Emerging enteropathogenic Escherichia coli strains?Escherichia coli Escherichia coli (ĕsh'ərĭk`ēə kō`lī), common bacterium that normally inhabits the intestinal tracts of humans and animals, but can cause infection in other parts of the body, especially the urinary tract. strains of nonenteropathogenic serogroups carrying eae but lacking the enteropathogenic enteropathogenic having pathogenicity for the intestine. enteropathogenic Escherichia coli strains of E. coli which cause enteritis by close association with enteric cells. Includes attaching and effacing E. coli. E. coli E. coli: see Escherichia coli. E. coli in full Escherichia coli Species of bacterium that inhabits the stomach and intestines. E. coli can be transmitted by water, milk, food, or flies and other insects. adherence factor plasmid and Shiga toxin Shiga toxins are a family of related toxins with two major groups, Stx1 and Stx2, whose genes are considered to be part of the genome of lambdoid prophages.[1] The toxins are named for Kiyoshi Shiga, who first described the bacterial origin of dysentery caused by DNA probe DNA probe An agent that binds directly to a predefined sequence of nucleic acids. Mentioned in: Legionnaires' Disease DNA probe, n See deoxyribonucleic acid probes. sequences were isolated from patients (children, adults, and AIDS patients) with and without diarrhea in Brazil. Although diverse in phenotype and genotype, some strains are potentially diarrheagenic. ********** Typical and atypical enteropathogenic Escherichia coli (EPEC EPEC enteropathogenic Escherichia coli. EPEC Enteropathic Escherichia coli, see there ) strains constitute two distinct groups of organisms that have in common the locus of enterocyte effacement The Locus of Enterocyte Effacement (LEE) is a pathogenicity island consisting of 35,000 base pairs in the bacteria Escherichia coli genome. The LEE encodes the Type III secretion system and Type III secreted proteins which are toxins responsible for attaching and effacing (LEE), a pathogenicity island Pathogenicity islands (PAIs) are a distinct class of genomic islands which are acquired by horizontal transfer. They are incorporated in the genome of pathogenic microorganisms but are usually absent from those non-pathogenic organisms of the same or closely related species. that promotes the development of attaching and effacing lesions (1,2). The LEE island encompasses the eae gene that encodes intimin, an outer membrane The outer membrane refers to the outside membranes of Gram-negative bacteria, the chloroplast, or the mitochondria. It is used to maintain the shape of the organelle contained within its structure, and it acts as a barrier against certain dangers. adhesin fundamental to the establishment of attaching and effacing lesions (1). Only typical EPEC strains bear the EPEC adherence factor (EAF EAF - Effort Adjustment Factor ) plasmid, in which a cryptic sequence used as a probe (EAF probe) to the category is located (1). Various evidence suggests that atypical EPEC are closer to Shiga toxin-producing E. coli (STEC STEC shiga toxin-producing Escherichia coli. ) (1), which cause diarrhea and hemolytic uremic syndrome hemolytic uremic syndrome n. A syndrome in which hemolytic anemia and thrombocytopenia occur with acute renal failure, marked in children by sudden gastrointestinal bleeding, urine that contains red blood cells and is scanty in volume, and (2). Although many STEC strains carry LEE, their main virulence mechanism is Shiga toxin(s) (Stx) production (2). Twelve EPEC serogroups (O26, O55, O86, O111, O114, O119, O125, O126, O127, O128, O142, and O158) are recognized, but recent studies have shown that most typical EPEC strains fall into only certain O:H serotypes within these serogroups, which differ from those of atypical EPEC (1). Furthermore, E. coli strains of non-EPEC serogroups that carry eae but lack the EAF probe sequence and stx genes (eae+ EAF--stx--E. coli) have been detected (3-6), but their role in endemic diarrhea has not been established, and no precise understanding of them exists. Recently, we extensively characterized a collection of such strains from a single city in Brazil (6). To extend our knowledge on the diversity of eae+ EAF stx- E. coli strains of non-EPEC serogroups, we compared their occurrence in three distinct cities in Brazil This article is about the municipalities of Brazil. The States of Brazil are divided into many municipalities. At present, Brazil has 5560 municipalities. The municipalities are linked below, by state. Note: state capitals are now listed within the respective state. and their genotypic and phenotypic characteristics. The Study The strains we studied were collected from patients of low socioeconomic status socioeconomic status, n the position of an individual on a socio-economic scale that measures such factors as education, income, type of occupation, place of residence, and in some populations, ethnicity and religion. in three cities The Three Cities is a collective description of the three fortified cities of Cospicua, Vittoriosa, and Senglea on the Island of Malta, which are enclosed by the massive line of fortification created by the Knights of St John, the Cottonera Lines. : Sao Paulo and Ribeirao Preto Ri·bei·rão Prê·to A city of southeast Brazil north-northwest of São Paulo. It is a processing center in an agricultural region. Population: 551,000. , in Sao Paulo State, and Rio de Janeiro Rio de Janeiro, city, Brazil Rio de Janeiro (rē`ō də zhänā`rō, Port. rē`  thĭ zhənĕē`r , in Rio de Janeiro State, Brazil.
