Chapter 7 : Distinguishing Pathovars from Nonpathovars:

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Distinguishing Pathovars from Nonpathovars: , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817688/9781555812683_Chap07-1.gif /docserver/preview/fulltext/10.1128/9781555817688/9781555812683_Chap07-2.gif


Most of the infectious disease organisms are classified as pathogens because they are unequivocally associated with human disease and do not occur as part of the commensal flora of the human host. Molecular biology methods play an important role in the classification of such organisms and the characterization of the epidemiology of these types of infections. This chapter focuses on , with an emphasis on the methodology and significance of differentiating pathovars from nonpathogenic strains in this species. While most of the techniques described in this chapter focus on differentiating pathovars from nonpathovars, which may be referred to as pathotype identification or “pathotyping,” the importance of molecular strain-typing systems to the epidemiologic characterization of a variety of diseases caused by is also discussed.

Citation: Riley L. 2004. Distinguishing Pathovars from Nonpathovars: , p 175-208. In Molecular Epidemiology of Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817688.ch7
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 7.1
Figure 7.1

HeLa cell association of different groups of associated with diarrhea. (A) EPEC strains attach to the surface of HeLa cells in discrete clusters called LA. (B) DAEC strains attach in a diffuse pattern on the surface of HeLa cells, but not on the glass surface. (C) A laboratory strain of (K-12) attaches in a diffuse pattern to the cells and the glass surface. (D) EAEC strains attach in a characteristic “stacked brick” pattern to the cells and the glass surface. With typical EPEC, the characteristic LA pattern of attachment led to the discovery of a specific set of genes necessary for this pattern and thus led to specific molecular virulence strain-typing methods to differentiate EPEC from other groups of .

