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Sharing of Virulent Escherichia coli Clones among Household Members of a Woman with Acute Cystitis

  1. James R. Johnson and
  2. Connie Clabots
  1. Mucosal and Vaccine Research Center, Veterans Affairs Medical Center, and Department of Medicine, University of Minnesota, Minneapolis
  1. Reprints or correspondence: Dr. James R. Johnson, Infectious Diseases (111F), Minneapolis VAMC, 1 Veterans Dr., Minneapolis, MN 55417 (johns007{at}umn.edu).
 
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Abstract

Background. Within-household transmission of extraintestinal pathogenic Escherichia coli (ExPEC) may contribute to the pathogenesis of urinary tract infection (UTI), but this is poorly understood.

Methods. A woman with acute UTI, 4 human household members who cohabitated with her, and the family's pet dog underwent prospective longitudinal surveillance for colonizing E. coli for 7–9 weeks after the woman's UTI episode. Unique clones were resolved by random amplified polymorphic DNA and pulsed-field gel electrophoresis analysis. Virulence genes, phylogenetic group, and O types were defined by PCR. Comparisons with reference strains were made using random amplified polymorphic DNA profiling.

Results. Serial fecal and urine samples from the 6 household members yielded 7 unique E. coli clones (4 of which were ExPEC and 3 of which were non-ExPEC). For 3 clones, extensive among-host sharing was evident in patterns suggesting host-to-host transmission. The mother's UTI clone, which represented E. coli O1:K1:H7, was the clone that was most extensively shared (in 5 hosts, including the dog) and most frequently recovered (in 45% of samples and at all 3 time points). The other 3 ExPEC clones corresponded with E. coli O6:K2:H1, O1:K1:H7, and O2:F10,F48.

Conclusions. E. coli clones, including ExPEC, can be extensively shared among human and animal household members in the absence of sexual contact and in patterns suggesting host-to-host transmission.

Each year in the United States, acute uncomplicated urinary tract infection (UTI) affects millions of women and is responsible for billions of dollars in health care costs [1]. Most acute UTI episodes are caused by distinctive Escherichia coli strains termed “extraintestinal pathogenic E. coli” (ExPEC) [2, 3]. Although the immediate source of the causative ExPEC strains usually is the host's own fecal flora [4], the proximal sources of these pathogens are poorly understood.

Possible person-to-person transmission of ExPEC has received much recent attention, primarily in the context of suspected sexual transmission, based on instances in which both members of a sexually active couple have exhibited colonization and/or symptomatic infection with the same E. coli clone [5–13]. However, other evidence supports the occurrence of nonsexual within-household transmission of ExPEC [14–17], including transmission among siblings [16] and between humans and pets [17]. Additionally, the food supply may represent a vehicle for transmission of ExPEC and antimicrobial-resistant E. coli to consumers [18–20]; this could result in colonization of multiple household members with the same E. coli clone(s), thereby creating the false appearance of within-household transmission.

To assess for within-household transmission of E. coli clones—and of ExPEC in particular—in relation to acute UTI, we performed prospective longitudinal microbiological surveillance involving the 6 members (5 humans and a pet dog) of the household of a woman with acute, uncomplicated UTI. We used state-of-the-art molecular methods to resolve and characterize unique fecal and urine E. coli clones. We then compared observed colonization patterns with molecular characteristics and the reported patterns of host-to-host contact and dietary intake.

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Patients and Methods

Patients. Study subjects included a 50-year-old premenopausal women with acute UTI (the mother) and all 5 cohabiting household members, including the father (aged 49 years), 2 daughters (both aged 13 years), a son (aged 11 years), and the family dog. Informed consent was obtained from all human subjects or their parents (for minors). Data regarding within-household patterns of physical contact, other relevant behaviors, and dietary practices were reported retrospectively by the parents via questionnaire and interview; food diaries were not kept. Clinical research procedures were in accordance with the guidelines of the authors' institutions and the Helsinki declaration of 1975, as revised in 1983.

