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The influence of probiotics on vaccine responses—A systematic review
Abstract
The immunomodulatory effects of probiotics may influence the response to vaccines. We systematically reviewed prospective randomised placebo-controlled studies in humans that have investigated the effect of probiotics on humoral vaccine responses. We found 26 studies, involving 3812 participants, investigating the effect of 40 different probiotic strains on the response to 17 different vaccines. A beneficial effect of probiotics was reported in about half of the studies. The evidence for a beneficial effect of probiotics on vaccine response was strongest for oral vaccinations and for parenteral influenza vaccination. However, there was substantial variation between studies in the choice of probiotic, strain, dose, viability, purity, and duration and timing of administration. The one study that investigated the effect of probiotic administration to mothers during pregnancy found lower vaccine responses in their infants. The studies in our review suggest that probiotics offer a relatively cheap intervention to improve vaccine efficacy and duration of protection. Future studies should focus on establishing optimal strains, doses and timing of administration in relation to vaccination.
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“The researchers found evidence suggesting that certain probiotics can enhance the immune system’s response to influenza vaccination, which increases the potential benefit for the elderly, in whom the response to influenza vaccination (seroconversion) is impaired [179].”
From The Potential Impact of Probiotics on Human Health: An Update on Their Health-Promoting Properties (2024) · cites this paper as [179]
Citations
Cites
Hill (2014) · doi:10.1038/nrgastro.2014.66 · Cited by 9,592
Sex differences in immune responses
Klein, S. L., & Flanagan, K. L. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2016.90 · Cited by 6,370
The gut microbiota and host health: a new clinical frontier
Marchesi, J. R., Adams, D. H., Fava, F., Hermes, G. D. A., Hirschfield, G. M., Hold, G., Quraishi, M. N., Kinross, J., Smidt, H., Tuohy, K. M., et al. (2016) · Gut · doi:10.1136/gutjnl-2015-309990 · Cited by 2,302
Guarino, A., Ashkenazi, S., Gendrel, D., Lo Vecchio, A., Shamir, R., & Szajewska, H. (2014) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000000375 · Cited by 935
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
Probiotics for the prevention of pediatric antibiotic-associated diarrhea
Goldenberg, J. Z., Lytvyn, L., Steurich, J., Parkin, P. C., Mahant, S., & Johnston, B. C. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd004827.pub4 · Cited by 635
Fiocchi, A., Pawankar, R., Cuello-Garcia, C., Ahn, K., Al-Hammadi, S., Agarwal, A., Beyer, K., Burks, W., Canonica, G. W., Ebisawa, M., et al. (2015) · World Allergy Organization Journal · doi:10.1186/s40413-015-0055-2 · Cited by 473
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
Cuello-Garcia, C. A., Brożek, J. L., Fiocchi, A., Pawankar, R., Yepes-Nuñez, J. J., Terracciano, L., Gandhi, S., Agarwal, A., Zhang, Y., & Schünemann, H. J. (2015) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2015.04.031 · Cited by 383
Improved immunogenicity of oral D x RRV reassortant rotavirus vaccine by Lactobacillus casei GG
Isolauri, E., Joensuu, J., Suomalainen, H., Luomala, M., & Vesikari, T. (1995) · Vaccine · doi:10.1016/0264-410x(95)93319-5 · Cited by 370
