Effect of Probiotics and Prebiotics on Immune Response to Influenza Vaccination in Adults: A Systematic Review and Meta-Analysis of Randomized Controlled Trials
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We conducted a meta-analysis to evaluate the effects of probiotics and prebiotics on the immune response to influenza vaccination in adults. We conducted a literature search of Pubmed, Embase, the Cochrane Library, the Cumulative Index to Nursing and Allied Health (CINAHL), Airiti Library, and PerioPath Index to Taiwan Periodical Literature in Taiwan. Databases were searched from inception to July 2017. We used the Cochrane Review risk of bias assessment tool to assess randomized controlled trial (RCT) quality. A total of 20 RCTs comprising 1979 adults were included in our systematic review. Nine RCTs including 623 participants had sufficient data to be pooled in a meta-analysis. Participants who took probiotics or prebiotics showed significant improvements in the H1N1 strain seroprotection rate (with an odds ratio (OR) of 1.83 and a 95% confidence interval (CI) of 1.19–2.82, p = 0.006, I2 = 0%), the H3N2 strain seroprotection rate (OR = 2.85, 95% CI = 1.59–5.10, p < 0.001, I2 = 0%), and the B strain seroconversion rate (OR = 2.11, 95% CI = 1.38–3.21, p < 0.001, I2 = 0%). This meta-analysis suggested that probiotics and prebiotics are effective in elevating immunogenicity by influencing seroconversion and seroprotection rates in adults inoculated with influenza vaccines.
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In a meta-analysis, in adults who received a vaccine to protect against influenza viruses, administration of probiotics was effective.
“Also, in a meta-analysis study, researchers reported that, in adults who received a vaccine to protect against influenza viruses, the administration of probiotics was effective [181].”
From The Potential Impact of Probiotics on Human Health: An Update on Their Health-Promoting Properties (2024) · cites this paper as [181]
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Bias in meta-analysis detected by a simple, graphical test
Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997) · BMJ · doi:10.1136/bmj.315.7109.629 · Cited by 56,722 · see citing works
Meta-analysis in clinical trials
DerSimonian, R., & Laird, N. (1986) · Controlled Clinical Trials · doi:10.1016/0197-2456(86)90046-2 · Cited by 39,552 · see citing works
Quantifying heterogeneity in a meta‐analysis
Higgins, J. P. T., & Thompson, S. G. (2002) · Statistics in Medicine · doi:10.1002/sim.1186 · Cited by 36,763 · see citing works
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gøtzsche, P. C., Ioannidis, J. P. A., Clarke, M., Devereaux, P. J., Kleijnen, J., & Moher, D. (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000100 · Cited by 28,164 · see citing works
Liberati, A., Altman, D. G., Tetzlaff, J., Mulrow, C., Gotzsche, P. C., Ioannidis, J. P. A., Clarke, M., Devereaux, P. J., Kleijnen, J., & Moher, D. (2009) · BMJ · doi:10.1136/bmj.b2700 · Cited by 17,648 · see citing works
Cochrane Handbook for Systematic Reviews of Interventions Version 5.0.1. The Cochrane Collaboration
Higgins, J., Green, S. R., & Higgins, J. (2008) · Cited by 5,544 · see citing works
Hobson, D., Curry, R. L., Beare, A. S., & Ward-Gardner, A. (1972) · Epidemiology and Infection · doi:10.1017/s0022172400022610 · Cited by 1,003 · see citing works
Use of the Inactivated Intranasal Influenza Vaccine and the Risk of Bell's Palsy in Switzerland
Mütsch, M., Zhou, W., Rhodes, P., Bopp, M., Chen, R. T., Linder, T. E., Spyr, C., & Steffen, R. P. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa030595 · Cited by 918 · see citing works
Mechanisms of probiotic actions – A review
Oelschlaeger, T. A. (2009) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2009.08.005 · Cited by 720 · see citing works
Aging of the innate immune system
Shaw, A. C., Joshi, S., Greenwood, H., Panda, A., & Lord, J. M. (2010) · Current Opinion in Immunology · doi:10.1016/j.coi.2010.05.003 · Cited by 647 · see citing works
Gill, H. S., Rutherfurd, K. J., Cross, M. L., & Gopal, P. K. (2001) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/74.6.833 · Cited by 485 · cited 1× · see citing works
“Probiotics induce cellular immunity in phagocyte and NK cells [33,41] and promote IgA secretion into saliva to enhance the vaccine effects [35,42].”
