Maternal supplementation with LGG reduces vaccine-specific immune responses in infants at high-risk of developing allergic disease

Frontiers in Immunology

Volumn 4, Issue NOV, 2013, Pages

  Licciardi, Paul V ^a,b   Ismail, Intan H ^a   Balloch, Anne ^a   Mui, Milton ^a   Hoe, Edwin ^a   Lamb, Karen ^a   Tang, Mimi L K ^a,b,c  

^a MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c ROYAL CHILDREN'S HOSPITAL   (Australia)

Author keywords

Immune modulation; LGG; Pneumococcal; Probiotic; Treg; Vaccine

Indexed keywords

HAEMOPHILUS INFLUENZAE TYPE B VACCINE; IMMUNOGLOBULIN G; PNEUMOCOCCUS VACCINE; PROBIOTIC AGENT; TETANUS TOXOID;

ALLERGIC DISEASE; ANTIBODY RESPONSE; ARTICLE; CELL CULTURE; CELL ISOLATION; CONTROLLED STUDY; ECZEMA; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNE RESPONSE; LACTOBACILLUS RHAMNOSUS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRENATAL DRUG EXPOSURE; RANDOMIZED CONTROLLED TRIAL (TOPIC); REGULATORY T LYMPHOCYTE; SUPPLEMENTATION;

EID: 84890371474     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00381     Document Type: Article

References (54)

