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Review

Vaccinating against Helicobacter pylori in the developing world

, , &
Pages 568-576 | Received 23 Sep 2013, Accepted 05 Nov 2013, Published online: 06 Nov 2013

References

  • The EUROGAST Study Group. An international association between Helicobacter pylori infection and gastric cancer. Lancet 1993; 341:1359 - 62; http://dx.doi.org/10.1016/0140-6736(93)90938-D; PMID: 8098787
  • NIH Consensus Conference. Helicobacter pylori in peptic ulcer disease. JAMA 1994; 272:65 - 9; http://dx.doi.org/10.1001/jama.1994.03520010077036; PMID: 8007082
  • Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, Sibley RK. Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 1991; 325:1127 - 31; http://dx.doi.org/10.1056/NEJM199110173251603; PMID: 1891020
  • Warren JR, Marshall BJ. Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 1983; 1:1273 - 5; PMID: 6134060
  • World Health Organization. Infection with Helicobacter pylori. Schistosomes, Liver Flukes and Helicobacter pylori. Volume 61. Lyon: International Agency for Research on Cancer, 1994:177-241.
  • Graham DYMH, Malaty HM, Evans DG, Evans DJ Jr., Klein PD, Adam E. Epidemiology of Helicobacter pylori in an asymptomatic population in the United States. Effect of age, race, and socioeconomic status. Gastroenterology 1991; 100:1495 - 501; PMID: 2019355
  • World Gastroenterology Organization. Helicobacter pylori in developing countries. WGO Global Guidelines, 2010:1 - 15.
  • Luther J, Kao JY. Considering global vaccination against Helicobacter pylori.. South Med J 2010; 103:185 - 6; http://dx.doi.org/10.1097/SMJ.0b013e3181cf3c19; PMID: 20134368
  • Yamaoka Y, Kato M, Asaka M. Geographic differences in gastric cancer incidence can be explained by differences between Helicobacter pylori strains. Intern Med 2008; 47:1077 - 83; http://dx.doi.org/10.2169/internalmedicine.47.0975; PMID: 18552463
  • Kruszon-Moran D, McQuillan GM. 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; (325):1 - 9; PMID: 15771149
  • National Cancer Institute. SEER Cancer Statistics Review, 1975-2008, In: Howlader N NA, Krapcho M, Neyman N, Aminou R, Waldron W, Altekruse SF, Kosary CL, Ruhl J, Tatalovich Z, Cho H, Mariotto A, Eisner MP, Lewis DR, Chen HS, Feuer EJ, Cronin KA, Edwards BK ed. Bethesda, MD, 2011.
  • Ruhl CE, Sayer B, Byrd-Holt DD, et al. Costs of digestive diseases. In: Everhart JE, ed. The burden of digestive diseases in the United States. US Department of Health and Human Services, Public Health Service, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases. Washington, D.C.: Government Printing Office, 2008:137-147.
  • Ladabaum U, Chey WD, Scheiman JM, Fendrick AM. Reappraisal of non-invasive management strategies for uninvestigated dyspepsia: a cost-minimization analysis. Aliment Pharmacol Ther 2002; 16:1491 - 501; http://dx.doi.org/10.1046/j.1365-2036.2002.01306.x; PMID: 12182749
  • Delaney B, Ford AC, Forman D, Moayyedi P, Qume M. Initial management strategies for dyspepsia. Cochrane Database Syst Rev 2005; CD001961; PMID: 16235292
  • You JH, Wong PL, Wu JC. Cost-effectiveness of Helicobacter pylori “test and treat” for patients with typical reflux symptoms in a population with a high prevalence of H. pylori infection: a Markov model analysis. Scand J Gastroenterol 2006; 41:21 - 9; http://dx.doi.org/10.1080/00365520510023873; PMID: 16373272
