Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract
Abstract
An in vitro methodology which mimics in vivo human upper gastrointestinal transit was developed. The transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species was determined by exposing washed cell suspensions at 37 degrees C to a simulated gastric juice (pH 2.0), containing pepsin (0.3% w/v) and sodium chloride (0.5% w/v), and a simulated small intestinal juice (pH 8.0), containing pancreatin USP (1 g l-1) and sodium chloride (5 g l-1), and monitoring changes in total viable count periodically. The methodology was also employed to determine the effect of adding milk proteins (1 g l-1), hog gastric mucin (1 g l-1) and soyabean trypsinchymotrypsin inhibitor [SBTCI] (1 g l-1) on transit tolerance. The majority (14 of 15) of isolates lost > 90% viability during simulated gastric transit. Only one isolate, Lactobacillus fermentum KLD, was considered intrinsically resistant. The addition of milk proteins, singly and in combination, generally improved gastric transit tolerance. In this regard, two isolates, Lact. casei 212.3 and Bifidobacterium infantis 25962, exhibited 100% gastric transit tolerance in the presence of milk proteins. In general, the addition of hog gastric mucin did not influence simulated gastric transit tolerance of lactobacilli but tended to increase that of bifidobacteria. However, it increased that of Lact. casei 242 and Lact. salivarius 43338 but diminished that of B. bifidum 2715 and B. animalis Bo. Selected bile salts-resistant isolates were intrinsically tolerant to simulated small intestinal transit. Only Lact. casei F19 and B. adolescentis 15703T showed significant reduction in viability after 240 min. In general, the addition of milk proteins and SBTCI did not affect simulated small intestinal transit tolerance. However, they significantly improved the intrinsic resistance of Lact. casei F19 but diminished that of B. breve 15700T. It is concluded that, whereas the majority of bile salts-resistant lactobacilli and bifidobacteria may be intrinsically sensitive to gastric transit, they are intrinsically resistant to small intestinal transit. In addition, it is postulated that milk proteins and mucin may function as both buffering agents and inhibitors of digestive protease activity in vivo, thereby protecting ingested bacterial strains during upper gastrointestinal transit.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Acid and bile tolerance are widely recognized essential selection criteria for probiotics because they reflect the ability to survive gastric acidity and small intestine bile salts, critical for in vivo persistence and functional efficacy.
“Acid and bile tolerance are widely recognized essential selection criteria, as they reflect the ability of microorganisms to survive gastric acidity and small intestine bile salts, critical for their in vivo persistence and functional efficacy [36, 37].”
From Comparative Genomics-Based Evaluation of <i>Lacticaseibacillus rhamnosus</i> KFOM 0134 as a Probiotic against <i>Staphylococcus aureus</i> (2026) · cites this paper as [36]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Still being checked.
Research works printed but not linked: 38
- Allen, A. (1981) Structure and function of gastrointestinal mucus. In Physiology of the Gastrointestinal Tract ed. Johnson, L.R. Chap. 20, pp. 617-639. New York: Raven Press.
- Alm, L., Leijonmarck, C-E., Persson, A-K. and Midtvedt, T. (1989) Survival of lactobacilli during digestion: an in vitro and in vivo study. In The Regulatory and Protective Role of the Normal Microflora ed. Grubb, R., Midtvedt, T. and Norin, E. Chap. 18, pp. 293-297. London: Macmillan Press.
- Berrada, N., Lemeland, J-F., Laroche, G., Thouvenot, P. and Piaia, M. (1991) Bifidobacterium from fermented milks: survival during gastric transit. Journal of Dairy Science 74 , 409-413.
- Charteris, W.P., O'Neill, E.T. and Kelly, P.M. (1994) An in vitro method to determine human gastric transit tolerance among potentially probiotic lactic acid bacteria and bifidobacteria. Irish Journal of Agricultural Food Research 33(2) , 203.
- Charteris, W.P., Kelly, P.M., Morelli, L. and Collins, J.K. (1997) Selective detection, enumeration and identification of potentially probiotic Lactobacillus and Bifidobacterium species in mixed bacterial populations. International Journal of Food Microbiology 35(1) , 1-17.
- Chauvie `re, G., Coconnier, M-H., Kerne `is, S., Fourniat, J. and Servin, A.L. (1992) Adhesion of human Lactobacillus acidophilus strain LB to human enterocyte-like Caco-2 cells. Journal of General Microbiology 138 , 1689-1696.
- Clark, P.A. and Martin, J.H. (1993) Survival of bifidobacteria under in vitro conditions simulating the human stomach. Abstract D139. Journal of Dairy Science 76 (Suppl. 1), 136.
- Clark, P.A., Cotton, L.N. and Martin, J.H. (1993) Selection of bifidobacteria for use as dietary adjuncts in cultured dairy foods: II-Tolerance to simulated pH of human stomachs. Cultured Dairy Products Journal 11 , 11-14.
