Skip to main content

Gut Immunology and Oral Vaccination

  • Chapter
  • First Online:
Molecular Vaccines

Abstract

Oral immunization is sought as a practical way to reduce the devastating morbidity and mortality caused by enteric diseases in children under the age of five living in the developing world. Licensed oral vaccines against polio, rotavirus, cholera and typhoid fever have had a major impact reducing global disease burden and mortality. A quandary that remains to be solved is the diminished immunogenicity and efficacy of these vaccines when given to subjects living in underdeveloped areas of the world as compared to people living in industrialized nations. Low socioeconomic status, poor living conditions, malnutrition and natural barriers that affect people living in less privileged countries are major determinants of vaccine performance. Novel protective antigens, adjuvants and immunization approaches to overcome these barriers are being explored. Understanding the processes involved in the induction of mucosal and systemic immunity by orally delivered antigens, the influence of multiple competing elements and the delicate balance between immune activation and tolerance in the gut is essential to assist the development and evaluation of vaccine candidates. Modern technology (e.g. genomics, proteomics, high throughput immunological assays using non-invasive specimens and mathematical modeling to dissect correlates of protection) will be essential to this task. Ultimately, well conducted clinical trials in high and low income countries will be needed to determine safety and effectiveness of vaccine candidates that appear to be promising in animal models. This chapter reviews the basis for immunological priming by orally delivered antigens in the gastrointestinal tract and the ensuing effector responses in humans. It also provides a summary of oral vaccines available, factors that affect efficacy of oral vaccines in developing countries as well as the ongoing efforts to develop more effective vaccine candidates.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Suzuki, K., Fagarasan, S.: Diverse regulatory pathways for IgA synthesis in the gut. Mucosal Immunol. 2, 468–471 (2009)

    PubMed  CAS  Google Scholar 

  2. Yamamoto, M., Pascual, D.W., Kiyono, H.: M cell-targeted mucosal vaccine strategies. Curr. Top. Microbiol. Immunol. 354, 39–52 (2012)

    PubMed  CAS  Google Scholar 

  3. Brandtzaeg, P.: Induction of secretory immunity and memory at mucosal surfaces. Vaccine 25, 5467–5484 (2007)

    PubMed  CAS  Google Scholar 

  4. Soloff, A.C., Barratt-Boyes, S.M.: Enemy at the gates: dendritic cells and immunity to mucosal pathogens. Cell Res. 20, 872–885 (2010)

    PubMed  CAS  Google Scholar 

  5. Sutherland, D.B., Fagarasan, S.: IgA synthesis: a form of functional immune adaptation extending beyond gut. Curr. Opin. Immunol. 24, 261–268 (2012)

    PubMed  CAS  Google Scholar 

  6. Cerutti, A.: Location, location, location: B-cell differentiation in the gut lamina propria. Mucosal Immunol. 1, 8–10 (2008)

    PubMed  CAS  Google Scholar 

  7. Macpherson, A.J., Geuking, M.B., McCoy, K.D.: Homeland security: IgA immunity at the frontiers of the body. Trends Immunol. 33, 160–167 (2012)

    PubMed  CAS  Google Scholar 

  8. Gibbons, D.L., Spencer, J.: Mouse and human intestinal immunity: same ballpark, different players; different rules, same score. Mucosal Immunol. 4, 148–157 (2011)

    PubMed  CAS  Google Scholar 

  9. Bemark, M., Boysen, P., Lycke, N.Y.: Induction of gut IgA production through T cell-dependent and T cell-independent pathways. Ann. N. Y. Acad. Sci. 1247, 97–116 (2012)

    PubMed  CAS  Google Scholar 

  10. Slack, E., Balmer, M.L., Fritz, J.H., Hapfelmeier, S.: Functional flexibility of intestinal IgA - broadening the fine line. Front Immunol. 3, 100 (2012)

    PubMed  Google Scholar 

  11. Mantis, N.J., Rol, N., Corthesy, B.: Secretory IgA’s complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol. 4, 603–611 (2011)

    PubMed  CAS  Google Scholar 

  12. Pabst, O.: New concepts in the generation and functions of IgA. Nat. Rev. Immunol. 12, 821–832 (2012)

    PubMed  CAS  Google Scholar 

  13. Kett, K., Brandtzaeg, P., Radl, J., Haaijman, J.J.: Different subclass distribution of IgA-producing cells in human lymphoid organs and various secretory tissues. J. Immunol. 136, 3631–3635 (1986)

    PubMed  CAS  Google Scholar 

  14. Israel, E.J., et al.: Expression of the neonatal Fc receptor, FcRn, on human intestinal epithelial cells. Immunology 92, 69–74 (1997)

    PubMed  CAS  Google Scholar 

  15. Neutra, M.R., Kozlowski, P.A.: Mucosal vaccines: the promise and the challenge. Nat. Rev. Immunol. 6, 148–158 (2006)

    PubMed  CAS  Google Scholar 

  16. Robbins, J.B., Chu, C., Schneerson, R.: Hypothesis for vaccine development: protective immunity to enteric diseases caused by nontyphoidal salmonellae and shigellae may be conferred by serum IgG antibodies to the O-specific polysaccharide of their lipopolysaccharides. Clin. Infect. Dis. 15, 346–361 (1992)

    PubMed  CAS  Google Scholar 

  17. Yoshida, M., et al.: Human neonatal fc receptor mediates transport of IgG into luminal secretions for delivery of antigens to mucosal dendritic cells. Immunity 20, 769–783 (2004)

    PubMed  CAS  Google Scholar 

  18. Boullier, S., et al.: Secretory IgA-mediated neutralization of Shigella flexneri prevents intestinal tissue destruction by down-regulating inflammatory circuits. J. Immunol. 183, 5879–5885 (2009)

    PubMed  CAS  Google Scholar 

  19. Devriendt, B., De Geest, B.G., Goddeeris, B.M., Cox, E.: Crossing the barrier: targeting epithelial receptors for enhanced oral vaccine delivery. J. Control. Release 160, 431–439 (2012)

    PubMed  CAS  Google Scholar 

  20. Kantele, A.: Peripheral blood antibody-secreting cells in the evaluation of the immune response to an oral vaccine. J. Biotechnol. 44, 217–224 (1996)

    PubMed  CAS  Google Scholar 

  21. Sigmundsdottir, H., Butcher, E.C.: Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat. Immunol. 9, 981–987 (2008)

    PubMed  CAS  Google Scholar 

  22. Quiding-Jarbrink, M., et al.: Differential expression of tissue-specific adhesion molecules on human circulating antibody-forming cells after systemic, enteric, and nasal immunizations. A molecular basis for the compartmentalization of effector B cell responses. J. Clin. Invest. 99, 1281–1286 (1997)

    PubMed  CAS  Google Scholar 

  23. Qadri, F., et al.: Enteric infections in an endemic area induce a circulating antibody-secreting cell response with homing potentials to both mucosal and systemic tissues. J. Infect. Dis. 177, 1594–1599 (1998)