Samples. Microbiological examination of samples from subjects (feces and urine samples only) was performed largely as described elsewhere [12, 13, 17]. Samples were collected at the time of the mother's UTI episode and twice later (i.e., at 3 and 7–9 weeks), to provide 3 samplings in total. (Sampling intervals were selected for convenience, to provide the laboratory time to process the previous round of samples before another round was collected. The second sampling, intended for week 6, was slightly delayed because of logistical factors.) Urine samples (obtained from the mother only) were collected in sterile containers as clean-catch, midstream, voided specimens. Fecal samples were collected in clean plastic food storage bags immediately after defecation. Samples were refrigerated pending their transfer to the research laboratory within 72 h of collection. No sampling was done of food, water, fomites, or environmental surfaces.

Sample processing. A small portion of each fecal sample was streaked for isolation on eosin-methylene blue agar. Urine samples were cultured quantitatively on eosin-methylene blue agar. After overnight incubation at 37°C, up to 5 presumptive E. coli colonies (characteristic colony morphology, lactose positive), as available, were selected from each fecal or urine culture for further analysis, with preference given to any distinctive morphotypes observed. Identity was confirmed by indole and citrate testing and was selectively verified using the API-20E (bioMérieux). If any of the initially selected colonies proved not to be E. coli, additional colonies (as available) from the primary plate were evaluated, to provide 5 total E. coli colonies, if possible.

Clonal analysis of E. coli isolates. To resolve discrete clones, all confirmed E. coli colonies from a given culture were screened in parallel by random amplified polymorphic DNA (RAPD) analysis, using arbitrary decamer primer 1290 [21]. A representative of each unique RAPD type (as determined by visual inspection of gel images) encountered previously was included when analyzing new isolates, to identify possible repeated recovery of the same clone. To confirm clonal identity and to permit across-host comparisons, 1 representative of each unique RAPD type per subject underwent PFGE analysis with XbaI in accordance with a standardized protocol [22]. Images were captured digitally and analyzed using the BioNumerics system (Applied Maths). A Dice coefficients similarity threshold of 94% (which corresponds approximately with a 3-band difference in profiles; authors' unpublished data) was used to resolve unique PFGE types, which were considered to represent distinct clones.

Colonization behavior. Each clone was assessed for the proportion of specimens and hosts from which it was recovered, the proportion of sampling points at which it was encountered, and its proportional contribution to the total number of colonies analyzed. Frequently isolated clones were defined as those recovered from >10% of specimens or that accounted for >6% of all colonies analyzed. Clones recovered from multiple hosts (whether concurrently or sequentially) were defined as shared clones.

Molecular characteristics of E. coli clones. Additional molecular typing was done for 1 representative of each unique clone from each subject, as available. Established, multiplex PCR-based assays were used to define major E. coli phylogenetic groups (A, B1, B2, and D) and 55 putative or proven ExPEC virulence factor genes (VFs) and variants thereof, including 3 papG alleles (P fimbriae adhesin) and 13 papA alleles (P fimbriae structural subunit) [23–26]. A novel PCR-based assay was used to resolve 12 UTI-associated O groups (O1, O2, O4, O6, O7, O12, O15, O16, O18, O25, O75, and O157) [27]. The VF score was the number of VFs detected per isolate, adjusted for multiple detection of the pap (P fimbriae), sfa/foc (S and F1C fimbriae), and kpsM II (groups 2 capsule) operons. Isolates were operationally defined as ExPEC if they were positive for at least 2 of the following VFs: papA and/or papC (P fimbriae structural subunit and assembly), sfa/foc, afa/dra (Dr binding adhesins), kpsM II, and iutA (aerobactin receptor) [28].

On the basis of VF profile, phylogenetic group, and O group, ExPEC clones were presumptively assigned to a recognized ExPEC clonal group. These presumptive assignments were confirmed at the genomic level by comparative RAPD analysis (as described above), using published isolates from the investigators' collections as reference strains for the respective clonal groups.

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Results

Case report. In January 2005, the index subject (the mother) developed acute urinary frequency, urgency, and dysuria. Symptoms resolved promptly after the institution of fluoroquinolone therapy. A pretherapy urine sample yielded >105 cfu/mL E. coli.

