Miller MJ (2011) Lactobacillus adhesion to mucus. Nutrients 3:613–636. https://doi.org/10.3390/nu3050613
Piepenbrink KH, Sundberg EJ (2016) Motility and adhesion through type IV pili in Gram-positive bacteria. Biochem Soc Trans 44:1659–1666. https://doi.org/10.1042/BST20160221
Hymes JP, Johnson BR, Barrangou R, Klaenhammer TR (2016) Functional analysis of an S-layer-associated fibronectin-binding protein in Lactobacillus acidophilus NCFM. Appl Environ Microbiol 82:2676–2685. https://doi.org/10.1128/AEM.00024-16
Rahbar Saadat Y, Yari Khosroushahi A, Pourghassem Gargari B (2019) A comprehensive review of anticancer, immunomodulatory and health beneficial effects of the lactic acid bacteria exopolysaccharides. Carbohydr Polym 217:79–89. https://doi.org/10.1016/j.carbpol.2019.04.025
Ayyash MM, Abdalla AK, AlKalbani NS et al (2021) Characterization of new probiotics from dairy and nondairy products—insights into acid tolerance, bile metabolism and tolerance, and adhesion capability. J Dairy Sci 104:8363–8379. https://doi.org/10.3168/jds.2021-20398
Papadimitriou K, Zoumpopoulou G, Foligné B et al (2015) Discovering probiotic microorganisms: in vitro, in vivo, genetic and omics approaches. Front Microbiol 6:. https://doi.org/10.3389/fmicb.2015.00058
Reid G, Burton J (2002) Use of Lactobacillus to prevent infection by pathogenic bacteria. Microbes Infect 4:319–324. https://doi.org/10.1016/S1286-4579(02)01544-7
Collins JW, La Ragione RM, Woodward MJ, Searle LEJ (2009) Application of prebiotics and probiotics in livestock. Prebiotics and probiotics science and technology. Springer, New York, New York, NY, pp 1123–1192
Aroutcheva A, Gariti D, Simon M et al (2001) Defense factors of vaginal lactobacilli. Am J Obstet Gynecol 185:375–379. https://doi.org/10.1067/mob.2001.115867
Lindgren SE, Dobrogosz WJ (1990) Antagonistic activities of lactic acid bacteria in food and feed fermentations. FEMS Microbiol Lett 87:149–164. https://doi.org/10.1111/j.1574-6968.1990.tb04885.x
Dicks LMT, Heunis TDJ, van Staden DA et al (2011) Medical and personal care applications of bacteriocins produced by lactic acid bacteria. Prokaryotic antimicrobial peptides. Springer, New York, New York, NY, pp 391–421
Rea MC, Ross RP, Cotter PD, Hill C (2011) Classification of bacteriocins from gram-positive bacteria. Prokaryotic antimicrobial peptides. Springer, New York, New York, NY, pp 29–53
Haller D, Blum S, Bode C et al (2000) Activation of human peripheral blood mononuclear cells by nonpathogenic bacteria in vitro: evidence of NK Cells as primary targets. Infect Immun 68:752–759. https://doi.org/10.1128/IAI.68.2.752-759.2000
Aattouri N, Lemonnier D (1997) Production of interferon induced by Streptococcus thermophilus: role of CD4+ and CD8+ lymphocytes. J Nutr Biochem 8:25–31. https://doi.org/10.1016/S0955-2863(96)00147-7
Cross M, Mortensen R, Kudsk J, Gill H (2002) Dietary intake of Lactobacillus rhamnosus HN001 enhances production of both Th1 and Th2 cytokines in antigen-primed mice. Med Microbiol Immunol 191:49–53. https://doi.org/10.1007/s00430-002-0112-7
Cross ML, Stevenson LM, Gill HS (2001) Anti-allergy properties of fermented foods: an important immunoregulatory mechanism of lactic acid bacteria? Int Immunopharmacol 1:891–901. https://doi.org/10.1016/S1567-5769(01)00025-X
Johansson MA, Björkander S, Mata Forsberg M et al (2016) Probiotic lactobacilli modulate Staphylococcus aureus-induced activation of conventional and unconventional T cells and NK cells. Front Immunol 7:. https://doi.org/10.3389/fimmu.2016.00273
Rizzello V, Bonaccorsi I, Dongarrà ML et al (2011) Role of natural killer and dendritic cell crosstalk in immunomodulation by commensal bacteria probiotics. J Biomed Biotechnol 2011:1–10. https://doi.org/10.1155/2011/473097
Sagheddu V, Uggeri F, Belogi L et al (2020) The biotherapeutic potential of Lactobacillus reuteri characterized using a target-specific selection process. Front Microbiol 11:. https://doi.org/10.3389/fmicb.2020.00532
Luerce TD, Gomes-Santos AC, Rocha CS et al (2014) Anti-inflammatory effects of Lactococcus lactis NCDO 2118 during the remission period of chemically induced colitis. Gut Pathog 6:33. https://doi.org/10.1186/1757-4749-6-33
Li S-C, Hsu W-F, Chang J-S, Shih C-K (2019) Combination of Lactobacillus acidophilus and Bifidobacterium animalis subsp. lactis shows a stronger anti-inflammatory effect than individual strains in HT-29 cells. Nutrients 11:969. https://doi.org/10.3390/nu11050969
Anderson RC, Cookson AL, McNabb WC et al (2010) Lactobacillus plantarum MB452 enhances the function of the intestinal barrier by increasing the expression levels of genes involved in tight junction formation. BMC Microbiol 10:316. https://doi.org/10.1186/1471-2180-10-316
Qin H-L (2005) Effect of Lactobacillus on the gut microflora and barrier function of the rats with abdominal infection. World J Gastroenterol 11:2591. https://doi.org/10.3748/wjg.v11.i17.2591
Karczewski J, Troost FJ, Konings I et al (2010) Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. American Journal of Physiology-Gastrointestinal and Liver Physiology 298:G851–G859. https://doi.org/10.1152/ajpgi.00327.2009
Blackwood BP, Yuan CY, Wood DR et al (2017) Probiotic Lactobacillus species strengthen intestinal barrier function and tight junction integrity in experimental necrotizing enterocolitis. J Probiotics Health 5:. https://doi.org/10.4172/2329-8901.1000159
Zyrek AA, Cichon C, Helms S et al (2007) Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKC? Redistribution resulting in tight junction and epithelial barrier repair. Cell Microbiol 9:804–816. https://doi.org/10.1111/j.1462-5822.2006.00836.x
Barnett A, Roy N, Cookson A, McNabb W (2018) Metabolism of caprine milk carbohydrates by probiotic bacteria and Caco-2:HT29–MTX epithelial co-cultures and their impact on intestinal barrier integrity. Nutrients 10:949. https://doi.org/10.3390/nu10070949
Mack DR, Ahrne S, Hyde L et al (2003) Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut 52:827–833. https://doi.org/10.1136/gut.52.6.827
Rijkers GT, Bengmark S, Enck P et al (2010) Guidance for substantiating the evidence for beneficial effects of probiotics: current status and recommendations for future research1–3. J Nutr 140:671S-676S. https://doi.org/10.3945/jn.109.113779
