The DOI matches its Crossref record; 70 of the 70 references it cites were found in a registry or an index.
Probiotics: Immunomodulation and Evaluation of Safety and Efficacy
Open accessAbstract
The intake of probiotics has been associated with beneficial effects on the immune system, such as improved disease resistance and diminished risk of allergies. This review gives an overview of the immunomodulatory effects of probiotics investigated with in vitro assays, experimental animal models, and clinical trials, and explores possible mechanisms underlying the immunomodulatory effects. Immunomodulation, however, is not always beneficial and might induce detrimental effects; therefore, a scheme is proposed for benefit-risk assessment of immunomodulation by probiotics. Within this scheme, expert judgment based on data derived from a panel of in vitro assays, animal models, and clinical trials should lead to conclusions on efficacy and safety aspects of probiotics.
Overview
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
Verification
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?
Cytokines have shown responses to probiotic supplementation in several trials.
“Cytokines, on the other hand, have in several trials shown responses to probiotic supplementation. 21”
From Clinical trial: multispecies probiotic supplementation alleviates the symptoms of irritable bowel syndrome and stabilizes intestinal microbiota (2008) · cites this paper as [21]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Toll-like receptors: critical proteins linking innate and acquired immunity
Akira, S., Takeda, K., & Kaisho, T. (2001) · Nature Immunology · doi:10.1038/90609 · Cited by 4,777
Podolsky, D. K. (2002) · New England Journal of Medicine · doi:10.1056/nejmra020831 · Cited by 3,183
Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial
Kalliomäki, M. A., Salminen, S., Arvilommi, H. S., Kero, P. O., Koskinen, P. J., & Isolauri, E. (2001) · The Lancet · doi:10.1016/s0140-6736(00)04259-8 · Cited by 2,443
Probiotics, prebiotics, and synbiotics—approaching a definition
Schrezenmeir, J., & de Vrese, M. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/73.2.361s · Cited by 1,533
Dendritic-cell control of pathogen-driven T-cell polarization
Kapsenberg, M. L. (2003) · Nature reviews. Immunology · doi:10.1038/nri1246 · Cited by 1,495
Kalliomäki, M. A., Salminen, S., Poussa, T. A., Arvilommi, H. S., & Isolauri, E. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13490-3 · Cited by 1,340
Kruis, W., Frič, P., Pokrotnieks, J., Lukáš, M., Fixa, B., Kaščák, M., Kamm, M. A., Weismueller, J., Beglinger, C., Stolte, M., et al. (2004) · Gut · doi:10.1136/gut.2003.037747 · Cited by 1,285
Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing
Kalliomäki, M., Kirjavainen, P., Eerola, E., Kero, P., Salminen, S., & Isolauri, E. (2001) · Journal of Allergy and Clinical Immunology · doi:10.1067/mai.2001.111237 · Cited by 1,255
Rembacken, B., Snelling, A. M., Hawkey, P. M., Chalmers, D. M., & Axon, A. (1999) · The Lancet · doi:10.1016/s0140-6736(98)06343-0 · Cited by 1,100
Probiotics: effects on immunity
Isolauri, E., Sütas, Y., Kankaanpää, P., Arvilommi, H. S., & Salminen, S. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/73.2.444s · Cited by 1,029
Probiotics in the management of atopic eczema
Isolauri, E., Arvola, T., Sütas, Y., Moilanen, E., & Salminen, S. (2000) · Clinical & Experimental Allergy · doi:10.1046/j.1365-2222.2000.00943.x · Cited by 981
Probiotics: A novel approach in the management of food allergy
