Cited by 329Probiotics and Fermented FoodsSalmonella and Campylobacter epidemiologyReproductive tract infections research

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Antagonistic activity exerted in vitro and in vivo by Lactobacillus casei (strain GG) against Salmonella typhimurium C5 infection

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Hudault, S, Liévin, V, Bernet-Camard, M F, Servin, A L·1997·Applied and Environmental Microbiology

DOI 10.1128/aem.63.2.513-518.1997PMC PMC168342

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Abstract

The aim of this study was to compare the antagonistic properties of Lactobacillus casei GG exerted in vitro against Salmonella typhimurium C5 in a cellular model, cultured enterocyte-like Caco-2 cells, to those exerted in vivo in an animal model, C3H/He/Oujco mice. Our results show that a 1-h contact between the invading strain C5 and either the culture or the supernatant of L. casei GG impeded the invasion by the Salmonella strain in Caco-2 cells, without modifying the viability of the strain. After neutralization at pH 7, no inhibition of the invasion by C5 was observed. The antagonistic activity of L. casei GG was examined in C3H/He/Oujco mice orally infected with C5 as follows: (i) L. casei GG was given daily to conventional animals as a probiotic, and (ii) it was given once to germ-free animals in order to study the effect of the population of L. casei GG established in the different segments of the gut. In vivo experiments show that after a single challenge with C5, this strain survives and persists at a higher level in the feces of the untreated conventional mice than in those of the treated group. In L. casei GG germ-free mice, establishment of L. casei GG in the gut significantly delayed the occurrence of 100% mortality of the animals (15 days after C5 challenge versus 9 days in germ-free mice [P < 0.01]). Cecal colonization level and translocation rate of C5 to the mesenteric lymph nodes, spleen, and liver were significantly reduced during the first 2 days post-C5 challenge, although the L. casei GG population level in the gut dramatically decreased in these animals.

