Advanced search
Publication Cover
Expert Review of Vaccines Volume 11, 2012 - Issue 4
Submit an article Journal homepage
247
Views
89
CrossRef citations to date
0
Altmetric
Review

Recent progress toward an enterotoxigenic Escherichia coli vaccine

Ann-Mari Svennerholm Gothenburg University Vaccine Research Institute (GUVAX) and Department of Microbiology and Immunology, Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg, Sweden. [email protected]
&
Anna Lundgren Gothenburg University Vaccine Research Institute (GUVAX) and Department of Microbiology and Immunology, Institute of Biomedicine, The Sahlgrenska Academy, University of Gothenburg, Sweden
Pages 495-507 | Published online: 09 Jan 2014

References

  • Qadri F, Svennerholm AM, Faruque AS, Sack RB. Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention. Clin. Microbiol. Rev. 18(3), 465–483 (2005).
  • Nataro JP, Kaper JB. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11(1), 142–201 (1998).
  • Sanchez J, Holmgren J. Virulence factors, pathogenesis and vaccine protection in cholera and ETEC diarrhea. Curr. Opin. Immunol. 17(4), 388–398 (2005).
  • Gaastra W, Svennerholm AM. Colonization factors of human enterotoxigenic Escherichia coli (ETEC). Trends Microbiol. 4(11), 444–452 (1996).
  • Wolf MK. Occurrence, distribution, and associations of O and H serogroups, colonization factor antigens, and toxins of enterotoxigenic Escherichia coli. Clin. Microbiol. Rev. 10(4), 569–584 (1997).
  • Svennerholm AM, Tobias J. Vaccines against enterotoxigenic Escherichia coli. Expert Rev. Vaccines 7(6), 795–804 (2008).
  • Walker RI, Steele D, Aguado T. Analysis of strategies to successfully vaccinate infants in developing countries against enterotoxigenic E. coli (ETEC) disease. Vaccine 25(14), 2545–2566 (2007).
  • Hill DR, Beeching NJ. Travelers’ diarrhea. Curr. Opin. Infect. Dis. 23(5), 481–487 (2010).
  • Paredes-Paredes M, Okhuysen PC, Flores J et al. Seasonality of diarrheagenic Escherichia coli pathotypes in the US students acquiring diarrhea in Mexico. J. Travel Med. 18(2), 121–125 (2011).
  • Ahn JY, Chung JW, Chang KJ et al. Clinical characteristics and etiology of travelers’ diarrhea among Korean travelers visiting South-East Asia. J. Korean Med. Sci. 26(2), 196–200 (2011).
  • Harris AM, Chowdhury F, Begum YA et al. Shifting prevalence of major diarrheal pathogens in patients seeking hospital care during floods in 1998, 2004, and 2007 in Dhaka, Bangladesh. Am. J. Trop. Med. Hyg. 79(5), 708–714 (2008).
  • Rivera FP, Ochoa TJ, Maves RC et al. Genotypic and phenotypic characterization of enterotoxigenic Escherichia coli strains isolated from Peruvian children. J. Clin. Microbiol. 48(9), 3198–3203 (2010).
  • Shaheen HI, Abdel Messih IA, Klena JD et al. Phenotypic and genotypic analysis of enterotoxigenic Escherichia coli in samples obtained from Egyptian children presenting to referral hospitals. J. Clin. Microbiol. 47(1), 189–197 (2009).
  • Isidean SD, Riddle MS, Savarino SJ, Porter CK. A systematic review of ETEC epidemiology focusing on colonization factor and toxin expression. Vaccine 29(37), 6167–6178 (2011).
  • Anantha RP, Mcveigh AL, Lee LH et al. Evolutionary and functional relationships of colonization factor antigen i and other class 5 adhesive fimbriae of enterotoxigenic Escherichia coli. Infect. Immun. 72(12), 7190–7201 (2004).
  • Bolin I, Wiklund G, Qadri F et al. Enterotoxigenic Escherichia coli with STh and STp genotypes is associated with diarrhea both in children in areas of endemicity and in travelers. J. Clin. Microbiol. 44(11), 3872–3877 (2006).
