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Journal of Clinical Microbiology, December 1998, p. 3609-3613, Vol. 36, No. 12
Departamento de Microbiologia, Imunologia e
Parasitologia, Universidade Federal de São Paulo, Escola Paulista
de Medicina, São Paulo, S.P., Brazil, CEP
04023-0621;
Instituto da Criança,
Hospital das Clínicas, Faculdade de Medicina da
Universidade de São Paulo, São Paulo, S.P., Brazil, CEP
05403-9002; and
Foodborne and
Diarrheal Diseases Branch, Centers for Disease Control and
Prevention, Atlanta, Georgia 303333
Received 8 June 1998/Returned for modification 23 July
1998/Accepted 21 September 1998
The correlation between various adherence patterns and
adherence-related DNA sequences in Escherichia coli
isolates from 1- to 4-year-old children with and without diarrhea in
São Paulo, Brazil, was evaluated. A total of 1,801 isolates
obtained from 200 patients and 200 age-matched controls were studied.
The adherence patterns found were classified as diffuse, aggregative,
aggregative in a 6-h assay, aggregative predominantly in coverslips,
localized, localized-like, and noncharacteristic. In general, the DNA
sequences used as probes showed excellent specificities (>93%), but
their sensitivities varied. Thus, the results of bioassays and assays with DNA probes normally used to search for adherent E. coli did not correlate well, and the best method for the
identification of these organisms in the clinical research setting
remains controversial. Isolates presenting diffuse adherence or
hybridizing with the related daaC probe, or both, were by
far the most frequent in patients (31.5, 26.0, and 23.0%,
respectively), followed by isolates presenting aggregative adherence or
hybridizing with the related EAEC probe, or both (21.5, 13.0, and
10.5%, respectively). None of the different combinations of adherence
patterns and adherence-related DNA sequences found were associated with
acute diarrhea.
The first step in the establishment
of the diarrheal diseases caused by the various categories of
diarrheagenic Escherichia coli is adherence to epithelial
cells of the intestinal mucosa. In vitro assays with eukaryotic cell
lines (HeLa and HEp-2 cells) have identified three distinct adherence
patterns among fecal isolates of E. coli: localized,
diffuse, and aggregative (37, 38, 41). Localized adherence
(LA) is characterized by formation of bacterial microcolonies on a
restricted area(s) of the cell surface, while diffuse adherence (DA) is
the scattered attachment of bacteria over the whole surface of the cell
(41). The pattern of aggregative adherence (AA) consists of
bacterial attachment to the cells and the intervening cell growth
surface in a stacked brick-like lattice (37).
The LA pattern was first detected in strains classified as
enteropathogenic E. coli (EPEC) among serogroups
associated with outbreaks of infantile diarrhea (41).
Although E. coli strains exhibiting DA (DAEC) have been
isolated at similar frequencies from feces of infants and young
children with acute diarrhea and nondiarrheic controls in some
populations (3, 10, 11, 14, 18), they were significantly
associated with diarrhea in other settings (1, 17, 24, 29,
33). E. coli strains showing AA, termed
enteroaggregative E. coli (EAEC), have been linked to
sporadic persistent diarrhea (3, 4, 7, 10, 13, 26, 27, 44)
and to outbreaks of diarrhea in both developing and developed countries
(8, 12, 28, 43). However, the role of EAEC in acute diarrhea
is still controversial: some studies have shown a correlation (7,
23, 25, 27, 34, 37), but others (1, 3, 6, 10, 11, 13-15,
17, 18, 24, 26, 29, 33, 44) have not.
DNA probes derived from adherence-related sequences have been
constructed (2, 5, 16, 31, 36) and used in hybridization assays for the detection of the different established and putative categories of diarrheagenic E. coli in many
epidemiological studies.
We evaluated the relationship between the LA, DA, and AA patterns and
hybridization with adherence-related DNA sequences and tested children
1 to 4 years old with and without acute diarrhea for the presence of
adherent E. coli strains.
Patients.
Rectal swab specimens were collected from 200 children with acute ( Microbiologic methods.
Adenovirus, Aeromonas
spp., thermophilic Campylobacter, Salmonella
spp., Shigella spp., Yersinia enterocolitica, and
rotavirus were searched for by standard methods (20, 30).
Five lactose-fermenting and any non-lactose-fermenting colonies typical
of E. coli were selected from the isolation plates.