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Background
Metabolic and Functional Properties of Lactic Acid Bacteria in the Gastro-intestinal Ecosystem: A comparative in vitro Studybetween Bacteria of Intestinal and Fermented Food Origin
Haller, D., Colbus, H., Gänzle, M. G., Scherenbacher, P., Bode, C., & Hammes, W. P. (2001) · Systematic and Applied Microbiology · doi:10.1078/0723-2020-00023 · Cited by 138
Antagonistic activity against Salmonella infection in vitro and in vivo for two Lactobacillus strains from swine and poultry
Tsai, C., Hsih, H.-Y., Chiu, H.-H., Lai, Y.-Y., Liu, J.-H., Yu, B., & Tsen, H. (2005) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2004.12.014 · Cited by 138
Lactobacillusstrains isolated from the vaginal microbiota of healthy women inhibitPrevotella biviaandGardnerella vaginalisin coculture and cell culture
Atassi, F., Brassart, D., Grob, P., Graf, F., & Servin, A. L. (2006) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2006.00162.x · Cited by 132
In vitro characterization of aggregation and adhesion properties of viable and heat-killed forms of two probiotic Lactobacillus strains and interaction with foodborne zoonotic bacteria, especially Campylobacter jejuni
Tareb, R., Bernardeau, M., Guéguen, M., & Vernoux, J. (2013) · Journal of Medical Microbiology · doi:10.1099/jmm.0.049965-0 · Cited by 135
“Adhesion to the intestinal mucosa could confer a competitive advantage important for maintenance of bacteria in the gastrointestinal tract and it is generally accepted that adhesion properties contribute to the efficacy of probiotic strains (Hudault et al., 1997; Servin & Coconnier, 2003).”
Background
Lactic acid bacteria affect serum cholesterol levels, harmful fecal enzyme activity, and fecal water content
Lee, D. K., Jang, S., Baek, E. H., Kim, M. J., Lee, K. S., Shin, H. S., Chung, M. J., Kim, J. E., Lee, K. O., & Ha, N. J. (2009) · Lipids in Health and Disease · doi:10.1186/1476-511x-8-21 · Cited by 133
Individual and co-operative roles of lactic acid and hydrogen peroxide in the killing activity of enteric strain Lactobacillus johnsonii NCC933 and vaginal strain Lactobacillus gasseri KS120.1 against enteric, uropathogenic and vaginosis-associated pathog
Atassi, F., & Servin, A. L. (2009) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2009.01887.x · Cited by 129
Purification and characterization of a bacteriocin produced by Lactobacillus acidophilus IBB 801
Zamfir, M., Callewaert, R., Cornea, P. C., Savu, L., Vatafu, I., & Vuyst, L. D. (1999) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.1999.00950.x · Cited by 127
“Like LA1, it produces, most probably, a nonproteinaceous substance with antimicrobial activity (Silva et al. 1987) that acts against Salm. typhimurium to block adhesion to Caco-2 cells in vitro and protect against infection in mice (Hudault et al. 1997).”
Background
Application of nontraditional meat starter cultures in production of Hungarian salami
Pidcock, K., Heard, G. M., & Henriksson, A. (2002) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(02)00002-8 · Cited by 126
Lactic acid bacteria to improve growth performance in young calves fed milk replacer and spray-dried whey powder
Frizzo, L. S., Soto, L. P., Zbrun, M. V., Bertozzi, E., Sequeira, G., Armesto, R. R., & Rosmini, M. R. (2010) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2010.03.005 · Cited by 122
Review article: the use of biotherapeutic agents in the prevention and treatment of gastrointestinal disease
Lewis, S. J., & Freedman, A. R. (1998) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.1998.00386.x · Cited by 121
Inhibition of Giardia intestinalis by Extracellular Factors from Lactobacilli: an In Vitro Study
Pérez, P. F., Minnaard, J., Rouvet, M., Knabenhans, C., Brassart, D., Antoni, G. L. D., & Schiffrin, E. J. (2001) · Applied and Environmental Microbiology · doi:10.1128/aem.67.11.5037-5042.2001 · Cited by 119
“There is a large body of evidence showing that LAB can modulate the intestinal mechanisms of defense against enteropathogens in “in vivo” models (4, 5, 17, 26, 28).”
Background
Probiotic properties of lactic acid bacteria isolated from traditionally fermented Xinjiang cheese
Azat, R., Liu, Y., Li, W., Kayir, A., Lin, D.-B., Zhou, W.-W., & Zheng, X.-D. (2016) · Journal of Zhejiang University SCIENCE B · doi:10.1631/jzus.b1500250 · Cited by 116
“These effects are mediated by production of antimicrobial metabolites such as organic acids (for example lactate, acetate, and butyrate), hydrogen peroxide, and bacteriocins, and competition with harmful bacteria for nutrients or adhesion receptors (Hudault et al., 1997; Fons et al., 2000).”
Characterization and antimicrobial spectrum of bacteriocins produced by lactic acid bacteria isolated from traditional Bulgarian dairy products
Simova, E. D., Бешкова, Д., & Dimitrov, Z. P. (2009) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2008.04052.x · Cited by 116
“According to other authors, the production of bacteriocins occurs in vivo and this is one of the main antagonistic mechanisms against colonization by undesirable bacteria (Hudault et al. 1997; Collado et al. 2005a,b).”