Citation: Riley L. 2004. Distinguishing Pathovars from Nonpathovars: , p 175-208. In Molecular Epidemiology of Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817688.ch7
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Abe, A.,, H. Obata,, S. Matsushita,, S. Yamada,, Y. Kudoh,, A. Bangtrakulnonth,, O. A. Ratchtrachenchat,, and H. Danbara. 1992. A sensitive method for the detection of enterotoxigenic Escherichia coli by the polymerase chain reaction using multiple primer pairs. Int. J. Med. Microbiol. Virol. Parasitol. Infect. Dis. 277: 170 178.
2. Adachi, J. A.,, Z. D. Jiang,, J. J. Mathewson,, M. P. Verenkar,, S. Thompson,, F. Martinez-Sandoval,, R. Steffen,, C. D. Ericsson,, and H. L. DuPont. 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.
3. Barnett, B. J.,, and D. S. Stephens. 1997. Urinary tract infection: an overview. Am. J. Med. Sci. 314: 245 249.
4. Baudry, B.,, S. J. Savarino,, P. Vial,, J. B. Kaper,, and M. M. Levine. 1990. A sensitive and specific DNA probe to identify enteroaggregative Escherichia coli, recently discovered diarrheal pathogen. J. Infect. Dis. 161: 1249 1251.
5. Bettelheim, K. A., 1997. Escherichia coli in the normal flora of humans and animals, p. 85 109. In M. Sussman (ed.), Escherichia coli: Mechanisms of Virulence. Cambridge University Press, Cambridge, England.
6. Bhan, M. K.,, V. Khoshoo,, H. Sommerfelt,, P. Raj,, S. Sazawal,, and R. Srivastava. 1989. Enteroaggregative Escherichia coli and Salmonella associated with nondysenteric persistent diarrhea. Pediatr. Infect. Dis. J. 8: 499 502.
7. Bhatnagar, S.,, M. K. Bhan,, H. Sommerfelt,, S. Szawal,, R. Kumar,, and S. Saini. 1993. Enteroaggregative Escherichia coli may be a new pathogen causing acute and persistent diarrhea. Scand. J. Infect. Dis. 25: 579 583.
8. Blattner, F. R.,, G. Plunkett III,, C. A. Bloch,, N. T. Perna,, V. Burland,, M. Riley,, J. Collado-Vides,, J. D. Glasner,, C. K. Rode,, G. F. Mayhew,, J. Gregor,, N. W. Davis,, H. A. Kirkpatrick,, M. A. Goeden,, D. J. Rose,, B. Mau,, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K12. Science 277: 1453 1462.
9. Boileau, C. R.,, H. M. D’Hauteville,, and P. J. Sansonetti. 1984. DNA hybridization technique to detect Shigella species and enteroinvasive Escherichia coli. J. Clin. Microbiol. 20: 959 961.
10. Booy, R.,, and S. Kroll. 1994. Bacterial meningitis in children. Curr. Opin. Pediatr. 6: 29 35.
11. Bopp, C. A.,, F. W. Brenner,, P. I. Fields,, J. G. Wells,, and N. A. Strockbine,. 2003. Escherichia, Shigella, and Salmonella, p. 654 671. In P. R. Murray,, E. J. Baron,, J. H. Jorgensen,, M. A. Pfaller,, and R. H. Yolken (ed.), Manual of Clinical Microbiology, 8th ed. ASM Press, Washington, D.C.
12. Boquet, P. 2001. The cytotoxic necrotizing factor 1 (CNF1) from Escherichia coli. Toxicon 39: 1673 1680.
13. Boyd, E. F.,, and D. L. Hartl. 1998. Chromosomal regions specific to pathogenic isolates of Escherichia coli have a phylogenetically clustered distribution. J. Bacteriol. 180: 1159 1165.
14. Bray, J. 1945. Isolation of antigenically homogenous strains of Bact. Coli neapolitanum from summer diarrhoea of infants. J. Pathol. Bacteriol. 57: 239 247.
15. Calderwood, S. B.,, D. W. K. Acheson,, G. T. Keusch,, T. J. Barrett,, P. M. Griffin,, N. A. Strockbine,, B. Swaminathan,, J. B. Kaper,, M. M. Levine,, B. S. Kaplan,, H. Karch,, A. D. O’Brien,, T. G. Obrig,, Y. Takeda,, P. I. Tarr,, and I. K. Wachsmuth. 1996. Proposed new nomenclature for SLT (VT) family. ASM News 62: 118 119.
16. Candrian, U.,, B. Furrer,, C. Hofelein,, R. Meyer,, M. Jermini,, and J. Luthy. 1991. Detection of Escherichia coli and identification of enterotoxigenic strains by primer-directed enzyme amplification or specific DNA sequences. Int. J. Food Microbiol. 12: 339 351.
17. Caprioli, A.,, V. Falbo,, L. G. Roda,, F. M. Ruggeri,, and C. Zona. 1983. Partial purification and characterization of an Escherichia coli toxic factor that induces morphologic cell alterations. Infect. Immun. 39: 1300 1306.
18. Centers for DiseaseControl and Prevention. 1995. Outbreak of acute gastroenteritis attributable to Escherichia coli serotype O104:H21—Helena, Montana, 1994. Morb. Mortal. Wkly. Rep. 44: 501503.
19. Cobeljic, M.,, B. Miljkovic-Selimovic,, D. Paunovic-Todosijevic,, Z. Velickovic,, Z. Lepsanovic,, D. Savic,, R. Ilic,, S. Konstantinovic,, B. Jovanovic,, and V. Kostic. 1996. Enteroaggregative Escherichia coli associated with an outbreak of diarrhoea in a neonatal nursery ward. Epidemiol. Infect. 117: 11 16.
20. Council of State and Territorial Epidemiologists. 1993. CSTE Position Statement 4. National Surveillance of Escherichia coli O157:H7. Council of State and Territorial Epidemiologists, Atlanta, Ga.
21. Cravioto, A.,, A. Tello,, A. Vavarro,, J. Ruiz,, H. Villafan,, F. Uribe,, and C. Eslava. 1991. Association of Escherichia coli Hep-2 adherence patterns with type and duration of diarrhoea. Lancet 337: 262 264.