The Sao Paulo strains were collected from 505 diarrheic and 505
nondiarrheic children (1-4 years of age) who visited Hospital Infantil
Menino Jesus (April 1989-March 1990) (7). These strains had been
previously characterized for various traits (6); in the present study,
we tested them for new gene sequences. The Rio de Janeiro strains were
collected from 372 diarrheic and 74 nondiarrheic children [less than or
equal to] 5 years of age at the Instituto de Puericultura e Pediatria
Martagao Gesteira, a public hospital at the Federal University of Rio de
Janeiro (January 1998-December 1999, and May-December 2001). Strains
from Ribeirao Preto were derived from 294 diarrheic children ([less than
or equal to] 9 years of age) and adults (18-52 years), including 42
adults with AIDS. Fecal samples from these patients were sent to the
Regional Laboratory of Instituto Adolfo Lutz Adolfo Lutz was a Brazilian physician, 1855-1940, father of tropical medicine and medical zoology in Brazil, and a pioneer epidemiologist and researcher in infectious diseases.Lutz was born in Rio de Janeiro, on December 18, 1855, to a family of Swiss origins. by Hospital Santa Lydia and different clinics in the vicinity (August 2000-June 2002). This study has been approved by the Universidade Federal de Sao Paulo, Escola Paulista de Medicina Ethical Committee for human experimentation. In all studies, five lactose-fermenting isolates and one nonlactose-fermenting isolate of each morphologic type, present in each fecal sample, were biochemically characterized as E. coli. Other well-established bacterial enteropathogens (Salmonella spp., Shigella shigella Any of the rod-shaped bacteria that make up the genus Shigella, which are normal inhabitants of the human intestinal tract and can cause dysentery, or shigellosis. Shigellae are gram-negative (see gram stain), non-spore-forming, stationary bacteria. S. spp., Aeromonas spp Aeromonas spp Microbiology A genus of gram-negative, facultatively anaerobic, nonspore-forming bacilli, which have been isolated from various foods, including dairy products, meats and vegetable; Aeromonas , Campylobacter Campylobacter Genus of gram-negative spiral-shaped bacteria infecting mammals. Many species, especially C. fetus, cause miscarriage in sheep and cattle. C. jejuni is a common cause of food poisoning. Sources include meats (particularly chicken) and unpasteurized milk. spp., and Yersinia enterocolitica Yersinia en·ter·o·co·lit·i·ca n. A bacterium that causes yersiniosis. ) and rotavirus rotavirus /ro·ta·vi·rus/ (ro´tah-vi?rus) any member of the genus Rotavirus. ro´taviral Rotavirus /Ro·ta·vi·rus/ (ro´tah-vi?rus were also searched for by standard methods (8). All E. coli isolates were tested by colony hybridization hybridization /hy·brid·iza·tion/ (hi?brid-i-za´shun) 1. crossbreeding; the act or process of producing hybrids. 2. molecular hybridization 3. with cloned or amplified genetic sequences for enterotoxigenic en·ter·o·tox·i·gen·ic adj. Of or being an organism containing or producing an enterotoxin. Enterotoxigenic E. coli, enteroinvasive E. coli, EPEC (eae and EAF probes), STEC (stx probes), and enteroaggregative E. coli, as previously described (6). The E. coli strains that were eae+ EAF- stx- were serotyped at the Instituto Adolfo Lutz (National Reference Center for E. coli Serotyping) by using antisera O1 to O173 and H1 to H56. In Sao Paulo and Rio de Janeiro, the eae+ EAF- stx- E. coli strains of non-EPEC serogroups occurred in similar frequencies in diarrheic and nondiarrheic children: 32 (6.3%) compared with 27 (5.3%), and 19 (5.1%) compared with 4 (5.4%), respectively. In Ribeirao