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. 2011 Aug;77(16):5813–5817. doi: 10.1128/AEM.02614-10

Adherent-Invasive Escherichia coli Phenotype Displayed by Intestinal Pathogenic E. coli Strains from Cats, Dogs, and Swine ▿

Margarita Martinez-Medina 1,*, Jesus Garcia-Gil 1, Nicolas Barnich 2, Lothar H Wieler 3, Christa Ewers 3
PMCID: PMC3165260  PMID: 21705530

Abstract

The adherent-invasive Escherichia coli (AIEC) pathotype, which has been associated with Crohn's disease, shows similar traits to human and animal extraintestinal pathogenic E. coli (ExPEC) with respect to their phylogenetic origin and virulence gene profiles. Here, we demonstrate that animal ExPEC strains generally do not share the AIEC phenotype. In contrast, this phenotype is very frequent among animal intestinal pathogenic E. coli (InPEC) strains, particularly of feline and canine origin, that genetically resemble ExPEC. These results strengthen the particular identity and disease specificity of the AIEC pathotype and the putative role animals might play in the transmission of AIEC-like strains to humans.

TEXT

Adherent-invasive Escherichia coli (AIEC) is a recently described pathotype that has been repeatedly associated with Crohn's disease (2, 4, 8, 9, 13). Nowadays, this pathotype can be identified only by phenotypical traits, because no specific virulence genes have been discovered to date. The identification of AIEC strains is based on their ability to adhere to and to invade intestinal epithelial cells, as well as their capacity to survive and replicate within macrophages (4). The AIEC strains isolated to date are clonally diverse and belong to distinct serotypes, and even though they primarily fall into the B2 phylogroup, AIEC strains belonging to the A, B1, and D phylogroups have also been isolated (2, 8, 9, 11, 13). Moreover, AIEC strains carry different sets of virulence-associated gene characteristics of extraintestinal pathogenic E. coli (ExPEC) strains (2, 4, 9), and some strains, including the prototype strain LF82, have been found to be genetically similar to distinct avian pathogenic E. coli (APEC) (2, 3, 10, 14). Due to the similarities observed between these pathotypes, we compared several genotypic and phenotypic characteristics of AIEC and human ExPEC strains in a previous study (10). We observed that although both pathotypes were genetically similar (in terms of virulence gene profiles, phylogenetic backgrounds, and pulsed-field gel electrophoresis profiles), the majority of human ExPEC strains did not share the AIEC phenotype, which gives to the pathotype a particular identity.

It is against this background that we sought to examine the AIEC phenotype among animal strains, either from extraintestinal or intestinal infections, commonly showing an ExPEC-typical genotype in order to (i) evaluate the impact of the similar phylogenetic background and virulence profile among animal strains on their AIEC-like phenotype properties, (ii) study host and disease specificity of the AIEC pathotype, and (iii) seek out a putative zoonotic risk of AIEC strains between humans and animals.

We analyzed the AIEC phenotype of 79 ExPEC strains causing extraintestinal disease (Table 1) and 45 intestinal pathogenic E. coli (InPEC) strains causing enteritis to animals (Table 2). Together, these strains were adopted from a larger collection of animal strains with available sequence types (C. Ewers and L. H. Wieler, unpublished data; strains have been deposited in the MLST database [http://mlst.ucc.ie/mlst/mlst/dbs/Ecoli/]). Virulence-associated genes linked with the ExPEC group were determined as described recently (5). Strains were selected with respect to sequence types (STs) that had already been found in AIEC strains from patients with Crohn's disease, including ST131, ST73, ST10, and ST101. A broad range of serotypes was included, and we preferentially chose motile strains with malX and kpsMTII virulence genes, which are common traits in AIEC strains (10, 15). This strain set is, of course, biased toward strains with characteristics frequently found in AIEC. However, this was intended, as we aimed to increase the chance to identify the AIEC phenotype among strains from different animal species rather than to provide prevalence data.

Table 1.

