JAC Advance Access originally published online on March 12, 2008
Journal of Antimicrobial Chemotherapy 2008 61(6):1244-1251; doi:10.1093/jac/dkn093
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Original research |
Dissemination of extended-spectrum β-lactamase-producing bacteria: the food-borne outbreak lesson
1 Servei de Microbiologia, Hospital Vall d'Hebron, Barcelona, Spain 2 Departament de Genètica i de Microbiologia de la Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain 3 Servei de Microbiologia, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain 4 Departament de Salut Pública, Universitat de Barcelona, Barcelona, Spain
* Correspondence address. Servei de Microbiologia, Hospital Vall d'Hebron, P. Vall d'Hebron, 119-129, 08035 Barcelona, Spain. Tel: +34-93-2746817; Fax: +34-93-2746801; E-mail: gprats{at}vhebron.net
Received 14 September 2007; returned 2 December 2007; revised 25 January 2008; accepted 16 February 2008
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Abstract |
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Objectives: Commensal and opportunistic bacteria producing extended-spectrum β-lactamases (ESBL-PB) have undergone a broad and rapid spread within the general population; however, the routes of dissemination have not been totally elucidated. The aim of this study was to determine whether individuals involved in an outbreak of acute gastroenteritis, in addition to the enteropathogenic microorganism, share an ESBL-PB as indirect demonstration of its transmission from a common food source.
Methods: From 2003 to 2004 in Barcelona, Spain, stool samples from 905 people involved in 132 acute gastroenteritis outbreaks and 226 food handlers related to the outbreaks were investigated.
Results: In 31 outbreaks, 58 diners carrying one or more ESBL-PB were detected. In 10 outbreaks, two or more diners shared the same ESBL-PB, and in four of them, the strain was shared with the food handlers.
Conclusions: This study provides circumstantial evidence that foods can be a transmission vector for ESBL-PB, probably from two reservoirs, food animals and food handlers.
Keywords: food handling , epidemiology , reservoir
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Introduction |
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The introduction of third- and fourth-generation cephalosporins as therapeutic agents has been followed by the dissemination of different extended-spectrum β-lactamases (ESBLs) that hydrolyse those β-lactam drugs and also monobactam antibiotics. ESBLs have been found in a great number of different bacterial species, but more frequently in Escherichia coli and Klebsiella pneumoniae. ESBL-producing members of both these species are frequently encountered among hospitalized patients as agents of diverse infections such as urinary tract infection, soft tissue infections, peritonitis, sepsis and others. Several reviews regarding the microbiology and clinical and therapeutic aspects of these β-lactamases are available.1–4
It is noteworthy that bacteria carrying these kinds of enzymes not only are found in hospitals but have also undergone a broad and rapid dissemination as commensal bacteria within the general population. Our group has previously communicated studies regarding the dissemination of these β-lactamases among hospitalized patients, ambulatory populations, foods and several animal species in Barcelona.5,6
We previously documented the broad dissemination of two multiresistant E. coli strains, together with Salmonella enterica, in 9 of 22 persons investigated in an outbreak of gastroenteritis.7 Likewise, strains carrying ESBLs have been detected in foods and food animals.5,6,8 Based on such observations, we and others have hypothesized that foods are probably one of the most important vehicles for the dissemination of resistant bacteria within the general population.7,9–12
To address this problem, we postulated that a systematic study of the presence of ESBL-producing bacteria (ESBL-PB) in faeces from individuals involved in outbreaks of gastroenteritis, i.e. persons who have shared a meal, should be a useful method to test our hypothesis. However, we have learnt from previous experiences that, in our setting, for several reasons, it is very difficult to obtain foods from outbreaks that occur in public establishments such as restaurants or summer camps. Consequently, we have resorted instead to studying several foods, particularly meats purchased in retail markets, with the objective of establishing an indirect correlation between bacteria carried by people and foods.