Harris, V. C., Armah, G., Fuentes, S., Korpela, K. E., Parashar, U., Victor, J. C., Tate, J., de Weerth, C., Giaquinto, C., Wiersinga, W. J., et al. (2017) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiw518 · Cited by 299
Long, J. E., Drayson, M. T., TAYLOR, A. E. R., Toellner, K., Lord, J. M., & Phillips, A. C. (2016) · Vaccine · doi:10.1016/j.vaccine.2016.04.032 · Cited by 294
Probiotic Administration in Early Life, Atopy, and Asthma: A Meta-analysis of Clinical Trials
Elazab, N., Mendy, A., Gasana, J., Vieira, E. R., Quizon, A., & Forno, E. (2013) · PEDIATRICS · doi:10.1542/peds.2013-0246 · Cited by 269
Use of Probiotics for Management of Acute Gastroenteritis
Szajewska, H., Guarino, A., Hojsak, I., Indrio, F., Kolaček, S., Shamir, R., Vandenplas, Y., & Weizman, Z. (2014) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000000320 · Cited by 267
Oral intake of Lactobacillus fermentum CECT5716 enhances the effects of influenza vaccination
Olivares, M. M., Díaz-Ropero, M. P., Sierra, S., Lara‐Villoslada, F., Fonollá, J., Navas, M., Rodríguez, J. M., & Xaus, J. (2007) · Nutrition · doi:10.1016/j.nut.2007.01.004 · Cited by 264
Modulation of humoral immune response through probiotic intake
He, F., Tuomola, E., Arvilommi, H. S., & Seppo, S. (2000) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2000.tb01504.x · Cited by 230
Boge, T., Remigy, M., Vaudaine, S., Tanguy, J., Bourdet‐Sicard, R., & van der Werf, S. (2009) · Vaccine · doi:10.1016/j.vaccine.2009.06.094 · Cited by 221
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
Probiotics, Immunomodulation, and Health Benefits
Gill, H., & Prasad, J. (2007) · Springer eBooks · doi:10.1007/978-0-387-74087-4_17 · Cited by 213
Genetic regulation of immune responses to vaccines in early life
Newport, M. J., Goetghebuer, T., Weiss, H. A., The MRC Gambia Twin Study Group, Whittle, H., Siegrist, C., & Marchant, A. (2004) · Genes and Immunity · doi:10.1038/sj.gene.6364051 · Cited by 208
de Vrese, M., Rautenberg, P., Laue, C., Koopmans, M., Herremans, T., & Schrezenmeir, J. (2005) · European Journal of Nutrition · doi:10.1007/s00394-004-0541-8 · Cited by 190
Paineau, D., Carcano, D., Leyer, G., Darquy, S., Alyanakian, M., Simoneau, G., Bergmann, J., Brassart, D., Bornet, F. R. J., & Ouwehand, A. C. (2008) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2008.00413.x · Cited by 187
Davidson, L. E., Fiorino, A.-M., Snydman, D. R., & Hibberd, P. L. (2011) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2010.289 · Cited by 170
Mullié, C., Yazourh, A., Thibault, H., Odou, M., Singer, E., Kalach, N., Kremp, O., & Romond, M. (2004) · Pediatric Research · doi:10.1203/01.pdr.0000141955.47550.a0 · Cited by 151
Bunout, D. C., Barrera, G. F., Hirsch, S., Gattas, V., de la Maza, M., Haschke, F., Steenhout, P. G., Klassen, P., Hager, C., Avendano, M., et al. (2004) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607104028005348 · Cited by 143
Ueno, N., Fujiya, M., Segawa, S., Nata, T., Moriichi, K., Tanabe, H., Mizukami, Y., Kobayashi, N., Ito, K., & Kohgo, Y. (2011) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21597 · Cited by 130
Probiotics for the Prevention of Pediatric Antibiotic-Associated Diarrhea
Hayes, S. R., & Vargas, A. J. (2016) · EXPLORE · doi:10.1016/j.explore.2016.08.015 · Cited by 123
Probiotics to Prevent or Treat Excessive Infant Crying
Sung, V., Collett, S., de Gooyer, T., Hiscock, H., Tang, M. L. K., & Wake, M. A. (2013) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2013.2572 · Cited by 119