- Conway, P.L., Gorbach, S.L. and Goldin, B.R. (1987) Survival of lactic acid bacteria in the human stomach and adhesion to intestinal cells. Journal of Dairy Science 70 , 1-12.
- Crociani, J., Grill, J-P., Huppert, M. and Ballongue, J. (1995) Adhesion of different bifidobacteria strains to human enterocytelike Caco-2 cells and comparison with in vivo study. Letters in Applied Microbiology 21 , 146-148.
- de Man, J.C., Rogosa, M. and Sharpe, M.E. (1960) A medium for cultivation of lactobacilli. Journal of Applied Bacteriology 23(1) , 130-135.
- Driessen, F.M. and de Boer, R. (1980) Fermented milks with selected intestinal bacteria: a healthy trend in new products. Netherlands Milk and Dairy Journal 43 , 367-382.
- Eisenstadt, E. et al . (1993) Gene mutation. In Methods for General Molecular Microbiology ed. Gerhardt, P. et al . Chap. 13, pp. 297316. Washington: American Society of Microbiology.
- Elo, S., Saxelin, M. and Salminen, S. (1991) Attachment of Lactobacillus casei strain GG to human colon carcinoma cell line Caco2: comparison with other dairy strains. Letters in Applied Microbiology 13 , 154-156.
- Fuller, R. (1992) History and development of probiotics. In Probiotics: The Scientific Basis ed. Fuller, R. Chap. 1, pp. 1-8. London: Chapman & Hall.
- Hill, M.J. (1990) Factors controlling the microflora of the healthy upper gastrointestinal tract. In Human Microbial Ecology ed. Hill, M.J. and Marsh, P.D. Chap. 2, pp. 57-85. Boca Raton, Florida: CRC Press.
- Hood, S.K. and Zottola, E.A. (1988) Effect of low pH on the ability of Lactobacillus acidophilus to survive and adhere to human intestinal cells. Journal of Food Science 53 , 1514-1516.
- Hove, H., Nordgaard-Andersen, I. and Mortensen, P.B. (1994) Effect of lactic acid bacteria on the intestinal production of lactate and short-chain fatty acids, and the absorption of lactose. American Journal of Clinical Nutrition 59(1) , 74-79.
- Jones, D., Pell, P.A. and Sneath, P.H.A. (1984) Maintenance of bacteria on glass beads at 60°C to 70°C. In Maintenance of Microorganisms ed. Kirsop, B.E. and Snell, J.J.S. Chap. 5, pp. 35-40. London: Academic Press.
- Keele, C.A. and Neil, E. (1965) Secretion of digestive juices. In Samson Wright's Applied Physiology , 11th edn. Chap. 60, pp. 353363. London: Oxford University Press.
- Klaenhammer, T.R. (1982) Microbiological considerations in the selection and preparation of Lactobacillus strains for use as dietary adjuncts. Journal of Dairy Science 65 , 1339-1349.
- Kolars, J.C., Levitt, M.D., Aouji, M. and Savaiano, D.A. (1984) Yoghurt: an autodigesting source of lactose. New England Journal of Medicine 310 , 1-3.
- Lindwall, S. and Fonde ´n, R. (1984) Passage and survival of L. acidophilus in the human gastrointestinal tract. IDF Bulletin 179 , 21.
- Ling, W.H., Ha ¨nninen, O., Mykka ¨nen, H., Salminen, S. and von Wright, A. (1992) Colonisation and faecal enzyme activities after oral Lactobacillus GG administration in elderly nursing home residents. Annals of Nutrition and Metabolism 36 , 162-166.
- Marteau, P., Pochart, P., Bouhnik, Y. and Rambaud, J-C. (1993) The fate and effects of transiting, non-pathogenic micro-organisms in the human intestine. In World Review of Nutrition and Dietetics . Vol. 74. Intestinal Flora, Immunity, Nutrition and Health ed. Simopoulos, A.P., Corring, T. and Re ´rat, A. Chap. 1, pp. 121. London: Krager.
- Mikelsaar, M. and Ma ¨ndar, R. (1994) Development of individual lactic acid microflora in the human microbial ecosystem. In Lactic Acid Bacteria ed. Salminen, S. and von Wright, A. Chap. 9, pp. 237-293. New York: Marcel Dekker Inc.
- Molin, G., Jeppson, B., Johansson, M-L., Ahrne ´, S., Nobaek, S., Sta ˚hl, M. and Bengmark, S. (1993) Numerical taxonomy of Lactobacillus spp. associated with healthy and diseased mucosa of the human intestines. Journal of Applied Bacteriology 74 , 314-323.
