Highlighted Text:
Show |
Hide
Full text loading...
Chapter 15 : Thomas Whittam, Shiga Toxin-Producing Escherichia coli, and the Clinical Consequences of Clonality
Authors:
Shana R. Leopold1,
Phillip I. Tarr2
VIEW AFFILIATIONS
HIDE AFFILIATIONS
Affiliations:
1: Departments of Pediatrics and Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63105;
2: Departments of Pediatrics and Molecular Microbiology, Washington University School of Medicine, St. Louis, MO 63105
Content Type: Monograph
Publication Year:
2011
Category: Bacterial Pathogenesis
Book DOI:
10.1128/9781555817114
Chapter DOI:
10.1128/9781555817114.ch15
MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
Preview this chapter:
Thomas Whittam, Shiga Toxin-Producing Escherichia coli, and the Clinical Consequences of Clonality, Page 1 of 2
< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555817114/9781555819354_Chap15-1.gif /docserver/preview/fulltext/10.1128/9781555817114/9781555819354_Chap15-2.gif
Abstract:
This chapter reviews the impact of Tom's contributions to the field of microbial evolution and to the evolution of one's understanding of the enteric pathogenicity of E. coli. Additional progress was made, also in Germany, in the 1920s: Adam demonstrated groups of E. coli that were biochemically distinct, which he termed ‘’dyspepsiekoli’’. The resulting genetic analysis categorized the species into four main groups (A, B1, B2, and D) and one minor group (E), and generated a widely used phylogenetic reference that has served as the foundation for investigators in the generation since. The putative cardinal virulence trait of E. coli O157:H7, namely, the possession of one or more Shiga toxin genes, was not by itself sufficient to cause severe human disease. The author says that Tom also identified different eae (intimin) alleles as different classes of EPEC and Shiga toxin-producing E. coli (STEC) were described, and framed his work in the context of microbial evolution, epidemiology, and clinical medicine. Despite these limitations, Tom expounded graciously and patiently on his theories of clonality. Tom's investigations into the emergence of diarrheagenic E. coli, and most particularly of the O157:H7 EHEC 1 clade, stand as monumental and enduring contributions to the field.
Citation:
Leopold S, Tarr P.
2011.
Thomas Whittam, Shiga Toxin-Producing Escherichia coli, and the Clinical Consequences of Clonality,
p 257-272.
In
Walk S, Feng P (ed),
Population Genetics of Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555817114.ch15
Figures
Thomas Whittam, Shiga Toxin-Producing Escherichia coli, and the Clinical Consequences of Clonality
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817114.ch15-1,webId=/content/author/10.1128/9781555817114.ch15-1,properties={foaf_givenname=Shana R., foaf_name=Shana R. Leopold, foaf_surname=Leopold, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817114.ch15-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817114.ch15-2,webId=/content/author/10.1128/9781555817114.ch15-2,properties={foaf_givenname=Phillip I., foaf_name=Phillip I. Tarr, foaf_surname=Tarr, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817114.ch15-aff2]]}]]
Citation:
Leopold S, Tarr P.
2011.
Thomas Whittam, Shiga Toxin-Producing Escherichia coli, and the Clinical Consequences of Clonality,
p 257-272.
In
Walk S, Feng P (ed),
Population Genetics of Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555817114.ch15
/content/10.1128/9781555817114.ch15.ch15fig01
Figure 1.
Early presentation on EHEC by Tom Whittam. (Left) Abstract book cover. (Right) Abstract of talk delivered by Tom Whittam on the afternoon of Tuesday, July 14, 1987.
10.1128/9781555817114/f0260-01_thmb.gif
10.1128/9781555817114/f0260-01.gif
Figure 1.
Early presentation on EHEC by Tom Whittam. (Left) Abstract book cover. (Right) Abstract of talk delivered by Tom Whittam on the afternoon of Tuesday, July 14, 1987.
Citation:
Leopold S, Tarr P.
2011.
Thomas Whittam, Shiga Toxin-Producing Escherichia coli, and the Clinical Consequences of Clonality,
p 257-272.
In
Walk S, Feng P (ed),
Population Genetics of Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555817114.ch15
/content/10.1128/9781555817114.ch15.ch15fig02
Figure 2.