    PubMed  CAS  Google Scholar 

  24. Kantele, A., et al.: Homing potentials of circulating lymphocytes in humans depend on the site of activation: oral, but not parenteral, typhoid vaccination induces circulating antibody-secreting cells that all bear homing receptors directing them to the gut. J. Immunol. 158, 574–579 (1997)

    PubMed  CAS  Google Scholar 

  25. Kantele, A., et al.: Differences in immune responses induced by oral and rectal immunizations with Salmonella typhi Ty21a: evidence for compartmentalization within the common mucosal immune system in humans. Infect. Immun. 66, 5630–5635 (1998)

    PubMed  CAS  Google Scholar 

  26. Herremans, T.M., Reimerink, J.H., Buisman, A.M., Kimman, T.G., Koopmans, M.P.: Induction of mucosal immunity by inactivated poliovirus vaccine is dependent on previous mucosal contact with live virus. J. Immunol. 162, 5011–5018 (1999)

    PubMed  CAS  Google Scholar 

  27. Sallusto, F., Geginat, J., Lanzavecchia, A.: Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22, 745–763 (2004)

    PubMed  CAS  Google Scholar 

  28. Kunkel, E.J., et al.: Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J. Exp. Med. 192, 761–768 (2000)

    PubMed  CAS  Google Scholar 

  29. Rabinowitz, K., Mayer, L.: Working out mechanisms of controlled/physiologic inflammation in the GI tract. Immunol. Res. 54, 14–24 (2012)

    PubMed  Google Scholar 

  30. Saurer, L., Mueller, C.: T cell-mediated immunoregulation in the gastrointestinal tract. Allergy 64, 505–519 (2009)

    PubMed  CAS  Google Scholar 

  31. Nagler-Anderson, C., Bhan, A.K., Podolsky, D.K., Terhorst, C.: Control freaks: immune regulatory cells. Nat. Immunol. 5, 119–122 (2004)

    PubMed  CAS  Google Scholar 

  32. Mucida, D., Salek-Ardakani, S.: Regulation of TH17 cells in the mucosal surfaces. J. Allergy Clin. Immunol. 123, 997–1003 (2009)

    PubMed  CAS  Google Scholar 

  33. Ivanov, I.I., et al.: Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4, 337–349 (2008)

    PubMed  CAS  Google Scholar 

  34. Lycke, N.: Recent progress in mucosal vaccine development: potential and limitations. Nat. Rev. Immunol. 12, 592–605 (2012)

    PubMed  CAS  Google Scholar 

  35. Mucida, D.: T-helping colitis. Gastroenterology 141, 801–805 (2011)

    PubMed  Google Scholar 

  36. Sarra, M., Pallone, F., MacDonald, T.T., Monteleone, G.: IL-23/IL-17 axis in IBD. Inflamm. Bowel Dis. 16, 1808–1813 (2010)

    PubMed  Google Scholar 

  37. McArthur, M.A., Sztein, M.B.: Heterogeneity of multifunctional IL-17A producing S. Typhi-specific CD8+ T cells in volunteers following Ty21a typhoid immunization. PLoS One 7, e38408 (2012)

    PubMed  CAS  Google Scholar 

  38. Crotty, S., Aubert, R.D., Glidewell, J., Ahmed, R.: Tracking human antigen-specific memory B cells: a sensitive and generalized ELISPOT system. J. Immunol. Methods 286, 111–122 (2004)

    PubMed  CAS  Google Scholar 

  39. Rojas, O.L., et al.: Evaluation of circulating intestinally committed memory B cells in children vaccinated with attenuated human rotavirus vaccine. Viral Immunol. 20, 300–311 (2007)

    PubMed  CAS  Google Scholar 

  40. Harris, A.M., et al.: Antigen-specific memory B-cell responses to Vibrio cholerae O1 infection in Bangladesh. Infect. Immun. 77, 3850–3856 (2009)

    PubMed  CAS  Google Scholar 

  41. Simon, J.K., et al.: Antigen-specific B memory cell responses to lipopolysaccharide (LPS) and invasion plasmid antigen (Ipa) B elicited in volunteers vaccinated with live-attenuated Shigella flexneri 2a vaccine candidates. Vaccine 27, 565–572 (2009)

    PubMed  CAS  Google Scholar 

  42. Wahid, R., Simon, R., Zafar, S.J., Levine, M.M., Sztein, M.B.: Live oral typhoid vaccine Ty21a induces cross-reactive humoral immune responses against Salmonella enterica serovar Paratyphi A and S. Paratyphi B in humans. Clin. Vaccine Immunol. 19, 825–834 (2012)

    PubMed  CAS  Google Scholar 

  43. Wahid, R., et al.: Oral priming with Salmonella Typhi vaccine strain CVD 909 followed by parenteral boost with the S. Typhi Vi capsular polysaccharide vaccine induces CD27+IgD-S. Typhi-specific IgA and IgG B memory cells in humans. Clin. Immunol. 138, 187–200 (2011)

    PubMed  CAS  Google Scholar 

  44. Plotkin, S.A.: Correlates of protection induced by vaccination. Clin. Vaccine Immunol. 17, 1055–1065 (2010)

    PubMed  CAS  Google Scholar 

  45. Chen, R.T., et al.: Measles antibody: reevaluation of protective titers. J. Infect. Dis. 162, 1036–1042 (1990)

    PubMed  CAS  Google Scholar 

  46. Ilan, Y.: Oral tolerance: can we make it work? Hum. Immunol. 70, 768–776 (2009)

    PubMed  CAS  Google Scholar 

  47. Tsuji, N.M., Kosaka, A.: Oral tolerance: intestinal homeostasis and antigen-specific regulatory T cells. Trends Immunol. 29, 532–540 (2008)

    PubMed  CAS  Google Scholar 

  48. Pabst, O., Mowat, A.M.: Oral tolerance to food protein. Mucosal Immunol. 5, 232–239 (2012)

    PubMed  CAS  Google Scholar 

  49. Sun, C.M., et al.: Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775–1785 (2007)

    PubMed  CAS  Google Scholar 

  50. Scott, C.L., Aumeunier, A.M., Mowat, A.M.: Intestinal CD103+ dendritic cells: master regulators of tolerance? Trends Immunol. 32, 412–419 (2011)

    PubMed  CAS  Google Scholar 

  51. Sabin, A.B.: Oral poliovirus vaccine: history of its development and use and current challenge to eliminate poliomyelitis from the world. J. Infect. Dis. 151, 420–436 (1985)

    PubMed  CAS  Google Scholar 

  52. Heaton, P.M., Goveia, M.G., Miller, J.M., Offit, P., Clark, H.F.: Development of a pentavalent rotavirus vaccine against prevalent serotypes of rotavirus gastroenteritis. J. Infect. Dis. 192(Suppl 1), S17–S21 (2005)

    PubMed  Google Scholar 

  53. De, V.B., et al.: A rotavirus vaccine for prophylaxis of infants against rotavirus gastroenteritis. Pediatr. Infect. Dis. J. 23, S179–S182 (2004)