- Pettersson, L., Graf, W., Alm, L., Lindwall, S. and Stromberg, A. (1983) Survival of Lactobacillus acidophilus NCDO 1748 in the human gastrointestinal tract. 1. Incubation with gastric juice in vitro . In Nutrition and the intestinal flora Swedish Nutrition Foundation Symposium XV. ed. Hallgren, B. pp. 123-127. Uppsala: Almqvist & Wiksell.
- Pettersson, L., Graf, W. and Sewelin, V. (1985) Survival of Lactobacillus acidophilus NCDO 1748 in the human gastrointestinal tract. 2. Ability to pass through the stomach and intestine in vivo . In Nutrition and the intestinal flora Swedish Nutrition Foundation Symposium XV. ed. Hallgren, B. pp. 127-130. Uppsala: Almqvist & Wiksell.
- Pochart, P., Marteau, P., Bouhnik, Y., Goderel, I., Bourlioux, P. and Rambaud, J.C. (1992) Survival of bifidobacteria ingested in a fermented milk during passage in the upper gastrointestinal tract: an in vivo study using intestinal perfusion. American Journal of Clinical Nutrition 55 , 78-80.
- Rambaud, J-C., Bouhnik, Y., Marteau, P. and Pochart, P. (1993) Manipulation of the human gut microflora. Proceedings of the Nutrition Society 52 , 357-366.
- Robins-Browne, R.M. and Levine, M.M. (1981) The fate of ingested lactobacilli in the proximal intestine. American Journal of Clinical Nutrition 34 , 514-519.
- Sakai, K., Mishima, T., Tachiki, T., Kumagai, H. and Tochikura, T. (1987) Mortality of bifidobacteria in boiled yoghurt. Journal of Fermentation Technology 65 , 215-220.
- Sarem-Damerdji, L-O., Sarem, F., Marchal, L. and Nicolas, J-P. (1995) In vitro colonisation ability of human colon mucosa by exogenous Lactobacillus strains. FEMS Microbiology Letters 131 , 133-137.
- Savaiano, D.A., El Anous, A., Smith, D.E. and Levitt, M.D. (1984) Lactose malabsorption from yoghurt, pasteurised yoghurt, sweet acidophilus milk and cultured milk in lactase-deficient individuals. American Journal of Clinical Nutrition 40 , 1219-1223.
- Scardovi, V. (1988) Irregular non-sporeforming Gram-positive rods. Genus Bifidobacterium Orla-Jensen 1924. In Bergey's Manual of Determinative Bacteriology , Vol. 2. Section 15, pp. 14181434. Baltimore: Williams & Wilkins.
- Sims, W. (1964) The effect of mucin on the survival of lactobacilli and Streptococci. Journal of General Microbiology 37 , 335-340.
- Tunnicliff, R. (1940) Action of gastric and salivary mucin on phagocytosis. Journal of Infectious Disease 66 , 189.
Cited by
Sorted by citations
Surviving the Acid Test: Responses of Gram-Positive Bacteria to Low pH
Cotter, P. D., & Hill, C. (2003) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.67.3.429-453.2003 · Cited by 1,378 · see citing works
Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens
Servin, A. L. (2004) · FEMS Microbiology Reviews · doi:10.1016/j.femsre.2004.01.003 · Cited by 1,234 · see citing works
Microencapsulation of probiotics for gastrointestinal delivery
Cook, M. T., Tzortzis, G., Charalampopoulos, D., & Khutoryanskiy, V. V. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.06.003 · Cited by 770 · see citing works
Probiotic potential of Lactobacillus strains isolated from dairy products
Maragkoudakis, P. A., Zoumpopoulou, G., Miaris, C., Kalantzopoulos, G., Pot, B., & Tsakalidou, E. (2006) · International Dairy Journal · doi:10.1016/j.idairyj.2005.02.009 · Cited by 618 · see citing works
Vinderola, C. G., & Reinheimer, J. A. (2003) · Food Research International · doi:10.1016/s0963-9969(03)00098-x · Cited by 570 · see citing works
Probiotics—From Metchnikoff to bioactives
Vasiljevic, T., & Shah, N. P. (2008) · International Dairy Journal · doi:10.1016/j.idairyj.2008.03.004 · Cited by 564 · see citing works
Kristensen, N. B., Bryrup, T., Allin, K. H., Nielsen, T., Hansen, T. H., & Pedersen, O. (2016) · Genome Medicine · doi:10.1186/s13073-016-0300-5 · Cited by 561 · see citing works
Picot, A., & Lacroix, C. (2004) · International Dairy Journal · doi:10.1016/j.idairyj.2003.10.008 · Cited by 549 · see citing works
Corcoran, B. M., Stanton, C., Fitzgerald, G. F., & Ross, R. P. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.6.3060-3067.2005 · Cited by 547 · see citing works
de Vries, M. C., Vaughan, E. E., Kleerebezem, M., & de Vos, W. M. (2006) · International Dairy Journal · doi:10.1016/j.idairyj.2005.09.003 · Cited by 516 · see citing works
Probiotic Gastrointestinal Transit and Colonization After Oral Administration: A Long Journey
Han, S., Lu, Y., Xie, J., Fei, Y., Zheng, G., Wang, Z., Liu, J., Lv, L., Ling, Z., Berglund, B., et al. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.609722 · Cited by 498 · see citing works
Hansen, L. T., Allan‐Wojtas, P., Jin, Y., & PAULSON, A. T. (2002) · Food Microbiology · doi:10.1006/fmic.2001.0452 · Cited by 472 · see citing works
Probiotic properties of human lactobacilli strains to be used in the gastrointestinal tract
Fernández, M. F., Boris, S., & Barbés, C. (2003) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2003.01850.x · Cited by 441 · see citing works
Lactic acid bacteria as probiotics.
