1887

Chapter 13 : Molecular Typing Methods for Analysis of Extraintestinal Pathogenic

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

Preview this chapter:
Zoom in
Zoomout

Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555816834/9781555814977_Chap13-1.gif /docserver/preview/fulltext/10.1128/9781555816834/9781555814977_Chap13-2.gif

Abstract:

, although perhaps best known as a cause of diarrheal disease, is actually responsible for more morbidity, mortality, and increased health care costs in the developed world as an extraintestinal pathogen. Two main categories of typing methods are relevant for studies involving extraintestinal pathogenic (ExPEC), including methods that define the strain’s phylogenetic and clonal background (at varying levels of resolution) and those that detect virulence-associated accessory traits. Alternative methods for resolving phylogenetic relationships at the clonal group level that are simpler and cheaper than multilocus sequence typing (MLST) include PCR-based genomic profiling methods, e.g., random amplified polymorphic DNA (RAPD) analysis and repetitive-element (REP) PCR, as performed using the ERIC, BOX, or REP primers. Methods for molecular typing of ExPEC find application in various kinds of studies, including between-population comparisons, assessments of individual isolates for their virulence potential or clonal similarity to other individual isolates, and assessments of colonization and transmission dynamics. The approaches used for statistical analysis of molecular typing data are an important consideration in population level studies involving ExPEC. Molecular typing of ExPEC for phylogenetic and clonal background, as well as accessory traits (e.g., virulence factors) can lead to important new insights into the origins, reservoirs, clinical and commensal behavior, and host group associations of this important group of . Attention to study design, population selection, specific molecular methods, and appropriate statistical analysis approaches can enhance the quality of typing studies involving ExPEC, which may lead to improvements in human or animal health.

Citation: Johnson J. 2011. Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , p 213-227. In Persing D, Tenover F, Tang Y, Nolte F, Hayden R, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555816834.ch13

Key Concept Ranking

Random Amplified Polymorphic DNA
0.46025586
0.46025586
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Phylogenetic distribution of extraintestinal virulence-associated traits in The dendrogram depicts phylogenetic relationships for the 72 members of the Reference collection, as inferred based on multilocus enzyme electrophoresis. The four major phylogenetic groups (A, B1, B2, and D) and the nonaligned strains (“non”) are bracketed and labeled. Bullets on the right indicate the presence of putative virulence genes P fimbriae; group II capsule synthesis; S and F1C fimbriae; aerobactin system; serum resistance; and type 1 fimbriae). Horizontal bars at right indicate the 10 ECOR strains isolated from humans with symptomatic urinary tract infection (UTI). The remaining strains, except for one asymptomatic bacteriuria isolate, are fecal isolates from healthy human or animal hosts. Note the concentration of (chromosomal) virulence genes and within phylogenetic groups B2 and D but their occasional joint appearance also in distant lineages, consistent with coordinate horizontal transfer. The more scattered phylogenetic distribution of is consistent with this gene’s typically plasmid location, whereas is nearly universally prevalent. Note also the concentration of UTI isolates within phylogenetic groups B2 and D and the association of virulence genes with UTI isolates. Reprinted from reference with permission.

Citation: Johnson J. 2011. Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , p 213-227. In Persing D, Tenover F, Tang Y, Nolte F, Hayden R, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555816834.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Phylogenetic relationships among 44 isolates as inferred by maximum parsimony from sequence analysis of eight housekeeping genes. A 50% consensus majority rule tree is shown. Bootstrap values (from 1,000 iterations) are shown where they are >50%. The data set, which contained a total of 3,865 characters, was not edited for recombination. ExPEC strains are identified by a bullet. Major clades are labeled as to Reference (EC) group (including “N” for nonaligned strains, e.g., EC37), based on their constituent EC strains, with group D split into two subgroups (D′ and D′). Individual clonal groups are labeled by characteristic O:K:H serotypes. Adapted (with permission) from reference .

Citation: Johnson J. 2011. Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , p 213-227. In Persing D, Tenover F, Tang Y, Nolte F, Hayden R, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555816834.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

RAPD analysis of strains 536, NU14, and RS218. RAPD profiles as generated using primer 1247 ( ) show O18:K1:H7 strains NU14 (cystitis, lane 3) and RS218 (neonatal meningitis, lane 4) to be indistinguishable from one another, but distinct from strain 536 (O6:K15:H31; pyelonephritis, lane 2). M (lanes 1 and 5), 100-bp marker. Reprinted from reference , with permission.

