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Possible Animal Origin of Human-Associated, Multidrug-Resistant, Uropathogenic Escherichia coli

  1. Meena Ramchandani1,
  2. Amee R. Manges1,
  3. Chitrita DebRoy2,
  4. Sherry P. Smith1,
  5. James R. Johnson3,4, and
  6. Lee W. Riley1
  1. 1Division of Infectious Diseases, School of Public Health, University of California, Berkeley, California
  2. 2Gastroenteric Disease Center, Department of Veterinary Science, Pennsylvania State University, University Park, Pennsylvania
  3. 3Mucosal and Vaccine Research Center, Minneapolis Veterans' Affairs Medical Center, Minneapolis
  4. 4Department of Medicine, University of Minnesota, Minneapolis
  1. Reprints or correspondence: Dr. Lee W. Riley, Div. of Infectious Diseases, School of Public Health, University of California, 140 Warren Hall, Berkeley, CA 94720 (lwriley{at}uclink4.berkeley.edu).
 
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Abstract

Background. The multistate occurrence of cases of urinary tract infection (UTI) caused by trimethoprim-sulfamethoxazole (TMP-SMZ)—resistant Escherichia coli strains belonging to a single clonal group (designated as clonal group A [CgA]) in the United States has raised an intriguing hypothesis that these infections may have been spread by contaminated food products. The present study attempted to determine if CgA strains could be traced to food animals.

Methods. A total of 495 animal and environmental E. coli isolates, which belonged to serogroups O11, O17, O73, and O77 and were collected between 1965 and 2002 by the Gastroenteric Disease Center at Pennsylvania State University (University Park, PA), were further subtyped by antimicrobial drug susceptibility, enterobacterial repetitive intergenic consensus (ERIC2) PCR, random amplified polymorphic DNA analysis, pulsed-field gel electrophoresis (PFGE), and virulence profile pattern.

Results. Of 495 isolates, 128 (26%) had an ERIC2 PCR electrophoretic pattern indistinguishable from that of the human prototype CgA strain, and 14 CgA isolates were resistant to TMP-SMZ. Cluster analysis of PFGE patterns showed that 1 of these 14 isolates, obtained from a cow in 1988, was 94% similar to a CgA uropathogenic human-associated E. coli strain. The pattern for this isolate was included among a cluster of PFGE patterns for 5 human-associated UTI isolates that were >80% similar to each other.

Conclusions. These observations suggest that drug-resistant, uropathogenic human-associated E. coli strains potentially have an animal origin. The possibility that human drug-resistant UTI could be a foodborne illness has serious public health implications.

Community-acquired urinary tract infections (UTIs) are among the most common infectious diseases in women. Nearly 1 in 3 women will have at least 1 episode of UTI requiring antimicrobial therapy by the age of 24 years, and almost one-half of all women will experience at least 1 episode of UTI during their lifetime [1]. Escherichia coli is the most common uropathogen isolated from persons with acute community-acquired UTIs, accounting for 75%–90% of cases [2].

Although UTI is usually not thought of as a disease that occurs as part of community outbreaks, there have been past instances of clusters of UTI caused by E. coli with identical serotypes in community settings. Clusters of community-acquired cystitis, pyelonephritis, and septicemia in south London in 1986 and 1987 were associated with E. coli O15:K52:H1, and this serotype has since been shown to be endemic in Barcelona, Spain [3, 4]. Another outbreak caused by E. coli O78:H10 was documented in greater Copenhagen during an 8-month period in 1991 [5].

Between October 1999 and January 2000, strains from a single multidrug-resistant E. coli clonal group, referred to as CgA (as defined by enterobacterial repetitive intergenic consensus [ERIC2] PCR electrophoretic pattern), were found to be responsible for nearly one-half of all trimethoprim-sulfamethoxazole (TMP-SMZ)—resistant community-acquired UTIs in a university community in California [6]. CgA strains were isolated from women with UTI in 2 other geographically distant university communities. They were also isolated from cases of pyelonephritis in at least 6 different states [7]. In the California university community where the UTI study by Manges et al. [6] was conducted, the intestines of 28% of 19 male and 43% of 23 female volunteers were found to be colonized at some point during a 6-month period with CgA E. coli. Some of the isolates from California were indistinguishable by PFGE analysis, a highly discriminating typing method, suggesting a point-source spread of these strains [6]. Community outbreaks of enteric pathogens, such as E. coli O157:H7 or Salmonella species, are well recognized to be caused by the multistate spread of contaminated food products [8–10]. The appearance of CgA E. coli as a cause of UTI in several different states and the recovery of such strains from the intestines of asymptomatic individuals in the university community in California suggested that this clonal group was possibly introduced into these communities by contaminated food products.