Cultures and clonal analysis. All 6 household members (the mother, the father, the 3 children, and the pet dog) provided fecal samples concurrent with the mother's acute cystitis episode and twice later (at weeks 3 and 7–9 after baseline), except for daughter 2, who did not provide a specimen at the second sampling. All fecal samples yielded E. coli. In addition, the mother provided follow-up urine samples at posttherapy weeks 3 and 7; these yielded 102 cfu/mL E. coli (at week 3) and no growth (at week 7). From the resulting 20 total cultures (17 fecal cultures and 3 urine cultures, including the index sample), selection of up to 5 E. coli colonies per culture (as available) yielded 88 total colonies for analysis.

Among the 88 E. coli colonies, sequential RAPD and PFGE analysis identified 7 unique clones (figures 1 and 2 and table 1). The 7 clones exhibited diverse colonization behaviors, variously occurring in 1–9 of the 20 cultures, accounting for 1–5 of the colonies analyzed per culture and representing 3–38 of the total 88 colonies (tables 1 and 2). Likewise, they were variously recovered at 1 sampling point only (clones B, C, F, and G) or all 3 sampling points (clones A, D, and E). Although 4 clones were recovered from only 1 host each (clones B, C, F, and G), 2 clones (clones D and E) were recovered from 3 hosts, and 1 clone (clone A) was recovered from 5 hosts.

Figure 1
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Figure 1

PFGE profiles of selected Escherichia coli isolates recovered from 6 household members. The dendrogram was inferred according to the unweighted pair group method with arithmetic means on the basis of Dice similarity coefficients, as derived from analysis of band positions. Isolates with ⩾94% similar profiles were defined as representing the same clone. One representative of each clone from each host and specimen type, as available, is shown. Asterisks denote urine isolates; all other isolates are from feces. Host designations are as follows: D1, daughter 1; D2, daughter 2; F, father; M, mother; S, son. Note that clones A and F, both representing E. coli O1:K1:H7, are tied as nearest neighbors at ∼80% similarity.

Figure 2
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Figure 2

Distribution of Escherichia coli clones among 6 household members by host, specimen type, and sampling point. Different colors correspond with unique clones (pulsotypes). The width of colored bar indicates number of colonies from that specimen accounted for by the particular clone (0–5). Bullet, no sample. NG, no growth.

Clone A, the mother's sole urine clone at the time of the acute cystitis episode (figure 2), was an outlier in the following respects: it was recovered from more subjects and more cultures than any other clone, was uniquely recovered from multiple hosts at all 3 sampling points, and was 1 of 2 clones recovered from the dog (figure 1 and table 2).

Patterns of clone sharing. Five of the 7 clones (clones A, B, D, E, and F) were recovered from a unique combination of hosts each, whereas clones C and G were recovered only from the father (table 1). Likewise, over the study period, each host was colonized with a unique combination of clones. Both clones from the dog were also recovered from multiple humans (figure 2 and table 1).

Complex temporal patterns of clone-sharing among hosts and of isolation of a particular clone from a given host were evident (figure 2 and table 1). Clones appeared to move from subject to subject over time. Examples included the seeming movement of clone A from mother, father, and dog (sampling 1), to son (sampling 2), to daughter 1 (sampling 3); of clone D from daughter 1 (sampling 1), to dog (sampling 2), to daughter 2 (sampling 3); and of clone E from daughter 2 (sampling 1) to mother and daughter 1 (sampling 2). Additionally, in an individual host, clones sometimes seemed to disappear but later reappear (e.g., clone B in the father, clone D in daughter 1, and clone A in the dog). Consequently, the extent of clone sharing (i.e., the proportion of potential sharing pairs that exhibited ⩾1 shared clone) was more extensive when all 3 sampling points were considered collectively (i.e., sharing documented within 13 of 15 potential sharing pairs overall) than when each sampling point was analyzed separately (i.e., 3 of 15 potential sharing pairs for the first sampling point, 2 of 10 for the second, and 6 of 15 for the third) (figure 3). Analysis of all 3 sampling points revealed 2 overlapping clone-sharing networks (i.e., mother, daughter 1, dog, father, and son; and mother, daughter 1, dog, and daughter 2), within which each member shared 1 or 2 clones with every other member (figure 3).