Origin and characteristics of the 79 animal ExPEC strains included in this studya

Strain Host species Pathotype Disease Serotype ST ST complex Ancestral group ADH_I
 INV_I
 REPL_I
 AIEC phenotype
Mean SD Mean SD Mean SD
IMT2312 Chicken APEC Colibacillosis O131:NM 10 STC10 A 0.2 0.1 ND ND −
IMT2488 Chicken APEC Colibacillosis Ont:H4 10 STC10 A 0.4 0.2 0.048 0.030 ND −
IMT9238 Chicken APEC Colibacillosis Ont:H6 10 STC10 A 0.4 0.1 0.022 0.011 ND −
IMT9706 Chicken APEC Colibacillosis O119:Hnt 10 STC10 A 0.3 0.1 0.030 0.014 ND −
IMT5110 Chicken APEC Colibacillosis O149:Hnt 100 STC165 A 0.1 0.1 0.001 0.001 ND −
IMT9712 Chicken APEC Colibacillosis O22:H31 373 STC168 A 3.7 3.6 0.031 0.039 ND −
IMT2358 Chicken APEC Colibacillosis O78:H4 915 None ABD 0.1 0.1 0.008 0.000 ND −
IMT5215 Chicken APEC Colibacillosis O5:H10 93 STC168 AxB1 0.3 0.2 0.019 0.003 ND −
IMT1939 Duck APEC Colibacillosis O78:H51 155 STC155 AxB1 0.3 0.1 0.050 0.049 ND −
IMT2095 Chicken APEC Colibacillosis O8:H19 162 STC469 AxB1 2.7 2.7 0.038 0.010 ND −
IMT5475 Duck APEC Colibacillosis O8:H4 359 STC101 AxB1 0.2 0.1 0.004 0.004 ND −
IMT5494 Duck APEC Colibacillosis O29:H51 359 STC101 AxB1 0.5 0.2 ND ND −
IMT2087 Chicken APEC Colibacillosis O78:H9 23 STC23 B1 0.2 0.2 0.088 0.061 ND −
IMT2125 Chicken APEC Colibacillosis O78:H9 23 STC23 B1 0.1 0.1 0.007 0.005 ND −
IMT2113 Chicken APEC Colibacillosis Ont:NM 101 STC101 B1 0.2 0.2 0.001 0.001 ND −
IMT5124 Chicken APEC Colibacillosis O78:Hnt 369 STC23 B1 0.1 0.1 0.001 0.001 ND −
IMT2097 Chicken APEC Colibacillosis O1:H7 95 STC95 B2 0.3 0.3 0.052 0.015 ND −
IMT2272 Chicken APEC Colibacillosis O2:Hnt 95 STC95 B2 0.2 0.0 0.018 0.007 ND −
IMT2297 Chicken APEC Colibacillosis O2:H5 95 STC95 B2 0.2 0.0 0.047 0.016 ND −
IMT2532 Chicken APEC Colibacillosis O18:H7 95 STC95 B2 0.3 0.2 0.014 0.010 ND −
IMT2537 Chicken APEC Colibacillosis O18:H7 95 STC95 B2 0.2 0.1 0.015 0.009 ND −
IMT2545 Chicken APEC Colibacillosis O1:H5 95 STC95 B2 0.1 0.1 0.001 0.001 ND −
IMT4517 Poultry APEC Colibacillosis O2:H7 95 STC95 B2 0.2 0.2 0.023 0.011 ND −