  • Mason J, Axon AT, Forman D, Duffett S, Drummond M, Crocombe W, Feltbower R, Mason S, Brown J, Moayyedi P, Leeds HELP Study Group. The cost-effectiveness of population Helicobacter pylori screening and treatment: a Markov model using economic data from a randomized controlled trial. Aliment Pharmacol Ther 2002; 16:559 - 68; http://dx.doi.org/10.1046/j.1365-2036.2002.01204.x; PMID: 11876711
  • Frenck RW Jr., Clemens J. Helicobacter in the developing world. Microbes Infect 2003; 5:705 - 13; http://dx.doi.org/10.1016/S1286-4579(03)00112-6; PMID: 12814771
  • Gisbert JP. The recurrence of Helicobacter pylori infection: incidence and variables influencing it. A critical review. Am J Gastroenterol 2005; 100:2083 - 99; http://dx.doi.org/10.1111/j.1572-0241.2005.50043.x; PMID: 16128956
  • Parsonnet J. What is the Helicobacter pylori global reinfection rate?. Can J Gastroenterol 2003; 17:Suppl B 46B - 8B; PMID: 12845351
  • Fukase K, Kato M, Kikuchi S, Inoue K, Uemura N, Okamoto S, Terao S, Amagai K, Hayashi S, Asaka M, Japan Gast Study Group. Effect of eradication of Helicobacter pylori on incidence of metachronous gastric carcinoma after endoscopic resection of early gastric cancer: an open-label, randomised controlled trial. Lancet 2008; 372:392 - 7; http://dx.doi.org/10.1016/S0140-6736(08)61159-9; PMID: 18675689
  • Rupnow MF, Shachter RD, Owens DK, Parsonnet J. Quantifying the population impact of a prophylactic Helicobacter pylori vaccine. Vaccine 2001; 20:879 - 85; http://dx.doi.org/10.1016/S0264-410X(01)00401-7; PMID: 11738753
  • Dale A, Thomas JE, Darboe MK, Coward WA, Harding M, Weaver LT. Helicobacter pylori infection, gastric acid secretion, and infant growth. J Pediatr Gastroenterol Nutr 1998; 26:393 - 7; http://dx.doi.org/10.1097/00005176-199804000-00006; PMID: 9552134
  • Weaver LT. Royal Society of Tropical Medicine and Hygiene Meeting at Manson House, London, 16 February 1995. Aspects of Helicobacter pylori infection in the developing and developed world. Helicobacter pylori infection, nutrition and growth of West African infants. Trans R Soc Trop Med Hyg 1995; 89:347 - 50; http://dx.doi.org/10.1016/0035-9203(95)90002-0; PMID: 7570858
  • Barabino A. Helicobacter pylori-related iron deficiency anemia: a review. Helicobacter 2002; 7:71 - 5; http://dx.doi.org/10.1046/j.1083-4389.2002.00073.x; PMID: 11966864
  • Blanchard T, Nedrud J. Helicobacter pylori vaccines. In: Sutton P, Hazel M, eds. Helicobacter pylori in the 21st century. Wallingford, UK: CABI, 2010.
  • Ferrero RL, Thiberge JM, Kansau I, Wuscher N, Huerre M, Labigne A. The GroES homolog of Helicobacter pylori confers protective immunity against mucosal infection in mice. Proc Natl Acad Sci U S A 1995; 92:6499 - 503; http://dx.doi.org/10.1073/pnas.92.14.6499; PMID: 7604021
  • Rossi G, Ruggiero P, Peppoloni S, Pancotto L, Fortuna D, Lauretti L, Volpini G, Mancianti S, Corazza M, Taccini E, et al. Therapeutic vaccination against Helicobacter pylori in the beagle dog experimental model: safety, immunogenicity, and efficacy. Infect Immun 2004; 72:3252 - 9; http://dx.doi.org/10.1128/IAI.72.6.3252-3259.2004; PMID: 15155627
  • Lee CK, Weltzin R, Thomas WD Jr., Kleanthous H, Ermak TH, Soman G, Hill JE, Ackerman SK, Monath TP. 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 - 72; http://dx.doi.org/10.1093/infdis/172.1.161; PMID: 7797906
