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Scientia Agriculturae Bohemica

The Journal of Czech University of Life Sciences Prague

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Effect Of Hydrolyzed Milk On The Adhesion Of Lactobacilli To Intestinal Cells*

T. Volštátová
  • Czech University of Life Sciences Prague, Faculty of Agrobiology, Food and Natural Resources, Prague, Czech Republic
  • Other articles by this author:
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/ J. Havlík
  • Corresponding author
  • Czech University of Life Sciences Prague, Faculty of Agrobiology, Food and Natural Resources, Prague, Czech Republic
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/ I. Doskočil
  • Czech University of Life Sciences Prague, Faculty of Agrobiology, Food and Natural Resources, Prague, Czech Republic
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/ M. Geigerová
  • Czech University of Life Sciences Prague, Faculty of Agrobiology, Food and Natural Resources, Prague, Czech Republic
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/ V. Rada
  • Czech University of Life Sciences Prague, Faculty of Agrobiology, Food and Natural Resources, Prague, Czech Republic
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Published Online: 2015-04-04 | DOI: https://doi.org/10.1515/sab-2015-0012


Milk is an essential part of the human diet and is undoubtedly a major calcium source in human nutrition, accepted well by most individuals. Knowledge on how the components from dairy products support or reduce the adherence of probiotics to the intestinal epithelium is limited. The purpose of this study was to investigate the effect of acid-hydrolyzed milk on the adhesion ability of two potentially probiotic strains (Lactobacillus plantarum S2, Lactobacillus gasseri R) to in vitro human intestinal epithelial model consisting of Caco-2 and mucus-secreting HT29-MTX co-culture. The adhesion of our tested strains L. gasseri and L. plantarum was 4.74 and 7.16%, respectively, when using inoculum of 2 × 108 CFU ml–1. Addition of acid-hydrolyzed milk to co-culture decreased the adherence by 53.7% for L. gasseri R and by 62.2% for L. plantarum S2. The results of this study evidently indicate the potential importance of the food matrix as a factor influencing probiotic colonization of the gut.

Key words: bacterial adhesion; acid-hydrolyzed milk; Lactobacillus gasseri R; Lactobacillus plantarum S2; cells of the small intestine; Caco-2; HT29-MTX


  • Almakhlafi H, McGuire J, Daeschel M (1994): Influence of preadsorbed milk-proteins on adhesion of Listeria monocytogenes to hydrophobic and hydrophilic silica surfaces. Applied and Environmental Microbiology, 60, 3560–3565.Google Scholar

  • Barnes LM, Lo MF, Adams MR, Chamberlain AHL (1999): Effect of milk proteins on adhesion of bacteria to stainless steel surfaces. Applied and Environmental Microbiology, 65, 4543–4548.PubMedGoogle Scholar

  • Bejar W, Farhat-Khemakhem A, Smaoui S, Makni M, Ben Farhat M, Abdelmalek B, Mellouli L, Maguin E, Bejar S, Chouayekh H (2011): Selection of Lactobacillus plantarum TN627 as a new probiotic candidate based on in vitro functional properties. Biotechnology and Bioprocess Engineering, 16, 1115–1123. doi: 10.1007/s12257-011-0198-0.Google Scholar

  • Brisson G, Payken HF, Sharpe JP, Jimenez-Flores R (2010): Characterization of Lactobacillus reuteri interaction with milk fat globule membrane components in dairy products. Journal of Agricultural and Food Chemistry, 58, 5612–5619. doi: 10.1021/jf904381s.CrossrefGoogle Scholar

  • Bustos I, García-Cayuela T, Hernández-Ledesma B, Peláez C, Requena T, Martínez-Cuesta MC (2012): Effect of flavan-3-ols on the adhesion of potential probiotic lactobacilli to intestinal cells. Journal of Agricultural and Food Chemistry, 60, 9082–9088. doi: 10.1021/jf301133g.PubMedCrossrefGoogle Scholar

  • Clarke SF, Murphy EF, O'Sullivan O, Lucey AJ, Humphreys M, Hogan A, Hayes P, O'Reilly M, Jeffery IB, Wood-Martin R, Kerins DM, Quigley E, Ross RP, O'Toole PW, Molloy MG, Falvey E, Shanahan F, Cotter PD (2014): Exercise and associated dietary extremes impact on gut microbial diversity. doi: 10.1136/gutjnl-2013-306541.CrossrefPubMedGoogle Scholar