Background
Bio-functional properties of probiotic Lactobacillus: current applications and research perspectives
Minj, J., Chandra, P., Paul, C., & Sharma, R. K. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2020.1774496 · Cited by 110
“teric lymph nodes, liver and the spleen and delayed the occurrences of mortality in the animals by 100% (Hudault et al. 1997).”
Background
Subtractive Screening for Probiotic Properties of Lactobacillus Species from the Human Gastrointestinal Tract in the Search for New Probiotics
Delgado, S., O’Sullivan, E. M., Fitzgerald, G. F., & Mayo, B. (2007) · Journal of Food Science · doi:10.1111/j.1750-3841.2007.00479.x · Cited by 104
Chapter 2 Adherence, Anti‐Adherence, and Oligosaccharides
Shoaf‐Sweeney, K. D., & Hutkins, R. W. (2008) · Advances in food and nutrition research · doi:10.1016/s1043-4526(08)00402-6 · Cited by 104
Probiotics: Functionality and commercial status
Scheinbach, S. (1998) · Biotechnology Advances · doi:10.1016/s0734-9750(98)00002-0 · Cited by 102
Antagonistic activity of Lactobacillus casei strain Shirota against gastrointestinal Listeria monocytogenes infection in rats
de Waard, R., Garssen, J., Bokken, G. C. A. M., & Vos, J. G. (2002) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(01)00699-7 · Cited by 101
Immune effect of heat-killed multistrain of Lactobacillus acidophilus against Salmonella typhimurium invasion to mice
Lin, W.-H., Yu, B., Lin, C.-K., Hwang, W.-Z., & Tsen, H.-Y. (2006) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2006.03073.x · Cited by 100
“…Microbiology 102 (2007) 22–31 ª 2006 The Authors Antagonistic effect of LAB strains against Salmonella invasion of cultured intestinal cells The antagonistic effect of LAB strains against Salmonella invasion was investigated according to the method of Tsai et al. (2005) and Hudault et al. (1997).”
BackgroundMethod
Protection activity of a novel probiotic strain of Bacillus subtilis against Salmonella Enteritidis infection
Thirabunyanon, M., & Thongwittaya, N. (2012) · Research in Veterinary Science · doi:10.1016/j.rvsc.2011.08.008 · Cited by 99
Inhibition of Salmonella typhimurium adhesion to Caco-2 cell cultures by Lactobacillus strain GG spent culture supernate: only a pH effect?
Lehto, E., & Salminen, S. (1997) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.1997.tb01037.x · Cited by 97
Effect of bacteriocin-producing lactobacilli on the survival of Escherichia coli and Listeria in a dynamic model of the stomach and the small intestine
Gänzle, M. G., Hertel, C., van der Vossen, J. M. B. M., & Hammes, W. P. (1999) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(99)00025-2 · Cited by 94
Lactobacillus delbrueckii ssp. bulgaricus B-30892 can inhibit cytotoxic effects and adhesion of pathogenic Clostridium difficile to Caco-2 cells
Banerjee, P., Merkel, G. J., & Bhunia, A. K. (2009) · Gut Pathogens · doi:10.1186/1757-4749-1-8 · Cited by 95
“Typhimurium [41] and L.”
Lactobacillus caseiDN-114 001 Inhibits the Ability of Adherent-InvasiveEscherichia coliIsolated from Crohn's Disease Patients To Adhere to and To Invade Intestinal Epithelial Cells
Ingrassia, I., Leplingard, A., & Darfeuille–Michaud, A. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.6.2880-2887.2005 · Cited by 92
“Several reports have confirmed the ability of probiotic Lactobacilli to inhibit the ability of pathogenic bacteria to adhere to and to invade intestinal epithelial cells (4, 10, 20, 26, 27).”
Antimicrobial proteinaceous compounds obtained from bifidobacteria: From production to their application
Cheikhyoussef, A., Pogori, N., Chen, W., & Zhang, H. (2008) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2008.03.012 · Cited by 86
Three Lactobacillus strains from healthy infant stool inhibit enterotoxigenic Escherichia coli grown in vitro
Tsai, C., Lin, P.-P., & Hsieh, Y.-M. (2007) · Anaerobe · doi:10.1016/j.anaerobe.2007.11.003 · Cited by 84
Is Lactobacillus rhamnosus GG Effective in Preventing the Onset of Antibiotic-Associated Diarrhoea: A Systematic Review
Hawrelak, J. A., Whitten, D. L., & Myers, S. P. (2005) · Digestion · doi:10.1159/000087637 · Cited by 84
Antagonistic Activities of Cell-Free Supernatants of Lactobacilli Against Extended-Spectrum β-Lactamase Producing Klebsiella pneumoniae and Pseudomonas aeruginosa
El‐Mokhtar, M. A., Hassanein, K. M. A., Ahmed, A. S., Gad, G. F., Amin, M. M., & Hassanein, O. F. (2020) · Infection and Drug Resistance · doi:10.2147/idr.s235603 · Cited by 81
The effect of calcium ions on adhesion and competitive exclusion of Lactobacillus ssp. and E. coli O138
Larsen, N., Nissen, P., & Willats, W. G. T. (2007) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2006.10.033 · Cited by 80
Lactobacillus acidophilus ATCC 4356 attenuates the atherosclerotic progression through modulation of oxidative stress and inflammatory process
Chen, L., Liu, W., Li, Y., Luo, S., Liu, Q., Zhong, Y., Jian, Z., & Bao, M. (2013) · International Immunopharmacology · doi:10.1016/j.intimp.2013.05.018 · Cited by 80
Dietary Calcium Phosphate Stimulates Intestinal Lactobacilli and Decreases the Severity of a Salmonella Infection in Rats