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Materials and methods |
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Outbreaks studied
From 2003 to 2004, 132 outbreaks of acute gastroenteritis were studied. In all outbreaks, stools of the affected individuals were collected by the officers of the Public Health Department after consent. In parallel with the search for a causal microorganism, the presence of enterobacteria carrying an ESBL in faecal samples was also investigated. The total number of affected persons studied was 905, ranging from 2 to 30 individuals per outbreak. In addition, 372 food handlers were investigated, of whom 226 were associated with the outbreaks and 146 were non-outbreak controls. In the case of individuals who were living together, only one representative of each household was studied. Persons who had taken antibiotics in the month prior to the study were excluded. Each outbreak has been identified in the text and tables by a number (outbreak reference number, ON).
Eight hundred and sixty-six samples of different cooked foods (ready to eat) obtained in 2003 from our hospital kitchen were investigated for contamination with ESBL-PB. In addition, 131 raw retail meat samples, including 47 chicken, 30 pork, 22 veal, 20 lamb and 12 rabbits, were purchased in 2004–06 from different grocery stores in Barcelona to evaluate for possible ESBL-PB contamination. No systematic surveillance approach was used; instead, different individuals were invited to purchase meat samples from their usual grocery market at their convenience. The meats were purchased from 52 different markets.
Stool and food samples processing
Stools were transported to the laboratory within 6 h of collection. Each sample was homogenized in peptone water and aliquots of 0.1 mL were plated on MacConkey agar supplemented with 2 mg/L of cefotaxime (MacC-CTX). Plates were incubated at 37°C overnight. The plates were checked by growing an SHV-2-producing K. pneumoniae strain, a TEM-3- and TEM-24-producing K. pneumoniae strain, and a CTX-M-9-producing E. coli strain.6
Twenty-five grams of each food sample, aseptically ground, was placed in 225 mL of peptone water and incubated at 37°C overnight. A volume of 1 mL of this culture was plated on MacC-CTX agar. Plates were incubated at 37°C overnight.
Whenever possible, three morphologically different colonies with appearance of enterobacteria from each MacC-CTX plate were subcultured and identified by conventional methods.13 Enterobacterial repetitive intergenic consensus (ERIC) profiling was used for clonal delineation of isolates from each plate (discussed subsequently). One representative per clone per plate was selected for the final study.
Antimicrobial susceptibility testing
Susceptibility to 23 antibiotics was determined by disc diffusion, following the CLSI recommendations for Enterobacteriaceae.14 Suggestive evidence of ESBL production was defined as synergy between co-amoxiclav and at least one of the following antibiotics: cefotaxime, ceftazidime, aztreonam or cefepime. The MICs of cefotaxime and ceftazidime, with and without clavulanic acid, were determined subsequently by the Etest (AB Biodisk, Solna, Sweden).
Detection and characterization of β-lactamases by isoelectric focusing, PCR amplification of DNA and sequencing were performed as previously described.15–17
Clonal relationships among the E. coli isolate within each stool and food samples were assessed by studying ERIC genomic DNA profiles, as generated using primers ERIC1 and ERIC2, as previously described.18 Images from ERIC-PCR were assessed by visual inspection.
Pulsed-field gel electrophoresis
Bacterial DNA was prepared as previously described and restricted with XbaI.19 Electrophoresis of the digested DNA was performed with a CHEF DRII System (BioRad, Richmond, CA, USA). Images from ethidium bromide-stained pulsed-field gel electrophoresis (PFGE) were captured digitally (Gel Compar II, version 3.0; Applied Maths, Sint-Martens-Latem, Belgium). For the purposes of the study, only isolates with indistinguishable profiles were considered to represent the same clone. The identity of isolates that could not be typed by PFGE (DNA smear) was established by comparing the phylogroup, ERIC pattern, susceptibility to 23 antibiotics and 15 virulence factors (discussed subsequently).
O and H antigens were determined at Laboratorio de Referencia de E. coli, Facultad de Veterinaria, Lugo, Spain, by agglutination employing all available O (O1–O185) and H (H1–H56) antisera.20
E. coli phylogenetic and virulence factor analysis
The E. coli phylogenetic group (A, B1, B2 and D) was determined by a triplex PCR method.21 Fifteen virulence genes associated with extraintestinal pathogenic E. coli were characterized by using an established multiplex PCR assay.22
Comparisons of associations were done using the 
2 test when all expected cell frequencies were 
5, 2 with Yates' correction when any expected cell frequency was 3 or 4, and Fisher's exact test (two-tailed) when any expected cell frequency was <3. Statistical analysis was performed with SPSS version 12.0 (SPSS Inc., Chicago, IL, USA), with significance set at P < 0.05.