Preto, such strains were found in 17 (5.8%) patients: 13 from children (1 month-9 years of age) and 4 from adults with AIDS (27-52 years of age). A total of 99 strains (one from each patient) were selected for further analysis. These strains had diverse serotypes (Table 1); 25 (25.2%) strains were nonmotile, 3 were rough, and 47 (47.5%) did not react with the O antisera tested. Among the 49 O-typable strains, 29 serogroups and 35 serotypes were found. The most frequent serotype serotype /se·ro·type/ (ser´o-tip) the type of a microorganism determined by its constituent antigens; a taxonomic subdivision based thereon. se·ro·type n. See serovar. v. was O51:H40 (10.1%), which occurred in all three areas studied. Most of the other serotypes occurred in one or two strains. All strains were tested for adherence to HeLa cells HeLa cells cells of the first continuously cultured carcinoma strain, descended from a human cervical carcinoma; used in the study of life processes, including viruses, at the cell level. (3- and 6-hour assays) (9). Four of them promoted sporadic adherence, four were nonadherent, and one was cytodetaching. For 88 of the 90 adherent adherent /ad·her·ent/ (-ent) sticking or holding fast, or having such qualities. strains, the adherence patterns could only be determined in 6 hours. Seventy-two (80.0%) of the 90 strains had variations of the localized adherence (LA) pattern of typical EPEC, which is characterized by compact bacterial clusters (10). These variant patterns included the following: LA-like pattern, which showed loose bacterial clusters (11); a pattern that showed loose and compact clusters; and a pattern identical to LA, despite its detection in only 6 hours (LA6). Other less frequent patterns included the following: the diffuse adherence typical of diffusely adhering E. coli, the aggregative adherence typical of enteroaggregative E. coli (2), and an association of diffuse adherence and LA or of aggregative adherence and LA. These mixed patterns were retained when individual colonies were tested. The aggregative adherence/LA pattern (two strains) was only recognized in the 3-hour assays. The prevalence of the different patterns varied by area of study, but the variations of LA were the most prevalent in all (72.7%) (Figure 1). [FIGURE 1 OMITTED] The ability to promote attaching and effacing lesions was tested by the fluorescent actin staining test (FAS) (7) in 94 strains; the 5 nonadherent or cytodetaching strains were not tested. Seventy (74.4%) of the strains tested were positive: 43 (72.9%), 15 (65.2%), and 12 (70.2%) of the strains from Sao Paulo, Rio de Janeiro, and Ribeirao Preto, respectively. Moreover, four distinct segments of the LEE region were found in all strains studied, as detected by hybridization with specific LEE sequences (LEE A, B, C, and D) (12), which suggests that all bear a complete LEE region. LEE insertion sites were detected by a combination of polymerase chain reaction polymerase chain reaction (pŏl`ĭmərās') (PCR), laboratory process in which a particular DNA segment from a mixture of DNA chains is rapidly replicated, producing a large, readily analyzed sample of a piece of DNA; the process is (PCR PCR polymerase chain reaction. PCR abbr. polymerase chain reaction Polymerase chain reaction (PCR) ) assays with primers for the seIC junctions and for conserved sequences of selC and pheU (12,13). LEE was inserted in selC in 46 strains: 24 (40.7%), 13 (56.6%), and 9 (53.0%) strains from Sao Paulo, Rio de Janeiro, and Ribeirao Preto, respectively. In addition, LEE was probably inserted in pheU in 29 (49.1%) and 3 (13.0%) of the Sao Paulo and Rio