1921
Volume 80, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Fifty-one published studies of travelers’ diarrhea (TD) were examined to look for regional differences in pathogens identified. Enterotoxigenic was detected in 1,678/5,518 (30.4%) of TD cases overall, with rates in Latin America/Caribbean (L. America), Africa, south Asia, and Southeast Asia of 1,109/3,302 (33.6%), 389/1,217 (31.2%), 153/499 (30.6%), and 36/500 (7.2%), respectively ( < 0.001). Enteroaggregative was the second most common agent in L. America, found in 166/689 (24.1%), compared with 3/165 (1.8%) in Africa and 33/206 (16%) in south Asia ( < 0.001). Other significantly regional differences were seen for enteropathogenic , diffusely adherent , , spp., , spp., , , rotavirus, noroviruses, and . The regional differences in pathogen identification identified will serve as a baseline for antimicrobial therapy recommendations and vaccines strategies.

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2009-04-01
2017-11-25
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References

  1. Kean BH, 1963. The diarrhea of travelers to Mexico. Summary of five-year study. Ann Intern Med 59 : 605–614.
  2. DuPont HL, Haynes GA, Pickering LK, Tjoa W, Sullivan P, Olarte J, 1977. Diarrhea of travelers to Mexico. Relative susceptibility of United States and Latin American students attending a Mexican University. Am J Epidemiol 105 : 37–41.
  3. Steffen R, van der Linde F, Gyr K, Schar M, 1983. Epidemiology of diarrhea in travelers. JAMA 249 : 1176–1180.
  4. Hoge CW, Shlim DR, Rajah R, Triplett J, Shear M, Rabold JG, Echeverria P, 1993. Epidemiology of diarrhoeal illness associated with coccidian-like organism among travellers and foreign residents in Nepal. Lancet 341 : 1175–1179.
  5. Taylor DN, Houston R, Shlim DR, Bhaibulaya M, Ungar BL, Echeverria P, 1988. Etiology of diarrhea among travelers and foreign residents in Nepal. JAMA 260 : 1245–1248.
  6. Varela G, Kean BH, Barrett EL, Keegan CJ, 1959. The diarrhea of travelers. II. Bacteriologic studies of U.S. students in Mexico. Am J Trop Med Hyg 8 : 353–357.
  7. DuPont HL, Formal SB, Hornick RB, Snyder MJ, Libonati JP, Sheahan DG, LaBrec EH, Kalas JP, 1971. Pathogenesis of Escherichia coli diarrhea. N Engl J Med 285 : 1–9.
  8. Butzler JP, Dekeyser P, Detrain M, Dehaen F, 1973. Related vibrio in stools. J Pediatr 82 : 493–495.
  9. Bishop RF, Davidson GP, Holmes IH, Ruck BJ, 1973. Virus particles in epithelial cells of duodenal mucosa from children with acute non-bacterial gastroenteritis. Lancet 2 : 1281–1283.
  10. Dolin R, Blacklow NR, DuPont H, Formal S, Buscho RF, Kasel JA, Chames RP, Hornick R, Chanock RM, 1971. Transmission of acute infectious nonbacterial gastroenteritis to volunteers by oral administration of stool filtrates. J Infect Dis 123 : 307–312.
  11. Gorbach SL, Kean BH, Evans DG, Evans DJ Jr, Bessudo D, 1975. Travelers’ diarrhea and toxigenic Escherichia coli. N Engl J Med 292 : 933–936.
  12. DuPont HL, Reves RR, Galindo E, Sullivan PS, Wood LV, Mendiola JG, 1982. Treatment of travelers’ diarrhea with trimethoprim/sulfamethoxazole and with trimethoprim alone. N Engl J Med 307 : 841–844.
  13. Guerena-Burgueno F, Hall ER, Taylor DN, Cassels FJ, Scott DA, Wolf MK, Roberts ZJ, Nesterova GV, Alving CR, Glenn GM, 2002. Safety and immunogenicity of a prototype enterotoxigenic Escherichia coli vaccine administered transcutaneously. Infect Immun 70 : 1874–1880.
  14. Peltola H, Siitonen A, Kyronseppa H, Simula I, Mattila L, Oksanen P, Kataja MJ, Cadoz M, 1991. Prevention of travellers’ diarrhoea by oral B-subunit/whole-cell cholera vaccine. Lancet 338 : 1285–1289.
  15. Yamada S, Matsushita S, Dejsirilert S, Kudoh Y, 1997. Incidence and clinical symptoms of Aeromonas-associated travellers’ diarrhoea in Tokyo. Epidemiol Infect 119 : 121–126.