22. Cravioto, A.,, R. J. Gross,, S. M. Scotland,, and B. Rowe. 1979. An adhesive factor found in strains of Escherichia coli belonging to the traditional infantile enteropathogenic serotypes. Curr. Microbiol. 3: 95 99.
23. Dalmau, D.,, F. Navarro,, B. Mirelis,, J. Blanco,, J. Garau,, and G. Prats. 1996. Escherichia coli bacteraemia: serotype O15:K52:H1 as a urinary pathogen. J. Hosp. Infect. 34: 233 234.
24. Day, N. P.,, S. M. Scotland,, and B. Rowe. 1981. Comparison of an Hep-2 tissue culture test with the Serény test for detection of enteroinvasiveness in Shigella spp. and Escherichia coli. J. Clin. Microbiol. 13: 596 597.
25. De, S. N. 1959. Enterotoxicity of bacteria-free culture filtrates of Vibrio cholerae. Nature 183: 1533 1534.
26. De, S. N.,, K. Bhattacharya,, and J. K. Sarkar. 1956. A study of the pathogenicity of strains of Bacterium coli from acute and chronic enteritis. J. Pathol. Bacteriol. 76: 155 158.
27. Deng, M. Y.,, D. O. Cliver,, S. P. Day,, and P. M. Fratamico. 1966. Enterotoxigenic Escherichia coli detected in foods by PCR and an enzyme-linked oligonucleotide probe. Int. J. Food Microbiol. 30: 217 229.
28. Donnenberg, M. S.,, and R. A. Welch,. 1996. Virulence determinants of uropathogenic Escherichia coli, p. 135 174. In H. L. T. Mobley, and J. W. Warren (ed.), Urinary Tract Infections: Molecular Pathogenesis and Clinical Management. American Society for Microbiology, Washington, D.C.
29. Donnenberg, M. S.,, and J. P. Nataro. 1995. Methods for studying adhesion of diarrheagenic Escherichia coli. Methods Enzymol. 253: 324 336.
30. Donnenberg, M. S.,, J. B. Kaper,, and B. B. Finlay. 1997. Interactions between enteropathogenic Escherichia coli and host epithelial cells. Trends Microbiol. 5: 109 114.
31. Donnenberg, M. S.,, and T. S. Whittam. 2001. Pathogenesis and evolution of virulence in enteropathogenic and enterohemorrhagic Escherichia coli. J. Clin. Investig. 107: 539 548.
32. Donta, S. T.,, H. W. Moon,, and S. C. Whipp. 1974. Detection of heat-labile Escherichia coli enterotoxin with the use of adrenal cells in tissue culture. Science 183: 334 336.
33. Dutta, N. K.,, M. V. Panse,, and D. R. Kulkarni. 1959. Role of cholera toxin in experimental cholera. J. Bacteriol. 78: 594 595.
34. Edwards, P. R.,, and W. H. Ewing. 1972. Identification of Enterobacteriaceae, 3rd ed. Burgess Publishing Co., Minneapolis, Minn.
35. Eisenstein, B. I. 1990. New molecular techniques for microbial epidemiology and the diagnosis of infectious diseases. J. Infect. Dis. 161: 595 602.
36. Evans, D. G.,, D. J. Evans,, and N. F. Pierce. 1973. Differences in the response of rabbit small intestine to heat-labile and heat-stable enterotoxins of Escherichia coli. Infect. Immun. 7: 873 880.
37. Fang, G. D.,, A. A. M. Lima,, C. V. Martins,, J. P. Nataro,, and R. L. Guerrant. 1995. Etiology and epidemiology of persistent diarrhea in northeastern Brazil: a hospital-based, prospective, case-control study. J. Pediatr. Gastroenterol. Nutr. 21: 137 144.
38. Farmer, J. J., III,. 1999. Enterobacteriaceae: introduction and identification, p. 442 458. In P. R. Murray,, E. J. Baron,, M. A. Pfaller,, F. C. Tenover,, and R. H. Yolken (ed.), Manual of Clinical Microbiology, 7th ed. ASM Press, Washington, D.C.
39. Feng, P.,, K. A. Lampel,, H. Karch,, and T. S. Whittam. 1998. Genotypic and phenotypic changes in the emergence of Escherichia coli O157:H7. J. Infect. Dis. 177: 1750 1753.
40. Ferguson, W. W.,, and R. C. June. 1952. Experiments on feeding adult volunteers with Escherichia coli 111.B4, an organism associated with infantile diarrhea. Am. J. Hyg. 55: 155 169.
41. Formal, S. B.,, T. L. Hale,, and P. J. Sansonetti. 1983. Invasive enteric pathogens. Rev. Infect. Dis. 5( Suppl. 4): S702 S707.
42. Franke, J.,, S. Franke,, H. Schmidt,, A. Schwarzkopf,, L. H. Wieler,, G. Baljer,, L. Beutin,, and H. Karch. 1994. Nucleotide sequence analysis of enteropathogenic Escherichia coli (EPEC) adherence factor probe and development of PCR for rapid detection of EPEC harboring virulence plasmids. J. Clin. Microbiol. 32: 2460 2463.
43. Frankel, G.,, J. A. Giron,, J. Valmassoi,, and G. K. Schoolnik. 1989. Multi-gene amplification: simultaneous detection of three virulence genes in diarrhoeal stool. Mol. Microbiol. 3: 1729 1734.
44. Frankel, G.,, L. Riley,, J. A. Giron,, J. Valmasooi,, A. Friedmann,, N. Strockbine,, S. Falkow,, and G. K. Schoolnik. 1990. Detection of Shigella in feces using DNA amplification. J. Infect. Dis. 161: 1252 1256.
45. Fratamico, P. M.,, S. K. Sackitey,, M. Wiedmann,, and M. Y. Deng. 1995. Detection of Escherichia coli O157:H7 by multiplex PCR. J. Clin. Microbiol. 33: 2188 2191.
