The influence of probiotics on vaccine responses – A systematic review

Vaccine

Volumn 36, Issue 2, 2018, Pages 207-213

  Zimmermann, Petra ^a   Curtis, Nigel ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Antibodies; Bifidobacteria; Immunoglobulin; Lactobacillus; Microbiome; Microbiota; Titer

Indexed keywords

BACTERIAL VACCINE; CHICKENPOX MEASLES MUMPS RUBELLA VACCINE; CHOLERA VACCINE; DIPHTHERIA PERTUSSIS POLIOMYELITIS TETANUS HAEMOPHILUS INFLUENZAE TYPE B HEPATITIS B VACCINE; DIPHTHERIA PERTUSSIS TETANUS HAEMOPHILUS INFLUENZAE TYPE B VACCINE; DIPHTHERIA PERTUSSIS TETANUS VACCINE; HAEMOPHILUS INFLUENZAE TYPE B VACCINE; HEPATITIS A VACCINE; HEPATITIS B VACCINE; INFLUENZA VACCINE; PERTUSSIS VACCINE; PNEUMOCOCCUS VACCINE; POLIOMYELITIS VACCINE; PROBIOTIC AGENT; RABIES VACCINE; ROTAVIRUS VACCINE; TETANUS TOXOID; TYPHOID VACCINE; VACCINE; PLACEBO;

BACTERIAL STRAIN; CLINICAL EFFECTIVENESS; DOSE RESPONSE; HUMAN; HUMORAL IMMUNITY; INFLUENZA VACCINATION; PREGNANCY; PRIORITY JOURNAL; PROTECTION; REVIEW; SYSTEMATIC REVIEW; IMMUNOLOGY; RANDOMIZED CONTROLLED TRIAL (TOPIC);

HUMANS; IMMUNITY, HUMORAL; PLACEBOS; PROBIOTICS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; VACCINES;

EID: 85029479568     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2017.08.069     Document Type: Review

References (60)