de Janeiro strains, respectively. In 13 strains, LEE is probably inserted in another site, since both loci loci [L.] plural of locus. loci Plural of locus, see there were intact. The LEE insertion site was undetermined in eight strains because both selC and pheU were disrupted, and the primers for the LEE junctions in selC yield no amplification. Strains with an undetermined LEE insertion site occurred in all three areas studied. Strains were also tested for 24 DNA sequences of established or putative virulence properties of pathogenic E. coli by colony hybridization (6). DNA probes were obtained from cloned genes (bfpA, perA, E-hly, EAEC EAEC enteroadherent Escherichia coli. EAEC Enteroadherent Escherichia coli, see there , daaC, cdt, cnf, hly) (6) or by PCR amplification, which used as templates the genomic DNA of EAEC prototype strains O42 (aafC, aggR, aspU, shf irp2, pet, and pic) and 17-2 (aggC and astA); extraintestinal pathogenic strains (ExPEC) J96 (pap) and KS52 (afa), and E. coli HB101 (pANN 801-13) (carrying the sfa probe). PCR primers and assay conditions used were described previously (6,14). Hybridization with 17 of the 24 sequences tested was detected among the strains; hly and irp2 (31.3% each) and astA (29.3%) were the most frequent. Thirty-four different combinations of these 17 sequences were found (Table 2). Their prevalence varied by location, but 25 (73.5%) occurred in two or fewer strains. Among the less frequent combinations found, some were of genes of ExPEC and EAEC, and others of genes of EPEC (bfpA) and EHEC EHEC enterohemorrhagic Escherichia coli. EHEC Enterohemorrhagic Escherichia coli, see there (Ehly). Moreover, 30.3% of the strains lacked all 24 DNA sequences tested, comprising the most frequent subgroup of strains in all three areas (Table 2). Although these strains carried only the eae gene and the four LEE probe sequences (LEE+ only strains), they may have carried virulence sequences other than those tested. Thus, one should not emphasize the virulence potential of these LEE+ strains solely on the basis of findings of significant differences in their frequencies between cases and controls. DNA sequences similar to bfpA were detected in 14 (14.1%) of the 99 strains studied, however, only 2 expressed Bfp in Western blot Western blot A technique developed in 1979 that is used to confirm ELISA results. HIV antigen is purified by electrophoresis and attached by blotting to a nylon or nitrocellulose filter. experiments (not shown); these two strains also carried perA and presented AA/LA in 3 hours. The HeLa pattern of the remaining bfpA+ strains varied, but none of them had compact clusters in 3 hours, which is typical of LA. Thus, Bfp expression was found only in strains presenting aggregative adherence/LA in 3 hours, as in typical LA of EPEC (1). PCR assays with specific primers for the variable region of intimin were used to identify five intimin types ([alpha], [beta], [delta], and [epsilon]) (15,16). Most strains had a nontypable intimin (64.6%), but the distribution of these strains varied (approximately 70% in Sao Paulo and 29%-35% in Rio de Janeiro and Ribeirao Preto). Recently, new schemes were proposed to identify intimin subtypes, which were not tested (17,18). The prevalence of typable intimins varied among the three areas analyzed. Intimin subtypes [beta] (11.1%) and [gamma] (12.1%) prevailed, and intimin [epsilon] was not found (Figure 2). The intimin types of two strains were not determined because amplification products of the expected size were obtained with four intimin pairs of primers. [FIGURE 2 OMITTED] Conclusions In this study, we sought