BackgroundSerum Antibody Responses after Intradermal Vaccination against Influenza
Belshe, R. B., Newman, F. K., Cannon, J. C., Duane, C. G., Treanor, J. J., Hoecke, C. V., Howe, B. J., & Dubin, G. O. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa043555 · Cited by 332 · see citing works
Haemagglutination-inhibiting antibody to influenza virus.
de Jong, J. C., Palache, A. M., BEYER, W. E. P., Rimmelzwaan, G. F., Boon, A. C. M., & Osterhaus, A. D. M. E. (2003) · PubMed · Cited by 319 · see citing works
Probiotic Effects on Cold and Influenza-Like Symptom Incidence and Duration in Children
Leyer, G. J., Li, S., Mubasher, M., Reifer, C. J., & Ouwehand, A. C. (2009) · PEDIATRICS · doi:10.1542/peds.2008-2666 · Cited by 305 · see citing works
Nutrition and immunity in the elderly: modification of immune responses with nutritional treatments
Lesourd, B. (1997) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/66.2.478s · Cited by 285 · 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
de Vrese, M., Winkler, P., Rautenberg, P., Harder, T., Noah, C., Laue, C., Ott, S. J., Hampe, J., Schreiber, S., Heller, K. J., et al. (2005) · Clinical Nutrition · doi:10.1016/j.clnu.2005.02.006 · Cited by 252 · see citing works
Prebiotics, probiotics, synbiotics, and the immune system: experimental data and clinical evidence
Frei, R., Akdis, M., & O’Mahony, L. (2015) · Current Opinion in Gastroenterology · doi:10.1097/mog.0000000000000151 · Cited by 240 · see citing works
Sheih, Y.-H., Chiang, B., Wang, L.-H., Liao, C.-K., & Gill, H. S. (2001) · Journal of the American College of Nutrition · doi:10.1080/07315724.2001.10719027 · Cited by 237 · see citing works
Vaccination in the elderly: an immunological perspective
Chen, W. H., Kozlovsky, B. F., Effros, R. B., Grubeck‐Loebenstein, B., Edelman, R., & Sztein, M. B. (2009) · Trends in Immunology · doi:10.1016/j.it.2009.05.002 · Cited by 228 · 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
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
Nutrition and immunity in the elderly
Lesourd, B., & Mazari, L. (1999) · Proceedings of The Nutrition Society · doi:10.1017/s0029665199000907 · Cited by 154 · see citing works
Vos, A. P., Haarman, M., VanGinkel, J. H., Knol, J., Garssen, J., Stahl, B., Boehm, G., & M’Rabet, L. (2007) · Pediatric Allergy and Immunology · doi:10.1111/j.1399-3038.2007.00515.x · Cited by 112 · 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
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
Effects of prebiotics on the immune response to vaccination in the elderly
Bunout, D., Hirsch, S., de la Maza, M., Munoz, C., Haschke, F., Steenhout, P., Klassen, P., Barrera, G., Gattas, V, & Petermann, M. (2002) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607102026006372 · Cited by 107 · see citing works
Growth of enterobacteria on fructo‐oligosaccharides
Hartemink, R., Laere, K. M. J. V., & ROMBOUTS, F. M. (1997) · Journal of Applied Microbiology · doi:10.1046/j.1365-2672.1997.00239.x · Cited by 107 · 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