Biochemically confirmed E. coli isolates were stored in
15.0% glycerol at HeLa cell adherence assays.
The HeLa cell adherence assays
were performed as described by Cravioto et al. (9) with HeLa
cells grown to 60% confluence and a single infection period of 3 h. Weakly adherent and nonadherent isolates were retested by the same
method with an additional incubation period of 3 h (6-h assay)
(9). The following E. coli strains were
included as controls: E2348/69 (LA) (36), C1845 (DA)
(5), and 0431-4/85 (AA) (18). Strains were tested
in duplicate and were examined blindly by immersion microscopy.
Search for adherence-related DNA sequences in E. coli.
The following specific DNA probes were used: daaC
(associated with the biogenesis of F1845, a fimbrial adhesin involved
in DA), a 350-bp PstI fragment of pSLM852 (5);
EAEC (EAEC adherence plasmid), a 1-kb EcoRI-PstI
fragment of pCVD432 (2); EAF (EPEC adherence factor), a 1-kb
BamHI-SalI fragment derived from plasmid pMAR2
(36); bfpA (encoding the subunits of a fimbrial
adhesin of EPEC strains, termed the bundle-forming pilus), an 852-bp
EcoRI fragment of pMSD207 (16); and
eaeA (encoding intimin, an outer membrane protein involved
in the attaching-effacing lesions promoted by EPEC and some STEC
strains), a 1-kb SalI-KpnI fragment from plasmid
from pCVD434 (31). The fragment probes were labeled with
[ Statistical analysis.
Analysis of patients and controls
maintained the matched pairs and used the Pike-Morrow adaptation of the
Mantel-Haenszel test to calculate P values (42).
Epi-Info 6.02 was used to perform the calculations.
E. coli adherence to HeLa cells.
The
adherence patterns of 273 isolates could not be determined because they
promoted complete detachment of the HeLa cell monolayers in the 3-h
assays. Among the remaining 1,801 E. coli isolates
tested (879 from patients and 922 from controls), 47.0% were
nonadherent (NA; i.e., sparse bacteria adhering to <1% of the cells
in the 6-h assay). The adherence patterns of the other isolates are
presented in Table 1.
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Adherence Patterns and Adherence-Related DNA
Sequences in Escherichia coli Isolates from Children with
and without Diarrhea in São Paulo City, Brazil
ABSTRACT
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
7 days) diarrhea (patients) and 200 children who
had not had any gastrointestinal signs or symptoms during the 30 days prior to collection (controls). These children were selected by a
computer-generated random-number table from among 505 patient-control pairs obtained for a study on the etiology of acute diarrheal diseases
(19). The population analyzed consisted of children visiting
the emergency room of the Hospital Infantil Menino Jesus, São
Paulo, Brazil, for medical attention between April 1989 and March 1990;
most children were of low socioeconomic status. Controls were matched
with case patients in the following age groups: 12 to 23, 24 to 35, and
36 to 59 months.
70°C. All E. coli isolates were
tested with specific DNA probes designed to detect enterotoxigenic
E. coli (ETEC) (LT-I, LT-II, ST-Ip, ST-Ih, and ST-II
probes), enteroinvasive E. coli (EIEC) (Inv probe), and Shiga-toxin-producing E. coli (STEC) (Stx1 and Stx2 probes),
as described previously (22).
-32P]dATP and used in colony hybridization assays
performed under stringent conditions as described by Maas
(35).
RESULTS
Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
TABLE 1.
Relationship between hybridization with DNA probes for
adherence-related sequences and patterns of adherence to HeLa cells
of E. coli isolated from children with and
without diarrhea
Correlation between adherence patterns and hybridization with adherence-related DNA probes. The relationship between the distinct adherence patterns detected and hybridization with specific DNA probes found in this study is presented in Table 1. The daaC probe reacted with 202 of 321 isolates with DA (sensitivity, 62.9%) and with 99 isolates that were NA or that presented adherence patterns distinct from DA (specificity, 93.3%). The EAEC probe detected 190 of the 256 isolates with AA and 5 of the 132 isolates with AAcs (sensitivity, 47.0%) and reacted with only 29 isolates showing none of the different AA types (specificity, 97.9%). The eaeA probe reacted with all isolates with LA and LAL (sensitivity, 100.0%) and with 60 non-LA- and non-LAL-producing isolates (specificity for the detection of LA- and LAL-producing E. coli, 96%). All isolates with LA hybridized with the EAF and bfpA probes, whereas none of the isolates with LAL reacted with the EAF probe, and only five (35.7%) isolates reacted with the bfpA probe. Most (60.3%) of the 273 cytodetaching isolates did not hybridize with any of the probes used.