to verify the frequency with which eae+ EAF- stx- E. coli strains of non-EPEC serogroups occur in persons of poor socioeconomic status in three Brazilian cities; we also compared these strains' genotypic and phenotypic characteristics. Although these strains occurred in 5% to 6% of the populations studied, including nondiarrheic children (in Sao Paulo and Ribeirao Preto), 73%-88 % of them were dissociated dis·so·ci·ate v. dis·so·ci·at·ed, dis·so·ci·at·ing, dis·so·ci·ates v.tr. 1. To remove from association; separate: from other well-established enteropathogens (not shown). Although O51:H40 was the most frequent serotype found and occurred in all three areas studied, the non-EPEC eae+ EAF- stx- strains comprised a large variety of serotypes, and many were O nontypable. Moreover, the strains had diverse adherence patterns and various combinations of pathogenic E. coli DNA DNA: see nucleic acid. DNA or deoxyribonucleic acid One of two types of nucleic acid (the other is RNA); a complex organic compound found in all living cells and many viruses. It is the chemical substance of genes. virulence sequences; the prevalence of these properties varied among the areas studied. Altogether, these data show that eae+ EAF-stx-E. coli strains outside the EPEC serogroups are even more diverse than already observed (6). As we have emphasized previously, such diversity challenges the diagnosis of these putative pathogens (6). All strains carried an apparently complete LEE region, and approximately 75.0% of them had the potential to promote attaching and effacing lesions in HeLa cells, as detected by FAS. Thus at least these FAS+ strains are potentially enteropathogenic, since they are capable of inducing attaching and effacing lesions in vitro in vitro /in vi·tro/ (in ve´tro) [L.] within a glass; observable in a test tube; in an artificial environment. in vi·tro adj. In an artificial environment outside a living organism. and may occur in diarrheic patients of various ages and in patients with AIDS. In the EPEC meeting held in 1995, a consensus definition of atypical EPEC was established, namely, that they are EAF-, eae+ strains that promote attaching and effacing lesions (19). Therefore, the FAS+ strains of our study could be classified as atypical EPEC. Whether these strains have additional virulence properties not present in typical EPEC remains to be elucidated. Studies on the virulence potential of selected strains at the cellular and molecular levels will certainly contribute to further understanding of this group of strains and aid in discriminating enteropathogenic strains within the group. These studies were supported by FINEP/MCT/PRONEX grant (41.96.0881.00) and FAPESP FAPESP Fundacao de Amparo a Pesquisa do Estado de Sao Paulo (Brazil) grant 95/9176-4 awarded to T.A.T.G. and 01/07921-7 awarded to B.E.C.G.
Table 1. Serotypes identified among eae+ EAF- stx- Escherichia
coli strains outside the enteropathogenic E. coli serogroups (a)
Serotype Serotype Serotype
(no. of strains) (no. of strains) (no. of strains)
O2ab:H45 O101:H33 ONT:H7 (3)
O2ab:HNT O104:H- ONT:8 (4)
O4: H1 O1044: H12 ONT: H9
O4: H16 O1099:H9 ONT:H11
O11: H2 O115:H8 ONT:H19 (3)
O11: H16 O118:HNT (2) ONT:H25
O13:H11 O121:H- ONT:H29,31
O16:H- O123:H19 ONT:H33 (3)
O19:H- O124:H40 ONT:H34
O39:H- O132:H8 ONT:H38
O41:H- O145:H- ONT:H40 (2)
O49:H10 O153:H7 ONT:H40,43(2)
O51: H40 (10) O154:H9 ONT:H46
O51: H- O157:H16 ONT:HNT (3)
O63:H6 (2) O162:H- OR:H11,21,40
O66:H8 O162:H33 OR:H11,21
O70:H2 ONT:H- (16) OR:H28
O85:H31 (3) ONT:H2 (2)
O98:H8 ONT:H6 (2)
(a) NT, nontypable with antisera O1 to O173 and H1 to H 56; H-,
nonmotile; R, rough strains.