  16. Clemens JD, Sack DA, Harris JR, Chakraborty J, Neogy PK, Stanton B, Huda N, Khan MU, Kay BA, Khan MR, et al., 1988. 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 : 372–377.
  17. Glenn GM, Flyer DC, Ellingsworth LR, Frech SA, Frerichs DM, Seid RC, Yu J, 2007. Transcutaneous immunization with heat-labile enterotoxin: development of a needle-free vaccine patch. Expert Rev Vaccines 6 : 809–819.
  18. McKenzie R, Bourgeois AL, Frech SA, Flyer DC, Bloom A, Kazempour K, Glenn GM, 2007. 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 : 3684–3691.
  19. Frech SA, DuPont HL, Bourgeois AL, McKenzie R, Belkind-Gerson J, Figueroa JF, Okhuysen PC, Guerrero NH, Martinez-Sandoval FG, Melendez-Romero JH, Jiang ZD, Asturias EJ, Halpern J, Torres OR, Hoffman AS, Villar CP, Kassem RN, Flyer DC, Andersen BH, Kazempour K, Breisch SA, Glenn GM, 2008. 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 : 2019–2025.
  20. Huang DB, Mohamed JA, Nataro JP, DuPont HL, Jiang ZD, Okhuysen PC, 2007. Virulence characteristics and the molecular epidemiology of enteroaggregative Escherichia coli isolates from travellers to developing countries. J Med Microbiol 56 : 1386–1392.
  21. Nataro JP, 2005. Enteroaggregative Escherichia coli pathogenesis. Curr Opin Gastroenterol 21 : 4–8.
  22. Adachi JA, Jiang ZD, Mathewson JJ, Verenkar MP, Thompson S, Martinez-Sandoval F, Steffen R, Ericsson CD, DuPont HL, 2001. Enteroaggregative Escherichia coli as a major etiologic agent in traveler’s diarrhea in 3 regions of the world. Clin Infect Dis 32 : 1706–1709.
  23. Hoge CW, Gambel JM, Srijan A, Pitarangsi C, Echeverria P, 1998. Trends in antibiotic resistance among diarrheal pathogens isolated in Thailand over 15 years. Clin Infect Dis 26 : 341–345.
  24. Kuschner RA, Trofa AF, Thomas RJ, Hoge CW, Pitarangsi C, Amato S, Olafson RP, Echeverria P, Sadoff JC, Taylor DN, 1995. Use of azithromycin for the treatment of Campylobacter enteritis in travelers to Thailand, an area where ciprofloxacin resistance is prevalent. Clin Infect Dis 21 : 536–541.
  25. Tribble DR, Sanders JW, Pang LW, Mason C, Pitarangsi C, Baqar S, Armstrong A, Hshieh P, Fox A, Maley EA, Lebron C, Faix DJ, Lawler JV, Nayak G, Lewis M, Bodhidatta L, Scott DA, 2007. Traveler’s diarrhea in Thailand: randomized, double-blind trial comparing single-dose and 3-day azithromycin-based regimens with a 3-day levofloxacin regimen. Clin Infect Dis 44 : 338–346.
  26. DuPont HL, Ericsson CD, Mathewson JJ, DuPont MW, 1992. Five versus three days of ofloxacin therapy for traveler’s diarrhea: a placebo-controlled study. Antimicrob Agents Chemother 36 : 87–91.
  27. DuPont HL, Haake R, Taylor DN, Ericsson CD, Jiang ZD, Okhuysen PC, Steffen R, 2007. Rifaximin treatment of pathogen-negative travelers’ diarrhea. J Travel Med 14 : 16–19.
  28. Caeiro JP, Estrada-Garcia MT, Jiang ZD, Mathewson JJ, Adachi JA, Steffen R, DuPont HL, 1999. Improved detection of enterotoxigenic Escherichia coli among patients with travelers’ diarrhea, by use of the polymerase chain reaction technique. J Infect Dis 180 : 2053–2055.
  29. Iijima Y, Tanaka S, Miki K, Kanamori S, Toyokawa M, Asari S, 2007. Evaluation of colony-based examinations of diarrheagenic Escherichia coli in stool specimens: low probability of detection because of low concentrations, particularly during the early stage of gastroenteritis. Diagn Microbiol Infect Dis 58 : 303–308.
  30. Meraz IM, Jiang ZD, Ericsson CD, Bourgeois AL, Steffen R, Taylor DN, Hernandez N, DuPont HL, 2008. Enterotoxigenic Escherichia coli and diffusely adherent E. coli as likely causes of a proportion of pathogen-negative travelers’ diarrhea: a PCR-based study. J Travel Med 15 : 412–418.