IMT4533 Chicken APEC Colibacillosis O18:Hnt 95 STC95 B2 0.4 0.4 0.038 0.008 ND −
IMT5211 Chicken APEC Colibacillosis O18:H7 95 STC95 B2 0.2 0.1 0.021 0.020 ND −
IMT5214 Chicken APEC Colibacillosis O1:NM 95 STC95 B2 0.2 0.1 0.001 0.001 ND −
IMT8989 Chicken APEC Colibacillosis O1:H7 95 STC95 B2 0.2 0.0 0.030 0.043 ND −
IMT9232 Chicken APEC Colibacillosis O1:H7 95 STC95 B2 0.7 0.1 0.022 0.016 ND −
IMT9241 Chicken APEC Colibacillosis O2:H4 95 STC95 B2 0.6 0.2 0.018 0.014 ND −
MT78 Chicken APEC Colibacillosis O2:Hnt 95 STC95 B2 6.1 7.0 0.997 0.859 34.6 25 −
IMT5112 Chicken APEC Colibacillosis O6:NM 127 STC127 B2 0.1 0.1 0.000 0.000 ND −
2363 Chicken APEC Colibacillosis Ont:Hnt 135 None B2 0.62 0.16 0.038 0.000 ND −
IMT21073 Chicken APEC Colibacillosis O2:H1 135 None B2 1.83 0.46 0.205 0.092 58 28 −
IMT2295 Chicken APEC Colibacillosis O2:Hnt 135 None B2 0.04 0.05 0.014 0.003 ND −
IMT2288 Chicken APEC Colibacillosis O2:H5 140 STC95 B2 0.4 0.4 0.018 0.006 ND −
IMT4534 Chicken APEC Colibacillosis O2:Hnt 140 STC95 B2 0.2 0.0 0.026 0.005 ND −
IMT5128 Chicken APEC Colibacillosis O2:H5 140 STC95 B2 0.3 0.3 0.028 0.004 ND −
IMT2290 Chicken APEC Colibacillosis O2:H6 141 None B2 1.7 0.2 0.045 0.032 ND −
IMT2477 Chicken APEC Colibacillosis O2:H6 141 None B2 0.2 0.2 0.043 0.005 ND −
IMT5160 Chicken APEC Colibacillosis Orough:H11 141 None B2 0.3 0.1 0.028 0.024 ND −
IMT2112 Poultry APEC Colibacillosis O2:H5 355 STC73 B2 0.3 0.1 0.032 0.003 ND −
IMT9713 Chicken APEC Colibacillosis O125:H10 372 None B2 0.1 0.1 0.002 0.001 ND −
IMT4542 Chicken APEC Colibacillosis O2:Hnt 1168 STC95 B2 0.3 0.0 0.044 0.016 ND −
IMT2111 Chicken APEC Colibacillosis O1:H15 38 STC38 D 1.2 0.4 0.030 0.005 ND −
IMT2487 Chicken APEC Colibacillosis O77:H18 69 STC69 D 0.2 0.0 0.019 0.007 ND −
IMT2282 Chicken APEC Colibacillosis O23:H15 70 None D 0.2 0.0 0.025 0.007 ND −
K416/97-2 Chicken APEC Colibacillosis O2:Hnt 115 None D 1.9 2.6 0.043 0.024 ND −
IMT2294 Chicken APEC Colibacillosis O2:H9 115 None D 0.0 0.0 0.011 0.006 ND −
IMT2261 Chicken APEC Colibacillosis O166:H15 349 STC349 D 8.3 3.1 0.066 0.055 ND −
