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Mucosal Vaccines for Enteric Bacterial Pathogens

  • Paolo PasqualiEmail author
Chapter

Abstract

Vaccination can be considered one of the most beneficial intervention to control infectious diseases in the history of mankind. In recent years, an intense interest has raised upon the development of novel vaccination approaches, especially against enteric pathogens. The interest has been fueled by knowledge of the molecular bases of pathogenesis of infectious diseases and by information regarding the biology of pathogens and their intimate relationship with the host. The use of attenuated bacteria in vaccine formulations has significant advantages compared to that of inactivated whole microbes, because by inducing a mild and limited infection they stimulate a robust and protective immune response. In addition, being able to naturally colonize the host, they can be used for mucosal delivery. Over the past few years, the possibility to induce oral immunization has been considered an attractive strategy which opened a new area of exploration. The development of vaccine against enteric pathogens is a challenging opportunity because a large number of bacterial pathogens exploit mucosal surface to penetrate and survive into the host. This chapter is aiming to make an overview of the progresses in the understanding of the interaction between host and enteric pathogens and in the development of the mucosal vaccines for human bacterial enteric diseases with an important impact on public health.

Keywords

Mucosal vaccines Bacterial infections Mucosal immunity 

References

  1. Ammendola S, Pasquali P, Pistoia C, Petrucci P, Petrarca P, Rotilio G, Battistoni A (2007) The high affinity Zn2+ uptake system ZnuABC is required for bacterial zinc homeostasis in intracellular environments and contributes to virulence of Salmonella enteric. Infect Immun 75:5867–5876PubMedCrossRefGoogle Scholar
  2. Anh DD, Canh DG, Lopez AL, Thiem VD, Long PT, Son NH, Deen J, von Seidlein L, Carbis R, Han SH, Shin SH, Attridge S, Holmgren J, Clemens J (2007) Safety and immunogenicity of a reformulated Vietnamese bivalent killed, whole-cell, oral cholera vaccine in adults. Vaccine 25:1149–1155PubMedCrossRefGoogle Scholar
  3. Arumugam M, Raes J, Pelletier E, LePaslier D, Yamada T, Mende DR, Fernandes GR, Tap J, Bruls T, Batto JM, Bertalan M, Borruel N, Casellas F, Fernandez L, Gautier L, Hansen T, Hattori M, Hayashi T, Kleerebezem M, Kurokawa K, Leclerc M, Levenez F, Manichanh C, Nielsen HB, Nielsen T, Pons N, Poulain J, Qin J, Sicheritz-Ponten T, Tims S, Torrents D, Ugarte E, Zoe-tendal EG, Wang J, Guarner F, Pedersen O, DeVos WM, Brunak S, Dore J, Consorti M, Weissenbach J, Ehrlich SD, Bork P, Antolin M, Artiguenave F, Blottiere HM, Almeida M, Brechot C, Cara C, Chervaux C, Cultrone A, Delorme C, Denariaz G, Dervyn R, Foerstner KU, Friss C, Van DeGuchte M, Guedon E, Haimet F, Huber W, Van Hylckama-Vlieg J, Jamet A, Juste C, Kaci G, Knol J, Lakhdari O, Layec S, LeRoux K, Maguin E, Merieux A, MeloMinardi R, M’Rini C, Muller J, Oozeer R, Parkhill J, Renault P, Rescigno M, Sanchez N, Sunagawa S, Torrejon A, Turner K, Vandemeulebrouck G, Varela E, Winogradsky Y, Zeller G (2011) Enterotypes of the human gut microbiome. Nature 43:174–180CrossRefGoogle Scholar