  • Sjoling A, Wiklund G, Savarino SJ, Cohen DI, Svennerholm AM. Comparative analyses of phenotypic and genotypic methods for detection of enterotoxigenic Escherichia coli toxins and colonization factors. J. Clin. Microbiol. 45(10), 3295–3301 (2007).
  • Rodas C, Iniguez V, Qadri F, Wiklund G, Svennerholm AM, Sjoling A. Development of multiplex PCR assays for detection of enterotoxigenic Escherichia coli colonization factors and toxins. J. Clin. Microbiol. 47(4), 1218–1220 (2009).
  • Sahl JW, Steinsland H, Redman JC et al. A comparative genomic analysis of diverse clonal types of enterotoxigenic Escherichia coli reveals pathovar-specific conservation. Infect. Immun. 79(2), 950–960 (2011).
  • Svennerholm AM. From cholera to enterotoxigenic Escherichia coli (ETEC) vaccine development. Indian J. Med. Res. 133(2), 188–196 (2011).
  • Lopez-Gigosos RM, Plaza E, Diez-Diaz RM, Calvo MJ. Vaccination strategies to combat an infectious globe: oral cholera vaccines. J. Glob. Infect. Dis. 3(1), 56–62 (2011).
  • Clemens JD, Sack DA, Harris JR et al. Cross-protection by B subunit-whole cell cholera vaccine against diarrhea associated with heat-labile toxin-producing enterotoxigenic Escherichia coli: results of a large-scale field trial. J. Infect. Dis. 158(2), 372–377 (1988).
  • Peltola H, Siitonen A, Kyronseppa H et al. Prevention of travellers’ diarrhoea by oral B-subunit/whole-cell cholera vaccine. Lancet 338(8778), 1285–1289 (1991).
  • Svennerholm A-M, Glenn G. Vaccines against enterotoxigenic Escherichia coli (ETEC). In: New Generation Vaccines. (4th Edition). Levine MM (Ed). Informa Health Care, NY, USA, 714–722 (2010).
  • Taxt A, Aasland R, Sommerfelt H, Nataro J, Puntervoll P. Heat-stable enterotoxin of enterotoxigenic Escherichia coli as a vaccine target. Infect. Immun. 78(5), 1824–1831 (2010).
  • Liu M, Zhang C, Mateo K, Nataro JP, Robertson DC, Zhang W. Modified heat-stable toxins (HSTA) of enterotoxigenic Escherichia coli lose toxicity but display antigenicity after being genetically fused to heat-labile toxoid LT(R192G). Toxins (Basel) 3(9), 1146–1162 (2011).
  • Qadri F, Saha A, Ahmed T, Al Tarique A, Begum YA, Svennerholm AM. Disease burden due to enterotoxigenic Escherichia coli in the first 2 years of life in an urban community in Bangladesh. Infect. Immun. 75(8), 3961–3968 (2007).
  • Levine MM, Nalin DR, Hoover DL, Bergquist EJ, Hornick RB, Young CR. Immunity to enterotoxigenic Escherichia coli. Infect. Immun. 23(3), 729–736 (1979).
  • Savarino SJ, O’Dowd A, Poole A et al. Advancement of an adhesin-based ETEC vaccine into clinical evaluation. Presented at: 6th International Conference on Vaccines for Enteric Diseases (VED 2011). Cannes, France, 14–16 September 2011.
  • Harro C, Chakraborty S, Feller A et al. Refinement of a human challenge model for evaluation of enterotoxigenic Escherichia coli vaccines. Clin. Vaccine Immunol. 18(10), 1719–1727 (2011).
  • Roy K, Hamilton D, Ostmann MM, Fleckenstein JM. Vaccination with EtpA glycoprotein or flagellin protects against colonization with enterotoxigenic Escherichia coli in a murine model. Vaccine 27(34), 4601–4608 (2009).
  • Roy K, Bartels S, Qadri F, Fleckenstein JM. Enterotoxigenic Escherichia coli elicits immune responses to multiple surface proteins. Infect. Immun. 78(7), 3027–3035 (2010).