Ljungh, Å., & Wadström, T. (2006) · PubMed · Cited by 427 · see citing works
Bao, Y., Zhang, Y., Zhang, Y., Liu, Y., Wang, S., Dong, X., Wang, Y., & Zhang, H. (2009) · Food Control · doi:10.1016/j.foodcont.2009.10.010 · Cited by 395 · see citing works
Discovering probiotic microorganisms: in vitro, in vivo, genetic and omics approaches
Papadimitriou, K., Ζουμποπούλου, Γ., Foligné, B., Alexandraki, V., Κάζου, Μ., Pot, B., & Tsakalidou, E. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00058 · Cited by 388 · see citing works
Huang, Y., & Adams, M. C. (2003) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2003.07.001 · Cited by 367 · see citing works
Annan, N. T., Borza, A., & Hansen, L. T. (2007) · Food Research International · doi:10.1016/j.foodres.2007.11.001 · Cited by 352 · see citing works
Sources, isolation, characterisation and evaluation of probiotics
Fontana, L., Bermudez-Brito, M., Plaza-Diaz, J., Muñoz-Quezada, S., & Gil, A. (2013) · British Journal of Nutrition · doi:10.1017/s0007114512004011 · Cited by 348 · see citing works
Shokryazdan, P., Sieo, C. C., Ramasamy, K., Liang, J. B., Alitheen, N. B., Jahromi, M. F., & Ho, Y. W. (2014) · BioMed Research International · doi:10.1155/2014/927268 · Cited by 331 · see citing works
Improved survival of Lactobacillus paracasei NFBC 338 in spray-dried powders containing gum acacia
Desmond, C., Ross, R. P., O’Callaghan, E. J., Fitzgerald, G. F., & Stanton, C. (2002) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.2002.01782.x · Cited by 317 · see citing works
Effect of alginate concentrations on survival of microencapsulated Lactobacillus casei NCDC-298
Mandal, S., Puniya, A. K., & Singh, K. P. (2006) · International Dairy Journal · doi:10.1016/j.idairyj.2005.10.005 · Cited by 315 · see citing works
Campana, R., van Hemert, S., & Baffone, W. (2017) · Gut Pathogens · doi:10.1186/s13099-017-0162-4 · Cited by 308 · see citing works
Shehata, M. G., Sohaimy, S. A. E., El-Sahn, M. A., & Youssef, M. (2016) · Annals of Agricultural Science Cairo · doi:10.1016/j.aoas.2016.03.001 · Cited by 307 · see citing works
Overcoming the technological hurdles in the development of probiotic foods
Ross, R. P., Desmond, C., Fitzgerald, G. F., & Stanton, C. (2005) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2005.02654.x · Cited by 300 · see citing works
Antibiotic resistance among commercially available probiotics
Sharma, P., Tomar, S. K., Goswami, P., Sangwan, V., & Singh, R. (2014) · Food Research International · doi:10.1016/j.foodres.2014.01.025 · Cited by 300 · see citing works
St‐Onge, M., Farnworth, E. R., & Jones, P. J. H. (2000) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/71.3.674 · Cited by 286 · see citing works
Nawaz, M., Wang, J., Zhou, A., Ma, C., Wu, X., Moore, J. E., Cherie Millar, B., & Xu, J. (2011) · Current Microbiology · doi:10.1007/s00284-010-9856-2 · Cited by 281 · see citing works
Probiotic Potential of 3 Lactobacilli Strains Isolated From Breast Milk
Martı́n, R., Olivares, M. M., Marín, M. L., Fernández, L., Xaus, J., & Rodríguez, J. M. (2005) · Journal of Human Lactation · doi:10.1177/0890334404272393 · Cited by 279 · see citing works
Cholesterol-Lowering Nutraceuticals and Functional Foods
Chen, Z., Jiao, R., & Ma, K. Y. (2008) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf801566r · Cited by 275 · see citing works
Application of in vitro methods for selection of Lactobacillus casei strains as potential probiotics
Mishra, V., & Prasad, D. N. (2005) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2004.10.047 · Cited by 273 · see citing works
Liu, H., Wang, S., Cai, Y., Guo, X., Cao, Z., Zhang, Y., Liu, S., Yuan, W., Zhu, W., Zheng, Y., et al. (2016) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2016.12.003 · Cited by 269 · see citing works
In vitro adherence and other properties of lactobacilli used in probiotic yoghurt-like products