NAMBA, K., Hatano, M., Yaeshima, T., Takase, M., & Suzuki, K. (2010) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.90749 · Cited by 111
Diarrhea in Preschool Children and Lactobacillus reuteri: A Randomized Controlled Trial
Gutiérrez‐Castrellón, P., López‐Velázquez, G., Díaz‐García, L., Jiménez-Gutiérrez, C., Mancilla-Ramı́rez, J., Estevez‐Jimenéz, J., & Parra, M. (2014) · PEDIATRICS · doi:10.1542/peds.2013-0652 · Cited by 109
Puyenbroeck, K. V., Hens, N., Coenen, S., Michiels, B., Beunckens, C., Molenberghs, G., Royen, P. V., & Verhoeven, V. (2012) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.111.026831 · Cited by 109
Liu, S., Hu, P., Du, X., Zhou, T., & Pei, X. (2013) · Indian Pediatrics · doi:10.1007/s13312-013-0123-z · Cited by 108
Lagos, R., Fasano, A., Wasserman, S. S., Prado, V., Martin, O. S., Abrego, P. L., Losonsky, G. A., Alegria, S., & Levine, M. M. (1999) · The Journal of Infectious Diseases · doi:10.1086/315051 · Cited by 108
Eloe‐Fadrosh, E. A., McArthur, M. A., Seekatz, A. M., Drábek, E. F., Rasko, D. A., Sztein, M. B., & Fraser, C. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062026 · Cited by 106
Kukkonen, A. K., Nieminen, T., Poussa, T. A., Savilahti, E., & Kuitunen, M. (2006) · Pediatric Allergy and Immunology · doi:10.1111/j.1399-3038.2006.00420.x · Cited by 106
West, C. E., Gothefors, L., Granström, M., Käyhty, H. M., Hammarström, M., & Hernell, O. (2008) · Pediatric Allergy and Immunology · doi:10.1111/j.1399-3038.2007.00583.x · Cited by 105
Jespersen, L., Tarnow, I., Eskesen, D. C., Melsæther, C., Michelsen, B., Bügel, S., Dragsted, L. O., Rijkers, G. T., & Calder, P. C. (2015) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.114.103531 · Cited by 105
Posteraro, B., Pastorino, R., Giannantonio, P. D., Ianuale, C., Amore, R., Ricciardi, W., & Boccia, S. (2014) · Vaccine · doi:10.1016/j.vaccine.2014.01.057 · Cited by 101
Wu, B., Yang, Y., Xu, X., & Wang, W. (2015) · World Journal of Pediatrics · doi:10.1007/s12519-015-0025-3 · Cited by 97
Silva, J. R. N., Camacho, L. A. B., Siqueira, M. M., Freire, M. D. S., Castro, Y. P., Maia, M. D. L. D. S., Yamamura, A. M. Y., Martins, R. D. M., & Leal, M. D. L. F. (2011) · Vaccine · doi:10.1016/j.vaccine.2011.05.019 · Cited by 96
Immunomodulatory effects of probiotics in different stages of life
Nova, E., Wärnberg, J., Gómez-Martínez, S., Díaz, L. E., Romeo, J., & Marcos, A. (2007) · British Journal Of Nutrition · doi:10.1017/s0007114507832983 · Cited by 96
Taylor, A. L., Hale, J., Wiltschut, J., Lehmann, H. S., Dunstan, J. A., & Prescott, S. L. (2006) · Clinical & Experimental Allergy · doi:10.1111/j.1365-2222.2006.02553.x · Cited by 81
Soh, 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
Bosch, M., Méndez, M., Pérez, M., Farrán-Codina, A., Fuentes, M. C., & Cuñé, J. (2012) · PubMed · doi:10.1590/s0212-16112012000200023 · Cited by 75
Maruyama, M., Abe, R., Shimono, T., Iwabuchi, N., Abe, F., & Xiao, J. (2015) · International Journal of Food Sciences and Nutrition · doi:10.3109/09637486.2015.1126564 · Cited by 75
Matsuda, F., Chowdhury, M. I., Saha, A., Asahara, T., Nomoto, K., Tarique, A. A., Ahmed, T., Nishibuchi, M., Cravioto, A., & Qadri, F. (2011) · Vaccine · doi:10.1016/j.vaccine.2010.12.133 · Cited by 53
Pérez, N., Iannicelli, J. C., Girard-Bosch, C., González, S., Varea, A., Disalvo, L., Apezteguía, M., Pernas, J., Vicentin, D., & Cravero, R. (2009) · European Journal of Nutrition · doi:10.1007/s00394-009-0063-5 · Cited by 43
L actobacillus in Jelly Enhances the Effect of Influenza Vaccination in Elderly Individuals