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Results |
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Outbreaks
Among the 132 outbreaks studied, in 31 outbreaks (23.5%) one or more of the investigated subjects (or diners or individuals) carried one or more ESBL-producing bacteria. Likewise, among the 905 individual subjects investigated in all outbreaks, 58 diners (6.4%) carried one or more ESBL-PB. The 31 outbreaks in which diners carrying ESBL-PB were detected were classified into two groups, according to the number of diners identified as carrying ESBL-PB: (i) only one ESBL-PB-positive diner and (ii) two or more such diners.
Group 1 (a single ESBL-PB-positive diner per outbreak) included 20 outbreaks and accounted for 168 total diners (range, 2–30 diners per outbreak) (Table 1), only 20 (12%) of whom carried ESBL-PB. In two of these outbreaks (ON 6 and ON 23), two strains, each carrying a different ESBL, were detected in the same diner. All 22 ESBL-PB strains were E. coli. In three of the six outbreaks within this group in which food handlers could be investigated (ON 31, 86 and 121), food handlers exhibited the same strains and β-lactamases as did the ESBL-PB-positive diners (Table 1).
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Group 2 (with two or more ESBL-PB-positive diners per outbreak) included 11 outbreaks and accounted for 107 total diners (range, 2–21 diners per outbreak), 37 (34.6%) of whom carried ESBL-PB (Table 2). In five outbreaks (ON 33, 48, 88, 95 and 173), two carriers were detected; in three outbreaks (ON 54, 140 and 179), three carriers were detected; and in the last three outbreaks (ON 16, 30 and 107), five, six and seven carriers, respectively, were detected. One individual carried simultaneously two ESBL-PB and another carried four (Table 2). Altogether, 41 ESBL-PB were detected: 38 were E. coli and 3 were K. pneumoniae. The characterized ESBLs included CTX-M-14 (16 strains), CTX-M-9 (15 strains), SHV-12 (4 strains) and TEM-52, CTX-M-1 and CTX-M-32 (2 strains each).
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In each of the five outbreaks with two ESBL-PB-positive diners, both implicated diners shared the same strain with the same ESBL. In one such outbreak (ON 48), one diner actually carried four distinct ESBL-PB (exceptionally four colonies were studied because they had clearly different morphotypes); one, which produced TEM-52, was shared with the outbreak's other implicated diner.
Each of the three outbreaks with three ESBL-PB-positive diners exhibited a unique sharing pattern of strains and ESBLs among the implicated diners. In ON 140, all three diners shared the same strain, with the same ESBL (K. pneumoniae with CTX-M-9). In contrast, in outbreak ON 54, two diners had the same strain and ESBL (E. coli with CTX-M-14), whereas the third had a different strain and ESBL (E. coli with CTX-M-9). Finally, in ON 179, all three individuals had a unique strain and ESBL (E. coli with CTX-M-9, SHV-12 and CTX-M-14).
In the outbreak with five ESBL-PB-positive diners (ON 16), two diners (D1 and D4) shared the same strain and ESBL (SHV-12). Two other diners (D3 and D5) shared a different strain and ESBL (CTX-M-14). Although both strains from the latter two diners were non-typeable by PFGE, they shared the same ERIC profile, phylogroup (Table 2), susceptibility pattern and combination of virulence factor genes (among the 15 evaluated) (data not shown). The fifth diner carried a different strain producing CTX-M-14 ESBL.
In the outbreak with six ESBL-positive diners, two diners (D1 and D2) shared the same strain and ESBL (CTX-M-9) (Table 2). The other four diners had different strains, two carrying a CTX-M-9, one CTX-M-14 and another SHV-12.
In outbreak ON 107, all seven diners who shared the meal were positive, carrying ESBL-PB (Table 2). One diner (D1) carried two different strains producing CTX-M-9 and CTX-M-32, respectively. Three additional diners shared the strain carrying CTX-M-9 and one diner shared the strain producing CTX-M-32. The two remaining individuals shared a strain different from the above strains, which produced CTX-M-14. All the isolates except those carrying CTX-M-32 were non-typeable by PFGE. The presumed identity between the strains was supported by their identical ERIC patterns, phylogenetic group (Table 2), susceptibility patterns and virulence factor profiles (data not shown).