Bovee-Oudenhoven, I. M. J., Lettink-Wissink, M. L. G., Wouters, J. T., & van der Meer, R. (1999) · Journal of Nutrition · doi:10.1093/jn/129.3.607 · Cited by 80
Characterization of a Lactobacillus brevis strain with potential oral probiotic properties
Fang, F., Xu, J., Qiao-yu, L., Xia, X., & Du, G. (2018) · BMC Microbiology · doi:10.1186/s12866-018-1369-3 · Cited by 80
In vitro fermentation of carbohydrates by porcine faecal inocula and their influence on Salmonella Typhimurium growth in batch culture systems
Martín‐Peláez, S., Gibson, G. R., Martín-Orúe, S. M., Klinder, A., Rastall, R. A., Ragione, R. M. L., Woodward, M. J., & Costabile, A. (2008) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2008.00610.x · Cited by 79
In vitro and in vivo probiotic assessment of Leuconostoc mesenteroides P45 isolated from pulque, a Mexican traditional alcoholic beverage
Gilés-Gómez, M., García, J. G. S., Matus, V., Quintana, I. C., Bolívar, F. G., & Escalante, A. (2016) · SpringerPlus · doi:10.1186/s40064-016-2370-7 · Cited by 79
“Previous reports describing assays in mice for the in vivo assessment of the anti-infective activity of potential probiotic LAB included animal groups ranging from 6 (Hudault et al. 1997) to 10–12 (Chiu et al.”
Background
Influence of pH, temperature and culture media on the growth and bacteriocin production by vaginalLactobacillus salivariusCRL 1328
Tomás, M. S. J., Bru, E., Wiese, B., Holgado, A. A. P. D. R., & Nader-Macı́as, M. E. (2002) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2002.01753.x · Cited by 78
“utilize to prevent the colonization by undesirable microorganisms (Hudault et al. 1997).”
Background
Screening from pickled vegetables the potential probiotic strains of lactic acid bacteria able to inhibit the Salmonella invasion in mice
Chiu, H.-H., Tsai, C., Hsih, H.-Y., & Tsen, H. (2007) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2007.03573.x · Cited by 75
“Antagonistic effect of LAB strains against Salmonella invasion to cultured cells The methods used were those described by Tsai et al. (2005) and Hudault et al. (1997).”
BackgroundMethodInfluential
Adhesive ability means inhibition activities for lactobacillus against pathogens and S-layer protein plays an important role in adhesion
Zhang, W., Wang, H., Liu, J., Zhao, Y., Gao, K., & Zhang, J. (2013) · Anaerobe · doi:10.1016/j.anaerobe.2013.06.005 · Cited by 75
“Adhesion to intestinal epithelial cell is considered to be the first step for the lactobacillus strains performing beneficial effects on the health of host, and high adhesive ability can promote the gut residence time of lactobacillus, exclusion of pathogens, and protection of epithelial cells [12,13].”
Background
Amelioration of TMAO through probiotics and its potential role in atherosclerosis
Din, A. U., Hassan, A., Zhu, Y. S., Yin, T., Gregersen, H. N., & Wang, G. (2019) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-019-10142-4 · Cited by 76
“Probiotic bacteria have shown multiple potential health effects, including blocking gastroenteric pathogens, neutralizing food mutagens produced in the colon (Hudault et al. 1997), and enhancing the immune response (Kawashima et al.”
Background
The colonization of a simulator of the human intestinal microbial ecosystem by a probiotic strain fed on a fermented oat bran product: effects on the gastrointestinal microbiota
Kontula, P., Jaskari, J., Nollet, L. M. L., Smet, I. D., von Wright, A., Poutanen, K. S., & Mattila, T. (1998) · Applied Microbiology and Biotechnology · doi:10.1007/s002530051284 · Cited by 73
“Silva et al. (1987) and Hudault et al. (1997) reported that Lactobacillus GG produces antimicrobials that are active at pH 3±5.”
Background
Identification and characterization of starter lactic acid bacteria and probiotics from Columbian dairy products
Vélez, M. P., Hermans, K., Verhoeven, T. L. A., Lebeer, S., Vanderleyden, J., & Keersmaecker, S. C. J. D. (2007) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2007.03294.x · Cited by 72
“This is also the case for the control strain L. rhamnosus GG which has been previously reported to antagonize Salmonella spp. (Hudault et al. 1997; De Keersmaecker et al. 2006b).”
Stress Responses in ProbioticLactobacillus casei
Hosseininezhad, M., Hussain, M. A., & Britz, M. L. (2013) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2012.675601 · Cited by 77
“Several health benefits have been reported for these strains including inhibition of pathogenic organisms (Hudault et al., 1997), increasing immune responses (Matsuzaki et al., 1998) and enhancing the immune system in the digestive tract (Paubert-Braquet et al., 1995; Peluso et al., 2007).”
Background
Impact of luxS and Suppressor Mutations on the Gastrointestinal Transit of Lactobacillus rhamnosus GG
Lebeer, S., Claes, I. J. J., Verhoeven, T. L. A., Shen, C., Lambrichts, I., Ceuppens, J. L., Vanderleyden, J., & Keersmaecker, S. C. J. D. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00133-08 · Cited by 72
“rhamnosus GG was previously shown to more permanently colonize the digestive tract of germ-free mice after a single administration (18).”
Background