Kotani, Y., Shinkai, S., OKAMATSU, H., Toba, M., Ogawa, K., Yoshida, H., Fukaya, T., Fujiwara, Y., Chaves, P. H. M., Kakumoto, K., et al. (2010) · Immunity & Ageing · doi:10.1186/1742-4933-7-11 · Cited by 102 · see citing works
Akatsu, H., Iwabuchi, N., Xiao, J., Matsuyama, Z., Kurihara, R., Okuda, K., Yamamoto, T., & Maruyama, M. (2012) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607112467819 · Cited by 94 · see citing works
Immunosenescence: Implications for vaccination programmes in adults
Lang, P. O., Govind, S., Michel, J. P., Aspinall, R., & Mitchell, W. A. (2011) · Maturitas · doi:10.1016/j.maturitas.2011.01.011 · Cited by 76 · 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
Langkamp‐Henken, B., Bender, B. S., Gardner, E. M., Herrlinger‐Garcia, K. A., Kelley, M. J., Murasko, D. M., Schaller, J. P., Stechmiller, J. K., Thomas, D. J., & Wood, S. M. (2003) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2004.52003.x · Cited by 69 · see citing works
Nutritional Formula Improved Immune Profiles of Seniors Living in Nursing Homes
Langkamp‐Henken, B., Wood, S. M., Herrlinger‐Garcia, K. A., Thomas, D. J., Stechmiller, J. K., Bender, B. S., Gardner, E. M., DeMichele, S. J., Schaller, J. P., & Murasko, D. M. (2006) · Journal of the American Geriatrics Society · doi:10.1111/j.1532-5415.2006.00982.x · Cited by 57 · see citing works
Akatsu, H., Nagafuchi, S., Kurihara, R., Okuda, K., Kanesaka, T., Ogawa, N., Kanematsu, T., Takasugi, S., Yamaji, T., Takami, M., et al. (2015) · Geriatrics and gerontology international/Geriatrics & gerontology international · doi:10.1111/ggi.12454 · Cited by 49 · see citing works
Immune Response to Influenza Vaccination in an Elderly Population
Brydak, L. B., Machała, M., Myśliwska, J., Myśliwski, A., & Trzonkowski, P. (2003) · Journal of Clinical Immunology · doi:10.1023/a:1023314029788 · Cited by 46 · see citing works
Przemska-Kosicka, A., Childs, C. E., Maidens, C., Dong, H., Todd, S., Gosney, M. A., Tuohy, K. M., & Yaqoob, P. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00591 · Cited by 43 · 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
Ageing, immunity and influenza: a role for probiotics?
Yaqoob, P. (2013) · Proceedings of The Nutrition Society · doi:10.1017/s0029665113003777 · Cited by 40 · see citing works
Enani, S. M., Przemska-Kosicka, A., Childs, C. E., Maidens, C. M., Dong, H., Conterno, L., Tuohy, K. M., Todd, S., Gosney, M., & Yaqoob, P. (2017) · Clinical Nutrition · doi:10.1016/j.clnu.2017.01.011 · Cited by 38 · see citing works
Lomax, A. R., Cheung, L. V. Y., Noakes, P. S., Miles, E. A., & Calder, P. C. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00490 · Cited by 32 · 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
Conge, G., Gouache, P., Desormeau-Bedot, J.-P., Loisillier, F., & Lemonnier, D. (1980) · annales de biologie animale biochimie biophysique · doi:10.1051/rnd:19800603 · Cited by 27 · see citing works
Use of probiotic bacteria as an adjuvant for an influenza vaccine.
French, P. W., & Penny, R. (2009) · International Journal of Probiotics and Prebiotics · Cited by 14 · see citing works
[Comparative effects of a diet enriched in live or heated yogurt on the immune system of the mouse].