In five of the aforementioned outbreaks, it was possible to study the food handlers. In only one outbreak, ON 107, did the food handlers exhibit the same strains as the diners (one handler had CTX-M-9 and the other had the CTX-M-32 producing strain) (Table 2).
Carriage of ESBL-PB was studied also in 372 asymptomatic food handlers. Of these, 146 were consecutively selected from routine controls carried out in 2003–04 by the Public Health Service and were not recently associated with an outbreak of gastroenteritis. In contrast, the other 226 food handlers were studied because they were associated with some of the above-described gastroenteritis outbreaks.
Within the first group of 146 non-outbreak-associated food handlers, 14 (9.6%) carried ESBL-PB; two of them carried two different ESBL-PB each. The 146 food handlers worked in 29 centres, ranging from 2 to 19 food handlers per centre. The 14 ESBL-PB-positive food handlers worked in 7 centres that collectively accounted for a total of 51 food handlers. Thus, 27.5% (14/51) of the food handlers in those centres with at least one ESBL-PB-positive food handler were ESBL-PB carriers. In all cases, the isolates were E. coli. The enzymes were CTX-M-14 (11 subjects), CTX-M-32 (2 subjects), SHV-12 (2 subjects) and CTX-M-1 (1 subject).
In the second group (outbreak-associated), the 226 food handlers were associated with 50 outbreaks out of the 132 studied. In 33 of these outbreaks, both the diners and the handlers were negative for ESBL-PB. In five additional outbreaks, the diners carried an ESBL-PB, but not the food handlers. In six outbreaks, although no diners were carriers, 10 food handlers carried ESBL-PB. All were non-clonal E. coli strains (Table 3). Finally, in 6 of the 31 outbreaks in which diners carried an ESBL-PB, as described earlier (Tables 1 and 2), nine handlers were positive for ESBL-PB, and in four of those outbreaks, the same ESBL-positive strain was found in the food handlers as in the diners (ON 31, 86, 121 and 107) (Tables 1–3).
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Taken together, from 372 food handlers investigated, 33 (8.9%) were carriers of ESBL-PB.
From the 866 different cooked (‘ready to eat’) food samples obtained from our hospital kitchen, only three (0.3%) yielded ESBL-PB, including two salads and a chicken sample. The three ESBL-PB were two E. coli (both CTX-M-14) and one K. pneumoniae (CTX-M-3).
From the 131 raw meat samples purchased from grocery stores, 35 (26.7%) yielded ESBL-PB. Twenty-seven (57.4%) of 47 retail chicken samples were positive, with 10 samples yielding two or three different ESBL-PB, for a total of 38 distinct strains. Seven (58%) of 12 rabbit samples were positive, and in one strain, two ESBLs were produced. One (5%) of 20 studied lamb samples was positive. In contrast, no ESBL-PB was found in the 30 pork and 22 veal samples.
The 38 ESBLs found in chicken were CTX-M-14 (14), CTX-M-9 (12), SHV-12 (6), CTX-M-1 (3), CTX-M-32 (2) and SHV-2 (1). The seven ESBLs found in rabbit included CTX-M-14 (3), SHV-12 (3; in one case associated with another CTX-M-14) and CTX-M-9 (1). The single lamb isolate carried CTX-M-14.
Phylogenetic group of ESBL-producing bacteria
The 96 ESBL-positive E. coli from humans were distributed by phylogenetic group in the descending order of prevalence as follows: group A, 51 (53.1%); group B1, 18 (18.8%); group B2, 15 (15.6%) and group D, 12 (12.5%). The 46 ESBL-positive E. coli isolates from foods exhibited a similar phylogenetic group distribution, i.e. group A, 24 (52.2%); group B1, 16 (34.8%) and group D, 6 (13%), except that group B2 was not encountered among the food isolates.