  31. Vargas M, Gascon J, Gallardo F, Jimenez De Anta MT, Vila J, 1998. Prevalence of diarrheagenic Escherichia coli strains detected by PCR in patients with travelers’ diarrhea. Clin Microbiol Infect 4 : 682–688.
  32. Ko G, Garcia C, Jiang ZD, Okhuysen PC, Belkind-Gerson J, Glass RI, DuPont HL, 2005. Noroviruses as a cause of traveler’s diarrhea among students from the United States visiting Mexico. J Clin Microbiol 43 : 6126–6129.
  33. Black RE, 1990. Epidemiology of travelers’ diarrhea and relative importance of various pathogens. Rev Infect Dis 12 (Suppl 1): S73–S79.
  34. DuPont HL, Jiang ZD, Okhuysen PC, Ericsson CD, de la Cabada FJ, Ke S, DuPont MW, Martinez-Sandoval F, 2005. A randomized, double-blind, placebo-controlled trial of rifaximin to prevent travelers’ diarrhea. Ann Intern Med 142 : 805–812.
  35. Sack DA, Kaminsky DC, Sack RB, Itotia JN, Arthur RR, Kapikian AZ, Orskov F, Orskov I, 1978. Prophylactic doxycycline for travelers’ diarrhea. Results of a prospective double-blind study of Peace Corps volunteers in Kenya. N Engl J Med 298 : 758–763.
  36. Salam I, Katelaris P, Leigh-Smith S, Farthing MJ, 1994. Randomised trial of single-dose ciprofloxacin for travellers’ diarrhoea. Lancet 344 : 1537–1539.
  37. Jiang ZD, Lowe B, Verenkar MP, Ashley D, Steffen R, Tornieporth N, von Sonnenburg F, Waiyaki P, DuPont HL, 2002. Prevalence of enteric pathogens among international travelers with diarrhea acquired in Kenya (Mombasa), India (Goa), or Jamaica (Montego Bay). J Infect Dis 185 : 497–502.
  38. Bolivar R, Conklin RH, Vollet JJ, Pickering LK, DuPont HL, Walters DL, Kohl S, 1978. Rotavirus in travelers’ diarrhea: study of an adult student population in Mexico. J Infect Dis 137 : 324–327.
  39. DuPont HL, Evans DG, Rios N, Cabada FJ, Evans DJ Jr, DuPont MW, 1982. Prevention of travelers’ diarrhea with trimethoprim-sulfamethoxazole. Rev Infect Dis 4 : 533–539.
  40. DuPont HL, Olarte J, Evans DG, Pickering LK, Galindo E, Evans DJ, 1976. Comparative susceptibility of Latin American and United States students to enteric pathogens. N Engl J Med 295 : 1520–1521.
  41. DuPont HL, Sullivan P, Evans DG, Pickering LK, Evans DJ Jr, Vollet JJ, Ericsson CD, Ackerman PB, Tjoa WS, 1980. Prevention of traveler’s diarrhea (emporiatric enteritis). Prophylactic administration of subsalicylate bismuth). JAMA 243 : 237–241.
  42. Merson MH, Morris GK, Sack DA, Wells JG, Feeley JC, Sack RB, Creech WB, Kapikian AZ, Gangarosa EJ, 1976. Travelers’ diarrhea in Mexico. A prospective study of physicians and family members attending a congress. N Engl J Med 294 : 1299–1305.
  43. DuPont HL, Ericsson CD, Galindo E, Wood LV, Morgan D, Bitsura JA, Mendiola JG, 1984. Furazolidone versus ampicillin in the treatment of traveler’s diarrhea. Antimicrob Agents Chemother 26 : 160–163.
  44. Ericsson CD, DuPont HL, Sullivan P, Galindo E, Evans DG, Evans DJ Jr, 1983. Bicozamycin, a poorly absorbable antibiotic, effectively treats travelers’ diarrhea. Ann Intern Med 98 : 20–25.
  45. Mathewson JJ, Johnson PC, DuPont HL, 1988. Enteroadherent Escherichia coli as a cause of travelers’ diarrhea. Advances in Research on Cholera and Related Diarrheas. Kuwahara S, Pierce NF, eds. Tokyo: KTK Scientific Publishers, 15–20.
  46. Sack RB, Santosham M, Froehlich JL, Medina C, Orskov F, Orskov I, 1984. Doxycycline prophylaxis of travelers’ diarrhea in Honduras, an area where resistance to doxycycline is common among enterotoxigenic Escherichia coli. Am J Trop Med Hyg 33 : 460–466.