Conge, G., Gouache, P., Desormeau-Bedot, J.-P., Loisillier, F., & Lemonnier, D. (1980) · PubMed · Cited by 7 · see citing works
Flagged first, then by citations
2 of the 51 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Nutrition, immunity and COVID-19
Calder, P. C. (2020) · BMJ Nutrition Prevention & Health · doi:10.1136/bmjnph-2020-000085 · Cited by 587 · see citing works
Wiertsema, S. P., van Bergenhenegouwen, J., Garssen, J., & Knippels, L. M. J. (2021) · Nutrients · doi:10.3390/nu13030886 · Cited by 558 · 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
The Gut Microbiota and Unhealthy Aging: Disentangling Cause from Consequence
DeJong, E. N., Surette, M. G., & Bowdish, D. M. E. (2020) · Cell Host & Microbe · doi:10.1016/j.chom.2020.07.013 · Cited by 370 · see citing works
Probiotics in Medicine: A Long Debate
Stavropoulou, E., & Bezirtzoglou, E. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.02192 · Cited by 297 · see citing works
Calder, P. C., Ortega, E. F., Meydani, S. N., Adkins, Y. C., Stephensen, C. B., Thompson, B., & Zwickey, H. L. (2022) · Advances in Nutrition · doi:10.1093/advances/nmac052 · Cited by 136 · see citing works
Gut microbiota and old age: Modulating factors and interventions for healthy longevity
Coman, V., & Vodnar, D. C. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.111095 · Cited by 124 · see citing works
Nutrition and immunity: lessons for COVID-19
Calder, P. C. (2021) · Nutrition and Diabetes · doi:10.1038/s41387-021-00165-0 · Cited by 113 · 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
Self-citationNutrition and immunity: lessons for COVID-19
Calder, P. C. (2021) · European Journal of Clinical Nutrition · doi:10.1038/s41430-021-00949-8 · Cited by 93 · see citing works
Lee, M.-D., Lin, C., Lei, W., Chang, H.-Y., Lee, H., Yeung, C., Chiu, N., Chi, H., Liu, J., Hsu, R., et al. (2018) · Nutrients · doi:10.3390/nu10040409 · Cited by 89 · see citing works
Self-citationKefir: A protective dietary supplementation against viral infection
Hamida, R. S., Shami, A., Ali, M. A., Almohawes, Z. N., Mohammed, A. E., & Bin-Meferij, M. M. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110974 · Cited by 85 · see citing works
Adjuvant Probiotics and the Intestinal Microbiome: Enhancing Vaccines and Immunotherapy Outcomes
Vitetta, L., Saltzman, E., Thomsen, M., Nikov, T., & Hall, S. (2017) · Vaccines · doi:10.3390/vaccines5040050 · Cited by 83 · see citing works
Healthy ageing: the natural consequences of good nutrition—a conference report
Marsman, D. S., Belsky, D. W., Gregori, D., Johnson, M. A., Dog, T. L., Meydani, S. N., Pigat, S., Sadana, R., Shao, A., & Griffiths, J. C. (2018) · European Journal of Nutrition · doi:10.1007/s00394-018-1723-0 · Cited by 81 · see citing works
Morais, A. H. D. A., Passos, T. S., Maciel, B. L. L., & da Silva-Maia, J. K. (2020) · Nutrients · doi:10.3390/nu12061737 · Cited by 77 · see citing works
Probiotics and prebiotics in clinical tests: an update
Brüssow, H. (2019) · F1000Research · doi:10.12688/f1000research.19043.1 · Cited by 78 · see citing works
Current Progress and Future Perspectives on the Use of Bacillus clausii
Ghelardi, E., y Abreu, A. T. A., Marzet, C. B., Calatayud, G. Á., Perez, M. I., & Castro, A. P. M. (2022) · Microorganisms · doi:10.3390/microorganisms10061246 · Cited by 79 · see citing works
Aging Fits the Disease Criteria of the International Classification of Diseases
Khaltourina, D. A., Matveyev, Y., Alekseev, A., Cortese, F., & Ioviţă, A. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111230 · Cited by 71 · see citing works
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
Microbiota and COVID-19: Long-term and complex influencing factors
Gang, J., Wang, H., Xue, X., & Zhang, S. J. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.963488 · Cited by 61 · see citing works
Ingestion, Immunity, and Infection: Nutrition and Viral Respiratory Tract Infections
Govers, C., Calder, P. C., Savelkoul, H. F. J., Albers, R., & van Neerven, R. J. J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.841532 · Cited by 66 · see citing works
Batista, K. S., de Albuquerque, J. G., de Vasconcelos, M. H. A., Bezerra, M. L. R., Barbalho, M. B. D. S., Pinheiro, R. O., & Aquino, J. D. S. (2021) · Nutrition Research Reviews · doi:10.1017/s0954422421000317 · Cited by 54 · see citing works
The emerging role of probiotics as a mitigation strategy against coronavirus disease 2019 (COVID-19)
Mirzaei, R., Attar, A., Papizadeh, S., Jeda, A. S., Hosseini‐Fard, S. R., Jamasbi, E., Kazemi, S., Amerkani, S., Talei, G. R., Moradi, P., et al. (2021) · Archives of Virology · doi:10.1007/s00705-021-05036-8 · Cited by 53 · see citing works
Could nutritional supplements act as therapeutic adjuvants in COVID-19?