Unexplained faint band in a gel. Primers within yehV in E. coli O55:H7 produced a prominent 340-bp amplicon (white oval) as expected because this gene is not disrupted by a bacteriophage. Primers across the same site in stx
1
–
stx
2
+ as well as stx
1
–
stx
2
+
E. coli O157:H7 yield fainter bands (black oval), whereas we anticipated a stronger band, as in the nontoxigenic progenitor strain, E. coli O55:H7, amplified using the same primer set. Subsequent work demonstrated that a truncated bacteriophage occupied this site in E. coli O157:H7 that did not contain stx
1 (black dashed oval); the bacteriophage-chromosome junction amplicons are within the white dashed borders. Additional amplifications led us to deduce the precise phylogeny of emergence of the three major E. coli O157: H7 subgroups (
14
,
56
,
87
,
88
). These data eventually led us to formulate a precise emergence of the EHEC 1 clade (see
Fig. 3
). Reproduced with permission from
Fig. 1
in reference
88
.
10.1128/9781555817114/f0264-01_thmb.gif
10.1128/9781555817114/f0264-01.gif
Figure 2.
Unexplained faint band in a gel. Primers within yehV in E. coli O55:H7 produced a prominent 340-bp amplicon (white oval) as expected because this gene is not disrupted by a bacteriophage. Primers across the same site in stx 1 – stx 2 + as well as stx 1 – stx 2 + E. coli O157:H7 yield fainter bands (black oval), whereas we anticipated a stronger band, as in the nontoxigenic progenitor strain, E. coli O55:H7, amplified using the same primer set. Subsequent work demonstrated that a truncated bacteriophage occupied this site in E. coli O157:H7 that did not contain stx 1 (black dashed oval); the bacteriophage-chromosome junction amplicons are within the white dashed borders. Additional amplifications led us to deduce the precise phylogeny of emergence of the three major E. coli O157: H7 subgroups ( 14 , 56 , 87 , 88 ). These data eventually led us to formulate a precise emergence of the EHEC 1 clade (see Fig. 3 ). Reproduced with permission from Fig. 1 in reference 88 .
Citation:
Leopold S, Tarr P.
2011.
Thomas Whittam, Shiga Toxin-Producing Escherichia coli, and the Clinical Consequences of Clonality,
p 257-272.
In
Walk S, Feng P (ed),
Population Genetics of Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555817114.ch15
/content/10.1128/9781555817114.ch15.ch15fig03
Figure 3.
Evolutionary scenario for EHEC 1 pathogens. E. coli O55:H7 belongs to the most ancestral subgroup (A) of the EHEC 1 clade. The second sphere from the left (lower row) depicts a probably extinct intermediate between O55:H7 and E. coli expressing the O157 lipopolysaccharide (LPS), with subgroup B consisting of the sorbitol-fermenting O157:H– and subgroup C consisting of E. coli O157:H7. We note several critical intraclade events. The ovals within clusters represent genomically sequenced strains (middle gray). Strains used for single nucleotide polymorphism (SNP) consensus sampling are black, inferred founders are light gray, and postulated organisms that are immediate progenitors to the next cluster or subgroup are white ovals. In cluster 1, screened strains were assigned to the main branch if they had each of the three signature SNPs among the 111 shared SNPs (
38
/
48
), and the minor branch if they lacked this set of SNPs (
10
/
48
). More extensive evolutionary detail is provided in Fig. S1 in reference
56
. Distances not drawn to scale. Reprinted with permission from reference
56
. GUD, β-d-glucuronidase; TAI, tellurite resistance- and adherence-conferring island.
10.1128/9781555817114/f0265-01_thmb.gif
10.1128/9781555817114/f0265-01.gif
Figure 3.
Evolutionary scenario for EHEC 1 pathogens. E. coli O55:H7 belongs to the most ancestral subgroup (A) of the EHEC 1 clade. The second sphere from the left (lower row) depicts a probably extinct intermediate between O55:H7 and E. coli expressing the O157 lipopolysaccharide (LPS), with subgroup B consisting of the sorbitol-fermenting O157:H– and subgroup C consisting of E. coli O157:H7. We note several critical intraclade events. The ovals within clusters represent genomically sequenced strains (middle gray). Strains used for single nucleotide polymorphism (SNP) consensus sampling are black, inferred founders are light gray, and postulated organisms that are immediate progenitors to the next cluster or subgroup are white ovals. In cluster 1, screened strains were assigned to the main branch if they had each of the three signature SNPs among the 111 shared SNPs ( 38 / 48 ), and the minor branch if they lacked this set of SNPs ( 10 / 48 ). More extensive evolutionary detail is provided in Fig. S1 in reference 56 . Distances not drawn to scale. Reprinted with permission from reference 56 . GUD, β-d-glucuronidase; TAI, tellurite resistance- and adherence-conferring island.
Citation:
Leopold S, Tarr P.
2011.
Thomas Whittam, Shiga Toxin-Producing Escherichia coli, and the Clinical Consequences of Clonality,
p 257-272.
In
Walk S, Feng P (ed),
Population Genetics of Bacteria.
ASM Press, Washington, DC.
doi: 10.1128/9781555817114.ch15
References
/content/book/10.1128/9781555817114.ch15
1.