    Google Scholar 

  54. Vesikari, T., et al.: Efficacy of human rotavirus vaccine against rotavirus gastroenteritis during the first 2 years of life in European infants: randomised, double-blind controlled study. Lancet 370, 1757–1763 (2007)

    PubMed  CAS  Google Scholar 

  55. Germanier, R., Fuer, E.: Isolation and characterization of Gal E mutant Ty 21a of Salmonella Typhi: a candidate strain for a live, oral typhoid vaccine. J. Infect. Dis. 131, 553–558 (1975)

    PubMed  CAS  Google Scholar 

  56. Desai, S.N., Clemens, J.D.: An overview of cholera vaccines and their public health implications. Curr. Opin. Pediatr. 24, 85–91 (2012)

    PubMed  CAS  Google Scholar 

  57. Ruiz-Palacios, G.M., et al.: Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N. Engl. J. Med. 354, 11–22 (2006)

    PubMed  CAS  Google Scholar 

  58. Vesikari, T., et al.: Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N. Engl. J. Med. 354, 23–33 (2006)

    PubMed  CAS  Google Scholar 

  59. Levine, M.M., et al.: Safety, immunogenicity, and efficacy of recombinant live oral cholera vaccines, CVD 103 and CVD 103-HgR. Lancet 2, 467–470 (1988)

    PubMed  CAS  Google Scholar 

  60. Clemens, J.D., et al.: Field trial of oral cholera vaccines in Bangladesh: results from three-year follow-up. Lancet 335, 270–273 (1990)

    PubMed  CAS  Google Scholar 

  61. Madhi, S.A., et al.: Effect of human rotavirus vaccine on severe diarrhea in African infants. N. Engl. J. Med. 362, 289–298 (2010)

    PubMed  CAS  Google Scholar 

  62. Patriarca, P.A., Wright, P.F., John, T.J.: Factors affecting the immunogenicity of oral poliovirus vaccine in developing countries: review. Rev. Infect. Dis. 13, 926–939 (1991)

    PubMed  CAS  Google Scholar 

  63. Zaman, K., et al.: Successful co-administration of a human rotavirus and oral poliovirus vaccines in Bangladeshi infants in a 2-dose schedule at 12 and 16 weeks of age. Vaccine 27, 1333–1339 (2009)

    PubMed  CAS  Google Scholar 

  64. Armah, G.E., et al.: Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in sub-Saharan Africa: a randomised, double-blind, placebo-controlled trial. Lancet 376, 606–614 (2010)

    PubMed  CAS  Google Scholar 

  65. World Health Organization: Polio vaccines and polio immunization in the pre-eradication era: WHO position paper. Wkly. Epidemiol. Rec. 85, 213–228 (2010)

    Google Scholar 

  66. Kew, O.: Reaching the last one per cent: progress and challenges in global polio eradication. Curr. Opin. Virol. 2, 188–198 (2012)

    PubMed  Google Scholar 

  67. Onorato, I.M., et al.: Mucosal immunity induced by enhance-potency inactivated and oral polio vaccines. J. Infect. Dis. 163, 1–6 (1991)

    PubMed  CAS  Google Scholar 

  68. Laassri, M., et al.: Effect of different vaccination schedules on excretion of oral poliovirus vaccine strains. J. Infect. Dis. 192, 2092–2098 (2005)

    PubMed  Google Scholar 

  69. Paul, Y.: Why polio has not been eradicated in India despite many remedial interventions? Vaccine 27, 3700–3703 (2009)

    PubMed  Google Scholar 

  70. John, T.J.: Antibody response of infants in tropics to five doses of oral polio vaccine. Br. Med. J. 1, 812 (1976)

    PubMed  CAS  Google Scholar 

  71. Posey, D.L., Linkins, R.W., Oliveria, M.J., Monteiro, D., Patriarca, P.A.: The effect of diarrhea on oral poliovirus vaccine failure in Brazil. J. Infect. Dis. 175(Suppl 1), S258–S263 (1997)

    PubMed  Google Scholar 

  72. Grassly, N.C., et al.: New strategies for the elimination of polio from India. Science 314, 1150–1153 (2006)

    PubMed  CAS  Google Scholar 

  73. Vashishtha, V.M., Kalra, A., John, T.J., Thacker, N., Agarwal, R.K.: Recommendations of 2nd National Consultative Meeting of Indian Academy of Pediatrics (IAP) on polio eradication and improvement of routine immunization. Indian Pediatr. 45, 367–378 (2008)

    PubMed  Google Scholar 

  74. Kaura, G., Biswas, T.: India reaches milestone of no cases of wild poliovirus for 12 months. BMJ 344, e1328 (2012)

    PubMed  Google Scholar 

  75. Strebel, P.M., et al.: Epidemiology of poliomyelitis in the United States one decade after the last reported case of indigenous wild virus-associated disease. Clin. Infect. Dis. 14, 568–579 (1992)

    PubMed  CAS  Google Scholar 

  76. Prevots, D.R., Burr, R.K., Sutter, R.W., Murphy, T.V.: Poliomyelitis prevention in the United States. Updated recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm. Rep. 49, 1–22 (2000)

    PubMed  CAS  Google Scholar 

  77. Parashar, U.D., et al.: Global mortality associated with rotavirus disease among children in 2004. J. Infect. Dis. 200(Suppl 1), S9–S15 (2009)

    PubMed  Google Scholar 

  78. Steele, A.D., et al.: Rotavirus vaccines for infants in developing countries in Africa and Asia: considerations from a world health organization-sponsored consultation. J. Infect. Dis. 200(Suppl 1), S63–S69 (2009)

    PubMed  Google Scholar 

  79. Meeting of the immunization Strategic Advisory Group of Experts, April 2009–conclusions and recommendations. Wkly. Epidemiol. Rec. 84, 220–236 (2009)

    Google Scholar 

  80. Glass, R.I., et al.: Rotavirus vaccines: current prospects and future challenges. Lancet 368, 323–332 (2006)

    PubMed  CAS  Google Scholar 

  81. Murphy, T.V., Smith, P.J., Gargiullo, P.M., Schwartz, B.: The first rotavirus vaccine and intussusception: epidemiological studies and policy decisions. J. Infect. Dis. 187, 1309–1313 (2003)

    PubMed  Google Scholar 

  82. Franco, M.A., Angel, J., Greenberg, H.B.: Immunity and correlates of protection for rotavirus vaccines. Vaccine 24, 2718–2731 (2006)

    PubMed  CAS  Google Scholar 

  83. Brown, K.A., Kriss, J.A., Moser, C.A., Wenner, W.J., Offit, P.A.: Circulating rotavirus-specific antibody-secreting cells (ASCs) predict the presence of rotavirus-specific ASCs in the human small intestinal lamina propria. J. Infect. Dis. 182, 1039–1043 (2000)

    PubMed  CAS  Google Scholar 

  84. Patel, M.M., et al.: Intussusception risk and health benefits of rotavirus vaccination in Mexico and Brazil. N. Engl. J. Med. 364, 2283–2292 (2011)

