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Molecular Analysis of Escherichia coli from Retail Meats (2002–2004) from the United States National Antimicrobial Resistance Monitoring System

  1. James R. Johnson1,3,
  2. James S. McCabe1,3,
  3. David G. White4,
  4. Brian Johnston1,3,
  5. Michael A. Kuskowski2,3, and
  6. Patrick McDermott4
  1. 1Departments of Medicine, Minnesota
  2. 2Medicine and Psychiatry, University of Minnesota, Minnesota
  3. 3Veterans Affairs Medical Center, Minneapolis, Minnesota
  4. 4Center for Veterinary Medicine, United States Food and Drug Administration, Laurel, Maryland
  1. Reprints or correspondence: Dr. James R. Johnson, Infectious Diseases (111F), Veterans Affairs Medical Center, 1 Veterans Drive, Minneapolis, MN 55417 (johns007{at}umn.edu).
 
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Abstract

Background.The origins and virulence potential of meat product-associated Escherichia coli are undefined.

Methods.Two hundred eighty-seven E. coli isolates (145 resistant and 142 susceptible to trimethoprim-sulfamethoxazole, nalidixic acid, and/or ceftiofur), recovered by the United States National Antimicrobial Monitoring System from retail beef, pork, chicken, and turkey products (from Oregon, Tennessee, Georgia, and Maryland, 2002–2004) underwent polymerase chain reaction testing for phylogenetic groupings and 59 virulence-associated genes.

Results.However analyzed, resistant and susceptible isolates differed minimally according to the assessed characteristics. In contrast, the 4 meat types differed greatly for multiple individual traits and aggregate virulence scores. Poultry isolates exhibited virulence genes associated with avian pathogenic E. coli; beef isolates exhibited traits associated with E. coli from diseased cattle. Overall, 20% of isolates qualified as extraintestinal pathogenic E. coli, with poultry isolates exhibiting significantly higher virulence scores than beef and pork isolates (P<.001 ).

Conclusions.Within this systematically collected, geographically distributed sample of recent retail meat isolates, the carriage of extraintestinal pathogenic E. coli virulence genes in antimicrobial-resistant and antimicrobial-susceptible E. coli appeared similar, whereas isolates from different types of meat differed, consistent with on-farm acquisition of resistance within host species-specific E. coli populations. A substantial minority of meat-source E. coli (whether susceptible or resistant) may represent potential human pathogens.

The food supply is a suspected source of antimicrobial-resistant and virulent Escherichia coli strains that may pose a health threat to consumers because of their resistance elements and potential to cause extraintestinal infections, such as cystitis, pyelonephritis, bacteremia, and meningitis [1-6]. Previous studies have documented the presence of antimicrobial-resistant E. coli in retail foods, especially meats (and particularly poultry products), and have shown that some food-source E. coli exhibit molecular characteristics that suggest human pathogenic potential [5-14]. Moreover, in some studies, despite the tremendous diversity of phylogenetic groups and virulence gene profiles among food-source E. coli, the drug-resistant and drug-susceptible populations have been largely indistinguishable according to these traits overall, while differing by food type [10-13, 15]. This fact has suggested that the resistant isolates, rather than being introduced from some alternate reservoir, likely originate from the same source population as the susceptible isolates, plausibly the intestinal microflora of a food-animal host, and that the resistant isolates have acquired resistance-conferring mobile elements or mutations under selection pressure from on-farm antimicrobial use.

However, these studies were of limited geographical scope [10-15], involved a single meat type (thereby precluding comparisons across meat type) [12, 15], and/or used isolates recovered before the year 2000 [12]. The availability from the National Antimicrobial Resistance Monitoring System (NARMS) of recent drug-resistant and drug-susceptible E. coli isolates from 4 types of retail meats, collected systematically from grocery stores in 4 geographically distributed sentinel sites (Oregon, Tennessee, Georgia, and Maryland), offered an opportunity to revisit this question by means of a more broadly representative and recent study population. Accordingly, we performed this study to further clarify the origins and extraintestinal virulence potential of food-source E. coli, especially drug-resistant strains. Because of the therapeutic relevance and use in agriculture of trimethoprim-sulfamethoxazole (cotrimoxazole), nalidixic acid (which is chemically related to fluoroquinolones), and ceftiofur (an extended-spectrum cephalosporin), or congeners thereof, we focused on strains resistant to these agents from retail meat products in selected US markets.