This study was undertaken to determine if uropathogenic E. coli could be traced to animals that are distributed as food products for human consumption. The large cluster of a single clonal group of uropathogenic E. coli in California and the knowledge that strains belonging to this group were found in multiple states provided us with an opportunity to determine if related E. coli strains could be identified from animal sources in the United States. The possibility that an agent of multidrug-resistant UTI in women could have an animal origin has major public health implications, especially in light of the practice of administering subtherapeutic doses of antimicrobial agents as growth promoters via animal feed in the United States [11–13].

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Materials and Methods

Bacterial strains. We examined 495 E. coli isolates provided by the Gastroenteric Disease Center at Pennsylvania State University (University Park, PA). These isolates represent the Center's entire collection of non—human-associated E. coli isolates belonging to serogroups O11, O17, O73, and O77, the same serogroups encountered among human-associated CgA isolates. The bacterial isolates were collected from an assortment of animal and environmental sources, including cows, turkeys, chickens, other animals (e.g., cats, dogs, goat, sheep), and water in the Unites States between 1965 and 2002. The investigators performed the strain typing analysis without knowledge of the animal source or the resistance patterns of the isolates.

Strain typing analyses. All E. coli isolates were initially typed by the ERIC2 PCR fingerprinting assay, as described elsewhere [14–18]. The CgA ERIC2 PCR electrophoretic pattern was defined by 4 predominant bands of approximately 1145, 1029, 908, and 720 bp; isolates exhibiting this pattern were considered to be members of CgA. A pyelonephritogenic isolate, CFT073 (kindly provided by Dr. Harry Mobley, University of Maryland, Baltimore), was used as a reference strain for each ERIC2 PCR run [19].

Nineteen CgA E. coli isolates collected after 1988 were typed by random amplified polymorphic DNA (RAPD) analysis with arbitrary decamer primers 1247, 1254, 1282, 1283, and 1290, with boiled lysates as template DNA and amplification conditions as described elsewhere [20]. Profiles from agarose gels were assessed visually for similarity.

The standardized protocol for molecular subtyping of E. coli O157:H7 by PFGE, as established by the Centers for Disease Control and Prevention (CDC; Atlanta, GA), was used to further characterize the E. coli isolates that were indistinguishable by ERIC2 fingerprinting [21]. XbaI-digested DNA was electrophoresed in the CHEF DR-II apparatus (Bio-Rad). The criteria for strain relatedness established by Tenover et al. [22] were used to compare PFGE patterns, with the pattern of the prototype CgA strain (SEQ102, deposited in the American Type Culture Collection [ATCC] as BAA-457) used as the reference.

Images of PFGE and ERIC2 PCR electrophoretic patterns were imported into a software program (GelCompar II, version 2.0 [Applied Maths]) for analysis. Dendrograms based on PFGE patterns were inferred from the Dice similarity coefficient matrix generated by GelCompar by means of the unweighted pair group method with arithmetic averages (UPGMA). A tolerance of 2% was used in the GelCompar pattern analyses. This criterion was established by iterated comparison of gel electrophoresis assays of the same E. coli isolates (control isolates CgA and CFT073). The dendrogram was generated from a comparison of all interpretable PFGE patterns obtained from CgA E. coli isolates from the animal, environmental, and human UTI sources in our study collection.

Antimicrobial susceptibility testing. Susceptibility to TMP-SMZ (for all isolates) and to 9 additional antimicrobial agents (for selected CgA isolates) was assessed by disk diffusion (Sensi-Disk, Becton Dickinson) [23]. The selected strains included all 14 CgA isolates that were TMP-SMZ resistant, plus 3 nonresistant CgA isolates collected between 1988 and 2002. The 9 antimicrobial agents included ampicillin, ciprofloxacin, amoxicillin/clavulanic acid, tetracycline, chloramphenicol, gentamicin, cephalothin, streptomycin, and kanamycin. NCCLS interpretive criteria were used to determine resistance [24]. Intermediately susceptible isolates were recorded as being susceptible. E. coli strain 25922 (ATCC) was used as the reference strain.