  • Ghiara P, Rossi M, Marchetti M, Di Tommaso A, Vindigni C, Ciampolini F, Covacci A, Telford JL, De Magistris MT, Pizza 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; PMID: 9393788
  • Radcliff FJ, Hazell SL, Kolesnikow T, Doidge C, Lee A. Catalase, a novel antigen for Helicobacter pylori vaccination. Infect Immun 1997; 65:4668 - 74; PMID: 9353048
  • Skene C, Young A, Every A, Sutton P. Helicobacter pylori flagella: antigenic profile and protective immunity. FEMS Immunol Med Microbiol 2007; 50:249 - 56; http://dx.doi.org/10.1111/j.1574-695X.2007.00263.x; PMID: 17521391
  • Sutton P, Doidge C, Pinczower G, Wilson J, Harbour S, Swierczak A, Lee A. Effectiveness of vaccination with recombinant HpaA from Helicobacter pylori is influenced by host genetic background. FEMS Immunol Med Microbiol 2007; 50:213 - 9; http://dx.doi.org/10.1111/j.1574-695X.2006.00206.x; PMID: 17567282
  • Satin B, Del Giudice G, Della Bianca V, Dusi S, Laudanna C, Tonello F, Kelleher D, Rappuoli R, Montecucco C, Rossi F. The neutrophil-activating protein (HP-NAP) of Helicobacter pylori is a protective antigen and a major virulence factor. J Exp Med 2000; 191:1467 - 76; http://dx.doi.org/10.1084/jem.191.9.1467; PMID: 10790422
  • Chen M, Lee A, Hazell S, Hu P, Li Y. Immunisation against gastric infection with Helicobacter species: first step in the prophylaxis of gastric cancer?. Zentralbl Bakteriol 1993; 280:155 - 65; http://dx.doi.org/10.1016/S0934-8840(11)80952-7; PMID: 8280938
  • Czinn SJ, Cai A, Nedrud JG. Protection of germ-free mice from infection by Helicobacter felis after active oral or passive IgA immunization. Vaccine 1993; 11:637 - 42; http://dx.doi.org/10.1016/0264-410X(93)90309-L; PMID: 8322486
  • Corthésy-Theulaz I, Porta N, Glauser M, Saraga E, Vaney AC, Haas R, Kraehenbuhl JP, Blum AL, Michetti P. Oral immunization with Helicobacter pylori urease B subunit as a treatment against Helicobacter infection in mice. Gastroenterology 1995; 109:115 - 21; http://dx.doi.org/10.1016/0016-5085(95)90275-9; PMID: 7797009
  • Doidge C, Crust I, Lee A, Buck F, Hazell S, Manne U. Therapeutic immunisation against Helicobacter infection. Lancet 1994; 343:914 - 5; http://dx.doi.org/10.1016/S0140-6736(94)90032-9; PMID: 7908372
  • Sutton P, Wilson J, Kosaka T, Wolowczuk I, Lee A. Therapeutic immunization against Helicobacter pylori infection in the absence of antibodies. Immunol Cell Biol 2000; 78:28 - 30; http://dx.doi.org/10.1046/j.1440-1711.2000.00881.x; PMID: 10651926
  • Cuenca R, Blanchard TG, Czinn SJ, Nedrud JG, Monath TP, Lee CK, Redline RW. Therapeutic immunization against Helicobacter mustelae in naturally infected ferrets. Gastroenterology 1996; 110:1770 - 5; http://dx.doi.org/10.1053/gast.1996.v110.pm8964402; PMID: 8964402
  • Marchetti M, Aricò B, Burroni D, Figura N, Rappuoli R, Ghiara P. Development of a mouse model of Helicobacter pylori infection that mimics human disease. Science 1995; 267:1655 - 8; http://dx.doi.org/10.1126/science.7886456; PMID: 7886456
  • Michetti P, Corthésy-Theulaz I, Davin C, Haas R, Vaney AC, Heitz M, Bille J, Kraehenbuhl JP, Saraga E, Blum AL. Immunization of BALB/c mice against Helicobacter felis infection with Helicobacter pylori urease. Gastroenterology 1994; 107:1002 - 11; PMID: 7926454
  • Weltzin R, Kleanthous H, Guirakhoo F, Monath TP, Lee CK. Novel intranasal immunization techniques for antibody induction and protection of mice against gastric Helicobacter felis infection. Vaccine 1997; 15:370 - 6; http://dx.doi.org/10.1016/S0264-410X(97)00203-X; PMID: 9141207
