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
Mechanisms of Colonisation and Colonisation Resistance of the Digestive Tract Part 2: Bacteria/Bacteria Interactions
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Background
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“strains of Lactobacillus (Bernet-Camard et al. 1997; Coconnier et al. 1997; Hudault et al. 1997; Coconnier et al. 2000; Hirano et al. 2003; Resta-Lenert and Barrett 2003; Ingrassia et al. 2005) and Bifidobacterium (Lievin-Le Moal et al.”
BackgroundResultInfluential
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The Lactobacillus plantarum strain ACA-DC287 isolated from a Greek cheese demonstrates antagonistic activity in vitro and in vivo against Salmonella enterica serovar Typhimurium
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Background
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Background
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Result
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Background
Invited review: “Probiotic” approaches to improving dairy production: Reassessing “magic foo-foo dust”
Jeni, R. E., Villot, C., Koyun, O. Y., Osorio-Doblado, A. M., Baloyi, J. J., Lourenco, J. M., Steele, M. A., & Callaway, T. R. (2023) · Journal of Dairy Science · doi:10.3168/jds.2023-23831 · Cited by 47
Comparative studies on potential probiotic characteristics of Lactobacillus acidophilus strains
Dixit, G., Samarth, D. P., Tale, V. S., & Bhadekar, R. K. (2013) · Eurasian Journal of Biosciences · doi:10.5053/ejobios.2013.7.0.1 · Cited by 38
Biofunctional Attributes and Storage Study of Soy Milk Fermented by Lactobacillus rhamnosus and Lactobacillus helveticus
Mishra, B. K., Hati, S., Das, S., & Prajapati, J. B. (2019) · Food Technology and Biotechnology · doi:10.17113/ftb.57.03.19.6103 · Cited by 36
“) in fermented food and yoghurt starter cultures possess antioxidant activity in vitro and in vivo, inducing the antioxidant defence mechanism in the host (9).”
Background
Lactobacillus casei ssp. rhamnosus enhances non specific protection against Plasmodium chabaudi AS in mice
Martínez-Gómez, F., Ixta-Rodríguez, O., Aguilar-Figueroa, B. R., Hernández-Cruz, R., & Monroy-Ostria, A. (2006) · Salud Pública de México · doi:10.1590/s0036-36342006000600008 · Cited by 35
Production of fermented chestnut purees by lactic acid bacteria
Blaiotta, G., Capua, M. D., Coppola, R., & Aponte, M. (2012) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2012.07.012 · Cited by 35
“rhamnosusGG can exerts antagonistic activity against Gram-negative pathogens (Hudault et al., 1997; Lehto and Salminen, 1997; Fayol-Messaoudi et al., 2005, 2007; Makras et al., 2006).”
BackgroundResult
Microbiological and immunological strategies for treatment of inflammatory bowel disease
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“In addition, adherence of probiotics to intestinal epithelial cells and the ensuing temporary colonization of the gut are probably of crucial importance for their beneficial health effect (Bernet et al. 1994; Hudault et al. 1997).”
Background
Probiotic research priorities for the healthy adult population: A review on the health benefits of Lactobacillus rhamnosus GG and Bifidobacterium animalis subspecies lactis BB-12
Flach, J., van der Waal, M., Kardinaal, A., Schloesser, J., Ruijschop, R., & Claassen, E. (2018) · Cogent Food & Agriculture · doi:10.1080/23311932.2018.1452839 · Cited by 37
Application of Prebiotics and Probiotics in Livestock
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Bacteriocin production by strain Lactobacillus delbrueckii ssp. bulgaricus BB18 during continuous prefermentation of yogurt starter culture and subsequent batch coagulation of milk
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“Authors accentuate, however, on the possible production of these substances in vivo, as they are assumed to be one of the antagonistic mechanisms used by bacteria of the normal microXora against colonization by harmful microorganisms [24].”
Background
Mitsuokella jalaludinii inhibits growth of Salmonella enterica serovar Typhimurium
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Cell surface proteins play an important role in probiotic activities of Lactobacillus reuteri
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Changes in Microflora of the Cloaca and Oviduct of Hens after Intracloacal or Intravaginal Inoculation with Salmonella enteritidis
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Probiotics, prebiotics and gut health
Vuyst, L. D., Avonts, L., & Makras, L. (2004) · Elsevier eBooks · doi:10.1533/9781855739017.3.416 · Cited by 34
Protective Effect of Potential Probiotic Strains from Fermented Ethiopian Food against Salmonella Typhimurium DT104 in Mice
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“mice was significantly different at 4, 7, and 11 days after inoculation with Salmonella Typhimurium C5 [45].”