Virulence factor profiling. Genotypes for 39 putative virulence factors and the 12 known papA alleles were determined for the same 17 E. coli isolates described above by multiplex PCR assays, supplemented by dot-blot hybridization, as described elsewhere [25–27]. The virulence profile of each animal isolate was then compared to the consensus profile of human-associated CgA isolates, which included the F16 allele of papA (P fimbriae structural subunit), iutA (aerobactin receptor), kpsM II (group 2 capsule), ompT (outer membrane protein T), and traT (associated with resistance in serum).

Statistical analyses. Data were analyzed with Epi Info software, version 6.04b (CDC). Proportions were compared by χ2 or Fisher's exact tests.

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Results

A total of 495 E. coli isolates collected from animal and environmental sources during 1965–2002 and representing serogroups O11, O17, O73, and O77 were analyzed. The sources of these isolates by serogroup are summarized in table 1.

Genotyping. Of 495 isolates, 128 (26%) exhibited the characteristic 4-band ERIC2 PCR electrophoretic pattern observed among human-associated CgA E. coli isolates (figure 1). Among 19 selected CgA E. coli isolates collected after 1988, a total of 15 showed a single RAPD pattern that was indistinguishable from that of the human-associated CgA reference BAA-457, whereas the other 4 exhibited distinct, albeit clearly related, patterns. PFGE was performed on 38 recently obtained CgA E. coli isolates identified by ERIC2 PCR from the animal and environmental collection. One TMP-SMZ—resistant CgA E. coli isolate from serogroup O17 (559), which was obtained from a cow in 1988, had a PFGE pattern that was 94% similar by the Dice coefficient to that of a human-associated CgA isolate (SEQ895) belonging to serogroup O77 (figure 2). By UPGMA analysis, this strain was grouped into 1 cluster comprised of 5 human-associated UTI CgA isolates with PFGE patterns that were >80% similar (figure 3).

Figure 1
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Figure 1

Enterobacterial repetitive intergenic consensus 2 PCR profiles of selected animal- and human-associated Escherichia coli isolates. Lane 1, human-associated reference strain CFT073; lane 2, prototype human-associated uropathogenic clonal group A (CgA) strain BAA-457 (serogroup O11; American Type Culture Collection); lanes 3–13, animal-associated E. coli isolates; lane 14, blank. Lanes 2–5 and 7–10 (underlined) show a CgA pattern. MW, 100-bp molecular weight marker.

Figure 2
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Figure 2

PFGE profiles of selected Escherichia coli isolates. Lanes 1 (strain BAA-457 [American Type Culture Collection], 3, 4, 7, and 8, human-associated uropathogenic E. coli strains (serogroups O11, O77, O17, O73, and O77, respectively) that exhibited the enterobacterial repetitive intergenic consensus 2 PCR clonal group A pattern; lanes 2, 5, and 6, animal-associated isolates (underlined). Analysis with the Dice coefficient revealed that strain 559, obtained from a cow (lane 2), has a PFGE pattern that is 94% similar to the pattern of an isolate, SEQ895 (lane 3), recovered from a human. MW, 100-bp molecular weight marker.

Figure 3
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Figure 3

Dendrogram based on unweighted pair group method with arithmetic averages cluster analysis of PFGE patterns of clonal group A (CgA) Escherichia coli isolates in urine specimens obtained from women with urinary tract infection (UTI) and from animals. All trimethoprim-sulfamethoxazole—resistant animal-associated isolates and selected nonresistant isolates were analyzed by PFGE. Strain 559 (serogroup O17) was isolated from a cow in 1988 and falls within a cluster of 5 UTI-associated E. coli isolates that were >80% similar to each other (by Dice coefficient similarity analysis) (bracket). Strain 559 is 94% similar to strain SEQ895 (figure 2, lane 3) and 91% similar to the prototype CgA strain (BAA-457 [American Type Culture Collection]; figure 2, lane 1).