  • Garhart CA, Redline RW, Nedrud JG, Czinn SJ. Clearance of Helicobacter pylori infection and resolution of postimmunization gastritis in a kinetic study of prophylactically immunized mice. Infect Immun 2002; 70:3529 - 38; http://dx.doi.org/10.1128/IAI.70.7.3529-3538.2002; PMID: 12065492
  • Jiang W, Baker HJ, Smith BF. Mucosal immunization with helicobacter, CpG DNA, and cholera toxin is protective. Infect Immun 2003; 71:40 - 6; http://dx.doi.org/10.1128/IAI.71.1.40-46.2003; PMID: 12496147
  • Kleanthous H, Tibbitts TJ, Gray HL, Myers GA, Lee CK, Ermak TH, Monath TP. Sterilizing immunity against experimental Helicobacter pylori infection is challenge-strain dependent. Vaccine 2001; 19:4883 - 95; http://dx.doi.org/10.1016/S0264-410X(01)00248-1; PMID: 11535342
  • Jeremy AH, Du Y, Dixon MF, Robinson PA, Crabtree JE. Protection against Helicobacter pylori infection in the Mongolian gerbil after prophylactic vaccination. Microbes Infect 2006; 8:340 - 6; http://dx.doi.org/10.1016/j.micinf.2005.06.025; PMID: 16213184
  • Eisenberg JC, Czinn SJ, Garhart CA, Redline RW, Bartholomae WC, Gottwein JM, Nedrud JG, Emancipator SE, Boehm BB, Lehmann PV, et al. Protective efficacy of anti-Helicobacter pylori immunity following systemic immunization of neonatal mice. Infect Immun 2003; 71:1820 - 7; http://dx.doi.org/10.1128/IAI.71.4.1820-1827.2003; PMID: 12654796
  • Gottwein JM, Blanchard TG, Targoni OS, Eisenberg JC, Zagorski BM, Redline RW, Nedrud JG, Tary-Lehmann M, Lehmann PV, Czinn SJ. Protective anti-Helicobacter immunity is induced with aluminum hydroxide or complete Freund’s adjuvant by systemic immunization. J Infect Dis 2001; 184:308 - 14; http://dx.doi.org/10.1086/322032; PMID: 11443556
  • Guy B, Hessler C, Fourage S, Haensler J, Vialon-Lafay E, Rokbi B, Millet MJ. Systemic immunization with urease protects mice against Helicobacter pylori infection. Vaccine 1998; 16:850 - 6; http://dx.doi.org/10.1016/S0264-410X(97)00258-2; PMID: 9627943
  • Eaton KA, 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 - 61; PMID: 11390498
  • Eaton KA, Ringler SR, Danon SJ. Murine splenocytes induce severe gastritis and delayed-type hypersensitivity and suppress bacterial colonization in Helicobacter pylori-infected SCID mice. Infect Immun 1999; 67:4594 - 602; PMID: 10456905
  • Stuller KA, Ding H, Redline RW, Czinn SJ, Blanchard TG. CD25+ T cells induce Helicobacter pylori-specific CD25- T-cell anergy but are not required to maintain persistent hyporesponsiveness. Eur J Immunol 2008; 38:3426 - 35; http://dx.doi.org/10.1002/eji.200838428; PMID: 19003932
  • Spangler BD. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol Rev 1992; 56:622 - 47; PMID: 1480112
  • Marchetti M, Rossi M, Giannelli V, Giuliani MM, Pizza M, Censini S, Covacci A, Massari P, Pagliaccia C, Manetti R, 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 - 7; http://dx.doi.org/10.1016/S0264-410X(97)00153-9; PMID: 9607006
  • Cárdenas-Freytag L, Cheng E, Mayeux P, Domer JE, Clements JD. Effectiveness of a vaccine composed of heat-killed Candida albicans and a novel mucosal adjuvant, LT(R192G), against systemic candidiasis. Infect Immun 1999; 67:826 - 33; PMID: 9916097
  • Czinn SJ, Blanchard T. Vaccinating against Helicobacter pylori infection. Nat Rev Gastroenterol Hepatol 2011; 8:133 - 40; http://dx.doi.org/10.1038/nrgastro.2011.1; PMID: 21304478
