Current Status and Prospects for a Helicobacter pylori Vaccine

Gastroenterology Clinics of North America

Volumn 44, Issue 3, 2015, Pages 677-689

  Blanchard, Thomas G ^a   Czinn, Steven J ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer; Clinical trials; Helicobacter pylori; Inflammation; Vaccine

Indexed keywords

HELICOBACTER PYLORI VACCINE; INTERLEUKIN 12; BACTERIAL VACCINE;

ANTIBODY RESPONSE; ANTIMICROBIAL THERAPY; BACTERIAL LOAD; BACTERIAL STRAIN; CANCER RISK; CLINICAL TRIAL (TOPIC); DEVELOPING COUNTRY; DRUG EFFICACY; DRUG MEGADOSE; DRUG SAFETY; ERADICATION THERAPY; GASTRIC MUCOSA; HEALTH CARE COST; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOREGULATION; NONHUMAN; PHASE 3 CLINICAL TRIAL (TOPIC); POPULATION RESEARCH; PREVALENCE; REVIEW; STOMACH CANCER; T LYMPHOCYTE; VACCINATION; COMPLICATION; HELICOBACTER INFECTIONS; IMMUNOLOGY; MICROBIOLOGY; STOMACH NEOPLASMS;

BACTERIAL VACCINES; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; STOMACH NEOPLASMS;

EID: 84940451496     PISSN: 08898553     EISSN: 15581942     Source Type: Journal    
DOI: 10.1016/j.gtc.2015.05.013     Document Type: Review

References (84)