Schillinger, U., Guigas, C., & Holzapfel, W. H. (2005) · International Dairy Journal · doi:10.1016/j.idairyj.2004.12.008 · Cited by 264 · see citing works
Madureira, A. R., Amorim, M., Gomes, A., Pintado, M., & Malcata, F. X. (2010) · Food Research International · doi:10.1016/j.foodres.2010.09.010 · Cited by 261 · see citing works
A dynamic model that simulates the human upper gastrointestinal tract for the study of probiotics
Mainville, I., Arcand, Y., & Farnworth, E. R. (2004) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2004.08.020 · Cited by 247 · see citing works
Lactobacillus fermentumME-3 – an antimicrobial and antioxidative probiotic
Mikelsaar, M., & Zilmer, M. (2009) · Microbial Ecology in Health and Disease · doi:10.1080/08910600902815561 · Cited by 225 · see citing works
Charalampopoulos, D., Pandiella, S. S., & Webb, C. (2003) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(02)00248-9 · Cited by 223 · see citing works
Pereira, D. I. A., McCartney, A. L., & Gibson, G. R. (2003) · Applied and Environmental Microbiology · doi:10.1128/aem.69.8.4743-4752.2003 · Cited by 215 · see citing works
Technologies with free and immobilised cells for probiotic bifidobacteria production and protection
Doleyres, Y., & Lacroix, C. (2005) · International Dairy Journal · doi:10.1016/j.idairyj.2004.11.014 · Cited by 214 · see citing works
Brinques, G. B., & Ayub, M. A. Z. (2010) · Journal of Food Engineering · doi:10.1016/j.jfoodeng.2010.10.006 · Cited by 210 · see citing works
Santini, C., Baffoni, L., Gaggìa, F., Granata, M., Gasbarri, R., Gioia, D. D., & Biavati, B. (2010) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2010.03.039 · Cited by 210 · see citing works
Health‐beneficial effects of probiotics: Its mode of action
OHASHI, Y., & USHIDA, K. (2009) · Animal Science Journal · doi:10.1111/j.1740-0929.2009.00645.x · Cited by 209 · see citing works
Intestinal microflora of human infants and current trends for its nutritional modulation
Mountzouris, K. C., McCartney, A. L., & Gibson, G. R. (2002) · British Journal Of Nutrition · doi:10.1079/bjnbjn2002563 · Cited by 207 · see citing works
In vitro testing of commercial and potential probiotic lactic acid bacteria
Jensen, H., Grimmer, S., Naterstad, K., & Axelsson, L. T. (2011) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2011.11.020 · Cited by 205 · see citing works
Monteagudo-Mera, A., Rodrı́guez-Aparicio, L. B., Rúa, J., Martı́nez-Blanco, H., Navasa, N., García‐Armesto, M. R., & Ferrero, M. Á. M. (2012) · Journal of Functional Foods · doi:10.1016/j.jff.2012.02.014 · Cited by 203 · see citing works
Vesa, Pochart, & Marteau (2000) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.2000.00763.x · Cited by 200 · see citing works
Guo, Z., Wang, J., Yan, L., Chen, W., Liu, X., & Zhang, H. (2009) · LWT · doi:10.1016/j.lwt.2009.05.025 · Cited by 196 · see citing works
Mathara, J. M., Schillinger, U., Guigas, C., Franz, C. M. A. P., Kutima, P. M., Mbugua, S. K., Shin, H. C., & Holzapfel, W. H. (2008) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2008.04.027 · Cited by 189 · see citing works
Molecular and physiological comparisons betweenSaccharomyces cerevisiaeandSaccharomyces boulardii
Fietto, J. L. R., Araújo, R. S., Valladão, F. N., Fietto, L. G., Brandão, R. L., Neves, M. J., Gomes, F. C. O., Nicoli, J. R., & Castro, I. M. (2004) · Canadian Journal of Microbiology · doi:10.1139/w04-050 · Cited by 189 · see citing works
Moayyedi, M., Eskandari, M. H., Rad, A. H. E., Ziaee, E., Khodaparast, M. H. H., & Golmakani, M. (2017) · Journal of Functional Foods · doi:10.1016/j.jff.2017.11.016 · Cited by 188 · see citing works
Saarela, M., Virkajärvi, I., Alakomi, H., Sigvart-Mattila, P., & Mättö, J. (2006) · International Dairy Journal · doi:10.1016/j.idairyj.2005.12.007 · Cited by 184 · see citing works
Cislaghi, F. P. D. C., Silva, C. D. R. E., Fritzen‐Freire, C. B., Lorenz, J. G., & Sant’Anna, E. S. (2012) · Journal of Food Engineering · doi:10.1016/j.jfoodeng.2012.06.006 · Cited by 184 · see citing works
