Survival of Probiotic Bacterial Cells in the Upper Gastrointestinal Tract and the Effect of the Surviving Population on the Colonic Microbial Community Activity and Composition

Overview

Journal Nutrients

Date 2024 Aug 29

PMID 39203927

Authors

Marlies Govaert

Chloe Rotsaert

Chelsea Vannieuwenhuyse

Cindy Duysburgh

Sophie Medlin

Massimo Marzorati

Harry Jarrett

Affiliations

Soon will be listed here.

Abstract

Many health-promoting effects have been attributed to the intake of probiotic cells. However, it is important that probiotic cells arrive at the site of their activity in a viable state in order to exert their beneficial effects. Careful selection of the appropriate probiotic formulation is therefore required as mainly the type of probiotic species/strain and the administration strategy may affect survival of the probiotic cells during the upper gastrointestinal (GIT) passage. Therefore, the current study implemented Simulator of the Human Microbial Ecosystem (SHIME) technology to investigate the efficacy of different commercially available probiotic formulations on the survival and culturability of probiotic bacteria during upper GIT passage. Moreover, Colon-on-a-Plate (CoaP™) technology was applied to assess the effect of the surviving probiotic bacteria on the gut microbial community (activity and composition) of three human donors. Significantly greater survival and culturability rates were reported for the delayed-release capsule formulation (>50%) as compared to the powder, liquid, and standard capsule formulations (<1%) ( < 0.05), indicating that the delayed-release capsule was most efficacious in delivering live bacteria cells. Indeed, administration of the delayed-release capsule probiotic digest resulted in enhanced production of SCFAs and shifted gut microbial community composition towards beneficial bacterial species. These results thus indicate that careful selection of the appropriate probiotic formulation and administration strategy is crucial to deliver probiotic cells in a viable state at the site of their activity (distal ileum and colon).

References

Hoefman S, Pommerening-Roser A, Samyn E, de Vos P, Heylen K . Efficient cryopreservation protocol enables accessibility of a broad range of ammonia-oxidizing bacteria for the scientific community. Res Microbiol. 2013; 164(4):288-92. DOI: 10.1016/j.resmic.2013.01.007. View

Hosmer J, McEwan A, Kappler U . Bacterial acetate metabolism and its influence on human epithelia. Emerg Top Life Sci. 2023; 8(1):1-13. PMC: 10903459. DOI: 10.1042/ETLS20220092. View

Taglialegna A . Keep calm with ammonia-producing microbiota. Nat Rev Microbiol. 2023; 22(1):2. DOI: 10.1038/s41579-023-00996-x. View

Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran L, Gratadoux J . Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008; 105(43):16731-6. PMC: 2575488. DOI: 10.1073/pnas.0804812105. View

Hens B, Tsume Y, Bermejo M, Paixao P, Koenigsknecht M, Baker J . Low Buffer Capacity and Alternating Motility along the Human Gastrointestinal Tract: Implications for in Vivo Dissolution and Absorption of Ionizable Drugs. Mol Pharm. 2017; 14(12):4281-4294. DOI: 10.1021/acs.molpharmaceut.7b00426. View

Moens F, Van den Abbeele P, Basit A, Dodoo C, Chatterjee R, Smith B . A four-strain probiotic exerts positive immunomodulatory effects by enhancing colonic butyrate production in vitro. Int J Pharm. 2018; 555:1-10. DOI: 10.1016/j.ijpharm.2018.11.020. View

Zhang J, Song L, Wang Y, Liu C, Zhang L, Zhu S . Beneficial effect of butyrate-producing Lachnospiraceae on stress-induced visceral hypersensitivity in rats. J Gastroenterol Hepatol. 2018; 34(8):1368-1376. PMC: 7379616. DOI: 10.1111/jgh.14536. View

Akkasheh G, Kashani-Poor Z, Tajabadi-Ebrahimi M, Jafari P, Akbari H, Taghizadeh M . Clinical and metabolic response to probiotic administration in patients with major depressive disorder: A randomized, double-blind, placebo-controlled trial. Nutrition. 2015; 32(3):315-20. DOI: 10.1016/j.nut.2015.09.003. View

Marzorati M, Calatayud M, Rotsaert C, Van Mele M, Duysburgh C, Durkee S . Comparison of protection and release behavior of different capsule polymer combinations based on L. acidophilus survivability and function and caffeine release. Int J Pharm. 2021; 607:120977. DOI: 10.1016/j.ijpharm.2021.120977. View

10.