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Methods

Retail meat sampling. NARMS retail meat monitoring is conducted in collaboration with the Centers for Disease Control and Prevention FoodNet program [16]. Microbiological analysis of meats for the presence of E. coli is conducted at 4 sites: Oregon, Tennessee, Georgia, and Maryland. FoodNet personnel at these sites purchased 40 retail meats per month, comprising 10 samples each of chicken breast, ground turkey, ground beef, and pork chops, from a convenience sampling of grocery stores. Samples were kept cold during transport from the grocery store(s) to the Food and Drug Administration (FDA) Center for Veterinary Medicine laboratory (Laurel, Maryland).

Microbiological analysis. Microbiological processing of the meat samples was performed in accordance with published NARMS protocols [17]. Upon arrival at the FDA Center for Veterinary Medicine laboratory, every isolate was streaked for purity on a blood agar plate and confirmed as E. coli with the Vitek 2 Compact microbial identification system (bioMérieux). Antimicrobial susceptibility testing was performed using the panel of 15 antimicrobials tested in the NARMS program. Antimicrobial minimum inhibitory concentrations were determined via the Sensititre automated antimicrobial susceptibility system (Trek Diagnostic Systems) with cation-adjusted Mueller-Hinton broth, and results were read after 18-24 h incubation at 36°C. The minimum inhibitory concentrations were interpreted in accordance with Clinical and Laboratory Standards Institute standards where available [6]. E. coli ATCC 25922, E. coli ATCC 35218, Enterococcus faecalis ATCC 29212, Staphylococcus aureus ATCC 29213, and Pseudomonas aeruginosa ATCC 27853 were used as quality control organisms to ensure the validity of the susceptibility testing.

Bacterial strains and molecular typing. Selected archived NARMS E. coli isolates (n=287; 2002–2004) from 4 types of retail meat items (ground beef, pork chops, chicken breast, and ground turkey) were studied. Isolates were tested in duplicate for the major E. coli phylogenetic groups (A, B1, B2, and D) and the presence of 59 virulence factor (VF)-encoding genes and molecular variants thereof, by means of multiplex polymerase chain reaction methods [18, 19]. The molecular cri terion for qualifying as extraintestinal pathogenic E. coli (ExPEC) was the presence of ⩾2 of 5 key VF genes, including papA and/or papC (counted as 1: P fimbriae), sfa/foc (S and F1C fimbriae), afa/dra (Dr-binding adhesins), iutA (aerobactin system), and kpsM II (group 2 capsules) [15]. The virulence score was the total number of VF genes detected, not counting multiple detection of the pap, sfa, foc, and kpsM operons (to avoid giving disproportionate weight to these VFs). During the testing, laboratory personnel were unaware of the resistance status and meat source of the isolates.

Statistical methods. Comparisons were made across meat types (with or without stratification by antimicrobial class, resistance status, or both) and between resistant versus susceptible isolates (with or without stratification by meat type, antimicrobial class, or both). Comparisons were based on 3 types of data, that is, individual traits, aggregate virulence scores, and principal coordinates analysis (PCoA) values, as described below.

Comparisons of proportions were tested using Fisher's exact test (2-tailed) or, for the distribution of isolates by meat type and locale (table 1), Pearson's χ2test. Because virulence scores exhibited a nonnormal distribution, comparisons of virulence scores were tested using the Mann-Whitney U test or the Kruskal-Wallis test.