Figure 3
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Figure 3

Clone-sharing relationships among 6 household members at 3 individual sampling points (top) and overall (bottom). Colored lines indicate presence of indicated clone (A, red; D, purple; E, green) in both members of a particular host pair, either at the same sampling point (top) or overall (bottom). More clone-sharing pairs are evident in the bottom panel than in the 3 top panels combined.

Contact and diet. The observed patterns of within-household strain sharing corresponded more closely with reported patterns of physical contact among household members than with commonality of diet. Although all household members had some direct physical contact with one another, the father and son had minimal contact with the two daughters. No sexual contact was reported during the study period. In contrast, although the family ate evening meals together, breakfasts differed by subject, the 3 children ate separate lunches prepared by the mother, and the (vegetarian) daughters ate somewhat different foods than did the father, mother, and son. The dog was fed almost exclusively commercial dog food and did not drink from household toilets.

Bacterial characteristics. The 7 clones exhibited diverse phylogenetic groups, O groups, and virulence profiles (table 2). For the 3 multiple-host clones (clones A, D, and E), these characteristics were strictly conserved among the multiple isolates tested. Four clones (A, D, F, and G)—all of which had VF scores ⩾10—fulfilled molecular criteria for ExPEC. According to VF profiles and O type (table 2), as well as RAPD analysis findings (figure 4), each of the ExPEC clones corresponded with a recognized ExPEC clonal group from phylogenetic group B2 or D; specifically, clones A and F represented E. coli O1:K1:H7 (e.g., urosepsis isolate H16) [24], clone D represented E. coli O6:K2:H1 (e.g., archetypal pyelonephritis isolate CFT073) [29] rather than E. coli O6:K15:H31 (e.g., archetypal pyelonephritis isolate 536) [30], and clone G represented an O2;F10,F48 clonal group (e.g., sepsis isolate CA040) [31] (figure 4). Notably, the 4 ExPEC clones included the mother's UTI clone (clone A) and 2 of the 3 shared or frequently isolated clones (clones A, D, and E). In contrast, of the 3 non-ExPEC clones, each of which had a VF score ⩽6, only 1 (clone E) was shared among multiple hosts or was frequently isolated (table 2).

Figure 4
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Figure 4

Random amplified polymorphic DNA profiles of selected Escherichia coli isolates. Profiles were generated using arbitrary decamer primer 1254. Lane numbers appear below gel. Lanes 1 and 10, ladder (250 bp); lanes 4, 6, 7, and 9, representatives of clones D, A, F, and G, respectively, from study subjects; lanes 2 and 3, group B2 reference strains 536 (O6:K15:H31) and CFT073 (O6:K2:H1), respectively; lane 5, group B2 reference strain H16 (O1:K1:H7); and lane 8, group D reference strain CA040 (O2:F10,F48).

Table 1
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Table 1

Distribution of 7 unique fecal Escherichia coli clones among 6 household members over 3 sampling points.

Table 2
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Table 2

Colonization behavior and molecular characteristics of 7 unique Escherichia coli clones recovered from 6 human and canine household members.

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Discussion

In this prospective, longitudinal, microbiological survey of household members of a woman with acute cystitis, we documented extensive within-household sharing of E. coli clones in patterns suggesting host-to-host transmission. The observed strain sharing involved all household members (including the dog), 3 of the 7 clones overall, and 2 of the 4 ExPEC clones. Strain sharing was most extensive for the mother's cystitis clone, which represented (virulence-associated) E. coli O1:K1:H7 [24, 32, 33].

The considerable observed among-host commonality of fecal E. coli clones suggests that the household members effectively functioned almost as a single extended intestinal tract, with occasional incursion of a fecal clone into the mother's urinary tract, with or without accompanying UTI symptoms. Potential mechanisms for the observed strain sharing include host-to-host transmission [10, 16] and coordinate acquisition from an external source—for example, the food supply [18–20]. Host-to-host transmission appeared to be the most likely explanation, because it was supported by the observed temporal patterns of strain sharing and the reported patterns of physical contact among household members.