Leist M, Hartung T (2013) Inflammatory findings on species extrapolations: humans are definitely no 70-kg mice. Arch Toxicol 87:563–567. https://doi.org/10.1007/s00204-013-1038-0
Seok J, Warren HS, Cuenca AG et al (2013) Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci 110:3507–3512. https://doi.org/10.1073/pnas.1222878110
Knight A (2007) Animal experiments scrutinised: systematic reviews demonstrate poor human clinical and toxicological utility. ALTEX 24:320–325. https://doi.org/10.14573/altex.2007.4.320
European Commission workshop (2010) Are mice relevant models for human disease? London
Baker DG (1998) Natural pathogens of laboratory mice, rats, and rabbits and their effects on research. Clin Microbiol Rev 11:231–266. https://doi.org/10.1128/CMR.11.2.231
Pan X, Yang Y, Zhang J-R (2014) Molecular basis of host specificity in human pathogenic bacteria. Emerg Microbes Infect 3:1–10. https://doi.org/10.1038/emi.2014.23
MacArthur Clark J (2018) The 3Rs in research: a contemporary approach to replacement, reduction and refinement. Br J Nutr 120:S1–S7. https://doi.org/10.1017/S0007114517002227
Russell WMS, Burch RL (1959) The principles of humane experimental technique, 1st edn. Methuen, London
Fenwick N, Griffin G, Gauthier C (2009) The welfare of animals used in science: how the “Three Rs” ethic guides improvements. Can Vet J 50:523–530
Ishibashi N, Yamazaki S (2001) Probiotics and safety. Am J Clin Nutr 73:465s–470s. https://doi.org/10.1093/ajcn/73.2.465s
Rousseau CF, Desvignes C, Kling F et al (2020) Microbiome product toxicology: regulatory view on translational challenges. Regulatory toxicology. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 1–29
Heinritz SN, Mosenthin R, Weiss E (2013) Use of pigs as a potential model for research into dietary modulation of the human gut microbiota. Nutr Res Rev 26:191–209. https://doi.org/10.1017/S0954422413000152
Isa K, Oka K, Beauchamp N et al (2016) Safety assessment of the Clostridium butyricum MIYAIRI 588 ® probiotic strain including evaluation of antimicrobial sensitivity and presence of Clostridium toxin genes in vitro and teratogenicity in vivo. Hum Exp Toxicol 35:818–832. https://doi.org/10.1177/0960327115607372
Endres JR, Clewell A, Jade KA et al (2009) Safety assessment of a proprietary preparation of a novel probiotic, Bacillus coagulans, as a food ingredient. Food Chem Toxicol 47:1231–1238. https://doi.org/10.1016/j.fct.2009.02.018
Liong M-T (2008) Safety of probiotics: translocation and infection. Nutr Rev 66:192–202. https://doi.org/10.1111/j.1753-4887.2008.00024.x
Pogačar MŠ, Mičetić-Turk D, Fijan S (2022) Probiotics: current regulatory aspects of probiotics for use in different disease conditions. In: Probiotics in the prevention and management of human diseases. Elsevier, pp 465–499
Tompkins TA, Hagen KE, Wallace TD, Fillion-Forté V (2008) Safety evaluation of two bacterial strains used in asian probiotic products. Can J Microbiol 54:391–400. https://doi.org/10.1139/W08-022
Shreiner AB, Kao JY, Young VB (2015) The gut microbiome in health and in disease. Curr Opin Gastroenterol 31:69–75. https://doi.org/10.1097/MOG.0000000000000139
Lane ER, Zisman T, Suskind D (2017) The microbiota in inflammatory bowel disease: current and therapeutic insights. J Inflamm Res 10:63–73. https://doi.org/10.2147/JIR.S116088
Wu H-J, Wu E (2012) The role of gut microbiota in immune homeostasis and autoimmunity. Gut Microbes 3:4–14. https://doi.org/10.4161/gmic.19320
Rohr M, Narasimhulu CA, Sharma D et al (2018) Inflammatory diseases of the gut. J Med Food 21:113–126. https://doi.org/10.1089/jmf.2017.0138
van Vliet MJ, Harmsen HJM, de Bont ESJM, Tissing WJE (2010) The role of intestinal microbiota in the development and severity of chemotherapy-induced mucositis. PLoS Pathog 6:e1000879. https://doi.org/10.1371/journal.ppat.1000879
Nemati S, Teimourian S (2017) An overview of inflammatory bowel disease: general consideration and genetic screening approach in diagnosis of early onset subsets. Middle East J Dig Dis 9:69–80. https://doi.org/10.15171/mejdd.2017.54
Ungaro R, Mehandru S, Allen PB et al (2017) Ulcerative colitis. The Lancet 389:1756–1770. https://doi.org/10.1016/S0140-6736(16)32126-2
Ha F, Khalil H (2015) Crohn’s disease: a clinical update. Therap Adv Gastroenterol 8:352–359. https://doi.org/10.1177/1756283X15592585
Loddo I, Romano C (2015) Inflammatory bowel disease: genetics, epigenetics, and pathogenesis. Front Immunol 6:. https://doi.org/10.3389/fimmu.2015.00551
Shokrani M (2012) Inflammatory bowel disease: diagnosis and research trends: the clinical lab is playing an increasingly important role. MLO Med Lab Obs 44:8, 10, 12; quiz 14
Fakhoury M, Al-Salami H, Negrulj R, Mooranian A (2014) Inflammatory bowel disease: clinical aspects and treatments. J Inflamm Res 113. https://doi.org/10.2147/JIR.S65979
Sartor RB (1997) Pathogenesis and immune mechanisms of chronic inflammatory bowel diseases. Am J Gastroenterol 92:5S-11S
Thoreson R, Cullen JJ (2007) Pathophysiology of inflammatory bowel disease: an overview. Surg Clin North Am 87:575–585. https://doi.org/10.1016/j.suc.2007.03.001
Hemarajata P, Versalovic J (2013) Effects of probiotics on gut microbiota: mechanisms of intestinal immunomodulation and neuromodulation. Therap Adv Gastroenterol 6:39–51. https://doi.org/10.1177/1756283X12459294
Fedorak RN, Feagan BG, Hotte N et al (2015) The probiotic VSL#3 has anti-inflammatory effects and could reduce endoscopic recurrence after surgery for Crohn’s disease. Clin Gastroenterol Hepatol 13:928-935.e2. https://doi.org/10.1016/j.cgh.2014.10.031
Bibiloni R, Fedorak RN, Tannock GW et al (2005) VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 100:1539–1546. https://doi.org/10.1111/j.1572-0241.2005.41794.x
Sniffen JC, McFarland LV, Evans CT, Goldstein EJC (2018) Choosing an appropriate probiotic product for your patient: an evidence-based practical guide. PLoS ONE 13:e0209205. https://doi.org/10.1371/journal.pone.0209205