Background
Development of Marine Probiotics
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“Another report suggests that Lactobacillus exerts antagonist activity against Salmonella typhimurium C5 infection both in vitro and in vivo (Hudault et al., 1997).”
Background
Cheese whey fermented with kefir micro‐organisms: Antagonism against Salmonella and immunomodulatory capacity
Londero, A., Iraporda, C., Garrote, G. L., & Abraham, A. G. (2014) · International Journal of Dairy Technology · doi:10.1111/1471-0307.12161 · Cited by 30
The combination of mixed lactic acid bacteria and dietary fiber lowers serum cholesterol levels and fecal harmful enzyme activities in rats
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“The major effects of probiotics are their antagonistic effects against pathogens (Hudault et al., 1997) and their ability to disrupt intestinal dysfunction in the human gut (PoolZobel et al., 1993; Salminen et al., 1993).”
Background
Orally administeredLactobacillus plantarumreduces pro-inflammatory interleukin secretion in sera fromListeria monocytogenesinfected mice
Puertollano, E., Puertollano, M. A., Cruz-Chamorro, L., de Cienfuegos, G. Á., Ruiz‐Bravo, A., & PABLO, M. A. D. (2007) · British Journal Of Nutrition · doi:10.1017/s0007114507832533 · Cited by 30
VaginalLactobacillusisolates inhibit uropathogenicEscherichia coli
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“As positive control strain, we used the Lactobacillus rhamnosus strain GG that displays antibacterial activity (Hudault et al., 1997; Silva et al., 1987).”
Method
Isolation of human faecal bifidobacteria which reduce signs of Salmonella infection when orogastrically dosed to mice
Henriksson, A., & Conway, P. L. (2001) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2001.01238.x · Cited by 30
“Previous studies have demonstrated that speci®c strains of Lactobacillus casei and Lact. acidophilus have a similar effect by protecting conventional and germ-free animals from infection by Salm. typhimurium (Hudault et al. 1997; Bernet-Camard et al. 1997).”
BackgroundResult
Adhesion and Colonization of the Probiotic Lactobacillus rhamnosus Labeled by Dsred2 in Mouse Gut
Li, C., Bei, T., Niu, Z., Guo, X. N., Wang, M., Lu, H., Gu, X., & Tian, H. (2019) · Current Microbiology · doi:10.1007/s00284-019-01706-8 · Cited by 29
[Bacteria of Lactobacillus casei group: characterization, viability as probiotic in food products and their importance for human health].
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Probiotic Microorganisms
Lee, Y. K., Margollés, A., Mayo, B., Ruas‐Madiedo, P., Gueimonde, M., Reyes‐Gavilán, C. G. D. L., Chapman, T. A., Chin, J. J.-C., Crittenden, R. G., Donohue, D., et al. (2008) · Wiley eBooks · doi:10.1002/9780470432624.ch1 · Cited by 28
Evaluation of in vitro and in vivo adhesion and immunomodulatory effect of Lactobacillus species strains isolated from chickens
Rocha, T. S., Baptista, A. A. S., Donato, T. C., Milbradt, E. L., Okamoto, A. S., Rodrigues, J., Coppola, M. P., & Filho, R. L. A. (2012) · Poultry Science · doi:10.3382/ps.2011-01803 · Cited by 28
Probiotic Bacteria and Enteric Infections
Paton, A., Morona, R., & Paton, J. (2011) · Springer eBooks · doi:10.1007/978-94-007-0386-5 · Cited by 30
Lactobacillus plantarum inhibits growth of Listeria monocytogenes in an in vitro continuous flow gut model, but promotes invasion of L. monocytogenes in the gut of gnotobiotic rats
Bernbom, N., Licht, T. R., Saadbye, P., Vogensen, F. K., & Nørrung, B. (2006) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2005.10.021 · Cited by 28
Food Supplements to Mitigate Detrimental Effects of Pelvic Radiotherapy
Segers, C., Verslegers, M., Baatout, S., Leys, N., Lebeer, S., & Mastroleo, F. (2019) · Microorganisms · doi:10.3390/microorganisms7040097 · Cited by 27
“acidophilus LA towards Salmonella Typhimurium C5 was observed, both in vitro and in germ-free mice, without affecting the normal gut microbiota [186,187].”