Akatsu, H., Arakawa, K., Yamamoto, T., Kanematsu, T., Matsukawa, N., Ohara, H., & Maruyama, M. (2013) · Journal of the American Geriatrics Society · doi:10.1111/jgs.12474 · Cited by 40
Youngster, I., Kozer, E., Lazarovitch, Z., Broide, E., & Goldman, M. (2011) · Archives of Disease in Childhood · doi:10.1136/adc.2010.197459 · Cited by 38
Martins, C. L., Garly, M. ‐., Bale, C., Rodrigues, A., Njie-Jobe, J., Benn, C. S., Whittle, H., & Aaby, P. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu117 · Cited by 38
Park, D. E., Johnson, T. S., Nonyane, B. A. S., Chandir, S., Conklin, L. M., Fleming-Dutra, K. E., Loo, J. D., Goldblatt, D., Whitney, C. G., O’Brien, K. L., et al. (2013) · The Pediatric Infectious Disease Journal · doi:10.1097/inf.0000000000000081 · Cited by 38
Human leukocyte antigen polymorphisms: variable humoral immune responses to viral vaccines
Ovsyannikova, I. G., Dhiman, N., Jacobson, R. M., & Poland, G. A. (2006) · Expert Review of Vaccines · doi:10.1586/14760584.5.1.33 · Cited by 35
Licciardi, P. V., Ismail, I. H., Balloch, A., Mui, M., Hoe, E., Lamb, K. E., & Tang, M. L. K. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00381 · Cited by 30
Nagafuchi, S., Yamaji, T., Kawashima, A., Saito, Y., Takahashi, T., Yamamoto, T., Maruyama, M., & Akatsu, H. (2015) · Pharmaceuticals · doi:10.3390/ph8020351 · Cited by 29
(2001) · PubMed · Cited by 28
Redondo, N., Nova, E., Gheorghe, A., Díaz, L. E., Hernández, A., & Marcos, A. (2017) · Nutrition & Metabolism · doi:10.1186/s12986-016-0154-2 · Cited by 26
Sang, L.-X., Chang, B., Wang, B., Liu, W., & Jiang, M. (2015) · PubMed Central · Cited by 22
Talking about cross-talk: the immune system and the microbiome
Zeevi, D., Korem, T., & Segal, E. (2016) · Genome biology · doi:10.1186/s13059-016-0921-4 · Cited by 21
Simondon, F., Preziosi, M.-P., Pinchinat, S., Yam, A., Chabirand, L., Wassilak, S. G. F., Pines, E., Trape, J., Salomon, H., & Hoffenbach, A. (1999) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s100960050221 · Cited by 20
Lalwani, S. K., Chatterjee, S., Chhatwal, J., Simon, A., Ravula, S. M., François, N., Mehta, S., Strezova, A., & Borys, D. (2014) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00068-14 · Cited by 9
Research works printed but not linked: 2
- Harris, 2016, The infant gut microbiome correlates significantly with rotavirus vaccine response in rural Ghana, J Infect Dis
- Redondo, 2017, Evaluation of Lactobacillus coryniformis CECT5711 strain as a coadjuvant in a vaccination process: a randomised clinical trial in healthy adults, Nutrition and Metabolism., 14
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Metadata
- Authors
- Zimmermann, P., & Curtis, N.
- Affiliations
- Royal Children's Hospital (AU)
- Corresponding author
- Zimmermann, Petra
- Venue
- Vaccine
- Publisher
- Elsevier BV
- Published
- 2018-01
- Volume
- 36
- Issue
- 2
- Pages
- 207-213
- ISSN
- 0264-410X (ISSN-L)
- OpenAlex
- W2755772860
- Cited by
- 142
- References
- 62
- Citations by year
- 2026: 13 · 2025: 16 · 2024: 14 · 2023: 14 · 2022: 21 · 2021: 23 · 2020: 12 · 2019: 17 · 2018: 11
- FWCI
- 1.21
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Vaccine (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
- Keywords
- probiotics, vaccine response, humoral immunity, immunomodulation, oral immunization, influenza vaccination, probiotic strains, vaccine efficacy, duration of protection
- MeSH terms
- Humans, Placebos, Vaccines, Randomized Controlled Trials as Topic, Probiotics, Immunity, Humoral
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