Authors: Hudault, S., Liévin, V, Bernet-Camard, M. F., & Servin, A. L.
Affiliations: Inserm (FR)
CJF 94.07 INSERM, UPR de Pharmacie Paris XI, Chatenay-Malabry, France.
Venue: Applied and Environmental Microbiology
Publisher: American Society for Microbiology
Published: 1997-02
Volume: 63
Issue: 2
Pages: 513-518
ISSN: 0099-2240 (ISSN-L)
1098-5336
DOI: 10.1128/aem.63.2.513-518.1997
PMC: PMC168342
OpenAlex: W2168298293
Cited by: 329
References: 37
Citations by year: 2026: 1 · 2024: 5 · 2023: 6 · 2022: 9 · 2021: 5 · 2020: 10 · 2019: 9 · 2018: 13 · 2017: 7 · 2016: 19 · 2015: 8 · 2014: 13 · 2013: 10 · 2012: 14
FWCI: 30.06
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Applied and Environmental Microbiology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Topics: Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
Keywords: Salmonella typhimurium, probiotics, antagonistic activity, Caco-2 cells, germ-free mice, intestinal colonization, bacterial translocation, mesenteric lymph nodes, gastrointestinal infections
MeSH terms: Animals, Antibiosis, Culture Media, Feces, Female, Germ-Free Life, Humans, Intestines, Lacticaseibacillus casei, Lymph Nodes, Mesentery, Mice, Inbred C3H, Salmonella Infections, Animal, Salmonella typhimurium, Caco-2 Cells, Mice

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Antagonistic activity exerted in vitro and in vivo by Lactobacillus casei (strain GG) against Salmonella typhimurium C5 infection

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