  47. Steffen R, Mathewson JJ, Ericsson CD, DuPont HL, Helminger A, Balm TK, Wolff K, Witassek F, 1988. Travelers’ diarrhea in West Africa and Mexico: fecal transport systems and liquid bismuth subsalicylate for self-therapy. J Infect Dis 157 : 1008–1013.
  48. Bouckenooghe AR, Jiang ZD, De La Cabada FJ, Ericsson CD, DuPont HL, 2002. Enterotoxigenic Escherichia coli as cause of diarrhea among Mexican adults and US travelers in Mexico. J Travel Med 9 : 137–140.
  49. DuPont HL, Ericsson CD, Mathewson JJ, de la Cabada FJ, Conrad DA, 1992. Oral aztreonam, a poorly absorbed yet effective therapy for bacterial diarrhea in US travelers to Mexico. JAMA 267 : 1932–1935.
  50. DuPont HL, Ericsson CD, Mathewson JJ, Marani S, Knellwolf-Cousin AL, Martinez-Sandoval FG, 1993. Zaldaride maleate, an intestinal calmodulin inhibitor, in the therapy of travelers’ diarrhea. Gastroenterology 104 : 709–715.
  51. DuPont HL, Ericsson CD, Mathewson JJ, Palazzini E, DuPont MW, Jiang ZD, Mosavi A, de la Cabada FJ, 1998. Rifaximin: a nonabsorbed antimicrobial in the therapy of travelers’ diarrhea. Digestion 59 : 708–714.
  52. Ericsson CD, DuPont HL, Mathewson JJ, 1997. Single dose ofloxacin plus loperamide compared with single dose or three days of ofloxacin in the treatment of traveler’s diarrhea. J Travel Med 4 : 3–7.
  53. Ericsson CD, DuPont HL, Mathewson JJ, West MS, Johnson PC, Bitsura JA, 1990. Treatment of traveler’s diarrhea with sulfame-thoxazole and trimethoprim and loperamide. JAMA 263 : 257–261.
  54. Gascon J, Vila J, Valls ME, Ruiz L, Vidal J, Corachan M, Prats G, Jimenez de Anta MT, 1993. Etiology of traveller’s diarrhea in Spanish travellers to developing countries. Eur J Epidemiol 9 : 217–223.
  55. Paredes P, Campbell-Forrester S, Mathewson JJ, Ashley D, Thompson S, Steffen R, Jiang ZD, Svennerholm AM, DuPont HL, 2000. Etiology of travelers’ diarrhea on a Caribbean island. J Travel Med 7 : 15–18.
  56. Taylor DN, Bourgeois AL, Ericsson CD, Steffen R, Jiang ZD, Halpern J, Haake R, DuPont HL, 2006. A randomized, double-blind, multicenter study of rifaximin compared with placebo and with ciprofloxacin in the treatment of travelers’ diarrhea. Am J Trop Med Hyg 74 : 1060–1066.
  57. Sack DA, Kaminsky DC, Sack RB, Wamola IA, Orskov F, Orskov I, Slack RC, Arthur RR, Kapikian AZ, 1977. Enterotoxigenic Escherichia coli diarrhea of travelers: a prospective study of American Peace Corps volunteers. Johns Hopkins Med J 141 : 63–70.
  58. Sack RB, Froehlich JL, Zulich AW, Hidi DS, Kapikian AZ, Orskov F, Orskov I, Greenberg HB, 1979. Prophylactic doxycycline for travelers’ diarrhea: results of a prospective double-blind study of Peace Corps volunteers in Morocco. Gastroenterology 76 : 1368–1373.
  59. Bourgeois AL, Gardiner CH, Thornton SA, Batchelor RA, Burr DH, Escamilla J, Echeverria P, Blacklow NR, Herrmann JE, Hyams KC, 1993. Etiology of acute diarrhea among United States military personnel deployed to South America and west Africa. Am J Trop Med Hyg 48 : 243–248.
  60. Haberberger RL, Scott DA, Thornton SA, Hyams KC, 1994. Diarrheal disease aboard a U.S. Navy ship after a brief port visit to a high risk area. Mil Med 159 : 445–448.
  61. Mattila L, Siitonen A, Kyronseppa H, Simula I, Oksanen P, Stenvik M, Salo P, Peltola H, 1992. Seasonal variation in etiology of travelers’ diarrhea. Finnish-Moroccan Study Group. J Infect Dis 165 : 385–388.