  • Michetti P, Kreiss C, Kotloff KL, Porta N, Blanco JL, Bachmann D, Herranz M, Saldinger PF, Corthésy-Theulaz I, Losonsky G, 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 - 12; http://dx.doi.org/10.1016/S0016-5085(99)70063-6; PMID: 10092302
  • Banerjee S, Medina-Fatimi A, Nichols R, Tendler D, Michetti M, Simon J, Kelly CP, Monath TP, Michetti P. 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 - 40; http://dx.doi.org/10.1136/gut.51.5.634; PMID: 12377799
  • Sougioultzis S, Lee CK, Alsahli M, Banerjee S, Cadoz M, Schrader R, Guy B, Bedford P, Monath TP, Kelly CP, et al. Safety and efficacy of E coli enterotoxin adjuvant for urease-based rectal immunization against Helicobacter pylori.. Vaccine 2002; 21:194 - 201; http://dx.doi.org/10.1016/S0264-410X(02)00467-X; PMID: 12450694
  • Kotloff KL, Sztein MB, Wasserman SS, Losonsky GA, DiLorenzo SC, Walker RI. 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 - 90; http://dx.doi.org/10.1128/IAI.69.6.3581-3590.2001; PMID: 11349017
  • Angelakopoulos H, Hohmann EL. Pilot study of phoP/phoQ-deleted Salmonella enterica serovar typhimurium expressing Helicobacter pylori urease in adult volunteers. Infect Immun 2000; 68:2135 - 41; http://dx.doi.org/10.1128/IAI.68.4.2135-2141.2000; PMID: 10722611
  • DiPetrillo MD, Tibbetts T, Kleanthous H, Killeen KP, Hohmann EL. Safety and immunogenicity of phoP/phoQ-deleted Salmonella typhi expressing Helicobacter pylori urease in adult volunteers. Vaccine 1999; 18:449 - 59; http://dx.doi.org/10.1016/S0264-410X(99)00246-7; PMID: 10519934
  • Bumann D, Metzger WG, Mansouri E, Palme O, Wendland M, Hurwitz R, Haas G, Aebischer T, von Specht BU, Meyer TF. 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 - 52; http://dx.doi.org/10.1016/S0264-410X(01)00391-7; PMID: 11738748
  • Aebischer T, Bumann D, Epple HJ, Metzger W, Schneider T, Cherepnev G, Walduck AK, Kunkel D, Moos V, Loddenkemper C, 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 - 72; http://dx.doi.org/10.1136/gut.2007.145839; PMID: 18417532
  • Graham DY, Opekun AR, Osato MS, El-Zimaity HM, Lee CK, Yamaoka Y, Qureshi WA, Cadoz M, Monath TP. Challenge model for Helicobacter pylori infection in human volunteers. Gut 2004; 53:1235 - 43; http://dx.doi.org/10.1136/gut.2003.037499; PMID: 15306577
  • Malfertheiner P, Schultze V, Rosenkranz B, Kaufmann SH, Ulrichs T, Novicki D, Norelli F, Contorni M, Peppoloni S, Berti D, et al. Safety and immunogenicity of an intramuscular Helicobacter pylori vaccine in noninfected volunteers: a phase I study. Gastroenterology 2008; 135:787 - 95; http://dx.doi.org/10.1053/j.gastro.2008.05.054; PMID: 18619971
  • 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
  • Blanchard TG, Czinn SJ, Redline RW, Sigmund N, Harriman G, Nedrud JG. Antibody-independent protective mucosal immunity to gastric helicobacter infection in mice. Cell Immunol 1999; 191:74 - 80; http://dx.doi.org/10.1006/cimm.1998.1421; PMID: 9918689
  • Ermak TH, Giannasca PJ, Nichols R, Myers GA, Nedrud J, Weltzin R, Lee CK, Kleanthous H, Monath TP. 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 - 88; http://dx.doi.org/10.1084/jem.188.12.2277; PMID: 9858514
  • Mohammadi M, Nedrud J, Redline R, Lycke N, Czinn SJ. Murine CD4 T-cell response to Helicobacter infection: TH1 cells enhance gastritis and TH2 cells reduce bacterial load. Gastroenterology 1997; 113:1848 - 57; http://dx.doi.org/10.1016/S0016-5085(97)70004-0; PMID: 9394724