46. Friedrich, A. W.,, M. Bielaszewska,, W. L. Zhang,, M. Pulz,, T. Kuczius,, A. Ammon,, and H. Karch. 2002. Escherichia coli harboring Shiga toxin 2 gene variants: frequency and association with clinical symptoms. J. Infect. Dis. 185: 74 84.
47. Gannon, V. P. J.,, S. D’Souza,, T. Graham,, R. K. King,, K. Rahn,, and S. Read. 1997. Use of the flagellar H7 gene as a target in multiple PCR assays and improved specificity in identification of enterohemorrhagic Escherichia coli strains. J. Clin. Microbiol. 35: 656 662.
48. Ghosh, S. N.,, and S. Mukerjee. 1959. Studies on the nature of ultrasonic extract of cholera vibrio. Part 1. Studies on toxicity and pathogenicity. Ann. Biochem. Exp. Med. 19: 173 180.
49. Gianella, R. A. 1976. Suckling mouse model for detection of Escherichia coli enterotoxin: characteristics of the model. Infect. Immun. 14: 95 99.
50. Girón, J. A.,, A. S. Y. Ho,, and G. K. Schoolnik. 1991. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254: 710 713.
51. Girón, J. A.,, M. S. Donnenberg,, W. C. Martin,, K. G. Jarvis,, and J. B. Kaper. 1993. Distribution of the bundle-forming pilus structural gene ( bfpA) among enteropathogenic Escherichia coli. J. Infect. Dis. 168: 1037 1041.
52. Gomes, T. A. T.,, V. Rassi,, K. L. MacDonald,, S. R. T. S. Ramos,, L. R. Trabulsi,, M. A. M. Vieira,, B. E. C. Guth,, J. A. N. Candeias,, C. Ivey,, M. R. F. Toledo,, and P. A. Blake. 1991. Enteropathogens associated with acute diarrheal disease in urban infants in Sao Paulo, Brazil. J. Infect. Dis. 164: 331 337.
53. Griffin, P. M., 1995. Escherichia coli O157:H7 and other enterohemorrhagic Escherichia coli, p. 739 761. In M. J. Blaser,, J. I. Ravdin,, H. B. Greenberg,, and R. L. Guerrant (ed.), Infections of the Gastrointestinal Tract. Raven Press, New York, N.Y.
54. Groisman, E. A.,, and H. Ochman. 1996. Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87: 791 794.
55. Guerrant, R. L.,, L. L. Brunton,, T. C. Schnaitman,, L. I. Rebhun,, and A. G. Gilman. 1974. Cyclic adenosine monophosphate and alteration of Chinese hamster ovary cell morphology: a rapid, sensitive in vitro assay for the enterotoxins of Vibrio cholerae and Escherichia coli. Infect. Immun. 10: 320 327.
56. Gunzberg, S. T.,, B. J. Chang,, J. Elliott,, V. Burke,, and M. Gracey. 1993. Diffuse and enteroaggregative patterns of adherence of enteric Escherichia coli isolated from aboriginal children from the Kimberley region of western Australia. J. Infect. Dis. 167: 755 758.
57. Gunzburg, S. T.,, N. G. Tornieporth,, and L. W. Riley. 1995. Identification of enteropathogenic Escherichia coli by PCR-based detection of the bundle-forming pilus gene. J. Clin. Microbiol. 33: 1375 1377.
58. Gupta, K.,, D. Sahm,, F. Daniel,, D. Mayfield,, and W. E. Stamm. 2001. Antimicrobial resistance among uropathogens that cause community-acquired urinary tract infections in women: A nationwide analysis. Clin. Infect. Dis. 33: 89 94.
59. Gupta, K.,, T. M. Hooton,, and W. E. Stamm. 2001. Increasing antimicrobial resistance and the management of uncomplicated community-acquired urinary tract infections. Ann. Intern. Med. 135: 41 50.
60. Hacker, J.,, G. Oehler-Blum,, I. Muhlodorfer,, and H. Tschape. 1997. Pathogenicity islands of virulent bacteria: structure, function, and impact on microbial evolution. Mol. Microbiol. 23: 1089 1097.
61. Hale, T. L.,, E. V. Oaks,, and S. B. Formal. 1985. Identification and antigenic characterization of virulence-associated, plasmid-coded proteins of Shigella spp. and enteroinvasive Escherichia coli. Infect. Immun. 50: 620 629.
62. Hale, T. L.,, P. J. Sansonetti,, P. A. Schad,, S. Austin,, and S. B. Formal. 1983. Characterization of virulence plasmids and plasmid-associated outer membrane proteins in Shigella flexneri, Shigella sonnei, and Escherichia coli. Infect. Immun. 40: 340 350.
63. Harris, J. R.,, I. K. Wachsmuth,, B. R. Davis,, and M. L. Cohen. 1982. Highmolecular- weight plasmid correlates with Escherichia coli enteroinvasiveness. Infect. Immun. 37: 1295 1298.
64. He, Y.,, J. E. Keen,, R. B. Westerman,, E. T. Littledike,, and J. Kwang. 1996. Monoclonal antibodies for detection of the H7 antigen of Escherichia coli. Appl. Environ. Microbiol. 62: 3325 3332.
65. Hedberg, C. W.,, S. J. Savarino,, J. M. Besser,, C. J. Paulus,, V. M. Thelen,, L. J. Myers,, D. N. Cameron,, T. J. Barrett,, J. B. Kaper,, and M. T. Osterholm. 1997. An outbreak of foodborne illness caused by Escherichia coli O39:NM, an agent not fitting into the existing scheme for classifying diarrheogenic E. coli. J. Infect. Dis. 176: 1625 1628.
66. Herweg, J. C.,, N. Middelkamp,, and H. K. Thornton. 1956. Escherichia coli diarrhea: the relationship of certain serotypes of Escherichia coli to sporadic and endemic cases of infantile diarrhea. J. Paediatr. 49: 629 641.