1. Lalwani, S., Chatterjee, S., Chhatwal, J., Simon, A., Ravula, S., Francois, N., et al. Randomized, open-label study of the impact of age on booster responses to the 10-valent pneumococcal nontypeable Haemophilus influenzae protein D conjugate vaccine in children in India. Clin Vaccine Immunol: CVI 21 (2014), 1292–1300.
2. Martins, C., Garly, M.L., Bale, C., Rodrigues, A., Njie-Jobe, J., Benn, C.S., et al. Measles virus antibody responses in children randomly assigned to receive standard-titer edmonston-zagreb measles vaccine at 4.5 and 9 months of age, 9 months of age, or 9 and 18 months of age. J Infect Dis 210 (2014), 693–700.
3. Simondon, F., Preziosi, M.P., Pinchinat, S., Yam, A., Chabirand, L., Wassilak, S., et al. Randomised study of the possible adjuvant effect of BCG vaccine on the immunogenicity of diphtheria-tetanus-acellular pertussis vaccine in Senegalese infants. Europ J Clin Microbiol Infect Dis: Off Publicat Europ Soc Clin Microbiol 18 (1999), 23–29.
4. Klein, S.L., Flanagan, K.L., Sex differences in immune responses. Nature reviews Immunology. 16 (2016), 626–638.
5. Posteraro, B., Pastorino, R., Di Giannantonio, P., Ianuale, C., Amore, R., Ricciardi, W., et al. The link between genetic variation and variability in vaccine responses: systematic review and meta-analyses. Vaccine 32 (2014), 1661–1669.
6. Ovsyannikova, I.G., Dhiman, N., Jacobson, R.M., Poland, G.A., Human leukocyte antigen polymorphisms: variable humoral immune responses to viral vaccines. Expert Review Vaccines 5 (2006), 33–43.
7. Newport, M.J., Goetghebuer, T., Weiss, H.A., Whittle, H., Siegrist, C.A., Marchant, A., Genetic regulation of immune responses to vaccines in early life. Genes Immun 5 (2004), 122–129.
8. Park, D.E., Johnson, T.S., Nonyane, B.A., Chandir, S., Conklin, L., Fleming-Dutra, K.E., et al. The differential impact of coadministered vaccines, geographic region, vaccine product and other covariates on pneumococcal conjugate vaccine immunogenicity. Pediatr Infect Dis J 33:Suppl 2 (2014), S130–S139.
9. Long, J.E., Drayson, M.T., Taylor, A.E., Toellner, K.M., Lord, J.M., Phillips, A.C., Morning vaccination enhances antibody response over afternoon vaccination: a cluster-randomised trial. Vaccine 34 (2016), 2679–2685.
10. Nascimento Silva, J.R., Camacho, L.A., Siqueira, M.M., Freire Mde, S., Castro, Y.P., Maia Mde, L., et al. Mutual interference on the immune response to yellow fever vaccine and a combined vaccine against measles, mumps and rubella. Vaccine 29 (2011), 6327–6334.
11. Mullooly, J., Black, S., Simultaneous administration of varicella vaccine and other recommended childhood vaccines–United States, 1995–1999. MMWR Morbidity Mortal Week Rep 50 (2001), 1058–1061.
12. Marchesi, J.R., Adams, D.H., Fava, F., Hermes, G.D., Hirschfield, G.M., Hold, G., et al. The gut microbiota and host health: a new clinical frontier. Gut. 65 (2016), 330–339.
13. Zeevi, D., Korem, T., Segal, E., Talking about cross-talk: the immune system and the microbiome. Genome Biol, 17, 2016, 50.
14. Harris, V.C., Armah, G., Fuentes, S., Korpela, K.E., Parashar, U., Victor, J.C., et al. The infant gut microbiome correlates significantly with rotavirus vaccine response in rural Ghana. J Infect Dis, 2016.
15. Huda, M.N., Lewis, Z., Kalanetra, K.M., Rashid, M., Ahmad, S.M., Raqib, R., et al. Stool microbiota and vaccine responses of infants. Pediatrics 134 (2014), e362–e372.
16. Eloe-Fadrosh, E.A., McArthur, M.A., Seekatz, A.M., Drabek, E.F., Rasko, D.A., Sztein, M.B., et al. Impact of oral typhoid vaccination on the human gut microbiota and correlations with S. Typhi-specific Immunol Res PloS one, 8, 2013, e62026.