Antibiotic susceptibility testing. Of 495 isolates, 72 (15%) were resistant to TMP-SMZ (table 2). Resistance to TMP-SMZ was similarly prevalent among non-CgA E. coli isolates (58 [16%] of 367) and CgA isolates (14 [10%] of 128) (P > .05). The most common serogroup among the TMP-SMZ—resistant isolates was O11 (69%). The TMP-SMZ—resistant CgA E. coli isolates were more likely to belong to serogroup O17 than to other serogroups. Among the 72 TMP-SMZ—resistant isolates, 13 (18%) were serogroup O17, whereas 9 (64%) of 14 TMP-SMZ—resistant CgA isolates were serogroup O17 (P = .0009, by 2-tailed Fisher's exact test). This is explained by the observation that most (56%) of the 128 CgA isolates were serogroup O17.

Figure 4
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Figure 4

Number of serogroup O11, O17, O73, and O77 Escherichia coli isolates sent to the Pennsylvania State University serotyping reference laboratory (University Park, PA) between 1965 and 2002. Clonal group A (CgA) and trimethoprim-sulfamethoxazole (TMP-SMZ)—resistant isolates are shown by year of collection.

Table 1
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Table 1

Sources of animal-associated and environmental Escherichia coli isolates, according to serotype.

Table 2
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Table 2

Frequency of trimethoprim-sulfamethoxazole (TMP-SMZ)—resistance and/or clonal group A (CgA) among 495 Escherichia coli isolates recovered from animal and environmental sources, according to serogroup.

All TMP-SMZ—resistant CgA and the 3 most recently recovered nonresistant CgA isolates (i.e., those recovered after 1988) were tested for susceptibility to 9 other antimicrobial agents. One isolate (59), collected in 2001 from a cow, was resistant to 9 antimicrobial agents. The human-associated CgA reference strain (BAA-457) is resistant to 6 drugs—tetracycline, streptomycin, trimethoprim, sulfonamide, ampicillin, and chloramphenicol. Three of 9 bovine isolates exhibited a similar pattern of resistance, except that they were not resistant to chloramphenicol. None of 22 human-associated CgA isolates tested against the same set of antimicrobial agents had a susceptibility profile identical to that of any of the animal isolates.

Virulence genotyping. Virulence profiles were analyzed for 17 selected CgA E. coli isolates. Although some similarities were seen, none of the virulence profiles of animal isolates were identical to the profiles of the human-associated CgA isolates from California, Minnesota, or Michigan.

Temporal isolations of CgA isolates. Of 495 isolates collected between 1965 and 2002, the earliest representative of CgA E. coli was collected in 1976 (figure 4); that is, of 14 isolates collected before 1976, none were CgA (P = .026, by 2-tailed Fisher's exact test). TMP-SMZ resistance did not appear in CgA isolates until 1987. Thus, of 34 CgA isolates collected between 1976 and 1986, none were resistant to TMP-SMZ, whereas 14 (15%) of 94 CgA isolates collected between 1987 and 2002 were resistant (P = .02, by 2-tailed Fisher's exact test).

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Discussion

The appearance of uropathogenic E. coli strains belonging to a single clonal group (as defined by ERIC2 PCR electrophoretic pattern, serogrouping, and PFGE) in multiple states during the same approximate period suggested dissemination by widely distributed contaminated food products [6]. A more recent study in Denver, Colorado, found that 10 (43%) of 23 TMP-SMZ—resistant E. coli isolates from cases of community-acquired UTI were CgA [28]. Suspected vehicles of infection in multistate enteric outbreaks often include food of animal origin, such as dairy and meat products. Drug-resistant E. coli O157:H7, Salmonella species, and Campylobacter species are frequent causes of such foodborne outbreaks [29]. The multidrug-resistant strains of these recognized enteric pathogens originate in the animal reservoir, where they are believed to undergo selection when antimicrobial agents are given for therapy or in subtherapeutic doses as growth promoters. We suspected that food prepared from animals might also be a source of human-associated, multidrug-resistant, uropathogenic E. coli.

