Diarrheal Diseases: New Challenges and Emerging Opportunities

  • Richard L. Guerrant


In keeping with the central theme, “Global Medicine: Current Status and Directions for the Twenty-First Century,” a discussion of diarrheal diseases is particularly relevant, as diarrheal diseases constitute a leading global cause of morbidity and mortality and provide a useful “barometer” of health. Indeed, health is one of the most universal human values, transcending all cultural, political and geographic boundaries; everyone would rather be healthy than sick. In only this century has some measure of health, like education, become an attainable goal for most, with existing societal resources. Despite this potential, growing disparity threatens global health and perhaps civilization itself. Diarrheal diseases provide a useful barometer of health or neglect of a people, as well as a poignant example of the tremendous potential that public health and recent scientific advances have for alleviating human suffering. We must dare to consider the possibility of a world with a certain minimum level of health for all, with food and energy potentially freely available by molecular biologic or other methods, such as engineered E. coli or cyanobacteria to produce carbohydrates for food and hydrocarbons for energy.


Hemolytic Uremic Syndrome Diarrheal Disease Shiga Toxin Enteric Infection Persistent Diarrhea 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Guerrant RL, Hughes JM, Lima NL, Crane JK (1990) Diarrhea in developed and developing countries: Magnitude, special settings, and etiologies. Rev Infect Dis [Suppl 1] 12: 41—S50Google Scholar
  2. 2.
    Schorling JB, Wanke CA, Schorling SK, McAuliffe JF, de Souza MA, Guerrant RL (1990) A prospective study of persistent diarrhea among children in an urban Brazilian slum: Patterns of occurrence and etiologic agents. Am J Epidemiol 132: 144–156PubMedGoogle Scholar
  3. 3.
    Bhatnagar S, Dosajh U (1986) Diarrhoeal disease morbidity in children below 5 years in urban slums of Delhi. Indian J Med Res 84: 53–58PubMedGoogle Scholar
  4. 4.
    Bennett JV, Holmberg SD, Rogers MF, Solomon SL (1987) Infectious and parasitic diseases. Am J Prev Med [Suppl] 3: 102Google Scholar
  5. 5.
    Ho M-S, Glass RI, Pinsky PR, et al (1988) Diarrheal deaths in American children are they preventable? JAMA 260: 3281–3285PubMedGoogle Scholar
  6. 6.
    Guerrant RL, Kirchhoff LV, Shields DS, et al (1983) Prospective study of diarrheal illnesses in northeastern Brazil: Patterns of disease, nutritional impact, etiologies, and risk factors. J Infect Dis 148: 986–997PubMedGoogle Scholar
  7. 7.
    Dingle JH, Badger DG, Jordan SWJr (1964) Illness in the home: A study of 25,000 illnesses in a group of Cleveland families. Cleveland,OH, Case Western Reserve University PressGoogle Scholar
  8. 8.
    Bartlett AV, Moore M, Gary GW, Starko KM, Erben JJ, Meredith BA (1985) Diarrheal illness among infants and toddlers in daycare centers. II Comparison with daycare home and households. J Pediatr 107: 503–509PubMedGoogle Scholar
  9. 9.
    Schorling JB, Guerrant RL (1990) Diarrhea and catch-up growth. Lancet 1335: 599–600Google Scholar
  10. 10.
    Schorling JB, McAuliffe JF, de Souza MA, Guerrant RL (1990) Malnutrition predisposes to greater diarrhea incidence and duration among children in an urban Brazilian slum. Int J Epidemiol 19: 728–735PubMedGoogle Scholar
  11. 11.
    Lima AAM, Fang G, Schorling JB, et al (1992) Persistent diarrhea in Northeast Brazil: Etiologies and interactions with malnutrition. Acta Paediatr Scand (In Press)Google Scholar
  12. 12.
    Bhan MK, Raj P, Levine MM, et al (1989) Enteroaggregative Escherichia coli associated with persistent diarrhea in a cohort of rural children in India. J Infect Dis 159: 1061— 1064PubMedGoogle Scholar
  13. 13.
    Bhan MK, Khoshoo V, Sommerfelt H, Pushker R, Sazawal S, Srivastava R (1989) Enteroaggregative Escherichia coli and Salmonella associated with nondysenteric persistent diarrhea. Pediatr Infect Dis J 8: 499–502PubMedGoogle Scholar
  14. 14.