    PubMed  CAS  Google Scholar 

  85. Shui, I.M., et al.: Risk of intussusception following administration of a pentavalent rotavirus vaccine in US infants. JAMA 307, 598–604 (2012)

    PubMed  CAS  Google Scholar 

  86. Breiman, R.F., et al.: Analyses of health outcomes from the 5 sites participating in the Africa and Asia clinical efficacy trials of the oral pentavalent rotavirus vaccine. Vaccine 30(Suppl 1), A24–A29 (2012)

    PubMed  Google Scholar 

  87. Block, S.L., et al.: Efficacy, immunogenicity, and safety of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine at the end of shelf life. Pediatrics 119, 11–18 (2007)

    PubMed  Google Scholar 

  88. Vesikari, T., et al.: Efficacy of a pentavalent rotavirus vaccine in reducing rotavirus-associated health care utilization across three regions (11 countries). Int. J. Infect. Dis. 11(Suppl 2), S29–S35 (2007)

    PubMed  Google Scholar 

  89. Ciarlet, M., Schodel, F.: Development of a rotavirus vaccine: clinical safety, immunogenicity, and efficacy of the pentavalent rotavirus vaccine. RotaTeq. Vaccine 27(Suppl 6), G72–G81 (2009)

    PubMed  CAS  Google Scholar 

  90. Zaman, K., et al.: Efficacy of pentavalent rotavirus vaccine against severe rotavirus gastroenteritis in infants in developing countries in Asia: a randomised, double-blind, placebo-controlled trial. Lancet 376, 615–623 (2010)

    PubMed  CAS  Google Scholar 

  91. Rennels, M.B., Ward, R.L., Mack, M.E., Zito, E.T.: Concurrent oral poliovirus and rhesus-human reassortant rotavirus vaccination: effects on immune responses to both vaccines and on efficacy of rotavirus vaccines. The US Rotavirus Vaccine Efficacy Group. J. Infect. Dis. 173, 306–313 (1996)

    PubMed  CAS  Google Scholar 

  92. Ciarlet, M., et al.: Concomitant use of the oral pentavalent human-bovine reassortant rotavirus vaccine and oral poliovirus vaccine. Pediatr. Infect. Dis. J. 27, 874–880 (2008)

    PubMed  Google Scholar 

  93. Cholera vaccines: WHO position paper. Wkly. Epidemiol. Rec. 85, 117–128 (2010)

    Google Scholar 

  94. Harris, J.B., LaRocque, R.C., Qadri, F., Ryan, E.T., Calderwood, S.B.: Cholera. Lancet 379, 2466–2476 (2012)

    PubMed  Google Scholar 

  95. Levine, M.M., et al.: Duration of infection-derived immunity to cholera. J. Infect. Dis. 143, 818–820 (1981)

    PubMed  CAS  Google Scholar 

  96. Levine, M.M., et al.: Immunity of cholera in man: relative role of antibacterial versus antitoxic immunity. Trans. R. Soc. Trop. Med. Hyg. 73, 3–9 (1979)

    PubMed  CAS  Google Scholar 

  97. Qadri, F., et al.: Antigen-specific immunoglobulin A antibodies secreted from circulating B cells are an effective marker for recent local immune responses in patients with cholera: comparison to antibody-secreting cell responses and other immunological markers. Infect. Immun. 71, 4808–4814 (2003)

    PubMed  CAS  Google Scholar 

  98. Qadri, F., et al.: Comparison of immune responses in patients infected with Vibrio cholerae O139 and O1. Infect. Immun. 65, 3571–3576 (1997)

    PubMed  CAS  Google Scholar 

  99. Glass, R.I., et al.: Seroepidemiological studies of El Tor cholera in Bangladesh: association of serum antibody levels with protection. J. Infect. Dis. 151, 236–242 (1985)

    PubMed  CAS  Google Scholar 

  100. Mosley, W.H., McCormack, W.M., Ahmed, A., Chowdhury, A.K., Barui, R.K.: Report of the 1966–67 cholera vaccine field trial in rural East Pakistan. 2. Results of the serological surveys in the study population–the relationship of case rate to antibody titre and an estimate of the inapparent infection rate with Vibrio cholerae. Bull. World Health Organ. 40, 187–197 (1969)

    PubMed  CAS  Google Scholar 

  101. Mosley, W.H., Ahmad, S., Benenson, A.S., Ahmed, A.: The relationship of vibriocidal antibody titre to susceptibility to cholera in family contacts of cholera patients. Bull. World Health Organ. 38, 777–785 (1968)

    PubMed  CAS  Google Scholar 

  102. Uddin, T., et al.: Mucosal immunologic responses in cholera patients in Bangladesh. Clin. Vaccine Immunol. 18, 506–512 (2011)

    PubMed  CAS  Google Scholar 

  103. Jayasekera, C.R., et al.: Cholera toxin-specific memory B cell responses are induced in patients with dehydrating diarrhea caused by Vibrio cholerae O1. J. Infect. Dis. 198, 1055–1061 (2008)

    PubMed  CAS  Google Scholar 

  104. Patel, S.M., et al.: Memory B cell responses to Vibrio cholerae O1 lipopolysaccharide are associated with protection against infection from household contacts of patients with cholera in Bangladesh. Clin. Vaccine Immunol. 19, 842–848 (2012)

    PubMed  CAS  Google Scholar 

  105. Charles, R.C., Ryan, E.T.: Cholera in the 21st century. Curr. Opin. Infect. Dis. 24, 472–477 (2011)

    PubMed  Google Scholar 

  106. van Loon, F.P., et al.: Field trial of inactivated oral cholera vaccines in Bangladesh: results from 5 years of follow-up. Vaccine 14, 162–166 (1996)

    PubMed  Google Scholar 

  107. Mahalanabis, D., et al.: A randomized, placebo-controlled trial of the bivalent killed, whole-cell, oral cholera vaccine in adults and children in a cholera endemic area in Kolkata, India. PLoS One 3, e2323 (2008)

    PubMed  Google Scholar 

  108. Saha, A., et al.: Safety and immunogenicity study of a killed bivalent (O1 and O139) whole-cell oral cholera vaccine Shanchol, in Bangladeshi adults and children as young as 1 year of age. Vaccine 29, 8285–8292 (2011)

    PubMed  Google Scholar 

  109. Anh, D.D., et al.: Safety and immunogenicity of a reformulated Vietnamese bivalent killed, whole-cell, oral cholera vaccine in adults. Vaccine 25, 1149–1155 (2007)

    PubMed  CAS  Google Scholar 

  110. Kanungo, S., et al.: Immune responses following one and two doses of the reformulated, bivalent, killed, whole-cell, oral cholera vaccine among adults and children in Kolkata, India: a randomized, placebo-controlled trial. Vaccine 27, 6887–6893 (2009)