Gupta P, Andrew H, Kirschner BS, Guandalini S (2000) Is Lactobacillus GG helpful in children with Crohn’s disease? Results of a preliminary, open-label study. J Pediatr Gastroenterol Nutr 31:453–457. https://doi.org/10.1097/00005176-200010000-00024
Hegazy SK (2010) Effect of probiotics on pro-inflammatory cytokines and NF-κB activation in ulcerative colitis. World J Gastroenterol 16:4145. https://doi.org/10.3748/wjg.v16.i33.4145
Astó E, Méndez I, Audivert S et al (2019) The efficacy of probiotics, prebiotic inulin-type fructans, and synbiotics in human ulcerative colitis: a systematic review and meta-analysis. Nutrients 11:293. https://doi.org/10.3390/nu11020293
Santos Rocha C, Gomes-Santos AC, Garcias Moreira T et al (2014) Local and systemic immune mechanisms underlying the anti-colitis effects of the dairy bacterium Lactobacillus delbrueckii. PLoS ONE 9:e85923. https://doi.org/10.1371/journal.pone.0085923
Plé C, Breton J, Richoux R et al (2016) Combining selected immunomodulatory Propionibacterium freudenreichii and Lactobacillus delbrueckii strains: reverse engineering development of an anti-inflammatory cheese. Mol Nutr Food Res 60:935–948. https://doi.org/10.1002/mnfr.201500580
Ma S, Yeom J, Lim Y-H (2020) Dairy Propionibacterium freudenreichii ameliorates acute colitis by stimulating MUC2 expression in intestinal goblet cell in a DSS-induced colitis rat model. Sci Rep 10:5523. https://doi.org/10.1038/s41598-020-62497-8
Jang S-E, Jeong J-J, Kim J-K et al (2018) Simultaneous amelioratation of colitis and liver injury in mice by Bifidobacterium longum LC67 and Lactobacillus plantarum LC27. Sci Rep 8:7500. https://doi.org/10.1038/s41598-018-25775-0
Chen X, Fu Y, Wang L et al (2019) Bifidobacterium longum and VSL#3® amelioration of TNBS-induced colitis associated with reduced HMGB1 and epithelial barrier impairment. Dev Comp Immunol 92:77–86. https://doi.org/10.1016/j.dci.2018.09.006
Sonis ST (2004) The pathobiology of mucositis. Nat Rev Cancer 4:277–284. https://doi.org/10.1038/nrc1318
Li H-L, Lu L, Wang X-S et al (2017) Alteration of gut microbiota and inflammatory cytokine/chemokine profiles in 5-fluorouracil induced intestinal mucositis. Front Cell Infect Microbiol 7:. https://doi.org/10.3389/fcimb.2017.00455
Chang C-T, Ho T-Y, Lin H et al (2012) 5-Fluorouracil induced intestinal mucositis via nuclear factor-κB activation by transcriptomic analysis and in vivo bioluminescence imaging. PLoS ONE 7:e31808. https://doi.org/10.1371/journal.pone.0031808
Batista VL, da Silva TF, de Jesus LCL et al (2020) Probiotics, prebiotics, synbiotics, and paraprobiotics as a therapeutic alternative for intestinal mucositis. Front Microbiol 11:. https://doi.org/10.3389/fmicb.2020.544490
Cordeiro BF, Oliveira ER, da Silva SH et al (2018) Whey protein isolate-supplemented beverage, fermented by Lactobacillus casei BL23 and Propionibacterium freudenreichii 138, in the prevention of mucositis in mice. Front Microbiol 9:. https://doi.org/10.3389/fmicb.2018.02035
Savassi B, Cordeiro BF, Silva SH et al (2021) Lyophilized symbiotic mitigates mucositis induced by 5-fluorouracil. Front Pharmacol 12:. https://doi.org/10.3389/fphar.2021.755871
Mi H, Dong Y, Zhang B et al (2017) Bifidobacterium Infantis ameliorates chemotherapy-induced intestinal mucositis via regulating T cell immunity in colorectal cancer rats. Cell Physiol Biochem 42:2330–2341. https://doi.org/10.1159/000480005
Kato S, Hamouda N, Kano Y et al (2017) Probiotic Bifidobacterium bifidum G9–1 attenuates 5-fluorouracil-induced intestinal mucositis in mice via suppression of dysbiosis-related secondary inflammatory responses. Clin Exp Pharmacol Physiol 44:1017–1025. https://doi.org/10.1111/1440-1681.12792
Justino PFC, Melo LFM, Nogueira AF et al (2015) Regulatory role of Lactobacillus acidophilus on inflammation and gastric dysmotility in intestinal mucositis induced by 5-fluorouracil in mice. Cancer Chemother Pharmacol 75:559–567. https://doi.org/10.1007/s00280-014-2663-x
Chang C-W, Liu C-Y, Lee H-C et al (2018) Lactobacillus casei variety rhamnosus probiotic preventively attenuates 5-fluorouracil/oxaliplatin-induced intestinal injury in a syngeneic colorectal cancer model. Front Microbiol 9:. https://doi.org/10.3389/fmicb.2018.00983
Quaresma M, Damasceno S, Monteiro C et al (2020) Probiotic mixture containing Lactobacillus spp. and Bifidobacterium spp. attenuates 5-fluorouracil-induced intestinal mucositis in mice. Nutr Cancer 72:1355–1365. https://doi.org/10.1080/01635581.2019.1675719
Tang Y, Wu Y, Huang Z et al (2017) Administration of probiotic mixture DM#1 ameliorated 5-fluorouracil–induced intestinal mucositis and dysbiosis in rats. Nutrition 33:96–104. https://doi.org/10.1016/j.nut.2016.05.003
De Jesus LCL, Drumond MM, de Carvalho A et al (2019) Protective effect of Lactobacillus delbrueckii subsp. Lactis CIDCA 133 in a model of 5 fluorouracil-induced intestinal mucositis. J Funct Foods 53:197–207. https://doi.org/10.1016/j.jff.2018.12.027
Bastos RW, Pedroso SHSP, Vieira AT et al (2016) Saccharomyces cerevisiae UFMG A-905 treatment reduces intestinal damage in a murine model of irinotecan-induced mucositis. Benef Microbes 7:549–557. https://doi.org/10.3920/BM2015.0190
Justino PFC, Franco AX, Pontier-Bres R et al (2020) Modulation of 5-fluorouracil activation of toll-like/MyD88/NF-κB/MAPK pathway by Saccharomyces boulardii CNCM I-745 probiotic. Cytokine 125:154791. https://doi.org/10.1016/j.cyto.2019.154791
Kim N, Yun M, Oh YJ, Choi H-J (2018) Mind-altering with the gut: modulation of the gut-brain axis with probiotics. J Microbiol 56:172–182. https://doi.org/10.1007/s12275-018-8032-4
Knezevic J, Starchl C, Tmava Berisha A, Amrein K (2020) Thyroid-gut-axis: how does the microbiota influence thyroid function? Nutrients 12:1769. https://doi.org/10.3390/nu12061769
López-Moreno A, Aguilera M (2020) Probiotics dietary supplementation for modulating endocrine and fertility microbiota dysbiosis. Nutrients 12:757. https://doi.org/10.3390/nu12030757
Hu S, Wang L, Jiang Z (2017) Dietary additive probiotics modulation of the intestinal microbiota. Protein Pept Lett 24:382–387. https://doi.org/10.2174/0929866524666170223143615
Tsai Y-L, Lin T-L, Chang C-J et al (2019) Probiotics, prebiotics and amelioration of diseases. J Biomed Sci 26:3. https://doi.org/10.1186/s12929-018-0493-6