Table 2. Prevalence of distinct combinations of virulence-related DNA
sequences in eae+ EAF- stx- Escherichia coli strains outside the EPEC
serogroups in three cities in Brazil (a)
No. (%) of strains
Total Sao Paulo
Genetic profile (b) (n = 99) (n = 59)
eae 31 (31.1) 19 (32.2)
eae hly astA pet irp2 8 (8.1) 8 (13.6)
eae hly 6 (6.1) 5 (8.5)
eae shf 5 (5.1) 1(1.7)
eae irp2 5 (5.1) 4 (6.8)
eae perA bfpA astA 4 (4.0) 1(1.7)
eae perA bfpA 4 (4.0) 0
eae hly daaC afa astA pet irp2 3 (3.0) 3 (5.1)
eae perA 3 (3.0) 0
eae perA hly astA pet irp2 2 (2.0) 1(1.7)
eae EHEC-hly astA 2 (2.0) 2 (3.4)
eae astA irp2 2 (2.0) 2 (3.4)
eae bfpA 2 (2.0) 1(1.7)
eae EHEC-hly 2 (2.0) 0
eae hly daaC afa pap sfa astA shf pet irp2 1(1.0) 1(1.7)
eae hly daaC afa shf irp2 1(1.0) 1(1.7)
eae perA bfpA hly pet 1(1.0) 0
eae perA hly daaC afa 1(1.0) 0
eae perA bfpA astA irp2 1(1.0) 1(1.7)
eae hly pap afa irp2 1(1.0) 0
eae hly daaC afa astA 1(1.0) 1(1.7)
eae hly astA shf irp2 1(1.0) 1(1.7)
eae perA bfpA hly 1(1.0) 0
eae hly astA irp2 1(1.0) 1(1.7)
eae hly shf irp2 1(1.0) 1(1.7)
eae perA astA 1(1.0) 0
eae EHEC-hly bfpA 1(1.0) 1(1.7)
eae hly shf 1(1.0) 1(1.7)
eae hly irp2 1(1.0) 1(1.7)
eae hly astA 1(1.0) 1(1.7)
eae astA shf 1(1.0) 0
eae shf irp2 1(1.0) 0
eae astA 1(1.0) 1(1.7)
eae cdt 1(1.0) 0
No. (%) of strains
Rio de Ribeirao
Janeiro Preto
Genetic profile (b) (n = 23) (n = 17)
eae 5 (21.8) 7 (41.1)
eae hly astA pet irp2 0 0
eae hly 0 1(5.9)
eae shf 3 (13.1) 1(5.9)
eae irp2 1(4.3) 0
eae perA bfpA astA 3 (13.1) 0
eae perA bfpA 4 (17.4) 0
eae hly daaC afa astA pet irp2 0 0
eae perA 0 3 (17.6)
eae perA hly astA pet irp2 0 1(5.9)
eae EHEC-hly astA 0 0
eae astA irp2 0 0
eae bfpA 1(4.3) 0
eae EHEC-hly 2 (8.7) 0
eae hly daaC afa pap sfa astA shf pet irp2 0 0
eae hly daaC afa shf irp2 0 0
eae perA bfpA hly pet 0 1(5.9)
eae perA hly daaC afa 0 1(5.9)
eae perA bfpA astA irp2 0 0
eae hly pap afa irp2 1(4.3) 0
eae hly daaC afa astA 0 0
eae hly astA shf irp2 0 0
eae perA bfpA hly 0 1(5.9)
eae hly astA irp2 0 0
eae hly shf irp2 0 0
eae perA astA 1(4.3) 0
eae EHEC-hly bfpA 0 0
eae hly shf 0 0
eae hly irp2 0 0
eae hly astA 0 0
eae astA shf 0 1(5.9)
eae shf irp2 1(4.3) 0
eae astA 0 0
eae cdt 1(4.3) 0
(a) EPEC, enteropathogenic Escherichia coli, EHEC, enterohemorrhagic
E. coli.
(b) All strains hybridized with the locus of enterocyte effacement
(LEE) A, LEE B, LEE C, and LEE D probes constructed by McDaniel et al.
(12), which suggested that they bear a complete LEE region.