1. Chen Y., Blaser M.J. Helicobacter pylori colonization is inversely associated with childhood asthma. J Infect Dis 2008, 198:553-560.
2. Corley D.A., Kubo A., Levin T.R., et al. Helicobacter pylori infection and the risk of Barrett's oesophagus: a community-based study. Gut 2008, 57:727-733.
3. Dellon E.S., Peery A.F., Shaheen N.J., et al. Inverse association of esophageal eosinophilia with Helicobacter pylori based on analysis of a US pathology database. Gastroenterology 2011, 141:1586-1592.
4. Eurogast Study Group An international association between Helicobacter pylori infection and gastric cancer. Lancet 1993, 341:1359-1362.
5. NIH Consensus Conference Helicobacter pylori in peptic ulcer disease. J Am Med Assoc 1994, 272:65-69.
6. Parsonnet J., Friedman G.D., Vandersteen D.P., et al. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 1991, 325:1127-1131.
7. Warren J.R., Marshall B.J. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 1983, 1:1273-1275.
8. World Health Organization Infection with Helicobacter pylori. Schistosomes, liver flukes and Helicobacter pylori 1994, vol. 61:177-241. International Agency for Research on Cancer, Lyon (France).
9. Frenck R.W., Clemens J. Helicobacter in the developing world. Microbes Infect 2003, 5:705-713.
10. Gisbert J.P. The recurrence of Helicobacter pylori infection: incidence and variables influencing it. A critical review. Am J Gastroenterol 2005, 100:2083-2099.
11. Parsonnet J. What is the Helicobacter pylori global reinfection rate?. Can J Gastroenterol 2003, 17(Suppl B):46B-48B.
12. Luther J., Kao J.Y. Considering global vaccination against Helicobacter pylori. South Med J 2010, 103:185-186.
13. Graham D.Y., Malaty H.M., Evans D.G., et al. Epidemiology of Helicobacter pylori in an asymptomatic population in the United States. Effect of age, race, and socioeconomic status. Gastroenterology 1991, 100:1495-1501.
14. Kruszon-Moran D., McQuillan G.M. Seroprevalence of six infectious diseases among adults in the United States by race/ethnicity: data from the third national health and nutrition examination survey, 1988-94. Adv Data 2005, 9:1-9.
15. Ferlay J., Soerjomataram I., Dikshit R., et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 2015, 136:E359-E386.
16. World Cancer Research Fund International. Stomach Cancer Statistics, 2013. Available at: . http://www.wcrf.org/int/cancer-facts-figures/data-specific-cancers/stomach-cancer-statistics.
17. Cancer incidence in five continents. Volume VIII. IARC Sci Publ 2002, (155):1-781.
18. Yaghoobi M., Bijarchi R., Narod S.A. Family history and the risk of gastric cancer. Br J Cancer 2010, 102:237-242.
19. Rupnow M.F., Shachter R.D., Owens D.K., et al. Quantifying the population impact of a prophylactic Helicobacter pylori vaccine. Vaccine 2001, 20:879-885.
20. Blanchard T., Nedrud J. Helicobacter pylori vaccines. Helicobacter pylori in the 21st century 2010, 167-189. CABI, Wallingford (United Kingdom). P. Sutton, M. Hazel (Eds.).
21. Chen M., Lee A., Hazell S., et al. Immunisation against gastric infection with Helicobacter species: first step in the prophylaxis of gastric cancer?. Zentralbl Bakteriol 1993, 280:155-165.
22. Czinn S.J., Cai A., Nedrud J.G. Protection of germ-free mice from infection by Helicobacter felis after active oral or passive IgA immunization. Vaccine 1993, 11:637-642.
23. Ghiara P., Rossi M., Marchetti M., et al. Therapeutic intragastric vaccination against Helicobacter pylori in mice eradicates an otherwise chronic infection and confers protection against reinfection. Infect Immun 1997, 65:4996-5002.
24. Lee C.K., Weltzin R., Thomas W.D., et al. Oral immunization with recombinant Helicobacter pylori urease induces secretory IgA antibodies and protects mice from challenge with Helicobacter felis. J Infect Dis 1995, 172:161-172.
25. Marchetti M., Arico B., Burroni D., et al. Development of a mouse model of Helicobacter pylori infection that mimics human disease. Science 1995, 267:1655-1658.
26. Michetti P., Corthesy-Theulaz I., Davin C., et al. Immunization of BALB/c mice against Helicobacter felis infection with Helicobacter pylori urease. Gastroenterology 1994, 107:1002-1011.
27. Weltzin R., Kleanthous H., Guirdkhoo F., et al. Novel intranasal immunization techniques for antibody induction and protection of mice against gastric Helicobacter felis infection. Vaccine 1997, 15:370-376.
28. Garhart C.A., Redline R.W., Nedrud J.G., et al. Clearance of Helicobacter pylori infection and resolution of postimmunization gastritis in a kinetic study of prophylactically immunized mice. Infect Immun 2002, 70:3529-3538.
29. Jeremy A.H., Du Y., Dixon M.F., et al. Protection against Helicobacter pylori infection in the Mongolian gerbil after prophylactic vaccination. Microbes Infect 2006, 8:340-346.
30. Jiang W., Baker H.J., Smith B.F. Mucosal immunization with Helicobacter, CpG DNA, and cholera toxin is protective. Infect Immun 2003, 71:40-46.
31. Kleanthous H., Tibbitts T.J., Gray H.L., et al. Sterilizing immunity against experimental Helicobacter pylori infection is challenge-strain dependent. Vaccine 2001, 19:4883-4895.
32. Eisenberg J.C., Czinn S.J., Garhart C.A., et al. Protective efficacy of anti-Helicobacter pylori immunity following systemic immunization of neonatal mice. Infect Immun 2003, 71:1820-1827.