Cristofori F, Indrio F, Miniello V et al (2018) Probiotics in celiac disease. Nutrients 10:1824. https://doi.org/10.3390/nu10121824
do Carmo MS, Santos C itapary dos, Araújo MC et al 2018 Probiotics, mechanisms of action, and clinical perspectives for diarrhea management in children Food Funct 9 5074 5095 https://doi.org/10.1039/C8FO00376A
Liu S, Liu H, Chen L et al (2020) Effect of probiotics on the intestinal microbiota of hemodialysis patients: a randomized trial. Eur J Nutr 59:3755–3766. https://doi.org/10.1007/s00394-020-02207-2
Vitellio P, Celano G, Bonfrate L et al (2019) Effects of Bifidobacterium longum and Lactobacillus rhamnosus on gut microbiota in patients with lactose intolerance and persisting functional gastrointestinal symptoms: a randomised, double-blind, cross-over study. Nutrients 11:. https://doi.org/10.3390/nu11040886
Li H-Y, Gan R-Y, Shang A et al (2021) Plant-based foods and their bioactive compounds on fatty liver disease: effects, mechanisms, and clinical application. Oxid Med Cell Longev 2021:1–23. https://doi.org/10.1155/2021/6621644
Wu T-R, Lin C-S, Chang C-J et al (2019) Gut commensal Parabacteroides goldsteinii plays a predominant role in the anti-obesity effects of polysaccharides isolated from Hirsutella sinensis. Gut 68:248–262. https://doi.org/10.1136/gutjnl-2017-315458
Stewart CJ, Embleton ND, Marrs ECL et al (2016) Temporal bacterial and metabolic development of the preterm gut reveals specific signatures in health and disease. Microbiome 4:67. https://doi.org/10.1186/s40168-016-0216-8
Zou J, Chassaing B, Singh V et al (2018) Fiber-mediated nourishment of gut microbiota protects against diet-induced obesity by restoring IL-22-mediated colonic health. Cell Host Microbe 23:41-53.e4. https://doi.org/10.1016/j.chom.2017.11.003
Huang L, Thonusin C, Chattipakorn N, Chattipakorn SC (2021) Impacts of gut microbiota on gestational diabetes mellitus: a comprehensive review. Eur J Nutr 60:2343–2360. https://doi.org/10.1007/s00394-021-02483-6
Bellikci-Koyu E, Sarer-Yurekli BP, Karagozlu C et al (2022) Probiotic kefir consumption improves serum apolipoprotein A1 levels in metabolic syndrome patients: a randomized controlled clinical trial. Nutr Res 102:59–70. https://doi.org/10.1016/j.nutres.2022.02.006
Barreto FM, Colado Simão AN, Morimoto HK et al (2014) Beneficial effects of Lactobacillus plantarum on glycemia and homocysteine levels in postmenopausal women with metabolic syndrome. Nutrition 30:939–942. https://doi.org/10.1016/j.nut.2013.12.004
Kassaian N, Feizi A, Aminorroaya A, Amini M (2019) Probiotic and synbiotic supplementation could improve metabolic syndrome in prediabetic adults: a randomized controlled trial. Diabetes Metab Syndr 13:2991–2996. https://doi.org/10.1016/j.dsx.2018.07.016
Bordalo Tonucci L, Dos Santos KMO, De Luces Fortes Ferreira CL et al (2017) Gut microbiota and probiotics: focus on diabetes mellitus. Crit Rev Food Sci Nutr 57:2296-2309. https://doi.org/10.1080/10408398.2014.934438
Bejar W, Hamden K, Ben Salah R, Chouayekh H (2013) Lactobacillus plantarum TN627 significantly reduces complications of alloxan-induced diabetes in rats. Anaerobe 24:4–11. https://doi.org/10.1016/j.anaerobe.2013.08.006
Groele L, Szajewska H, Szypowska A (2017) Effects of Lactobacillus rhamnosus GG and Bifidobacterium lactis Bb12 on beta-cell function in children with newly diagnosed type 1 diabetes: protocol of a randomised controlled trial. BMJ Open 7:e017178. https://doi.org/10.1136/bmjopen-2017-017178
Niibo M, Shirouchi B, Umegatani M et al (2019) Probiotic Lactobacillus gasseri SBT2055 improves insulin secretion in a diabetic rat model. J Dairy Sci 102:997–1006. https://doi.org/10.3168/jds.2018-15203
Kijmanawat A, Panburana P, Reutrakul S, Tangshewinsirikul C (2019) Effects of probiotic supplements on insulin resistance in gestational diabetes mellitus: a double-blind randomized controlled trial. J Diabetes Investig 10:163–170. https://doi.org/10.1111/jdi.12863
Davidson SJ, Barrett HL, Price SA et al (2021) Probiotics for preventing gestational diabetes. Cochrane Database Syst Rev 4:CD009951. https://doi.org/10.1002/14651858.CD009951.pub3
Crovesy L, Ostrowski M, Ferreira DMTP et al (2017) Effect of Lactobacillus on body weight and body fat in overweight subjects: a systematic review of randomized controlled clinical trials. Int J Obes (Lond) 41:1607–1614. https://doi.org/10.1038/ijo.2017.161
Toral M, Gómez-Guzmán M, Jiménez R et al (2014) The probiotic Lactobacillus coryniformis CECT5711 reduces the vascular pro-oxidant and pro-inflammatory status in obese mice. Clin Sci (Lond) 127:33–45. https://doi.org/10.1042/CS20130339
Razmpoosh E, Javadi M, Ejtahed H-S, Mirmiran P (2016) Probiotics as beneficial agents in the management of diabetes mellitus: a systematic review. Diabetes Metab Res Rev 32:143–168. https://doi.org/10.1002/dmrr.2665
Yadav H, Jain S, Sinha PR (2007) Antidiabetic effect of probiotic dahi containing Lactobacillus acidophilus and Lactobacillus casei in high fructose fed rats. Nutrition 23:62–68. https://doi.org/10.1016/j.nut.2006.09.002
Kim S-W, Park K-Y, Kim B et al (2013) Lactobacillus rhamnosus GG improves insulin sensitivity and reduces adiposity in high-fat diet-fed mice through enhancement of adiponectin production. Biochem Biophys Res Commun 431:258–263. https://doi.org/10.1016/j.bbrc.2012.12.121
Matsuzaki T, Yamazaki R, Hashimoto S, Yokokura T (1997) Antidiabetic effects of an oral administration of Lactobacillus casei in a non-insulin-dependent diabetes mellitus (NIDDM) model using KK-Ay mice. Endocr J 44:357–365. https://doi.org/10.1507/endocrj.44.357
Tabuchi M, Ozaki M, Tamura A et al (2003) Antidiabetic effect of Lactobacillus GG in streptozotocin-induced diabetic rats. Biosci Biotechnol Biochem 67:1421–1424. https://doi.org/10.1271/bbb.67.1421
Andreasen AS, Larsen N, Pedersen-Skovsgaard T et al (2010) Effects of Lactobacillus acidophilus NCFM on insulin sensitivity and the systemic inflammatory response in human subjects. Br J Nutr 104:1831–1838. https://doi.org/10.1017/S0007114510002874
Zhang Q, Wu Y, Fei X (2016) Effect of probiotics on glucose metabolism in patients with type 2 diabetes mellitus: a meta-analysis of randomized controlled trials. Medicina (B Aires) 52:28–34. https://doi.org/10.1016/j.medici.2015.11.008