17. Lagos, R., Fasano, A., Wasserman, S.S., Prado, V., San Martin, O., Abrego, P., et al. Effect of small bowel bacterial overgrowth on the immunogenicity of single-dose live oral cholera vaccine CVD 103-HgR. J Infect Dis 180 (1999), 1709–1712.
18. Mullie, C., Yazourh, A., Thibault, H., Odou, M.F., Singer, E., Kalach, N., et al. Increased poliovirus-specific intestinal antibody response coincides with promotion of Bifidobacterium longum-infantis and Bifidobacterium breve in infants: a randomized, double-blind, placebo-controlled trial. Pediat Res 56 (2004), 791–795.
19. Hill, C., Guarner, F., Reid, G., Gibson, G.R., Merenstein, D.J., Pot, B., et al. Expert consensus document. the international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat RevGastroenterol Hepatol 11 (2014), 506–514.
20. Gill H, Prasad J. Probiotics, immunomodulation, and health benefits. Advances in Experimental Medicine & Biology.606:423-54.
21. Nova E, Warnberg J, Gomez-Martinez S, Diaz LE, Romeo J, Marcos A. Immunomodulatory effects of probiotics in different stages of life. British Journal of Nutrition.98 Suppl 1:S90-5.
22. Szajewska, H., Guarino, A., Hojsak, I., Indrio, F., Kolacek, S., Shamir, R., et al. Use of probiotics for management of acute gastroenteritis: a position paper by the ESPGHAN Working Group for Probiotics and Prebiotics. J Pediat Gastroenterol Nutrit 58 (2014), 531–539.
23. Guarino, A., Ashkenazi, S., Gendrel, D., Lo Vecchio, A., Shamir, R., Szajewska, H., European society for pediatric gastroenterology, hepatology, and nutrition/european society for pediatric infectious diseases evidence-based guidelines for the management of acute gastroenteritis in children in europe: update 2014. J Pediat Gastroenterol Nutrit 59 (2014), 132–152.
24. Goldenberg, J.Z., Lytvyn, L., Steurich, J., Parkin, P., Mahant, S., Johnston, B.C., Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database System Rev, 2015, Cd004827.
25. Hatakka, K., Savilahti, E., Ponka, A., Meurman, J.H., Poussa, T., Nase, L., et al. Effect of long term consumption of probiotic milk on infections in children attending day care centres: double blind, randomised trial. BMJ (Clinical research ed), 322, 2001, 1327.
26. Liu, S., Hu, P., Du, X., Zhou, T., Pei, X., Lactobacillus rhamnosus GG supplementation for preventing respiratory infections in children: a meta-analysis of randomized, placebo-controlled trials. Indian pediatrics 50 (2013), 377–381.
27. Gutierrez-Castrellon, P., Lopez-Velazquez, G., Diaz-Garcia, L., Jimenez-Gutierrez, C., Mancilla-Ramirez, J., Estevez-Jimenez, J., et al. Diarrhea in preschool children and Lactobacillus reuteri: a randomized controlled trial. Pediatrics 133 (2014), e904–e909.
28. Fiocchi, A., Pawankar, R., Cuello-Garcia, C., Ahn, K., Al-Hammadi, S., Agarwal, A., et al. World allergy organization-mcmaster university guidelines for allergic disease prevention (GLAD-P): probiotics. World Allergy Organization J, 8, 2015, 4.
29. Cuello-Garcia, C.A., Brozek, J.L., Fiocchi, A., Pawankar, R., Yepes-Nunez, J.J., Terracciano, L., et al. Probiotics for the prevention of allergy: A systematic review and meta-analysis of randomized controlled trials. J Allergy Clin Immunol 136 (2015), 952–961.
30. Wu, B.B., Yang, Y., Xu, X., Wang, W.P., Effects of Bifidobacterium supplementation on intestinal microbiota composition and the immune response in healthy infants. World J Pediat: WJP 12 (2016), 177–182.
31. Soh, S.E., Ong, D.Q., Gerez, I., Zhang, X., Chollate, P., Shek, L.P., et al. Effect of probiotic supplementation in the first 6 months of life on specific antibody responses to infant Hepatitis B vaccination. Vaccine 28 (2010), 2577–2579.
32. Taylor, A.L., Hale, J., Wiltschut, J., Lehmann, H., Dunstan, J.A., Prescott, S.L., Effects of probiotic supplementation for the first 6 months of life on allergen- and vaccine-specific immune responses. Clin Exp Allergy: J British Soc Allergy Clin Immunol 36 (2006), 1227–1235.