Figure 1
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Figure 1

Principal coordinates analysis of phylogenetic group and virulence gene content for 287 Escherichia coli isolates from retail meats. Note the spatial separation of the 4 meat types (chicken [n=116 ], pork [n=43 ], turkey [n=94 ], and beef [n=34 ]) on the axis 1-versus-axis 3 plane, which provided the greatest separation of the data and statistically significant differences (P<.001 for axis 1, P=.009 for axis 3) according to multivariate analysis of variance. Colored lines encircle the corresponding (meat type-specific) data points, except for outliers. Almost all the differences were between beef or pork isolates and chicken or turkey isolates (P⩽.001 for each comparison). In contrast, beef and pork isolates did not differ significantly on any of the first 3 axes; chicken and poultry isolates differed significantly only on axis 3 (P=.02 ).

Figure 2
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Figure 2

Principal coordinates analysis of phylogenetic group and virulence gene content for 287 Escherichia coli isolates from retail meats. The analysis involved all isolates selected on the basis of resistance to trimethoprim-sulfamethoxazole (n=61 ), nalidixic acid (n=48 ), or ceftiofur (n=36 ) and the corresponding susceptible control isolates (total, n=142 ). Note the near-complete overlap of resistant versus susceptible isolates on the axis 1-versus-axis 3 plane. The axis 1-versus-axis 2 and axis 2 -versus-axis 3 plots yielded similar findings, as did separate plots for each meat type-drug combination (not shown).

Table 1
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Table 1

Distribution of 287 meat-source Escherichia coli isolates among the 4 study locales, by meat type

Overall similarity relationships among the individual isolates with respect to VF profiles and phylogenetic group were assessed by using PCoA, which is a multivariate technique related to correspondence analysis that allows one to plot the major patterns within a dataset containing multiple traits and multiple samples [20]. By means of Genalex6 [20], PCoA was applied to the VF and phylogenetic group dataset to collapse the multiple VFs and phylogenetic groups for simplified comparisons by meat type or resistance status. Each axis in PCoA represents a unique weighted composite of all the individual variables in the dataset. Individual isolates are assigned values on each axis on the basis of their results for the study variables and each variable's weighting factor on the particular axis. Each successive axis captures the largest possible share of the residual variance not accounted for by previous axes. Values for each isolate from the first 3 PCoA axes, which capture most of variance within the dataset, were plotted to facilitate visual assessment of the spatial separation of the isolates on the axis 1-versus-axis 2, axis 1-versus-axis 3, and axis 2-versus-axis 3 planes. These values also were used in multivariate analysis of variance (ANOVA) to determine whether the comparison groups (ie, different meat types or resistance phenotypes) differed significantly according to the first 3 PCoA axes, individually and combined. If the initial multivariate ANOVA identified a significant overall difference, univariate ANOVA was used to test pairwise comparisons of individual groups according to each PCoA axis, with use of a Bonferroni correction for multiple post-hoc comparisons as appropriate.

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Results

Study isolates. The 287 E. coli isolates from retail beef, pork, turkey, and chicken products were selected from NARMS samples collected from 2002 through 2004, distributed fairly evenly among the 4 NARMS sites (table 2). Resistance to one or both of the antimicrobial classes other that for which the isolate was selected was present in fewer than 10% of isolates overall (table 2).

Table 2
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Table 2

Distribution of 287 Escherichia coli isolates from different retail meats according to resistance status, by antimicrobial class and meat type

Isolates were characterized molecularly for phylogenetic group and virulence gene content (table 3). All 4 phylogenetic groups were detected within the population, as were 47 of 59 individual VFs or variants, for a total of 51 analyzable markers. These data were then used to compare the 4 meat types and, separately, the resistant versus susceptible isolates, according to individual traits (univariate comparisons), aggregate virulence scores, and a synthesis of the individual traits as provided by PCoA.

Table 3
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Table 3

Differences among Escherichia coli isolates from 4 different retail meats according to phylogenetic group distribution and virulence gene content

Univariate comparisons. Among the 287 study isolates, many differences were apparent among the 4 meat types according to the prevalence of 51 individual traits, whereas the resistant and susceptible isolates differed minimally for these same traits. For example, with all isolates combined, 23 (42%) of 55 comparisons involving the 4 meat types yielded P<.05, and 13 (24%) yielded P⩽.01 (table 3). Notably, many of these differences reflected a higher prevalence among poultry isolates of virulence genes associated with avian pathogenic E. coli (eg, iutA, iroN, ireA, iss, traT, tsh, pic, cvaC, and hlyF ) [21-23] or a higher prevalence among beef isolates of virulence genes associated with E. coli from diseased cattle (ie, afaE8 and clpG ) [24, 25] (table 3). In contrast, only 2 (4%) of 51 similar comparisons between resistant and susceptible isolates yielded P<.05, which is within the range expected by chance alone, and none yielded P⩽.01 (not shown). Comparable results were obtained after stratification by antimicrobial class and/or meat type (not shown).