33. Gottwein J.M., Blanchard T.G., Targoni O.S., et al. Protective anti-Helicobacter immunity is induced with aluminum hydroxide or complete Freund's adjuvant by systemic immunization. J Infect Dis 2001, 184:308-314.
34. Guy B., Hessler C., Fourage S., et al. Systemic immunization with urease protects mice against Helicobacter pylori infection. Vaccine 1998, 16:850-856.
35. Malfertheiner P., Selgrad M., Wex T., et al. Efficacy of an investigational recombinant antigen based vaccine against a CagA H. pylori infectious challenge in healthy volunteers. Gastroenterology 2012, 142:S-184.
36. Blanchard T.G., Czinn S.J., Redline R.W., et al. Antibody-independent protective mucosal immunity to gastric Helicobacter infection in mice. Cell Immunol 1999, 191:74-80.
37. Ermak T.H., Giannasca P.J., Nichols R., et al. Immunization of mice with urease vaccine affords protection against Helicobacter pylori infection in the absence of antibodies and is mediated by MHC class II-restricted responses. J Exp Med 1998, 188:2277-2288.
38. Sutton P., Wilson J., Kosaka T., et al. Therapeutic immunization against Helicobacter pylori infection in the absence of antibodies. Immunol Cell Biol 2000, 78:28-30.
39. Radcliff F.J., Hazell S.L., Kolesnikow T., et al. Catalase, a novel antigen for Helicobacter pylori vaccination. Infect Immun 1997, 65:4668-4674.
40. Skene C., Young A., Every A., et al. Helicobacter pylori flagella: antigenic profile and protective immunity. FEMS Immunol Med Microbiol 2007, 50:249-256.
41. Ferrero R.L., Thiberge J.M., Kansau I., et al. The GroES homolog of Helicobacter pylori confers protective immunity against mucosal infection in mice. Proc Natl Acad Sci U S A 1995, 92:6499-6503.
42. Sutton P., Doidge C., Pinczower G., et al. Effectiveness of vaccination with recombinant HpaA from Helicobacter pylori is influenced by host genetic background. FEMS Immunol Med Microbiol 2007, 50:213-219.
43. Satin B., Del Giudice G., Della Bianca V., et al. The neutrophil-activating protein (HP-NAP) of Helicobacter pylori is a protective antigen and a major virulence factor. J Exp Med 2000, 191:1467-1476.
44. Kotloff K.L., Sztein M.B., Wasserman S.S., et al. Safety and immunogenicity of oral inactivated whole-cell Helicobacter pylori vaccine with adjuvant among volunteers with or without subclinical infection. Infect Immun 2001, 69:3581-3590.
45. Rossi G., Ruggiero P., Peppoloni S., et al. Therapeutic vaccination against Helicobacter pylori in the beagle dog experimental model: safety, immunogenicity, and efficacy. Infect Immun 2004, 72:3252-3259.
46. Corthesy-Theulaz I., Porta N., Glauser M., et al. Oral immunization with Helicobacter pylori urease B subunit as a treatment against Helicobacter infection in mice. Gastroenterology 1995, 109:115-121.
47. Doidge C., Crust I., Lee A., et al. Therapeutic immunisation against Helicobacter infection. Lancet 1994, 343:914-915.
48. Cuenca R., Blanchard T.G., Czinn S.J., et al. Therapeutic immunization against Helicobacter mustelae in naturally infected ferrets. Gastroenterology 1996, 110:1770-1775.
49. Michetti P., Kreiss C., Kotloff K.L., et al. Oral immunization with urease and Escherichia coli heat-labile enterotoxin is safe and immunogenic in Helicobacter pylori-infected adults. Gastroenterology 1999, 116:804-812.
50. Billingham R.E., Brent L., Medawar P.B. Actively acquired tolerance of foreign cells. Nature 1953, 172:603-606.
51. Cihak J., Lehmann-Grube F. Immunological tolerance to lymphocytic choriomeningitis virus in neonatally infected virus carrier mice: evidence supporting a clonal inactivation mechanism. Immunology 1978, 34:265-275.
52. Freire de Melo F., Rocha A.M., Rocha G.A., et al. A regulatory instead of an IL-17 T response predominates in Helicobacter pylori-associated gastritis in children. Microbes Infect 2012, 14:341-347.
53. Harris P.R., Wright S.W., Serrano C., et al. Helicobacter pylori gastritis in children is associated with a regulatory T-cell response. Gastroenterology 2008, 134:491-499.
54. Aebischer T., Bumann D., Epple H.J., et al. Correlation of T cell response and bacterial clearance in human volunteers challenged with Helicobacter pylori revealed by randomised controlled vaccination with Ty21a-based Salmonella vaccines. Gut 2008, 57:1065-1072.
55. Banerjee S., Medina-Fatimi A., Nichols R., et al. Safety and efficacy of low dose Escherichia coli enterotoxin adjuvant for urease based oral immunisation against Helicobacter pylori in healthy volunteers. Gut 2002, 51:634-640.
56. Sougioultzis S., Lee C.K., Alsahli M., et al. Safety and efficacy of E coli enterotoxin adjuvant for urease-based rectal immunization against Helicobacter pylori. Vaccine 2002, 21:194-201.
57. Marchetti M., Rossi M., Giannelli V., et al. Protection against Helicobacter pylori infection in mice by intragastric vaccination with H. pylori antigens is achieved using a non-toxic mutant of E. coli heat-labile enterotoxin (LT) as adjuvant. Vaccine 1998, 16:33-37.
58. Summerton N.A., Welch R.W., Bondoc L., et al. Toward the development of a stable, freeze-dried formulation of Helicobacter pylori killed whole cell vaccine adjuvanted with a novel mutant of Escherichia coli heat-labile toxin. Vaccine 2010, 28:1404-1411.