    PubMed  CAS  Google Scholar 

  111. Alam, M.M., et al.: Antigen-specific memory B-cell responses in Bangladeshi adults after one- or two-dose oral killed cholera vaccination and comparison with responses in patients with naturally acquired cholera. Clin. Vaccine Immunol. 18, 844–850 (2011)

    PubMed  CAS  Google Scholar 

  112. Clemens, J.D., et al.: Biotype as determinant of natural immunising effect of cholera. Lancet 337, 883–884 (1991)

    PubMed  CAS  Google Scholar 

  113. Ali, M., Emch, M., Park, J.K., Yunus, M., Clemens, J.: Natural cholera infection-derived immunity in an endemic setting. J. Infect. Dis. 204, 912–918 (2011)

    PubMed  CAS  Google Scholar 

  114. Tacket, C.O., et al.: Randomized, double-blind, placebo-controlled, multicentered trial of the efficacy of a single dose of live oral cholera vaccine CVD 103-HgR in preventing cholera following challenge with Vibrio cholerae O1 El tor inaba three months after vaccination. Infect. Immun. 67, 6341–6345 (1999)

    PubMed  CAS  Google Scholar 

  115. Cryz, S.J., Levine, M.M., Kaper, J.B., Furer, E., Althaus, B.: Randomized double-blind placebo controlled trial to evaluate the safety and immunogenicity of the live oral cholera vaccine strain CVD 103-HgR in Swiss adults. Vaccine 8, 577–580 (1990)

    PubMed  Google Scholar 

  116. Tacket, C.O., et al.: Onset and duration of protective immunity in challenged volunteers after vaccination with live oral cholera vaccine CVD 103-HgR. J. Infect. Dis. 166, 837–841 (1992)

    PubMed  CAS  Google Scholar 

  117. Suharyono, S.C., et al.: Safety and immunogenicity of single-dose live oral cholera vaccine CVD 103-HgR in 5-9-year-old Indonesian children. Lancet 340, 689–694 (1992)

    PubMed  CAS  Google Scholar 

  118. Simanjuntak, C.H., et al.: Safety, immunogenicity, and transmissibility of single-dose live oral cholera vaccine strain CVD 103-HgR in 24- to 59-month-old Indonesian children. J. Infect. Dis. 168, 1169–1176 (1993)

    PubMed  CAS  Google Scholar 

  119. Gotuzzo, E., et al.: Safety, immunogenicity, and excretion pattern of single-dose live oral cholera vaccine CVD 103-HgR in Peruvian adults of high and low socioeconomic levels. Infect. Immun. 61, 3994–3997 (1993)

    PubMed  CAS  Google Scholar 

  120. Su-Arehawaratana, P., et al.: Safety and immunogenicity of different immunization regimens of CVD 103-HgR live oral cholera vaccine in soldiers and civilians in Thailand. J. Infect. Dis. 165, 1042–1048 (1992)

    PubMed  CAS  Google Scholar 

  121. Richie, E.E., et al.: Efficacy trial of single-dose live oral cholera vaccine CVD 103-HgR in North Jakarta, Indonesia, a cholera-endemic area. Vaccine 18, 2399–2410 (2000)

    PubMed  CAS  Google Scholar 

  122. Ali, M., et al.: Herd immunity conferred by killed oral cholera vaccines in Bangladesh: a reanalysis. Lancet 366, 44–49 (2005)

    PubMed  Google Scholar 

  123. Perry, R.T., et al.: A single dose of live oral cholera vaccine CVD 103-HgR is safe and immunogenic in HIV-infected and HIV-noninfected adults in Mali. Bull. World Health Organ. 76, 63–71 (1998)

    PubMed  CAS  Google Scholar 

  124. Shin, S., Desai, S.N., Sah, B.K., Clemens, J.D.: Oral vaccines against cholera. Clin. Infect. Dis. 52, 1343–1349 (2011)

    PubMed  Google Scholar 

  125. Levine, M.M.: Enteric infections and the vaccines to counter them: future directions. Vaccine 24, 3865–3873 (2006)

    PubMed  CAS  Google Scholar 

  126. Calain, P., et al.: Can oral cholera vaccination play a role in controlling a cholera outbreak? Vaccine 22, 2444–2451 (2004)

    PubMed  CAS  Google Scholar 

  127. Garcia, L., et al.: The vaccine candidate Vibrio cholerae 638 is protective against cholera in healthy volunteers. Infect. Immun. 73, 3018–3024 (2005)

    PubMed  CAS  Google Scholar 

  128. Mahalanabis, D., et al.: Randomized placebo controlled human volunteer trial of a live oral cholera vaccine VA1.3 for safety and immune response. Vaccine 27, 4850–4856 (2009)

    PubMed  CAS  Google Scholar 

  129. Ochiai, R.L., et al.: A study of typhoid fever in five Asian countries: disease burden and implications for controls. Bull. World Health Organ. 86, 260–268 (2008)

    PubMed  Google Scholar 

  130. Lin, F.Y., et al.: The epidemiology of typhoid fever in the Dong Thap Province. Mekong Delta region of Vietnam. Am. J. Trop. Med. Hyg. 62, 644–648 (2000)

    PubMed  CAS  Google Scholar 

  131. Sinha, A., et al.: Typhoid fever in children aged less than 5 years. Lancet 354, 734–737 (1999)

    PubMed  CAS  Google Scholar 

  132. Brooks, W.A., et al.: Bacteremic typhoid fever in children in an urban slum, Bangladesh. Emerg. Infect. Dis. 11, 326–329 (2005)

    PubMed  Google Scholar 

  133. Connor, B.A., Schwartz, E.: Typhoid and paratyphoid fever in travellers. Lancet Infect. Dis. 5, 623–628 (2005)

    PubMed  Google Scholar 

  134. Charles, R.C., et al.: Characterization of anti-Salmonella enterica serotype Typhi antibody responses in bacteremic Bangladeshi patients using Immuno-affinity Proteomic-based Technology (IPT). Clin. Vaccine Immunol. 17, 1188–1195 (2010)

    PubMed  CAS  Google Scholar 

  135. Ortiz, V., Isibasi, A., Garcia Ortigoza, E., Kumate, J.: Immunoblot detection of class-specific humoral immune response to outer membrane proteins isolated from Salmonella typhi in humans with typhoid fever. J. Clin. Microbiol. 27, 1640–1645 (1989)

    PubMed  CAS  Google Scholar 

  136. Sheikh, A., et al.: Salmonella enterica serovar Typhi-specific immunoglobulin A antibody responses in plasma and antibody in lymphocyte supernatant specimens in Bangladeshi patients with suspected typhoid fever. Clin. Vaccine Immunol. 16, 1587–1594 (2009)

    PubMed  CAS  Google Scholar 

  137. Lanata, C.F., et al.: Vi serology in detection of chronic Salmonella typhi carriers in an endemic area. Lancet 2, 441–443 (1983)

    PubMed  CAS  Google Scholar 

  138. Losonsky, G.A., et al.: Development and evaluation of an enzyme-linked immunosorbent assay for serum Vi antibodies for detection of chronic Salmonella typhi carriers. J. Clin. Microbiol. 25, 2266–2269 (1987)