Notably, clone A, the mother's UTI clone, appeared to move progressively through the household, from the mother, father, and dog (sampling 1); to daughter 1 (sampling 2); to the son (sampling 3). This pattern seems highly unlikely to be explained by either food source or sexual transmission, but it fits well with nonsexual host-to-host transmission. Previous studies have focused mainly on sexual contact as a mechanism for within-household transmission of E. coli strains [5–11], whereas the present findings indicate that other routes of transmission must be considered, because strain sharing involved siblings, parents, children, and the household pet, whereas no sexual activity was reported during the study period.

Strain sharing was more evident when analyzed longitudinally than at any single sampling point, because clones tended to be detected inconsistently in a particular individual, and they would appear de novo in a new host when no longer detectable in a previously colonized host. It is possible that some of the apparent “coming and going” of clones in individual hosts represented sampling error, with clones actually persisting in the particular host but varying in prevalence within the fecal population, such that they intermittently escaped detection by the 5-colony sampling method used [34].

In contrast to the extensive strain sharing observed for 3 clones, other clones occurred sporadically in a single host each. Future studies would be needed to determine whether this phenomenon is associated with specific bacterial or host characteristics, such as male sex (as noted here with 3 of 4 single-host clones).

The mother's acute cystitis strain was the most extensively recovered clone overall, being detected at least once in all household members (including the dog) other than daughter 2, as well as in multiple individuals at each sampling. This is reminiscent of findings previously reported from surveillance of a sexually active couple and their pet cat, among whom the most extensively recovered clone (of 14 clones total)—and the only clone that colonized all 3 subjects—caused an episode of acute cystitis in the woman [17]. Taken together, these data suggest that UTI-causing clones may be especially able to persist in individuals and to spread among closely associated hosts.

Any association of UTI-causing clones with prolonged and multiple-host colonization may occur in part because a clone's ability to persist and spread within households increases the odds that a vulnerable individual will be exposed to the clone and, thus, will develop UTI due to it. The observed trends associating colonization behavior with virulence characteristics and phylogenetic background, although not amenable to statistical analysis here because of the small numbers, are consistent with statistically supported observations from previous studies [11, 17], which suggest that certain bacterial traits may directly contribute to both urovirulence and enhanced colonization and transmission ability. Clearly, however, ExPEC status is not required for a strain to be a persistent or multiple-host colonizer, as illustrated by clone E; despite being non-ExPEC, this was the second most extensively isolated and shared clone overall. Likewise, persistent colonization with an ExPEC strain does not necessarily lead to UTI, as illustrated by daughter 1 and clone D.

Notably, the mother's cystitis clone (clone A) was not recovered again from the mother after antimicrobial therapy, yet it persisted in multiple other household members, including the dog. This pattern suggests that household members could serve as reservoirs for recolonization of an individual with UTI, once the antibiotic effect and any immunity induced by the infection episode has waned, thereby predisposing the individual to same-strain recurrent UTI. This phenomenon might provide the undefined external reservoir that has been postulated to account for widely separated same-strain recurrent UTI episodes in some women, particularly those in whom sustained colonization with the causative strain is not detected [35–38]. Extended household surveillance (ideally involving multiple households) after an episode of cystitis in 1 household member would be useful to test this hypothesis.

If within-household strain sharing does contribute to UTI risk, interventions that reduce within-household transmission of E. coli, including transmission involving pets [39, 40], potentially could protect against UTI. Sexual transmission clearly is but one of many possible mechanisms for transmission. Consequently, more broadly targeted preventive interventions—or interventions targeted specifically toward the relevant transmission mechanisms, if these can be defined—likely would be needed. Additional study is needed to determine whether within-household strain-sharing networks similar to those observed here are common, and whether identifiable exposures (e.g., type or frequency of among-host contact, or extent of shared foods or fomites) are explanatory. Such associations could provide insights into the mechanisms of within-household strain sharing, as is needed for the development of effective preventive interventions. Likewise, comparisons of (1) households in which a member has experienced UTI with (2) non-UTI households could help identify associations between strain sharing and UTI risk.