    Fang GD, Lima AM, Wanke CA, Kaper JB, Levine MM, Guerrant RL (1991) HEp2 celladherent E. coli: Potential causes of persistent diarrhea of multiple genotypes and different adherence phenotypes. Clin Res 39: 223A, 39: 223A,Google Scholar
  15. 15.
    Soave R, Armstrong D (1986) Cryptosporidium and cryptosporidiosis. Rev Infect Dis 8: 1012–1023PubMedGoogle Scholar
  16. 16.
    Fayer R, Ungar BLP (1986) Cryptosporidium spp. and cryptosporidiosis. Microbiol Rev 50: 458–484PubMedGoogle Scholar
  17. 17.
    Janoff EN, Reller LB (1987) Cryptosporidium species, a protean protozoan. J Clin Microbiol; 25: 967–975PubMedGoogle Scholar
  18. 18.
    Guerrant RL, Petri WA, Weikel CS (1990) Parasitic causes of diarrhea. In: Lebenthal E, Duffey M (eds) Pathophysiology of secretory diarrhea. New York, Raven Press, Ltd., 273–280Google Scholar
  19. 19.
    Sallon S, Deckelbaum RJ, Schmid I, Harlap S, Baras M, Spira DT (1988) Cryptosporidium, malnutrition, and chronic diarrhea in children. Am J Dis Child 142: 312–316PubMedGoogle Scholar
  20. 20.
    MacFarlane DE, Horner-Bryce J (1987) Cryptosporidiosis in wellnourished and malnourished children. Acta Paediatr Scand 76: 474–477PubMedGoogle Scholar
  21. 21.
    Sarabia-Arce S, Salazar-Lindo E, Gilman RH, Naranjo J, Miranda E (1990) Case-control study of Cryptosporidium parvum infection in Peruvian children hospitalized for diarrhea: possible association with malnutrition and nosocomial infection. Pediatr Infect Dis J 9: 627–631PubMedGoogle Scholar
  22. 22.
    Pickering LK, Evans DG, DuPont HL, et al (1981) Diarrhea caused by Shigella, rotavirus and Giardia in daycare centers: Prospective study. J Pediatr 99: 51–56PubMedGoogle Scholar
  23. 23.
    Bartlett AV, Moore M, Gary GW, Starko KM, Erben JJ, Meredith BA (1985) Diarrheal illness among infants and toddlers in daycare centers. I. Epidemiology and pathogens. J Pediatr 107: 495–502PubMedGoogle Scholar
  24. 24.
    Lima NL, Guerrant RL, Kaiser DL, Germanson T, Farr BM (1990) A retrospective cohort study of nosocomial diarrhea as a risk factor for nosocomial infection. J Infect Dis 161: 948–952PubMedGoogle Scholar
  25. 25.
    Koch KL, Phillips DJ, Aber RC, Current WL (1985) Cryptosporidiosis in hospital personnel. Ann Intern Med 102: 593–596PubMedGoogle Scholar
  26. 26.
    McFarland LV, Mulligan ME, Kwok RYY, Starnm WE (1989) Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 320: 204–210PubMedGoogle Scholar
  27. 27.
    Soave R, Johnson WD Jr (1988) Animal reservoirs of Cryptosporidium spp and Isospora belli. J Infect Dis 158: 910Google Scholar
  28. 28.
    Colebunders R, Francis H, Mann JM, et al (1987) Persistent diarrhea, strongly associated with HIV infeciton in Kinshasa, Zaire. Am J Gastroenterol 82: 859–864PubMedGoogle Scholar
  29. 29.
    Antony MA, Brandt LJ, Klein RS, Bernstein LH (1988) Infectious diarrhea in patients with AIDS. Dig Dis Sci 33: 1141–1146PubMedGoogle Scholar
  30. 30.
    Guerrant RL, Bobak DL (1991) Bacterial and protozoal gastroenteritis. N Engl J Med 325: 327–340PubMedGoogle Scholar
  31. 31.
    Brandtzaeg P, Halstensen TS, Kett K, et al (1989) Immunobiology and immunopathology of human gut mucosa: humoral immunity and intraepithelial lymphocytes. Gastroenterol 97: 1562–1584Google Scholar
  32. 32.