Citation: Johnson J. 2011. Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , p 213-227. In Persing D, Tenover F, Tang Y, Nolte F, Hayden R, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555816834.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

PFGE or RAPD profiles of 27 unique fecal isolates from an eight-member household. Isolates are all unique by host and clone (strain). The dendrogram is based on Dice similarity coefficients among the individual RAPD profiles (top four lanes; these four isolates were refractory to PFGE analysis) or XbaI PFGE profiles (other lanes). The vertical dashed line indicates the 94% similarity level. Boxes ( = 7) encompass isolates from different hosts that represent the same RAPD type (≥82% profile similarity) or PFGE type (≥94% profile similarity), i.e., are shared strains. The eight hosts include two adults (index subject and other adult), two children, and four pets. Children and pets are numbered sequentially within their category. The seven shared clones (and the respective host types involved in strain sharing) are R344 (child-adult), R342 (adult-adult), 360 (adult-child), 065 (pet-pet), 202 (pet-pet), 204 (pet-child), and 201 (pet-pet). Reprinted from reference with permission.

Citation: Johnson J. 2011. Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , p 213-227. In Persing D, Tenover F, Tang Y, Nolte F, Hayden R, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555816834.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5
FIGURE 5

Detection of virulence genes by multiplex PCR. Each primer pool contains six primer pairs directed toward different putative or proven virulence genes associated with extraintestinal pathogenic (ExPEC). + and –, positive-control and negative-control target DNA pools, respectively. M, 100-bp ladder. PCR products are labeled as to target sequence. PAI, pathogenicity island marker Different primer pairs are used to detect multiple regions or variants within the (P fimbriae), (group 2 and 3 capsule), and (S and F1C fimbriae) operons. Primer pairs for I and II, III (in pool 5) comprise flanking primers that amplify across the entire region, separately for allele I versus alleles II and III (which have homologous flanking regions). Allele-specific internal primers (in pools 2, 3, and 4) provide confirmatory detection of each variant. Reprinted from reference with permission.

Citation: Johnson J. 2011. Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , p 213-227. In Persing D, Tenover F, Tang Y, Nolte F, Hayden R, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555816834.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 6
FIGURE 6

PCR analysis of (P fimbriae) operon. Open boxes represent genes within the operon (including structural subunit; usher; minor tip pilins; and adhesin). Forward and reverse primers (right- and left-pointing black triangles, respectively, above and below the operon) are used in combinations as shown to yield the indicated PCR products (thin rectangles, below operon). Heavy-striped rectangles, and allele PCR products. Solid black rectangles, gene PCR products. Fine-striped rectangles, long PCR operon fragments (as generated using either flanking or internal allele-specific reverse primers, as illustrated for allele I-I′). Reprinted from reference with permission.

Citation: Johnson J. 2011. Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , p 213-227. In Persing D, Tenover F, Tang Y, Nolte F, Hayden R, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555816834.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 7
FIGURE 7

Distribution of 243 ExPEC isolates from human feces and poultry products on the axis 1-axis 2 plane, by principal coordinates analysis. Data included extended virulence genotypes (60 traits) and phylogenetic groups (A, B1, B2, and D). The axes have no units; they reflect the total score for each isolate, as derived by summing the isolate’s partial score for each variable (which is the product of the loading score assigned to the particular variable for a given axis and the isolate’s status for that variable). Axis 1 (positive values to the right and negative values to the left of the solid vertical line) accounted for 37% of total variance and showed significant differences between human susceptible isolates and each of the other groups. Axis 2 (positive values above and negative values below the dashed horizontal line) accounted for 20% of total variance and did not show any significant between-group differences. Resistant, resistant to trimethoprim-sulfamethoxazole, nalidixic acid (quinolones), and/or ceftriaxone or ceftazidime (extended-spectrum cephalosporins). Susceptible, susceptible to all these agents (regardless of other possible resistances). Upper panel, human isolates. Lower panel, poultry isolates. Group symbols: filled circles, resistant isolates; open circles, susceptible isolates. Adapted from reference with permission.