IMT14972 Dog UPEC UTI Ont:NM 10 STC10 A 0.0 0.0 0.000 0.000 ND −
VB 973164 Pig UPEC UTI O128:NM 10 STC10 A 0.0 0.0 ND ND −
VB 985583 Dog UPEC UTI Ont:NM 10 STC10 A 0.0 0.0 0.000 0.000 ND −
VB 991926 Cat UPEC UTI O49:H32 10 STC10 A 0.0 0.0 0.004 0.004 ND −
VB 905336 Cat UPEC UTI Ont:NM 10 STC10 A 0.8 1.0 0.000 0.000 ND −
VB 993928 Cat UPEC UTI Ont:H35 10 STC10 A 0.1 0.0 0.030 0.013 ND −
IMT15499 Pig UPEC UTI Unknown 880 STC10 A 0.5 0.6 0.011 0.004 ND −
IMT15532 Pig UPEC UTI Unknown 891 STC10 A 0.5 0.6 0.050 0.000 ND −
VB 960678.1 Dog UPEC UTI O19:NM 1254 STC101 AxB1 0.0 0.0 0.000 0.000 ND −
IMT15513 Pig UPEC UTI O86:Hnt 101 STC101 B1 0.4 0.4 0.046 0.016 ND −
VB 996714.1 Dog UPEC UTI O15:H10 101 STC101 B1 0.1 0.0 0.047 0.042 ND −
IMT14958 Cat UPEC UTI O22:H1 73 STC73 B2 0.2 0.3 0.047 0.038 ND −
IMT14966 Dog UPEC UTI O6:H1 73 STC73 B2 0.4 0.5 0.023 0.024 ND −
IMT14980 Cat UPEC UTI O6:H1 73 STC73 B2 0.0 0.0 0.004 0.003 ND −
IMT14995 Cat UPEC UTI O6:H1 73 STC73 B2 0.0 0.0 0.015 0.023 ND −
IMT15033 Cat UPEC UTI O25:H1 73 STC73 B2 0.1 0.1 0.052 0.003 ND −
IMT9096 Cat UPEC UTI O2:H1 73 STC73 B2 0.8 0.9 0.035 0.007 ND −
IMT12556 Dog UPEC UTI O25b:H4 131 None B2 0.6 0.7 0.041 0.008 ND −
VB 977549 Dog UPEC UTI O25b:H4 131 None B2 0.1 0.1 ND ND −
VB 999294 Dog UPEC UTI O25b:H4 131 None B2 0.3 0.2 ND ND −
VB 973707 Dog UPEC UTI O25b:H4 131 None B2 4.3 0.6 ND ND −
VB 984674 Dog UPEC UTI O25b:H4 131 None B2 0.4 0.3 ND ND −
BF 187735 Dog UPEC UTI O25b:H4 131 None B2 0.3 0.2 ND ND −
VB 991463 Dog UPEC UTI O2:Hnt 135 None B2 1.85 0.49 0.103 0.004 976 210 +
IMT15525 Pig ExPEC GTI Ont:H21 101 STC101 B1 0.4 0.5 0.048 0.018 ND −
IMT15459 Pig ExPEC GTI O114:Hnt 101 STC101 B1 0.9 1.2 0.045 0.002 ND −
IMT15466 Pig ExPEC GTI Ont:H21 101 STC101 B1 0.2 0.3 0.063 0.039 ND −
IMT15469 Pig ExPEC GTI Orough:NM 101 STC101 B1 0.5 0.6 0.007 0.006 ND −
IMT15472 Pig ExPEC GTI Ont:H21 101 STC101 B1 0.3 0.4 0.034 0.015 ND −
IMT15497 Pig ExPEC GTI Ont:NM 101 STC101 B1 0.1 0.1 0.001 0.001 ND −
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a