Abu-Ali, G. S.,, L. M. Ouellette,, S. T. Henderson,, D. W. Lacher,, J. T. Riordan,, T. S. Whittam, and, S. D. Manning. 2010. Increased adherence and expression of virulence genes in a lineage of Escherichia coli O157:H7 commonly associated with human infections. PLoS One 5: e10167.
2.
Abu-Ali, G. S.,, L. M. Ouellette,, S. T. Henderson,, T. S. Whittam, and, S. D. Manning. 2010. Differences in adherence and virulence gene expression between two outbreak strains of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 156: 408– 419.
3.
Adam, A. 1927. Dyspepsiekoli. Zur Frage der bakteriellen ätiologie der sogenannten alimentären Intoxikation. Jahrbuch Kinderheilkd. 116: 8.
4.
Adam, A. 1956. Sauglings-Enteritis. Georg Thieme Verlag, Stuttgart, Germany.
5.
Adam, A. 1923. über die Biologie der Dyspepsiecoli und ihre Beziehungen zur Pathogenese der Dyspepsie und Intoxikation. Jahrbuch Kinderheilkd. 101: 295.
6.
Adam, A.,, and C. Froboese. 1925. Untersuchungen zur Pathologie der Durchfallserkrankungen des Säuglings. Jahrbuch Kinderheilkd. 39: 267.
7.
Alpers, K.,, D. Werber,, C. Frank,, J. Koch,, A. W. Friedrich,, H. Karch,, M. an der Heiden,, R. Prager,, A. Fruth,, M. Bielaszewska,, G. Morlock,, A. Heissenhuber,, A. Diedler,, A. Gerber, and, A. Ammon. 2009. Sorbitol-fermenting enterohaemorrhagic Escherichia coli O157:H – causes another outbreak of haemolytic uraemic syndrome in children. Epidemiol. Infect. 137: 389– 395.
8.
Armstrong, J. G. 1958. Acute gastroenteritis; a review of 821 cases treated at the Hospital for Sick Children during the year 1956. J. Pediatr. 53: 704– 718.
9.
Bachmann, B. J. 1990. Linkage map of Escherichia coli K-12, edition 8. Microbiol. Rev. 54: 130– 197.
10.
Banerjea, A.,, D. N. Chatterji, and, K. Pramanick. 1957. Gastro-enteritis in different age-groups and its association with certain serological types of Escherichia coli. Ann. Biochem. Exp. Med. 17: 99.
11.
Barcak, G. J.,, and R. E. Wolf, Jr. 1988. Comparative nucleotide sequence analysis of growth-rate-regulated gnd alleles from natural isolates of Escherichia coli and from Salmonella typhimurium LT-2. J. Bacteriol. 170: 372– 379.
12.
Barnard, P. J.,, and M. Kibel. 1965. The haemolytic-uraemic syndrome of infancy and childhood. A report of eleven cases. Cent. Afr. J. Med. 11: 31– 34.
13.
Bergan, T. (ed.). 1984. Methods in Microbiology, vol. 14. Academic Press, London, United Kingdom.
14.
Besser, T. E.,, N. Shaikh,, N. J. Holt,, P. I. Tarr,, M. E. Konkel,, P. Malik-Kale,, C. W. Walsh,, T. S. Whittam, and, J. L. Bono. 2007. Greater diversity of Shiga toxin-encoding bacteriophage insertion sites among Escherichia coli O157:H7 isolates from cattle than in those from humans. Appl. Environ. Microbiol. 73: 671– 679.
15.
Bielaszewska, M.,, R. Prager,, L. Vandivinit,, A. Müsken,, A. Mellmann,, N. J. Holt,, P. I. Tarr,, H. Karch, and, W. Zhang. 2009. Detection and characterization of the fimbrial sfp cluster in enterohemorrhagic Escherichia coli O165:H25/NM isolates from humans and cattle. Appl. Environ. Microbiol. 75: 64– 71.
16.
Bilge, S. S.,, J. C. Vary, Jr.,, S. F. Dowell, and, P. I. Tarr. 1996. Role of the Escherichia coli O157:H7 O side chain in adherence and analysis of an rfb locus. Infect. Immun. 64: 4795– 4801.
17.
Bisercic, M.,, J. Y. Feutrier, and, P. R. Reeves. 1991. Nucleotide sequences of the gnd genes from nine natural isolates of Escherichia coli: evidence of intragenic recombination as a contributing factor in the evolution of the polymorphic gnd locus. J. Bacteriol. 173: 3894– 3900.
18.