New insights in antibiotic resistance of Lactobacillus species from fermented foods
Abriouel, H., Muñoz, M. D. C. C., Lerma, L. L., Montoro, B. P., Bockelmann, W., Pichner, R., Kabisch, J., Cho, G., Franz, C. M. A. P., Gálvez, A., et al. (2015) · Food Research International · doi:10.1016/j.foodres.2015.09.016 · Cited by 188 · see citing works
Microbial-Based and Microbial-Targeted Therapies for Inflammatory Bowel Diseases
Oka, A., & Sartor, R. B. (2020) · Digestive Diseases and Sciences · doi:10.1007/s10620-020-06090-z · Cited by 185 · see citing works
Importance of S-layer proteins in probiotic activity of Lactobacillus acidophilus M92
Frece, J., Kos, B., Svetec, I., Zgaga, Z., Mrša, V., & Suskovic, J. (2005) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2004.02473.x · Cited by 179 · see citing works
Azcárate-Peril, M. A., Altermann, E., Goh, Y. J., Tallon, R., Sanozky-Dawes, R., Pfeiler, E. A., O’Flaherty, S., Buck, B. L., Dobson, A., Duong, T., et al. (2008) · Applied and Environmental Microbiology · doi:10.1128/aem.00054-08 · Cited by 177 · see citing works
Zárate, G., Chaia, A. P., González, S., & Oliver, G. (2000) · Journal of Food Protection · doi:10.4315/0362-028x-63.9.1214 · Cited by 176 · see citing works
de Souza, B. M. S., Borgonovi, T. F., Casarotti, S. N., Todorov, S. D., & Penna, A. L. B. (2019) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-018-9406-y · Cited by 177 · see citing works
The Use of Lactic Acid Bacteria as a Probiotic in Swine Diets
Yang, F., Hou, C., Zeng, X., & Qiao, S. (2015) · Pathogens · doi:10.3390/pathogens4010034 · Cited by 172 · see citing works
Effect of prebiotic carbohydrates on the growth and tolerance of Lactobacillus
Hernández‐Hernández, O., Muthaiyan, A., Moreno, F. J., Montilla, A., Sanz, M. L., & Ricke, S. C. (2012) · Food Microbiology · doi:10.1016/j.fm.2011.12.022 · Cited by 171 · see citing works
In vitro selection of probiotic lactobacilli: a critical appraisal.
Morelli, L. (2000) · PubMed · Cited by 171 · see citing works
Numbers and strains of lactobacilli in some probiotic products
Coeuret, V., Guéguen, M., & Vernoux, J. (2004) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2004.04.015 · Cited by 170 · see citing works
Survival of Microencapsulated Probiotic Bacteria after Processing and during Storage: A Review
Dianawati, D., Mishra, V. K., & Shah, N. P. (2015) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2013.798779 · Cited by 170 · see citing works
St-Onge, M.-P., Farnworth, E. R., Savard, T., Chabot, D., Mafu, A., & Jones, P. J. (2002) · BMC Complementary and Alternative Medicine · doi:10.1186/1472-6882-2-1 · Cited by 167 · see citing works
Gardiner, G., Stanton, C., Lynch, P. B., Collins, J. K., Fitzgerald, G., & Ross, R. P. (1999) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(99)75363-4 · Cited by 165 · see citing works
A novel eukaryotic cell culture model to study antiviral activity of potential probiotic bacteria
Botić, T., Klingberg, T. D., Weingartl, H., & Cencič, A. (2007) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2006.10.044 · Cited by 163 · see citing works
Ren, D., Li, C., Qin, Y., Yin, R., Du, S., Ye, F., Liu, C., Liu, H., Wang, M., Li, Y., et al. (2014) · Anaerobe · doi:10.1016/j.anaerobe.2014.07.004 · Cited by 163 · see citing works
Immobilization Technologies in Probiotic Food Production
Mitropoulou, G., Nedović, V., Goyal, A., & Kourkoutas, Y. (2013) · Journal of Nutrition and Metabolism · doi:10.1155/2013/716861 · Cited by 161 · see citing works
Viability of microencapsulated bifidobacteria in simulated gastric juice and bile solution
Lian, W.-C. (2003) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(02)00563-9 · Cited by 159 · see citing works
Targeted delivery of probiotics to enhance gastrointestinal stability and intestinal colonisation
Dodoo, C. C., Wang, J., Basit, A. W., Stapleton, P. D., & Gaisford, S. (2017) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2017.07.068 · Cited by 156 · see citing works
