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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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.
“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]
Cites
Hill (2014) · doi:10.1038/nrgastro.2014.66 · Cited by 9,592 · see citing works
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 · see citing works
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 · see citing works
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 · 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
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 625 · see citing works
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 · 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
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 226 · see citing works
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 · 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
Probiotics, Immunomodulation, and Health Benefits
Gill, H., & Prasad, J. (2007) · Springer eBooks · doi:10.1007/978-0-387-74087-4_17 · Cited by 213 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 128 · see citing works
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 · see citing works
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 · see citing works
NAMBA, K., Hatano, M., Yaeshima, T., Takase, M., & Suzuki, K. (2010) · Bioscience Biotechnology and Biochemistry · doi:10.1271/bbb.90749 · Cited by 111 · see citing works
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 · see citing works
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 · see citing works
Liu, S., Hu, P., Du, X., Zhou, T., & Pei, X. (2013) · Indian Pediatrics · doi:10.1007/s13312-013-0123-z · Cited by 108 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 104 · see citing works
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 104 · see citing works
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 103 · see citing works
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 · see citing works
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 · see citing works
Wu, B., Yang, Y., Xu, X., & Wang, W. (2015) · World Journal of Pediatrics · doi:10.1007/s12519-015-0025-3 · Cited by 92 · see citing works
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 80 · see citing works
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 · see citing works
Bosch, M., Méndez, M., Pérez, M., Farrán-Codina, A., Fuentes, M. C., & Cuñé, J. (2012) · PubMed · doi:10.1590/s0212-16112012000200023 · Cited by 75 · see citing works
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 · see citing works
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 · see citing works
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 42 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Sang, L.-X., Chang, B., Wang, B., Liu, W., & Jiang, M. (2015) · PubMed Central · Cited by 22 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Flagged first, then by citations
2 of the 62 references couldn’t be matched to a known paper.
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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Factors That Influence the Immune Response to Vaccination
Zimmermann, P., & Curtis, N. C. (2019) · Clinical Microbiology Reviews · doi:10.1128/cmr.00084-18 · Cited by 940 · see citing works
Self-citationMucosal vaccines — fortifying the frontiers
Lavelle, E. C., & Ward, R. W. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-021-00583-2 · Cited by 763 · see citing works
The Potential Impact of Probiotics on Human Health: An Update on Their Health-Promoting Properties
Maftei, N.-M., Raileanu, C. R., Balta, A. A., Ambrose, L., Boev, M., Marin, D. B., & Lisa, E. L. (2024) · Microorganisms · doi:10.3390/microorganisms12020234 · Cited by 381 · see citing works
Lynn, D. J., Benson, S. C., Lynn, M. A., & Pulendran, B. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-021-00554-7 · Cited by 300 · see citing works
Tian, M., He, X., Feng, Y., Wang, W., Chen, H., Gong, M., Liu, D., Clarke, J. L., & van Eerde, A. (2021) · Antibiotics · doi:10.3390/antibiotics10050539 · Cited by 277 · see citing works
Early-Life Antibiotic-Driven Dysbiosis Leads to Dysregulated Vaccine Immune Responses in Mice
Lynn, M. A., Tumes, D. J., Choo, J. M., Sribnaia, A., Blake, S. J., Leong, L. E. X., Young, G. P., Marshall, H. S., Wesselingh, S. L., Rogers, G. B., et al. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.04.009 · Cited by 199 · see citing works
The role of the gut microbiome in shaping the immune system of chickens
Broom, L. J., & Kogut, M. H. (2018) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2018.10.002 · Cited by 191 · 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
Role of the Microbiota in the Modulation of Vaccine Immune Responses
Ciabattini, A., Olivieri, R., Lazzeri, E., & Medaglini, D. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01305 · Cited by 151 · see citing works
The influence of the intestinal microbiome on vaccine responses
Zimmermann, P., & Curtis, N. C. (2018) · Vaccine · doi:10.1016/j.vaccine.2018.04.066 · Cited by 146 · see citing works