Citation: Johnson J. 2011. Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , p 213-227. In Persing D, Tenover F, Tang Y, Nolte F, Hayden R, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555816834.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 8
FIGURE 8

RAPD and PFGE profiles of isolates from humans and poultry. Three pairs of poultry resistant (PR) and human resistant (HR) isolates, with identical virulence profiles, exhibited >82% within-pair similarity according to composite RAPD profiles, as generated using primers 1254 and 1290. PFGE analysis with XbaI showed a three-band difference between isolates 28 (PR) and 49 (HR) (middle pair; lanes 5 and 6). M, marker (for RAPD gels, 250-bp ladder; for PFGE, O157:H7). Lane numbers are shown below gel image. Strain identifiers and source/resistance group are shown above gel image. Reproduced (with permission) from reference .

Citation: Johnson J. 2011. Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , p 213-227. In Persing D, Tenover F, Tang Y, Nolte F, Hayden R, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555816834.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 9
FIGURE 9

Distribution of virulence factor scores by source and resistance status among 243 ExPEC isolates from human feces and poultry products. Resistant, resistant to trimethoprim-sulfamethoxazole, nalidixic acid (quinolones), and/or ceftriaxone or ceftazidime (extended-spectrum cephalosporins). Susceptible, susceptible to all these agents (regardless of other possible resistances). The virulence scores of the human susceptible isolates are, on average, approximately 4 points greater than those of the human resistant or poultry isolates. Adapted (with permission) from reference .

Citation: Johnson J. 2011. Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , p 213-227. In Persing D, Tenover F, Tang Y, Nolte F, Hayden R, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555816834.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 10
FIGURE 10

Dendrogram based on extended virulence profiles of 243 ExPEC isolates from human feces and poultry products. The dendrogram (shown here in simplified form) was constructed by the unweighted pair group method using average linkages based on pairwise similarity relationships according to the aggregate presence or absence of 60 individual virulence genes plus phylogenetic group (A, B1, B2, and D). Triangles indicate arborizing subclusters. Major clusters 1, 2, and 3 and subclusters 1a, 1b, 2a, 2b, 3a, and 3b are so labeled. Boxes to the right of the dendrogram depict the distribution (by source group) of constituent members of each subcluster. Resistant, resistant to trimethoprim-sulfamethoxazole, nalidixic acid (quinolones), and/or ceftriaxone or ceftazidime (extended-spectrum cephalosporins). Susceptible, susceptible to all these agents (regardless of other possible resistances). Adapted (with permission) from reference .

Citation: Johnson J. 2011. Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , p 213-227. In Persing D, Tenover F, Tang Y, Nolte F, Hayden R, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555816834.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 11
FIGURE 11

Similarity relationships among 130 isolates of serogroup O6 from humans (H), dogs (D), and cats (C) according to extended virulence profiles. Black triangles represent arborizing clusters, which are numbered sequentially as 1 through 7. Only two isolates did not fall within one of the clusters (not shown). Host species code (H, D, or C) and sequence type (ST) ( , 625, or 127) for each isolate are indicated in columns to the right of the dendrogram. The positions of reference strains 536 (O6:K15:H31) and CFT073 (O6:K2:H1) in the dendrogram are indicated. Reprinted from reference , with permission.