  • Pappo J, Torrey D, Castriotta L, Savinainen A, Kabok Z, Ibraghimov A. Helicobacter pylori infection in immunized mice lacking major histocompatibility complex class I and class II functions. Infect Immun 1999; 67:337 - 41; PMID: 9864234
  • Saldinger PF, Porta N, Launois P, Louis JA, Waanders GA, Bouzouréne H, Michetti P, Blum AL, Corthésy-Theulaz IE. Immunization of BALB/c mice with Helicobacter urease B induces a T helper 2 response absent in Helicobacter infection. Gastroenterology 1998; 115:891 - 7; http://dx.doi.org/10.1016/S0016-5085(98)70261-6; PMID: 9753492
  • Guy B, Hessler C, Fourage S, Rokbi B, Millet MJ. Comparison between targeted and untargeted systemic immunizations with adjuvanted urease to cure Helicobacter pylori infection in mice. Vaccine 1999; 17:1130 - 5; http://dx.doi.org/10.1016/S0264-410X(98)00332-6; PMID: 10195624
  • Akhiani AA, Pappo J, Kabok Z, Schön K, Gao W, Franzén LE, Lycke N. Protection against Helicobacter pylori infection following immunization is IL-12-dependent and mediated by Th1 cells. J Immunol 2002; 169:6977 - 84; PMID: 12471132
  • Aebischer T, Laforsch S, Hurwitz R, Brombacher F, Meyer TF. Immunity against Helicobacter pylori: significance of interleukin-4 receptor alpha chain status and gender of infected mice. Infect Immun 2001; 69:556 - 8; http://dx.doi.org/10.1128/IAI.69.1.556-558.2001; PMID: 11119552
  • Garhart CA, Heinzel FP, Czinn SJ, Nedrud JG. Vaccine-induced reduction of Helicobacter pylori colonization in mice is interleukin-12 dependent but gamma interferon and inducible nitric oxide synthase independent. Infect Immun 2003; 71:910 - 21; http://dx.doi.org/10.1128/IAI.71.2.910-921.2003; PMID: 12540573
  • Garhart CA, Nedrud JG, Heinzel FP, Sigmund NE, Czinn SJ. Vaccine-induced protection against Helicobacter pylori in mice lacking both antibodies and interleukin-4. Infect Immun 2003; 71:3628 - 33; http://dx.doi.org/10.1128/IAI.71.6.3628-3633.2003; PMID: 12761151
  • Panthel K, Faller G, Haas R. Colonization of C57BL/6J and BALB/c wild-type and knockout mice with Helicobacter pylori: effect of vaccination and implications for innate and acquired immunity. Infect Immun 2003; 71:794 - 800; http://dx.doi.org/10.1128/IAI.71.2.794-800.2003; PMID: 12540559
  • Sayi A, Kohler E, Hitzler I, Arnold I, Schwendener R, Rehrauer H, Müller A. The CD4+ T cell-mediated IFN-gamma response to Helicobacter infection is essential for clearance and determines gastric cancer risk. J Immunol 2009; 182:7085 - 101; http://dx.doi.org/10.4049/jimmunol.0803293; PMID: 19454706
  • Sawai N, Kita M, Kodama T, Tanahashi T, Yamaoka Y, Tagawa Y, Iwakura Y, Imanishi J. Role of gamma interferon in Helicobacter pylori-induced gastric inflammatory responses in a mouse model. Infect Immun 1999; 67:279 - 85; PMID: 9864227
  • Ding H, Nedrud JG, Blanchard TG, Zagorski BM, Li G, Shiu J, Xu J, Czinn SJ. 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; http://dx.doi.org/10.1371/journal.pone.0069384; PMID: 23874957
  • DeLyria ES, Nedrud JG, Ernst PB, Alam MS, Redline RW, Ding H, Czinn SJ, Xu J, Blanchard TG. Vaccine-induced immunity against Helicobacter pylori in the absence of IL-17A. Helicobacter 2011; 16:169 - 78; http://dx.doi.org/10.1111/j.1523-5378.2011.00839.x; PMID: 21585602
  • Velin D, Favre L, Bernasconi E, et al. Interleukin-17 is a critical mediator of vaccine-induced reduction of Helicobacter infection in the mouse model. Gastroenterology 2009;136:2237-2246 e1.