    PubMed  CAS  Google Scholar 

  139. Mirza, N.B., Wamola, I.A., Estambale, B.A., Mbithi, E., Poillet, M.: Typhim Vi vaccine against typhoid fever: a clinical trial in Kenya. East Afr. Med. J. 72, 162–164 (1995)

    PubMed  CAS  Google Scholar 

  140. Murphy, J.R., et al.: Characteristics of humoral and cellular immunity to Salmonella typhi in residents of typhoid-endemic and typhoid-free regions. J. Infect. Dis. 156, 1005–1009 (1987)

    PubMed  CAS  Google Scholar 

  141. Butler, T., Ho, M., Acharya, G., Tiwari, M., Gallati, H.: Interleukin-6, gamma interferon, and tumor necrosis factor receptors in typhoid fever related to outcome of antimicrobial therapy. Antimicrob. Agents Chemother. 37, 2418–2421 (1993)

    PubMed  CAS  Google Scholar 

  142. Levine, M.M., et al.: Progress in vaccines to prevent typhoid fever. Rev. Infect. Dis. 11, S552–S567 (1989)

    PubMed  Google Scholar 

  143. Black, R.E., et al.: Efficacy of one or two doses of Ty21a Salmonella typhi vaccine in enteric-coated capsules in a controlled field trial. Chilean Typhoid Committee. Vaccine 8, 81–84 (1990)

    PubMed  CAS  Google Scholar 

  144. Levine, M.M., Ferreccio, C., Cryz, S., Ortiz, E.: Comparison of enteric-coated capsules and liquid formulation of Ty21a typhoid vaccine in randomised controlled field trial. Lancet 336, 891–894 (1990)

    PubMed  CAS  Google Scholar 

  145. Wahdan, M.H., Serie, C., Cerisier, Y., Sallam, S., Germanier, R.: A controlled field trial of live Salmonella Typhi strain Ty 21a oral vaccine against typhoid: three-year results. J. Infect. Dis. 145, 292–295 (1982)

    PubMed  CAS  Google Scholar 

  146. Simanjuntak, C., et al.: Oral immunisation against typhoid fever in Indonesia with Ty21a vaccine. Lancet 338, 1055–1059 (1991)

    PubMed  CAS  Google Scholar 

  147. Levine, M.M., Ferreccio, C., Black, R.E., Germanier, R.: Large-scale field trial of Ty21a live oral typhoid vaccine in enteric-coated capsule formulation. Lancet 1, 1049–1052 (1987)

    PubMed  CAS  Google Scholar 

  148. Levine, M.M., et al.: Duration of efficacy of Ty21a, attenuated Salmonella Typhi live oral vaccine. Vaccine 17(Suppl 2), S22–S27 (1999)

    PubMed  Google Scholar 

  149. Ferreccio, C., Levine, M.M., Rodriguez, H., Contreras, R.: Comparative efficacy of two, three, or four doses of TY21a live oral typhoid vaccine in enteric-coated capsules: a field trial in an endemic area. J. Infect. Dis. 159, 766–769 (1989)

    PubMed  CAS  Google Scholar 

  150. Black, R., et al.: Immunogenicity of Ty21a attenuated Salmonella Typhi given with sodium bicarbonate or in enteric-coated capsules. Dev. Biol. Stand. 53, 9–14 (1983)

    PubMed  CAS  Google Scholar 

  151. Kantele, A.: Antibody-secreting cells in the evaluation of the immunogenicity of an oral vaccine. Vaccine 8, 321–326 (1990)

    PubMed  CAS  Google Scholar 

  152. D’Amelio, R., et al.: Comparative analysis of immunological responses to oral (Ty21a) and parenteral (TAB) typhoid vaccines. Infect. Immun. 56, 2731–2735 (1988)

    PubMed  Google Scholar 

  153. Tagliabue, A., et al.: Cellular immunity against Salmonella Typhi after live oral vaccine. Clin. Exp. Immunol. 62, 242–247 (1985)

    PubMed  CAS  Google Scholar 

  154. Salerno-Goncalves, R., Fernandez-Vina, M., Lewinsohn, D.M., Sztein, M.B.: Identification of a human HLA-E-restricted CD8+ T cell subset in volunteers immunized with Salmonella enterica serovar Typhi strain Ty21a typhoid vaccine. J. Immunol. 173, 5852–5862 (2004)

    PubMed  CAS  Google Scholar 

  155. Salerno-Goncalves, R., Pasetti, M.F., Sztein, M.B.: Characterization of CD8+ effector T cell responses in volunteers immunized with Salmonella enterica serovar Typhi strain Ty21a typhoid vaccine. J. Immunol. 169, 2196–2203 (2002)

    PubMed  CAS  Google Scholar 

  156. Sztein, M.B.: Cell-mediated immunity and antibody responses elicited by attenuated Salmonella enterica Serovar Typhi strains used as live oral vaccines in humans. Clin. Infect. Dis. 45(Suppl 1), S15–S19 (2007)

    PubMed  CAS  Google Scholar 

  157. Salerno-Goncalves, R., Wahid, R., Sztein, M.B.: Ex Vivo kinetics of early and long-term multifunctional human leukocyte antigen E-specific CD8+ cells in volunteers immunized with the Ty21a typhoid vaccine. Clin. Vaccine Immunol. 17, 1305–1314 (2010)

    PubMed  CAS  Google Scholar 

  158. Salerno-Goncalves, R., Wahid, R., Sztein, M.B.: Immunization of volunteers with Salmonella enterica serovar Typhi strain Ty21a elicits the oligoclonal expansion of CD8+ T cells with predominant Vbeta repertoires. Infect. Immun. 73, 3521–3530 (2005)

    PubMed  CAS  Google Scholar 

  159. Czerkinsky, C., Holmgren, J.: Enteric vaccines for the developing world: a challenge for mucosal immunology. Mucosal Immunol. 2, 284–287 (2009)

    PubMed  CAS  Google Scholar 

  160. Holmgren, J., Svennerholm, A.M.: Vaccines against mucosal infections. Curr. Opin. Immunol. 24, 343–353 (2012)

    PubMed  CAS  Google Scholar 

  161. Patel, M., et al.: Oral rotavirus vaccines: how well will they work where they are needed most? J. Infect. Dis. 200(Suppl 1), S39–S48 (2009)

    PubMed  Google Scholar 

  162. Qadri, F., Bhuiyan, T.R., Sack, D.A., Svennerholm, A.M.: Immune responses and protection in children in developing countries induced by oral vaccines. Vaccine 31, 452–460 (2012)

    PubMed  Google Scholar 

  163. Cooper, P.J., et al.: Albendazole treatment of children with ascariasis enhances the vibriocidal antibody response to the live attenuated oral cholera vaccine CVD 103-HgR. J. Infect. Dis. 182, 1199–1206 (2000)