Citation: Johnson J. 2011. Molecular Typing Methods for Analysis of Extraintestinal Pathogenic , p 213-227. In Persing D, Tenover F, Tang Y, Nolte F, Hayden R, van Belkum A (ed), Molecular Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555816834.ch13
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555816834.ch13
1. Berg, D. E.,, N. S. Akopyants, and, D. Kersulyte. 1994. Fingerprinting microbial genomes using the RAPD or AP-PCR method. Methods Mol. Cell. Biol. 5:1324.
2. Bidet, P.,, A. Metais,, F. Mahjoub-Messai,, L. Durand,, M. Dehem,, Y. Aujard,, E. Bingen,, X. Nassif, and, S. Bonacorsi. 2007. Detection and identification by PCR of a highly virulent phylogenetic subgroup among extraintestinal pathogenic Escherichia coli B2 strains. Appl. Environ. Microbiol. 73:23732377.
3. Bingen-Bidois, M.,, M. Terki,, D. Barraud,, S. Bonacorsi,, O. Clermont,, N. Brahimi,, C. Loukil, and, E. Bingen. 2002. Escherichia coli pathogenicity island-like domains. Infect. Immun. 70:32163226.
4. Clermont, O.,, S. Bonacorsi, and, E. Bingen. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66:45554558.
5. Clermont, O.,, J. R. Johnson,, M. Menard, and, E. Denamur. 2007. Determination of Escherichia coli O types by allele-specific polymerase chain reaction: application to the O types involved in human septicemia. Diagn. Microbiol. Infect. Dis. 57:129136.
6. Foxman, B.,, S. D. Manning,, P. Tallman,, R. Bauer,, L. Zhang,, J. S. Koopman,, B. Gillespie,, J. D. Sobel, and, C. F. Marrs. 2002. Uropathogenic Escherichia coli are more likely than commensal E. coli to be shared between heterosexual sex partners. Am. J. Epidemiol. 156:11331140.
7. Foxman, B.,, L. Zhang,, P. Tallman,, B. C. Andree,, A. M. Geiger,, J. S. Koopman,, B. W. Gillespie,, K. A. Palin,, J. D. Sobel,, C. K. Rode,, C. A. Bloch, and, C. F. Marrs. 1996. Transmission of uropathogens between sex partners. J. Infect. Dis. 175:989992.
8. Gordon, D. M.,, O. Clermont,, H. Tolley, and, E. Denamur. 2008. Assigning Escherichia coli strains to phylogenetic groups: multi-locus sequence typing versus the PCR triplex method. Environ. Microbiol. 10:24842496.
9. Herzer, P. J.,, S. Inouye,, M. Inouye, and, T. S. Whittam. 1990. Phylogenetic distribution of branched RNS-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J. Bacteriol. 172:61756181.
10. Johnson, J. R. 2000. Development of polymerase chain reaction-based assays for bacterial gene detection. J. Microbiol. Methods 41:201209.
11. Johnson, J. R.,, and J. J. Brown. 1996. A novel multiplyprimed polymerase chain reaction assay for identification of variant papG genes encoding the Gal(α1-4)Gal-binding PapG adhesins of Escherichia coli. J. Infect. Dis. 173:920926.
12. Johnson, J. R.,, J. J. Brown,, U. B. Carlino, and, T. A. Russo. 1998. Colonization with and acquisition of uropathogenic Escherichia coli strains as revealed by polymerase chain reaction-based detection. J. Infect. Dis. 177:11201124.
13. Johnson, J. R.,, and C. Clabots. 2006. Sharing of virulent Escherichia coli clones among household members of a woman with acute cystitis. Clin. Infect. Dis. 43:e101e108.
14. Johnson, J. R.,, O. Clermont,, M. Menard,, M. A. Kuskowski,, B. Picard, and, E. Denamur. 2006. Experimental mouse lethality of Escherichia coli isolates, in relation to accessory traits, phylogenetic group, and ecological source. J. Infect. Dis. 194:11411150.
15. Johnson, J. R.,, P. Delavari,, M. Kuskowski, and, A. L. Stell. 2001. Phylogenetic distribution of extraintestinal virulence-associated traits in Escherichia coli. J. Infect. Dis. 183:7888.