Yun SI, Park HO, Kang JH (2009) Effect of Lactobacillus gasseri BNR17 on blood glucose levels and body weight in a mouse model of type 2 diabetes. J Appl Microbiol 107:1681–1686. https://doi.org/10.1111/j.1365-2672.2009.04350.x
Chen P, Zhang Q, Dang H et al (2014) Oral administration of Lactobacillus rhamnosus CCFM0528 improves glucose tolerance and cytokine secretion in high-fat-fed, streptozotocin-induced type 2 diabetic mice. J Funct Foods 10:318–326. https://doi.org/10.1016/j.jff.2014.06.014
Chen P, Zhang Q, Dang H et al (2014) Antidiabetic effect of Lactobacillus casei CCFM0412 on mice with type 2 diabetes induced by a high-fat diet and streptozotocin. Nutrition 30:1061–1068. https://doi.org/10.1016/j.nut.2014.03.022
Marazza JA, LeBlanc JG, de Giori GS, Garro MS (2013) Soymilk fermented with Lactobacillus rhamnosus CRL981 ameliorates hyperglycemia, lipid profiles and increases antioxidant enzyme activities in diabetic mice. J Funct Foods 5:1848–1853. https://doi.org/10.1016/j.jff.2013.09.005
Manaer T, Yu L, Zhang Y et al (2015) Anti-diabetic effects of shubat in type 2 diabetic rats induced by combination of high-glucose-fat diet and low-dose streptozotocin. J Ethnopharmacol 169:269–274. https://doi.org/10.1016/j.jep.2015.04.032
Dolatkhah N, Hajifaraji M, Abbasalizadeh F et al (2015) Is there a value for probiotic supplements in gestational diabetes mellitus? A randomized clinical trial. J Health Popul Nutr 33:25. https://doi.org/10.1186/s41043-015-0034-9
Castaner O, Goday A, Park Y-M et al (2018) The gut microbiome profile in obesity: a systematic review. Int J Endocrinol 2018:1–9. https://doi.org/10.1155/2018/4095789
Al-Assal K, Martinez AC, Torrinhas RS et al (2018) Gut microbiota and obesity. Clin Nutr Exp 20:60–64. https://doi.org/10.1016/j.yclnex.2018.03.001
Abenavoli L, Scarpellini E, Colica C et al (2019) Gut microbiota and obesity: a role for probiotics. Nutrients 11:2690. https://doi.org/10.3390/nu11112690
Davis CD (2016) The gut microbiome and its role in obesity. Nutr Today 51:167–174. https://doi.org/10.1097/NT.0000000000000167
Cerdó T, García-Santos J, G. Bermúdez M, Campoy C (2019) The role of probiotics and prebiotics in the prevention and treatment of obesity. Nutrients 11:635. https://doi.org/10.3390/nu11030635
Luoto R, Kalliomäki M, Laitinen K, Isolauri E (2010) The impact of perinatal probiotic intervention on the development of overweight and obesity: follow-up study from birth to 10 years. Int J Obes 34:1531–1537. https://doi.org/10.1038/ijo.2010.50
Ejtahed H-S, Angoorani P, Soroush A-R et al (2019) Probiotics supplementation for the obesity management; a systematic review of animal studies and clinical trials. J Funct Foods 52:228–242. https://doi.org/10.1016/j.jff.2018.10.039
Bubnov RV, Babenko LP, Lazarenko LM et al (2017) Comparative study of probiotic effects of Lactobacillus and Bifidobacteria strains on cholesterol levels, liver morphology and the gut microbiota in obese mice. EPMA Journal 8:357–376. https://doi.org/10.1007/s13167-017-0117-3
Alisi A, Bedogni G, Baviera G et al (2014) Randomised clinical trial: the beneficial effects of VSL#3 in obese children with non-alcoholic steatohepatitis. Aliment Pharmacol Ther 39:1276–1285. https://doi.org/10.1111/apt.12758
Famouri F, Shariat Z, Hashemipour M et al (2017) Effects of probiotics on nonalcoholic fatty liver disease in obese children and adolescents. J Pediatr Gastroenterol Nutr 64:413–417. https://doi.org/10.1097/MPG.0000000000001422
Sanchis-Chordà J, del Pulgar EMG, Carrasco-Luna J et al (2018) Bifidobacterium pseudocatenulatum CECT 7765 supplementation improves inflammatory status in insulin-resistant obese children. Eur J Nutr. https://doi.org/10.1007/s00394-018-1828-5
Jung S, Lee YJ, Kim M et al (2015) Supplementation with two probiotic strains, Lactobacillus curvatus HY7601 and Lactobacillus plantarum KY1032, reduced body adiposity and Lp-PLA2 activity in overweight subjects. J Funct Foods 19:744–752. https://doi.org/10.1016/j.jff.2015.10.006
Gomes AC, de Sousa RGM, Botelho PB et al (2017) The additional effects of a probiotic mix on abdominal adiposity and antioxidant status: a double-blind, randomized trial. Obesity 25:30–38. https://doi.org/10.1002/oby.21671
Higashikawa F, Noda M, Awaya T et al (2016) Antiobesity effect of Pediococcus pentosaceus LP28 on overweight subjects: a randomized, double-blind, placebo-controlled clinical trial. Eur J Clin Nutr 70:582–587. https://doi.org/10.1038/ejcn.2016.17
Sanchez M, Darimont C, Panahi S et al (2017) Effects of a diet-based weight-reducing program with probiotic supplementation on satiety efficiency, eating behaviour traits, and psychosocial behaviours in obese individuals. Nutrients 9:284. https://doi.org/10.3390/nu9030284
Szulińska M, Łoniewski I, van Hemert S et al (2018) Dose-dependent effects of multispecies probiotic supplementation on the lipopolysaccharide (LPS) level and cardiometabolic profile in obese postmenopausal women: a 12-week randomized clinical trial. Nutrients 10:773. https://doi.org/10.3390/nu10060773
Chen Y-C, Greenbaum J, Shen H, Deng H-W (2017) Association between gut microbiota and bone health: potential mechanisms and prospective. J Clin Endocrinol Metab 102:3635–3646. https://doi.org/10.1210/jc.2017-00513
Ohlsson C, Sjögren K (2018) Osteomicrobiology: a new cross-disciplinary research field. Calcif Tissue Int 102:426–432. https://doi.org/10.1007/s00223-017-0336-6
Rupesh K S (2015) Probiotics and bone health: it takes guts to improve bone density. Int J Immunother Cancer Res 018–022. https://doi.org/10.17352/2455-8591.000005
Sjögren K, Engdahl C, Henning P et al (2012) The gut microbiota regulates bone mass in mice. J Bone Miner Res 27:1357–1367. https://doi.org/10.1002/jbmr.1588
Britton RA, Irwin R, Quach D et al (2014) Probiotic L. reuteri treatment prevents bone loss in a menopausal ovariectomized mouse model. J Cell Physiol 229:1822–1830. https://doi.org/10.1002/jcp.24636
Clynes MA, Harvey NC, Curtis EM et al (2020) The epidemiology of osteoporosis. Br Med Bull. https://doi.org/10.1093/bmb/ldaa005
