Probiotic bacteria stimulate virus-specific neutralizing antibodies following a booster polio vaccination
Abstract
Background Orally ingested probiotic bacteria may modulate the immune response and increase antibody titers against enteric infections by bacteria or viruses. Even though positive effects of probiotics on respiratory tract infections have been reported, overall only few studies have examined effects on virus infections concerning organs other than the gastrointestinal tract.Aim of the study It was the aim of the study to investigate whether and how probiotics affect the immune response to a standardized enterovirus challenge (polio) and infections not limited to the gastrointestinal tract in healthy adults.Methods In a randomized, controlled and double-blind study 64 volunteers consumed for 5 weeks chemically acidified clotted milk without bacteria or with 10(10)/serving (Lactobacillus rhamnosus ) GG or Lactobacillus acidophilus CRL431 added. In the second week subjects were vaccinated orally against polio 1, 2 and 3. Polio virus neutralizing serum activity, the primary parameter, was determined by the standard neutralization test (WHO) before and three times after vaccination. Polio-specific IgA, IgG and IgM were detected by ELISAs.Results Probiotics increased poliovirus neutralizing antibody titers (NT) and affected the formation of poliovirus-specific IgA and IgG in serum. The maximum increase after immunization was about 2, 2.2, or 4-fold higher, respectively, for NT, IgG or, IgA, in volunteers consuming probiotics instead of placebo. No consistent difference was noted between bacterial strains.Conclusions Probiotics induce an immunologic response that may provide enhanced systemic protection of cells from virus infections by increasing production of virus neutralizing antibodies.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Probiotic strains including LGG increase IgA in animal models and virus-neutralizing serum immunoglobulins in humans when administered as adjuncts to some viral vaccines.
“probiotic strains, including LGG, have been shown to increase IgA in animal models (Wang Y. et al., 2017), and virus neutralizing serum immunoglobulins in humans when administered as adjuncts to some viral vaccines (De Vrese et al., 2005).”
From Viral Infections, the Microbiome, and Probiotics (2021) · cites this paper as De Vrese et al., 2005
Cites
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 1,519 · see citing works
Self-citationProbiotics: 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 1,021 · see citing works
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 · see citing works
LactobacillusTherapy for Acute Infectious Diarrhea in Children: A Meta-analysis
Niel, C. W. V., Feudtner, C., Garrison, M. M., & Christakis, D. (2002) · PEDIATRICS · doi:10.1542/peds.109.4.678 · Cited by 599 · see citing works
Link‐Amster, H., Rochat, F., Saudan, K.-Y., Mignot, O., & Aeschlimann, J. (1994) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.1994.tb00011.x · Cited by 432 · see citing works
Melmed, G., Thomas, L. S., Lee, N., Tesfay, S. Y., Lukasek, K., Michelsen, K. S., Zhou, Y., Hu, B., Arditi, M., & Abreu, M. T. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.3.1406 · Cited by 431 · see citing works
The Scientific Basis for Probiotic Strains ofLactobacillus
Reid, G. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.9.3763-3766.1999 · Cited by 399 · see citing works
Meta‐analysis: the effect of probiotic administration on antibiotic‐associated diarrhoea
Cremonini, F., Caro, S. D., Nista, E. C., Bartolozzi, F., Capelli, G., Gasbarrini, A., & Gasbarrini, A. (2002) · Alimentary Pharmacology & Therapeutics · doi:10.1046/j.1365-2036.2002.01318.x · Cited by 385 · see citing works
Matsuguchi, T., Takagi, A., Matsuzaki, T., Nagaoka, M., Ishikawa, K., Yokokura, T., & Yoshikai, Y. (2003) · Clinical Diagnostic Laboratory Immunology · doi:10.1128/cdli.10.2.259-266.2003 · Cited by 328 · see citing works
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 · see citing works
Suzuki, M., Hisamatsu, T., & Podolsky, D. K. (2003) · Infection and Immunity · doi:10.1128/iai.71.6.3503-3511.2003 · Cited by 217 · see citing works
Overview of Functional Foods: Emphasis on Probiotic Bacteria
Sanders, M. E. (1998) · International Dairy Journal · doi:10.1016/s0958-6946(98)00056-9 · Cited by 186 · see citing works
Faden, H. S., Modlin, J. F., THOMS, M. L., McBean, A. M., Ferdon, M. B., & Ogra, P. L. O. (1990) · The Journal of Infectious Diseases · doi:10.1093/infdis/162.6.1291 · Cited by 178 · see citing works