Adhesion index (ADH_I), calculated as the mean number of bacteria per cell, and invasion index (INV_I), calculated as the percentage of intracellular bacteria of total bacteria inoculated, are detailed. Survival/replication index (REPL_I), calculated as the percentage of intracellular bacteria at 24 h postinfection, has been investigated only for those invasive strains. AIEC phenotype is positive (+) if ADH_I ≥ 1, INV_I ≥ 0.1, and REPL_I ≥ 100. Abbreviations: ND, not determined; UTI, urinary tract infection; GTI, genital tract infection.

Table 2.

Origin and characteristics of 45 animal intestinal pathogenic strains included in this studya

Strain Host species Serotype ST ST complex Ancestral group ADH_I
 INV_I
 REPL_I
 AIEC phenotype
Mean SD Mean SD Mean SD
IMT15384 Dog O6:H1 10 STC10 A 0.28 0.17 0.008 0.006 ND −
IMT15419 Dog Ont:H32 10 STC10 A 1.50 0.42 0.015 0.014 ND −
VB 900719 Dog Ont:Hnt 10 STC10 A 15.25 4.60 0.445 0.049 449 410 +
VB 903359 Dog Ont:NM 10 STC10 A 0.08 0.07 0.002 0.003 ND −
BF 137999 Dog Ont:NM 10 STC10 A 0.06 0.05 0.001 0.001 ND −
VB 904411 Dog Ont:Hnt 10 STC10 A 0.18 0.11 0.028 0.003 ND −
VB 904860 Dog Ont:H37 10 STC10 A 7.93 1.52 1.975 0.177 439 212 +
VB 905637 Dog Ont:NM 10 STC10 A 0.28 0.05 0.002 0.002 ND −
IMT 13347 Swine Unknown 10 STC10 A 20.25 11.67 0.178 0.018 259 95 +
IMT 13359 Swine Unknown 10 STC10 A 1.48 0.11 0.678 0.315 942 138 +
IMT 13398 Swine Unknown 10 STC10 A 3.55 1.39 0.063 0.036 ND −
IMT 13425 Swine Unknown 10 STC10 A 0.01 0.01 0.001 0.001 ND −
IMT 13497 Swine Unknown 10 STC10 A 0.00 0.00 0.001 0.001 ND −
IMT 13473 Swine Unknown 10 STC10 A 0.00 0.00 0.000 0.000 ND −
VB 934275 Dog Ont:NM 617 STC10 A 0.02 0.02 0.005 0.001 ND −
IMT15422 Dog Ont:H37 1238 STC10 A 9.08 2.67 0.235 0.115 609 97 +
IMT15383 Cat O6:Hnt 73 STC73 B2 0.34 0.22 0.310 0.014 477 85 +
IMT15401 Cat O25:NM 73 STC73 B2 4.93 0.39 0.423 0.180 1,153 159 +
IMT15407 Cat O25:H1 73 STC73 B2 3.03 1.66 0.163 0.067 1,399 535 +
IMT15412 Cat O6:H1 73 STC73 B2 1.43 0.67 0.370 0.021 658 169 +
IMT15417 Cat O6:H1 73 STC73 B2 1.60 1.35 0.242 0.173 980 60 +
IMT15418 Cat O25:H1 73 STC73 B2 0.16 0.21 0.040 0.001 ND −
IMT15423 Cat O6:H1 73 STC73 B2 1.17 0.64 0.292 0.183 1,541 190 +
IMT15430 Cat O25:H1 73 STC73 B2 6.39 1.05 0.155 0.000 2,074 1,081 +
IMT15444 Cat O6:H1 73 STC73 B2 1.43 0.18 2.350 0.212 1,013 985 +
IMT15445 Cat Unknown 73 STC73 B2 3.28 0.81 0.238 0.138 741 494 +
IMT15447 Cat O25:H1 73 STC73 B2 1.04 0.24 1.450 0.424 91 14 −
IMT15448 Cat O6:H1 73 STC73 B2 1.08 0.55 0.580 0.312 777 456 +
VB 900990 Cat O6:H1 73 STC73 B2 4.70 1.20 0.463 0.187 604 61 +
VB 901947 Cat O22:Hnt 73 STC73 B2 2.23 0.25 0.150 0.035 1,060 603 +
VB 901857 Cat O6:H1 73 STC73 B2 0.16 0.22 0.390 0.156 762 408 +
VB 902289 Cat O25:H1 73 STC73 B2 1.35 0.14 1.375 0.247 1,287 409 +
VB 902302 Cat O6:H1 73 STC73 B2 5.20 3.32 0.248 0.032 83 23 −
VB 902827 Cat O25:H1 73 STC73 B2 1.03 0.32 0.245 0.127 647 286 +
VB 903648 Cat O25:H1 73 STC73 B2 4.45 3.61 1.378 0.735 345 138 +
BF 138088 Cat O6:H1 73 STC73 B2 3.68 0.53 0.145 0.014 757 324 +
VB 905481 Cat O25:H1 73 STC73 B2 1.93 0.53 1.268 0.848 522 349 +
BF 138148 Cat O25:NM 73 STC73 B2 0.12 0.06 0.018 0.004 ND −
IMT15380 Dog O6:H1 73 STC73 B2 1.52 0.77 0.395 0.085 1,504 548 +
IMT15424 Dog O22:H1 73 STC73 B2 1.04 0.09 0.234 0.164 639 17 +
IMT15441 Dog O6:NM 73 STC73 B2 0.12 0.09 0.004 0.002 ND −
VB 900402 Dog Ont:H1 73 STC73 B2 2.18 1.10 0.039 0.024 ND −
VB 900782 Dog O25:H1 73 STC73 B2 1.50 0.28 0.830 0.844 1,159 847 +
VB 901616 Dog O25:H1 73 STC73 B2 0.37 0.39 0.079 0.075 ND −
VB 903606 Dog O6:H1 73 STC73 B2 2.38 0.95 0.026 0.006 ND −
Open in a new tab
a