Bokete, T. N.,, T. S. Whittam,, R. A. Wilson,, C. R. Clausen,, C. M. O’Callahan,, S. L. Moseley,, T. R. Fritsche, and, P. I. Tarr. 1997. Genetic and phenotypic analysis of Escherichia coli with enteropathogenic characteristics isolated from Seattle children. J. Infect. Dis. 175: 1382– 1389.
19.
Boyer, K. M.,, N. J. Petersen,, I. Farzaneh,, C. P. Pattison,, M. C. Hart, and, J. E. Maynard. 1975. An outbreak of gastroenteritis due to E. coli 0142 in a neonatal nursery. J. Pediatr. 86: 919– 927.
20.
Bray, J. 1973. Bray’s discovery of pathogenic Esch. coli as a cause of infantile gastroenteritis. Arch. Dis. Child. 48: 923– 926.
21.
Bray, J. 1945. Isolation of antigenically homogeneous strains of Bact. coli neapolitanum from summer diarrhoea of infants. J. Pathol. Bacteriol. 57: 239.
22.
Brooks, J. T.,, E. G. Sowers,, J. G. Wells,, K. D. Greene,, P. M. Griffin,, R. M. Hoekstra, and, N. A. Strockbine. 2005. Non-O157 Shiga toxinproducing Escherichia coli infections in the United States, 1983–2002. J. Infect. Dis. 192: 1422– 1429.
23.
Castellani, A.,, and A. J. Chalmers. 1919. Manual of Tropical Medicine, 3rd ed. William Wood, New York, NY.
24.
Caugant, D. A.,, B. R. Levin,, G. Lidin-Janson,, T. S. Whittam,, C. Svanborg Edén, and, R. K. Selander. 1983. Genetic diversity and relationships among strains of Escherichia coli in the intestine and those causing urinary tract infections. Prog. Allergy 33: 203– 227.
25.
Clausen, C. R.,, and D. L. Christie. 1982. Chronic diarrhea in infants caused by adherent enteropathogenic Escherichia coli. J. Pediatr. 100: 358– 361.
26.
Cooper, M. L.,, E. W. Walters,, H. M. Keller,, J. M. Sutherland, and, H. J. Wiseman. 1955. Epidemic diarrhea among infants associated with the isolation of a new serotype of Escherichia coli: E. coli 0127:B8. Pediatrics 16: 215– 227.
27.
Darrasse, H.,, L. Le Minor,, D. Piechaud, and, P. Nicolle. 1957. Pathogenic enterobacteria from Dakar. Bull. Soc. Pathol. Exot. Filiales 50: 257– 281. (In French.)
28.
Davydov, V. P. 1958. Serologic characteristics of Escherichia coli isolated in infants with gastrointestinal diseases. Zh. Mikrobiol. Epidemiol. Immunobiol. 29: 56– 60. (In Russian.)
29.
Derham, R. J.,, and M. M. Rogerson. 1957. Gastroenteritis in infancy. AMA J. Dis. Child. 93: 113– 121.
30.
Drimmer-Herrnheiser, H.,, and A. L. Olitzki. 1951. The association of Escherichia coli (serotypes 0111:B4 and 055:B5) with cases of acute infantile gastroenteritis in Jerusalem. Acta Med. Orient. 10: 219– 223.
31.
Dykhuizen, D. E.,, and L. Green. 1991. Recombination in Escherichia coli and the definition of biological species. J. Bacteriol. 173: 7257– 7268.
32.
Escherich, T. 1885. Die darmbakterien des neugeborenen und säuglings. Fortschr. Med. 3: 515– 522, 547– 554.
33.
Escherich, T. 1886. Die Darmbakterien des Säuglings und Ihre Beziehungen zur Physiologie der Verdauung. Fernidnand Enke, Stuttgart, Germany.
34.
Escherich, T. 1988. The intestinal bacteria of the neonate and breast-fed infant. 1884. Rev. Infect. Dis. 10: 1220– 1225.
35.
Escherich, T. 1989. The intestinal bacteria of the neonate and breast-fed infant. 1885. Rev. Infect. Dis. 11: 352– 356.
36.
Ewing, W. H.,, H. W. Tatum, and, B. R. Davis. 1957. The occurrence of Escherichia coli serotypes associated with diarrheal diseases in the United States. Public Health Lab. 15: 118.
37.
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.
38.
Feng, P. C.,, S. R. Monday,, D. W. Lacher,, L. Allison,, A. Siitonen,, C. Keys,, M. Eklund,, H. Nagano,, H. Karch,, J. Keen, and, T. S. Whittam. 2007. Genetic diversity among clonal lineages within Escherichia coli O157:H7 stepwise evolutionary model. Emerg. Infect. Dis. 13: 1701– 1706.
39.
