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Journal of Clinical Microbiology, March 1999, p. 778-781, Vol. 37, No. 3
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Clonal Diversity of Chilean Isolates of
Enterohemorrhagic Escherichia coli from Patients with
Hemolytic-Uremic Syndrome, Asymptomatic Subjects, Animal
Reservoirs, and Food Products
Maritza
Rios,1
Valeria
Prado,1,*
Michele
Trucksis,2
Carolina
Arellano,1
Consuelo
Borie,3
Marcela
Alexandre,4
Alberto
Fica,1 and
Myron M.
Levine2
Programa de Microbiología y
Micología, Instituto de Ciencias Biomédicas, Facultad de
Medicina, Universidad de Chile,1
Laboratorio de Microbiología, Departamento de Medicina
Preventiva Animal, Facultad de Ciencias Veterinarias y Pecuarias,
Universidad de Chile,3 and
Servicio de
Salud Metropolitano del Ambiente,4 Santiago,
Chile, and
Center for Vaccine Development, University of
Maryland School of Medicine, Baltimore, Maryland
212012
Received 8 June 1998/Returned for modification 24 July
1998/Accepted 21 October 1998
 |
ABSTRACT |
To determine clonal relationship among Chilean enterohemorrhagic
Escherichia coli (EHEC) strains from different sources
(clinical infections, animal reservoirs, and food), 54 EHEC isolates
(44 of E. coli O157, 5 of E. coli O111, and 5 of E. coli O26) were characterized for virulence genes by
colony blot hybridization and by pulsed-field gel electrophoresis
(PFGE). By colony blotting, 12 different genotypes were identified
among the 44 E. coli O157 isolates analyzed, of which the
genetic profile stx1+
stx2+ hly+
eae+ was the most prevalent. All human O157 strains
that were associated with sporadic cases of hemolytic-uremic syndrome
(HUS) carried both the stx1 and
stx2 toxin-encoding genes and were
eaeA positive. Only 9 of 13 isolates from human controls
were stx1+
stx2+, and 8 carried the
eaeA gene. Comparison of profiles obtained by PFGE of
XbaI-digested genomic DNA showed a great diversity among
the E. coli O157 isolates, with 37 different profiles among 39 isolates analyzed. Cluster analysis of PFGE profiles showed a wide
distribution of clinical isolates obtained from HUS cases and
asymptomatic individuals and a clonal relationship among O157 isolates
obtained from HUS cases and pigs. Analysis of virulence genes showed
that a correlation exists among strains with the genotype
stx1+
stx2+ eae+
and pathogenic potential. A larger difference in the PFGE restriction patterns was observed among the EHEC strains of serogroups O26 and
O111. These results indicate that several different EHEC clones circulate in Chile and suggest that pigs are an important animal reservoir for human infections by EHEC. Guidelines have been proposed for better practices in the slaughter of animals in Chile.
| |
TEXT |
Enterohemorrhagic Escherichia
coli (EHEC), an important and emergent food-borne pathogen, has
been associated with bloody and nonbloody diarrhea and hemolytic-uremic
syndrome (HUS) (5, 13). In Chilean children, EHEC is the
main cause of HUS, with incidence rates between 3 and 4.2 cases per
100,000 children below the age of 4 years (3, 20). Several
virulence factors contribute to the pathogenicity of EHEC strains,
including Shiga toxin 1 (Stx1) and/or Stx2, an eae locus
that codes for the ability to produce an attaching-and-effacing lesion,
and the EHEC hly operon that encodes an RTX (repeats in
toxin) toxin designated EHEC hemolysin (Hly) and is required for
expression of EHEC fimbrial antigen. EHEC strains belonging to serotype
O157:H7, as well as other serogroups, are also associated with HUS
disease (8, 13).
In the United States, most of the O157:H7 strains associated with human
disease express Stx2, either alone or combined with Stx1
(11). In Chile, E. coli serogroup O157 bacteria
expressing both Stx1 and Stx2 are the microorganisms most frequently
isolated from children with HUS, although strains that express only
Stx1 are also highly prevalent (15). A similar toxigenic
pattern has been determined in EHEC strains obtained from asymptomatic children (15).