16. Johnson, J. R.,, P. Delavari,, T. T. O’Bryan,, K. Smith, and, S. Tatini. 2005. Contamination of retail foods, particularly turkey, from community markets (Minnesota, 1999-2000) with antimicrobial-resistant and extraintestinal pathogenic Escherichia coli. Foodborne Pathog. Dis. 2:3849.
17. Johnson, J. R.,, P. Delavari, and, T. O’Bryan. 2001. Escherichia coli O18:K1:H7 isolates from acute cystitis and neonatal meningitis exhibit common phylogenetic origins and virulence factor profiles. J. Infect. Dis. 183:425434.
18. Johnson, J. R.,, A. Gajewski,, A. J. Lesse, and, T. A. Russo. 2003. Extraintestinal pathogenic Escherichia coli as a cause of invasive non-urinary infections. J. Clin. Microbiol. 41:57985802.
19. Johnson, J. R.,, B. Johnston,, C. R. Clabots,, M. A. Kuskowski,, E. Roberts, and, C. DebRoy. 2008. Virulence genotypes and phylogenetic background of Escherichia coli serogroup O6 isolates from humans, dogs, and cats. J. Clin. Microbiol. 46:417422.
20. Johnson, J. R.,, N. Kaster,, M. A. Kuskowski, and, G. V. Ling. 2003. Identification of urovirulence traits in Escherichia coli by comparison of urinary and rectal E. coli isolates from dogs with urinary tract infection. J. Clin. Microbiol. 41:337345.
21. Johnson, J. R.,, M. A. Kuskowski,, A. Gajewski,, D. F. Sahm, and, J. A. Karlowsky. 2004. Virulence characteristics and phylogenetic background of multidrug-resistant and antimicrobial-susceptible clinical isolates of Escherichia coli from across the United States, 2000-2001. J. Infect. Dis. 190:17391744.
22. Johnson, J. R.,, M. A. Kuskowski,, M. Menard,, A. Gajewski,, M. Xercavins, and, J. Garau. 2006. Similarity of human and chicken-source Escherichia coli isolates in relation to ciprofloxacin resistance status. J. Infect. Dis. 194:7178.
23. Johnson, J. R.,, M. A. Kuskowski,, T. T. O’Bryan,, R. Colodner, and, R. Raz. 2005. Virulence genotype and phylogenetic origin in relation to antibiotic resistance profile among Escherichia coli urine sample isolates from Israeli women with acute uncomplicated cystitis. Antimicrob. Agents Chemother. 46:2631.
24. Johnson, J. R.,, M. A. Kuskowski,, T. T. O’Bryan, and, J. N. Maslow. 2002. Epidemiological correlates of virulence genotype and phylogenetic background among Escherichia coli blood isolates from adults with diverse source bacteremia. J. Infect. Dis. 10:14391447.
25. Johnson, J. R.,, M. A. Kuskowski,, K. Owens,, A. Gajewski, and, P. L. Winokur. 2003. Phylogenetic origin and virulence genotype in relation to resistance to fluoroquinolones and/or extended spectrum cephalosporins and cephamycins among Escherichia coli isolates from animals and humans. J. Infect. Dis. 188:759768.
26. Johnson, J. R.,, M. A. Kuskowski,, K. Owens,, S. Soto,, J. P. Horcajada,, M. T. Jimenez de Anta, and, J. Vila. 2005. Extended virulence genotypes of Escherichia coli isolates from patients with cystitis, pyelonephritis, or prostatitis. J. Infect. Dis. 191:4650.
27. Johnson, J. R.,, M. A. Kuskowski,, K. Smith,, T. T. O’Bryan, and, S. Tatini. 2005. Antimicrobial-resistant and extraintestinal pathogenic Escherichia coli in retail foods. J. Infect. Dis. 191:10401049.
28. Johnson, J. R.,, A. R. Manges,, T. T. O’Bryan, and, L. R. Riley. 2002. A disseminated multi-drug resistant clonal group of extraintestinal pathogenic Escherichia coli as a cause of pyelonephritis. Lancet 359:22492251.
29. Johnson, J. R.,, A. C. Murray,, A. Gajewski,, M. Sullivan,, P. Snippes,, M. A. Kuskowski, and, K. E. Smith. 2003. Isolation and molecular characterization of nalidixic acidresistant extraintestinal pathogenic Escherichia coli from retail chicken products. Antimicrob. Agents Chemother. 47:21612168.