Self-citationThe Evolving Microbiome from Pregnancy to Early Infancy: A Comprehensive Review
Mesa, M. D., Loureiro, B., Iglesia, I., Gonzalez, S. F., Llurba, E., García‐Algar, Ó., Solana, M. J., Cabero-Pérez, M. J., Sainz, T., Martínez, L., et al. (2020) · Nutrients · doi:10.3390/nu12010133 · Cited by 146 · see citing works
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Jain, N. (2020) · Gut microbes · doi:10.1080/19490976.2020.1824564 · Cited by 106 · see citing works
Microbiome as a tool and a target in the effort to address antimicrobial resistance
Relman, D. A., & Lipsitch, M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1717163115 · Cited by 105 · see citing works
Yeh, T.-L., Shih, P.-C., Liu, S.-J., Lin, C.-H., Liu, J.-M., Lei, W.-T., & Lin, C.-Y. (2018) · Drug Design Development and Therapy · doi:10.2147/dddt.s155110 · Cited by 93 · see citing works
Interventions to improve oral vaccine performance: a systematic review and meta-analysis
Church, J. A., Parker, E. P. K., Kirkpatrick, B. D., Grassly, N. C., & Prendergast, A. J. (2019) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(18)30602-9 · Cited by 75 · see citing works
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Emerging Frontiers in Microbiome Engineering
Inda, M. E., Broset, E., Lu, T. K., & de la Fuente‐Núñez, C. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.08.007 · Cited by 73 · see citing works
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Mechanisms linking the human gut microbiome to prophylactic and treatment strategies for COVID-19
Walton, G., Gibson, G. R., & Hunter, K. A. (2020) · British Journal Of Nutrition · doi:10.1017/s0007114520003980 · Cited by 66 · see citing works
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Tsai, C. J., Loh, J. M. S., Fujihashi, K., & Kiyono, H. (2023) · Expert Review of Vaccines · doi:10.1080/14760584.2023.2268724 · Cited by 63 · see citing works
The early-life gut microbiome and vaccine efficacy
Jordan, A., Carding, S. R., & Hall, L. J. (2022) · The Lancet Microbe · doi:10.1016/s2666-5247(22)00185-9 · Cited by 58 · see citing works
Desselberger, U. (2018) · Pathogens · doi:10.3390/pathogens7030057 · Cited by 55 · see citing works
Vibrio cholerae at the Intersection of Immunity and the Microbiome
Weil, A. A., Seykora, R., & Harris, J. B. (2019) · mSphere · doi:10.1128/msphere.00597-19 · Cited by 60 · see citing works
Fuloria, S., Mehta, J., Talukdar, M. P., Sekar, M., Gan, S. H., Subramaniyan, V., Rani, N. N. I. M., Begum, M. Y., Chidambaram, K., Nordin, R. B., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.950913 · Cited by 47 · see citing works
Tomalka, J. A., Suthar, M. S., Deeks, S. G., & Sékaly, R. (2022) · Nature Immunology · doi:10.1038/s41590-022-01130-4 · Cited by 45 · see citing works
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Nunez, N., Réot, L., & Menu, E. (2021) · Vaccines · doi:10.3390/vaccines9060584 · Cited by 37 · see citing works
dos Santos, C. I., Campos, C. D. L., Neto, W. R. N., do Carmo, M. S., Nogueira, F. A. B., Ferreira, R. M., Costa, E. P. D. S., Gonzaga, L. F., Araújo, J. M. M., Monteiro, J. D. M., et al. (2021) · Journal of Fungi · doi:10.3390/jof7100794 · Cited by 38 · see citing works
Mohr, A. E., Basile, A. J., Crawford, M. S., Sweazea, K. L., & Carpenter, K. C. (2020) · Journal of the Academy of Nutrition and Dietetics · doi:10.1016/j.jand.2019.08.018 · Cited by 37 · see citing works
Is the oral microbiome a source to enhance mucosal immunity against infectious diseases?
Zenobia, C., Herpoldt, K., & Freire, M. (2021) · npj Vaccines · doi:10.1038/s41541-021-00341-4 · Cited by 37 · see citing works
Bianchini, S., Orabona, C., Camilloni, B., Berioli, M. G., Argentiero, A., Matino, D., Alunno, A., Albini, E., Vacca, C., Pallotta, M. T., et al. (2019) · Human Vaccines & Immunotherapeutics · doi:10.1080/21645515.2019.1633877 · Cited by 36 · see citing works
Immune modulatory capacity of probiotic lactic acid bacteria and applications in vaccine development
Mojgani, N., Shahali, Y., & Dadar, M. (2020) · Beneficial Microbes · doi:10.3920/bm2019.0121 · Cited by 35 · see citing works
Akatsu, H. (2021) · Vaccines · doi:10.3390/vaccines9020136 · Cited by 36 · see citing works
The immunological interplay between vaccination and the intestinal microbiota
Zimmermann, P. (2023) · npj Vaccines · doi:10.1038/s41541-023-00627-9 · Cited by 35 · see citing works
Self-citationLenoir-Wijnkoop, I., Merenstein, D., Korchagina, D., Broholm, C., Sanders, M. E., & Tancredi, D. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00980 · Cited by 34 · see citing works
Church, J. A., Rukobo, S., Govha, M., Lee, B., Carmolli, M. P., Chasekwa, B., Ntozini, R., Mutasa, K., McNeal, M., Majo, F. D., et al. (2019) · Clinical Infectious Diseases · doi:10.1093/cid/ciz140 · Cited by 32 · see citing works
Wong‐Chew, R. M., de Castro, J.-A. A., Morelli, L., Perez, M. I., & Özen, M. (2022) · Expert Review of Clinical Immunology · doi:10.1080/1744666x.2022.2085559 · Cited by 33 · see citing works
Probiotics as Adjuvants in Vaccine Strategy: Is There More Room for Improvement?