Fournelle, H. J.,, I. L. Wallace, and, V. Rader. 1958. A bacteriological and parasito-logical survey of enteric infections in an Alaskan Eskimo area. Am. J. Public Health Nations Health 48: 1489– 1497.
40.
Goldschmidt, R. 1933. Untersuchungen zur Atiologie der Durchfallserkrankungen des Säuglings. Jahrbuch Kinderheilkd. 139: 318.
41.
Gunzer, F.,, H. Böhm,, H. Rüssmann,, M. Bitzan,, S. Aleksic, and, H. Karch. 1992. Molecular detection of sorbitol-fermenting Escherichia coli O157 in patients with hemolytic-uremic syndrome. J. Clin. Microbiol. 30: 1807– 1810.
42.
Hayashi, T.,, K. Makino,, M. Ohnishi,, K. Kurokawa,, K. Ishii,, K. Yokoyama,, C. G. Han,, E. Ohtsubo,, K. Nakayama,, T. Murata,, M. Tanaka,, T. Tobe,, T. Iida,, H. Takami,, T. Honda,, C. Sasakawa,, N. Ogasawara,, T. Yasunaga,, S. Kuhara,, T. Shiba,, M. Hattori, and, H. Shinagawa. 2001. Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res. 8: 11– 22.
43.
Herweg, J. C.,, J. N. Middelkamp, and, H. K. Thornton. 1956. Escherichia coli diarrhea; the relationship of certain serotypes of Escherichia coli to sporadic and epidemic cases of infantile diarrhea. J. Pediatr. 49: 629– 641.
44.
Herzer, P. J.,, S. Inouye,, M. Inouye, and, T. S. Whittam. 1990. Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J. Bacteriol. 172: 6175– 6181.
45.
Hinton, N. A.,, and R. R. MacGregor. 1958. A study of infections due to pathogenic serogroups of Escherichia coli. Can. Med. Assoc. J. 79: 359– 364.
46.
Holzel, A. 1974. Correspondence: Bray’s discovery of pathogenic Esch. coli as a cause of infantile gastroenteritis. Arch. Dis. Child. 49: 668.
47.
Jarvis, K. G.,, J. A. Girón,, A. E. Jerse,, T. K. McDaniel,, M. S. Donnenberg, and, J. B. Kaper. 1995. Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc. Natl. Acad. Sci. USA 92: 7996– 8000.
48.
Jenke, C.,, D. Harmsen,, T. Weniger,, J. Rothganger,, E. Hyytia-Trees,, M. Bielaszewska,, H. Karch, and, A. Mellmann. Phylogenetic analysis of enterohemorrhagic Escherichia coli O157, Germany, 1987–2008. Emerg. Infect. Dis. 16: 610– 616.
49.
Jerse, A. 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.
50.
Judicial Commission of the International Committee on Bacteriological Nomenclature. 1958. Conservation of the family name Enterobacteriaceae, of the name of the type genus, and designation of the type species. Intl. Bull. Bacteriol. Nomencl. Taxon. 8: 73– 74.
51.
Kaplan, B. S.,, R. W. Chesney, and, K. N. Drummond. 1975. Hemolytic uremic syndrome in families. N. Engl. J. Med. 292: 1090– 1093.
52.
Karmali, M. A.,, B. T. Steele,, M. Petric, and, C. Lim. 1983. Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin and cytotoxin-producing Escherichia coli in stools. Lancet 1: 619– 620.
53.
Kauffmann, F. 1954. Enterobacteriaceae, 2nd ed. Ejnar Munksgaard, Copenhagen, Denmark.
54.
Konowalchuk, J.,, J. I. Speirs, and, S. Stavric. 1977. Vero response to a cytotoxin of Escherichia coli. Infect. Immun. 18: 775– 779.
55.
Lanata, C. F.,, W. Mendoza, and, R. E. Black. 2002. Improving Diarrhoea Estimates. World Health Organization, Geneva, Switzerland.
56.
Leopold, S. R.,, V. Magrini,, N. J. Holt,, N. Shaikh,, E. R. Mardis,, J. Cagno,, Y. Ogura,, A. Iguchi,, T. Hayashi,, A. Mellmann,, H. Karch,, T. E. Besser,, S. A. Sawyer,, T. S. Whittam, and, P. I. Tarr. 2009. A precise reconstruction of the emergence and constrained radiations of Escherichia coli O157 portrayed by backbone concatenomic analysis. Proc. Natl. Acad. Sci. USA 106: 8713– 8718.
57.
Manning, S. D.,, A. S. Motiwala,, A. C. Springman,, W. Qi,, D. W. Lacher,, L. M. Ouellette,, J. M. Mladonicky,, P. Somsel,, J. T. Rudrik,, S. E. Dietrich,, W. Zhang,, B. Swaminathan,, D. Alland, and, T. S. Whittam. 2008. Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks. Proc. Natl. Acad. Sci. USA 105: 4868– 4873.