  • Ahren C, Jertborn M, Svennerholm AM. Intestinal immune responses to an inactivated oral enterotoxigenic Escherichia coli vaccine and associated immunoglobulin A responses in blood. Infect. Immun. 66(7), 3311–3316 (1998).
  • Qadri F, Ahmed F, Ahmed T, Svennerholm AM. Homologous and cross-reactive immune responses to enterotoxigenic Escherichia coli colonization factors in Bangladeshi children. Infect. Immun. 74(8), 4512–4518 (2006).
  • Hall ER, Wierzba TF, Ahren C et al. Induction of systemic antifimbria and antitoxin antibody responses in Egyptian children and adults by an oral, killed enterotoxigenic Escherichia coli plus cholera toxin B subunit vaccine. Infect. Immun. 69(5), 2853–2857 (2001).
  • Jertborn M, Ahren C, Svennerholm AM. Dose-dependent circulating immunoglobulin A antibody-secreting cell and serum antibody responses in Swedish volunteers to an oral inactivated enterotoxigenic Escherichia coli vaccine. Clin. Diagn. Lab. Immunol. 8(2), 424–428 (2001).
  • Harro C, Sack D, Bourgeois AL et al. A combination vaccine consisting of three live attenuated enterotoxigenic Escherichia coli strains expressing a range of colonization factors and LTB is well tolerated and immunogenic in a placebo-controlled double-blind Phase I trial in healthy adults. Clin. Vaccine Immunol. 18(12), 118–127 (2011).
  • Jertborn M, Ahren C, Holmgren J, Svennerholm AM. Safety and immunogenicity of an oral inactivated enterotoxigenic Escherichia coli vaccine. Vaccine 16(2–3), 255–260 (1998).
  • Lundgren A, Castenbladh-Leach S, Svennerholm A-M. Identification of optimal methods to assess B- and T-cell immune responses against oral enteric vaccines in humans. Presented at: 5th International Conference on Vaccines for Enteric Diseases (VED 2009). Malaga, Spain, 9–11 September 2009.
  • Savarino SJ, Hall ER, Bassily S et al. Oral, inactivated, whole cell enterotoxigenic Escherichia coli plus cholera toxin B subunit vaccine: results of the initial evaluation in children. PRIDE Study Group. J. Infect. Dis. 179(1), 107–114 (1999).
  • Qadri F, Ahmed T, Ahmed F, Begum YA, Sack DA, Svennerholm AM. Reduced doses of oral killed enterotoxigenic Escherichia coli plus cholera toxin B subunit vaccine is safe and immunogenic in Bangladeshi infants 6–17 months of age: dosing studies in different age groups. Vaccine 24(10), 1726–1733 (2006).
  • Mckenzie R, Bourgeois AL, Engstrom F et al. Comparative safety and immunogenicity of two attenuated enterotoxigenic Escherichia coli vaccine strains in healthy adults. Infect. Immun. 74(2), 994–1000 (2006).
  • Lundgren A, Kaim J, Jertborn M. Parallel analysis of mucosally derived B- and T-cell responses to an oral typhoid vaccine using simplified methods. Vaccine 27(33), 4529–4536 (2009).
  • Mckenzie R, Darsley M, Thomas N et al. 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(36), 4731–4739 (2008).
  • Carpenter CM, Hall ER, Randall R et al. Comparison of the antibody in lymphocyte supernatant (ALS) and ELISPOT assays for detection of mucosal immune responses to antigens of enterotoxigenic Escherichia coli in challenged and vaccinated volunteers. Vaccine 24(18), 3709–3718 (2006).
  • Rao MR, Wierzba TF, Savarino SJ et al. Serologic correlates of protection against enterotoxigenic Escherichia coli diarrhea. J. Infect. Dis. 191(4), 562–570 (2005).
  • Steinsland H, Valentiner-Branth P, Gjessing HK, Aaby P, Molbak K, Sommerfelt H. Protection from natural infections with enterotoxigenic Escherichia coli: longitudinal study. Lancet 362(9380), 286–291 (2003).