33. Kukkonen, K., Nieminen, T., Poussa, T., Savilahti, E., Kuitunen, M., Effect of probiotics on vaccine antibody responses in infancy–a randomized placebo-controlled double-blind trial. Pediatr Allergy Immunol 17 (2006), 416–421.
34. Youngster, I., Kozer, E., Lazarovitch, Z., Broide, E., Goldman, M., Probiotics and the immunological response to infant vaccinations: a prospective, placebo controlled pilot study. Arch Dis Child 96 (2011), 345–349.
35. Matsuda, F., Chowdhury, M.I., Saha, A., Asahara, T., Nomoto, K., Tarique, A.A., et al. Evaluation of a probiotics, Bifidobacterium breve BBG-01, for enhancement of immunogenicity of an oral inactivated cholera vaccine and safety: a randomized, double-blind, placebo-controlled trial in Bangladeshi children under 5 years of age. Vaccine 29 (2011), 1855–1858.
36. Perez, N., Iannicelli, J.C., Girard-Bosch, C., Gonzalez, S., Varea, A., Disalvo, L., et al. Effect of probiotic supplementation on immunoglobulins, isoagglutinins and antibody response in children of low socio-economic status. Europ J Nutrit 49 (2010), 173–179.
37. West, C.E., Gothefors, L., Granstrom, M., Kayhty, H., Hammarstrom, M.L., Hernell, O., Effects of feeding probiotics during weaning on infections and antibody responses to diphtheria, tetanus and Hib vaccines. Pediatr Allergy Immunol 19 (2008), 53–60.
38. Isolauri, E., Joensuu, J., Suomalainen, H., Luomala, M., Vesikari, T., Improved immunogenicity of oral D x RRV reassortant rotavirus vaccine by Lactobacillus casei GG. Vaccine 13 (1995), 310–312.
39. Licciardi, P.V., Ismail, I.H., Balloch, A., Mui, M., Hoe, E., Lamb, K., et al. Maternal supplementation with lgg reduces vaccine-specific immune responses in infants at high-risk of developing allergic disease. Front Immunol, 4, 2013, 381.
40. Maruyama, M., Abe, R., Shimono, T., Iwabuchi, N., Abe, F., Xiao, J.Z., The effects of non-viable Lactobacillus on immune function in the elderly: a randomised, double-blind, placebo-controlled study. Internat J Food Sci Nutrit 67 (2016), 67–73.
41. Jespersen, L., Tarnow, I., Eskesen, D., Morberg, C.M., Michelsen, B., Bugel, S., et al. Effect of Lactobacillus paracasei subsp. paracasei, L. casei 431 on immune response to influenza vaccination and upper respiratory tract infections in healthy adult volunteers: a randomized, double-blind, placebo-controlled, parallel-group study. Am J Clin Nutrit 101 (2015), 1188–1196.
42. Akatsu, H., Arakawa, K., Yamamoto, T., Kanematsu, T., Matsukawa, N., Ohara, H., et al. Lactobacillus in jelly enhances the effect of influenza vaccination in elderly individuals. J Am Geriatr Soc 61 (2013), 1828–1830.
43. Bosch, M., Mendez, M., Perez, M., Farran, A., Fuentes, M.C., Cune, J., Lactobacillus plantarum CECT7315 and CECT7316 stimulate immunoglobulin production after influenza vaccination in elderly. Nutr Hosp 27 (2012), 504–509.
44. Van Puyenbroeck, K., Hens, N., Coenen, S., Michiels, B., Beunckens, C., Molenberghs, G., et al. Efficacy of daily intake of Lactobacillus casei Shirota on respiratory symptoms and influenza vaccination immune response: a randomized, double-blind, placebo-controlled trial in healthy elderly nursing home residents. Am J Clin Nutrit 95 (2012), 1165–1171.
45. Rizzardini, G., Eskesen, D., Calder, P.C., Capetti, A., Jespersen, L., Clerici, M., Evaluation of the immune benefits of two probiotic strains Bifidobacterium animalis ssp. lactis, BB-12(R) and Lactobacillus paracasei ssp. paracasei, L. casei 431(R) in an influenza vaccination model: a randomised, double-blind, placebo-controlled study. Br J Nutr 107 (2012), 876–884.