Limitations of the study include that only 1 household was studied, only 5 E. coli colonies (as available) were analyzed per sample, and there was no direct investigation regarding mechanisms of transmission or external sources for the clones. Strengths include the longitudinal study design, the attention to cocolonization involving non-sex partners (including the family pet), and the use of extended virulence genotyping and genomic profiling to relate colonizing clones to known virulence ExPEC clonal groups.

In summary, we documented extensive commonality of E. coli clones among the human and canine members of the household of a woman with acute UTI. Strain sharing was most evident when analyzed longitudinally, was most extensive for the mother's (ExPEC) cystitis clone, involved members of familiar virulent ExPEC clonal groups, and occurred in patterns suggesting host-to-host transmission. These findings support the hypothesis that within-household transmission may contribute to UTI pathogenesis and suggest that nonsexual modes of transmission deserve attention.

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Acknowledgments

This material is based on work supported by the Office of Research and Development, Medical Research Service, Department of Veterans Affairs. Dave Prentiss created the figures. We thank the study subjects for their contributions.

Potential conflicts of interest. J.R.J. has received grants and/or honoraria from Merck, Bayer, Ortho-McNeil, Wyeth-Ayerst, and Procter & Gamble and is a consultant to Rochester Medical. C.C.: no conflicts.

  • Received July 13, 2006.
  • Accepted August 15, 2006.
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References

