A systematic review of experimental infections with enterotoxigenic Escherichia coli (ETEC)

Vaccine

Volumn 29, Issue 35, 2011, Pages 5869-5885

  Porter, Chad K ^a   Riddle, Mark S ^a   Tribble, David R ^b   Louis Bougeois, A ^c   McKenzie, Robin ^c   Isidean, Sandra D ^a   Sebeny, Peter ^d   Savarino, Stephen J ^a  

^a NAVAL MEDICAL RESEARCH CENTER   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d US Naval Medical Research Unit No 3 Egypt   (Egypt)

Author keywords

Challenge; Clinical trial; Enterotoxigenic Escherichia coli

Indexed keywords

ANTIBIOTIC AGENT; ANTIBODY; ANTIGEN; BACTERIAL VACCINE; BICARBONATE; BISMUTH SALICYLATE; COLONIZATION FACTOR ANTIBODY; COTRIMOXAZOLE; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; INFUSION FLUID; LACTOBACILLUS VACCINE; LIVE VACCINE; O ANTIGEN; ORAL REHYDRATION SOLUTION; PLACEBO; SOMATIC ANTIGEN; UNCLASSIFIED DRUG;

ABDOMINAL CRAMP; ABDOMINAL PAIN; ACUTE INFECTIOUS GASTROENTERITIS; ANOREXIA; ANTIBIOTIC THERAPY; ANTIBODY TITER; BACTERIAL COLONIZATION; BACTERIAL STRAIN; CAMPYLOBACTER JEJUNI; COLONY FORMING UNIT; DATA ANALYSIS; DISEASE COURSE; DISEASE DURATION; DISEASE SEVERITY; ENTERITIS; ENTEROPATHOGENIC ESCHERICHIA COLI INFECTION; ENTEROTOXIGENIC ESCHERICHIA COLI; ENTEROTOXIGENIC ESCHERICHIA COLI B7A; ENTEROTOXIGENIC ESCHERICHIA COLI DS26 1; ENTEROTOXIGENIC ESCHERICHIA COLI E24377A; ENTEROTOXIGENIC ESCHERICHIA COLI H10407; ENTEROTOXIGENIC ESCHERICHIA COLI LSN03 016011 A; ENTEROTOXIGENIC ESCHERICHIA COLI WS0115A; EXPERIMENTAL INFECTION; FECES ANALYSIS; FEVER; GASTROENTERITIS; HEADACHE; HUMAN; IMMUNOPROPHYLAXIS; INFECTION PREVENTION; INFECTIOUS DIARRHEA; INNATE IMMUNITY; IRRITABLE COLON; LACTOBACILLUS ACIDOPHILUS; LOOSE FECES; MALAISE; NAUSEA; ORAL REHYDRATION THERAPY; OUTCOME ASSESSMENT; PATHOGENICITY; PRIORITY JOURNAL; REVIEW; SEROLOGY; SYSTEMATIC REVIEW; VERNER MORRISON SYNDROME; VIBRIO CHOLERAE; VOMITING;

ADULT; ANTIBODIES, BACTERIAL; CLINICAL TRIALS AS TOPIC; DIARRHEA; ENTEROTOXIGENIC ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; HUMAN EXPERIMENTATION; HUMANS; MALE; MIDDLE AGED; VIRULENCE; YOUNG ADULT;

EID: 79960728374     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.05.021     Document Type: Review

References (77)