30. Johnson, J. R.,, A. C. Murray,, M. A. Kuskowski,, S. Schubert,, M.-F. Prere,, B. Picard,, R. Colodner,, R. Raz, and Trans-Global Initiative for Antimicrobial Resistance Analysis (TIARA) Investigators. 2005. Distribution and characteristics of Escherichia coli clonal group A. Emerg. Infect. Dis. 11:141145.
31. Johnson, J. R.,, and T. T. O’Bryan. 2004. Detection of the Escherichia coli group 2 polysaccharide capsule synthesis gene kpsM by a rapid and specific PCR-based assay. J. Clin. Microbiol. 42:17731776.
32. Johnson, J. R.,, and T. T. O’Bryan. 2000. Improved repetitive element PCR fingerprinting for resolving pathogenic and nonpathogenic phylogenetic groups within Escherichia coli. Clin. Diagn. Lab. Immunol. 7:265273.
33. Johnson, J. R.,, T. T. O’Bryan,, M. A. Kuskowski, and, J. N. Maslow. 2001. Ongoing horizontal and vertical transmission of virulence genes and papA alleles among Escherichia coli blood isolates from patients with diversesource bacteremia. Infect. Immun. 69:53635374.
34. Johnson, J. R.,, Owens,, A. Manges, and, L. Riley. 2004. Rapid and specific detection of Escherichia coli clonal group A by gene-specific PCR. J. Clin. Microbiol. 42:26182622.
35. Johnson, J. R.,, K. Owens,, A. Gajewski, and, C. Clabots. 2008. Escherichia coli colonization patterns among human household members and pets, with attention to acute urinary tract infection. J. Infect. Dis. 197:218–224.
36. Johnson, J. R.,, K. Owens,, A. Gajewski, and, M. A. Kuskowski. 2005. Bacterial characteristics in relation to clinical source among Escherichia coli isolates from women with acute cystitis or pyelonephritis and uninfected women. J. Clin. Microbiol. 43:60646072.
37. Johnson, J. R.,, K. Owens,, T. T. O’Bryan,, M. Sabate, and, G. Prats. 2004. Rapid and specific detection of the O15:K52:H1 clonal group of Escherichia coli by gene-specific PCR. J. Clin. Microbiol. 42:38413843.
38. Johnson, J. R.,, K. L. Owens,, C. R. Clabots,, S. J. Weissman, and, S. B. Cannon. 2006. Phylogenetic relationships among clonal groups of extraintestinal pathogenic Escherichia coli as assessed by multi-locus sequence analysis. Microbes Infect. 8:17021713.
39. Johnson, J. R.,, and T. A. Russo. 2002. Extraintestinal pathogenic Escherichia coli (ExPEC): the “other bad E. coli”. J. Lab. Clin. Med. 139:155162.
40. Johnson, J. R.,, and T. A. Russo. 2004. Chapter 8.6.1.4, Molecular epidemiology of extraintestinal pathogenic Escherichia coli. In R. Curtiss III et al. (ed.), EcoSal: Escherichia coli and Salmonella: Cellular and Molecular Biology, American Society for Microbiology, Washington, DC. http://www.ecosal.org.
41. Johnson, J. R.,, M. R. Sannes,, C. Croy,, B. Johnston,, C. Clabots,, M. A. Kuskowski,, J. Bender,, K. E. Smith,, P. L. Winokur, and, E. A. Belongia. 2007. Antimicrobial drug-resistant Escherichia coli isolates from humans and poultry products, Minnesota and Wisconsin, 2002-2004. Emerg. Infect. Dis. 13:838846.
42. Johnson, J. R.,, F. Scheutz,, F. Ulleryd,, M. Kuskowski,, T. T. O’Bryan, and, T. Sandberg. 2005. Phylogenetic and pathotypic comparison of concurrent urine and rectal Escherichia coli isolates from men with febrile urinary tract infection. J. Clin. Microbiol. 43:38953900.
43. Johnson, J. R.,, F. Scheutz,, P. Ulleryd,, M. A. Kuskowski,, T. T. O’Bryan, and, T. Sandberg. 2005. Host-pathogen relationships among Escherichia coli isolates from men with febrile urinary tract infection. Clin. Infect. Dis. 40:813822.
44. Johnson, J. R.,, A. E. Stapleton,, T. A. Russo,, F. S. Scheutz,, J. J. Brown, and, J. N. Maslow. 1997. Characteristics and prevalence within serogroup O4 of a “J96-like” clonal group of uropathogenic Escherichia coli O4:H5 containing the “Class I” and “Class III” alleles of papG. Infect. Immun. 65:21532159.
45. Johnson, J. R.,, and A. L. Stell. 2000. Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J. Infect. Dis. 181:261272.