    PubMed  CAS  Google Scholar 

  164. Lagos, R., 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, 1709–1712 (1999)

    PubMed  CAS  Google Scholar 

  165. Albert, M.J., et al.: Supplementation with zinc, but not vitamin A, improves seroconversion to vibriocidal antibody in children given an oral cholera vaccine. J. Infect. Dis. 187, 909–913 (2003)

    PubMed  CAS  Google Scholar 

  166. Ahmed, T., Svennerholm, A.M., Al, T.A., Sultana, G.N., Qadri, F.: Enhanced immunogenicity of an oral inactivated cholera vaccine in infants in Bangladesh obtained by zinc supplementation and by temporary withholding breast-feeding. Vaccine 27, 1433–1439 (2009)

    PubMed  CAS  Google Scholar 

  167. 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, 310–312 (1995)

    PubMed  CAS  Google Scholar 

  168. Waggie, Z., et al.: Randomized trial of type 1 and type 3 oral monovalent poliovirus vaccines in newborns in Africa. J. Infect. Dis. 205, 228–236 (2012)

    PubMed  CAS  Google Scholar 

  169. Patel, M., Steele, A.D., Parashar, U.D.: Influence of oral polio vaccines on performance of the monovalent and pentavalent rotavirus vaccines. Vaccine 30(Suppl 1), A30–A35 (2012)

    PubMed  CAS  Google Scholar 

  170. Kau, A.L., Ahern, P.P., Griffin, N.W., Goodman, A.L., Gordon, J.I.: Human nutrition, the gut microbiome and the immune system. Nature 474, 327–336 (2011)

    PubMed  CAS  Google Scholar 

  171. Gerson, C.D., Kent, T.H., Saha, J.R., Siddiqi, N., Lindenbaum, J.: Recovery of small-intestinal structure and function after residence in the tropics. II. Studies in Indians and Pakistanis living in New York City. Ann. Intern. Med. 75, 41–48 (1971)

    PubMed  CAS  Google Scholar 

  172. Levine, M.M.: Immunogenicity and efficacy of oral vaccines in developing countries: lessons from a live cholera vaccine. BMC Biol. 8, 129 (2010)

    PubMed  Google Scholar 

  173. Black, R.E., et al.: Maternal and child undernutrition: global and regional exposures and health consequences. Lancet 371, 243–260 (2008)

    PubMed  Google Scholar 

  174. Overbeck, S., Rink, L., Haase, H.: Modulating the immune response by oral zinc supplementation: a single approach for multiple diseases. Arch. Immunol. Ther. Exp. (Warsz.) 56, 15–30 (2008)

    CAS  Google Scholar 

  175. Kaufman, D.R., et al.: Vitamin A deficiency impairs vaccine-elicited gastrointestinal immunity. J. Immunol. 187, 1877–1883 (2011)

    PubMed  CAS  Google Scholar 

  176. Semba, R.D., et al.: Depressed immune response to tetanus in children with vitamin A deficiency. J. Nutr. 122, 101–107 (1992)

    PubMed  CAS  Google Scholar 

  177. Qadri, F., et al.: Suppressive effect of zinc on antibody response to cholera toxin in children given the killed, B subunit-whole cell, oral cholera vaccine. Vaccine 22, 416–421 (2004)

    PubMed  CAS  Google Scholar 

  178. Newton, S., et al.: Vitamin a supplementation does not affect infants’ immune responses to polio and tetanus vaccines. J. Nutr. 135, 2669–2673 (2005)

    PubMed  CAS  Google Scholar 

  179. Bahl, R., et al.: Effect of vitamin A administered at Expanded Program on Immunization contacts on antibody response to oral polio vaccine. Eur. J. Clin. Nutr. 56, 321–325 (2002)

    PubMed  CAS  Google Scholar 

  180. Semba, R.D., et al.: Integration of vitamin A supplementation with the expanded program on immunization does not affect seroconversion to oral poliovirus vaccine in infants. J. Nutr. 129, 2203–2205 (1999)

    PubMed  CAS  Google Scholar 

  181. Walker, A.: Breast milk as the gold standard for protective nutrients. J. Pediatr. 156, S3–S7 (2010)

    PubMed  CAS  Google Scholar 

  182. Newburg, D.S., et al.: Role of human-milk lactadherin in protection against symptomatic rotavirus infection. Lancet 351, 1160–1164 (1998)

    PubMed  CAS  Google Scholar 

  183. Goveia, M.G., DiNubile, M.J., Dallas, M.J., Heaton, P.M., Kuter, B.J.: Efficacy of pentavalent human-bovine (WC3) reassortant rotavirus vaccine based on breastfeeding frequency. Pediatr. Infect. Dis. J. 27, 656–658 (2008)

    PubMed  Google Scholar 

  184. Moon, S.S., et al.: Inhibitory effect of breast milk on infectivity of live oral rotavirus vaccines. Pediatr. Infect. Dis. J. 29, 919–923 (2010)

    PubMed  Google Scholar 

  185. Yatsunenko, T., et al.: Human gut microbiome viewed across age and geography. Nature 486, 222–227 (2012)

    PubMed  CAS  Google Scholar 

  186. Turnbaugh, P.J., et al.: A core gut microbiome in obese and lean twins. Nature 457, 480–484 (2009)

    PubMed  CAS  Google Scholar 

  187. Bjorksten, B.: Diverse microbial exposure - consequences for vaccine development. Vaccine 30, 4336–4340 (2012)

    PubMed  Google Scholar 

  188. Sartono, E., et al.: Oral polio vaccine influences the immune response to BCG vaccination. A natural experiment. PLoS One 5, e10328 (2010)

    PubMed  Google Scholar 

  189. Kirkpatrick, B.D., et al.: The novel oral typhoid vaccine M01ZH09 is well tolerated and highly immunogenic in 2 vaccine presentations. J. Infect. Dis. 192, 360–366 (2005)

    PubMed  CAS  Google Scholar 

  190. Kirkpatrick, B.D., et al.: Evaluation of Salmonella enterica serovar Typhi (Ty2 aroC-ssaV-) M01ZH09, with a defined mutation in the Salmonella pathogenicity island 2, as a live, oral typhoid vaccine in human volunteers. Vaccine 24, 116–123 (2006)

    PubMed  CAS  Google Scholar 

  191. Lyon, C.E., et al.: In a randomized, double-blinded, placebo-controlled trial, the single oral dose typhoid vaccine, M01ZH09, is safe and immunogenic at doses up to 1.7 x 10(10) colony-forming units. Vaccine 28, 3602–3608 (2010)

    PubMed  CAS  Google Scholar 

  192. Tran, T.H., et al.: A randomised trial evaluating the safety and immunogenicity of the novel single oral dose typhoid vaccine M01ZH09 in healthy Vietnamese children. PLoS One 5, e11778 (2010)

    PubMed  Google Scholar 

  193. Puzzling diversity of rotaviruses. Lancet 335, 573–575 (1990)

    Google Scholar 

  194. Tacket, C.O., Levine, M.M.: CVD 908, CVD 908-htrA, and CVD 909 live oral typhoid vaccines: a logical progression. Clin. Infect. Dis. 45(Suppl 1), S20–S23 (2007)