1. DuPont H.L., Formal S.B., Hornick R.B., Snyder M.J., Libonati J.P., Sheahan D.G., et al. Pathogenesis of Escherichia coli diarrhea. N Engl J Med 1971, 285(1):1-9.
2. Bill and Melinda Gates Foundation. ; accessed 26 February 2010. http://www.gatesfoundation.org/.
3. Svennerholm A.M., Tobias J. Vaccines against enterotoxigenic Escherichia coli. Expert Rev Vaccines 2008, 7(6):795-804.
4. Cryz S.J., Kaper J., Tacket C., Nataro J., Levine M.M. Vibrio cholerae CVD103-HgR live oral attenuated vaccine: construction, safety, immunogenicity, excretion and non-target effects. Dev Biol Stand 1995, 84:237-244.
5. Moorthy V.S., Diggs C., Ferro S., Good M.F., Herrera S., Hill A.V., et al. Report of a consultation on the optimization of clinical challenge trials for evaluation of candidate blood stage malaria vaccines, 18-19 March 2009, Bethesda, MD, USA. Vaccine 2009, 27(42):5719-5725.
6. Egger M., Smith G.D., Altman D.G. Systematic reviews in health care 2001, BMJ Publishing Group, London, GB, p. 487. 2nd ed.
7. Shojania K.G., et al. Chapter 3. Evidence-based review methodology. Making health care safer: a critical analysis of patient safety practices 2001, University of California at San Francisco (UCSF)-Stanford University Evidence-based Practice Center, p. 29-38.
8. Simmonds M.C., Higgins J.P., Stewart L.A., Tierney J.F., Clarke M.J., Thompson S.G. Meta-analysis of individual patient data from randomized trials: a review of methods used in practice. Clin Trials 2005, 2(3):209-217.
9. DerSimonian R., Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986, 7(3):177-188.
10. Higgins J.P., Whitehead A., Turner R.M., Omar R.Z., Thompson S.G. Meta-analysis of continuous outcome data from individual patients. Stat Med 2001, 20(15):2219-2241.
11. Turner R.M., Omar R.Z., Yang M., Goldstein H., Thompson S.G. A multilevel model framework for meta-analysis of clinical trials with binary outcomes. Stat Med 2000, 19(24):3417-3432.
12. Evans D.G., Satterwhite T.K., Evans D.J., DuPont H.L. Differences in serological responses and excretion patterns of volunteers challenged with enterotoxigenic Escherichia coli with and without the colonization factor antigen. Infect Immun 1978, 19(3):883-888.
13. Satterwhite T.K., Evans D.G., DuPont H.L., Evans D.J. Role of Escherichia coli colonisation factor antigen in acute diarrhoea. Lancet 1978, 2(8082):181-184.
14. Graham D.Y., Estes M.K., Gentry L.O. Double-blind comparison of bismuth subsalicylate and placebo in the prevention and treatment of enterotoxigenic Escherichia coli-induced diarrhea in volunteers. Gastroenterology 1983, 85(5):1017-1022.
15. Graham D.Y., Evans D.G. Prevention of diarrhea caused by enterotoxigenic Escherichia coli: lessons learned with volunteers. Rev Infect Dis 1990, 12(Suppl. 1):S68-72.
16. Levine M., Morris J.G., Losonsky G., Boedeker E.C., Rowe B. Fimbriae (pili) adhesins as vaccines. Protein-carbohydrate interactions in biologic systems: the molecular biology of microbial pathogenicity 1986, 143-145. Academic Press, London. D.L. Lark, S. Mormakr, B.-E. Uhlin, H. Wolf-Wath (Eds.).
17. Tacket C.O., Levine M.M. Vaccines against enterotoxigenic Escherichia coli infections: part ii: live oral vaccines and subunit (purified fimbriae and toxin subunit) vaccines. New generation vaccines 1997, 879. Marcel Dekker, Inc., New York. second ed. M.M. Levine, G.C. Woodrow, J.B. Kaper, G.S. Cobon (Eds.).
18. Lanata C.F., Kaper J.B., Baldini M.M., Black R.E., Levine M.M. Sensitivity and specificity of DNA probes with the stool blot technique for detection of Escherichia coli enterotoxins. J Infect Dis 1985, 152(5):1087-1090.
19. Levine M.M., Bergquist E.J., Nalin D.R., Waterman D.H., Hornick R.B., Young C.R., et al. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1978, 1(8074):1119-1122.
20. DuPont H.L., Cooperstock M., Corrado M.L., Fekety R., Murray D.M. Evaluation of new anti-infective drugs for the treatment of acute infectious diarrhea. Infectious Diseases Society of America and the Food and Drug Administration. Clin Infect Dis 1992, 15(Suppl 1):S228-S235.
21. McKenzie R., Bourgeois A.L., Frech S.A., Flyer D.C., Bloom A., Kazempour K., 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 2007, 25(18):3684-3691.