  4. Belkaid Y, Rouse BT (2005) Natural regulatory T cells in infectious disease. Nat Immunol 6:353–360PubMedCrossRefGoogle Scholar
  5. Bishop AL, Camilli A (2011) Vibrio cholerae: lessons for mucosal vaccine design. Expert Rev Vaccines 10:79–94PubMedCrossRefGoogle Scholar
  6. Blaschitz C, Raffatellu M (2010) Th17 cytokines and the gut mucosal barrier. J Clin Immunol 30:196–203PubMedCrossRefGoogle Scholar
  7. Brandtzaeg P (2007) Induction of secretory immunity and memory at mucosal surfaces. Vaccine 25:5467–5484PubMedCrossRefGoogle Scholar
  8. Brandtzaeg P (2010) Food allergy: separating the science from the mythology. Nat Rev Gastroenterol Hepatol 7:380–400PubMedCrossRefGoogle Scholar
  9. Calain P, Chaine JP, Johnson E, Hawley ML, O’Leary MJ, Oshitani H, Chaignat CL (2004) Can oral cholera vaccination play a role in controlling a cholera outbreak? Vaccine 22:2444–2451PubMedCrossRefGoogle Scholar
  10. Caprioli A, Morabito S, Brugère H, Oswald E (2005) Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res 36:289–311PubMedCrossRefGoogle Scholar
  11. Cash RA, Music SI, Libonati JP, Craig JP, Pierce NF, Hornick RB (1974) Response of man to infection with Vibrio cholerae. II. Protection from illness afforded by previous disease and vaccine. J Infect Dis 130:325–333PubMedCrossRefGoogle Scholar
  12. Cerutti A (2008) The regulation of IgA class switching. Nat Rev Immunol 8:421–434PubMedCrossRefGoogle Scholar
  13. Chen Y, Chou K, Fuchs E, Havran WL, Boismenu R (2002) Protection of the intestinal mucosa by intraepithelial γ δ T cells. Proc Natl Acad Sci USA 99:14338–14343PubMedCrossRefGoogle Scholar
  14. Clemens JD, Sack DA, Harris JR, Van Loon F, Chakraborty J, Ahmed F, Rao MR, Khan MR, Yunus M, Huda N, Stanton BF, Kay BA, Eeckels R, Clemens JD, Rao MR, Kay BA, Sack DA, Harris JR, Stanton BF, Walter S, Eeckels R, Svennerholm A-M, Holmgren J (1990) Field trial of oral cholera vaccines in Bangladesh: results from three-year follow-up. Lancet 335:270–273PubMedCrossRefGoogle Scholar
  15. Clemens JD, Sack DA, Ivanoff B (2001) Misleading negative findings in a field trial of killed, oral cholera vaccine in Peru. J Infect Dis 183:1306–1309PubMedCrossRefGoogle Scholar
  16. Cohen MB, Giannella RA, Bean J, Taylor DN, Parker S, Hoeper A, Wowk S, Hawkins J, Kochi SK, Schiff G, Killeen KP (2002) Randomized, controlled human challenge study of the safety, immunogenicity, and protective efficacy of a single dose of Peru-15, a live attenuated oral cholera vaccine. Infect Immun 70:1965–1970PubMedCrossRefGoogle Scholar
  17. Daley A, Randall R, Darsley M, Choudhry N, Thomas N, Sanderson IR, Croft NM, Kelly P (2007) Genetically modified enterotoxigenic Escherichia colivaccines induce mucosal immune responses without inflammation. Gut 56:1550–1556PubMedCrossRefGoogle Scholar
  18. De Calisto J, Villablanca EJ, Wang S, Bono MR, Rosemblatt M, Mora JR (2012) T-cell homing to the gut mucosa: general concepts and methodological considerations. Methods Mol Biol 757:411–434PubMedCrossRefGoogle Scholar
  19. Dougan G, John V, Palmer S, Mastroeni P (2011) Immunity to salmonellosis. Immunol Rev 240:196–210PubMedCrossRefGoogle Scholar