  1. ↵
    1. Russo TA,
    2. Johnson JR
    . Medical and economic impact of extraintestinal infections due to Escherichia coli: an overlooked epidemic. Microbes Infect 2003;5:449-56.
    CrossRefMedlineWeb of Science
  2. ↵
    1. Russo TA,
    2. Johnson JR
    . A proposal for an inclusive designation for extraintestinal pathogenic Escherichia coli: ExPEC. J Infect Dis 2000;181:1753-4.
    FREE Full Text
  3. ↵
    1. Johnson JR,
    2. Owens K,
    3. Gajewski A,
    4. Kuskowski MA
    . Bacterial characteristics in relation to clinical source among Escherichia coli isolates from women with acute cystitis or pyelonephritis and uninfected women. J Clin Microbiol 2005;43:6064-72.
    Abstract/FREE Full Text
  4. ↵
    1. Grüneberg RN
    . Relationship of infecting urinary organism to the faecal flora in patients with symptomatic urinary infection. Lancet 1969;1:766-8.
    Medline
  5. ↵
    1. Stamey TA,
    2. Timothy M,
    3. Millar M,
    4. Mihara G
    . Recurrent urinary infections in adult women: the role of introital enterobacteria. Calif Med 1971;115:1-19.
    MedlineWeb of Science
    1. Wong ES,
    2. Stamm WE
    . Sexual acquisition of urinary tract infection in a man. JAMA 1983;250:3087-8.
    Abstract/FREE Full Text
    1. Bailey RR,
    2. Peddie BA,
    3. Swainson CP,
    4. Kirkpatrick D
    . Sexual acquisition of urinary tract infection in a man. Nephron 1986;44:217-8.
    MedlineWeb of Science
    1. Al-Wali W,
    2. Hamilton-Miller JMT,
    3. Joshi S,
    4. Brumfitt W
    . A case of recurrently sexually transmitted urinary tract infection. Genitourin Med 1989;65:397-8.
    MedlineWeb of Science
    1. Hebelka M,
    2. Lincoln K,
    3. Sandberg T
    . Sexual acquisition of acute pyelonephritis in a man. Scand J Infect Dis 1993;25:141-3.
    MedlineWeb of Science
  10. ↵
    1. Foxman B,
    2. Zhang L,
    3. Tallman P,
    4. et al
    . Transmission of uropathogens between sex partners. J Infect Dis 1997;175:989-92.
    Abstract/FREE Full Text
  11. ↵
    1. Foxman B,
    2. Manning SD,
    3. Tallman P,
    4. et al
    . Uropathogenic Escherichia coli are more likely than commensal E. coli to be shared between heterosexual sex partners. Am J Epidemiol 2002;156:1133-40.
    Abstract/FREE Full Text
  12. ↵
    1. Johnson JR,
    2. Delavari P
    . Concurrent fecal colonization with extraintestinal pathogenic Escherichia coli in a homosexual man with recurrent urinary infection and his male sex partner. Clin Infect Dis 2002;35:e65-8.
    Abstract/FREE Full Text
  13. ↵
    1. Johnson JR,
    2. Brown JJ,
    3. Carlino UB,
    4. Russo TA
    . Colonization with and acquisition of uropathogenic Escherichia coli strains as revealed by polymerase chain reaction-based detection. J Infect Dis 1998;177:1120-4.
    Abstract/FREE Full Text
  14. ↵
    1. Hannah EL,
    2. Angulo FJ,
    3. Johnson JR,
    4. Haddadin B,
    5. Williamson J,
    6. Samore MH
    . Drug-resistant E. coli, rural Idaho. Emerg Infect Dis 2005;11:1614-7.
    MedlineWeb of Science
    1. Reves RR,
    2. Fong M,
    3. Pickering LK,
    4. Bartlett AI,
    5. Alvarez M,
    6. Murray BE
    . Risk factors for fecal colonization with trimethoprim-resistant and multiresistant Escherichia coli among children in day-care centers in Houston, Texas. Antimicrob Agents Chemother 1990;34:1429-34.
    Abstract/FREE Full Text
  16. ↵
    1. Tullus K,
    2. Horlin K,
    3. Svenson SB,
    4. Källenius G
    . Epidemic outbreaks of acute pyelonephritis caused by nosocomial spread of P fimbriated Escherichia coli in children. J Infect Dis 1984;150:728-36.
    Abstract/FREE Full Text
  17. ↵
    1. Murray AC,
    2. Kuskowski MA,
    3. Johnson JR
    . Virulence factors predict Escherichia coli colonization patterns among human and animal household members. Ann Intern Med 2004;140:848-9.
    FREE Full Text
  18. ↵
    1. Johnson JR,
    2. Delavari P,
    3. O'Bryan TT,
    4. Smith K,
    5. Tatini S
    . Contamination of retail foods, particularly turkey, from community markets (Minnesota, 1999–2000) with antimicrobial-resistant and extraintestinal pathogenic Escherichia coli. Foodborne Pathog Dis 2005;2:38-49.
    CrossRefMedlineWeb of Science
    1. Johnson JR,
    2. Kuskowski MA,
    3. Smith K,
    4. O'Bryan TT,
    5. Tatini S
    . Antimicrobial-resistant and extraintestinal pathogenic Escherichia coli in retail foods. J Infect Dis 2005;191:1040-9.
    Abstract/FREE Full Text
  20. ↵
    1. Johnson JR,
    2. Kuskowski MA,
    3. Menard M,
    4. Gajewski A,
    5. Xercavins M,
    6. Garau J
    . Similarity of human and chicken-source Escherichia coli isolates in relation to ciprofloxacin resistance status. J Infect Dis 2006;194:71-8.