  • Chowdhury F, Begum YA, Alam MM et al. Concomitant enterotoxigenic Escherichia coli infection induces increased immune responses to Vibrio cholerae O1 antigens in patients with cholera in Bangladesh. Infect. Immun. 78(5), 2117–2124 (2010).
  • Cuburu N, Kweon MN, Song JH et al. Sublingual immunization induces broad-based systemic and mucosal immune responses in mice. Vaccine 25(51), 8598–8610 (2007).
  • Lebens M, Shahabi V, Backstrom M, Houze T, Lindblad N, Holmgren J. Synthesis of hybrid molecules between heat-labile enterotoxin and cholera toxin B subunits: potential for use in a broad-spectrum vaccine. Infect. Immun. 64(6), 2144–2150 (1996).
  • Norton EB, Lawson LB, Freytag LC, Clements JD. Characterization of a mutant Escherichia coli heat-labile toxin, LT(R192G/L211A), as a safe and effective oral adjuvant. Clin. Vaccine Immunol. 18(4), 546–551 (2011).
  • Glenn GM, Villar CP, Flyer DC et al. Safety and immunogenicity of an enterotoxigenic Escherichia coli vaccine patch containing heat-labile toxin: use of skin pretreatment to disrupt the stratum corneum. Infect. Immun. 75(5), 2163–2170 (2007).
  • Lundgren A, Leach S, Jertborn M et al. Clinical trial of an inactivated whole cell ETEC prototype vaccine. Presented at: 6th International Conference on Vaccines for Enteric Diseases (VED 2011). Cannes, France, 14–16 September 2011.
  • Baudner BC, Giudice GD. Determining the activity of mucosal adjuvants. Methods Mol. Biol. 626, 261–285 (2010).
  • Mckenzie R, Bourgeois AL, Frech SA et al. Transcutaneous immunization with the heat-labile toxin (LT) of enterotoxigenic Escherichia coli (ETEC): protective efficacy in a double-blind, placebo-controlled challenge study. Vaccine 25(18), 3684–3691 (2007).
  • Frech SA, Dupont HL, Bourgeois AL et al. Use of a patch containing heat-labile toxin from Escherichia coli against travellers’ diarrhoea: a phase II, randomised, double-blind, placebo-controlled field trial. Lancet 371(9629), 2019–2025 (2008).
  • Katz DE, Delorimier AJ, Wolf MK et al. Oral immunization of adult volunteers with microencapsulated enterotoxigenic Escherichia coli (ETEC) CS6 antigen. Vaccine 21(5–6), 341–346 (2003).
  • Otto W, Najnigier B, Stelmasiak T, Robins-Browne RM. Randomized control trials using a tablet formulation of hyperimmune bovine colostrum to prevent diarrhea caused by enterotoxigenic Escherichia coli in volunteers. Scand. J. Gastroenterol. 46(7–8), 862–868 (2011).
  • Tacket CO, Losonsky G, Link H et al. Protection by milk immunoglobulin concentrate against oral challenge with enterotoxigenic Escherichia coli. N. Engl. J. Med. 318(19), 1240–1243 (1988).
  • Jobling S, Rasulova F, Poole S, Al E. Optimized production and evaluation of pilus adhesin plus enterotoxin B subunit chimers as novel candidate vaccines against diarrhea caused by enterotoxigenic E. coli. cholerae & other bacterial enteric infections. United States-Japan Cooperative Medical Science program. Presented at: 42nd Annual Joint Panel Meeting, TX, USA, 5–7 December 2007.
  • Tobias J, Svennerholm AM, Carlin NI, Lebens M, Holmgren J. Construction of a non-toxigenic Escherichia coli oral vaccine strain expressing large amounts of CS6 and inducing strong intestinal and serum anti-CS6 antibody responses in mice. Vaccine 29(48), 8863–8869 (2011).
  • Sack DA, Shimko J, Torres O et al. Randomised, double-blind, safety and efficacy of a killed oral vaccine for enterotoxigenic E. coli diarrhoea of travellers to Guatemala and Mexico. Vaccine 25(22), 4392–4400 (2007).