Kanis JA, Cooper C, Rizzoli R, Reginster J-Y (2019) European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int 30:3–44. https://doi.org/10.1007/s00198-018-4704-5
Lee CS, Kim J-Y, Kim BK et al (2021) Lactobacillus- fermented milk products attenuate bone loss in an experimental rat model of ovariectomy-induced post-menopausal primary osteoporosis. J Appl Microbiol 130:2041–2062. https://doi.org/10.1111/jam.14852
Desfita S, Sari W, Yusmarini Y et al (2021) Effect of fermented soymilk-honey from different probiotics on osteocalcin level in menopausal women. Nutrients 13:3581. https://doi.org/10.3390/nu13103581
Jansson P-A, Curiac D, Lazou Ahrén I et al (2019) Probiotic treatment using a mix of three Lactobacillus strains for lumbar spine bone loss in postmenopausal women: a randomised, double-blind, placebo-controlled, multicentre trial. Lancet Rheumatol 1:e154–e162. https://doi.org/10.1016/S2665-9913(19)30068-2
Takimoto T, Hatanaka M, Hoshino T et al (2018) Effect of Bacillus subtilis C-3102 on bone mineral density in healthy postmenopausal Japanese women: a randomized, placebo-controlled, double-blind clinical trial. Biosci Microbiota Food Health 37:87–96. https://doi.org/10.12938/bmfh.18-006
Nilsson AG, Sundh D, Bäckhed F, Lorentzon M (2018) Lactobacillus reuteri reduces bone loss in older women with low bone mineral density: a randomized, placebo-controlled, double-blind, clinical trial. J Intern Med 284:307–317. https://doi.org/10.1111/joim.12805
Jafarnejad S, Djafarian K, Fazeli MR et al (2017) Effects of a multispecies probiotic supplement on bone health in osteopenic postmenopausal women: a randomized, double-blind, controlled trial. J Am Coll Nutr 36:497–506. https://doi.org/10.1080/07315724.2017.1318724
Dar HY, Pal S, Shukla P et al (2018) Bacillus clausii inhibits bone loss by skewing Treg-Th17 cell equilibrium in postmenopausal osteoporotic mice model. Nutrition 54:118–128. https://doi.org/10.1016/j.nut.2018.02.013
Gholami A, Dabbaghmanesh MH, Ghasemi Y et al (2022) The ameliorative role of specific probiotic combinations on bone loss in the ovariectomized rat model. BMC Complement Med Ther 22:241. https://doi.org/10.1186/s12906-022-03713-y
Montazeri-Najafabady N, Ghasemi Y, Dabbaghmanesh MH et al (2019) Supportive role of probiotic strains in protecting rats from ovariectomy-induced cortical bone loss. Probiotics Antimicrob Proteins 11:1145–1154. https://doi.org/10.1007/s12602-018-9443-6
Yu J, Cao G, Yuan S et al (2021) Probiotic supplements and bone health in postmenopausal women: a meta-analysis of randomised controlled trials. BMJ Open 11:e041393. https://doi.org/10.1136/bmjopen-2020-041393
Tak PP, Bresnihan B (2000) The pathogenesis and prevention of joint damage in rheumatoid arthritis: advances from synovial biopsy and tissue analysis. Arthritis Rheum 43:2619–2633. https://doi.org/10.1002/1529-0131(200012)43:12%3c2619::AID-ANR1%3e3.0.CO;2-V
Conigliaro P, Triggianese P, De Martino E et al (2019) Challenges in the treatment of rheumatoid arthritis. Autoimmun Rev 18:706–713. https://doi.org/10.1016/j.autrev.2019.05.007
Dhanoa H (2019) Probiotics for the management of rheumatoid arthritis. In: Bioactive food as dietary interventions for arthritis and related inflammatory diseases. Elsevier, pp 23–35
Amdekar S, Singh V, Singh R et al (2011) Lactobacillus casei reduces the inflammatory joint damage associated with collagen-induced arthritis (CIA) by reducing the pro-inflammatory cytokines. J Clin Immunol 31:147–154. https://doi.org/10.1007/s10875-010-9457-7
Gohil P, Patel V, Deshpande S et al (2018) Anti-arthritic activity of cell wall content of Lactobacillus plantarum in freund’s adjuvant-induced arthritic rats: involvement of cellular inflammatory mediators and other biomarkers. Inflammopharmacology 26:171–181. https://doi.org/10.1007/s10787-017-0370-z
Mohammed AT, Khattab M, Ahmed AM et al (2017) The therapeutic effect of probiotics on rheumatoid arthritis: a systematic review and meta-analysis of randomized control trials. Clin Rheumatol 36:2697–2707. https://doi.org/10.1007/s10067-017-3814-3
Wang Z, Xue K, Bai M et al (2017) Probiotics protect mice from CoCrMo particles-induced osteolysis. Int J Nanomedicine 12:5387–5397. https://doi.org/10.2147/IJN.S130485
Lei M, Hua L-M, Wang D-W (2016) The effect of probiotic treatment on elderly patients with distal radius fracture: a prospective double-blind, placebo-controlled randomised clinical trial. Benef Microbes 7:631–637. https://doi.org/10.3920/BM2016.0067
Collins FL, Irwin R, Bierhalter H et al (2016) Lactobacillus reuteri 6475 increases bone density in intact females only under an inflammatory setting. PLoS ONE 11:e0153180. https://doi.org/10.1371/journal.pone.0153180
Cheng L-H, Liu Y-W, Wu C-C et al (2019) Psychobiotics in mental health, neurodegenerative and neurodevelopmental disorders. J Food Drug Anal 27:632–648. https://doi.org/10.1016/j.jfda.2019.01.002
Burokas A, Arboleya S, Moloney RD et al (2017) Targeting the microbiota-gut-brain axis: prebiotics have anxiolytic and antidepressant-like effects and reverse the impact of chronic stress in mice. Biol Psychiatry 82:472–487. https://doi.org/10.1016/j.biopsych.2016.12.031
Riezzo G, Chimienti G, Orlando A et al (2019) Effects of long-term administration of Lactobacillus reuteri DSM-17938 on circulating levels of 5-HT and BDNF in adults with functional constipation. Benef Microbes 10:137–147. https://doi.org/10.3920/BM2018.0050
Martinowich K, Lu B (2008) Interaction between BDNF and serotonin: role in mood disorders. Neuropsychopharmacology 33:73–83. https://doi.org/10.1038/sj.npp.1301571
Heldt SA, Stanek L, Chhatwal JP, Ressler KJ (2007) Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol Psychiatry 12:656–670. https://doi.org/10.1038/sj.mp.4001957
Lu Y, Christian K, Lu B (2008) BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 89:312–323. https://doi.org/10.1016/j.nlm.2007.08.018
Sarkar A, Lehto SM, Harty S et al (2016) Psychobiotics and the manipulation of bacteria–gut–brain signals. Trends Neurosci 39:763–781. https://doi.org/10.1016/j.tins.2016.09.002
Dinan TG, Cryan JF (2017) The microbiome-gut-brain axis in health and disease. Gastroenterol Clin North Am 46:77–89. https://doi.org/10.1016/j.gtc.2016.09.007