    Musch MW, Miller RJ, Field M (1982) Stimulation of colonic secretion by lipoxygenase metabolites of arachidonic acid. Science 217: 1255–1256PubMedGoogle Scholar
  33. 33.
    Kimberg DV, Field M, Johnson J, Henderson A, Gershon E (1971) Stimnulation of intestinal mucosal adenyl cyclase by cholera enterotoxin and prostaglandins. J Clin Invest 50: 1218–1230PubMedGoogle Scholar
  34. 34.
    Chen LC, Rohde JE, Sharp GWG (1971) Intestinal adenyl-cyclase activity in human cholera. Lancet 1: 939–941PubMedGoogle Scholar
  35. 35.
    Guerrant RL, Chen LC, Sharp GWG (1975) Intestinal adenyl-cyclase activity in canine cholera: Correlation with fluid accumulation. J Infect Dis 125: 377–381Google Scholar
  36. 36.
    Guth BEC, Pickett CL, Twiddy EM, et al (1986) Production of Type II heat-labile enterotoxin (LT-II) by Escherichia coli isolated from food and human feces. Infect Immun 54: 587–589PubMedGoogle Scholar
  37. 37.
    Hughes JM, Murad F, Chang B, Guerrant RL (1978) Role of cyclic GMP in the action of heat-stable enterotoxins of Escherichia coli. Nature 271: 755–756PubMedGoogle Scholar
  38. 38.
    Field M, Graf Jr LH, Mata LJ (1978) Heat stable enterotoxin of E. coli. In vitro effects on guanylate cyclase activity, cyclic GMP concentration, and ion transport in small intestine. Proc Natl Acad Sci USA 75: 2800PubMedGoogle Scholar
  39. 39.
    Guerrant RL, Hughes JM, Chang B, Robertson DC, Murad F (1980)Activation of intestinal guanylate cyclase by heat-stable enterotoxin of E. coli: Studies of tissue specificity, potential receptors and intermediates. J Infect Dis 142: 220–228PubMedGoogle Scholar
  40. 40.
    Kennedy DJ, Greenberg RN, Dunn JA, Abernathy R, Ryerse JS, Guerrant RL (1984) Effects of Escherichia coli heat-stable enterotoxin STb on intestines of mice, rats, rabbits, and piglets. Infect Immun 46: 639–643PubMedGoogle Scholar
  41. 41.
    Weikel CS, Nellans HN, Guerrant RL (1986) The in vivo and in vitro effects of a novel enterotoxin, STb, produced by Escherichia coli. J Infect Dis 153: 893–901PubMedGoogle Scholar
  42. 42.
    Guerrant RL, Dickens MD, Wenzel RP, Kapikian AZ (1976) Toxigenic bacterial diarrhea: Nursery outbreak involving multiple bacterial strains. J Pediatr 89: 885–891PubMedGoogle Scholar
  43. 43.
    Wachsmuth K, Wells J, Shipley P (1979) Heat-labile enterotoxin production in isolates from a shipboard outbreak of human diarrheal illness. Infect Immun 24: 793— 797PubMedGoogle Scholar
  44. 44.
    Honda T, Shimizu M, Takeda Y (1976) Isolation of a factor causing morphological changes of Chinese hamster ovary cells from the culture filtrates of Vibrio parahemolyticus. Infect Immun 14: 1028–1033PubMedGoogle Scholar
  45. 45.
    Sandefur PD, Peterson JW (1977) Neutralization of Salmonella toxin-induced elongation of Chinese hamster ovary cells by cholera antitoxin. Infect Immun 15: 988–992PubMedGoogle Scholar
  46. 46.
    Ruiz-Palacios GM, Torres J, Torres NI (1983) Cholera-like enterotoxin produced by Campylobacter jejuni. Characterization and clinical significance. Lancet 2: 250–252PubMedGoogle Scholar
  47. 47.
    Ruiz-Palacios GM, Lopez-Vidal Y, Torres J, Torres N (1985) Serum antibodies to heatlabile enterotoxin of Campylobacter jejuni. J Infect Dis 152: 413–416Google Scholar
  48. 48.
    Daikoku T, Kawagughi M, Takama K, Suzuki S (1990) Partial purification and characterization of the enterotoxin produced by Campylobacter jejuni. Infect Immun 58: 2414— 2419PubMedGoogle Scholar
  49. 49.