59. Bumann D., Metzger W.G., Mansouri E., et al. Safety and immunogenicity of live recombinant Salmonella enterica serovar Typhi Ty21a expressing urease A and B from Helicobacter pylori in human volunteers. Vaccine 2001, 20:845-852.
60. Metzger W.G., Mansouri E., Kronawitter M., et al. Impact of vector-priming on the immunogenicity of a live recombinant Salmonella enterica serovar typhi Ty21a vaccine expressing urease A and B from Helicobacter pylori in human volunteers. Vaccine 2004, 22:2273-2277.
61. Graham D.Y., Opekun A.R., Osato M.S., et al. Challenge model for Helicobacter pylori infection in human volunteers. Gut 2004, 53:1235-1243.
62. Blanchard T.G., Eisenberg J.C., Matsumoto Y. Clearance of Helicobacter pylori infection through immunization: the site of T cell activation contributes to vaccine efficacy. Vaccine 2004, 22:888-897.
63. Malfertheiner P., Schultze V., Rosenkranz B., et al. Safety and immunogenicity of an intramuscular Helicobacter pylori vaccine in noninfected volunteers: a phase I study. Gastroenterology 2008, 135:787-795.
64. Dubois A., Lee C.K., Fiala N., et al. Immunization against natural Helicobacter pylori infection in nonhuman primates. Infect Immun 1998, 66:4340-4346.
65. Lee C.K., Soike K., Hill J., et al. Immunization with recombinant Helicobacter pylori urease decreases colonization levels following experimental infection of rhesus monkeys. Vaccine 1999, 17:1493-1505.
66. Lee C.K., Soike K., Giannasca P., et al. Immunization of rhesus monkeys with a mucosal prime, parenteral boost strategy protects against infection with Helicobacter pylori. Vaccine 1999, 17:3072-3082.
67. Solnick J.V., Canfield D.R., Hansen L.M., et al. Immunization with recombinant Helicobacter pylori urease in specific-pathogen-free rhesus monkeys (Macaca mulatta). Infect Immun 2000, 68:2560-2565.
68. Anderson K.M., Czinn S.J., Redline R.W., et al. Induction of CTLA-4-mediated anergy contributes to persistent colonization in the murine model of gastric Helicobacter pylori infection. J Immunol 2006, 176:5306-5313.
69. Eaton K.A., Mefford M., Thevenot T. The role of T cell subsets and cytokines in the pathogenesis of Helicobacter pylori gastritis in mice. J Immunol 2001, 166:7456-7461.
70. Matsumoto Y., Blanchard T.G., Drakes M.L., et al. Eradication of Helicobacter pylori and resolution of gastritis in the gastric mucosa of IL-10-deficient mice. Helicobacter 2005, 10:407-415.
71. Rad R., Brenner L., Bauer S., et al. CD25+/Foxp3+ T cells regulate gastric inflammation and Helicobacter pylori colonization in vivo. Gastroenterology 2006, 131:525-537.
72. Raghavan S., Suri-Payer E., Holmgren J. Antigen-specific in vitro suppression of murine Helicobacter pylori-reactive immunopathological T cells by CD4CD25 regulatory T cells. Scand J Immunol 2004, 60:82-88.
73. Sayi A., Kohler E., Toller I.M., et al. TLR-2-activated B cells suppress Helicobacter-induced preneoplastic gastric immunopathology by inducing T regulatory-1 cells. J Immunol 2011, 186:878-890.
74. Fan X.J., Chua A., Shahi C.N., et al. Gastric T lymphocyte responses to Helicobacter pylori in patients with H pylori colonisation. Gut 1994, 35:1379-1384.
75. Karttunen R. Blood lymphocyte proliferation, cytokine secretion and appearance of T cells with activation surface markers in cultures with Helicobacter pylori. Comparison of the responses of subjects with and without antibodies to H. pylori. Clin Exp Immunol 1991, 83:396-400.
76. Karttunen R., Andersson G., Poikonen K., et al. Helicobacter pylori induces lymphocyte activation in peripheral blood cultures. Clin Exp Immunol 1990, 82:485-488.
77. Karttunen R., Karttunen T., Ekre H.P., et al. Interferon gamma and interleukin 4 secreting cells in the gastric antrum in Helicobacter pylori positive and negative gastritis. Gut 1995, 36:341-345.
78. Lindholm C., Quiding-Jarbrink M., Lonroth H., et al. Local cytokine response in Helicobacter pylori-infected subjects. Infect Immun 1998, 66:5964-5971.
79. Sharma S.A., Miller G.G., Perez-Perez G.I., et al. Humoral and cellular immune recognition of Helicobacter pylori proteins are not concordant. Clin Exp Immunol 1994, 97:126-132.
80. Lundgren A., Suri-Payer E., Enarsson K., et al. Helicobacter pylori-specific CD4+ CD25high regulatory T cells suppress memory T-cell responses to H. pylori in infected individuals. Infect Immun 2003, 71:1755-1762.
81. Ding H., Nedrud J.G., Blanchard T.G., et al. Th1-mediated immunity against Helicobacter pylori can compensate for lack of Th17 cells and can protect mice in the absence of immunization. PLoS One 2013, 8:e69384.
82. ClinicalTrials.gov A phase III clinical trial with oral recombinant Helicobacter pylori vaccine in Chinese children 2015, 2014. National Institutes of Health, Bethesda, Maryland.
83. Blanchard T.G., Czinn S.J., Maurer R., et al. Urease-specific monoclonal antibodies prevent Helicobacter felis infection in mice. Infect Immun 1995, 63:1394-1399.
84. IHS, editor. China develops world's first H. Pylori vaccine, given green light by SFDA. April 23, 2009, Englewood, Colorado. Available at: . https://www.ihs.com/country-industry-forecasting.html?ID=106595607.