22. Frech S.A., Dupont H.L., Bourgeois A.L., McKenzie R., Belkind-Gerson J., Figueroa J.F., 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 2008, 371(9629):2019-2025.
23. Bolin I., Wiklund G., Qadri F., Torres O., Bourgeois A.L., Savarino S., Svennerholm A.M. 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 2006, 44(11):3872-3877.
24. Mattila L. Clinical features and duration of traveler's diarrhea in relation to its etiology. Clin Infect Dis 1994, 19(4):728-734.
25. Sanders J.W., Isenbarger D.W., Walz S.E., Pang L.W., Scott D.A., Tamminga C., et al. An observational clinic-based study of diarrheal illness in deployed United States military personnel in Thailand: presentsion and outcome of Campylobacter infection. Am J Trop Med Hyg 2002, 67(5):533-538.
26. Qadri F., Svennerholm A.M., Faruque A.S., Sack R.B. Enterotoxigenic Escherichia coli in developing countries: epidemiology, microbiology, clinical features, treatment, and prevention. Clin Microbiol Rev 2005, 18(3):465-483.
27. Qadri F., Das S.K., Faruque A.S., Fuchs G.J., Albert M.J., Sack R.B., et al. Prevalence of toxin types and colonization factors in enterotoxigenic Escherichia coli isolated during a 2-year period from diarrheal patients in Bangladesh. J Clin Microbiol 2000, 38(1):27-31.
28. Porter C.K., Riddle M.S., Tribble D.R., Putnam S.D., Rockabrand D.M., Frenck R.W., et al. The epidemiology of travelers' diarrhea in Incirlik, Turkey: a region with a predominance of heat-stabile toxin producing enterotoxigenic Escherichia coli. Diagn Microbiol Infect Dis 2010, 66(3):241-247.
29. Intercell provides update on clinical trials for the patch-based Travelers' Diarrhea vaccine. ; accessed 15 December 2010, Editor. http://www.intercell.com/.
30. Evans D.G., Evans D.J., Opekun A.R., Graham D.Y. Non-replicating oral whole cell vaccine protective against enterotoxigenic Escherichia coli (ETEC) diarrhea: stimulation of anti-CFA (CFA/I) and anti-enterotoxin (anti-LT) intestinal IgA and protection against challenge with ETEC belonging to heterologous serotypes. FEMS Microbiol Immunol 1988, 1(3):117-125.
31. Evans D.J., Evans D.G., Opekun A.R., Graham D.Y. Immunoprotective oral whole cell vaccine for enterotoxigenic Escherichia coli diarrhea prepared by in situ destruction of chromosomal and plasmid DNA with colicin E2. FEMS Microbiol Immunol 1988, 1(1):9-18.
32. Rao G., Aliwalas M.G., Slaymaker E., Brown B. Bismuth revisited: an effective way to prevent travelers' diarrhea. J Travel Med 2004, 11(4):239-241.
33. DuPont H.L., Ericsson C.D., Johnson P.C., de la Cabada F.J. Use of bismuth subsalicylate for the prevention of travelers' diarrhea. Rev Infect Dis 1990, 12(Suppl. 1):S64-S67.
34. DuPont H.L., Ericsson C.D., Johnson P.C., Bitsura J.A., DuPont M.W., de la Cabada F.J. Prevention of travelers' diarrhea by the tablet formulation of bismuth subsalicylate. JAMA 1987, 257(10):1347-1350.
35. Steffen R., DuPont H.L., Heusser R., Helminger A., Witassek F., Manhart M.D., et al. Prevention of traveler's diarrhea by the tablet form of bismuth subsalicylate. Antimicrob Agents Chemother 1986, 29(4):625-627.
36. Black R.E., Levine M.M., Clements M.L., Cisneros L., Daya V. Treatment of experimentally induced enterotoxigenic Escherichia coli diarrhea with trimethoprim, trimethoprim-sulfamethoxazole, or placebo. Rev Infect Dis 1982, 4(2):540-545.
37. Dupont H.L., Ericsson C.D., Galindo E., Dupont M.W., Mendiola Gomez J. Antimicrobial therapy of travellers' diarrhoea. Scand J Gastroenterol Suppl 1983, 84:99-105.
38. Thornton S.A., Wignall S.F., Kilpatrick M.E., Bourgeois A.L., Gardiner C., Batchelor R.A., et al. Norfloxacin compared to trimethoprim/sulfamethoxazole for the treatment of travelers' diarrhea among U.S. military personnel deployed to South America and West Africa. Mil Med 1992, 157(2):55-58.
39. Ericsson C.D., Johnson P.C., Dupont H.L., Morgan D.R., Bitsura J.A., de la Cabada F.J. Ciprofloxacin or trimethoprim-sulfamethoxazole as initial therapy for travelers' diarrhea. A placebo-controlled, randomized trial. Ann Intern Med 1987, 106(2):216-220.