67. Hiruta, N.,, T. Murase,, and N. Okamura. 2001. An outbreak of diarrhoea due to multiple antimicrobial-resistant Shiga toxin-producing Escherichia coli O26:H11 in a nursery. Epidemiol. Infect. 127: 221 227.
68. Honda, T.,, S. Taga,, Y. Takeda,, and T. Miwatani. 1981. Modified Elek test for detection of heat-labile enterotoxin of enterotoxigenic Escherichia coli. J. Clin. Microbiol. 13: 1 5.
69. Hyams, K. C.,, A. L. Bourgeois,, B. R. Merrell,, P. Rozmajzl,, J. Escamilla,, S. A. Thornton,, G. M. Wasserman,, A. Burke,, P. Echeverria,, K. Y. Green, et al. 1991. Diarrheal disease during Operation Desert Shield. N. Engl. J. Med. 325: 1423 1428.
70. Jelacic, J. K.,, T. Damrow,, G. S. Chen,, S. Jelacic,, M. Bielaszwska,, M. Ciol,, H. M. Carvalho,, A. R. Melton-Celsa,, A. D. O’Brien,, and P. I. Tarr. 2003. Shiga toxin-producing Escherichia coli in Montana: bacterial genotypes and clinical profiles. J. Infect. Dis. 188: 719 729.
71. Jerse, A. E.,, E. J. Yu,, B. D. Tall,, and J. B. Kaper. 1990. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc. Natl. Acad. Sci. USA 87: 7839 7843.
72. Johnson, J. R. 1991. Virulence factors in Escherichia coli urinary tract infection. Clin. Microbiol. Rev. 4: 80 128.
73. Johnson, J. R.,, A. R. Manges,, T. T. O’Bryan,, and L. W. Riley. 2002. A broadly disseminated multi-drug resistant clonal group of extraintestinal pathogenic Escherichia coli as a significant cause of acute pyelonephritis in the U.S. Lancet 359: 2249 2251.
74. Johnson, J. R.,, P. Delavari,, M. Kuskowski,, and A. L. Stell. 2001. Phylogenetic distribution of extraintestinal virulence-associated traits in E. coli. J. Infect. Dis. 183: 78 88.
75. Johnson, W. M.,, and H. Lior. 1988. A new heat-labile cytolethal distending toxin (CLDT) produced by Escherichia coli isolates from clinical material. Microb. Pathog. 4: 103 113.
76. Jones, J. B.,, R. E. Stall,, and H. Bouzar. 1998. Diversity among xanthomonads pathogenic on pepper and tomato. Annu. Rev. Phytopathol. 36: 41 58.
77. Karmali, M. A.,, T. Steele,, M. Petric,, and C. Lim. 1983. Sporadic cases of haemolytic uremic syndrome associated with faecal cytotoxins and cytotoxin-producing Escherichia coli in stools. Lancet i: 619 620.
78. Kauffman, F. 1947. The serology of the coli group. J. Immunol. 57: 71 100.
79. Kenny, B.,, R. Devinney,, M. Stein,, D. J. Reinscheid,, E. A. Frey,, and B. B. Finlay. 1997. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91: 511 520.
80. Kimura, R.,, R. E. Mandrell,, J. C. Galland,, D. Hyatt,, and L. W. Riley. 2000. Restriction-site-specific (RSS)-PCR as a rapid test to detect enterohemorrhagic Escherichia coli O157:H7 strains in environmental samples. Appl. Environ. Microbiol. 66: 2513 2519.
81. Kirby, A. C.,, E. G. Hall,, and W. Coackley. 1950. Neonatal diarrhoea and vomiting: outbreaks in the same maternity unit. Lancet ii: 201 207.
82. Knutton, S.,, T. Baldwin,, P. H. Williams,, and A. S. McNeish. 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 1298.
83. Konowalchuk, J.,, J. I. Speirs,, and S. Stavric. 1977. Vero response to a cytotoxin of Escherichia coli. Infect. Immun. 18: 775 779.
84. Lan, R.,, and P. R. Reeves. 2001. When does a clone deserve a name? A perspective on bacterial species based on population genetics. Trends Microbiol. 9: 419 424.
85. Laurelle, L. 1889. Étude bactériologique sur les peritonitis par perforation. La Cellule 5: 60 123.
86. Lesage, A. A. 1897. Contribution a l’etude des enteritis infantiles—sero-diagnostic des races de Bacterium coli. C. R. Soc. Biol. (Paris) 49: 900 901.
87. Levine, M. M. 1987. Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic and enteroadherent. J. Infect. Dis. 155: 377 389.
88. Levine, M. M.,, E. J. Bergquist,, D. R. Nalin,, D. H. Waterman,, R. B. Hornick,, C. R. Young,, S. Sotman,, and B. Rowe. 1978. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are noninvasive. Lancet i: 1119 1122.
89. Manges, A. R.,, J. R. Johnson,, B. Foxman,, T. T. O’Bryan,, K. R. Fullerton,, and L. W. Riley. 2001. Widespread distribution of urinary tract infections caused by a multidrug resistant Escherichia coli clonal group. N. Engl. J. Med. 345: 1007 1013.
90. Manges, A. R.,, P. S. Dietrich,, and L. W. Riley. 2003. Multidrug-resistant Escherichia coli clonal groups causing community-acquired pyelonephritis. Clin. Infect. Dis. 38: 329 334.
91. McDaniel, T. K.,, K. G. Jarvis,, M. S. Donnenberg,, and J. B. Kaper. 1995. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc. Natl. Acad. Sci. USA 92: 1664 1668.
92. Merson, M. H.,, G. K. Morris,, D. A. Sack,, J. G. Wells,, J. C. Feeley,, R. B. Sack,, W. B. Creech,, A. Z. Kapikian,, and E. J. Gangarosa. 1976. Traveller’s diarrhea in Mexico. A prospective study of physicians and family members attending a congress. N. Engl. J. Med. 294: 1299 1305.