    PubMed  CAS  Google Scholar 

  195. Levine, M.M., Kotloff, K.L., Barry, E.M., Pasetti, M.F., Sztein, M.B.: Clinical trials of Shigella vaccines: two steps forward and one step back on a long, hard road. Nat. Rev. Microbiol. 5, 540–553 (2007)

    PubMed  CAS  Google Scholar 

  196. McKenzie, R., et al.: Safety and immunogenicity of an oral, inactivated, whole-cell vaccine for Shigella sonnei: preclinical studies and a Phase I trial. Vaccine 24, 3735–3745 (2006)

    PubMed  CAS  Google Scholar 

  197. Mel, D.M., Terzin, A.L., Vuksic, L.: Studies on vaccination against bacillary dysentery. 3. Effective oral immunization against Shigella flexneri 2a in a field trial. Bull. World. Health Organ. 32, 647–655 (1965)

    PubMed  CAS  Google Scholar 

  198. Porter, C.K., Thura, N., Ranallo, R.T., Riddle, M.S.: The Shigella human challenge model. Epidemiol. Infect. 141, 223–232 (2013). doi:10.1017/S0950268812001677

    CAS  Google Scholar 

  199. Barzu, S., Fontaine, A., Sansonetti, P., Phalipon, A.: Induction of a local anti-IpaC antibody response in mice by use of a Shigella flexneri 2a vaccine candidate: implications for use of IpaC as a protein carrier. Infect. Immun. 64, 1190–1196 (1996)

    PubMed  CAS  Google Scholar 

  200. Coster, T.S., et al.: Vaccination against shigellosis with attenuated Shigella flexneri 2a strain SC602. Infect. Immun. 67, 3437–3443 (1999)

    PubMed  CAS  Google Scholar 

  201. Rahman, K.M., et al.: Safety, dose, immunogenicity, and transmissibility of an oral live attenuated Shigella flexneri 2a vaccine candidate (SC602) among healthy adults and school children in Matlab, Bangladesh. Vaccine 29, 1347–1354 (2011)

    PubMed  CAS  Google Scholar 

  202. Harro, C., et al.: A combination vaccine consisting of three live attenuated enterotoxigenic Escherichia coli strains expressing a range of colonization factors and heat-labile toxin subunit B is well tolerated and immunogenic in a placebo-controlled double-blind phase I trial in healthy adults. Clin. Vaccine Immunol. 18, 2118–2127 (2011)

    PubMed  CAS  Google Scholar 

  203. Darsley, M.J., et al.: The oral, live attenuated enterotoxigenic Escherichia coli vaccine ACE527 reduces the incidence and severity of diarrhea in a human challenge model of diarrheal disease. Clin. Vaccine Immunol. 19, 1921–1931 (2012)

    PubMed  CAS  Google Scholar 

  204. Tacket, C.O., Sztein, M.B., Losonsky, G.A., Wasserman, S.S., Estes, M.K.: Humoral, mucosal, and cellular immune responses to oral Norwalk virus-like particles in volunteers. Clin. Immunol. 108, 241–247 (2003)

    PubMed  CAS  Google Scholar 

  205. el-Kamary, S.S., et al.: Adjuvanted intranasal Norwalk virus-like particle vaccine elicits antibodies and antibody-secreting cells that express homing receptors for mucosal and peripheral lymphoid tissues. J. Infect. Dis. 202, 1649–1658 (2010)

    PubMed  CAS  Google Scholar 

  206. Atmar, R.L., et al.: Norovirus vaccine against experimental human Norwalk Virus illness. N. Engl. J. Med. 365, 2178–2187 (2011)

    PubMed  CAS  Google Scholar 

  207. Herbst-Kralovetz, M., Mason, H.S., Chen, Q.: Norwalk virus-like particles as vaccines. Expert Rev. Vaccines 9, 299–307 (2010)

    PubMed  CAS  Google Scholar 

  208. Tan, M., Jiang, X.: Norovirus P particle: a subviral nanoparticle for vaccine development against norovirus, rotavirus and influenza virus. Nanomedicine (Lond.) 7, 889–897 (2012)

    CAS  Google Scholar 

  209. Norton, E.B., Lawson, L.B., Freytag, L.C., Clements, J.D.: Characterization of a mutant Escherichia coli heat-labile toxin, LT(R192G/L211A), as a safe and effective oral adjuvant. Clin. Vaccine Immunol. 18, 546–551 (2011)

    PubMed  CAS  Google Scholar 

  210. Brandtzaeg, P.: Food allergy: separating the science from the mythology. Nat. Rev. Gastroenterol. Hepatol. 7, 380–400 (2010)

    PubMed  CAS  Google Scholar 

  211. Lewis, D.J., et al.: Transient facial nerve paralysis (Bell’s palsy) following intranasal delivery of a genetically detoxified mutant of Escherichia coli heat labile toxin. PLoS One 4, e6999 (2009)

    PubMed  Google Scholar 

  212. Woodland, D.L.: Jump-starting the immune system: prime-boosting comes of age. Trends Immunol. 25, 98–104 (2004)

    PubMed  CAS  Google Scholar 

  213. Galen, J.E., et al.: Mucosal immunization with attenuated Salmonella enterica serovar Typhi expressing protective antigen of anthrax toxin (PA83) primes monkeys for accelerated serum antibody responses to parenteral PA83 vaccine. J. Infect. Dis. 199, 326–335 (2009)

    PubMed  CAS  Google Scholar 

  214. Azevedo, M.S., et al.: An oral versus intranasal prime/boost regimen using attenuated human rotavirus or VP2 and VP6 virus-like particles with immunostimulating complexes influences protection and antibody-secreting cell responses to rotavirus in a neonatal gnotobiotic pig model. Clin. Vaccine Immunol. 17, 420–428 (2010)

    PubMed  CAS  Google Scholar 

  215. Schoub, B.D., Mphahlele, M.J., Ngcobo, N.J., Hoosen, A.A., Meheus, A.: Introducing new vaccines into the South African national immunisation programme - a case study. Vaccine 30(Suppl 3), C1–C2 (2012)

    PubMed  Google Scholar 

  216. Cohen, D., et al.: Double-blind vaccine-controlled randomised efficacy trial of an investigational Shigella sonnei conjugate vaccine in young adults. Lancet 349, 155–159 (1997)

    PubMed  CAS  Google Scholar 

  217. Pavot, V., Rochereau, N., Genin, C., Verrier, B., Paul, S.: New insights in mucosal vaccine development. Vaccine 30, 142–154 (2012)

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Emily DeBoy for contributing to the design and construction of Fig. 3.1.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marcela F. Pasetti PhD .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Wien

About this chapter

Cite this chapter

Tennant, S.M., Muhsen, K., Pasetti, M.F. (2013). Gut Immunology and Oral Vaccination. In: Giese, M. (eds) Molecular Vaccines. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1419-3_3

Download citation

Publish with us

Policies and ethics