Essential procedures for clinical microbiology
Isenberg, H. D. (1998) · ASM Press eBooks · Cited by 160 · see citing works
Emini, E. A., Jameson, B. A., Lewis, A., Larsen, G. R., & Wimmer, E. (1982) · Journal of Virology · doi:10.1128/jvi.43.3.997-1005.1982 · Cited by 138 · see citing works
Adam, A., Petit, J. F., Lefrancier, P., et al. (1981) · Molecular and Cellular Biochemistry · doi:10.1007/bf00225295 · Cited by 136 · see citing works
The Immunological Activities of Bacterial Peptidoglycans
Stewart-Tull, D. E. S. (1980) · Annual Review of Microbiology · doi:10.1146/annurev.mi.34.100180.001523 · Cited by 129 · see citing works
Probiotics and Immune Response
Blum, S., Haller, D., Pfeifer, A. C., & Schiffrin, E. J. (2002) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-002-0013-y · Cited by 87 · see citing works
Parant, M., Parant, F., & CHEDID, L. A. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.7.3395 · Cited by 73 · see citing works
Cramblett, H. G. (1970) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpedi.1970.02100050464019 · Cited by 36 · see citing works
Sabin, A. B., Michaels, R. H., Ziring, P. R., D, S. K. M., & Warren, J. D. (1963) · PubMed · Cited by 34 · see citing works
Korhonen, R., Korpela, R., & Moilanen, E. (2002) · Inflammation · doi:10.1023/a:1019720701230 · Cited by 33 · see citing works
Herremans, M. M., van Loon, A. M., Reimerink, J. H. J., Rümke, H. C., van der Avoort, H. G. A. M., Kimman, T. G., & Koopmans, M. (1997) · Clinical and Diagnostic Laboratory Immunology · doi:10.1128/cdli.4.5.499-503.1997 · Cited by 29 · see citing works
Self-citationEFFECT OF ORAL POLIOVIRUS VACCINE IN NEWBORN CHILDREN
Sabin, A. B., Michaels, R. H., Ziring, P. R., D, S. K. M., & Warren, J. D. (1963) · PEDIATRICS · doi:10.1542/peds.31.4.641 · Cited by 23 · see citing works
Herremans, M. M. P. T., Reimerink, J. H. J., Ras, A., van der Avoort, H. G. A. M., Kimman, T. G., van Loon, A. M., Spaendonck, C.-V., & Koopmans, M. (1997) · Clinical and Diagnostic Laboratory Immunology · doi:10.1128/cdli.4.6.659-664.1997 · Cited by 22 · see citing works
Self-citationNibbeling, R., Reimerink, J. H. J., Agboatwalla, M., Naquib, T., Ras, A., Poelstra, P., van der Avoort, H. G. A. M., & van Loon, A. M. (1994) · Clinical and Diagnostic Virology · doi:10.1016/0928-0197(94)90044-2 · Cited by 21 · see citing works
Okutomi, T., Inagawa, H., Nishizawa, T., et al. (1990) · PubMed · Cited by 18 · see citing works
Edevåg, G., Wahrén, B., Osterhaus, A. D. M. E., et al. (1995) · Journal of Clinical Microbiology · doi:10.1128/jcm.33.11.2927-2930.1995 · Cited by 11 · see citing works
Probiotics and Immune Response
Blum, S., Haller, D., Pfeifer, A. C., et al. (2002) · Clinical Reviews in Allergy & Immunology · doi:10.1385/criai:22:3:287 · Cited by 10 · see citing works
Lykova, E. A., Vorob'ev, A. A., Bokovoĭ, A. G., Pobedinskaia, I. N., Gevondian, V. S., Gevondyan, N. M., Дмитриевич, М. С., Vi, M., Dzis, N. B., Makkaveeva, L. F., et al. (2000) · PubMed · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Bifidobacterium longum subspecies infantis: champion colonizer of the infant gut
Underwood, M. A., German, J. B., Lebrilla, C. B., & Mills, D. A. (2015) · Pediatric Research · doi:10.1038/pr.2014.156 · Cited by 439 · see citing works
Stool microbiota and vaccine responses of infants
Huda, M. N., Lewis, Z., Kalanetra, K. M., Rashid, M., Ahmad, S. M., Raqib, R., Qadri, F., Underwood, M. A., Mills, D. A., & Stephensen, C. B. (2014) · PEDIATRICS · doi:10.1542/peds.2013-3937 · Cited by 392 · see citing works
Rizzardini, G., Eskesen, D., Calder, P. C., Capetti, A., Jespersen, L., & Clerici, M. (2012) · British Journal Of Nutrition · doi:10.1017/s000711451100420x · Cited by 217 · see citing works
Viral Infections, the Microbiome, and Probiotics
Harper, A., Vijayakumar, V., Ouwehand, A. C., ter Haar, J., Obis, D., Espadaler, J., Binda, S., Desiraju, S., & Day, R. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.596166 · Cited by 177 · see citing works
Wang, Y., Liu, L., Moore, D. J., Shen, X., Peek, R. M., Acra, S. A., Li, H., Ren, X., Polk, D. B., & Yan, F. (2017) · Mucosal Immunology · doi:10.1038/mi.2016.57 · Cited by 149 · see citing works
The influence of probiotics on vaccine responses—A systematic review
Zimmermann, P., & Curtis, N. (2018) · Vaccine · doi:10.1016/j.vaccine.2017.08.069 · Cited by 142 · see citing works
How can probiotics and prebiotics impact mucosal immunity?