Peroni, D. G., & Morelli, L. (2021) · Vaccines · doi:10.3390/vaccines9080811 · Cited by 31 · see citing works
The Interplay between Immunosenescence and Microbiota in the Efficacy of Vaccines
Cianci, R., Franza, L., Massaro, M. G., Borriello, R., Vito, F., & Gambassi, G. (2020) · Vaccines · doi:10.3390/vaccines8040636 · Cited by 31 · see citing works
Shenoy, S. (2021) · Inflammation Research · doi:10.1007/s00011-021-01510-w · Cited by 31 · see citing works
Boosting vaccine effectiveness: The groundbreaking role of probiotics
Abavisani, M., Ebadpour, N., Khoshrou, A., & Sahebkar, A. (2024) · Journal of Agriculture and Food Research · doi:10.1016/j.jafr.2024.101189 · Cited by 29 · see citing works
Systematic review of the impact of intestinal microbiota on vaccine responses
Ardura‐Garcia, C., Curtis, N. C., & Zimmermann, P. (2024) · npj Vaccines · doi:10.1038/s41541-024-01000-0 · Cited by 29 · see citing works
Self-citationTopical Microbial Therapeutics against Respiratory Viral Infections
Spacova, I., Boeck, I. D., Bron, P. A., Delputte, P., & Lebeer, S. (2021) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2021.03.009 · Cited by 29 · see citing works
Immunization of preterm infants: current evidence and future strategies to individualized approaches
Fortmann, M. I., Dirks, J., Goedicke‐Fritz, S., Liese, J. G., Zemlin, M., Morbach, H., & Härtel, C. (2022) · Seminars in Immunopathology · doi:10.1007/s00281-022-00957-1 · Cited by 36 · see citing works
Challenges of a one-health approach to the development of alternatives to antibiotics
McAllister, T. A., Wang, Y., Diarra, M. S., Alexander, T. W., & Stanford, K. (2018) · Animal Frontiers · doi:10.1093/af/vfy002 · Cited by 27 · see citing works
Aboleila, S. M., Salah, A. S., Mohamed, R. A., & Diab, A. M. (2022) · Aquaculture Research · doi:10.1111/are.15989 · Cited by 23 · see citing works
Karl, J. P. (2020) · Military Medicine · doi:10.1093/milmed/usaa261 · Cited by 23 · see citing works
Forsgård, R. A., Rode, J., Lobenius-Palmér, K., Kamm, A., Patil, S., Tacken, M. G. J., Lentjes, M. A. H., Axelsson, J., Grompone, G., Montgomery, S., et al. (2023) · Gut Microbes · doi:10.1080/19490976.2023.2229938 · Cited by 24 · see citing works
Ray, S., Narayanan, A., Vesterbacka, J., Blennow, O., Chen, P., Gao, Y., Gabarrini, G., Ljunggren, H., Buggert, M., Manoharan, L., et al. (2023) · npj Biofilms and Microbiomes · doi:10.1038/s41522-023-00461-w · Cited by 23 · see citing works
The Exposome and Immune Health in Times of the COVID-19 Pandemic
Morales, J. S., Valenzuela, P. L., Castillo‐García, A., Butragueño, J., Jiménez‐Pavón, D., Carrera‐Bastos, P., & Lucía, A. (2021) · Nutrients · doi:10.3390/nu14010024 · Cited by 22 · see citing works
Domnich, A., Manini, I., Calabrò, G. E., de Waure, C., & Montomoli, E. (2019) · Vaccines · doi:10.3390/vaccines7040215 · Cited by 22 · see citing works
Rossouw, C., Ryan, F. J., & Lynn, D. J. (2024) · FEBS Journal · doi:10.1111/febs.17241 · Cited by 22 · see citing works
Cram, J. A., Fiore-Gartland, A. J., Srinivasan, S., Karuna, S., Pantaleo, G., Tomaras, G. D., Fredricks, D. N., & Kublin, J. G. (2019) · PLoS ONE · doi:10.1371/journal.pone.0225622 · Cited by 21 · see citing works
Santos, F. D. S., Maubrigades, L. R., Gonçalves, V. S., Ferreira, M. R. A., Brasil, C. L., Cunha, R. C., Conceição, F. R., & Leite, F. P. L. (2021) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2021.110272 · Cited by 21 · see citing works
Recent advances in influenza vaccines
Pawelec, G., & McElhaney, J. E. (2020) · F1000Research · doi:10.12688/f1000research.22611.1 · Cited by 20 · see citing works
Probiotics: A gut response to the COVID-19 pandemic but what does the evidence show?