  20. Eberl G (2010) A new vision of immunity: homeostasis of the superorganism. Mucosal Immunol 3:450–460PubMedCrossRefGoogle Scholar
  21. Faria AM, Weiner HL (2005) Oral tolerance. Immunol Rev 206:232–259PubMedCrossRefGoogle Scholar
  22. Finkelstein RA (1962) Vibriocidal antibody inhibition (VAI) analysis: a technique for the identification of the predominant vibriocidal antibodies in serum and for the detection and identification of Vibrio cholerae antigens. J Immunol 89:264–271Google Scholar
  23. Fraser A, Paul M, Goldberg E, Acosta CJ, Leibovici L (2007) Typhoid fever vaccines: systematic review and meta-analysis of randomised controlled trials. Vaccine 25:7848–7857PubMedCrossRefGoogle Scholar
  24. Gaastra W, Svennerholm AM (1996) Colonization factors of human enterotoxigenic Escherichia coli (ETEC). Trends Microbiol 4:444–452PubMedCrossRefGoogle Scholar
  25. Gaboriau-Routhiau V, Rakotobe S, Lecuyer E, Mulder I, Lan A, Bridonneau C, Rochet V, Pisi A, De Paepe M, Brandi G, Eberl G, Snel J, Kelly D, Cerf-Bensussan N (2009) The keyrole of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31:677–689PubMedCrossRefGoogle Scholar
  26. García L, Jidy MD, García H, Rodríguez BL, Fernández R, Año G, Cedré B, Valmaseda T, Suzarte E, Ramírez M, Pino Y, Campos J, Menéndez J, Valera R, González D, González I, Pérez O, Serrano T, Lastre M, Miralles F, Del Campo J, Maestre JL, Pérez JL, Talavera A, Pérez A, Marrero K, Ledón T, Fando R (2005) The vaccine candidate Vibrio cholerae 638 is protective against cholera in healthy volunteers. Infect Immun 73:3018–3024PubMedCrossRefGoogle Scholar
  27. Girard MP, Steele D, Chaignat CL, Kieny MP (2006) A review of vaccine research and development: human enteric infections. Vaccine 24:2732–2750PubMedCrossRefGoogle Scholar
  28. Great Britain Medical Research Council (1956) BCG and whole bacillus vaccines in the prevention of tuberculosis in adolescence and early life. Br Med J 1:413–466CrossRefGoogle Scholar
  29. Holmgren J, Czerkinsky C (2005) Mucosal immunity and vaccines. Nat Med 11:S45–S53PubMedCrossRefGoogle Scholar
  30. Ismail AS, Behrendt CL, Hooper LV (2009) Reciprocal interactions between commensal bacteria and γδ intraepithelial lymphocytes during mucosal injury. J Immunol 182:3047–3054PubMedCrossRefGoogle Scholar
  31. Ismail AS, Severson KM, Vaishnava S, Behrendt CL, Yu X, Benjamin JL, Ruhn KA, Hou B, DeFranco AL, Yarovinsky F, Hooper Lora V (2011) γδ intraepithelial lymphocytes are essential mediators of host-microbial homeostasis at the intestinal mucosal surface. Proc Natl Acad Sci USA 108:8743–8748PubMedCrossRefGoogle Scholar
  32. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, Tanoue T, Imaoka A, Itoh K, Takeda K, Umesaki Y, Honda K, Littman DR (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139:485–498PubMedCrossRefGoogle Scholar
  33. Kosiewicz MM, Zirnheld A, Alard P (2011) Gut microbiota, immunity, and disease: a complex relationship. Front Microbiol 2:1–11Google Scholar
  34. Kotloff KL, Nataro JP, Losonsky GA, Wasserman SS, Hale TL, Taylor DN, Sadoff JC, Levine MM (1995) A modified Shigella volunteer challenge model in which the inoculum is administered with bicarbonate buffer: clinical experience and implications for Shigella infectivity. Vaccine 13:1488–1494PubMedCrossRefGoogle Scholar