Majamaa, H., & Isolauri, E. (1997) · Journal of Allergy and Clinical Immunology · doi:10.1016/s0091-6749(97)70093-9 · Cited by 929
The intestinal microflora in allergic Estonian and Swedish 2‐year‐old children
Björkstén, Naaber, P., Sepp, & Mikelsaar (1999) · Clinical & Experimental Allergy · doi:10.1046/j.1365-2222.1999.00560.x · Cited by 927
Mimura, T., Rizzello, F., Helwig, U., Poggioli, G., Schreiber, S., Talbot, I. C., Nicholls, R. J., Gionchetti, P., Campieri, M., & Kamm, M. A. (2003) · Gut · doi:10.1136/gut.53.1.108 · Cited by 912
Christensen, H. R., Frøkiær, H., & Pestka, J. J. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.1.171 · Cited by 905
Demonstration of safety of probiotics—A review
Salminen, S. (1998) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(98)00128-7 · Cited by 884
Rachmilewitz, D., Katakura, K., Karmeli, F., Hayashi, T., Reinus, C., Rudensky, B., Akira, S., Takeda, K., Lee, J., Takabayashi, K., et al. (2004) · Gastroenterology · doi:10.1053/j.gastro.2003.11.019 · Cited by 859
Hatakka, K., Savilahti, E., Pönkä, A., Meurman, J. H., Poussa, T., Näse, L., Saxelin, M., & Korpela, R. (2001) · BMJ · doi:10.1136/bmj.322.7298.1327 · Cited by 645
Toll signaling pathways in the innate immune response
Anderson, K. V. (2000) · Current Opinion in Immunology · doi:10.1016/s0952-7915(99)00045-x · Cited by 634
Effect of probiotic strains in children with atopic dermatitis
Rosenfeldt, V., Benfeldt, E., Nielsen, S. D., Michaelsen, K. F., Jeppesen, D. L., Valerius, N. H., & Pærregaard, A. (2003) · Journal of Allergy and Clinical Immunology · doi:10.1067/mai.2003.389 · Cited by 614
Modulation of human dendritic cell phenotype and function by probiotic bacteria
Hart, A. L., Lammers, K., Brigidi, P., Vitali, B., Rizzello, F., Gionchetti, P., Campieri, M., Kamm, M. A., Knight, S. C., & Stagg, A. J. (2004) · Gut · doi:10.1136/gut.2003.037325 · Cited by 555
Weizman, Z., Asli, G., & Alsheikh, A. (2005) · Pediatrics · doi:10.1542/peds.2004-1815 · Cited by 548
Giacinto, C. D., Marinaro, M., Sanchez, M., Strober, W., & Boirivant, M. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.6.3237 · Cited by 522
Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization
Mohamadzadeh, M., Olson, S. D., Kalina, W. V., Ruthel, G. T., Demmin, G. L., Warfield, K. L., Bavari, S., & Klaenhammer, T. R. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500098102 · Cited by 465
Interleukin‐10 generation in atopic children following oral Lactobacillus rhamnosus GG
Pessi, T., Sütas, Y., Hurme, M., & Isolauri, E. (2000) · Clinical & Experimental Allergy · doi:10.1046/j.1365-2222.2000.00948.x · Cited by 430
Intestinal microflora of Estonian and Swedish infants
Sepp, E., Julge, K., Vasar, M., Naaber, P., Björkstén, B., & Mikelsaar, M. (1997) · Acta Paediatrica · doi:10.1111/j.1651-2227.1997.tb15178.x · Cited by 416
Miettinen, M., Matikainen, S., Vuopio‐Varkila, J., Pirhonen, J., Varkila, K., Kurimoto, M., & Julkunen, I. (1998) · Infection and Immunity · doi:10.1128/iai.66.12.6058-6062.1998 · Cited by 343
Lactobacillus GG effect in increasing IFN-γ production in infants with cow's milk allergy
Pohjavuori, E., Viljanen, M., Korpela, R., Kuitunen, M., Tiittanen, M., Vaarala, O., & Savilahti, E. (2004) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2004.03.036 · Cited by 335
Rosenfeldt, V., Benfeldt, E., Valerius, N. H., Pærregaard, A., & Michaelsen, K. F. (2004) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2004.06.068 · Cited by 326