Background
The Influence of Antibacterial and Antioxidative Probiotic Lactobacilli on Gut Mucosa in a Mouse Model ofSalmonellaInfection
Truusalu, K., Naaber, P., Kullisaar, T., Tamm, H., Mikelsaar, R.-H., Zilmer, K., Rehema, A., Zilmer, M., & Mikelsaar, M. (2004) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v16i4.7924 · Cited by 26
Lactobacillus in Food Animal Production—A Forerunner for Clean Label Prospects in Animal-Derived Products
Dewi, G., & Johny, A. K. (2022) · Frontiers in Sustainable Food Systems · doi:10.3389/fsufs.2022.831195 · Cited by 29
Coexpression of bile salt hydrolase gene and catalase gene remarkably improves oxidative stress and bile salt resistance in Lactobacillus casei
Wang, G., Yin, S., An, H., Chen, S., & Hao, Y. (2010) · Journal of Industrial Microbiology & Biotechnology · doi:10.1007/s10295-010-0871-x · Cited by 25
“Lactobacillus casei strains are commonly used in food fermentation, and several strains are recognized as putative candidates of probiotics [10].”
Background
Amelioration of intestinal and systemic sequelae of murine Campylobacter jejuni infection by probiotic VSL#3 treatment
Ekmekçiu, I., Fiebiger, U., Stingl, K., Bereswill, S., & Heimesaat, M. M. (2017) · Gut Pathogens · doi:10.1186/s13099-017-0168-y · Cited by 25
Antimicrobial potential of probiotic or potentially probiotic lactic acid bacteria, the first results of the international European research project PROPATH of the PROEUHEALTH cluster
Vuyst, L. D., Makras, L., Avonts, L., Holo, H., Yi, Q., Servin, A. L., Fayol-Messaoudi, D., Berger, C. N., Ζουμποπούλου, Γ., Tsakalidou, E., et al. (2004) · Microbial Ecology in Health and Disease · doi:10.1080/08910600410032303 · Cited by 25
“Typhimurium, and that blocks cell adhesion to Caco-2 cells and protects against infection in mice (31, 32).”
Background
Preclinical and Clinical Pharmacology of Biotherapeutic Agents:Saccharomyces boulardii
Periti, P., & Tonelli, F. (2001) · Journal of Chemotherapy · doi:10.1179/joc.2001.13.5.473 · Cited by 25
Characterization of Iturin V, a Novel Antimicrobial Lipopeptide from a Potential Probiotic Strain Lactobacillus sp. M31
Singh, S. S., Akhtar, M. N., Sharma, D., Mandal, S. M., & Korpole, S. (2021) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-021-09796-2 · Cited by 24
“Similarly, human cathelicidin LL37 has been shown to increase the IL-6 production [52, 53].”
Background
Impairment of Swimming Motility by Antidiarrheic Lactobacillus acidophilus Strain LB Retards Internalization of Salmonella enterica Serovar Typhimurium within Human Enterocyte-Like Cells
Moal, V. L.-L., Amsellem, R., & Servin, A. L. (2011) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.00418-11 · Cited by 24
“rhamnosus strain GG significantly decreased the translocation rate of Salmonella (25).”
Background
Kefir as a Probiotic Dairy Beverage: Determination Lactic Acid Bacteria and Yeast
Kıvanç, M., & YAPICI, E. (2015) · ETP International Journal of Food Engineering · doi:10.18178/ijfe.1.1.55-60 · Cited by 24
“[24] explained the role of lactobacilli in the prevention and treatment of gastrointestinal disorders.”
Background
Complete genome analysis of Lactobacillus fermentum SK152 from kimchi reveals genes associated with its antimicrobial activity
Yoo, D., Bagon, B. B., Valeriano, V. D., Oh, J. K., Kim, H., Cho, S., & Kang, D. (2017) · FEMS Microbiology Letters · doi:10.1093/femsle/fnx185 · Cited by 24
Clinical Management of the Microbiome in Irritable Bowel Syndrome
Andrews, C. N., Sidani, S., & Marshall, J. K. (2019) · Journal of the Canadian Association of Gastroenterology · doi:10.1093/jcag/gwz037 · Cited by 25
“(54)) and niche competition (55), and to inhibit cell invasion by pathogens (56).”