Mazzoli R, Pessione E, Dufour M et al (2010) Glutamate-induced metabolic changes in Lactococcus lactis NCDO 2118 during GABA production: combined transcriptomic and proteomic analysis. Amino Acids 39:727–737. https://doi.org/10.1007/s00726-010-0507-5
Barrett E, Ross RP, O’Toole PW et al (2012) γ-Aminobutyric acid production by culturable bacteria from the human intestine. J Appl Microbiol 113:411–417. https://doi.org/10.1111/j.1365-2672.2012.05344.x
Schousboe A, Waagepetersen HS (2007) GABA: homeostatic and pharmacological aspects. pp 9–19
O’Mahony SM, Clarke G, Borre YE et al (2015) Serotonin, tryptophan metabolism and the brain-gut-microbiome axis. Behav Brain Res 277:32–48. https://doi.org/10.1016/j.bbr.2014.07.027
Roshchina V V. (2016) New trends and perspectives in the evolution of neurotransmitters in microbial, plant, and animal cells. pp 25–77
Bravo JA, Forsythe P, Chew MV et al (2011) Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci 108:16050–16055. https://doi.org/10.1073/pnas.1102999108
Teame T, Wang A, Xie M et al (2020) Paraprobiotics and postbiotics of probiotic lactobacilli, their positive effects on the host and action mechanisms: a review. Front Nutr 7:. https://doi.org/10.3389/fnut.2020.570344
Bercik P, Verdu EF, Foster JA et al (2010) Chronic gastrointestinal inflammation induces anxiety-like behavior and alters central nervous system biochemistry in mice. Gastroenterology 139:2102-2112.e1. https://doi.org/10.1053/j.gastro.2010.06.063
Allen AP, Hutch W, Borre YE et al (2016) Bifidobacterium longum 1714 as a translational psychobiotic: modulation of stress, electrophysiology and neurocognition in healthy volunteers. Transl Psychiatry 6:e939–e939. https://doi.org/10.1038/tp.2016.191
Mohammadi AA, Jazayeri S, Khosravi-Darani K et al (2016) The effects of probiotics on mental health and hypothalamic–pituitary–adrenal axis: a randomized, double-blind, placebo-controlled trial in petrochemical workers. Nutr Neurosci 19:387–395. https://doi.org/10.1179/1476830515Y.0000000023
Athari Nik Azm S, Djazayeri A, Safa M et al (2018) Lactobacilli and bifidobacteria ameliorate memory and learning deficits and oxidative stress in β-amyloid (1–42) injected rats. Appl Physiol Nutr Metab 43:718–726. https://doi.org/10.1139/apnm-2017-0648
Mehrabadi S, Sadr SS (2020) Assessment of probiotics mixture on memory function, inflammation markers, and oxidative stress in an Alzheimer’s disease model of rats. Iran Biomed J 24:220–228. https://doi.org/10.29252/ibj.24.4.220
Fasano A, Visanji NP, Liu LWC et al (2015) Gastrointestinal dysfunction in Parkinson’s disease. Lancet Neurol 14:625–639. https://doi.org/10.1016/S1474-4422(15)00007-1
Borzabadi S, Oryan S, Eidi A et al (2018) The effects of probiotic supplementation on gene expression related to inflammation, insulin and lipid in patients with Parkinson’s disease: a randomized, double-blind, placebocontrolled trial. Arch Iran Med 21:289–295
Hsieh T-H, Kuo C-W, Hsieh K-H et al (2020) Probiotics alleviate the progressive deterioration of motor functions in a mouse model of Parkinson’s disease. Brain Sci 10:206. https://doi.org/10.3390/brainsci10040206
Cassani E, Privitera G, Pezzoli G et al (2011) Use of probiotics for the treatment of constipation in Parkinson’s disease patients. Minerva Gastroenterol Dietol 57:117–121
American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders. American Psychiatric Association
Shaaban SY, El Gendy YG, Mehanna NS et al (2018) The role of probiotics in children with autism spectrum disorder: a prospective, open-label study. Nutr Neurosci 21:676–681. https://doi.org/10.1080/1028415X.2017.1347746
Carlessi AS, Borba LA, Zugno AI et al (2021) Gut microbiota–brain axis in depression: the role of neuroinflammation. Eur J Neurosci 53:222–235. https://doi.org/10.1111/ejn.14631
Westfall S, Lomis N, Kahouli I et al (2017) Microbiome, probiotics and neurodegenerative diseases: deciphering the gut brain axis. Cell Mol Life Sci 74:3769–3787. https://doi.org/10.1007/s00018-017-2550-9
Reid G, Charbonneau D, Erb J et al (2003) Oral use of Lactobacillus rhamnosus GR-1 and L. fermentum RC-14 significantly alters vaginal flora: randomized, placebo-controlled trial in 64 healthy women. FEMS Immunol Med Microbiol 35:131–134. https://doi.org/10.1016/S0928-8244(02)00465-0
Strus M, Chmielarczyk A, Kochan P et al (2012) Studies on the effects of probiotic Lactobacillus mixture given orally on vaginal and rectal colonization and on parameters of vaginal health in women with intermediate vaginal flora. European Journal of Obstetrics & Gynecology and Reproductive Biology 163:210–215. https://doi.org/10.1016/j.ejogrb.2012.05.001
Gueniche A, Philippe D, Bastien P et al (2014) Randomised double-blind placebo-controlled study of the effect of Lactobacillus paracasei NCC 2461 on skin reactivity. Benef Microbes 5:137–145. https://doi.org/10.3920/BM2013.0001
Fabbrocini G, Bertona M, Picazo Ó et al (2016) Supplementation with Lactobacillus rhamnosus SP1 normalises skin expression of genes implicated in insulin signalling and improves adult acne. Benef Microbes 7:625–630. https://doi.org/10.3920/BM2016.0089
West CE, Rydén P, Lundin D et al (2015) Gut microbiome and innate immune response patterns in <scp>I</scp> g <scp>E</scp> -associated eczema. Clin Exp Allergy 45:1419–1429. https://doi.org/10.1111/cea.12566
Prado FC, Parada JL, Pandey A, Soccol CR (2008) Trends in non-dairy probiotic beverages. Food Res Int 41:111–123. https://doi.org/10.1016/j.foodres.2007.10.010
Kolaček S, Hojsak I, Berni Canani R et al (2017) Commercial probiotic products: a call for improved quality control. A position paper by the ESPGHAN working group for probiotics and prebiotics. J Pediatr Gastroenterol Nutr 65:117–124. https://doi.org/10.1097/MPG.0000000000001603
Shah NP (2000) Probiotic bacteria: selective enumeration and survival in dairy foods. J Dairy Sci 83:894–907. https://doi.org/10.3168/jds.S0022-0302(00)74953-8
Chapman CMC, Gibson GR, Rowland I (2011) Health benefits of probiotics: are mixtures more effective than single strains? Eur J Nutr 50:1–17. https://doi.org/10.1007/s00394-010-0166-z