Long-term consumption of infant formulas containing live probiotic bacteria: tolerance and safety
Saavedra, J. M., Abi‐Hanna, A., Moore, N. D., & Yolken, R. H. (2004) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/79.2.261 · Cited by 278
Pelto, Isolauri, Lilius, Nuutila, & Salminen (1998) · Clinical & Experimental Allergy · doi:10.1046/j.1365-2222.1998.00449.x · Cited by 275
Murosaki, S., Yamamoto, Y., Ito, K., Inokuchi, T., Kusaka, H., Ikeda, H., & Yoshikai, Y. (1998) · Journal of Allergy and Clinical Immunology · doi:10.1016/s0091-6749(98)70055-7 · Cited by 273
Helin, T., Haahtela, S., & Haahtela, T. (2002) · Allergy · doi:10.1034/j.1398-9995.2002.1s3299.x · Cited by 245
von der Weid, T., Bulliard, C., & Schiffrin, E. J. (2001) · Clinical and Diagnostic Laboratory Immunology · doi:10.1128/cdli.8.4.695-701.2001 · Cited by 241
Hatakka, K., Martio, J., Korpela, M. M., Herranen, M., Poussa, T. A., Laasanen, T., Saxelin, M., Vapaatalo, H., Moilanen, E., & Korpela, R. (2003) · Scandinavian Journal of Rheumatology · doi:10.1080/03009740310003695 · Cited by 235
Braat, H., van den Brande, J., van Tol, E., Hommes, D. W., Peppelenbosch, M. P., & van Deventer, S. J. H. (2004) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/80.6.1618 · Cited by 235
Lactobacilli from human gastrointestinal mucosa are strong stimulators of IL-12 production
Hessle, C. C., Hanson, L. A., & Wold, A. E. (1999) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1999.00885.x · Cited by 230
Matsuzaki, T., Yamazaki, R., Hashimoto, S., & Yokokura, T. (1998) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(98)75549-3 · Cited by 225
Fabia, R. B., Ar'Rajab, A., Johansson, M. L., Wïllén, R., Andersson, R. E., Molin, G., & Bengmark, S. (1993) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365529309096063 · Cited by 194
Sheil, B., McCarthy, J., O’Mahony, L., Bennett, M. W., Ryan, P., Fitzgibbon, J. J., Kiely, B., Collins, J. K., & Shanahan, F. (2004) · Gut · doi:10.1136/gut.2003.027789 · Cited by 187
Probiotics and intestinal health effects: a clinical perspective
Marteau, P. R., Seksik, P., & Jian, R. (2002) · British Journal Of Nutrition · doi:10.1079/bjn2002629 · Cited by 183
Immunomodulation by treatment with Lactobacillus casei strain Shirota
Matsuzaki, T. (1998) · International Journal of Food Microbiology · doi:10.1016/s0168-1605(98)00046-4 · Cited by 180
Matsuzaki, T., Nagata, Y., KADO, S., UCHIDA, K., Kato, I., Hashimoto, S., & Yokokura, T. (1997) · Apmis · doi:10.1111/j.1699-0463.1997.tb05066.x · Cited by 175
Cross, M. L., Stevenson, L. M., & Gill, H. S. (2001) · International Immunopharmacology · doi:10.1016/s1567-5769(01)00025-x · Cited by 172
Immune and Clinical Impact of Lactobacillus acidophilus on Asthma
Wheeler, J. G., Shema, S. J., Bogle, M. L., Shirrell, M. A., Burks, A. W., Pittler, A., & Helm, R. M. (1997) · Annals of Allergy Asthma & Immunology · doi:10.1016/s1081-1206(10)63007-4 · Cited by 161
Agostoni, C. V., Axelsson, I., Braegger, C., Goulet, O., Koletzko, B. V., Michaelsen, K. F., Rigo, J., Shamir, R., Szajewska, H., Turck, D., et al. (2004) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-200404000-00001 · Cited by 160
Sturm, A., Rilling, K., Baumgart, D. C., Gargas, K., Abou-Ghazalé, T., Raupach, B., Eckert, J., Schumann, R. R., Enders, C., Sonnenborn, U., et al. (2005) · Infection and Immunity · doi:10.1128/iai.73.3.1452-1465.2005 · Cited by 145
Lactobacillus GG Bacteria Ameliorate Arthritis in Lewis Rats
Baharav, E., Weinberger, A., Mor, F., & Halpern, M. (2004) · The Journal of Nutrition · doi:10.1093/jn/134.8.1964 · Cited by 144