46. Johnson, J. R.,, A. L. Stell,, P. Delavari,, A. C. Murray,, M. Kuskowski, and, W. Gaastra. 2001. Phylogenetic and pathotypic similarities between Escherichia coli isolates from urinary tract infections in dogs and extraintestinal infections in humans. J. Infect. Dis. 183:897906.
47. Johnson, J. R.,, A. L. Stell,, N. Kaster,, C. Fasching, and, T. T. O’Bryan. 2001. Novel molecular variants of allele I of the Escherichia coli P fimbrial adhesin gene papG. Infect. Immun. 69:23182327.
48. Johnson, J. R.,, A. L. Stell,, T. T. O’Bryan,, M. Kuskowski,, B. Nowicki,, C. Johnson,, J. M. Maslow,, A. Kaul,, J. Kavle, and, G. Prats. 2002. Global molecular epidemiology of the O15:K52:H1 extraintestinal pathogenic Escherichia coli clonal group: evidence of distribution beyond Europe. J. Clin. Microbiol. 40:19131923.
49. Johnson, J. R.,, A. L. Stell,, F. Scheutz,, T. T. O’Bryan,, T. A. Russo,, U. B. Carlino,, C. C. Fasching,, J. Kavle,, L. van Dijk, and, W. Gaastra. 2000. Analysis of F antigen-specific papA alleles of extraintestinal pathogenic Escherichia coli using a novel multiplex PCR-based assay. Infect. Immun. 68:15871599.
50. Johnson, J. R.,, S. J. Weissman,, A. L. Stell,, E. Tritchina,, D. E. Dykhuizen, and, E. V. Sokurenko. 2001. Clonal and pathotypic analysis of archetypal Escherichia coli cystitis isolate NU14. J. Infect. Dis. 184:15561565.
51. Kruskal, J. B.,, and M. Wish. 1978. Multidimensional Scaling. Sage Publications, Beverly Hills, CA.
52. Le Gall, T.,, O. Clermont,, S. Gouriou,, B. Picard,, X. Nassif,, E. Denamur, and, O. Tenaillon. 2007. Extraintestinal virulence is a coincidental by-product of commensalism in B2 phylogenetic group Escherichia coli strains. Mol. Biol. Evol. 24:23732384.
53. Lin, J.-J.,, J. Kuo, and, J. Ma. 1996. A PCR-based DNA fingerprinting technique: AFLP for molecular typing of bacteria. Nucleic Acids Res. 24:36493650.
54. Lloyd, A. L.,, D. A. Rasko, and, H. L. Mobley. 2007. Defining genomic islands and uropathogen-specific genes in uropathogenic Escherichia coli. J. Bacteriol. 189:35323546.
55. Madico, G.,, N. S. Akopyants, and, D. E. Berg. 1995. Arbitrarily primed PCR DNA fingerprinting of Escherichia coli O157:H7 strains by using templates from boiled cultures. J. Clin. Microbiol. 33:15341536.
56. Manges, A. R.,, J. R. Johnson,, B. Foxman,, T. T. O’Bryan,, K. E. 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. 345:10071013.
57. Manges, A. R.,, J. R. Johnson, and, L. W. Riley. 2004. Intestinal population dynamics of urinary tract infectioncausing Escherichia coli within heterosexual couples. Curr. Issues Intest. Microbiol. 5:4957.
58. Moreno, E.,, A. Andreu,, T. Perez,, M. Sabate,, J. R. Johnson, and, G. Prats. 2006. Relationship between Escherichia coli strains causing urinary tract infection in women and the dominant faecal flora of the same hosts. Epidemiol. Infect. 134:10151023.
59. Moreno, E.,, A. Andreu,, C. Pigrau,, M. A. Kuskowski,, J. R. Johnson, and, G. Prats. 2008. Relationship between Escherichia coli strains causing acute cystitis in women and the fecal E. coli population of the host. J. Clin. Microbiol. 46:25292534.
60. Moreno, E.,, G. Prats,, M. Sabate,, T. Perez,, J. R. Johnson, and, A. Andreu. 2006. Quinolone, fluoroquinolone and trimethoprim/sulfamethoxazole resistance in relation to virulence determinants and phylogenetic background among uropathogenic Escherichia coli. J. Antimicrob. Chemother. 57:204211.
61. Murray, A. C.,, M. A. Kuskowski, and, J. R. Johnson. 2004. Virulence factors predict Escherichia coli colonization patterns among human and animal household members. Ann. Intern. Med. 140:848849.