93. Misselwitz, J.,, H. Karch,, M. Bielazewska,, U. John,, F. Ringelmann,, G. Ronnefarth,, and L. Patzer. 2003. Cluster of hemolytic-uremic syndrome caused by Shiga toxin-producing Escherichia coli O26:H11. Pediatr. Infect. Dis. J. 22: 349 354.
94. Mobley, H. L.,, and J. W. Warren (eds.). 1996. Urinary Tract Infections: Molecular Pathogenesis and Clinical Management. ASM Press, Washington, D.C.
95. Moon, H. W.,, S. C. Whipp,, R. A. Argenzio,, M. M. Levine,, and R. A. Giannella. 1983. Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect. Immun. 41: 1340 1351.
96. Moseley, S. L.,, I. Huq,, A. R. M. A. Alim,, M. So,, M. Samadpour-Motalebi,, and S. Falkow. 1980. Detection of enterotoxigenic Escherichia coli by DNA colony hybridization. J. Infect. Dis. 142: 892 898.
97. Moseley, S .L.,, P. Echeverria,, J. Seriwatana,, C. Tiparat,, W. Chaicumpa,, T. Sakuldaipeara,, and S. Falkow. 1982. Identification of enterotoxigenic Escherichia coli by colony hybridization using three enterotoxin gene probes. J. Infect. Dis. 145: 863 869.
98. Nataro, J. P.,, and J. B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11: 142 201.
99. Nataro, J. P.,, J. B. Kaper,, R. Robins-Browne,, V. Prado,, P. Vial,, and M. M. Levine. 1987. Patterns of adherence of diarrheagenic Escherichia coli to Hep-2 cells. Pediatr. Infect. Dis. J. 6: 829 831.
100. Nataro, J. P.,, J. B. Kaper,, R. Robins-Browne,, V. Prado,, P. Vial,, and M. M. Levine. 1987. Patterns of adherence of diarrheagenic Escherichia coli to Hep-2 cells. Pediatr. Infect. Dis. J. 6: 829 831.
101. Nataro, J. P.,, K. O. Maher,, P. Mackie,, and J. B. Kaper. 1987. Characterization of plasmids encoding the adherence factor of enteropathogenic Escherichia coli. Infect. Immun. 55: 2370 2377.
102. Nataro, J. P.,, M. M. Baldini,, J. P. Kaper,, R. E. Black,, N. Bravo,, and M. M. Levine. 1985. Detection of an adherence factor in enteropathogenic Escherichia coli with a DNA probe. J. Infect. Dis. 152: 560 565.
103. Neter, E.,, O. Westphal,, O. Luderitz,, R. M. Gino,, and E. A. Gorzunski. 1955. Demonstration of antibodies against enteropathogenic Escherichia coli in sera of children of various ages. Paediatrics 16: 801 807.
104. O’Brien, A. D.,, and G. D. LaVeck. 1983. Purification and characterization of a Shigella dysenteriae 1-like toxin produced by Escherichia coli. Infect. Immun. 40: 675 683.
105. O’Brien, A. D.,, G. D. LaVeck,, M. R. Thompson,, and S. B. Formal. 1982. Production of Shigella dysenteriae type 1-like cytotoxin by Escherichia coli. J. Infect. Dis. 146: 763 769.
106. Ochman, H.,, and R. K. Selander. 1984. Standard reference strains of Escherichia coli from natural population. J. Bacteriol. 157: 690 692.
107. Olesen, B.,, H. J. Kolmos,, F. Orskov,, and I. Orskov. 1994. Cluster of multiresistant Escherichia coli O78:H10 in greater Greater Copenhagen. Scand. J. Infect. Dis. 26: 406 410.
108. Olesen, B.,, H. J. Kolmos,, F. Orskov,, and I. Orskov. 1995. A comparative study of nosocomial and community-acquired strains of Escherichia coli causing bacteraemia in a Danish University Hospital. J. Hosp. Infect. 31: 295 304.
109. Olive, D. M. 1989. Detection of enterotoxigenic Escherichia coli after polymerase chain reaction amplification with a thermostable DNA polymerase. J. Clin. Microbiol. 27: 261 265.
110. Ostroff, S. M.,, P. I. Tarr,, M. A. Neill,, J. H. Lewis,, N. Hargrett-Bean,, and J. M. Kobayashi. 1989. Toxin genotypes and plasmid profiles as determinants of systemic sequelae in Escherichia coli O157:H7 infections. J. Infect. Dis. 160: 994 998.
111. Paciorek, J. 2002. Virulence properties of Escherichia coli faecal strains isolated in Poland from healthy children and strains belonging to serogroups O18, O26, O44, O86, O126 and O127 isolated from children with diarrhoea. J. Med. Microbiol. 51: 548 556.
112. Panda, C. S.,, L. W. Riley,, S. N. Kumari,, and K. Prakash. 1990. Comparison of alkaline phosphatase-conjugated oligonucleotide DNA probe with the Sereny test for identification of Shigella strains. J. Clin. Microbiol. 28: 2122 2124.
113. Perna, N. T.,, G. Plunkett III,, V. Burland,, B. Mau,, J. D. Glasner,, D. J. Rose,, G. F. Mayhew,, P. S. Evans,, J. Gregor,, H. A. Kirkpatrick,, G. Posfai,, J. Hackett,, S. Klink,, A. Boutin,, Y. Shao,, L. Miller,, E. J. Grotbeck,, N. W. Davis,, A. Lim,, E. T. Dimalanta,, K. D. Potamousis,, J. Apodaca,, T. S. Anantharaman,, J. Lin,, G. Yen,, D. C. Schwartz,, R. A. Welch,, and F. R. Blattner. 2001. Genome sequence of enterohemorrhagic Escherichia coli O157:H7. Nature 409: 529 533.
114. Picard, B.,, J. S. Garcia,, S. Gouriou,, P. Duriez,, N. Brahimi,, E. Bingen,, J. Elion,, and E. Denamur. 1999. The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect. Immun. 67: 546 553.
115. Prats, G.,, F. Navarro,, B. Mirelis,, D. Dalmau,, N. Margall,, P. Coll,, A. Stell,, and J. R. Johnson. 2000. Escherichia coli serotype O15:K52:H1 as an uropathogenic clone. J. Clin. Microbiol. 38: 201 209.