  62. Sharp TW, Thornton SA, Wallace MR, Defraites RF, Sanchez JL, Batchelor RA, Rozmajzl PJ, Hanson RK, Echeverria P, Kapikian AZ, et al., 1995. Diarrheal disease among military personnel during Operation Restore Hope, Somalia, 1992–1993. Am J Trop Med Hyg 52 : 188–193.
  63. Echeverria P, Jackson LR, Hoge CW, Arness MK, Dunnavant GR, Larsen RR, 1993. Diarrhea in U.S. troops deployed to Thailand. J Clin Microbiol 31 : 3351–3352.
  64. Murphy GS Jr, Echeverria P, Jackson LR, Arness MK, LeBron C, Pitarangsi C, 1996. Ciprofloxacin- and azithromycin-resistant Campylobacter causing traveler’s diarrhea in U.S. troops deployed to Thailand in 1994. Clin Infect Dis 22 : 868–869.
  65. Petruccelli BP, Murphy GS, Sanchez JL, Walz S, DeFraites R, Gelnett J, Haberberger RL, Echeverria P, Taylor DN, 1992. Treatment of traveler’s diarrhea with ciprofloxacin and loperamide. J Infect Dis 165 : 557–560.
  66. Echeverria P, Ramirez G, Blacklow NR, Ksiazek T, Cukor G, Cross JH, 1979. Travelers’ diarrhea among U.S. Army troops in South Korea. J Infect Dis 139 : 215–219.
  67. Sriratanaban A, Reinprayoon S, 1982. Vibrio parahaemolyticus: a major cause of travelers’ diarrhea in Bangkok. Am J Trop Med Hyg 31 : 128–130.
  68. Echeverria P, Sack RB, Blacklow NR, Bodhidatta P, Rowe B, McFarland A, 1984. Prophylactic doxycycline for travelers’ diarrhea in Thailand. Further supportive evidence of Aeromonas hydrophila as an enteric pathogen. Am J Epidemiol 120 : 912–921.
  69. Guerrant RL, Rouse JD, Hughes JM, Rowe B, 1980. Turista among members of the Yale Glee Club in Latin America. Am J Trop Med Hyg 29 : 895–900.
  70. Shore EG, Dean AG, Holik KJ, Davis BR, 1974. Enterotoxin-producing Escherichia coli and diarrheal disease in adult travelers: a prospective study. J Infect Dis 129 : 577–582.
  71. Black FT, Gaarslev K, Orskov F, Orskov I, Stenderup A, Stenderup J, Christensen O, 1983. Mecillinam, a new prophylactic for travellers’ diarrhoea. A prospective double-blind study in tourists travelling to Egypt and the Far East. Scand J Infect Dis 15 : 189–193.
  72. Jertborn M, Svennerholm AM, Iwarson S, 1988. A prospective study of serum antibody responses to enterotoxinogenic Escherichia coli in Swedish travellers. Scand J Infect Dis 20 : 69–75.
  73. Pitkanen T, 1982. Travellers’ diarrhoea caused by Campylobacter jejuni. Ann Clin Res 14 : 111–113.
  74. DuPont HL, Jiang ZD, Ericsson CD, Adachi JA, Mathewson JJ, DuPont MW, Palazzini E, Riopel LM, Ashley D, Martinez-Sandoval F, 2001. Rifaximin versus ciprofloxacin for the treatment of traveler’s diarrhea: a randomized, double-blind clinical trial. Clin Infect Dis 33 : 1807–1815.
  75. Gallardo F, Gascon J, Ruiz J, Corachan M, Jimenez de Anta M, Vila J, 1998. Campylobacter jejuni as a cause of traveler’s diarrhea: clinical features and antimicrobial susceptibility. J Travel Med 5 : 23–26.
  76. Hyams KC, Bourgeois AL, Merrell BR, Rozmajzl P, Escamilla J, Thornton SA, Wasserman GM, Burke A, Echeverria P, Green KY, et al., 1991. Diarrheal disease during Operation Desert Shield. N Engl J Med 325 : 1423–1428.
  77. Jelinek T, Lotze M, Eichenlaub S, Loscher T, Nothdurft HD, 1997. Prevalence of infection with Cryptosporidium parvum and Cyclospora cayetanensis among international travellers. Gut 41 : 801–804.
  78. Vila J, Ruiz J, Gallardo F, Vargas M, Soler L, Figueras MJ, Gascon J, 2003. Aeromonas spp. and traveler’s diarrhea: clinical features and antimicrobial resistance. Emerg Infect Dis 9 : 552–555.
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  • Received : 03 Oct 2008
  • Accepted : 20 Dec 2008

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