40. Tacket C.O., Losonsky G., Link H., Hoang Y., Guesry P., Hilpert H., et al. Protection by milk immunoglobulin concentrate against oral challenge with enterotoxigenic Escherichia coli. N Engl J Med 1988, 318(19):1240-1243.
41. Freedman D.J., Tacket C.O., Delehanty A., Maneval D.R., Nataro J., Crabb J.H. Milk immunoglobulin with specific activity against purified colonization factor antigens can protect against oral challenge with enterotoxigenic Escherichia coli. J Infect Dis 1998, 177(3):662-667.
42. Walker R.I., Steele D., Aguado T. Analysis of strategies to successfully vaccinate infants in developing countries against enterotoxigenic E. coli (ETEC) disease. Vaccine 2007, 25(14):2545-2566.
43. Dhar U., Bennish M.L., Khan W.A., Seas C., Huq Khan E., Albert M.J., et al. Clinical features, antimicrobial susceptibility and toxin production in Vibrio cholerae O139 infection: comparison with V. cholerae O1 infection. Trans R Soc Trop Med Hyg 1996, 90(4):402-405.
44. Harro C., DeNearing B., Marcum A., Feller A., Chakraborty S., Hnizda B., et al. Development of a low-dose challenge model for evaluation of vaccines for enterotoxigenic E. coli (ETEC) in volunteers. 5th International Vaccines for Enteric Diseases Conference 2009.
45. Yamamoto T., Echeverria P. Detection of the enteroaggregative Escherichia coli heat-stable enterotoxin 1 gene sequences in enterotoxigenic E. coli strains pathogenic for humans. Infect Immun 1996, 64(4):1441-1445.
46. Fleckenstein J.M., Kopecko D.J., Warren R.L., Elsinghorst E.A. Molecular characterization of the tia invasion locus from enterotoxigenic Escherichia coli. Infect Immun 1996, 64(6):2256-2265.
47. Lindenthal C., Elsinghorst E.A. Enterotoxigenic Escherichia coli TibA glycoprotein adheres to human intestine epithelial cells. Infect Immun 2001, 69(1):52-57.
48. Fleckenstein J.M., Lindler L.E., Elsinghorst E.A., Dale J.B. Identification of a gene within a pathogenicity island of enterotoxigenic Escherichia coli H10407 required for maximal secretion of the heat-labile enterotoxin. Infect Immun 2000, 68(5):2766-2774.
49. Patel S.K., Dotson J., Allen K.P., Fleckenstein J.M. Identification and molecular characterization of EatA, an autotransporter protein of enterotoxigenic Escherichia coli. Infect Immun 2004, 72(3):1786-1794.
50. Roy K., Hamilton D., Allen K.P., Randolph M.P., Fleckenstein J.M. The EtpA exoprotein of enterotoxigenic Escherichia coli promotes intestinal colonization and is a protective antigen in an experimental model of murine infection. Infect Immun 2008, 76(5):2106-2112.
51. Miller F.G., Grady C. The ethical challenge of infection-inducing challenge experiments. Clin Infect Dis 2001, 33(7):1028-1033.
52. Halvorson H.A., Schlett C.D., Riddle M.S. Postinfectious irritable bowel syndrome-a meta-analysis. Am J Gastroenterol 2006, 101(8):1894-1899. quiz 1942.
53. Thabane M., Kottachchi D.T., Marshall J.K. Systematic review and meta-analysis: the incidence and prognosis of post-infectious irritable bowel syndrome. Aliment Pharmacol Ther 2007, 26(4):535-544.
54. Okhuysen P.C., Jiang Z.D., Carlin L., Forbes C., DuPont H.L. Post-diarrhea chronic intestinal symptoms and irritable bowel syndrome in North American travelers to Mexico. Am J Gastroenterol 2004, 99(9):1774-1778.
55. Tuteja A.K., Talley N.J., Gelman S.S., Alder S.C., Thompson C., Tolman K., et al. Development of functional diarrhea, constipation, irritable bowel syndrome, and dyspepsia during and after traveling outside the USA. Dig Dis Sci 2008, 53(1):271-276.
56. Garcia Rodriguez L.A., Ruigomez A., Panes J. Acute gastroenteritis is followed by an increased risk of inflammatory bowel disease. Gastroenterology 2006, 130(6):1588-1594.
57. Porter C.K., Tribble D.R., Aliaga P.A., Halvorson H.A., Riddle M.S. Infectious gastroenteritis and risk of developing inflammatory Bowel disease. Gastroenterology 2008.
58. Ternhag A., Torner A., Svensson A., Ekdahl K., Giesecke J. Short- and long-term effects of bacterial gastrointestinal infections. Emerg Infect Dis 2008, 14(1):143-148.