    Aimoto S, Takao T, Shimonishi Y, et al (1982) Amino-acid sequence of a heat stable enterotoxin produced by human enterotoxigenic Escherichia coli. Eur J Biochem 129: 257–263PubMedGoogle Scholar
  50. 50.
    Takao T, Hitouji T, Aimoto S, et al (1983) Amino-acid sequence of a heat-stable enterotoxin isolated from enterotoxigenic Escherichia coli strain 18D. FEBS 152: 1–5Google Scholar
  51. 51.
    Guarino A, Giannella R, Thompson MR (1989) Citrobacter freundii produces an 18-amino-acid heat-stable enterotoxin identical to the 18-amino-acid Escherichia coli heatstable enterotoxin (ST Ia) . Infect Immun 57: 649–652PubMedGoogle Scholar
  52. 52.
    Takeda T, Balakrish Nair G, Suzuki K, Shimonishi Y (1990) Production of a monoclonal antibody to Vibrio cholerae Non-O1 heat-stable enterotoxin (ST) which is cross-reactive with Yersinia enterocolitica ST. Infect Immun 58: 2755–2759PubMedGoogle Scholar
  53. 53.
    Lyerly DM, Krivan HC, Wilkins TD (1988) Clostridium difficile: Its disease and toxins. J Clin Microbiol 1: 1–18Google Scholar
  54. 54.
    Kapral FA (1985) Staphylococcus aureus delta toxin as an enterotoxin. Ciba Found Symp 112: 215–229PubMedGoogle Scholar
  55. 55.
    Scheifele DW (1990) Role of bacterial toxins in neonatal necrotizing enterocolitis. J Pediatr 117 (No 1, Part 2) : 45–S46Google Scholar
  56. 56.
    Fasano A, Kay BA, Russell RG, Maneval Jr DR, Levine MM (1990) Enterotoxin and cytotoxin production by enteroinvasive Escherichia coli. Infect Immun 58: 3717–3723PubMedGoogle Scholar
  57. 57.
    Savarino SJ, Fasano A, Robertson DC, Levine MM (1991) Enteroaggregative Escherichia coli elaborate a heat-stable enterotoxin demonstrable in an in vitro rabbit intestinal model. J Clin Invest 87: 1450–1455PubMedGoogle Scholar
  58. 58.
    Lima AAM, Lyerly DM, Wilkins TD, Innes DJ, Guerrant RL (1988) Effects of Clostridium difficile toxins A and B in rabbit small and large intestine in vivo and on cultured cells in vitro. Infect Immun 56: 582–588PubMedGoogle Scholar
  59. 59.
    Lima AAM, Innes DJ, Chadee K, Lyerly DM, Wilkins TD, Guerrant RL (1989) Clostridium difficile toxin A: Early sequential histopathologic effectts in rabbit small intestine. Lab invest 61: 419–425PubMedGoogle Scholar
  60. 60.
    Field M, Rao MC, Chang EB (1989) Intestinal electrolyte transport and diarrheal disease (Parts 1 & 2) . N Engl J Med 32: 800–806 and 879–883Google Scholar
  61. 61.
    Moore R, Pothoulakis C, LaMont JT, Carlson S, Madara JL (1990) C. difficile toxin A increases intestinal permeability and induces Cl-secretion. Am Physiol Soc Gl 65—Gl 72Google Scholar
  62. 62.
    Myers LL, Shoop DS, Stackhouse LL, et al (1987) Isolation of enterotoxigenic Bacteroides fragilis from humans with diarrhea. J Clin Microbiol 25: 2330–2333PubMedGoogle Scholar
  63. 63.
    Myers LL, Shoop DS, Collins JE (1990) Rabbit model to evaluate enterovirulence of Bacteroides fragilis. J Clin Microbiol 28: 1658–1660PubMedGoogle Scholar
  64. 64.
    Weikel CS, Grieco FD, Reuben J, Myers LL, Sack RB (1990) HT29/C1 cells treated with crude Bacteroides fragilis enterotoxin dramatically alter their morphology. Presented US Japan Cholera Conference, Kyoto (in press)Google Scholar
  65. 65.
    Keusch GT, Grady GF, Mata LJ (1972) The pathogenesis of Shigella diarrhea I. Enterotoxin production by Shigella dysenteriae 1. J Clin Invest 51: 1212–1218PubMedGoogle Scholar
  66. 66.