    Abstract/FREE Full Text
  21. ↵
    1. Berg DE,
    2. Akopyants NS,
    3. Kersulyte D
    . Fingerprinting microbial genomes using the RAPD or AP-PCR method. Methods Mol Cell Biol 1994;5:13-24.
  22. ↵
    Centers for Disease Control and Prevention. Standardized molecular subtyping of foodborne bacterial pathogens by pulsed-field gel electrophoresis, training course [abstract]. Atlanta, GA; 1998.
  23. ↵
    1. Clermont O,
    2. Bonacorsi S,
    3. Bingen E
    . Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000;66:4555-8.
    Abstract/FREE Full Text
  24. ↵
    1. Johnson JR,
    2. Stell AL
    . Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 2000;181:261-72.
    Abstract/FREE Full Text
    1. Johnson JR,
    2. Stell AL,
    3. Scheutz F,
    4. et al
    . Analysis of F antigen-specific papA alleles of extraintestinal pathogenic Escherichia coli using a novel multiplex PCR-based assay. Infect Immun 2000;68:1587-99.
    Abstract/FREE Full Text
  26. ↵
    1. Johnson JR,
    2. Gajewski A,
    3. Lesse AJ,
    4. Russo TA
    . Extraintestinal pathogenic Escherichia coli as a cause of invasive non-urinary infections. J Clin Microbiol 2003;41:5798-802.
    Abstract/FREE Full Text
  27. ↵
    1. Clermont O,
    2. Johnson JR,
    3. Menard M,
    4. Denamur E
    . 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. (in press).
  28. ↵
    1. Johnson JR,
    2. Murray AC,
    3. Gajewski A,
    4. et al
    . Isolation and molecular characterization of nalidixic acid-resistant extraintestinal pathogenic Escherichia coli from retail chicken products. Antimicrob Agents Chemother 2003;47:2161-8.
    Abstract/FREE Full Text
  29. ↵
    1. Welch R,
    2. Burland V,
    3. Plunkett Gr,
    4. et al
    . Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A 2002;99:17020-4.
    Abstract/FREE Full Text
  30. ↵
    1. Blum G,
    2. Ott M,
    3. Lischewski A,
    4. et al
    . Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type pathogen. Infect Immun 1994;62:606-14.
    Abstract/FREE Full Text
  31. ↵
    1. Johnson JR,
    2. O'Bryan TT,
    3. Kuskowski MA,
    4. Maslow JN
    . Ongoing horizontal and vertical transmission of virulence genes and papA alleles among Escherichia coli blood isolates from patients with diverse-source bacteremia. Infect Immun 2001;69:5363-74.
    Abstract/FREE Full Text
  32. ↵
    1. Johnson JR,
    2. Clabots C,
    3. Rosen H
    . Effect of inactivation of the global oxidative stress regulator oxyR on the colonization ability of Escherichia coli O1:K1:H7 in a mouse model of ascending urinary tract infection. Infect Immun 2006;74:461-8.
    Abstract/FREE Full Text
  33. ↵
    1. Achtman M,
    2. Mercer A,
    3. Kusecek B,
    4. et al
    . Six widespread bacterial clones among Escherichia coli K1 isolates. Infect Immun 1983;39:315-35.
    Abstract/FREE Full Text
  34. ↵
    1. Bettelheim KA,
    2. Faiers M,
    3. Shooter RA
    . Serotypes of Escherichia coli in normal stools. Lancet 1972;1:1224-6.
    MedlineWeb of Science
  35. ↵
    1. Russo T,
    2. Stapleton A,
    3. Wenderoth S,
    4. Hooton TM,
    5. Stamm WE
    . Chromosomal restriction fragment length polymorphism analysis of Escherichia coli causing recurrent urinary tract infections in young women. J Infect Dis 1995;172:440-5.
    Abstract/FREE Full Text
    1. Jacobson SH,
    2. Kuhn I,
    3. Brauner A
    . Biochemical fingerprinting of urinary Escherichia coli causing recurrent infections in women with pyelonephritic renal scarring. Scand J Urol Nephrol 1992;26:373-7.
    MedlineWeb of Science
    1. Brauner A,
    2. Jacobson SH,
    3. Kuhn I
    . Urinary Escherichia coli causing recurrent infections: a prospective follow-up of biochemical phenotypes. Clin Nephrol 1992;38:318-23.
    MedlineWeb of Science
  38. ↵
    1. Ikäheimo R,
    2. Siitonen A,
    3. Heiskanen T,
    4. et al
    . Recurrence of urinary tract infection in a primary care setting: analysis of a 1-year follow-up of 179 patients. Clin Infect Dis 1996;22:91-9.
    Abstract/FREE Full Text
  39. ↵
    1. Johnson JR,
    2. Stell A,
    3. Delavari P
    . Canine feces as a reservoir of extraintestinal pathogenic Escherichia coli. Infect Immun 2001;69:1306-14.
    Abstract/FREE Full Text
  40. ↵
    1. Johnson JR,
    2. Delavari P,
    3. Stell AL,
    4. Whittam TS,
    5. Carlino U,
    6. Russo TA
    . Molecular comparison of extraintestinal Escherichia coli isolates from the same electrophoretic lineages from humans and domestic animals. J Infect Dis 2001;183:154-9.
    Abstract/FREE Full Text
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  1. Clin Infect Dis. (2006) 43 (10): e101-e108. doi: 10.1086/508541
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