Epidemiologic analysis of outbreaks of EHEC strains has shown that
human infections are usually linked to the consumption of improperly
cooked or processed beef (5). Studies carried out in Chile
have suggested that cows and pigs are important animal reservoirs of
this human pathogen; e.g., 34% of the cows and 69% of the pigs
slaughtered in Santiago were colonized with EHEC strains with a toxin
profile similar to that of human isolates (2). O157
represented the most prevalent EHEC serogroup isolated from pigs,
hamburger meat, ground beef, and sausage products purchased from
different supermarkets in Santiago.
To determine clonal relatedness among bacterial isolates of EHEC,
different typing methods have been used (9, 11, 15). Recent
reports have shown that pulsed-field gel electrophoresis (PFGE) typing
has a high degree of discriminatory power and reproducibility, superior
to those of ribotyping and other molecular techniques (9).
In this study, we used colony blot hybridization and PFGE typing to
establish clonal relatedness among EHEC isolates obtained from sporadic
cases of HUS, asymptomatic individuals, animal reservoirs, and food
products, all within Santiago, Chile.
Fifty-four Chilean EHEC isolates were included in this study.
Twenty-three human isolates from sporadic cases of HUS or asymptomatic controls obtained between March 1995 and March 1996. Twenty-three isolates from animals were obtained directly from the intestinal contents of pigs and cows slaughtered in Santiago from January to March
1994 (cows) and in March 1995 (pigs). EHEC strains isolated from eight
food products obtained in October 1996 from hamburger meat, ground
beef, or sausage products sold by different supermarkets in Santiago
were also included. All samples were cultured on MacConkey agar, and 10 colonies per sample were tested for EHEC, both biochemically and by
colony blot hybridization. We considered EHEC any strain containing
genes that code for the production of at least one of the cytotoxins.
Strains identified as EHEC were serogrouped by using commercial
antisera (Probac, São Paulo, Brazil).
The sorbitol phenotypes of bacterial isolates were determined as
previously described (10). Colony hybridizations were
performed as previously described (4), by using biotinylated
probes to detect the presence of the stx1,
stx2, eae, and hly EHEC
virulence genes and including positive and negative controls
(4).
PFGE.
Genomic DNA for contour-clamped homogeneous electric
field electrophoresis was prepared as previously described
(19), with minor modifications. A 2-mm slice of an agarose
plug in which EHEC genomic DNA was embedded was digested for 4 h
with 20 U of XbaI (Gibco BRL) and 20 U of SfiI
(New England BioLabs) for all strains and with 20 U of AvrII
(New England BioLabs) for some strains. Restriction fragments of DNA
were separated on a 1.5% agarose gel by PFGE with a CHEF-DR III
apparatus (Bio-Rad Laboratories). A lambda ladder (New England BioLabs)
was used as a molecular size marker. Southern blot hybridizations from
SfiI-digested chromosomal DNAs of O157 isolates resolved by
PFGE were performed as described by Sambrook et al. (16) by
using a biotinylated CVD434 probe containing the central region of the
eae gene.
Profiles derived from the PFGE analysis with SfiI and
XbaI of O157 serogroup isolates were compared for the
presence or absence of 48.5- to 436.5-kb bands. The analysis of PFGE
patterns was performed by using Statistica version 4.5 from Statsoft
Inc. The resulting matrix was used to construct a dendrographic tree
employing the unweighted pair-group method with arithmetic means method included in this software. The discriminatory abilities of the typing
systems used were estimated by Simpson's index of diversity (D) (6).
The origin and characteristics of the 54 EHEC isolates studied are
summarized in Table
1. Of the 44 O157
isolates, 31 (70.4%)
were
stx1+
stx2+, 10 (22.7%) were
stx1+, and 3 (6.8%) were
stx2+. The
eae locus was
detected in 33 of the 44 O157 isolates, and
the Hly-encoding gene was
detected in 36 of these strains. The
genetic loci
stx1,
stx2, and
eae were found in all five, O26 serogroup
isolates analyzed,
and the Hly-encoding region was detected in
four of these isolates. For
all five of the O111 isolates analyzed,
the genotype was
stx1+
stx2+ eae+,
and three isolates carried the locus encoding EHEC Hly.