1. Clemens J, Jodar L. Introducing new vaccines into developing countries: obstacles, opportunities and complexities. Nat Med (2005) 11(4 Suppl):S12-5. doi:10.1038/nm1225
2. Del Giudice G. Vaccination strategies. An overview. Vaccine (2003) 21(Suppl 2):S83-8. doi:10.1016/S0264-410X(03)00205-6
3. Schijns VE. Immunological concepts of vaccine adjuvant activity. Curr Opin Immunol (2000) 12(4):456-63. doi:10.1016/S0952-7915(00)00120-5
4. O'Hagan DT, De Gregorio E. The path to a successful vaccine adjuvant-'the long and winding road'. Drug Discov Today (2009) 14(11-12):541-51. doi:10.1016/j.drudis.2009.02.009
5. Amar J, Chabo C, Waget A, Klopp P, Vachoux C, Bermudez-Humaran LG, et al. Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment. EMBO Mol Med (2011) 3(9):559-72. doi:10.1002/emmm.201100159
6. Lob-Levyt J. Contribution of the GAVI Alliance to improving health and reducing poverty. Philos Trans R Soc Lond B Biol Sci (2011) 366(1579):2743-7. doi:10.1098/rstb.2011.0040
7. Woodrow KA, Bennett KM, Lo DD. Mucosal vaccine design and delivery. Annu Rev Biomed Eng (2012) 14:17-46. doi:10.1146/annurev-bioeng-071811-150054
8. Kool M, Fierens K, Lambrecht BN. Alum adjuvant: some of the tricks of the oldest adjuvant. J Med Microbiol (2012) 61(Pt 7):927-34. doi:10.1099/jmm.0.038943-0
9. WHO. Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria. (2001). Available from: www.who.int/foodsafety/publications/fs_management/en/probiotics.pdf
10. Tang ML, Lahtinen SJ, Boyle RJ. Probiotics and prebiotics: clinical effects in allergic disease. Curr Opin Pediatr (2010) 22(5):626-34. doi:10.1097/MOP.0b013e32833d9728
11. Oelschlaeger TA. Mechanisms of probiotic actions-a review. Int J Med Microbiol (2010) 300(1):57-62. doi:10.1016/j.ijmm.2009.08.005
12. Hajela N, Nair GB, Ganguly NK. Are probiotics a feasible intervention for prevention of diarrhoea in the developing world? Gut Pathog (2010) 2(1):10. doi:10.1186/1757-4749-2-10
13. 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 (2011) 96(4):345-9. doi:10.1136/adc.2010.197459
14. Rizzardini G, Eskesen D, Calder PC, Capetti A, Jespersen L, Clerici M. Evaluation of the immune benefits of two probiotic strains Bifidobacterium animalis ssp. lactis, BB-12® and Lactobacillus paracasei ssp. paracasei, L. casei 431® in an influenza vaccination model: a randomised, double-blind, placebo-controlled study. Br J Nutr (2011) 107(6):876-84. doi:10.1017/S000711451100420X
15. Boyle RJ, Ismail IH, Kivivuori S, Licciardi PV, Robins-Browne RM, Mah LJ, et al. Lactobacillus GG treatment during pregnancy for the prevention of eczema: a randomized controlled trial. Allergy (2011) 66(4):509-16. doi:10.1111/j.1398-9995.2010.02507.x
16. Ritz N, Mui M, Balloch A, Curtis N. Non-specific effect of Bacille Calmette-Guerin vaccine on routine immunisations. Vaccine (2013) 31(30):3098-103. doi:10.1016/j.vaccine.2013.03.059
17. Balloch A, Licciardi PV, Leach A, Nurkka A, Tang ML. Results from an inter-laboratory comparison of pneumococcal serotype-specific IgG measurement and critical parameters that affect assay performance. Vaccine (2010) 28(5):1333-40. doi:10.1016/j.vaccine.2009.11.011
18. Stoop JW, Zegers BJ, Sander PC, Ballieux RE. Serum immunoglobulin levels in healthy children and adults. Clin Exp Immunol (1969) 4(1):101-12.
19. Williams CM, Rahman S, Hubeau C, Ma HL. Cytokine pathways in allergic disease. Toxicol Pathol (2012) 40(2):205-15. doi:10.1177/0192623311430694
20. Yagi R, Zhu J, Paul WE. An updated view on transcription factor GATA3-mediated regulation of Th1 and Th2 cell differentiation. Int Immunol (2011) 23(7):415-20. doi:10.1093/intimm/dxr029
21. Russell FM, Licciardi PV, Balloch A, Biaukula V, Tikoduadua L, Carapetis JR, et al. Safety and immunogenicity of the 23-valent pneumococcal polysaccharide vaccine at 12 months of age, following one, two, or three doses of the 7-valent pneumococcal conjugate vaccine in infancy. Vaccine (2010) 28(18):3086-94. doi:10.1016/j.vaccine.2010.02.065
22. Marchant A, Pihlgren M, Goetghebuer T, Weiss HA, Ota MO, Schlegel-Hauter SE, et al. Council Gambia Twin Study: predominant influence of environmental determinants on the persistence and avidity maturation of antibody responses to vaccines in infants. J Infect Dis (2006) 193(11):1598-605. doi:10.1086/503775
23. Feleszko W, Jaworska J, Rha RD, Steinhausen S, Avagyan A, Jaudszus A, et al. Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin Exp Allergy (2007) 37(4):498-505. doi:10.1111/j.1365-2222.2006.02629.x
24. de Roock S, van Elk M, van Dijk ME, Timmerman HM, Rijkers GT, Prakken BJ, et al. Lactic acid bacteria differ in their ability to induce functional regulatory T cells in humans. Clin Exp Allergy (2010) 40(1):103-10. doi:10.1111/j.1365-2222.2009.03344.x
25. Lopez P, Gonzalez-Rodriguez I, Sanchez B, Gueimonde M, Margolles A, Suarez A. Treg-inducing membrane vesicles from Bifidobacterium bifidum LMG13195 as potential adjuvants in immunotherapy. Vaccine (2012) 30(5):825-9. doi:10.1016/j.vaccine.2011.11.115
26. Smelt MJ, de Haan BJ, Bron PA, van Swam I, Meijerink M, Wells JM, et al. L. plantarum, L. salivarius, and L. lactis attenuate Th2 responses and increase Treg frequencies in healthy mice in a strain dependent manner. PLoS One (2012) 7(10):e47244. doi:10.1371/journal.pone.0047244
27. Rutten NB, Besseling-van der Vaart I, Klein M, de Roock S, Vlieger AM, Rijkers GT. In vitro assessment of the immunomodulatory effects of multispecies probiotic formulations for management of allergic diseases. Benef Microbes (2011) 2(3):183-92. doi:10.3920/BM2011.0012
28. Josefowicz SZ, Lu LF, Rudensky AY. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol (2012) 30:531-64. doi:10.1146/annurev.immunol.25.022106.141623