Brahma, S., Naik, A. S., & Lordan, R. (2022) · Clinical Nutrition ESPEN · doi:10.1016/j.clnesp.2022.08.023 · Cited by 20 · see citing works
Pharmacological Efficacy of Probiotics in Respiratory Viral Infections: A Comprehensive Review
Wahab, S., Almaghaslah, D., Mahmood, S. E., Ahmad, M. F., Alsayegh, A. A., Haddash, Y. M. A., Rahman, M. A., Ahamd, I., Ahmad, W., Khalid, M., et al. (2022) · Journal of Personalized Medicine · doi:10.3390/jpm12081292 · Cited by 18 · see citing works
Probiotic Fermented Foods and Health Promotion
Ashraf, S. A., Elkhalifa, A. E. O., Ahmad, M. F., Patel, M. B., Adnan, M., & Sulieman, A. M. E. (2022) · Springer eBooks · doi:10.1007/978-3-030-82902-5_6 · Cited by 17 · see citing works
Giraldo, P. C., Sanches, J. M., Sparvoli, L. G., do Amaral, R. L. G., Migliorini, I., Gil, C. D., Taddei, C. R., Witkin, S. S., & Discacciati, M. G. (2021) · Brazilian Journal of Microbiology · doi:10.1007/s42770-021-00616-x · Cited by 16 · see citing works
Parreño, V. G., Bai, M., Liu, F., Jing, J., Olney, E., Li, G., Wen, K., Yang, X., Bui, T., Kocher, J., et al. (2022) · Vaccines · doi:10.3390/vaccines10091529 · Cited by 16 · see citing works
Factors Influencing Microbiota in Modulating Vaccine Immune Response: A Long Way to Go
Ponziani, F. R., Coppola, G., Rio, P., Caldarelli, M., Borriello, R., Gambassi, G., Gasbarrini, A., & Cianci, R. (2023) · Vaccines · doi:10.3390/vaccines11101609 · Cited by 17 · see citing works
Vaccine Interactions With the Infant Microbiome: Do They Define Health and Disease?
Ruck, C. E., Odumade, O. A., & Smolen, K. K. (2020) · Frontiers in Pediatrics · doi:10.3389/fped.2020.565368 · Cited by 15 · see citing works
Montazeri‐Najafabady, N., Kazemi, K., & Gholami, A. (2022) · Biologia · doi:10.1007/s11756-022-01147-y · Cited by 16 · see citing works
Functional Food Ingredients Enhancing Immune Health: A Systematic Review
Skenderidou, I., Leontopoulos, S., & Skenderidis, P. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26178408 · Cited by 15 · see citing works
Immune Aging, Immunosenescence, and Inflammaging: Implications for Vaccine Response in Older Adults
Falahi, S., Abdoli, A., & Kenarkoohi, A. (2025) · Health Science Reports · doi:10.1002/hsr2.71119 · Cited by 18 · see citing works
El‐Saadony, M. T., Saad, A. M., Sitohy, M. Z., Alkafaas, S. S., Dladla, M., Ghosh, S., Mohammed, D. M., Ibrahim, E. H., Fahmy, M. A., Elkelish, A., et al. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1713426 · Cited by 13 · see citing works
Reens, A. L., Cabral, D. J., Liang, X., Norton, J. E., Therien, A. G., Hazuda, D. J., & Swaminathan, G. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.643255 · Cited by 13 · see citing works
Rafiee, M., Sereshki, N., Alipour, R., Ahmadipanah, V., Sarvar, D. P., & Wilkinson, D. M. (2022) · BMC Immunology · doi:10.1186/s12865-022-00506-3 · Cited by 13 · see citing works
Impact of the Host Microbiome on Vaccine Responsiveness: Lessons Learned and Future Perspective
Stefanetti, G., & Kasper, D. L. (2022) · Biochemistry · doi:10.1021/acs.biochem.2c00309 · Cited by 13 · see citing works
Influence of biotic interventions on the immune response to vaccines in young and older adults
Spacova, I., Patusco, R., Lebeer, S., & Jensen, M. G. (2023) · Clinical Nutrition · doi:10.1016/j.clnu.2023.01.001 · Cited by 12 · see citing works
Modulation of oral vaccine efficacy by the gut microbiota
Hou, Y., Li, J., & Wu, Y. (2025) · npj Vaccines · doi:10.1038/s41541-025-01240-8 · Cited by 10 · see citing works
A paediatric influenza update 100 years after the Skyros island Spanish flu outbreak