59. Tribble D.R., Baqar S., Carmolli M.P., Porter C., Pierce K.K., Sadigh K., et al. Campylobacter jejuni strain CG8421: a refined model for the study of Campylobacteriosis and evaluation of Campylobacter vaccines in human subjects. Clin Infect Dis 2009, 49(10):1512-1519.
60. Tribble D.R., Baqar S., Scott D.A., Oplinger M.L., Trespalacios F., Rollins D., et al. Assessment of the duration of protection in Campylobacter jejuni experimental infection in humans. Infect Immun 2010, 78(4):1750-1759.
61. Levine M.M., Caplan E.S., Waterman D., Cash R.A., Hornick R.B., Snyder M.J. Diarrhea caused by Escherichia coli that produce only heat-stable enterotoxin. Infect Immun 1977, 17(1):78-82.
62. Levine M.M., Nalin D.R., Hoover D.L., Bergquist E.J., Hornick R.B., Young C.R. Immunity to enterotoxigenic Escherichia coli. Infect Immun 1979, 23(3):729-736.
63. Levine M.M., Rennels M.B., Cisneros L., Hughes T.P., Nalin D.R., Young C.R. Lack of person-to-person transmission of enterotoxigenic Escherichia coli despite close contact. Am J Epidemiol 1980, 111(3):347-355.
64. Clements M.L., Levine M.M., Black R.E., Robins-Browne R.M., Cisneros L.A., Drusano G.L., et al. Lactobacillus prophylaxis for diarrhea due to enterotoxigenic Escherichia coli. Antimicrob Agents Chemother 1981, 20(1):104-108.
65. Levine M.M., Black R.E., Brinton C.C., Clements M.L., Fusco P., Hughes T.P., et al. Reactogenicity, immunogenicity and efficacy studies of Escherichia coli type 1 somatic pili parenteral vaccine in man. Scand J Infect Dis Suppl 1982, 33:83-95.
66. Evans D.G., Graham D.Y., Evans D.J. Administration of purified colonization factor antigens (CFA/I, CFA/II) of enterotoxigenic Escherichia coli to volunteers. Response to challenge with virulent enterotoxigenic Escherichia coli. Gastroenterology 1984, 87(4):934-940.
67. Levine M.M., Ristaino P., Marley G., Smyth C., Knutton S., Boedeker E., et al. Coli surface antigens 1 and 3 of colonization factor antigen II-positive enterotoxigenic Escherichia coli: morphology, purification, and immune responses in humans. Infect Immun 1984, 44(2):409-420.
68. Tacket C.O., Reid R.H., Boedeker E.C., Losonsky G., Nataro J.P., Bhagat H., et al. Enteral immunization and challenge of volunteers given enterotoxigenic E. coli CFA/II encapsulated in biodegradable microspheres. Vaccine 1994, 12(14):1270-1274.
69. Tacket C.O., Losonsky G., Livio S., Edelman R., Crabb J., Freedman D. Lack of prophylactic efficacy of an enteric-coated bovine hyperimmune milk product against enterotoxigenic Escherichia coli challenge administered during a standard meal. J Infect Dis 1999, 180(6):2056-2059.
70. Coster T.S., Wolf M.K., Hall E.R., Cassels F.J., Taylor D.N., Liu C.T., et al. Immune response, ciprofloxacin activity, and gender differences after human experimental challenge by two strains of enterotoxigenic Escherichia coli. Infect Immun 2007, 75(1):252-259.
71. McKenzie R., Darsley M., Thomas N., Randall R., Carpenter C., Forbes E., 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 2008, 26(36):4731-4739.
72. McKenzie R, Porter C, Cantrell J, DeNearing B, O'Dowd A, Grahek S, et al. Volunteer Challenge with Enterotoxigenic Escherichia coli that Express Intestinal Colonization Factor Fimbriae CS17 and CS19. J Infect Dis. doi:10.1093/infdis/JIR220.
73. Sack D.A., Merson M.H., Wells J.G., Sack R.B., Morris G.K. Diarrhoea associated with heat-stable enterotoxin-producing strains of Escherichia coli. Lancet 1975, 2(7928):239-241.
74. Scotland S.M., McConnell M.M., Willshaw G.A., Rowe B., Field A.M. Properties of wild-type strains of enterotoxigenic Escherichia coli which produce colonization factor antigen II, and belong to serogroups other than O6. J Gen Microbiol 1985, 131(9):2327-2333.
75. Center for Disease Control Diarrheal illness on a cruise ship caused by enterotoxigenic Escherichia coli. MMWR 1976, 25:229.
76. Evans D.J., Evans D.G. Three characteristics associated with enterotoxigenic Escherichia coli isolated from man. Infect Immun 1973, 8(3):322-328.
77. Khalil S.B., Cassels F.J., Shaheen H.I., Pannell L.K., El-Ghorab N., Kamal K., et al. Characterization of an enterotoxigenic Escherichia coli strain from Africa expressing a putative colonization factor. Infect Immun 1999, 67(8):4019-4026.