116. Riley, L. W.,, R. S. Remis,, S. D. Helgerson,, H. B. McGee,, J. G. Wells,, B. R. Davis,, R. J. Herbert,, H. Olcott,, L. Johnson,, N. Hargrett,, P. A. Blake,, and M. L. Cohen. 1983. Outbreaks of hemorrhagic colitis associated with a rare Escherichia coli serotype. N. Engl. J. Med. 308: 681 685.
117. Riley, L. W., 1988. Infectious diseases associated with Escherichia coli, p. 237 261. In A. Balows,, W. J. Hausler, Jr.,, M. Ohashi,, and A. Turano (ed.), Laboratory Diagnosis of Infectious Diseases, Principles and Practice, vol. 1. Springer-Verlag, New York, N. Y.
118. Robins-Browne, R. M. 1987. Traditional enteropathogenic Escherichia coli of infantile diarrhea. Rev. Infect. Dis. 9: 28 53.
119. Rothbaum, R.,, A. J. McAdams,, R. Giannella,, and J. C. Partin. 1982. A clinicopathological study of enterocyte-adherent Escherichia coli: a cause of protracted diarrhea in infants. Gastroenterology 83: 441 454.
120. Rowe, B. 1979. The role of Escherichia coli in gastroenteritis. Clin. Gastroenterol. 8: 625 644.
121. Russo, T. A.,, and J. R. Johnson. 2000. Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J. Infect. Dis. 181: 1753 1754.
122. Sakazaki, R.,, K. Tamura,, and M. Saito. 1967. Enteropathogenic Escherichia coli associated with diarrhea in children and adults. Jpn. J. Med. Sci. Biol. 20: 387 399.
123. Sansonetti, P. J.,, D. J. Kopecko,, and S. B. Formal. 1982. Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect. Immun. 35: 852 860.
124. Scaletsky, I. C. A.,, R. M. Silva,, and L. R. Trabulsi. 1984. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect. Immun. 45: 534 536.
125. Schmidt, H.,, C. Geitz,, P. I. Tarr,, M. Frosch,, and H. Karch. 1999. Non- O157:H7 pathogenic Shiga toxin-producing Escherichia coli: phenotypic and genetic profiling of virulence traits and evidence for clonality. J. Infect. Dis. 179: 115 123.
126. Schultsz, C.,, G. J. Pool,, R. van Ketel,, B. de Wever,, P. Speelman,, and J. Dankert. 1994. Detection of enterotoxigenic Escherichia coli in stool samples by using nonradioactively labeled oligonucleotide DNA probes and PCR. J. Clin. Microbiol. 32: 2393 2397.
127. Seigel, R. R.,, C. S. Sant’anna,, K. Salgado,, P. deJesus,, and L. W. Riley. 1996. Acute diarrhea among children from high and low socioeconomic communities in Salvador, Brazil. Int. J. Infect. Dis. 1: 28 34.
128. Sereny, B. 1957. Experimental keratoconjunctivitis shigellosa. Acta Microbiol. Acad. Sci. Hung. 4: 367 376.
129. Sethabutr, O.,, M. Venkatesan,, G. S. Murphy,, B. Eampokalap,, C. W. Hoge,, and P. Echeverria. 1993. Detection of Shigellae and enteroinvasive Escherichia coli by amplification of the invasion plasmid antigen H DNA sequence in patients with dysentery. J. Infect. Dis. 167: 458 461.
130. Silva, R. M.,, M. R. F. Toledo,, and L. R. Trabulsi. 1980. Biochemical and cultural characteristics of invasive Escherichia coli. J. Clin. Microbiol. 11: 441 444.
131. Sinclair, W. A.,, H. H. Lyon,, and W. T. Johnson. 1987. Diseases of Trees and Shrubs. Cornell University Press, Ithaca, N.Y.
132. Smith, H. R.,, and S. M. Scotland. 1993. Isolation and identification methods for Escherichia coli O157 and other Vero cytotoxin producing strains. J. Clin. Pathol. 46: 10 17.
133. Smith, H. R.,, S. M. Scotland,, G. A. Willshaw,, B. Rowe,, A. Cravioto,, and C. Eslava. 1994. Isolates of Escherichia coli O44:H18 of diverse origin are enteroaggregative. J. Infect. Dis. 170: 1610 1613.
134. Smith, H. W.,, and C. L. Gyles. 1970. The relationship between two apparently different enterotoxins produced by enteropathogenic strains of Escherichia coli of porcine origin. J. Med. Microbiol. 3: 387 401.
135. Sowers, E. G.,, J. G. Wells,, and N. A. Strockbine. 1996. Evaluation of commercial latex reagents for identification of O157 and H7 antigens of Escherichia coli. J. Clin. Microbiol. 34: 1286 1289.
136. Speirs, J.,, S. Stavric,, and B. Buchanan. 1991. Assessment of two commercial agglutination kits for detecting Escherichia coli heat-labile enterotoxin. Can. J. Microbiol. 37: 877 880.
137. Stamm, W. E.,, and S. R. Norrby. 2001. Urinary tract infections: disease panorama and challenges. J. Infect. Dis. 183( Suppl. 1): S1 S4.
138. Strockbine, N. A.,, J. G. Wells,, and T. J. Barrett,. 1998. Isolation of STEC from clinical specimens. In J. B. Kaper, and A. D. O’Brien (ed.), Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli. ASM Press, Washington D.C.
139. Sussman, M., 1997. Escherichia coli and human disease, p. 3 48. In M. Sussman (ed.), Escherichia coli: Mechanisms of Virulence. Cambridge University Press, Cambridge, England.
140. Tarr, C. L.,, T. M. Large,, C. L. Moeller,, D. W. Lacher,, P. I. Tarr,, D. W. Acheson,, and T. S. Whittam. 2002. Molecular characterization of a serotype O121:H19 clone, a distinct Shiga toxin-producing clone of pathogenic Escherichia coli. Infect. Immun. 70: 6853 6859.