All strains carrying an ESBL-PB were analysed by PFGE in an effort to detect identical strains within a given outbreak (including the corresponding food handlers) and, possibly, across outbreaks.
Two strains were implicated in several outbreaks each. One was detected in four people from two different outbreaks (ON 86 and ON 88). It belonged to phylogroup A, exhibited serotype O8:H9 and produced CTX-M-14. The two outbreaks appeared to be unrelated, having occurred in two different cities, 75 km apart, in February and March 2004, respectively.
Another strain was isolated from six different individuals in three different outbreaks (ON 31, ON 33 and ON 48). It belonged to phylogroup B2 and exhibited serotype O84:H4. Five of the isolates produced CTX-M-14, but one produced CTX-M-9. The three outbreaks appeared unrelated, having occurred in three cities more than 150 km apart, two in July 2003 and the other in September 2004.
A different strain was recovered from two retail chicken samples that were purchased from two different groceries on separate dates, i.e. 23 and 30 May 2005, respectively. The strain belonged to phylogroup B1, exhibited provisional serotype O26,O100:H25 and produced CTX-M-9 β-lactamase. No strain identity was detected between foods and humans.
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Discussion |
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There is evidence that commensal and potentially opportunistic E. coli can spread broadly within the general population. Some uropathogenic E. coli serotypes have been detected in different parts of the world. For example, E. coli O15:K52:H1, an extraintestinal pathogenic clone, has been detected in England and other European countries, as well as in the USA.23,24 Likewise, representatives of E. coli clonal group A (O11/17/73/77:K52:H18) have been found in different states in the USA and in multiple continents.25,26
Also, there is some evidence that microorganisms from animals can reach men.12,27 In the last several years, a great dissemination of enterobacteria carrying ESBLs has been detected within the healthy, general population.6 This causes great concern because such microorganisms are potential opportunists and also can transfer their resistance genes to other bacteria. However, the mode(s) of transmission of those bacteria within the general population has not been clearly determined.
In 2003, we detected in a summer camp the dissemination of two multiresistant E. coli strains, together with S. enterica, in 9 persons out of 22 investigated in an outbreak of gastroenteritis. We raised the hypothesis that water or foods were probably the vehicles for the simultaneous dissemination of Salmonella and resistant E. coli among the campers.7
Here, we have attempted to study the presence of ESBLs in individuals (diners) involved in food-borne outbreaks, in food handlers associated with those outbreaks, in food handlers not associated with food outbreaks and in the consumed foods. However, for several insurmountable reasons, it has not been possible for us to obtain a significant number of foods related to the outbreaks. Consequently, we have purchased different kinds of meats from several butcher shops in the hope of gaining insights into the prevalence of ESBL-PB contamination of foods.
In 2001 and 2002, the prevalence of ESBLs among patients admitted in our hospitals and within the general population in our city was 1.7% and 3.3%, respectively, but in 2003, the prevalence in both groups increased to 1.9% and 6.6%, respectively.6,17
Overall, among the 905 diners involved in the 132 studied outbreaks, we found 58 individuals carrying one or more bacteria producing an ESBL. This represents 6.4% of the studied population, similar to the 6.6% of carriers found concurrently in the general population.6 This is somewhat surprising because according to our initial hypothesis, the frequency of carriers in outbreak situations would be greater than that in the general population. However, the number of outbreaks and individuals involved in the study is quite large, such that a phenomenon of ‘dilution’ is possible.
Among the 20 outbreaks in which only one diner was detected carrying an ESBL-producing strain, in six it was possible to investigate the food handlers, and in three of these (50%) the handlers shared ESBL-PB with the diners. Likewise, of the 11 outbreaks in which two or more diners carried ESBL-PB, in 10 outbreaks (91%) diners from the same outbreak shared one or more ESBL-producing strains, and in one instance, the food handlers also carried the same strain.
The source of the strains found in the diners could be the foods they consumed or the food handlers. In the latter instance, the food handlers could have become colonized initially from handling (or possibly consuming) contaminated foods at their workplace. Thus, it all comes back to food, with or without the food handlers acting as intermediate vectors.