Miller J, Cullingham C, Peery R . The influence of a priori grouping on inference of genetic clusters: simulation study and literature review of the DAPC method. Heredity (Edinb). 2020; 125(5):269-280. PMC: 7553915. DOI: 10.1038/s41437-020-0348-2. View

11.

Wang X, Gibson G, Costabile A, Sailer M, Theis S, Rastall R . Prebiotic Supplementation of Fecal Fermentations Inhibits Proteolysis by Gut Bacteria, and Host Diet Shapes Gut Bacterial Metabolism and Response to Intervention. Appl Environ Microbiol. 2019; 85(9). PMC: 6495761. DOI: 10.1128/AEM.02749-18. View

12.

Klindworth A, Pruesse E, Schweer T, Peplies J, Quast C, Horn M . Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 2012; 41(1):e1. PMC: 3592464. DOI: 10.1093/nar/gks808. View

13.

Ruiz L, Margolles A, Sanchez B . Bile resistance mechanisms in Lactobacillus and Bifidobacterium. Front Microbiol. 2014; 4:396. PMC: 3872040. DOI: 10.3389/fmicb.2013.00396. View

14.

Perreau C, Thabuis C, Verstrepen L, Ghyselinck J, Marzorati M . Ex Vivo Colonic Fermentation of NUTRIOSE Exerts Immuno-Modulatory Properties and Strong Anti-Inflammatory Effects. Nutrients. 2023; 15(19). PMC: 10574048. DOI: 10.3390/nu15194229. View

15.

Riviere A, Selak M, Lantin D, Leroy F, De Vuyst L . Bifidobacteria and Butyrate-Producing Colon Bacteria: Importance and Strategies for Their Stimulation in the Human Gut. Front Microbiol. 2016; 7:979. PMC: 4923077. DOI: 10.3389/fmicb.2016.00979. View

16.

Jones R, Zhu X, Moan E, Murff H, Ness R, Seidner D . Inter-niche and inter-individual variation in gut microbial community assessment using stool, rectal swab, and mucosal samples. Sci Rep. 2018; 8(1):4139. PMC: 5841359. DOI: 10.1038/s41598-018-22408-4. View

17.

Takahashi K, Nishida A, Fujimoto T, Fujii M, Shioya M, Imaeda H . Reduced Abundance of Butyrate-Producing Bacteria Species in the Fecal Microbial Community in Crohn's Disease. Digestion. 2016; 93(1):59-65. DOI: 10.1159/000441768. View

18.

Kassinen A, Krogius-Kurikka L, Makivuokko H, Rinttila T, Paulin L, Corander J . The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology. 2007; 133(1):24-33. DOI: 10.1053/j.gastro.2007.04.005. View

19.

Maeda H, Fujimoto C, Haruki Y, Maeda T, Kokeguchi S, Petelin M . Quantitative real-time PCR using TaqMan and SYBR Green for Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, Prevotella intermedia, tetQ gene and total bacteria. FEMS Immunol Med Microbiol. 2003; 39(1):81-6. DOI: 10.1016/S0928-8244(03)00224-4. View

20.

Radjabzadeh D, Bosch J, Uitterlinden A, Zwinderman A, Ikram M, van Meurs J . Gut microbiome-wide association study of depressive symptoms. Nat Commun. 2022; 13(1):7128. PMC: 9726982. DOI: 10.1038/s41467-022-34502-3. View