Costagliola, G., Spada, E., Comberiati, P., & Peroni, D. G. (2021) · The Italian Journal of Pediatrics/Italian journal of pediatrics · doi:10.1186/s13052-021-00990-0 · Cited by 49 · see citing works
Are Nutraceuticals Effective in COVID-19 and Post-COVID Prevention and Treatment?
Catalano, A. A., Iacopetta, D., Ceramella, J., Maio, A. C. D., Basile, G., Giuzio, F., Bonomo, M. G., Aquaro, S., Walsh, T. J., Sinicropi, M. S., et al. (2022) · Foods · doi:10.3390/foods11182884 · Cited by 47 · see citing works
Probiotics and probiotic-based vaccines: A novel approach for improving vaccine efficacy
Kazemifard, N., Dehkohneh, A., & Ghavami, S. B. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.940454 · Cited by 47 · see citing works
Portella, C. F. S., Ghelman, R., Abdala, C. V. M., & Schveitzer, M. C. (2020) · Integrative Medicine Research · doi:10.1016/j.imr.2020.100473 · Cited by 42 · see citing works
The Potential Role of Probiotics in Protection against Influenza a Virus Infection in Mice
Lu, W., Fang, Z., Liu, X., Li, L., Zhang, P., Zhao, J., Zhang, H., & Chen, W. (2021) · Foods · doi:10.3390/foods10040902 · Cited by 44 · see citing works
Singh, S. P., Kola, P., Kaur, D., Singla, G., Mishra, V., Panesar, P. S., Mallikarjunan, K., & Krishania, M. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.679312 · Cited by 41 · see citing works
Influence of human gut microbiome on the healthy and the neurodegenerative aging
Borrego-Ruiz, A., & Borrego, J. J. (2024) · Experimental Gerontology · doi:10.1016/j.exger.2024.112497 · Cited by 42 · see citing works
From the Role of Microbiota in Gut‐Lung Axis to SARS‐CoV‐2 Pathogenesis
Badi, S. A., Tarashi, S., Fateh, A., Rohani, P., Masotti, A., & Siadat, S. D. (2021) · Mediators of Inflammation · doi:10.1155/2021/6611222 · Cited by 37 · see citing works
Kayasaki, F., Okagawa, T., Konnai, S., Kohara, J., Sajiki, Y., Watari, K., Ganbaatar, O., Goto, S., Nakamura, H., Shimakura, H., et al. (2021) · Veterinary Microbiology · doi:10.1016/j.vetmic.2020.108976 · 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
The direct and indirect effects of bioactive compounds against coronavirus
Tomaş, M., Çapanoğlu, E., Bahrami, A., Hosseini, H., Akbari‐Alavijeh, S., Shaddel, R., Rehman, A., Rezaei, A., Rashidinejad, A., Garavand, F., et al. (2021) · Food Frontiers · doi:10.1002/fft2.119 · Cited by 36 · 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
Akatsu, H. (2021) · Vaccines · doi:10.3390/vaccines9020136 · Cited by 36 · see citing works
Kageyama, Y., Nishizaki, Y., Aida, K., Yayama, K., Ebisui, T., Akiyama, T., & Nakamura, T. (2021) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2021.10942 · Cited by 37 · see citing works
Ducloux, D., Legendre, M., Bamoulid, J., Saas, P., Courivaud, C., & Crépin, T. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.720402 · Cited by 34 · see citing works
The intestinal microbiota and improving the efficacy of COVID-19 vaccinations
Chen, J., Vitetta, L., Henson, J. D., & Hall, S. (2021) · Journal of Functional Foods · doi:10.1016/j.jff.2021.104850 · Cited by 32 · see citing works
Sanders, M. E., Goh, Y. J., & Klaenhammer, T. R. (2019) · ASM Press eBooks · doi:10.1128/9781555819972.ch32 · Cited by 32 · 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
Shenoy, S. (2021) · Inflammation Research · doi:10.1007/s00011-021-01510-w · Cited by 31 · see citing works
Wischmeyer, P. E., Tang, H., Ren, Y., Bohannon, L. M., Jiang, D., Bergens, M. A., Ramirez, Z. E., Andermann, T. M., Messina, J. A., Sung, J., et al. (2023) · Clinical Nutrition · doi:10.1016/j.clnu.2023.11.043 · Cited by 30 · 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
Mgbodile, F. C., & Nwagu, T. N. (2023) · Biotechnology Reports · doi:10.1016/j.btre.2023.e00795 · Cited by 32 · see citing works
Wang, Y.-H., Limaye, A., Liu, J., & Wu, T.-N. (2022) · Journal of Traditional and Complementary Medicine · doi:10.1016/j.jtcme.2022.08.004 · Cited by 30 · see citing works
Lifelong partners: Gut microbiota-immune cell interactions from infancy to old age
Brown, J. A., Bashir, H., & Zeng, M. Y. (2025) · Mucosal Immunology · doi:10.1016/j.mucimm.2025.01.006 · Cited by 30 · see citing works
Effects of diets, foods and nutrients on immunity: Implications for COVID‐19?