58.
Martineau, B.,, R. Raymond, and, G. Jeliu. 1958. Bacteriological and clinical study of gastro-enteritis with enteropathogenic Escherichia coli 0127:B8. Can. Med. Assoc. J. 79: 351– 359.
59.
McGraw, E. A.,, J. Li,, R. K. Selander, and, T. S. Whittam. 1999. Molecular evolution and mosaic structure of α, β, and γ intimins of pathogenic Escherichia coli. Mol. Biol. Evol. 16: 12– 22.
60.
Mellmann, A.,, M. Bielaszewska,, R. Köck,, A. W. Friedrich,, A. Fruth,, B. Middendorf,, D. Harmsen,, M. A. Schmidt, and, H. Karch. 2008. Analysis of collection of hemolytic uremic syndrome-associated enterohemorrhagic Escherichia coli. Emerg. Infect. Dis. 14: 1287– 1290.
61.
Milkman, R. 1973. Electrophoretic variation in Escherichia coli from natural sources. Science 182: 1024– 1026.
62.
Monday, S. R.,, T. S. Whittam, and, P. C. Feng. 2001. Genetic and evolutionary analysis of mutations in the gusA gene that cause the absence of β-glucuronidase activity in Escherichia coli O157:H7. J. Infect. Dis. 184: 918– 921.
63.
Neill, M. A.,, P. I. Tarr,, C. R. Clausen,, D. L. Christie, and, R. O. Hickman. 1987. Escherichia coli O157:H7 as the predominant pathogen associated with the hemolytic uremic syndrome: a prospective study in the Pacific Northwest. Pediatrics 80: 37– 40.
64.
Nelson, K.,, and R. K. Selander. 1994. Intergeneric transfer and recombination of the 6-phosphogluconate dehydrogenase gene ( gnd) in enteric bacteria. Proc. Natl. Acad. Sci. USA 91: 10227– 10231.
65.
Neter, E. 1955. Escherichia coli diarrhea: an outbreak among infants on a surgical ward. AMA Am. J. Dis. Child. 89: 564– 566.
66.
Neter, E.,, R. F. Korns, and, R. E. Trussel. 1953. Association of Escherichia coli sero-group 0111 with two hospital outbreaks of epidemic diarrhea of the newborn infant in New York State during 1947. Pediatrics 12: 377– 383.
67.
Neter, E.,, O. Westphal,, O. Luderitz,, R. M. Gino, and, E. A. Gorzynski. 1955. Demonstration of antibodies against enteropathogenic Escherichia coli in sera of children of various ages. Pediatrics 16: 801– 808.
68.
O’Brien, A. O.,, T. A. Lively,, M. E. Chen,, S. W. Rothman, and, S. B. Formal. 1983. Escherichia coli O157:H7 strains associated with haemorrhagic colitis in the United States produce a Shigella dysenteriae 1 (SHIGA) like cytotoxin. Lancet 1: 702.
69.
Ochman, H.,, and R. K. Selander. 1984. Standard reference strains of Escherichia coli from natural populations. J. Bacteriol. 157: 690– 693.
70.
Ochman, H.,, T. S. Whittam,, D. A. Caugant, and, R. K. Selander. 1983. Enzyme polymorphism and genetic population structure in Escherichia coli and Shigella. J. Gen. Microbiol. 129: 2715– 2726.
71.
Ochoa, T. J.,, L. Ecker,, F. Barletta,, M. L. Mispireta,, A. I. Gil,, C. Contreras,, M. Molina,, I. Amemiya,, H. Verastegui,, E. R. Hall,, T. G. Cleary, and, C. F. Lanata. 2009. Age-related susceptibility to infection with diarrheagenic E. coli in infants from peri-urban areas of Lima, Peru. Clin. Infect. Dis. 49: 1694– 1702.
72.
Ocklitz, H. W.,, E. F. Schmidt, and, J. Bahr. 1957. Clinical comparison of specific intestinal infections in infants. Z. Kinderheilkd. 79: 290– 316. (In German.)
73.
Ogura, Y.,, T. Ooka,, A. Iguchi,, H. Toh,, M. Asadulghani,, K. Oshima,, T. Kodama,, H. Abe,, K. Nakayama,, K. Kurokawa,, T. Tobe,, M. Hattori, and, T. Hayashi. 2009. Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli. Proc. Natl. Acad. Sci. USA 106: 17939– 17944.
74.