Adhesion index (ADH_I), calculated as the mean number of bacteria per cell, and invasion index (INV_I), calculated as the percentage of intracellular bacteria of total bacteria inoculated, are detailed. Survival/replication index (REPL_I), calculated as the percentage of intracellular bacteria at 24 h postinfection, has been investigated only for those invasive strains. AIEC phenotype is positive (+) if ADH_I ≥ 1, INV_I ≥ 0.1, and REPL_I ≥ 100. ND, not determined.

As for the ExPEC strain collection, the present study includes 49 APEC strains isolated from colibacillosis in poultry; 24 uropathogenic E. coli strains (UPEC) from cystitis and pyelonephritis in cats, dogs, and pigs; and six strains causing upper genital tract infections in pigs (Table 1) (7). As determined by STRUCTURE analysis of concatenated sequences of the seven housekeeping genes included in MLST analyses (6), the distribution of ancestral groups was 50.6% B2, 17.7% A, 15.2% B1, and 7.6% D. Seven other strains were categorized under hybrid groups AxB1 (7.6%) and ABD (1.3%), which resemble highly recombining strains supposed to have acquired genetic material from all four major phylogenetic groups (16). With regard to the InPEC strain collection, we included 22 strains causing enteritis in cats, 17 in dogs, and six in swine. These strains belonged to phylogroups B2 (64.4%) and A (35.6%) (Table 2).

To identify the AIEC phenotype, we determined the ability of strains to adhere to and to invade intestinal epithelial cells, as well as their capacity to survive and replicate within macrophages by performing gentamicin protection assays over intestine-407 epithelial cells (ATCC CCL-6) and murine J774A1.1 macrophages (ATCC TIB-67), respectively (9). Assays for strains resistant to gentamicin were carried out with kanamycin at a final concentration of 100 μg·ml−1. All assays were performed on 24-well plates in triplicate. AIEC prototype strain LF82 and nonpathogenic E. coli strain C600 were used as controls.

In parallel, we performed correspondence analysis to determine whether or not a particular distribution of virulence-associated genes correlated with each pathotype (Canoco software version 4.5 for Windows; biplot scaling). We compared the 124 animal strains included in the present study with 22 human intestinal AIEC and 37 human mucosa-associated E. coli (non-AIEC) strains from a previous study (10). Fifty-two virulence genes were included in the analysis after removing genes that were present in all the strains or in a single strain.

Only one out of the 79 animal ExPEC strains analyzed shared the AIEC phenotype despite the mindful selection of strains. Approximately 16% of APEC strains were adherent to intestine-407 cells, but only two were invasive (IMT21073 and BEN2332, formerly named MT78). These results are in agreement with those of a previous study that described the adhesion and invasion ability of the MT78 strain to avian heterophils and macrophages (12). Among the UPEC and genital tract infection-associated strains, 10.2% were classified as adherent, but only UPEC strain VB 991463, which belonged to the same phylogroup (B2) and sequence type (ST135) as the LF82 strain, presented the complete AIEC phenotype. These results provided evidence for a particular identity of the AIEC pathotype, since animal ExPEC strains, although being genetically similar to AIEC strains, did not share the AIEC phenotype.