Lockyer, S. (2020) · Nutrition Bulletin · doi:10.1111/nbu.12470 · Cited by 27 · see citing works
Lemme‐Dumit, J. M., Cazorla, S. I., Perdigón, G., & Maldonado-Galdeano, C. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.660854 · Cited by 25 · see citing works
Patient Nutrition and Probiotic Therapy in COVID-19: What Do We Know in 2021?
Hawryłkowicz, V., Lietz–Kijak, D., Kaźmierczak-Siedlecka, K., Sołek-Pastuszka, J., Stachowska, L., Folwarski, M., Parczewski, M., & Stachowska, E. (2021) · Nutrients · doi:10.3390/nu13103385 · Cited by 25 · see citing works
Karl, J. P. (2020) · Military Medicine · doi:10.1093/milmed/usaa261 · Cited by 23 · see citing works
Gastrointestinal Disease and COVID-19: A Review of Current Evidence
Chen, F., Dai, Z., Huang, C., Chen, H., Wang, X., & Li, X. (2021) · Digestive Diseases · doi:10.1159/000519412 · Cited by 23 · see citing works
Sandionigi, A., Giani, A. D., Tursi, F., Michelotti, A., Cestone, E., Giardina, S., Zampolli, J., & Gennaro, P. D. (2022) · BioMed Research International · doi:10.1155/2022/3860896 · Cited by 24 · see citing works
Microbiota and the Response to Vaccines Against Respiratory Virus
Gonçalves, J. I. B., Borges, T. J., & de Souza, A. P. D. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.889945 · 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
Wischmeyer, P. E., Tang, H., Ren, Y., Bohannon, L. M., Ramirez, Z. E., Andermann, T. M., Messina, J. A., Sung, J., Jensen, D., Jung, S., et al. (2022) · medRxiv · doi:10.1101/2022.01.04.21268275 · 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
A Rapid Advice Guideline for the Prevention of Novel Coronavirus Through Nutritional Intervention
Budhwar, S., Sethi, K., & Chakraborty, M. (2020) · Current Nutrition Reports · doi:10.1007/s13668-020-00325-1 · Cited by 23 · see citing works
Probiotics in the Management of Mental and Gastrointestinal Post-COVID Symptomes
Łoniewski, I., Skonieczna‐Żydecka, K., Sołek-Pastuszka, J., & Marlicz, W. M. (2022) · Journal of Clinical Medicine · doi:10.3390/jcm11175155 · Cited by 22 · see citing works
Galacto-Oligosaccharides and the Elderly Gut: Implications for Immune Restoration and Health
Hu, Y., Aljumaah, M. R., & Azcárate-Peril, M. A. (2024) · Advances in Nutrition · doi:10.1016/j.advnut.2024.100263 · Cited by 23 · see citing works
Gastrointestinal Microbiome and Multiple Health Outcomes: Umbrella Review
Chang, C., Yuan, X., Zhang, X., Chen, X., & Li, K. (2022) · Nutrients · doi:10.3390/nu14183726 · Cited by 22 · 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
Vaccines, Microbiota and Immunonutrition: Food for Thought
Renzo, L. D., Franza, L., Monsignore, D., Esposito, E., Rio, P., Gasbarrini, A., Gambassi, G., Cianci, R., & LORENZO, A. D. (2022) · Vaccines · doi:10.3390/vaccines10020294 · Cited by 17 · see citing works
Impact of the intestinal environment on the immune responses to vaccination.