Olarte, J.,, M. Ramos-Alvarez, and, E. Galindo. 1957. Isolation of Shigella, Salmonella & coli enteropathogens in rectal swabs of 802 cases of sporadic diarrhea. Bol. Med. Hosp. Infant. Mex. 14: 257– 262; English transl. 263– 268. (In Spanish.)
75.
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.
76.
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 enterohaemorrhagic Escherichia coli O157:H7. Nature 409: 529– 533.
77.
Pollock, K. G.,, M. E. Locking,, T. J. Beattie,, H. Maxwell,, I. Ramage,, D. Hughes,, J. Cowieson,, L. Allison,, M. Hanson, and, J. M. Cowden. 2010. Sorbitol-fermenting Escherichia coli O157, Scotland. Emerg. Infect. Dis. 16: 881– 882.
78.
Quilligan, J. J., Jr.,, M. Biddle,, J. W. Dedrick,, M. L. Scott, and, I. Burnett. 1957. Recovery of enteropathogenic types of Escherichia coli from infants with diarrhea. AMA J. Dis. Child. 93: 420– 424.
79.
Quilligan, J. J., Jr.,, and S. Shadomy. 1958. Enteropathogenic Escherichia coli diarrhea. AMA J. Dis. Child. 95: 134– 138.
80.
Reid, S. D.,, C. J. Herbelin,, A. C. Bumbaugh,, R. K. Selander, and, T. S. Whittam. 2000. Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406: 64– 67.
81.
Riley, L. W.,, R. S. Remis,, S. D. Helgerson,, H. B. McGee,, J. G. Wells,, B. R. Davis,, R. J. Hebert,, E. S. Olcott,, L. M. Johnson,, N. T. Hargrett,, P. A. Blake, and, M. L. Cohen. 1983. Hemorrhagic colitis associated with a rare Escherichia coli serotype. N. Engl. J. Med. 308: 681– 685.
82.
Riordan, J. T.,, S. B. Viswanath,, S. D. Manning, and, T. S. Whittam. 2008. Genetic differentiation of Escherichia coli O157:H7 clades associated with human disease by real-time PCR. J. Clin. Microbiol. 46: 2070– 2073.
83.
Robins-Browne, R. M. 1987. Traditional enteropathogenic Escherichia coli of infantile diarrhea. Rev. Infect. Dis. 9: 28– 53.
84.
Rodrigues, J.,, I. C. Scaletsky,, L. C. Campos,, T. A. Gomes,, T. S. Whittam, and, L. R. Trabulsi. 1996. Clonal structure and virulence factors in strains of Escherichia coli of the classic serogroup O55. Infect. Immun. 64: 2680– 2686.
85.
Rothbaum, R. J.,, R. A. Giannella, and, J. C. Partin. 1982. Diarrhea caused by adherent enteropathogenic E. coli. J. Pediatr. 101: 486.
86.
Samadpour, M.,, J. E. Ongerth,, J. Liston,, N. Tran,, D. Nguyen,, T. S. Whittam,, R. A. Wilson, and, P. I. Tarr. 1994. Occurrence of Shiga-like toxin-producing Escherichia coli in retail fresh seafood, beef, lamb, pork, and poultry from grocery stores in Seattle, Washington. Appl. Environ. Microbiol. 60: 1038– 1040.
87.
Shaikh, N.,, N. J. Holt,, J. R. Johnson, and, P. I. Tarr. 2007. Fim operon variation in the emergence of enterohemorrhagic Escherichia coli: an evolutionary and functional analysis. FEMS Microbiol. Lett. 273: 58– 63.
88.
Shaikh, N.,, and P. I. Tarr. 2003. Escherichia coli O157:H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. J. Bacteriol. 185: 3596– 3605.
89.
Shulman, S. T.,, H. C. Friedmann, and, R. H. Sims. 2007. Theodor Escherich: the first pediatric infectious diseases physician? Clin. Infect. Dis. 45: 1025– 1029.
90.
Steele, B. T.,, N. Murphy,, G. S. Arbus, and, C. P. Rance. 1982. An outbreak of hemolytic uremic syndrome associated with ingestion of fresh apple juice. J. Pediatr. 101: 963– 965.
91.
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.
92.
Tarr, C. L.,, A. M. Nelson,, L. Beutin,, K. E. Olsen, and, T. S. Whittam. 2008. Molecular characterization reveals similar virulence gene content in unrelated clonal groups of Escherichia coli of serogroup O174 (OX3). J. Bacteriol. 190: 1344– 1349.
93.
Tarr, P. I.,, C. R. Clausen,, T. S. Whittam, and, R. A. Wilson. 1998. Antibiotic resistance and O antigen expression in Escherichia coli. J. Infect. Dis. 177: 1774– 1775.
94.