Contrary to animal ExPEC, up to 57.7% of preselected animal InPEC strains phenotypically resembled the AIEC pathotype, and a higher proportion (72.4%) was observed among B2 isolates. These InPEC strains caused enteritis to animals but genetically resembled ExPEC strains rather than classical intestinal pathogenic E. coli. Similarly, the AIEC pathotype is genetically similar to ExPEC but different from diarrheagenic E. coli pathovars and has been particularly related to ileal Crohn's disease and granulomatous colitis in boxer dogs, a disease which highly resembles ulcerative colitis and Crohn's disease in humans (2, 4, 9, 15). To our knowledge, this is the first study demonstrating the occurrence of AIEC in cats, even though these animals also suffer from inflammatory bowel disease (1). Although the nonarbitrary strain selection might have accounted for the exceptional high frequency of AIEC among intestinal strains from cats (81.8%), it stays a matter of concern that warrants future investigations.

Correspondence analysis of virulence gene (VG) profiles showed that no particular VG distribution was associated to a certain group of strains (see Fig. 1). Strains clustered with regard to their phylogenetic affiliation (data not shown) but not by their extraintestinal/intestinal origin, human/animal host source, or AIEC phenotype. Human and animal AIEC strains appeared scattered in the plot, indicating their genetic diversity and the lack of a genetic marker for the identification of that pathotype. However, we found malX and kpsMTII more prevalent in animal and human strains with the AIEC phenotype (71.4% of AIEC-like versus 47% of non-AIEC [P = 0.003] and 71.4% versus 52% [P = 0.013], respectively, taking into account a total of 173 strains used for correspondence analysis). These virulence genes have already been detected in the LF82 strain and four other AIEC strains from human intestine, two human UPEC and two sepsis-causing E. coli strains also with the AIEC phenotype, and three AIEC strains from boxer dogs (10, 15).

Fig. 1.

Fig. 1.

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Correspondence analysis of the distribution of 52 virulence-associated genes in 79 animal ExPEC, 45 animal InPEC (this study), 22 human AIEC, and 37 human mucosa-associated non-AIEC strains (data obtained from reference 10). Eigenvalues (Eig.) and percentages of variance are provided for each axis.

The detection of AIEC strains in the intestinal tracts of cats, dogs, and swine provides further support for the absence of host specificity of this pathotype, which has already been observed by Simpson et al. in boxer dogs (15). They show that the AIEC pathotype is disease specific rather than host specific. We hold up this hypothesis because the InPEC strains included in the present study were isolated from animals with enteritis. Unfortunately, detailed data on the clinical history of the strains were not available, and thus it was not possible to correlate the presence of AIEC with the type or severity of intestinal disease. Nevertheless, our data support the association of AIEC with an altered intestinal state possibly linked to inflammatory bowel disease. Finally, the presence of AIEC in the intestine of several animal species suggests a putative zoonotic risk. Further studies analyzing the real prevalence of AIEC in well-characterized diseased animals are needed in order to detect putative reservoirs of AIEC strains, even in the intestine of asymptomatic carriers, and to evaluate the dimension of the risk with respect to the implementation of prevention and control measures and thus to public health.

Acknowledgments

We are grateful to Maryvonne Dho-Moulin for kindly providing APEC strain MT78. We also thank Ivonne Stamm and Peter A. Kopp from the IDEXX VetMedLab (Ludwigsburg, Germany) for providing E. coli strains from animal sources.

This work was funded by the Spanish Ministry of Education and Science (SAF2010-15896) and supported by the ANR in the frame of ERA-NET Pathogenomics and from the Deutsche Forschungsgemeinschaft (German Research Foundation; WI 1436/5-3).

Footnotes

▿

Published ahead of print on 24 June 2011.

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