Wang, C.-Y., Lin, P.-R., Ng, C.-C., & Shyu, Y.-T. (2010) · Anaerobe · doi:10.1016/j.anaerobe.2010.10.003 · Cited by 155 · see citing works
Probiotics as an immune modulator
KANG, H.-J., & IM, S.-H. (2015) · Journal of Nutritional Science and Vitaminology · doi:10.3177/jnsv.61.s103 · Cited by 151 · see citing works
Minelli, E. B., Benini, A., Marzotto, M., Sbarbati, A., Ruzzenente, O., Ferrario, R., Hendriks, H., & Dellaglio, F. (2004) · International Dairy Journal · doi:10.1016/j.idairyj.2004.01.007 · Cited by 150 · see citing works
Goh, Y. J., & Klaenhammer, T. R. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.00030-10 · Cited by 149 · see citing works
Armando, M. R., Pizzolitto, R. P., Dogi, C. A., Cristofolini, A., Merkis, C., Poloni, V., Dalcero, A. M., & Cavaglieri, L. R. (2012) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2012.05331.x · Cited by 149 · see citing works
Administration of Lactobacillus paracasei ameliorates type 2 diabetes in mice
Dang, F., Jiang, Y., Pan, R., Zhou, Y., Wu, S. L., Wang, R., Zhuang, K., Zhang, W., Li, T., & Man, C. (2018) · Food & Function · doi:10.1039/c8fo00081f · Cited by 148 · see citing works
Probiotic assessment of Enterococcus faecalis CP58 isolated from human gut
Nueno‐Palop, C., & Narbad, A. (2011) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2010.12.029 · Cited by 145 · see citing works
Carbohydrate preference, acid tolerance and bile tolerance in five strains of Bifidobacterium
Vernazza, C. L., Gibson, G. R., & Rastall, R. A. (2006) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2006.02832.x · Cited by 143 · see citing works
Technological aspects related to the use of bifidobacteria in dairy products
Roy, D. (2005) · Le Lait · doi:10.1051/lait:2004026 · Cited by 145 · see citing works
How probiotics face food stress: They get by with a little help
Fiocco, D., Longo, A., Arena, M. P., Russo, P., Spano, G., & Capozzi, V. (2019) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2019.1580673 · Cited by 143 · see citing works
Guerra, N. P., Bernárdez, P. F., Méndez, J., Cachaldora, P., & Pastrana, L. M. (2006) · Animal Feed Science and Technology · doi:10.1016/j.anifeedsci.2006.05.010 · Cited by 143 · see citing works
Grimoud, J., Durand, H., Courtin, C., MONSAN, P. F., Ouarné, F., Théodorou, V., & Roques, C. G. (2010) · Anaerobe · doi:10.1016/j.anaerobe.2010.07.005 · Cited by 142 · see citing works
Chenoll, E., Casinos, B., Bataller, E., Astals, P., Echevarría, J., Iglesias, J. R., Balbarie, P., Ramón, D., & Genovés, S. (2010) · Applied and Environmental Microbiology · doi:10.1128/aem.01820-10 · Cited by 142 · see citing works
ASSESSMENT OF POTENTIAL PROBIOTIC PROPERTIES OF LACTIC ACID BACTERIA AND YEAST STRAINS
Gotcheva, V., Hristozova, E., Hristozova, T., Guo, M., Рошкова, З., & Angelov, A. (2002) · Food Biotechnology · doi:10.1081/fbt-120016668 · Cited by 141 · see citing works
Survival of Bacillus cereus spores and vegetative cells in acid media simulating human stomach
Clavel, T., Carlin, F., Lairon, D., Nguyen‐The, C., & Schmitt, P. (2004) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2004.02292.x · Cited by 140 · see citing works
A novel strain of Bacteroides fragilis enhances phagocytosis and polarises M1 macrophages
Deng, H., Li, Z., Tan, Y., Guo, Z., Liu, Y., Wang, Y., Yuan, Y., Yang, R., Bi, Y., Bai, Y., et al. (2016) · Scientific Reports · doi:10.1038/srep29401 · Cited by 137 · see citing works
Probiotic Properties of Lactobacillus Strains Isolated from Tibetan Kefir Grains
Zheng, Y.-C., Lu, Y., Wang, J., Yang, L., Pan, C., & Huang, Y. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069868 · Cited by 136 · see citing works
Role of probiotic Lactobacillus fermentum KKL1 in the preparation of a rice based fermented beverage
Ghosh, K., Ray, M., Adak, A., Halder, S. K., Das, A., Jana, A., Parua (Mondal), S., Vágvölgyi, C., Das Mohapatra, P. K., Pati, B. R., et al. (2015) · Bioresource Technology · doi:10.1016/j.biortech.2015.01.130 · Cited by 136 · see citing works