Tarr, P. I.,, M. A. Neill,, C. R. Clausen,, J. W. Newland,, R. J. Neill, and, S. L. Moseley. 1989. Genotypic variation in pathogenic Escherichia coli O157:H7 isolated from patients in Washington, 1984–1987. J. Infect. Dis. 159: 344– 347.
95.
Tarr, P. I.,, M. A. Neill,, C. R. Clausen,, S. L. Watkins,, D. L. Christie, and, R. O. Hickman. 1990. Escherichia coli O157:H7 and the hemolytic uremic syndrome: importance of early cultures in establishing the etiology. J. Infect. Dis. 162: 553– 556.
96.
Tarr, P. I.,, L. M. Schoening,, Y.-L. Yea,, T. R. Ward,, S. Jelacic, and, T. S. Whittam. 2000. Acquisition of the rfb-gnd cluster in evolution of Escherichia coli O55 and O157. J. Bacteriol. 182: 6183– 6191.
97.
Thomas, M. E.,, and R. E. Charter. 1956. Aetiology of juvenile diarrhoea; laboratory investigation of specimens referred from general practices in North-East London. Br. Med. J. 2: 339– 341.
98.
Vanaja, S. K.,, A. C. Springman,, T. E. Besser,, T. S. Whittam, and, S. D. Manning. 2010. Differential expression of virulence and stress fitness genes between Escherichia coli O157:H7 strains with clinical or bovine-biased genotypes. Appl. Environ. Microbiol. 76: 60– 68.
99.
Varela, G. A.,, A. Aguirre, and, J. Carrillo. 1946. E. coli—gomes, nueva especie aislada de un caso mortal de diarrea. Bol. Med. Hosp. Infant. Mex. 3: 623– 627.
100.
Werber, D.,, S. C. Behnke,, A. Fruth,, R. Merle,, S. Menzler,, S. Glaser,, L. Kreien-brock,, R. Prager,, H. Tschäpe,, P. Roggentin,, J. Bockemühl, and, A. Ammon. 2007. Shiga toxin-producing Escherichia coli infection in Germany: different risk factors for different age groups. Am. J. Epidemiol. 165: 425– 434.
101.
Whittam, T. S. 1998. Evolution of Escherichia coli O157:H7 and other Shiga toxin-producing E. coli strains, p. 195–209. In J. B. Kaper and, A. D. O’Brien (ed.), Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli Strains. ASM Press, Washington, DC.
102.
Whittam, T. S. 1995. Genetic population structure and pathogenicity in enteric bacteria, p. 217–245. In S. Baumberg,, J. P. W. Young,, E. M. H. Wellington, and, J. R. Saunders (ed.), Population Genetics of Bacteria. Cambridge University Press, Cambridge, United Kingdom.
103.
Whittam, T. S.,, and S. E. Ake. 1993. Genetic polymorphisms and recombination in natural populations of Escherichia coli, p. 223–245. In N. Takahata and, A. G. Clark (ed.), Mechanisms of Molecular Evolution. Sinauer Associates, Sunderland, MA.
104.
Whittam, T. S.,, and E. A. McGraw. 1996. Clonal analysis of EPEC serogroups. Rev. Microbiol. 27: 7– 16.
105.
Whittam, T. S.,, H. Ochman, and, R. K. Selander. 1983. Multilocus genetic structure in natural populations of Escherichia coli. Proc. Natl. Acad. Sci. USA 80: 1751– 1755.
106.
Whittam, T. S.,, I. K. Wachsmuth, and, R. A. Wilson. 1988. Genetic evidence of clonal descent of Escherichia coli O157:H7 associated with hemorrhagic colitis and hemolytic uremic syndrome. J. Infect. Dis. 157: 1124– 1133.
107.
Whittam, T. S.,, and R. A. Wilson. 1988. Genetic relationships among pathogenic Escherichia coli of serogroup O157. Infect. Immun. 56: 2467– 2473.
108.
Whittam, T. S.,, M. L. Wolfe,, I. K. Wachsmuth,, F. Ørskov,, I. Ørskov, and, R. A. Wilson. 1993. Clonal relationships among Escherichia coli strains that cause hemorrhagic colitis and infantile diarrhea. Infect. Immun. 61: 1619– 1629.
109.
Whittam, T. S.,, I. K. Wachsmuth, and, R. A. Wilson. 1987. Clonal nature of O157: H7 Escherichia coli associated with outbreaks of hemorrhagic colitis, abstr. GEN-1. In Abstracts of the 1st International Symposium and Workshop on Verocytotoxin (Shiga-like Toxin)-Producing Escherichia coli ( VTEC) Infections.
110.
Wisnia, S.,, and D. Schlossberg. 1997. Wit and Wisdom of Baseball. Publications International Limited, Lincolnwood, IL.