46. Davidson, L.E., Fiorino, A.M., Snydman, D.R., Hibberd, P.L., Lactobacillus GG as an immune adjuvant for live-attenuated influenza vaccine in healthy adults: a randomized double-blind placebo-controlled trial. Europ J Clin Nutrit 65 (2011), 501–507.
47. Namba, K., Hatano, M., Yaeshima, T., Takase, M., Suzuki, K., Effects of Bifidobacterium longum BB536 administration on influenza infection, influenza vaccine antibody titer, and cell-mediated immunity in the elderly. Biosci Biotechnol Biochem 74 (2010), 939–945.
48. Boge, T., Remigy, M., Vaudaine, S., Tanguy, J., Bourdet-Sicard, R., van der Werf, S., A probiotic fermented dairy drink improves antibody response to influenza vaccination in the elderly in two randomised controlled trials. Vaccine 27 (2009), 5677–5684.
49. Olivares, M., Diaz-Ropero, M.P., Sierra, S., Lara-Villoslada, F., Fonolla, J., Navas, M., et al. Oral intake of Lactobacillus fermentum CECT5716 enhances the effects of influenza vaccination. Nutrition 23 (2007), 254–260.
50. Bunout, D., Barrera, G., Hirsch, S., Gattas, V., de la Maza, M.P., Haschke, F., et al. Effects of a nutritional supplement on the immune response and cytokine production in free-living Chilean elderly. JPEN J Parenter Enteral Nutr 28 (2004), 348–354.
51. Redondo, N., Nova, E., Gheorghe, A., Diaz, L.E., Hernandez, A., Marcos, A., Evaluation of Lactobacillus coryniformis CECT5711 strain as a coadjuvant in a vaccination process: a randomised clinical trial in healthy adults. Nutrition and Metabolism., 14(1), 2017 no pagination.
52. Paineau, D., Carcano, D., Leyer, G., Darquy, S., Alyanakian, M.A., Simoneau, G., et al. Effects of seven potential probiotic strains on specific immune responses in healthy adults: a double-blind, randomized, controlled trial. FEMS Immunol Med Microbiol 53 (2008), 107–113.
53. de Vrese, M., Rautenberg, P., Laue, C., Koopmans, M., Herremans, T., Schrezenmeir, J., Probiotic bacteria stimulate virus-specific neutralizing antibodies following a booster polio vaccination. Europ J Nutrit 44 (2005), 406–413.
54. Fang, H., Elina, T., Heikki, A., Seppo, S., Modulation of humoral immune response through probiotic intake. FEMS Immunol Med Microbiol 29 (2000), 47–52.
55. Redondo, N., Nova, E., Gheorghe, A., Diaz, L.E., Hernandez, A., Marcos, A., Evaluation of Lactobacillus coryniformis CECT5711 strain as a coadjuvant in a vaccination process: a randomised clinical trial in healthy adults. Nutrit Metabolism, 14, 2017, 2.
56. Sung, V., Collett, S., de Gooyer, T., Hiscock, H., Tang, M., Wake, M., Probiotics to prevent or treat excessive infant crying: systematic review and meta-analysis. JAMA Pediatrics 167 (2013), 1150–1157.
57. Elazab, N., Mendy, A., Gasana, J., Vieira, E.R., Quizon, A., Forno, E., Probiotic administration in early life, atopy, and asthma: a meta-analysis of clinical trials. Pediatrics 132 (2013), e666–e676.
58. Sang, L.-X., Chang, B., Wang, B.-Y., Liu, W.-X., Jiang, M., Live and heat-killed probiotic: effects on chronic experimental colitis induced by dextran sulfate sodium (DSS) in rats. Internat J Clin Exp Med 8 (2015), 20072–20078.
59. Ueno, N., Fujiya, M., Segawa, S., Nata, T., Moriichi, K., Tanabe, H., et al. Heat-killed body of lactobacillus brevis SBC8803 ameliorates intestinal injury in a murine model of colitis by enhancing the intestinal barrier function. Inflammat Bow Dis 17 (2011), 2235–2250.
60. Nagafuchi, S., Yamaji, T., Kawashima, A., Saito, Y., Takahashi, T., Yamamoto, T., et al. Effects of a formula containing two types of prebiotics, bifidogenic growth stimulator and galacto-oligosaccharide, and fermented milk products on intestinal microbiota and antibody response to influenza vaccine in elderly patients: a randomized controlled trial. Pharmaceuticals (Basel, Switzerland). 8 (2015), 351–365.