  35. Lavelle EC, O’Hagan DT (2006) Delivery systems and adjuvants for oral vaccines. Expert Opin Drug Deliv 3:747–762PubMedCrossRefGoogle Scholar
  36. Lee SH, Hava DL, Waldor MK, Camilli A (1999) Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection. Cell 99:625–634PubMedCrossRefGoogle Scholar
  37. Lehner MD, Hartung T (2002) Endotoxin tolerance mechanisms and beneficial effects in bacterial infection. Rev Physiol Biochem Pharmacol 144:95–141PubMedCrossRefGoogle Scholar
  38. Levine MM, Kotloff KL, Barry EM, Pasetti MF, Sztein MB (2007) Clinical trials of Shigella vaccines: two steps forward and one step back on a long, hard road. Nat Rev Microbiol 5:540–553PubMedCrossRefGoogle Scholar
  39. Liang W, Wang S, Yu F, Zhang L, Qi G, Liu Y, Gao S, Kan B (2003) Construction and evaluation of a safe, live, oral Vibrio cholerae vaccine candidate, IEM108. Infect Immun 71:5498–5504PubMedCrossRefGoogle Scholar
  40. Lindow JC, Fimlaid KA, Bunn JY, Kirkpatrick BD (2011) Antibodies in action: role of human opsonins in killing Salmonella enterica Serovar Typhi. Infect Immun 79:3188–3194PubMedCrossRefGoogle Scholar
  41. Lonnroth I, Holmgren J (1973) Subunit structure of cholera toxin. J Gen Microbiol 76:417–427PubMedCrossRefGoogle Scholar
  42. Lucas MES, Deen JL, von Seidlein L, Wang XY, Ampuero J, Puri M, Ali M, Ansaruzzaman M, Amos J, Macuamule A, Cavailler P, Guerin PJ, Mahoudeau C, Kahozi-Sangwa P, Chaignat CL, Barreto A, Songane FF, Clemens JD (2005) Effectiveness of mass oral cholera vaccination in Beira, Mozambique. N Engl J Med 352:757–767PubMedCrossRefGoogle Scholar
  43. Mahalanabis D, Lopez AL, Sur D, Manna B, Kanungo S, von Seidlein L, Carbis R, Han SH, Shin SH, Attridge S, Rao R, Holmgren J, Clemens J, Bhattacharya SK (2008) 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:e2323PubMedCrossRefGoogle Scholar
  44. Mahalanabis D, Ramamurthy T, Nair GB, Ghosh A, Shaikh S, Sen B, Thungapathra M, Ghosh RK, Pazhani GP, Nandy RK, Jana S, Bhattacharya SK (2009) Randomized placebo controlled human volunteer trial of a live oral cholera vaccine VA1.3 for safety and immune response. Vaccine 27:4850–4856PubMedCrossRefGoogle Scholar
  45. Mantis NJ, Rol N, Corthésy B (2011) Secretory IgA’s complex roles in immunity and mucosal homeostasis in the gut. Mucosal Immunol 4:603–611PubMedCrossRefGoogle Scholar
  46. Masopust D, Vezys V, Wherry EJ, Barber DL, Ahmed R (2006) Cutting edge: gut microenvironment promotes differentiation of a unique memory CD8 T cell population. J Immunol 76:2079–2083Google Scholar
  47. Mastroeni P, Villarreal-Ramos B, Hormaeche CE (1993) Adoptive transfer of immunity to oral challenge with virulent salmonellae in innately susceptible BALB/c mice requires both immune serum and T cells. Infect Immun 61:3981–3984PubMedGoogle Scholar
  48. Mazmanian SK, Round JL, Kasper DL (2008) A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453:620–625PubMedCrossRefGoogle Scholar
  49. Mbow ML, De Gregorio E, Valiante NM, Rappuoli R (2011) New adjuvants for human vaccines. Curr Opin Immunol 22:411–416CrossRefGoogle Scholar
  50. McGuckin MA, Linden SK, Sutton P, Florin TH (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9:265–278PubMedCrossRefGoogle Scholar