All of the O157 strains isolated from symptomatic patients, including
those from sporadic cases of HUS, carried both the
stx1 and
stx2 toxin genes
and were
eaeA positive, while 9 of 13 isolates
from
asymptomatic human controls were
stx1+
stx2+ and 8 carried the
eaeA gene. The locus encoding the production
of hemolysin
was detected in 5 of 8 and 7 of 13 O157 isolates
from HUS cases and
asymptomatic controls, respectively. Of the
O157 porcine strains,
72.7% had a predominating genotype of
stx1+
stx2+ and 94.7% had a predominating
phenotype of
eae+.
By using this typing method, we distinguished 12 different genotypes
among all of the O157 isolates analyzed. The genetic
profile
stx1+
stx2+ hly+
eae+ was the most prevalent (21 of 44 isolates),
followed by the genetic
profile
stx1+
stx2+ hly
eae+ (7 of 44 isolates). A negative sorbitol
fermentation phenotype
was associated with 81% of
stx1+
stx2+ hly+
eae+ O157 isolates and with 100% of human
isolates.
Comparison of E. coli strains by PFGE.
The
profiles of chromosomal DNA fragments generated by using
XbaI were compared in 48 of the 54 isolates (39 strains were serogroup O157) in accordance with the criteria of Tenover et al.
(18). Among the 39 O157 isolates, we found 37 different XbaI PFGE patterns. Thirty-six O157 strains were considered
genetically unrelated because their PFGE patterns showed more than six
nonmatching bands, consistent with the occurrence of more than two
independent genetic events. Only two clinical O157 isolates, obtained
from epidemiologically unrelated HUS cases, showed the same restriction pattern by Xba I-PFGE analysis. This finding was confirmed
by using the restriction enzymes SfiI and AvrII.
By PFGE, we could discriminate between two O157 strains although they
had the same virulence genotype and sorbitol phenotype. Among the O157
isolates of animal origin, two porcine strains (isolated from different animals from different farms) were genetically indistinguishable by
PFGE and by eae RFLP of SfiI-digested chromosomal
DNA. These two porcine strains differed greatly from the clinical
isolates described above.
From the dendrogram analysis of
XbaI-digested strains, we
observed that O157 isolates were distributed among three different
branches of the phylogenetic tree (clusters A, B, and C in Fig.
1). All but one isolate of clinical
origin were in cluster A;
the exception was an isolate from an HUS
case, whereas the majority
of isolates from asymptomatic subjects were
in cluster C (
P =
0.027, Fisher two-tailed test).
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|
FIG. 1.
Dendrogram analysis of Chilean O157 EHEC strains
isolated from food products, animal reservoirs, children with HUS, and
healthy controls. The tree was constructed applying the unweighted
pair-group method with arithmetic means to a matrix resulting from
comparison of XbaI PFGE patterns. A, B, and C are
genetically related clusters of strains. HUS1 to HUS7, EHEC isolates
from HUS patients; C1 to C12, EHEC isolates from asymptomatic patients;
P1 to P11, EHEC isolates from pigs; B1 to B3, EHEC isolates from
bovines; F1 to F6, EHEC isolates from food products.
|
|
Among O157 isolates of animal and food origin, porcine isolates were
located predominantly in cluster A, and isolates of food
and bovine
origin were predominantly in cluster B (
P = 0.0009,
Fisher two-tailed
test).
Analysis of virulence genes revealed a correlation of the
eae+ strains with clusters A and B but not with
cluster C (Table
2).
In strains of
clusters A and B, the predominant genotype was
stx1+
stx2+ hly+
eae+, whereas none of the cluster C isolates carried
the four virulence
genes combined together.
Major differences in PFGE restriction patterns were also observed among
EHEC strains belonging to serogroups O26 and O111,
but because of the
low number of isolates, the dendrographic analysis
was not
performed.
The high discriminatory power of this DNA fingerprinting method was
confirmed by the diversity index, Simpson's
D value,
obtained
for
XbaI PFGE types of EHEC serogroup O157
(
D value of 0.973)
in comparison with the discrimination
based on the presence of
virulence genes (
D value of 0.777).
By using PFGE typing, this
study shows that during the study period,
there was great bacterial
diversity among the EHEC strains of human,
animal, or food
origin.
A relationship between the genetic makeup of EHEC isolates and their
pathogenic potential for humans has been proposed (
11).