62. Nicolas-Chanoine, M. H.,, J. Blanco,, V. Leflon-Guibout,, R. Demarty,, M. P. Alonso,, M. M. Canica,, Y. J. Park,, J. P. Lavigne,, J. Pitout, and, J. R. Johnson. 2008. Intercontinental emergence of Escherichia coli clone O25:H4-ST131 producing CTX-M-15. J. Antimicrob. Chemother. 61:273281.
63. Noller, A. C.,, M. C. McEllistrem,, A. G. Pacheco,, D. J. Boxrud, and, L. H. Harrison. 2003. Multilocus variable-number tandem repeat analysis distinguishes outbreak and sporadic Escherichia coli O157:H7 isolates. J. Clin. Microbiol. 41:53895397.
64. Peakall, R.,, and P. E. Smouse. 2006. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6:288295.
65. Plos, K.,, T. Carter,, S. Hull,, R. Hull, and, C. Svanborg Edén. 1990. Frequency and organization of pap homologous DNA in relation to clinical origin of uropathogenic Escherichia coli. J. Infect. Dis. 161:518524.
66. Ribot, E. M.,, M. A. Fair,, R. Gautom,, D. N. Cameron,, S. B. Hunter,, B. Swaminathan, and, T. J. Barrett. 2006. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog. Dis. 3:5967.
67. Russo, T. A.,, and J. R. Johnson. 2000. A proposal for an inclusive designation for extraintestinal pathogenic Escherichia coli: ExPEC. J. Infect. Dis. 181:17531754.
68. Russo, T. A.,, and J. R. Johnson. 2003. Medical and economic impact of extraintestinal infections due to Escherichia coli: an overlooked epidemic. Microbes Infect. 5:449456.
69. Sannes, M. R.,, E. A. Belongia,, B. Kieke,, K. E. Smith,, A. Kieke,, M. Vandermause,, J. Bender,, C. Clabots,, P. L. Winokur, and, J. R. Johnson. 2008. Predictors of antimicrobial-resistant Escherichia coli in the feces of vegetarians and newly hospitalized adults in Minnesota and Wisconsin. J. Infect. Dis. 193:430434.
70. Sannes, M. R.,, M. A. Kuskowski,, K. Owens,, A. Gajewski, and, J. R. Johnson. 2004. Virulence factor profiles and phylogenetic background of Escherichia coli isolates from veterans with bacteremia and uninfected control subjects. J. Infect. Dis. 190:21212128.
71. Tartof, S. Y.,, O. D. Solberg,, A. R. Manges, and, L. W. Riley. 2005. Analysis of a uropathogenic Escherichia coli clonal group by multilocus sequence typing. J. Clin. Microbiol. 43:58605864.
72. van Belkum, A.,, D. C. Melles,, J. K. Peeters,, W. B. van Leeuwen,, E. van Duijkeren,, X. W. Huijsdens,, E. Spalburg,, A. J. de Neeling,, H. A. Verbrugh, and the Dutch Working Party on Surveillance and Research of MRSA-SOM. 2008. Methicillin-resistant and -susceptible Staphylococcus aureus sequence type 398 in pigs and humans. Emerg. Infect. Dis. 14:479483.
73. Versalovic, J.,, M. Schneid,, F. J. de Bruijn, and, J. R. Lupski. 1994. Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol. Cell. Biol. 5:2540.
74. Vila, J.,, K. Simon,, J. Ruiz,, J. P. Horcajada,, M. Velasco,, M. Barranco,, A. Moreno, and, J. Mensa. 2002. Are quinolone-resistant uropathogenic Escherichia coli less virulent? J. Infect. Dis. 186:10391042.
75. Weissman, S. J.,, V. Beskhlebnaya,, V. Chesnokova,, S. Chattopadhyay,, W. E. Stamm,, T. M. Hooton, and, E. V. Sokurenko. 2007. Differential stability and trade-off effects of pathoadaptive mutations in the Escherichia coli FimH adhesin. Infect. Immun. 75:35483555.
76. Wirth, T.,, D. Falush,, R. Lan,, F. Colles,, P. Mensa,, L. H. Wieler,, H. Karch,, P. R. Reeves,, M. C. J. Maiden,, H. Ochman, and, M. Achtman. 2006. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol. Microbiol. 60:11361151.
77. Woods, C. R.,, J. Versalovic,, T. Koeuth, and, J. Lupski. 1993. Whole-cell repetitive element sequence-based polymerase chain reaction allows rapid assessment of clonal relationships of bacterial isolates. J. Clin. Microbiol. 31:19271931.

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