Mammas, I., Theodoridou, M., Thiagarajan, P., Melidou, A., Papaioannou, G. C., Korovessi, P., Koutsaftiki, C., Papatheodoropoulou, A., Calachanis, M., Dalianis, T., et al. (2019) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2019.7515 · Cited by 10 · see citing works
Zimmermann, P., Kurth, S., Giannoukos, S., Stocker, M., & Bokulich, N. A. (2025) · BMJ Open · doi:10.1136/bmjopen-2024-092938 · Cited by 9 · see citing works
Self-citationBai, Y., Wang, G., Qi, H., Wang, Y., Xu, C., Yue, L., Hou, X., & Yu, L. (2019) · Research in Veterinary Science · doi:10.1016/j.rvsc.2019.12.016 · Cited by 9 · see citing works
Genetically Modified Lactic Acid Bacteria: a Promising Mucosal Delivery Vector for Vaccines
Chowdhury, M. R., Islam, M. A., Yurina, V., & Shimosato, T. (2025) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-025-10667-3 · Cited by 9 · see citing works
Crosstalk between COVID-19 and the gut-brain axis: a gut feeling
Kalam, N., & Balasubramaniam, V. R. M. T. (2024) · Postgraduate Medical Journal · doi:10.1093/postmj/qgae030 · Cited by 8 · see citing works
Diet, microbiome, and probiotics establish a crucial link in vaccine efficacy
Dutta, S., Chatterjee, N., Gallina, N. L. F., Kar, S., Koley, H., Nanda, P. K., Biswas, O., Das, A. K., Biswas, S., Bhunia, A. K., et al. (2025) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2025.2480230 · Cited by 7 · see citing works
Sørensen, C. A., Fuglsang, E., Jørgensen, C. S., Laursen, R. P., Larnkjær, A., Mølgaard, C., Ritz, C., Michaelsen, K. F., Krogfelt, K. A., & Frøkiær, H. (2018) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2018.07.031 · Cited by 7 · see citing works
Liu, M., Dai, X., Li, J., Xiao, D., Chen, B., Wang, Z., Tang, Y., Zeng, Y., Zhang, D., Ni, X., et al. (2024) · Aquaculture · doi:10.1016/j.aquaculture.2024.742051 · Cited by 6 · see citing works
The antiviral effects and underlying mechanisms of probiotics on viral infections
Javanshir, N., Ebrahimi, V., Mazhary, Z., Jahromi, B. S., Zuo, T., & Fard, N. A. (2025) · Microbial Pathogenesis · doi:10.1016/j.micpath.2025.107377 · Cited by 6 · see citing works
The “Microbiome”: A Protagonist in COVID-19 Era
Merra, G., Capacci, A., Cenname, G., Esposito, E., Dri, M., Renzo, L. D., & Marchetti, M. (2022) · Microorganisms · doi:10.3390/microorganisms10020296 · Cited by 6 · see citing works
Morales, C. G., Jimenez, N. R., Herbst‐Kralovetz, M. M., & Lee, N. (2022) · Medical Sciences · doi:10.3390/medsci10030052 · Cited by 6 · see citing works
Hunter, J., & Harnett, J. (2023) · Australian Journal of General Practice · doi:10.31128/ajgp-12-22-6631 · Cited by 6 · see citing works
Gulliver, E. L., Simone, S. K. D., Chonwerawong, M., & Forster, S. C. (2024) · Microbial Biotechnology · doi:10.1111/1751-7915.70041 · Cited by 5 · see citing works
Jeron, A., Boehme, J. D., Volckmar, J., Gereke, M., Yevsa, T., Geffers, R., Guzmán, C. A., Schreiber, J., Stegemann‐Koniszewski, S., & Bruder, D. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19092602 · Cited by 5 · see citing works
Haile, A. F., Woodfint, R. M., Kim, E., Joldrichsen, M. R., Berhe, N., Gebreyes, W. A., & Boyaka, P. N. (2021) · Vaccines · doi:10.3390/vaccines9111240 · Cited by 5 · see citing works
Vadopalas, L., Badaras, Š., Ružauskas, M., Lėlė, V., Starkutė, V., Zavistanavičiūtė, P., Zokaitytė, E., Bartkevičs, V., Klupšaitė, D., Mozūrienė, E., et al. (2020) · Animals · doi:10.3390/ani10071201 · Cited by 4 · see citing works
Increasing Efficacy of Covid-19 Vaccines by Lifestyle Interventions.