  51. McKenzie R, Bourgeois AL, Engstrom F, Hall E, Chang HS, Gomes JG, Kyle JL, Cassels F, Turner AK, Randall R, Darsley M, Lee C, Bedford P, Shimko J, Sack DA (2006) Comparative safety and immunogenicity of two attenuated enterotoxigenic Escherichia coli vaccine strains in healthy adults. Infect Immun 74:994–1000PubMedCrossRefGoogle Scholar
  52. McKenzie R, Darsley M, Thomas N, Randall R, Carpenter C, Forbes E, Finucane M, Sack RB, Hall E, Bourgeois AL (2008) A double-blind, placebo-controlled trial to evaluate the efficacy of PTL-003, an attenuated enterotoxigenic E. coli (ETEC) vaccine strain, in protecting against challenge with virulent ETEC. Vaccine 26:4731–4739PubMedCrossRefGoogle Scholar
  53. Meeusen EN (2011) Exploiting mucosal surfaces for the development of mucosal vaccines. Vaccine 29:8506–8511PubMedCrossRefGoogle Scholar
  54. Mestecky J (1987) The common mucosal immune system and current strategies for induction of immune responses in external secretions. J Clin Immunol 7:265–276PubMedCrossRefGoogle Scholar
  55. Mittrucker HW, Kaufmann SHE (2004) Mini-review: regulatory T cells and infection: suppression revisited. Eur J Immunol 34:306–312PubMedCrossRefGoogle Scholar
  56. Mosley WH, Ahmad S, Benenson AS, Ahmed A (1968) The relationship of vibriocidal antibody titre to susceptibility to cholera in family contacts of cholera patients. Bull World Health Organ 38:777–785PubMedGoogle Scholar
  57. Muller C, Bang IS, Velayudhan J, Karlinsey J, Papenfort K, Vogel J, Fang FC (2009) Acid stress activation of the sigma(E) stress response in Salmonella enterica serovar Typhimurium. Mol Microbiol 71:1228–1238PubMedCrossRefGoogle Scholar
  58. Neoh SH, Rowley D (1970) The antigens of Vibrio cholerae involved in the vibriocidal action of antibody and complement. J Infect Dis 121:505–513PubMedCrossRefGoogle Scholar
  59. Ouellette AJ (2011) Paneth cell a-defensins in enteric innate immunity. Cell Mol Life Sci 68:2215–2229PubMedCrossRefGoogle Scholar
  60. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, Churcher C, Mungall KL, Bentley SD, Holden MT, Sebaihia M, Baker S, Basham D, Brooks K, Chillingworth T, Connerton P, Cronin A, Davis P, Davies RM, Dowd L, White N, Farrar J, Feltwell T, Hamlin N, Haque A, Hien TT, Holroyd S, Jagels K, Krogh A, Larsen TS, Leather S, Moule S, O’Gaora P, Parry C, Quail M, Rutherford K, Simmonds M, Skelton J, Stevens K, Whitehead S, Barrell BG (2001) Complete genome sequence of a multiple drug resistant Salmonella enteric serovar Typhi CT18. Nature 413:848–852PubMedCrossRefGoogle Scholar
  61. Pasetti MF, Levine MM, Sztein MB (2003) Animal models paving the way for clinical trials of attenuated Salmonella enterica serovar Typhi live oral vaccines and live vectors. Vaccine 21:401–418PubMedCrossRefGoogle Scholar
  62. Pasetti MF, Simon JK, Sztein MB, Levine MM (2011) Immunology of gut mucosal vaccines. Immunol Rev 239:125–148PubMedCrossRefGoogle Scholar
  63. Pasquali P, Adone R, Gasbarre LC, Pistoia C, Petrucci P, Ciuchini F (2003) Brucella abortus RB51 induces protection to mice orally infected with virulent strain B.abortus 2308. Infect Immun 71:2326–2330PubMedCrossRefGoogle Scholar