29. Lesiak A, Smolewski P, Sobolewska-Sztychny D, Sysa-Jedrzejowska A, Narbutt J. The role of T-regulatory cells and toll-like receptors 2 and 4 in atopic dermatitis. Scand J Immunol (2012) 76(4):405-10. doi:10.1111/j.1365-3083.2012.02739.x
30. Kalliomaki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet (2001) 357(9262):1076-9. doi:10.1016/S0140-6736(00)04259-8
31. Rautava S, Kalliomaki M, Isolauri E. Probiotics during pregnancy and breast-feeding might confer immunomodulatory protection against atopic disease in the infant. J Allergy Clin Immunol (2002) 109(1):119-21. doi:10.1067/mai.2002.120273
32. Huurre A, Laitinen K, Rautava S, Korkeamaki M, Isolauri E. Impact of maternal atopy and probiotic supplementation during pregnancy on infant sensitization: a double-blind placebo-controlled study. Clin Exp Allergy (2008) 38(8):1342-8. doi:10.1111/j.1365-2222.2008.03008.x
33. Prescott SL, Wickens K, Westcott L, Jung W, Currie H, Black PN, et al. Supplementation with Lactobacillus rhamnosus or Bifidobacterium lactis probiotics in pregnancy increases cord blood interferon-gamma and breast milk transforming growth factor-beta and immunoglobin A detection. Clin Exp Allergy (2008) 38(10):1606-14. doi:10.1111/j.1365-2222.2008.03061.x
34. Ismail IH, Licciardi PV, Oppedisano F, Boyle RJ, Tang ML. Relationship between breast milk sCD14, TGF-beta1 and total IgA in the first month and development of eczema during infancy. Pediatr Allergy Immunol (2013) 24(4):352-60. doi:10.1111/pai.12075
35. Khosravi A, Mazmanian SK. Disruption of the gut microbiome as a risk factor for microbial infections. Curr Opin Microbiol (2013) 16(2):221-7. doi:10.1016/j.mib.2013.03.009
36. Rautava S, Luoto R, Salminen S, Isolauri E. Microbial contact during pregnancy, intestinal colonization and human disease. Nat Rev Gastroenterol Hepatol (2012) 9(10):565-76. doi:10.1038/nrgastro.2012.144
37. Grzeskowiak L, Gronlund MM, Beckmann C, Salminen S, von Berg A, Isolauri E. The impact of perinatal probiotic intervention on gut microbiota: double-blind placebo-controlled trials in Finland and Germany. Anaerobe (2012) 18(1):7-13. doi:10.1016/j.anaerobe.2011.09.006
38. Rinne M, Kalliomaki M, Salminen S, Isolauri E. Probiotic intervention in the first months of life: short-term effects on gastrointestinal symptoms and long-term effects on gut microbiota. J Pediatr Gastroenterol Nutr (2006) 43(2):200-5. doi:10.1097/01.mpg.0000228106.91240.5b
39. Osborn DA, Sinn JK. Probiotics in infants for prevention of allergic disease and food hypersensitivity. Cochrane Database Syst Rev (2007) (4):CD006475.
40. Boyle RJ, Bath-Hextall FJ, Leonardi-Bee J, Murrell DF, Tang ML. Probiotics for treating eczema. Cochrane Database Syst Rev (2008) (4):CD006135. doi:10.1002/14651858.CD006135.pub2
41. Ismail IH, Licciardi PV, Tang ML. Probiotic effects in allergic disease. J Paediatr Child Health (2013) 49(9):709-15. doi:10.1111/jpc.12175
42. Lahtinen SJ, Boyle RJ, Kivivuori S, Oppedisano F, Smith KR, Robins-Browne R, et al. Prenatal probiotic administration can influence Bifidobacterium microbiota development in infants at high risk of allergy. J Allergy Clin Immunol (2009) 123(2):499-501. doi:10.1016/j.jaci.2008.11.034
43. Ferreira RB, Antunes LC, Finlay BB. Should the human microbiome be considered when developing vaccines? PLoS Pathog (2010) 6(11):e1001190. doi:10.1371/journal.ppat.1001190
44. Licciardi PV, Tang ML. Vaccine adjuvant properties of probiotic bacteria. Discov Med (2011) 12(67):525-33.
45. 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. Eur J Nutr (2005) 44(7):406-13. doi:10.1007/s00394-004-0541-8
46. Fang H, Elina T, Heikki A, Seppo S. Modulation of humoral immune response through probiotic intake. FEMS Immunol Med Microbiol (2000) 29(1):47-52. doi:10.1111/j.1574-695X.2000.tb01504.x
47. Olivares M, Diaz-Ropero MP, Sierra S, Lara-Villoslada F, Fonolla J, Navas M, et al. Oral intake of Lactobacillus fermentum CECT5716 enhances the effects of influenza vaccination. Nutrition (2007) 23(3):254-60. doi:10.1016/j.nut.2007.01.004
48. Bosch M, Mendez M, Perez M, Farran A, Fuentes MC, Cune J. Lactobacillus plantarum CECT7315 and CECT7316 stimulate immunoglobulin production after influenza vaccination in elderly. Nutr Hosp (2012) 27(2):504-9. doi:10.1590/S0212-16112012000200023
49. Soh SE, Ong DQ, Gerez I, Zhang X, Chollate P, Shek LP, et al. Effect of probiotic supplementation in the first 6 months of life on specific antibody responses to infant Hepatitis B vaccination. Vaccine (2010) 28(14):2577-9. doi:10.1016/j.vaccine.2010.01.020
50. Mullie C, Yazourh A, Thibault H, Odou MF, 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. Pediatr Res (2004) 56(5):791-5. doi:10.1203/01.PDR.0000141955.47550.A0
51. Khan AA, Zahidie A, Rabbani F. Interventions to reduce neonatal mortality from neonatal tetanus in low and middle income countries-a systematic review. BMC Public Health (2013) 13(1):322. doi:10.1186/1471-2458-13-322
52. O'Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, McCall N, et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet (2009) 374(9693):893-902. doi:10.1016/S0140-6736(09)61204-6
53. Wilson-Welder JH, Torres MP, Kipper MJ, Mallapragada SK, Wannemuehler MJ, Narasimhan B. Vaccine adjuvants: current challenges and future approaches. J Pharm Sci (2009) 98(4):1278-316. doi:10.1002/jps.21523
54. Stam J, van Stuijvenberg M, Garssen J, Knipping K, Sauer PJ. A mixture of three prebiotics does not affect vaccine specific antibody responses in healthy term infants in the first year of life. Vaccine (2011) 29(44):7766-72. doi:10.1016/j.vaccine.2011.07.110