Hosomi, K., & Kunisawa, J. (2020) · Vaccine · doi:10.1016/j.vaccine.2020.08.079 · Cited by 17 · see citing works
Picó-Monllor, J. A., Ruzafa-Costas, B., Núñez-Delegido, E., Sánchez-Pellicer, P., Peris-Berraco, J., & Navarro‐López, V. (2021) · Nutrients · doi:10.3390/nu13124419 · Cited by 18 · see citing works
Omer, A. K., Khorshidi, S., Mortazavi, N., & Rahman, H. S. (2022) · International Journal of General Medicine · doi:10.2147/ijgm.s361001 · Cited by 17 · see citing works
Inserra, F., Tajer, C. D., Antonietti, L., Mariani, J. A., Ferder, L., & Manucha, W. A. (2021) · Vaccine · doi:10.1016/j.vaccine.2021.07.031 · Cited by 16 · see citing works
Effect of probiotics as an immune modulator for the management of COVID-19
Ray, M., Manjunath, A., & Halami, P. M. (2023) · Archives of Microbiology · doi:10.1007/s00203-023-03504-0 · Cited by 16 · see citing works
Foods to deliver immune-supporting nutrients
Calder, P. C. (2021) · Current Opinion in Food Science · doi:10.1016/j.cofs.2021.12.006 · Cited by 16 · see citing works
Development and management of gastrointestinal symptoms in long-term COVID-19
He, K.-Y., Lei, X., Zhang, L., Wu, D., Li, J., Lu, L., Laila, U. E., Cui, C.-Y., Xu, Z.-X., & Jian, Y. (2023) · Frontiers in Microbiology · doi:10.3389/fmicb.2023.1278479 · Cited by 15 · see citing works
Mashhadi, N. S., Kazemi, M., Saadat, S., & Moradi, S. (2021) · Expert Review of Respiratory Medicine · doi:10.1080/17476348.2021.1918546 · Cited by 15 · see citing works
Probiotics for the Management of Infectious Diseases: Reviewing the State of the Art
Wiegers, C., van de Burgwal, L., & Larsen, O. F. A. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.877142 · Cited by 15 · 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
Tunc, H. A., Childs, C. E., Swann, J. R., & Calder, P. C. (2024) · Age and Ageing · doi:10.1093/ageing/afae033 · 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
Nutrition and immunity: lessons from coronavirus disease-2019
Calder, P. C. (2023) · Proceedings of The Nutrition Society · doi:10.1017/s0029665123004792 · Cited by 12 · see citing works
The effect of partially hydrolyzed guar gum on preventing influenza infection
Takahashi, C., & Kozawa, M. (2021) · Clinical Nutrition ESPEN · doi:10.1016/j.clnesp.2020.11.030 · Cited by 11 · see citing works
Gut microbiota on human health and disease
Duttaroy, A. K. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-822405-2.00006-2 · Cited by 12 · 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
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
Immunonutrition and SARS-CoV-2 Infection in Children with Obesity
D’Auria, E., Calcaterra, V., Verduci, E., Ghezzi, M., Lamberti, R., Vizzuso, S., Baldassarre, P., Pendezza, E., Perico, V., Bosetti, A., et al. (2022) · Nutrients · doi:10.3390/nu14091701 · Cited by 10 · see citing works
Potential of Synbiotics and Probiotics as Chemopreventive Agent
Chin, K. W., Khoo, S. C., Paul, R. P. M., Luang‐In, V., Lam, S. D., & Ling, N. (2024) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-024-10299-z · Cited by 9 · see citing works
Microbiota and probiotics: chances and challenges – a symposium report
Ruxton, C. H. S., Kajita, C., Rocca, P., & Pot, B. (2023) · Gut Microbiome · doi:10.1017/gmb.2023.4 · Cited by 9 · see citing works
Vicente‐Gil, S., Simón, R., Mérida, S. N., Nuñez-Ortiz, N., Fouz, B., Serra, C. R., Ordás, M. C., Abós, B., Herranz-Jusdado, J. G., Morel, E., et al. (2025) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2025.110335 · Cited by 8 · see citing works
Deciphering the Potential of Probiotics in Vaccines