The availability of a large collection of strains belonging to a single uropathogenic E. coli clonal group (CgA) enabled us to compare antimicrobial susceptibility patterns, ERIC2 PCR fingerprints, RAPD profiles, PFGE patterns, and virulence profiles of E. coli isolates from animal and environmental sources in the United States. All available E. coli isolates from serogroups O11, O17, O73, and O77 collected between 1965 and 2002 were analyzed. The evidence suggesting that some of these food animal—associated isolates are related to the human-associated CgA isolates is as follows: of 495 isolates, 128 (26%) exhibited a characteristic 4-band CgA ERIC PCR electrophoresis pattern indistinguishable from that observed for the human-associated CgA isolates; 79% of these non—human-associated CgA isolates were indistinguishable from the reference human-associated CgA isolate by RAPD analysis; and 1 cow isolate exhibited a PFGE pattern that was 94% similar to the pattern of a human-associated CgA isolate (and 91% similar to the prototype strain BAA-457) and was also grouped into a cluster of human-associated UTI isolates with PFGE patterns that were >80% similar (figure 3). However, despite similarities, none of the antibiotic susceptibility patterns or virulence factor profiles completely matched any of those of the comparator human-associated CgA isolates. There was also a greater diversity of RAPD and virulence factor profiles among animal CgA isolates than among human-associated CgA isolates, suggesting that the animal CgA strains are evolutionarily older than the human-associated isolates.

It is, of course, unlikely that the E. coli isolates examined in this study are representative of all animal and environmental E. coli isolates in the United States from the 4 serogroups studied, because they were sent to the Gastroenteric Disease Center primarily for diagnostic purposes. This could result in a substantial selection bias. However, among the animal isolates collected from 1965 to 2002, those exhibiting the ERIC2 PCR CgA pattern were not observed until 1976, whereas TMP-SMZ—resistant CgA strains did not appear until 1987. The serogroups to which the human-associated CgA strains belong are not included among the traditional so-called uropathogenic E. coli serogroups (O1, O2, O4, O6, O7, O16, O18, O25, and O75), which suggests that, in humans, drug-resistant CgA strains may have become a cause of UTI relatively recently [30]. This would be consistent with the recent appearance of animal-associated E. coli isolates with the drug-resistant ERIC2 PCR CgA pattern.

PFGE is a highly discriminating method for typing E. coli strains. Because this study analyzed isolates collected during a large interval of time (1965–2002) and from a large geographic area, it was unlikely that we would find PFGE patterns indistinguishable from those of the human-associated CgA isolates collected during a 4-month period between 1999 and 2000 [6]. The closest match we found in the PFGE patterns of any animal and human-associated isolates was 94% by the Dice coefficient. This mismatch is most likely to be due to the fact that these strains were isolated >10 years apart. Even among the human-associated CgA isolates, only those identified in a limited temporal and geographic setting produced indistinguishable PFGE patterns (figure 3). Thus, it is remarkable that this study found even 1 close match between human- and animal-associated isolates.

The possibility that UTI can be caused by drug-resistant E. coli spread by contaminated food products has serious public health implications. In the university community in California, if it were not for the CgA strains, the overall prevalence of TMP-SMZ—resistant UTIs during the 4-month study period would have been 11% instead of 22% [6]. Introduction by contaminated food products of a single clone of E. coli that happens to be drug-resistant could abruptly alter the prevalence of drug-resistant UTI in that community. Therefore, the typical recommendation to limit the use of antimicrobial agents to prevent emergence of drug resistance in the human population would not necessarily prevent drug-resistant UTI. Indeed, in a study in the United Kingdom, despite a huge decrease in sulfonamide prescriptions received by humans between 1991 and 1999, the prevalence of sulfonamide-resistant E. coli strains increased during the same period [31]. In addition to recognized drug-resistant foodborne enteric diseases, drug-resistant UTI may have to be included among drug-resistant infectious diseases spread via food of animal origin.

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Acknowledgments

We thank Peter Dietrich and the staff of Tang Health Center for their help, which enabled us to initiate this new study.

Financial support. National Institutes of Health (grant RO3 AI053754) and US Department of Agriculture National Research Initiative Competitive Grants Program (grant 00–35212–9408).

Potential conflicts of interest. All authors: no conflicts.

  • Received July 13, 2004.
  • Accepted September 8, 2004.
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  1. Clin Infect Dis. (2005) 40 (2): 251-257. doi: 10.1086/426819
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