    O’Brien AD, Holmes RK (1987) Shiga and shiga-like toxins. Microbiol Rev 51 : 206–220PubMedGoogle Scholar
  67. 67.
    Karmali MA, Petric M, Lim C, Fleming PC, Arbus GS, Lior H (1985) The association between ideopathic hemolytic uremic syndrome and infection by verotoxin producing E. coli.J Infect Dis 151: 775–782PubMedGoogle Scholar
  68. 68.
    Obrig TG, Moran RP, Colinas RJ (1985) Ribonuclease activity associated with the 60-S ribosome inactivating proteins Ricin A, phytolaccin and shiga toxin. Biochem Biophys Res Commun 1300: 8790–8840Google Scholar
  69. 69.
    Reisbig R, Olsnes S, Eiklid K (1981) The cytotoxic activity of Shigella toxin: Evidence for catalytic inactivation of the 60-S ribosomal subunit. J Biol Chem 2560: 8739–8744Google Scholar
  70. 70.
    Jackson MP (1990) Structure-function analysis of Shiga toxin and the Shiga-like toxins. Microbial Pathogenesis 8: 235–242PubMedGoogle Scholar
  71. 71.
    Samuel JE, Perera LP, Ward S, O’Brien AD, Ginsburg V, Krivan HC (1990) Comparison of the glycolipid receptor specificities of Shiga-like toxin type II and Shiga-like toxin type II variants. Infect Immun 58: 611–618PubMedGoogle Scholar
  72. 72.
    Karmali MA(1989) Infection by verocytotoxin-producing Escherichia coli. Clin Microbiol Rev 2: 15–38PubMedGoogle Scholar
  73. 73.
    Riley LW, Remis RS, Helgerson SD, et al (1983) Outbreak of hemorrhagic colitis associated with a rare E. coli serotype. N Engl J Med 308: 681–685PubMedGoogle Scholar
  74. 74.
    Bridgewater FAJ, Morgan RS, Rowson KEK, Wright GP (1955) The neurotoxin of Shigella shigae. Morphological and functional lesions produced in the central nervous system of rabbits. Br J Exp Pathol 36: 447–453Google Scholar
  75. 75.
    Cavanagh JB, Howard JG, Whitby JL (1956) The neurotoxin of Shigella shigae: A comparative stududy of the effects produced in various laboratory animals. Br J Exp Med 370: 272–278Google Scholar
  76. 76.
    Howard JG (1955) Observations on the intoxication produced in micece and rabbits by the neurotoxin of Shigella shigae. Br J Exp Pathol 36: 439–446PubMedGoogle Scholar
  77. 77.
    Wiley RG, Donohue-Rolfe A, Keusch GT (1985) Axonally transported Shigella cytotoxin is neurotoxic? J Neuropathol Exp Neurol 440: 496–506Google Scholar
  78. 78.
    Ashkenazi A, Cleary KR, Pickering LK, Murray BE, Cleary TG (1990) The association of Shiga toxin and other cytotoxins with the neurologic manifestations of shigellosis. J Infect Dis 161: 961–965PubMedGoogle Scholar
  79. 79.
    Kasimir S, Schonfeld W, Alouf JE, Konig W (1990) Effect of Staphylococcus aureus deltatoxin on human granulocyte functions and platelet-activating-factor metabolism. Infect Immun 58: 1653–1659PubMedGoogle Scholar
  80. 80.
    Lawrence GW, Lehmann D, Anian G, et al (1990) Impact of active immunization against enteritis necroticans in Papua New Guinea. Lancet 336: 1165–1167PubMedGoogle Scholar
  81. 81.
    Johnson WM, Lior H (1984) Toxins produced by Campylobacter jejuni and Campylobacter coli. Lancet 1: 229–230PubMedGoogle Scholar
  82. 82.
    Yeen WP, Pothocheary SD, Pang T (1983) Demonstration of a cytotoxin from Campylobacter jejuni. J Clin Pathol 36: 1237–1240PubMedGoogle Scholar
  83. 83.
    Guerrant RL, Wanke CA, Pennie RA, Barrett LJ, Lima AAM, O’Brien AD (1987) Production of a unique cytotoxin by Campylobacter jejuni. Infect Immun 55: 2526–2530PubMedGoogle Scholar
  84. 84.