Kato, I., Endo-Tanaka, K., & Yokokura, T. (1998) · Life Sciences · doi:10.1016/s0024-3205(98)00315-4 · Cited by 130
Colonization of congenitally immunodeficient mice with probiotic bacteria
Wagner, R. D., WARNER, T. F. C. S., Roberts, L., Farmer, J., & Balish, E. (1997) · Infection and Immunity · doi:10.1128/iai.65.8.3345-3351.1997 · Cited by 129
The Use of Probiotics in Gastrointestinal Disease
Madsen, K. L. (2001) · Canadian Journal of Gastroenterology · doi:10.1155/2001/690741 · Cited by 125
Stimulation of the Secretion of Pro‐Inflammatory Cytokines by Bifidobacterium Strains
He, F., Morita, H., Ouwehand, A. C., Hosoda, M., Hiramatsu, M., Kurisaki, J., Isolauri, E., Benno, Y., & Salminen, S. (2002) · Microbiology and Immunology · doi:10.1111/j.1348-0421.2002.tb02765.x · Cited by 122
Regulating the Safety of Probiotics - The European Approach
von Wright, A. (2005) · Current Pharmaceutical Design · doi:10.2174/1381612053382322 · Cited by 118
Osman, N., Adawi, D., Ahrné, S., Jeppsson, B. W., & Molin, G. (2004) · Digestive Diseases and Sciences · doi:10.1023/b:ddas.0000017459.59088.43 · Cited by 106
Alvarez, S., Herrero, C., Bru, E., & Perdigón, G. (2001) · Journal of Food Protection · doi:10.4315/0362-028x-64.11.1768 · Cited by 104
Cross, M. L., Mortensen, R., Kudsk, J., & Gill, H. S. (2002) · Medical Microbiology and Immunology · doi:10.1007/s00430-002-0112-7 · Cited by 92
Maassen, C. B. M., Holten, J., Balk, F. R. M., et al. (1998) · Veterinary Quarterly · doi:10.1080/01652176.1998.9694976 · Cited by 76
Probiotics and inflammatory bowel disease: from fads and fantasy to facts and future
Shanahan, F. (2002) · British Journal Of Nutrition · doi:10.1079/bjn2002624 · Cited by 74
Probiotic Therapy Fails to Improve Gut Permeability in a Hapten Model of Colitis
R. J. Kennedy, M. H. (2000) · Scandinavian Journal of Gastroenterology · doi:10.1080/003655200453601 · Cited by 68
Effects of dietary yoghurt on immunological and clinical parameters of rhinopathic patients
Aldinucci, C., Bellussi, L. M., Monciatti, G., et al. (2002) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1601465 · Cited by 60
Effect of oral administration of Lactobacillus casei on alloxan‐induced diabetes in mice
Matsuzaki, T., Nagata, Y., KADO, S., UCHIDA, K., Hashimoto, S., & Yokokura, T. (1997) · Apmis · doi:10.1111/j.1699-0463.1997.tb05065.x · Cited by 58
Impact of Dietary Yogurt on Immune Function
Wheeler, J. G., Bogle, M. L., Shema, S. J., et al. (1997) · The American Journal of the Medical Sciences · doi:10.1097/00000441-199702000-00011 · Cited by 55
CD154 inhibits tumor-induced apoptosis in dendritic cells and tumor growth
Esche, C., Gambotto, A. A., Satoh, Y., Gerein, V., Robbins, P. D., Watkins, S. C., Lotze, M. T., & Shurin, M. R. (1999) · European Journal of Immunology · doi:10.1002/(sici)1521-4141(199907)29:07 · Cited by 55
Probiotics against allergy: data, doubts, and perspectives
Matricardi, P. M. (2002) · Allergy · doi:10.1034/j.1398-9995.2002.1a3299.x · Cited by 52
From reactive arthritis to rheumatoid arthritis
Toivanen, P. (2001) · Journal of Autoimmunity · doi:10.1006/jaut.2000.0496 · Cited by 42
de Waard, R., Garssen, J., Snel, J., et al. (2001) · Clinical and Diagnostic Laboratory Immunology · doi:10.1128/cdli.8.4.762-767.2001 · Cited by 36
de Waard, R., Claassen, E., Bokken, G. C. A. M., et al. (2003) · Clinical and Vaccine Immunology · doi:10.1128/cdli.10.1.59-65.2003 · Cited by 32
Lactic acid bacteria in a changing legislative environment.