Mikelsaar M, Lazar V, Onderdonk A, Donelli G (2011) Do probiotic preparations for humans really have efficacy? Microb Ecol Health Dis 22:10128. https://doi.org/10.3402/mehd.v22i0.10128
Selle K, Klaenhammer TR (2013) Genomic and phenotypic evidence for probiotic influences of Lactobacillus gasseri on human health. FEMS Microbiol Rev 37:915–935. https://doi.org/10.1111/1574-6976.12021
Dianawati D, Mishra V, Shah NP (2016) Viability, acid and bile tolerance of spray dried probiotic bacteria and some commercial probiotic supplement products kept at room temperature. J Food Sci 81:M1472–M1479. https://doi.org/10.1111/1750-3841.13313
de Simone C (2019) The unregulated probiotic market. Clin Gastroenterol Hepatol 17:809–817. https://doi.org/10.1016/j.cgh.2018.01.018
Cinque B, La Torre C, Lombardi F et al (2016) Production conditions affect the in vitro anti-tumoral effects of a high concentration multi-strain probiotic preparation. PLoS ONE 11:e0163216. https://doi.org/10.1371/journal.pone.0163216
Cinque B, La Torre C, Lombardi F et al (2017) VSL#3 probiotic differently influences IEC-6 intestinal epithelial cell status and function. J Cell Physiol 232:3530–3539. https://doi.org/10.1002/jcp.25814
Trinchieri V, Laghi L, Vitali B et al (2017) Efficacy and safety of a multistrain probiotic formulation depends from manufacturing. Front Immunol 8:. https://doi.org/10.3389/fimmu.2017.01474
Grześkowiak Ł, Isolauri E, Salminen S, Gueimonde M (2011) Manufacturing process influences properties of probiotic bacteria. Br J Nutr 105:887–894. https://doi.org/10.1017/S0007114510004496
Elo S, Saxelin M, Salminen S (1991) Attachment of Lactobacillus casei strain GG to human colon carcinoma cell line Caco-2: comparison with other dairy strains. Lett Appl Microbiol 13:154–156. https://doi.org/10.1111/j.1472-765X.1991.tb00595.x
Kukkonen K, Savilahti E, Haahtela T et al (2008) Long-term safety and impact on infection rates of postnatal probiotic and prebiotic (synbiotic) treatment: randomized, double-blind, placebo-controlled trial. Pediatrics 122:8–12. https://doi.org/10.1542/peds.2007-1192
Clements ML, Levine MM, Ristaino PA et al (1983) Exogenous lactobacilli fed to man - their fate and ability to prevent diarrheal disease. Prog Food Nutr Sci 7:29–37
Auclair J, Frappier M, Millette M (2015) Lactobacillus acidophilus CL1285, Lactobacillus casei LBC80R, and Lactobacillus rhamnosus CLR2 (Bio-K+): characterization, manufacture, mechanisms of action, and quality control of a specific probiotic combination for primary prevention of clostridium difficile infection. Clin Infect Dis 60:S135–S143. https://doi.org/10.1093/cid/civ179
Nivoliez A, Camares O, Paquet-Gachinat M et al (2012) Influence of manufacturing processes on in vitro properties of the probiotic strain Lactobacillus rhamnosus Lcr35®. J Biotechnol 160:236–241. https://doi.org/10.1016/j.jbiotec.2012.04.005
Barroso FAL, de Jesus LCL, da Silva TF et al (2022) Lactobacillus delbrueckii CIDCA 133 ameliorates chemotherapy-induced mucositis by modulating epithelial barrier and TLR2/4/Myd88/NF-κB signaling pathway. Front Microbiol 13:. https://doi.org/10.3389/fmicb.2022.858036
Guarner F, Khan AG, Garisch J et al (2012) World gastroenterology organisation global guidelines. J Clin Gastroenterol 46:468–481. https://doi.org/10.1097/MCG.0b013e3182549092
Koutsoumanis K, Allende A, Alvarez‐Ordóñez A et al (2022) Update of the list of QPS‐recommended biological agents intentionally added to food or feed as notified to EFSA 15: suitability of taxonomic units notified to EFSA until September 2021. EFSA Journal 20:. https://doi.org/10.2903/j.efsa.2022.7045
FDA (2023) New Dietary Ingredient (NDI) Notification process. In: USA Government. https://www.fda.gov/food/dietary-supplements/new-dietary-ingredient-ndi-notification-process. Accessed 15 Jul 2023
De Filippis F, Pasolli E, Ercolini D (2020) The food-gut axis: lactic acid bacteria and their link to food, the gut microbiome and human health. FEMS Microbiol Rev 44:454–489. https://doi.org/10.1093/femsre/fuaa015
O’Toole PW, Marchesi JR, Hill C (2017) Next-generation probiotics: the spectrum from probiotics to live biotherapeutics. Nat Microbiol 2:17057. https://doi.org/10.1038/nmicrobiol.2017.57
Vallabhaneni S, Walker TA, Lockhart SR et al (2015) Notes from the field: fatal gastrointestinal mucormycosis in a premature infant associated with a contaminated dietary supplement–Connecticut, 2014. MMWR Morb Mortal Wkly Rep 64:155–156
Besselink MG, van Santvoort HC, Buskens E et al (2008) Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. The Lancet 371:651–659. https://doi.org/10.1016/S0140-6736(08)60207-X
Martin IW, Tonner R, Trivedi J et al (2017) Saccharomyces boulardii probiotic-associated fungemia: questioning the safety of this preventive probiotic’s use. Diagn Microbiol Infect Dis 87:286–288. https://doi.org/10.1016/j.diagmicrobio.2016.12.004
Atıcı S, Soysal A, Karadeniz Cerit K et al (2017) Catheter-related Saccharomyces cerevisiae fungemia following Saccharomyces boulardii probiotic treatment: in a child in intensive care unit and review of the literature. Med Mycol Case Rep 15:33–35. https://doi.org/10.1016/j.mmcr.2017.02.002
Weese JS (2003) Evaluation of deficiencies in labeling of commercial probiotics. Can Vet J 44:982–983
Toscano M, de Vecchi E, Rodighiero V, Drago L (2013) Microbiological and genetic identification of some probiotics proposed for medical use in 2011. J Chemother 25:156–161. https://doi.org/10.1179/1973947812Y.0000000068
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Conceptualization: TdS; Writing of the manuscript: TdS, RG, MA, AF, LdJ, FB, NC-R, JL, and LT; Revision of the manuscript: EG, GJ, and VA; Supervision: YLL, EG, GJ, and VA. All authors have read and approved the final version of this paper.
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da Silva, T.F., Glória, R., Americo, M.F. et al. Unlocking the Potential of Probiotics: A Comprehensive Review on Research, Production, and Regulation of Probiotics. Probiotics & Antimicro. Prot. (2024). https://doi.org/10.1007/s12602-024-10247-x
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DOI: https://doi.org/10.1007/s12602-024-10247-x