  64. Pasquali P, Ammendola S, Pistoia C, Petrucci P, Tarantino M, Rotilio G, Battistoni A (2008) Atten­uated Salmonella enterica serovar Typhimurium lacking ZnuABC transporter (S.Typhimurium SA 186) confer immune-based protection against challenge infections in mice. Vaccine 26:3421–3426PubMedCrossRefGoogle Scholar
  65. Pesciaroli M, Ammendola S, Pistoia C, Petrucci P, Tarantino M, Battistoni A, Pasquali P (2011) Atten­uated Salmonella enterica serovar Typhimurium lacking ZnuABC transporter (S.Typhimurium SA 186) confers immune-based protection against challenge infections in streptomycin pretreated mice. Vaccine 29:1783–1790PubMedCrossRefGoogle Scholar
  66. Petrarca P, Ammendola S, Pasquali P, Battistoni A (2010) The Zur-regulated ZinT protein is an auxiliary component of the high affinity ZnuABC zinc transporter that facilitates metal recruitment during severe zinc shortage. J Bacteriol 192:1553–1564PubMedCrossRefGoogle Scholar
  67. Podolski DK (2002) Inflammatory bowel disease. N Engl J Med 347:417–429CrossRefGoogle Scholar
  68. Qadri F, Chowdhury MI, Faruque SM, Salam MA, Ahmed T, Begum YA, Saha A, Alam MS, Zaman K, Seidlein LV, Park E, Killeen KP, Mekalanos JJ, Clemens JD, Sack DA, Peru-15 Study Group (2005) Randomized, controlled study of the safety and immunogenicity of Peru-15, a live attenuated oral vaccine candidate for cholera, in adult volunteers in Bangladesh. J Infect Dis 192:573–579PubMedCrossRefGoogle Scholar
  69. Qadri F, Chowdhury MI, Faruque SM, Salam MA, Ahmed T, Begum YA, Saha A, Al Tarique A, Seidlein LV, Park E, Killeen KP, Mekalanos JJ, Clemens JD, Sack DA, PXV Study Group (2007) Peru-15, a live attenuated oral cholera vaccine, is safe and immunogenic in Bangladeshi toddlers and infants. Vaccine 25:231–238PubMedCrossRefGoogle Scholar
  70. Quiding-Järbrink M, Nordström I, Granström G, Kilander A, Jertborn M, Butcher EC, Lazarovits AI, Holmgren J, Czerkinsky C (1997) 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 99:1281–1286PubMedCrossRefGoogle Scholar
  71. Raffatellu M, Wilson RP, Winter SE, Bäumler AJ (2008) Clinical pathogenesis of typhoid fever. J Infect Dev Ctries 2:260–266PubMedGoogle Scholar
  72. Richie EE, Punjabi NH, Sidharta YY, Peetosutan KK, Sukandar MM, Wasserman SS, Lesmana MM, Wangsasaputra FF, Pandam SS, Levine MM, O’Hanley PP, Cryz SJ, Simanjuntak CH (2000) Efficacy trial of single-dose live oral cholera vaccine CVD 103-HgR in North Jakarta, Indonesia, a cholera-endemic area. Vaccine 18:2399–2410PubMedCrossRefGoogle Scholar
  73. Salmi M, Jalkanen S (2005) Lymphocyte homing to the gut: attraction, adhesion, and commitment. Immunol Rev 206:100–113PubMedCrossRefGoogle Scholar
  74. Samandari T, Kotloff KL, Losonsky GA, Picking WD, Sansonetti PJ, Levine MM, Sztein MB (2000) Production of IFN-γ and IL-10 to Shigella invasins by mononuclear cells from volunteers orally inoculated with a shiga toxin-deleted Shigella dysenteriae type 1 strain. J Immunol 164:2221–2232PubMedGoogle Scholar
  75. Sanchez J, Holmgren J (2005) Virulence factors, pathogenesis and vaccine protection in cholera and ETEC diarrhea. Curr Opin Immunol 17:388–398PubMedCrossRefGoogle Scholar
  76. Sanchez JL, Vasquez B, Begue RE, Meza R, Castellares G, Cabezas C, Watts DM, Svennerholm AM, Sadoff JC, Taylor DN (1994) Protective efficacy of oral whole-cell/recombinant-B-subunit cholera vaccine in Peruvian military recruits. Lancet 344:1273–1276PubMedCrossRefGoogle Scholar