Xu, C., Aqib, A. I., Fatima, M., Muneer, S., Zaheer, T., Peng, S., Ibrahim, E. H., & Li, K. (2024) · Vaccines · doi:10.3390/vaccines12070711 · 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
Recombinant Probiotic Preparations: Current State, Development and Application Prospects
Khablenko, A., Danylenko, S., Yalovenko, O., Дуган, О. М., Potemska, O., & Prykhodko, D. (2023) · Innovative Biosystems and Bioengineering · doi:10.20535/ibb.2022.6.3-4.268349 · 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
Bogard, G., Makki, K., Rodrigues, P. B., Tan, J., Molendi‐Coste, O., Barthelemy, J., Descat, A., Bouilloux, F., Lecœur, C., Grangette, C., et al. (2025) · Scientific Reports · doi:10.1038/s41598-025-21363-1 · Cited by 5 · see citing works
Chen, L., Pan, C., Huang, S., Chan, C.-H., & Huang, H.-Y. (2021) · Scientific Reports · doi:10.1038/s41598-021-98791-2 · Cited by 5 · see citing works
Immunomodulatory Effects of Probiotic Lactobacillus casei On GM-CSF-adjuvanted Influenza Dna Vaccine
Mahooti, M., Abdolalipour, E., Farahmand, B., Shirian, S., & Ghaemi, A. (2022) · Future Virology · doi:10.2217/fvl-2021-0327 · Cited by 5 · see citing works
Oligosaccharide equine feed supplement, Immulix, has minor impact on vaccine responses in mice
Henriksen, I. W., Castro-Mejía, J. L., Mentzel, C. M. J., Lindenberg, F., & Hansen, A. K. (2022) · Scientific Reports · doi:10.1038/s41598-021-04132-8 · Cited by 5 · see citing works
Human microbiome in post-acute COVID-19 syndrome (PACS)
Fallah, A., Sedighian, H., Kachuei, R., & Fooladi, A. A. I. (2024) · Current Research in Microbial Sciences · doi:10.1016/j.crmicr.2024.100324 · 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
Nutraceuticals: Health effects and clinical applications
Chen, O., & Mah, E. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-821848-8.00043-3 · 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
Baştürk, A., Ceylan, M. M., Alaca, K., & Yıldız, G. (2021) · European Journal of Nutrition & Food Safety · doi:10.9734/ejnfs/2021/v13i1230468 · Cited by 3 · see citing works
Dhakad, P. K., Mishra, R., & Mishra, I. (2023) · Natural Resources for Human Health · doi:10.53365/nrfhh/175070 · 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
Maulana, S., Platini, H., Musthofa, F., Andriani, D., Purba, F. D., Iskandarsyah, A., & Hinduan, Z. R. (2021) · Kumawula Jurnal Pengabdian Kepada Masyarakat · doi:10.24198/kumawula.v4i3.33744 · Cited by 3 · see citing works
- Authors
- Lei, W.-T., Shih, P.-C., Liu, S.-J., Lin, C.-Y., & Yeh, T.-L.
- Affiliations
- Mackay Memorial Hospital (TW)
- Corresponding author
- Yeh, Tzu-Lin
- Venue
- Nutrients
- Publisher
- MDPI AG
- Published
- 2017-10-27
- Volume
- 9
- Issue
- 11
- Pages
- 1175
- ISSN
- 2072-6643 (ISSN-L)
- PMC
- PMC5707647
- OpenAlex
- W2765429016
- Cited by
- 134
- References
- 51
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 16 · 2023: 10 · 2022: 27 · 2021: 38 · 2020: 18 · 2019: 7 · 2018: 5 · 2017: 1
- FWCI
- 0.92
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Nutrients (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Mackay Memorial Hospital
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Health Sciences › Nursing › Nutrition and Dietetics › Microbial Metabolites in Food Biotechnology
- Keywords
- probiotics, prebiotics, influenza vaccination, vaccine immunogenicity, seroprotection rate, seroconversion, H1N1, H3N2, adults, gut microbiota
- MeSH terms
- Seroconversion, Adult, Aged, Aged, 80 and over, Female, Humans, Immunity, Influenza, Human, Influenza Vaccines, Male, Influenza B virus, Vaccination, Probiotics, Influenza A Virus, H1N1 Subtype, Influenza A Virus, H3N2 Subtype, Prebiotics
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