  • Coconnier MH, Klaenhammer TR, Kerneis S, Bernet MF, Servin AL (1992): Protein-mediated adhesion of Lactobacillus acidophilus BG2FO4 on human enterocyte and mucussecreting cell lines in culture. Applied and Environmental Microbiology, 58, 2034–2039.Google Scholar

  • Collado MC, Meriluoto J, Salminen S (2008): Adhesion and aggregation properties of probiotic and pathogen strains. European Food Research and Technology, 226, 1065–1073. doi: 10.1007/s00217-007-0632-x.Web of ScienceCrossrefGoogle Scholar

  • Coppa GV, Zampini L, Galeazzi T, Facinelli B, Ferrante L, Capretti R, Orazio G (2006): Human milk oligosaccharides inhibit the adhesion to Caco-2 cells of diarrheal pathogens: Escherichia coli, Vibrio cholerae, and Salmonella fyris. Pediatric Research, 59, 377–382. doi: 10.1203/01.pdr.0000200805.45593.17.CrossrefGoogle Scholar

  • Del Re B, Sgorbati B, Miglioli M, Palenzona D (2000): Adhesion, autoaggregation and hydrophobicity of 13 strains of Bifidobacterium longum. Letters in Applied Microbiology, 31, 438–442. doi: 10.1046/j.1365-2672.2000.00845.x.CrossrefGoogle Scholar

  • Dhanani AS, Gaudana SB, Bagchi T (2011): The ability of Lactobacillus adhesin EF-Tu to interfere with pathogen adhesion. European Food Research and Technology, 232, 777–785. doi: 10.1007/s00217-011-1443-7.Web of ScienceCrossrefGoogle Scholar

  • Di Caro S, Tao H, Grillo A, Elia C, Gasbarrini G, Sepulveda AR, Gasbarrini A (2005): Effect of Lactobacillus GG on genes expression pattern in small bowel mucosa. Digestive and Liver Disease, 37, 320–329.CrossrefGoogle Scholar

  • Gagnon M, Zihler Berner A, Chervet N, Chassard C, Lacroix C (2013): Comparison of the Caco-2, HT-29 and the mucus-secreting HT29-MTX intestinal cell models to investigate Salmonella adhesion and invasion. Journal of Microbiological Methods, 94, 274–279. doi: 10.1016/j.mimet.2013.06.027.Web of SciencePubMedGoogle Scholar

  • García-Cayuela T, Korany AM, Bustos I, Gómez de Cadinaños LP, Requena T, Peláez C, Martínez-Cuesta MC (2014): Adhesion abilities of dairy Lactobacillus plantarum strains showing an aggregation phenotype. Food Research International, 57, 44–50. doi: 10.1016/j.foodres.2014.01.010.Web of ScienceCrossrefGoogle Scholar

  • Greene JD, Klaenhammer TR (1994): Factors involved in adherence of lactobacilli to human Caco-2 cells. Applied and Environmental Microbiology, 60, 4487–4494.PubMedGoogle Scholar

  • Janer C, Díaz J, Peláez C, Requena T (2004): The effect of caseinomacropeptide and whey protein concentrate on Streptococcus mutans adhesion to polystyrene surfaces and cell aggregation. Journal of Food Quality, 27, 233–238. doi: 10.1111/j.1745-4557.2004.tb00652.x.CrossrefGoogle Scholar

  • Jensen H, Grimmer S, Naterstad K, Axelsson L (2012): In vitro testing of commercial and potential probiotic lactic acid bacteria. International Journal of Food Microbiology, 153, 216–222. doi: 10.1155/2008/357964.CrossrefGoogle Scholar

  • Kmeť V, Drugdová Z (2012): Antimicrobial susceptibility of microflora from ovine cheese. Folia Microbiologica, 57, 291–293. doi: 10.1007/s12223-012-0128-3.CrossrefPubMedWeb of ScienceGoogle Scholar

  • Laparra JM, Sanz Y (2009): Comparison of in vitro models to study bacterial adhesion to the intestinal epithelium. Letters in Applied Microbiology, 49, 695–701. doi: 10.1111/j.1472-765X.2009.02729.x.CrossrefWeb of ScienceGoogle Scholar

  • Martínez-Maqueda D, Miralles B, Cruz-Huerta E, Recio I (2013): Casein hydrolysate and derived peptides stimulate mucin secretion and gene expression in human intestinal cells. International Dairy Journal, 32, 13–19. doi: 10.1016/j.idairyj.2013.03.010.CrossrefGoogle Scholar

  • Mattar AF, Teitelbaum DH, Drongowski RA, Yongyi F, Harmon CM, Coran AG (2002): Probiotics up-regulate MUC-2 mucin gene expression in a Caco-2 cell-culture model. Pediatric Surgery International, 18, 586–590. doi: 10.1007/s00383-002-0855-7.CrossrefGoogle Scholar