    Perez-Perez GL, Cohn DL, Guerrant RL, Patton CM, Reller LB, Blaser MJ (1989) Clinical and immunologic significance of cholera-like toxin and cytotoxin production by Campylobacter species in patients with acute inflammatory diarrhea in the USA. J Infect Dis 160: 460–467PubMedGoogle Scholar
  85. 85.
    Leunk RD, Johnson PT, David BC, Kraft WG, Morgan DR (1988) Cytotoxic activity in broth-culture filtrates of Campylobacter J Med Microbiol 26: 93–99PubMedGoogle Scholar
  86. 86.
    Leunk RD, Ferguson MA, Morgan DR, Low DE, Simor AE (1990) Antibody to cytotoxin in infection by Helicobacter J Clin Microbiol 28: 1181–1184PubMedGoogle Scholar
  87. 87.
    Guerrant RL, Lingwood CA (1991) Glycoconjugate receptors for adhesins and toxins. In: Marshall, McCallum and Guerrant (eds) Gastroduodenal Disease and Helicobacter pylori (in press)Google Scholar
  88. 88.
    Smoot DT, Mobley HLT, Chippendale GR, Lewison JF, Resau JH (1990) Helicobacter pylori urease activity is toxic to human gastric epithelial cells. Infect Inmnun 58: 1992—1994Google Scholar
  89. 89.
    Fasano A, Baudry B, Pumplin DW, et al (1991) Vibrio cholerae produces a second enterotoxin which affects intestinal tight junctions. PNAS (in press)Google Scholar
  90. 90.
    Evans DG, Silver RP, Evans DJ, Chase DG, Gorbach SL (1975) Plasmid-controlled colonization factor associated with virulence in Escherichia coli enterotoxigenic for humans. Infect Immun 12: 656–667PubMedGoogle Scholar
  91. 91.
    Satterwhite TK, Evans DG, DuPont HL, Evans DJ (1978) Role of Escherichia coli colonization factor antigen in acute diarrhea. Lancet 2: 181–183PubMedGoogle Scholar
  92. 92.
    Levine MM, Kaper JB, Black RE, Clements ML (1983) New knowledge on pathogenesis of bacterial enteric infections as applied to vaccine development. Microbiol Rev 47: 510–550PubMedGoogle Scholar
  93. 93.
    Karch H, Heesemann J, Laufs R, et al (1987) A plasmid of enterohemorrhagic Escherichia coli 0157:H7 is required for expression of a new fimbrial antigen and for adhesion to epithelial cells. Infect Immun 55: 455–461PubMedGoogle Scholar
  94. 94.
    Toth I, Cohen ML, Rumschlag HS, et al (1990) Influence of the 60-Megadalton plasmid on adherence of Escherichia coli 0157:H7 and genetic derivatives. Infect Immun 58: 1223–1231PubMedGoogle Scholar
  95. 95.
    Baldini MA, Kaper JB, Levine MM, Candy DCA, Moon HW (1983) Plasmnid-mediated adhesin in enteropathogenic Escherichia coli. J Pediatr Gastroenterol Nutr 2: 534–538PubMedGoogle Scholar
  96. 96.
    Ulshen MH, Rollo JL (1980) Pathogenesis of Escherichia coli gastroenteritis in man, another mechanism. N Engl J Med 302: 99–101PubMedGoogle Scholar
  97. 97.
    Polotsky YE, Dragunskaya EM, Seliverstova GV, et al (1977) Pathogenic effect of enterotoxigenic Escherichia coli and Escherichia coli causing infantile diarrhoea. Acta Microbiol Acad Sci Hung 4: 221Google Scholar
  98. 98.
    Rothbaum R, McAdams AJ, Giannella R, Partin JC (1982) A clinicopathologic study of enterocyte-adherent Escherichia coli: A cause of protracted diarrhea in children. Gastroenterol 83: 441–454Google Scholar
  99. 99.
    Levine MM, Nalin DR, Hornick RB, et al (1978) Escherichia roli strains that cause diarrhea but do not produce heat-labile or heat-stable enterotoxins and are noninvasive. Lancet 1: 1119–1122PubMedGoogle Scholar
  100. 100.
    Guerrant RL (1980) Yet another pathogenic mechanism for Escherichia coli diarrhea. N Engl J Med 302: 113–114PubMedGoogle Scholar
  101. 101.
    Cravioto A, Gross RJ, Scotland S, et al (1979) An adhesive factor found in strains of Escherichia coli belonging to the traditional infantile enteropathogenic serotypes. Curr Microbiol 3: 95–99Google Scholar
  102. 102.