Feord, J. (2002) · PubMed · Cited by 26
Lactic acid bacteria in a changing legislative environment
Feord, J. (2002) · Antonie van Leeuwenhoek · doi:10.1023/a:1020648018998 · Cited by 25
Flagged first, then by citations
Cited by
Sorted by citations
KAJANDER, K., MYLLYLUOMA, E., RAJILIĆ‐STOJANOVIĆ, M., KYRÖNPALO, S., RASMUSSEN, M., JÄRVENPÄÄ, S., ZOETENDAL, E. G., DE VOS, W. M., VAPAATALO, H., & KORPELA, R. (2008) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2007.03542.x · Cited by 367
The non-pathogenic Escherichia coli strain Nissle 1917 – features of a versatile probiotic
Sonnenborn, U., & Schulze, J. (2009) · Microbial Ecology in Health and Disease · doi:10.3109/08910600903444267 · Cited by 232
Dicks, L., & Botes, M. (2010) · Beneficial Microbes · doi:10.3920/bm2009.0012 · Cited by 207
A critical review of antibiotic resistance in probiotic bacteria
Li, T., Teng, D., Mao, R., Hao, Y., Wang, X., & Wang, J. (2020) · Food Research International · doi:10.1016/j.foodres.2020.109571 · Cited by 172
Singh, A., Hacini-Rachinel, F., Gosoniu, M. L., Bourdeau, T., Holvoet, S., Doucet-Ladeveze, R., Beaumont, M., Mercenier, A., & Nutten, S. (2013) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2012.197 · Cited by 93
Nielsen, C., Balachandran, P., Christensen, O., Pugh, N., Tamta, H., Sufka, K., Wu, X., Walsted, A., Schjørring-Thyssen, M., Enevold, C., et al. (2010) · Planta Medica · doi:10.1055/s-0030-1250043 · Cited by 56
Liu, B., Zhong, X., Liu, Z., Guan, X., Wang, Q., Qi, R., Zhou, X., & Huang, J. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242417570 · Cited by 21
Metadata
- Authors
- Ezendam, J., & Loveren, H.
- Affiliations
- National Institute for Public Health and the Environment (NL)
- Maastricht University (NL)
- Corresponding author
- Ezendam, Janine
- Venue
- Nutrition Reviews
- Publisher
- Oxford University Press (OUP)
- Published
- 2006-01
- Volume
- 64
- Issue
- 1
- Pages
- 1-14
- ISSN
- 0029-6643 (ISSN-L)
- 1753-4887
- OpenAlex
- W2154503456
- Cited by
- 103
- References
- 70
- Citations by year
- 2025: 3 · 2024: 6 · 2023: 6 · 2022: 4 · 2021: 2 · 2020: 3 · 2019: 4 · 2018: 2 · 2017: 5 · 2016: 2 · 2015: 6 · 2014: 7 · 2013: 12 · 2012: 8
- FWCI
- 1.17
- Type
- journal article
- Language
- en
- Open access
- Licence
- other-oa
- Locations
- Nutrition Reviews (publishedVersion)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion, other-oa)
- Rivm (National Institute for Public Health and the Environment) (submittedVersion, other-oa)
- Rivm (National Institute for Public Health and the Environment) (submittedVersion)
- Rivm Repository (Netherlands National Institute for Public Health and the Environment) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Nursing › Nutrition and Dietetics › Microbial Metabolites in Food Biotechnology
- Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
- Keywords
- probiotics, immunomodulation, probiotic safety, probiotic efficacy, disease resistance, allergy risk, risk-benefit assessment, immune system
- MeSH terms
- Animals, Consumer Product Safety, Disease Models, Animal, Humans, Immune System, Immune System Diseases, Immunologic Factors, Randomized Controlled Trials as Topic, Treatment Outcome, Risk Assessment, Immunity, Mucosal, Evidence-Based Medicine, 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