  • Bourgeois AL, Halpern J, Grahek S et al. Vaccination of travellers to Guatemala (GU) and Mexico (MX) with an oral killed vaccine (OKV) for enterotoxigenic E coli (ETEC): Impact of vaccine “take” on risk of ETEC disease and infection with enteric pathogens. Presented at: 4th International Conference on Vaccines for Enteric Diseases (VED 2007). Lisbon, Portugal, 25–27 April 2007.
  • Tobias J, Lebens M, Bolin I, Wiklund G, Svennerholm AM. Construction of non-toxic Escherichia coli and Vibrio cholerae strains expressing high and immunogenic levels of enterotoxigenic E. coli colonization factor I fimbriae. Vaccine 26(6), 743–752 (2008).
  • Tobias J, Lebens M, Kallgard S, Nicklasson M, Svennerholm AM. Role of different genes in the CS6 operon for surface expression of enterotoxigenic Escherichia coli colonization factor CS6. Vaccine 26(42), 5373–5380 (2008).
  • Tobias J, Holmgren J, Hellman M, Nygren E, Lebens M, Svennerholm AM. Over-expression of major colonization factors of enterotoxigenic Escherichia coli, alone or together, on non-toxigenic E. coli bacteria. Vaccine 28(43), 6977–6984 (2010).
  • Holmgren J, Blomquist M, Bourgeois AL et al. Preclinical evaluation of an oral inactivated ETEC vaccine, based on E. coli overexpressing CFA/I, CS3, CS5, and CS6 together with LTB/CTB subunit, and of the adjuvant effect of co-administration with dmLT. Presented at: 6th International Conference on Vaccines for Enteric Diseases (VED 2011). Cannes, France, 14–16 September 2011.
  • Daley A, Randall R, Darsley M et al. Genetically modified enterotoxigenic Escherichia coli vaccines induce mucosal immune responses without inflammation. Gut 56(11), 1550–1556 (2007).
  • Turner AK, Stephens JC, Beavis JC et al. Generation and characterization of a live attenuated enterotoxigenic Escherichia coli combination vaccine expressing six colonization factors and LTB. Clin. Vaccine Immunol. 18(12), 128–135 (2011).
  • Harro C, Sack D, Darsley M et al. Volunteers receiving live attenuated ETEC vaccine (ACE527) have reduced severity of illness following H10407 challenge. Presented at: 6th International Conference on Vaccines for Enteric Diseases (VED 2011). Cannes, France, 14–16 September 2011.
  • Barry EM, Wang J, Wu T, Davis T, Levine MM. Immunogenicity of multivalent Shigella-ETEC candidate vaccine strains in a guinea pig model. Vaccine 24(18), 3727–3734 (2006).
  • Levine MM, Svennerholm A-M. Immunoprophylaxis and immunologic control. In: Textbook of Travel Medicine and Health (3rd Edition). BC Decker, ON, Canada, 215–232 (2007).
  • Roland KL, Cloninger C, Kochi SK et al. Construction and preclinical evaluation of recombinant Peru-15 expressing high levels of the cholera toxin B subunit as a vaccine against enterotoxigenic Escherichia coli. Vaccine 25(51), 8574–8584 (2007).
  • Sack D, Qadri F, Svennerholm AM. Determinants of responses to oral vaccines in developing countries. Ann. Nestlé 66, 71–963 (2008).
  • Ahmed T, Svennerholm AM, Al Tarique A, Sultana GN, 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(9), 1433–1439 (2009).
  • Ahmed T, Arifuzzaman M, Lebens M, Qadri F, Lundgren A. CD4+ T-cell responses to an oral inactivated cholera vaccine in young children in a cholera endemic country and the enhancing effect of zinc supplementation. Vaccine 28(2), 422–429 (2009).
  • Wenneras C, Erling V. Prevalence of enterotoxigenic Escherichia coli-associated diarrhoea and carrier state in the developing world. J. Health Popul. Nutr. 22(4), 370–382 (2004).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.