Gasmi, A., Mujawdiya, P. K., Noor, S., Piscopo, S., Resimont, S., & Menzel, A. (2022) · PubMed Central · doi:10.22092/ari.2021.356491.1854 · Cited by 4 · see citing works
Brasil, C. L., Gonçalves, V. S., Santos, F. D. S., Rodrigues, P. R. C., Leite, F. P. L., & Pereira, D. I. B. (2024) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2024.110726 · Cited by 4 · see citing works
Can the Therapeutic Spectrum of Probiotics be Extended: Exploring Potential of Gut Microbiome
Rastogi, S., Singh, A., Nandi, A., Gupta, A., Agarwal, J., & Kostova, I. P. (2022) · Recent Advances in Anti-Infective Drug Discovery · doi:10.2174/2772434418666221124124317 · Cited by 4 · see citing works
Vaccinations in preterm infants: Which and when?
Schmitt, C., Goedicke‐Fritz, S., Fortmann, M. I., & Zemlin, M. (2025) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2025.101670 · Cited by 10 · see citing works
Mucosal immunity and vaccine development
Hong, W., Alu, A., Zhang, Z., Zhang, Y. L., He, X., Xu, L., Li, M., He, W., & Wang, J. (2026) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-026-02687-4 · Cited by 3 · see citing works
Çocuklarda Kanıta Dayalı Probiyotik Kullanımı
Kural, B. (2020) · OSMANGAZİ JOURNAL OF MEDICINE · doi:10.20515/otd.681546 · Cited by 3 · see citing works
Zhao, S., Lok, K. Y. W., Sin, Z. Y., Peng, Y., Fan, H. S. L., Nagesh, N., Choi, M. S. L., Kwok, J. Y. Y., Choi, E. P. H., Zhang, X., et al. (2023) · npj Vaccines · doi:10.1038/s41541-023-00745-4 · Cited by 3 · see citing works
Pediococcus pentosaceus MIANGUAN Enhances the Immune Response to Vaccination in Mice
Chen, Y., Cao, Z., Lu, S., Wang, Z., Ma, C., Zhang, G., Chen, M.-S., Yang, J., Ren, Z.-H., & Xu, J.-G. (2024) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-023-10205-z · Cited by 3 · see citing works
Pandya, A., Pulakkat, S., Jadhav, S. A., & Patravale, V. B. (2021) · Springer eBooks · doi:10.1007/978-981-16-5628-6_11 · Cited by 3 · see citing works
Saridag, G., ERDOĞAN, S., Özalp, T., Ural, K., & Erdoğan, H. (2023) · Macedonian Veterinary Review · doi:10.2478/macvetrev-2023-0025 · Cited by 2 · see citing works
İnsan bağırsak mikrobiyomunu COVID-19 için tedavi stratejileriyle ilişkilendiren mekanizmalar
Akın, N., & Özışık, D. (2023) · Uludağ Üniversitesi Ziraat Fakültesi dergisi/Bursa uludağ üniversitesi ziraat fakültesi dergisi · doi:10.20479/bursauludagziraat.1276832 · Cited by 2 · see citing works
Schrock, J., Yan, M., Dolatyabi, S., Patil, V., Yadagiri, G., Renu, S., Ramesh, A., Wood, R., Hanson, J., Yu, Z., et al. (2024) · Current Microbiology · doi:10.1007/s00284-024-03785-8 · Cited by 2 · see citing works
- 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 · 2017: 1
- 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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