  • Oliveira R (1997): Understanding adhesion: a means for preventing fouling. Experimental Thermal and Fluid Science, 14, 316–322. doi: 10.1016/S0894-1777(96)00134-3.CrossrefGoogle Scholar

  • Ouwehand AC, Salminen SJ (1998): The health effects of cultured milk products with viable and non-viable bacteria. International Dairy Journal, 8, 749–758. doi: 10.1016/S0958-6946(98)00114-9.CrossrefGoogle Scholar

  • Ouwehand AC, Tuomola EM, Tolkko S, Salminen S (2001): Assessment of adhesion properties of novel probiotic strains to human intestinal mucus. International Journal of Food Microbiology, 64, 119–126. doi: 10.1016/S0168-1605(00)00440-2.PubMedCrossrefGoogle Scholar

  • Ouwehand AC, Salminen S, Isolauri E (2002): Probiotics: an overview of beneficial effects. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 82, 279–289. doi: 10.1007/978-94-017-2029-8_18.CrossrefGoogle Scholar

  • Parkar SG, Stevenson DE, Skinner MA (2008): The potential influence of fruit polyphenols on colonic microflora and human gut health. International Journal of Food Microbiology, 124, 295–298. doi: 10.1016/j.ijfoodmicro.2008.03.017.PubMedWeb of ScienceCrossrefGoogle Scholar

  • Phelan M, Aherne-Bruce SA, O'Sullivan D, Fitzgerald RJ, O'Brien NM (2009): Potential bioactive effects of casein hydrolysates on human cultured cells. International Dairy Journal, 19, 279–285. doi: 10.1016/j.idairyj.2008.12.004.Web of ScienceCrossrefGoogle Scholar

  • Reniero R, Cocconcelli P, Bottazi V, Morelli L (1992): High frequency of conjugation in Lactobacillus mediated by an aggregation-promoting factor. Journal of General Microbiology, 138, 763–768. doi: 10.1099/00221287-138-4-763.CrossrefGoogle Scholar

  • Rojas M, Ascencio F, Conway PL (2002): Purification and characterization of a surface protein from Lactobacillus fermentum 104R that binds to porcine small intestinal mucus and gastric mucin. Applied and Environmental Microbiology, 68, 2330–2336. doi: 10.1128/AEM.68.5.2330-2336.2002.CrossrefGoogle Scholar

  • Roos S, Jonsson H (2002): A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology, 148, 433–442.CrossrefPubMedGoogle Scholar

  • Strömqvist M, Falk P, Bergström S, Hansson L, Lönnerdal B, Normark S, Hernell O (1995): Human milk κ-casein and inhibition of Helicobacter pylori adhesion to human gastric mucosa. Journal of Pediatric Gastroenterology and Nutrition, 21, 288–296. doi: 10.1097/00005176-199510000-00006.CrossrefGoogle Scholar

  • Tuomola EM, Salminen SJ (1998): Adhesion of some probiotic and dairy Lactobacillus strains to Caco-2 cell cultures. International Journal of Food Microbiology, 41, 45–51. doi: 10.1016/S0168-1605(98)00033-6.CrossrefPubMedGoogle Scholar

  • Vlková E, Rada V, Šmehilová M, Killer J (2008): Auto-aggregation and co-aggregation ability in bifidobacteria and clostridia. Folia Microbiologica, 53, 263–269. doi: 10.1007/s12223-008-0040-z.Web of SciencePubMedCrossrefGoogle Scholar

  • Wang B, Wei H, Yuan J, Li Q, Li Y, Li N, Li J (2008): Identification of a surface protein from Lactobacillus reuteri JCM1081 that adheres to porcine gastric mucin and human enterocyte-like HT-29 cells. Current Microbiology, 57, 33–38. doi: 10.1007/s00284-008-9148-2.CrossrefPubMedGoogle Scholar

About the article

Received: 2014-11-05

Accepted: 2015-01-11

Published Online: 2015-04-04

Published in Print: 2015-03-01

*Supported by the Internal Grant Agency of the Czech University of Life Sciences Prague (CIGA), Project No. 20142013, and by Ministry of Education, Youth and Sports of the Czech Republic, Project No. LD14070.

Citation Information: Scientia Agriculturae Bohemica, Volume 46, Issue 1, Pages 21–25, ISSN (Online) 1805-9430, ISSN (Print) 1211-3174, DOI: https://doi.org/10.1515/sab-2015-0012.

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