Prevalence of adherence patterns and adherence-related DNA sequences in patients and control children. The distribution of the E. coli isolates showing different patterns of adherence or related DNA sequences in patients and controls is presented in Table 2. Approximately 50% of the children studied carried more than one type of isolate. The statistical analysis of the association with diarrhea was performed for those children in whose stools none of the other pathogens were identified (adenovirus, Aeromonas, Campylobacter, EIEC, ETEC, rotavirus, Salmonella, Shigella, and STEC).
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DISCUSSION |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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In this study we analyzed the correlation between different adherence patterns and the presence of adherence-related DNA sequences in E. coli isolates from diarrheic and control children. The adherence-related DNA probes used showed excellent specificities (>93.0%), but their sensitivities varied. The low sensitivities of the daaC and EAEC probes found in this study (62.9 and 47.0%, respectively) are in accordance with those found in other field studies and confirms the heterogeneous nature of the DAEC and EAEC categories (2, 11, 13, 17, 29). It is interesting that none of the isolates that showed AA6h reacted with the EAEC probe; whether these isolates comprise a homogeneous population remains to be established. Furthermore, all 56 isolates that were both EAEC and daaC positive produced AA but not DA, and the significance of daaC in these isolates is under investigation. All isolates with LA carried eaeA, bfpA, and EAF, whereas all isolates with LAL carried eaeA (100.0%) and occasionally bfpA (35.7%). So far, the distribution of bfpA has not been extensively analyzed, but this probe is considered to be more sensitive than the EAF probe in detecting LA-producing E. coli (16). However, our data suggest that both probes are equally sensitive in detecting LA.
The different combinations of adherence patterns and adherence-related sequences found in this study demonstrated that the results obtained with the DNA probes and by the bioassays normally used to search for DAEC and EAEC do not correlate well. Moreover, although adherence to HEp-2 and HeLa cells has been used as the "gold standard" assay for the detection of these categories of isolates, variations in the AA (29, 32) and LA (22, 40) patterns are occasionally reported, and thus, the best method of identifying these organisms in the clinical research setting remains controversial.
None of the different adherence patterns or adherence-related DNA sequences, or a combination of both, were associated with acute diarrhea in children 1 to 4 years old in São Paulo. This lack of association was observed even when the data for any of the three age groups studied (12 to 23, 24 to 35, and 36-59 months) were analyzed (data not shown).
The children studied here were selected from a larger population in which Shigella and rotavirus were the most frequent pathogens found (19). Although DAEC and EAEC were very frequently found in these children, they were not associated with acute diarrhea, suggesting that both categories are heterogeneous and each comprises pathogenic and nonpathogenic strains or that the high level of asymptomatic carriage of DAEC and EAEC, often observed with other well-established enteropathogens (20), masks an association with the disease in our population. The low incidence of E. coli with LA found in this study is probably due to differences in the risk factors that these children have (39), since LA is mainly detected among strains of EPEC serotypes, which prevail in the first year of life (21).
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ACKNOWLEDGMENTS |
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We are indebted to J. B. Kaper, M. M. Levine, J. A. Girón, and S. L. Moseley for providing the probes used in this study, to B. E. C. Guth for critical reading of the manuscript, and L. R. M. Marques for helpful suggestions.
This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Financiadora de Estudos e Projetos/Ministério da Ciência e Tecnologia/Programa de Apoio a Núcleos de Excelência (FINEP/MCT/PRONEX).
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FOOTNOTES |
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* Corresponding author. Mailing address: Departamento de Microbiologia, Immunologia e Parasitologia, Universidade Federal de São Paulo, Escola Paulista de Medecina, Rua Botucatu 862, 3° Andar, São Paulo, S.P., Brazil, CEP 04023-062. Phone: 055-011-5084-3213. Fax: 055-011-571-6504. E-mail: tatgomes.dmip{at}epm.br.
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Journal of Clinical Microbiology, December 1998, p. 3609-3613, Vol. 36, No. 12
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Copyright © 1998, American Society for Microbiology. All rights reserved.
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