141. Taylor, J.,, and K. A. Bettelheim. 1966. The action of chloroform-killed suspensions of enteropathogenic Escherichia coli on ligated rabbit-gut segments. J. Gen. Microbiol. 42: 309 313.
142. Toledo, M. R. F.,, M. C. B. Alvariza,, J. Murahovschi,, S. R. T. S. Ramos,, and L. R. Trabulsi. 1983. Enteropathogenic Escherichia coli serotypes and endemic diarrhea in infants. Infect. Immun. 39: 586 589.
143. Tornieporth, N. G.,, J. John,, K. Salgado,, P. de Jesus,, E. Latham,, M. C. Melo,, S. T. Gunzburg,, and L. W. Riley. 1995. Differentiation of pathogenic Escherichia coli strains in Brazilian children by PCR. J. Clin. Microbiol. 33: 1371 1374.
144. Trabulsi, L. R.,, L. C. Campos,, T. S. Whittam,, T. A. T. Gomes,, J. Rodrigues,, and A. G. Goncalves. 1996. Traditional and non-traditional enteropathogenic Escherichia coli serogroups. Rev. Microbiol. Sao Paulo 27(Suppl. 1): 1 6.
145. Trabulsi, L. R.,, R. Keller,, and T. A. T. Gomes. 2002. Typical and atypical enteropathogenic Escherichia coli. Emerg. Infect. Dis. 8: 508 513.
146. Tullus, K.,, K. Horlin,, S. B. Svenson,, and G. Kallenius. 1984. Epidemic outbreaks of acute pyelonephritis caused by nosocomial spread of P fimbriated Escherichia coli in children. J. Infect. Dis. 150: 728 736.
147. van Doorn, J.,, T. C. Hollinger,, and P. M. Boonekamp. 1997. Pathovar-specific detection of Xanthomonas campestri in Hyacinths. Acta Hort. 430: 649 650.
148. Vila, J.,, M. Vargas,, J. Ruiz,, M. Espasa,, M. Pujol,, M. Corachan,, M. T. Jimenez de Anta,, and J. Gascon. 2001. Susceptibility patterns of enteroaggregative Escherichia coli associated with traveller’s diarrhoea: emergence of quinolone resistance. J. Med. Microbiol. 50: 996 1000.
149.Viljanen, M, T. Peltola, S. Junnila, L. Olkkonen, H. Jarvinen, and M. Kuistila. 1990. Outbreak of diarrhoea due to Escherichia coli O111:B4 in school children and adults: association of Vi antigen-like reactivity. Lancet 336: 831841.
150. von Sonnenburg, F.,, N. Tornieporth,, P. Waiyaki,, B. Lowe,, L. F. Peruski,, H. L. DuPont,, J. J. Mathewson,, and R. Steffen. 2000. Risk and aetiology of diarrhoea at various tourist destinations. Lancet 356: 133 134.
151. Wells, J. G.,, B. R. Davis,, I. K. Wachsmuth,, L. W. Riley,, R. S. Remis,, and R. Sokolov. 1983. Laboratory investigation of outbreaks of hemorrhagic colitis associated with a rare Escherichia coli serotype. J. Clin. Microbiol. 18: 512 520.
152. Wentworth, F. H.,, D. W. Brock,, C. S. Stulberg,, and R. H. Page. 1956. Clinical, bacteriological, and serological observations of two human volunteers following ingestion of Escherichia coli O127:B8. Proc. Soc. Exp. Biol. Med. 91: 586 588.
153. Werber, D.,, A. Fruth,, A. Liesegang,, M. Littmann,, U. Buchholz,, R. Prager,, H. Karch,, T. Breuer,, H. Tschape,, and A. Ammon. 2002. A multistate outbreak of Shiga toxin-producing Escherichia coli O26:H11 infections in Germany, detected by molecular subtyping surveillance. J. Infect. Dis. 186: 419 422.
154. Whittam, T. S.,, I. K. Wachsmuth,, and R. A. Wilson. 1988. Genetic evidence of clonal descent of Escherichia coli O157:H7 association with hemorrhagic colitis and hemolytic uremic syndrome. J. Infect. Dis. 157: 1124 1133.
155. World Health Organization. 1998. Zoonotic Non-O157 Shiga Toxin- Producing Escherichia coli (STEC). Report of a WHO Scientific Working Group Meeting, p. 135. Department of Communicable Disease Surveillance and Response, World Health Organization, Geneva, Switzerland.


Generic image for table
Table 7.1

Classification of associated with diarrhea by serotypes

Adapted from reference with permission.

Citation: Riley L. 2004. Distinguishing Pathovars from Nonpathovars: , p 175-208. In Molecular Epidemiology of Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817688.ch7
Generic image for table
Table 7.2

Gene targets for DNA probe- or PCR-based detection of associated with diarrhea

Citation: Riley L. 2004. Distinguishing Pathovars from Nonpathovars: , p 175-208. In Molecular Epidemiology of Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817688.ch7
Generic image for table
Table 7.3

Classification of EPEC into “typical” and “atypical” EPEC serotypes

Adapted from reference .

Citation: Riley L. 2004. Distinguishing Pathovars from Nonpathovars: , p 175-208. In Molecular Epidemiology of Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817688.ch7
Generic image for table
Table 7.4

Putative virulence factors (genes) included in typing strains isolated from urinary tract infectionsm

Adapted from reference .

Citation: Riley L. 2004. Distinguishing Pathovars from Nonpathovars: , p 175-208. In Molecular Epidemiology of Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817688.ch7

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error