Virulence scores. Similar relationships were observed when comparisons were made on the basis of aggregate virulence scores, which in the total population ranged from 0 to 15.75 (median, 7.0; bimodal peaks at 2.5 and 7.0). That is, when virulence scores were compared across the 4 meat types (by using the Kruskal-Wallis test), with or without stratification by antimicrobial class and/or susceptibility status, 9 (75%) of the 12 total comparisons yielded P<.05, and 7 (58%) yielded P⩽.01, evidence of marked meat type-specific differences in virulence scores. In contrast, when virulence scores of susceptible and resistant isolates were compared (by using the Mann-Whitney test), with or without stratification by meat type and/or antimicrobial class, only 2 (12%) of the 17 total comparisons yielded P<.05, and none yielded P⩽.01, evidence against resistant status-specific differences in virulence scores.

PCoA. For an integrated analysis, PCoA was used to collapse the entire dataset, including VF gene variants that were omitted from the virulence score calculation, into a small number of derived variables (ie, principal coordinates or axes). With all isolates combined in a PCoA on the basis of the 51 unique study variables (comprising 47 detected virulence markers and 4 phylogenetic groups), the first 3 axes of the PCoA captured 40%, 22%, and 15%, respectively, of total variance in the dataset (collectively, 77%).

The PCoA showed a clear separation of the 4 meat types, particularly on the axis 1-versus-axis 3 plane (figure 1), in which chicken and turkey isolates (which were fairly similarly distributed) extended into a large region devoid of beef and pork isolates. The overall (4-group, 3-axis) multivariate ANOVA was highly significant (P<.001 ). Univariate ANOVA showed a significant 4-group difference for axis 1 (P<.001 ) and axis 3 (P=.009 ) but not axis 2 (P=.28 ). Axis 1 yielded significant differences (P⩽.001 ) between beef or pork and chicken or turkey, but no difference between beef and pork or between chicken and turkey. Axis 3 yielded a marginally significant difference between chicken and turkey (P=.02 ). In contrast to these significant separations by meat type, the PCoA showed complete overlap of the resistant and susceptible isolates on the same 3 axes (figure 2), and a multivariate ANOVA based on the first 3 PCoA axes yielded P=0.28.

Inferred virulence of meat-source E. coli. Overall, 57 (20%) of the 287 total meat-source E. coli isolates satisfied molecular criteria for ExPEC, suggesting possible pathogenic potential for humans. When the 3 antimicrobial classes were analyzed separately, the proportion of isolates qualifying as ExPEC did not differ significantly by meat type or resistance status. However, when all isolates were combined, the resistant isolates actually were somewhat more likely than susceptible isolates to be ExPEC (25% vs 15%; P=.038 ). Poultry isolates were somewhat more likely to be ExPEC (47 [22%] of 210 isolates) than were beef and pork isolates (10 [13%] of 77 isolates; P=.095 ) and exhibited significantly higher aggregate virulence scores (median score, 8 [range, 0-14] vs median score, 2 [range, 0-10]; P<.001 ).

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Discussion

In this study, we characterized 287 antimicrobial-resistant and antimicrobial-susceptible E. coli isolates from retail meats (2002–2004) for phylogenetic background and a broad range of virulence-associated traits, then we made comparisons by resistance status and meat type. We found that, whereas resistant and susceptible isolates exhibited no more differences than would be expected by chance alone, isolates from different meat types differed considerably according to numerous individual traits and aggregate virulence scores. These findings are consistent with the hypothesis that drug-resistant E. coli in retail meats derive primarily from an initially drug-susceptible, host species-specific, food animal-associated microflora within which resistance has emerged under selection pressure, most likely from on-farm antimicrobial use.