Abadía‐García, L., Cardador‐Martínez, A., del Campo, S. T. M., Arvizu‐Medrano, S. M., Castaño‐Tostado, E., Regalado‐González, C., García-Almendárez, B. E., & Amaya‐Llano, S. L. (2013) · International Dairy Journal · doi:10.1016/j.idairyj.2013.04.005 · Cited by 135 · see citing works
In vitro assessment of probiotic bacteria: From survival to functionality
Morelli, L. (2007) · International Dairy Journal · doi:10.1016/j.idairyj.2007.01.015 · Cited by 131 · see citing works
Selecting Lactic Acid Bacteria for Their Safety and Functionality by Use of a Mouse Colitis Model
Daniel, C., Poiret, S., Goudercourt, D., Dennin, V., Leyer, G. J., & Pot, B. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.00109-06 · Cited by 131 · see citing works
Yu, Z., Zhang, X., Li, S., Li, C., Li, D., & Yang, Z. (2013) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-012-1202-3 · Cited by 129 · see citing works
Giulio, B. D., Orlando, P., Barba, G., Coppola, R., ROSA, M. D., Sada, A., Prisco, P. P. D., & Nazzaro, F. (2005) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-004-4735-2 · Cited by 129 · see citing works
Ruíz, L., Ruas‐Madiedo, P., Gueimonde, M., Reyes‐Gavilán, C. G. D. L., Margollés, A., & Sánchez, B. (2011) · Genes & Nutrition · doi:10.1007/s12263-010-0207-5 · Cited by 127 · see citing works
Choi, A.-R., Patra, J. K., Kim, W. J., & Kang, S. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01963 · Cited by 126 · see citing works
Probiotic characteristics of lactic acid bacteria isolated from kimchi
Chang, J. ‐., Shim, Y. Y., Cha, S.-K., & Chee, K. M. (2009) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2009.04648.x · Cited by 123 · see citing works
Coghetto, C. C., Brinques, G. B., Siqueira, N. M., Pletsch, J. S., Soares, R. M. D., & Ayub, M. A. Z. (2016) · Journal of Functional Foods · doi:10.1016/j.jff.2016.03.036 · Cited by 122 · see citing works
Genetic heterogeneity and functional properties of intestinal bifidobacteria
Mättö, J., Malinen, E., Suihko, M. ‐., Alander, M., Palva, A., & Saarela, M. (2004) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2004.02340.x · Cited by 121 · see citing works
Michida, H., Tamalampudi, S., Pandiella, S. S., Webb, C., Fukuda, H., & Kondo, A. (2005) · Biochemical Engineering Journal · doi:10.1016/j.bej.2005.09.004 · Cited by 120 · see citing works
Ingredient selection criteria for probiotic microorganisms in functional dairy foods
Charteris, W. P., Kelly, P. M., Morelli, L., & Collins, J. K. (1998) · International Journal of Dairy Technology · doi:10.1111/j.1471-0307.1998.tb02516.x · Cited by 120 · see citing works
- Authors
- Charteris, Kelly, Morelli, & Collins
- Affiliations
- Università Cattolica del Sacro Cuore (IT)
- Venue
- Journal of Applied Microbiology
- Publisher
- Oxford University Press (OUP)
- Published
- 1998-06
- Volume
- 84
- Issue
- 5
- Pages
- 759-768
- ISSN
- 1364-5072 (ISSN-L)
- 1365-2672
- OpenAlex
- W2072505334
- Cited by
- 774
- References
- 0
- Citations by year
- 2026: 26 · 2025: 17 · 2024: 34 · 2023: 36 · 2022: 28 · 2021: 33 · 2020: 22 · 2019: 36 · 2018: 39 · 2017: 39 · 2016: 44 · 2015: 55 · 2014: 39 · 2013: 45 · 2012: 48
- FWCI
- 12.50
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Applied Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
- Keywords
- probiotics, Lactobacillus, Bifidobacterium, simulated gastric fluid, bile salt tolerance, milk protein, Lactobacillus casei, Bifidobacterium infantis, Lactobacillus fermentum, Lactobacillus salivarius, Bifidobacterium animalis, Bifidobacterium breve, Bifidobacterium adolescentis
- MeSH terms
- Adult, Bacterial Adhesion, Bifidobacterium, Chymotrypsin, Digestive System, Gastric Juice, Gastrointestinal Transit, Humans, Infant, Newborn, Lactobacillus, Milk Proteins, Models, Biological, Mucins, Pancreatic Juice, Trypsin Inhibitors, Probiotics
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review