Background
Lactobacillus plantarum (VR1) isolated from an Ayurvedic medicine (Kutajarista) ameliorates in vitro cellular damage caused by Aeromonas veronii
Kumar, H., Rangrez, A. Y., Dayananda, K. M., Atre, A. N., Patole, M. S., & Shouche, Y. S. (2011) · BMC Microbiology · doi:10.1186/1471-2180-11-152 · Cited by 23
“coli [9,10], Helicobacter pylori [11], Salmonella typhimurium [12], Shigella dysenteriae [13], using in vitro and in vivo systems.”
Background
A synbiotic marine oligosaccharide microcapsules for enhancing Bifidobacterium longum survivability and regulatory on intestinal probiotics
Chang, L., Wang, P., Sun, S., Shen, Z., & Jiang, X. (2020) · International Journal of Food Science & Technology · doi:10.1111/ijfs.14650 · Cited by 23
Oral supplementation ofBifidobacterium longumstrain BR-108 alters cecal microbiota by stimulating gut immune system in mice irrespectively of viability
Makioka‐Itaya, Y., Tsukahara, T., 伊地知哲生, & Inoüe, R. (2018) · Bioscience Biotechnology and Biochemistry · doi:10.1080/09168451.2018.1451738 · Cited by 26
Histological examination of non-lactating bovine udders inoculated with Lactobacillus perolens CRL 1724
Frola, I. D., Pellegrino, M., Magnano, G., Giraudo, J., Espeche, M. C., Nader-Macı́as, M. E., & Bogni, C. I. (2012) · Journal of Dairy Research · doi:10.1017/s0022029912000581 · Cited by 22
“Other reports also showed that lactic acid bacterial strains with adhesion ability may hinder the contact between the epithelial cells and the pathogenic bacteria (Hudault et al. 1997; Coconnier et al. 2000).”
Background
Effect of Propionibacterium freudenreichii on Salmonella multiplication, motility, and association with avian epithelial cells
Nair, D. V. T., & Johny, A. K. (2016) · Poultry Science · doi:10.3382/ps/pew367 · Cited by 22
Protection of probiotic bacteria in a synbiotic matrix following aerobic storage at 4 °C
Chaluvadi, S., Hotchkiss, A. T., Call, J. E., Luchansky, J. B., Phillips, J. G., Liu, L., & Yam, K. L. (2012) · Beneficial Microbes · doi:10.3920/bm2012.0005 · Cited by 24
“Probiotic bacteria, primarily included in the genera Lactobacillus and Bifidobacterium, compete in the gastro-intestinal (GI) tract with pathogenic bacteria such as members of the Enterobacteriaceae family, and Clostridium difficile (Gibson and Wang, 1994; Hudault et al., 1997; Lievin et al., 2000).”
Background
An In Vitro Assay To Evaluate Competitive Exclusion Products for Poultry
Wagner, R. D., Holland, M. A., & Cerniglia, C. E. (2002) · Journal of Food Protection · doi:10.4315/0362-028x-65.5.746 · Cited by 22
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Supplementation of xylitol-containing chewing gum with probiotics: a double blind, randomised pilot study focusing on saliva flow and saliva properties
Gueimonde, L., Vesterlund, S., García-Pola, M., Gueimonde, M., Söderling, E. M., & Salminen, S. (2016) · Food & Function · doi:10.1039/c5fo01497b · Cited by 20
Dietary carbohydrates and the colonic microflora
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Antibacterial effects of probiotics isolated from yoghurts against some common bacterial pathogens
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Effect of culturing lactic acid bacteria with varying skim milk concentration on bacteria survival during heat treatment
Suo, X., Huang, S., Wang, J., Fu, N., Jeantet, R., & Chen, X. D. (2020) · Journal of Food Engineering · doi:10.1016/j.jfoodeng.2020.110396 · Cited by 19
“Lactobacillus rhamnosus GG exhibits antimicrobial activity against certain intestinal pathogens (De Keersmaecker et al., 2006; Hudault et al., 1997).”
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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