  • Flach CF, Östberg AK, Nilsson AT, Malefyt RdeW, Raghavan S. Proinflammatory cytokine gene expression in the stomach correlates with vaccine-induced protection against Helicobacter pylori infection in mice: an important role for interleukin-17 during the effector phase. Infect Immun 2011; 79:879 - 86; http://dx.doi.org/10.1128/IAI.00756-10; PMID: 21078851
  • Ismail HF, Fick P, Zhang J, Lynch RG, Berg DJ. Depletion of neutrophils in IL-10(-/-) mice delays clearance of gastric Helicobacter infection and decreases the Th1 immune response to Helicobacter. J Immunol 2003; 170:3782 - 9; PMID: 12646644
  • Matsumoto Y, Blanchard TG, Drakes ML, Basu M, Redline RW, Levine AD, Czinn SJ. Eradication of Helicobacter pylori and resolution of gastritis in the gastric mucosa of IL-10-deficient mice. Helicobacter 2005; 10:407 - 15; http://dx.doi.org/10.1111/j.1523-5378.2005.00349.x; PMID: 16181351
  • Dooley CP, Cohen H, Fitzgibbons PL, Bauer M, Appleman MD, Perez-Perez GI, Blaser MJ. Prevalence of Helicobacter pylori infection and histologic gastritis in asymptomatic persons. N Engl J Med 1989; 321:1562 - 6; http://dx.doi.org/10.1056/NEJM198912073212302; PMID: 2586553
  • Bamford KB, Fan X, Crowe SE, Leary JF, Gourley WK, Luthra GK, Brooks EG, Graham DY, Reyes VE, Ernst PB. Lymphocytes in the human gastric mucosa during Helicobacter pylori have a T helper cell 1 phenotype. Gastroenterology 1998; 114:482 - 92; http://dx.doi.org/10.1016/S0016-5085(98)70531-1; PMID: 9496938
  • D’Elios MM, Manghetti M, De Carli M, Costa F, Baldari CT, Burroni D, Telford JL, Romagnani S, Del Prete G. T helper 1 effector cells specific for Helicobacter pylori in the gastric antrum of patients with peptic ulcer disease. J Immunol 1997; 158:962 - 7; PMID: 8993017
  • Smythies LE, Waites KB, Lindsey JR, Harris PR, Ghiara P, Smith PD. Helicobacter pylori-induced mucosal inflammation is Th1 mediated and exacerbated in IL-4, but not IFN-gamma, gene-deficient mice. J Immunol 2000; 165:1022 - 9; PMID: 10878379
  • Karttunen R, Karttunen T, Ekre HP, MacDonald TT. Interferon gamma and interleukin 4 secreting cells in the gastric antrum in Helicobacter pylori positive and negative gastritis. Gut 1995; 36:341 - 5; http://dx.doi.org/10.1136/gut.36.3.341; PMID: 7698689
  • Mohammadi M, Czinn S, Redline R, Nedrud J. Helicobacter-specific cell-mediated immune responses display a predominant Th1 phenotype and promote a delayed-type hypersensitivity response in the stomachs of mice. J Immunol 1996; 156:4729 - 38; PMID: 8648119
  • Luzza F, Parrello T, Monteleone G, Sebkova L, Romano M, Zarrilli R, Imeneo M, Pallone F. Up-regulation of IL-17 is associated with bioactive IL-8 expression in Helicobacter pylori-infected human gastric mucosa. J Immunol 2000; 165:5332 - 7; PMID: 11046068
  • Shiomi S, Toriie A, Imamura S, Konishi H, Mitsufuji S, Iwakura Y, Yamaoka Y, Ota H, Yamamoto T, Imanishi J, et al. IL-17 is involved in Helicobacter pylori-induced gastric inflammatory responses in a mouse model. Helicobacter 2008; 13:518 - 24; http://dx.doi.org/10.1111/j.1523-5378.2008.00629.x; PMID: 19166417
  • Horvath DJ Jr., Washington MK, Cope VA, Algood HM. IL-23 Contributes to control of chronic Helicobacter pylori infection and the development of T helper responses in a mouse model. Front Immunol 2012; 3:56; http://dx.doi.org/10.3389/fimmu.2012.00056; PMID: 22566937
  • Fan XJ, Chua A, Shahi CN, McDevitt J, Keeling PW, Kelleher D. Gastric T lymphocyte responses to Helicobacter pylori in patients with H pylori colonisation. Gut 1994; 35:1379 - 84; http://dx.doi.org/10.1136/gut.35.10.1379; PMID: 7959191
  • 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; http://dx.doi.org/10.1111/j.1365-2249.1991.tb05650.x; PMID: 1900743