The near absence of significant differences in phylogenetic distribution and virulence gene content between antimicrobial-resistant and antimicrobial-susceptible E. coli isolates from a given meat type suggests that the resistant and susceptible isolates derive from the same source population, with resistant isolates having arisen from susceptible progenitors by mutation or acquisition of mobile resistance elements. These findings largely replicate those of several previous studies that involved different sampling strategies, locales, resistance phenotypes, and time periods [10-13], thereby extending the previous observations to a more broadly representative and contemporary US sample. The consistency of findings across studies suggests that the relationships are robust and biologically valid.

In contrast to the near absence of differences by resistance status, the multiple differences noted by meat type suggest that the isolates likely originate from the intestinal flora of their respective source-host species, consistent with on-farm selection for resistance. Supporting this inference was the excess of avian pathogenic E. coli -associated virulence genes among the poultry isolates [21-23] and of bovine pathogenic E. coli -associated virulence genes among the beef isolates [24, 25]. These meat type-specific differences are consistent with findings from previous, more geographically limited studies [10, 11], which again suggests that the relationships hold generally.

Finally, the substantial proportion of meat-source isolates that represent ExPEC, regardless of resistance status or meat type, as has been noted in multiple studies [10-13, 15], suggests a potential public health hazard for consumers. That the resistant isolates, compared with the susceptible isolates, were actually somewhat more likely to represent ExPEC (and, within 2 subgroups, exhibited higher virulence scores) may be attributable in part to our inclusion of iutA in the operational definition of ExPEC, because iutA is known to sometimes occur on plasmids that contain both resistance elements and other virulence genes [26-28]. In any event, the observed relationships contradict the notion that drug-resistant E. coli are necessarily less virulent than susceptible E. coli, as has been proposed on the basis of observations from human clinical isolates [28-34], which may represent an admixture of human-source susceptible isolates and external-source resistant isolates. The finding that poultry-source isolates were somewhat more likely to qualify as ExPEC and exhibited significantly higher aggregate virulence scores, compared with beef and pork isolates, is consistent with previous work and adds to the evidence implicating poultry products as probable important vehicles for foodborne dissemination of virulent, antimicrobial-resistant E. coli [10-13, 15].

Limitations of our study include small numbers within certain subgroups, sampling from only 4 locales, attention to only 3 drug classes, and reliance on molecular typing (rather than animal experimentation) for virulence assessment. Strengths include the systematic and distributed sampling approach, broad range of traits assessed, focus on clinically relevant resistance phenotypes, and multiple complementary methods used for statistical analysis.

In summary, we found that among 287 recent E. coli isolates from retail meats from across the United States, resistant and susceptible isolates differed minimally according to phylogenetic group distribution and virulence gene content (however assessed). In contrast, isolates from different meat types differed considerably according to these same traits. These findings are consistent with the hypothesis that antimicrobial-resistant E. coli in retail meats derive primarily from a host species-specific, food animal-associated microflora within which resistance emerges either as a direct effect of selection pressure from on-farm antimicrobial use or as part of the adaptation of the organisms to their respective hosts. Regardless, these data support efforts during production and distribution to reduce (1) the prevalence, density, and antimicrobial resistance capability of E. coli in food animals and (2) the contamination of the resulting retail meat products.

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Acknowledgments

This study is based on work supported by the Office of Research and Development, Medical Research Service, Department of Veterans Affairs, and the Center for Veterinary Medicine, US Food and Drug Administration. We acknowledge Sonya Bodies-Jones, Stuart Gaines, Shawn McDermott, and Sherry Ayers for microbiological support.

Possible conflicts of interest. Dr. Johnson has received grants, consultancies, and/or honoraria from Merck, Bayer, Ortho-McNeil, Wyeth-Ayerst, Rochester Medical, and Procter & Gamble. All other authors: no conflicts.

  • Received January 11, 2009.
  • Accepted March 4, 2009.
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  1. Clin Infect Dis. (2009) 49 (2): 195-201. doi: 10.1086/599830
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