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Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli enterohemorrhagic Escherichia coli EHEC Any of the E coli serotypes–eg O29, O39, O145 that produces shiga-like toxins, causing bloody inflammatory diarrhea, evoking a HUS. See Escherichia coli O157:H7, Hemolytic uremic syndrome. . Infect Immun. 1989;57:1290-13. (12.) McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci U S A. 1995;92:1664-8. (13.) Sperandio V, Kaper JB, Bortolini MR, Neves BC, Keller R, Trabulsi LR. Characterization of the locus of enterocyte effacement (LEE) in different enteropathogenic Escherichia coli (EPEC) and Shiga-toxin producing Escherichia coli (STEC) serotypes. FEMS FEMS Federation of European Microbiological Societies FEMS Federation of European Materials Societies FEMS Fabrication Engineering Management System FEMS Facility Equipment Maintenance System (PMEL/TMDE) Microbiol Lett. 1998;164:133-9. (14.) Elias WP, Uber AP, Tomita S, Trabulsi LR, Gomes TAT. Combinations of putative virulence markers in typical and variant enteroaggregative Escherichia coli strains from children with and without diarrhea. Epidemiol Infect. 2002; 129:49-55. (15.) Adu-Bobie J, Frankel G, Bain C, Goncalves AG, Trabulsi LR, Douce a. 1. Sweet; pleasant. 2. Sober; prudent; sedate; modest. And this is a douce, honest man. - Sir W. Scott. G, et al. Detection of intimin alpha, beta, gamma, and delta, four intimin derivatives by attaching and effacing microbial microbial pertaining to or emanating from a microbe. microbial digestion the breakdown of organic material, especially feedstuffs, by microbial organisms. pathogens. J Clin Microbiol. 1998;36:662-8. (16.) Oswald E, Schmidt H, Morabito S, Karch H, Marches O, Caprioli A. Typing of intimin genes in human and animal enterohemorrhagic Escherichia coli: characterization of a new intimin variant. Infect Immun. 2000;68:64-71. (17.) Jenkins C, Lawson AJ, Cheasty T, Willshaw GA, Wright P, Dougan G, et al. Subtyping intimin genes from enteropathogenic Escherichia coli associated with outbreaks and sporadic cases in the United Kingdom and Eire. Mol Cell Probes. 2003;17:149-56. (18.) Zhang WL, Kohler B, Oswald E, Beutin L, Karch H, Morabito S, et al. Genetic diversity of intimin genes of attaching and effacing Escherichia coli strains. J Clin Microbiol. 2002;40:4486-92. (19.) Kaper, JB. Defining EPEC. Proceedings of the International Symposium on Enteropathogenic Escherichia coli (EPEC). Rev Microbiol Sao Paulo. 1996;27:130-3. Address for correspondence: Tania
CEP abbr. congenital erythropoietic porphyria 04023-062; fax: 55-115571-6504; email: tatgomes@ecb.epm.br Dr. Gomes is associate professor of microbiology in the Department of Microbiology, Immunology and Parasitology Parasitology The scientific study of parasites and of parasitism. Parasitism is a subdivision of symbiosis and is defined as an intimate association between an organism (parasite) and another, larger species of organism (host) upon which the parasite is at Sao Paulo Medical School, Federal University of Sao Paulo. She studies the epidemiology of diarrhea and the potential virulence factors of diarrheagenic E. coli, with emphasis on enteropathogenic, attaching-effacing, and enteroaggregative categories. Tania A.T. Gomes, * Kinue Irino, ([dagger]) Dennys M. Girao * ([double dagger]) ([section])([paragraph]), Valeria B.C. Girao, ([paragraph]) Beatriz E.C. Guth, * Tania M.I. Vaz, * ([dagger]) Fabiana C. Moreira, * Silvia H. Chinarelli, (#) and Monica A.M. Vieira * * Universidade Federal de Sao Paulo, Sao Paulo, Brazil; ([dagger]) Instituto Adolfo Lutz, Sao Paulo, Brazil; ([double dagger]) Universidade de Sao Paulo, Sao Paulo, Brazil; ([section]) Instituto Butantan, Sao Paulo, Brazil; ([paragraph]) Universidade Federal de Rio de Janeiro, Rio de Janeiro, Brazil; and (#) Instituto Adolfo Lutz, Ribeirao Preto, Sao Paulo, Brazil |
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