  • Karttunen R, Andersson G, Poikonen K, Kosunen TU, Karttunen T, Juutinen K, Niemelä S. Helicobacter pylori induces lymphocyte activation in peripheral blood cultures. Clin Exp Immunol 1990; 82:485 - 8; http://dx.doi.org/10.1111/j.1365-2249.1990.tb05476.x; PMID: 2124957
  • Sharma SA, Miller GG, Perez-Perez GI, Gupta RS, Blaser MJ. Humoral and cellular immune recognition of Helicobacter pylori proteins are not concordant. Clin Exp Immunol 1994; 97:126 - 32; http://dx.doi.org/10.1111/j.1365-2249.1994.tb06590.x; PMID: 8033409
  • 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 - 8; http://dx.doi.org/10.1111/j.0300-9475.2004.01447.x; PMID: 15238076
  • Harris PR, Wright SW, Serrano C, Riera F, Duarte I, Torres J, Peña A, Rollán A, Viviani P, Guiraldes E, et al. Helicobacter pylori gastritis in children is associated with a regulatory T-cell response. Gastroenterology 2008; 134:491 - 9; http://dx.doi.org/10.1053/j.gastro.2007.11.006; PMID: 18242215
  • Raghavan S, Fredriksson M, Svennerholm AM, Holmgren J, Suri-Payer E. Absence of CD4+CD25+ regulatory T cells is associated with a loss of regulation leading to increased pathology in Helicobacter pylori-infected mice. Clin Exp Immunol 2003; 132:393 - 400; http://dx.doi.org/10.1046/j.1365-2249.2003.02177.x; PMID: 12780684
  • Rad R, Brenner L, Bauer S, Schwendy S, Layland L, da Costa CP, Reindl W, Dossumbekova A, Friedrich M, Saur D, et al. CD25+/Foxp3+ T cells regulate gastric inflammation and Helicobacter pylori colonization in vivo. Gastroenterology 2006; 131:525 - 37; http://dx.doi.org/10.1053/j.gastro.2006.05.001; PMID: 16890606
  • Arnold IC, Lee JY, Amieva MR, Roers A, Flavell RA, Sparwasser T, Müller A. Tolerance rather than immunity protects from Helicobacter pylori-induced gastric preneoplasia. Gastroenterology 2011; 140:199 - 209; http://dx.doi.org/10.1053/j.gastro.2010.06.047; PMID: 20600031
  • Anderson KM, Czinn SJ, Redline RW, Blanchard TG. Induction of CTLA-4-mediated anergy contributes to persistent colonization in the murine model of gastric Helicobacter pylori infection. J Immunol 2006; 176:5306 - 13; PMID: 16621997
  • Rubtsov YP, Rasmussen JP, Chi EY, Fontenot J, Castelli L, Ye X, Treuting P, Siewe L, Roers A, Henderson WR Jr., et al. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 2008; 28:546 - 58; http://dx.doi.org/10.1016/j.immuni.2008.02.017; PMID: 18387831
  • Blanchard TG, Yu F, Hsieh CL, Redline RW. Severe inflammation and reduced bacteria load in murine helicobacter infection caused by lack of phagocyte oxidase activity. J Infect Dis 2003; 187:1609 - 15; http://dx.doi.org/10.1086/374780; PMID: 12721941
  • Romani L, Fallarino F, De Luca A, Montagnoli C, D’Angelo C, Zelante T, Vacca C, Bistoni F, Fioretti MC, Grohmann U, et al. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 2008; 451:211 - 5; http://dx.doi.org/10.1038/nature06471; PMID: 18185592
  • Berg DJ, Lynch NA, Lynch RG, Lauricella DM. Rapid development of severe hyperplastic gastritis with gastric epithelial dedifferentiation in Helicobacter felis-infected IL-10(-/-) mice. Am J Pathol 1998; 152:1377 - 86; PMID: 9588906
  • Chen Y, Blaser MJ. Helicobacter pylori colonization is inversely associated with childhood asthma. J Infect Dis 2008; 198:553 - 60; http://dx.doi.org/10.1086/590158; PMID: 18598192
  • Arnold IC, Dehzad N, Reuter S, Martin H, Becher B, Taube C, Müller A. Helicobacter pylori infection prevents allergic asthma in mouse models through the induction of regulatory T cells. J Clin Invest 2011; 121:3088 - 93; http://dx.doi.org/10.1172/JCI45041; PMID: 21737881
  • Luther J, Dave M, Higgins PD, Kao JY. Association between Helicobacter pylori infection and inflammatory bowel disease: a meta-analysis and systematic review of the literature. Inflamm Bowel Dis 2010; 16:1077 - 84; http://dx.doi.org/10.1002/ibd.21116; PMID: 19760778

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