Moreover, the fact that in some outbreaks with diners carrying ESBL-PB, the food handlers were negative whereas in others the handlers shared the resistant strains with the diners suggests the possibility that both food animals and food handlers could be a reservoir of those microorganisms. In fact, 14 (27.5%) of 51 food handlers without a recent relationship to a food-borne outbreak were carriers; this exceeds the 6.6% general population prevalence value (P < 0.001).
Particularly interesting is outbreak 107, involving 7 diners, in which two food handlers each carried a different ESBL-producing strain (CTX-M-9 versus CTX-M-32). All diners carried ESBL-PB. Three had CTX-M-9-producing strains, one had a CTX-M-32-producing strain and the other had both these variants, whereas two additional diners shared a different CTX-M-14-producing strain. It is evident that, in contrast to outbreaks with few contaminated diners, in other outbreaks, like this one, a massive dissemination of ESBL-PB could be produced.
Nosocomial outbreaks of bacteria producing ESBLs have been described.1,4,28 However, the detection of infections caused by clonal strains within the ambulatory population has been less evident.29 In this study, we have been able to detect two E. coli strains, O8:H9 and O84:H4, in different outbreaks, evidence that probably some clones spread consistently within the population. Five of the six strains of the O84:H4 serotype produced CTX-M-14 and the other produced CTX-M-9, which is in accord with the high mobility observed in the genetic elements encoding ESBLs.19
The prepared foods had a low prevalence of contamination by ESBL-PB (3 of 866 samples). In contrast, the fresh foods purchased in groceries had a high prevalence of ESBL-PB (26.7%). Particularly frequently contaminated was retail chicken (57.4% of the samples). Among the 131 food items studied, only two retail chicken samples, from two different markets, shared an ESBL-producing strain, which was from provisional serotype O26,O100:H25. The other retail meats did not share any strains; therefore, cross-contamination in the groceries was not detected. The high prevalence of contaminated meats is probably an increased risk for food handlers' carriage and also for diners who could ingest the bacteria by eating the contaminated foods directly or through cross-contamination of non-cooked foods (e.g. salads), as in enteropathogenic bacteria.30
All but three ESBL-PB detected in humans were E. coli. Seven of the nine different ESBLs detected among the human-source E. coli were also detected in foods and accounted for all of the food-source ESBLs identified. In contrast, five strains isolated from humans produced a β-lactamase not detected in foods: three had CTX-M-15 and two had TEM-52. Interestingly, four of the latter five strains were from phylogenetic group B2, whereas no group B2 strain was isolated from foods in this study. E. coli phylogroups A and B1 are highly adapted to animals and B2 to men. Taking into account the strains' phylogenetic origin, it is probable that in our study the majority of strains carrying ESBLs originated in food animals, whereas a small minority were of human origin.8
A limitation of this study has been the impossibility of obtaining the actual foods manipulated by the food handlers and consumed by the diners involved in the outbreaks. Had this been possible, it would have allowed the opportunity to directly confirm the hypothesis that the food is a vehicle for the dissemination of resistant bacteria within the general population, as happens with the enteropathogenic bacteria, by cross-contamination between raw meats and raw vegetables.
In conclusion, this study provides circumstantial evidence that foods are a transmission vector for ESBL-PB, probably from two reservoirs: food animals and food handlers. On the basis of these results, the magnitude of this mode of transmission in comparison with other possible transmission routes should be determined in future studies. Perhaps, until the reservoirs can be eliminated, if this is possible, foods should be subject to a control programme for resistant bacteria, as is now done for intestinal pathogenic bacteria.
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This work was supported by grant from the Fondo de Investigación Sanitaria (PI020358, PI020372 and PI020918) and from the Ministerio de Sanidad y Consumo, Instituto de Salud Carlos III, Spanish Network for the Research in Infectious Diseases (REIPI RD06/0008). S. L. received a grant from the Institut de Recerca Hospital Universitari Vall d'Hebron.
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None to declare.
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Acknowledgements |
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We are grateful to J. R. Johnson (Minneapolis VA Medical Center, Minneapolis, MN, USA) for critically reading and providing helpful comments during the writing of this manuscript. We thank Jesús E. Blanco (Laboratorio de Referencia de E. coli. Facultad de Veterinaria, Lugo, Spain) for the determination of O and H antigens.
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References |
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