    Nataro JP, Kaper JB, Robins-Browne R, et al (1987) Patterns of adherence of diarrheagenic Escherichia coli to HEP-2 cells. Pediatr Infect Dis J 6: 829–831PubMedGoogle Scholar
  103. 103.
    Knutton S, Baldwin T, Williams PH, McNeish AS (1989) Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun 57: 1290–1298PubMedGoogle Scholar
  104. 104.
    Jerse AE, Martin WC, Galen JE, Kaper JB (1990) Oligonucleotide probe for detection of the enteropathogenic Escherichia coli (EPEC) adherence factor of localized adherent EPEC. J Clin Microbiol 28: 2842–2844PubMedGoogle Scholar
  105. 105.
    Mathewson JJ, Cravioto A (1989) HEp-2 cell adherence as an assay for virulence among diarrheagenic Esch eri chi a coli. J Infect Dis 159: 1057—1060PubMedGoogle Scholar
  106. 106.
    Vial P, Robins-Browne R, Lior H, et al (1988) Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrhcal disease. J Infect Dis 158: 70–79PubMedGoogle Scholar
  107. 107.
    Bilge SS, Clausen CR, Lau W, Moseley SL (1989) Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. J Bacteriol 171: 4281–4289PubMedGoogle Scholar
  108. 108.
    Giron JA, Fry J, Frankel G, et al (1991) Diffuse-adhering Escherichia coli (DAEC) as a putative cause of diarrhea in Mayan children in Mexico. J Infect Dis 163: 507–513PubMedGoogle Scholar
  109. 109.
    Sansonetti PJ, Hale TL, Oakes EV (1985) Genetics of virulence in enteroinvasive Eschericia coli. Microbiol 1: 74–77Google Scholar
  110. 110.
    Maurelli AT, Sansonetti P (1988) Identification of a chromosomal gene controlling temperature-regulated expression of Shigella virulence. Proc Natl Acad Sci USA 85: 2820–2824PubMedGoogle Scholar
  111. 111.
    Isberg RL, Voorhis DL, Falkow S (1987) Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell 50: 769–778PubMedGoogle Scholar
  112. 112.
    Finlay BB, Heffron F, Falkow S (1989) Epithelial cell surfaces induce Salmonella proteins required for bacterial adherence and invasion. Science 243: 940–943PubMedGoogle Scholar
  113. 113.
    Ravdin JI, Guerrant RL (1981) Role of adherence in cytopathogenic mechanisms of Entamoeba histolytica. J Clin Invest 68: 1305–1313PubMedGoogle Scholar
  114. 114.
    Guerrant RL, Brush JE, Ravdin JI, et al (1981) Interaction between Entamoeba histolytica and human polymorphonuclear leukocytes. J Infect Dis 143: 83–93PubMedGoogle Scholar
  115. 115.
    Petri WA Jr, Chapman MD, Snodgrass T, Mann BJ, Broman J, Ravdin JI (1989) Subunit structure of the galactose and N-acetyl-D-galactosamine-inhibitable adherence lectin of Entamoeba histolytica. J Biol Chem 264: 3007–3012PubMedGoogle Scholar
  116. 116.
    Isberg R (1991) Discrimination between intracellular uptake and surface adhesion of bacterial pathogens. Science 252: 934–938PubMedGoogle Scholar
  117. 117.
    Guerrant RL (1988) Vaccines against enteric infections. Current Opinion in Infectious Diseases 1: 868–876Google Scholar
  118. 118.
    Clemens D, Sack DA, Harris JR, et al (1988) Impact of B subunit killed whole-cell and killed whole-cell-only oral vaccines against cholera upon treated diarrhoeal illness and mortality in an area endemic for cholera. Lancet 1: 1375–1378PubMedGoogle Scholar
  119. 119.
    Clemens JD, Sack DA, Harris JR, Van Loon F, Chakraborty J, Ahmen F (1990) Field trial of oral cholera vaccines in Bangladesh: results from three-year follow-up. Lancet 335 (1684) : 270–273PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1992

Authors and Affiliations

  • Richard L. Guerrant
    • 1
  1. 1.Division of Geographic MedicineUniversity of Virginia School of MedicineCharlottesvilleUSA

Personalised recommendations