  77. Shin S, Desai SN, Sah BK, Clemens JD (2011) Oral vaccines against cholera. Clin Infect Dis 52:1343–1349PubMedCrossRefGoogle Scholar
  78. Soloff AC, Barratt-Boyes SM (2010) Enemy at the gates: dendritic cells and immunity to mucosal pathogens. Cell Res 20:872–885PubMedCrossRefGoogle Scholar
  79. Spangler BD (1992) Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol Rev 56:622–647PubMedGoogle Scholar
  80. Strockbine NA, Maurelli AT (2005) Bergey’s manual of systematic bacteriology. Brenner, New YorkGoogle Scholar
  81. Strugnell RA, Wijburg OL (2010) The role of secretory antibodies in infection immunity. Nat Rev Microbiol 8:656–667PubMedCrossRefGoogle Scholar
  82. Sur D, Lopez AL, Kanungo S, Paisley A, Manna B, Ali M, Niyogi SK, Park JK, Sarkar B, Puri MK, Kim DR, Deen JL, Holmgren J, Carbis R, Rao R, Nguyen TV, Donner A, Ganguly NK, Nair GB, Bhattacharya SK, Clemens JD (2009) Efficacy and safety of a modified killed-whole-cell oral cholera vaccine in India: an interim analysis of a cluster-randomised, double-blind, placebo-controlled trial. Lancet 374:1694–1702PubMedCrossRefGoogle Scholar
  83. Tacket CO, Losonsky G, Nataro JP, Cryz SJ, Edelman R, Kaper JB, Levine MM (1992) Onset and duration of protective immunity in challenged volunteers after vaccination with live oral cholera vaccine CVD 103-HgR. J Infect Dis 166:837–841PubMedCrossRefGoogle Scholar
  84. Tarr PI, Gordon CA, Chandler WL (2005) Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet 365:1073–1086PubMedGoogle Scholar
  85. Taylor DN, Cardenas V, Sanchez JL, Bégué RE, Gilman R, Bautista C, Perez J, Puga R, Gaillour A, Meza R, Echeverria P, Sadoff J (2000) Two-year study of the protective efficacy of the oral whole cell plus recombinant B subunit cholera vaccine in Peru. J Infect Dis 181:1667–1673PubMedCrossRefGoogle Scholar
  86. Thiem VD, Deen JL, von Seidlein L, Canh do G, Anh DD, Park JK, Ali M, Danovaro-Holliday MC, Son ND, Hoa NT, Holmgren J, Clemens JD (2006) Long-term effectiveness against cholera of oral killed whole-cell vaccine produced in Vietnam. Vaccine 24:4297–4303PubMedCrossRefGoogle Scholar
  87. Valera R, García HM, Jidy MD, Mirabal M, Armesto MI, Fando R, García L, Fernández R, Año G, Cedré B, Ramírez M, Bravo L, Serrano T, Palma S, González D, Miralles F, Medina V, Nuñez F, Plasencia Y, Martínez JC, Mandarioti A, Lugones J, Rodríguez BL, Moreno A, González D, Baro M, Solis RL, Sierra G, Barbera R, Domínguez F, Gutiérrez C, Kouri G, Campa C, Menéndez J (2009) Randomized, double-blind, placebo-controlled trial to evaluate the safety and immunogenicity of live oral cholera vaccine 638 in Cuban adults. Vaccine 27:6564–6569PubMedCrossRefGoogle Scholar
  88. World Health Organization (2006) Future directions for research on enterotoxigenic Escherichia coli vaccines for developing countries. Wkly Epidemiol Rec 81:97Google Scholar

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© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Department of Veterinary Public Health and Food SafetyIstituto Superiore di SanitàRomeItaly

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