O'Flaherty, S., Saulnier, D., Pot, B., & Versalovic, J. (2010) · Gut Microbes · doi:10.4161/gmic.1.5.12924 · Cited by 103 · see citing works
de Vrese, M., Kristen, H., Rautenberg, P., Laue, C., & Schrezenmeir, J. (2011) · Journal of Dairy Research · doi:10.1017/s002202991100063x · Cited by 84 · see citing works
Self-citationSoh, S. E., Ong, D. Q. R., Gerez, I., Zhang, X., Chollate, P., Shek, L. P.-C., Lee, B. W., & Aw, M. (2010) · Vaccine · doi:10.1016/j.vaccine.2010.01.020 · Cited by 78 · see citing works
How the gut microbiome regulates host immune responses to viral vaccines
Vlasova, A. N., Takanashi, S., Miyazaki, A., Rajashekara, G., & Saif, L. J. (2019) · Current Opinion in Virology · doi:10.1016/j.coviro.2019.05.001 · Cited by 67 · see citing works
Immunological Effects of Probiotics and their Significance to Human Health
Gill, H. S., Grover, S., Batish, V. K., & Gill, P. (2009) · Prebiotics and Probiotics Science and Technology · doi:10.1007/978-0-387-79058-9_23 · Cited by 13 · see citing works
- Authors
- de Vrese, M., Rautenberg, P., Laue, C., Koopmans, M., Herremans, T., & Schrezenmeir, J.
- Affiliations
- Christian-Albrechts-Universität zu Kiel (DE)
- National Institute for Public Health and the Environment (NL)
- Venue
- European Journal of Nutrition
- Published
- 2004-12-01
- Volume
- 44
- Issue
- 7
- Pages
- 406-413
- ISSN
- 1436-6207 (ISSN-L)
- 1436-6215
- OpenAlex
- W2017162748
- Cited by
- 190
- References
- 30
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 5 · 2023: 6 · 2022: 8 · 2021: 10 · 2020: 8 · 2019: 7 · 2018: 6 · 2017: 10 · 2016: 6 · 2015: 7 · 2014: 13 · 2013: 15 · 2012: 13
- FWCI
- 7.84
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- European Journal of Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Rivm Repository (Netherlands National Institute for Public Health and the Environment) (submittedVersion)
- OpenAgrar (submittedVersion)
- 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 › Immunology › Immune responses and vaccinations
- Keywords
- probiotics, Lactobacillus rhamnosus GG, polio vaccination, oral polio vaccine, poliovirus neutralizing antibodies, booster vaccination, IgA, IgG, IgM, acidified milk
- MeSH terms
- Adult, Antibodies, Viral, Double-Blind Method, Enzyme-Linked Immunosorbent Assay, Humans, Immunoglobulin A, Immunoglobulin G, Immunoglobulin M, Immunization, Secondary, Lactobacillus acidophilus, Male, Neutralization Tests, Poliomyelitis, Poliovirus Vaccine, Oral, Viral Vaccines, Poliovirus, Probiotics, Lacticaseibacillus rhamnosus
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