Some
investigators have suggested that individuals infected with
Stx2-producing EHEC serogroup O157 are at a higher risk of progress
to
HUS (
7,
11). This hypothesis is not supported by the
toxigenic
profiles of EHEC isolates from Chilean patients with HUS or
acute
diarrhea. In these patients, the cytotoxin profiles were similar,
with a predominant genotype of
stx1+
stx2+ or
stx1+ alone (
3,
14). The
EHEC serogroup O157 strains included
in the present study showed a
predominant genotype of
stx1+
stx2+, genetic characteristics also
detected among porcine strains
and isolates obtained from contaminated
food products. The genotype
stx2+
alone was found in only a few O157 isolates obtained from different
origins. Thus, the role of each Shiga-like toxin in the pathogenesis
of
infection caused by EHEC strains and, more specifically, in
the
development of HUS remains
controversial.
Previous results have shown a clear association between the
enterohemolytic phenotype of EHEC strains and their pathogenic
potential for humans, especially among O157 isolates (
17).
In
this study, we detected the
hly locus in 50 to 60% of
the serogroup
O157 isolates obtained from humans, regardless of the
severity
of the clinical manifestations, suggesting that the
relationship
of the expression of the Hly phenotype with the risk of
developing
HUS needs further
investigation.
The most significant correlation of a specific genotype with HUS
disease was the presence of the
eae locus among O157
isolates;
the
eae locus was detected in 100% of the strains
from HUS cases
versus 61.5% of the strains isolated from the
asymptomatic group
and 17% of the
E. coli O157 isolates
associated with cluster C.
Interestingly, in animal reservoirs, this
genotype was also found
in 100% of colonized pigs while it was absent
among bovine
isolates.
These results support previous findings indicating that in Chile, pigs
appear to be an important animal reservoir for EHEC
strains with a high
pathogenic potential for humans (
2). Our
results of
XbaI PFGE typing analysis of the 39 Chilean O157 isolates
of
human, food, and animal origin support this hypothesis. Most
of the
isolates obtained from pigs clustered with HUS-associated
O157 strains
within the same branch of the phylogenetic tree.
In contrast, O157
isolates from human control cases and of bovine
or contaminated-food
origin were located in different clusters.
Despite the frequent
isolation of EHEC strains from pigs, there
are only a few reports that
associate porcine EHEC with HUS (
1)
or that identify porcine
products like sausages as a source of
infection (
12).
Moreover, a previous report indicating that
a minority of EHEC isolates
from pigs possessed the
eae gene (
1)
contrasts
with our findings, in which all porcine isolates were
eae positive.
Surprisingly, the PFGE analysis of Chilean EHEC isolates demonstrated
greater clonal diversity than expected. Only two clinical
isolates
obtained from epidemiologically unrelated HUS cases and
two isolates of
porcine origin (but from different farms) showed
the same restriction
pattern. By using
XbaI PFGE typing, we could
differentiate
EHEC isolates that share virulence markers identified
by DNA probes,
confirming the high discriminatory power of this
technique.
In conclusion, these results demonstrate that EHEC strains were
widespread in Chile and infect animals and humans, as well
as
contaminate food products. There seems to be simultaneous circulation
of several different EHEC clones in Chile, a country where pigs
appear
to be an important animal reservoir of EHEC strains with
high
pathogenic potential for humans. However, confirmation of
this
hypothesis needs more-detailed molecular microbiological
studies of
clonal relatedness among EHEC strains isolated from
human and pig
reservoirs.
Based on our findings, guidelines have been proposed to the Ministry of
Health for the slaughtering of animals in Chile in
order to reduce the
contamination of meat products with EHEC and
prevent human
infection.
| |
ACKNOWLEDGMENTS |
This research was supported by Proyecto Fondecyt 1950736-95.
We are grateful to Center for Vaccine Development, Molecular
Pathogenesis Structure/Unit Section group members Ying-Kang Deng, Adel
Taalat, and Tim Conn for their valuable help, technical assistance, and
encouragement. We gratefully acknowledge Miguel O'Ryan for critically
reading the manuscript.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Programa
Microbiología y Micología, ICBM, Facultad
Medicina-Oriente, Universidad de Chile, Avenida Condell 303, Santiago,
Chile. Phone or Fax: 562-2045460. E-mail:
vprado{at}machi.med.uchile.cl.
| |
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Journal of Clinical Microbiology, March 1999, p. 778-781, Vol. 37, No. 3
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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