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Antimicrobial Agents and Chemotherapy, June 2007, p. 2201-2204, Vol. 51, No. 6
0066-4804/07/$08.00+0     doi:10.1128/AAC.01389-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Preservation of Integron Types among Enterobacteriaceae Producing Extended-Spectrum ß-Lactamases in a Spanish Hospital over a 15-Year Period (1988 to 2003){triangledown}

Elisabete Machado,1,3,4 Joana Ferreira,1,3 Ângela Novais,1 Luísa Peixe,3 Rafael Cantón,1,2 Fernando Baquero,1,2 and Teresa M. Coque1,2*

Hospital Universitario Ramón y Cajal, IMSALUD, Madrid, Spain,1 Unidad de Resistencia a Antibióticos y Virulencia Bacteriana Asociada al Consejo Superior de Investigaciones Científicas, Madrid, Spain,2 REQUIMTE, Faculdade de Farmácia, Universidade do Porto, Porto, Portugal,3 Faculdade de Ciências da Saúde, Universidade Fernando Pessoa, Porto, Portugal4

Received 6 November 2006/ Returned for modification 27 December 2006/ Accepted 22 March 2007


   ABSTRACT
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The variable presence of integrons among extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae species (0 to 66%) is described. Association between blaESBL and integrons occurred when these are linked to specific ESBL-type genes (In60 bearing ISCR1 and blaCTX-M-9) or when ESBL genes were superimposed onto selected plasmids carrying integrons. Some integrons were identical to those found during decades worldwide, illustrating the preservation of the genetic elements carrying them.


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Integrons are recombination and expression genetic elements able to capture genes as part of genetic structures known as gene cassettes (10, 20). Different integron classes have been described, and classes 1, 2, and 3 have been associated with antibiotic resistance (10, 20). Dissemination of these antibiotic resistance integrons (ARI), which are unable to promote their own mobilization, is mainly linked to transposons and/or plasmids (6, 15, 21, 24, 25, 35, 36).

The occurrence of ARI among Enterobacteriaceae from different environments has been extensively documented (3, 10, 14, 19, 29, 31, 37, 40), although with particular emphasis in Escherichia coli (11, 14, 33-35, 42). Extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae are usually resistant to different antibiotic families. The association of particular beta-lactamase genes with class 1 integrons by location of bla genes within integron platforms (blaVIM, blaIMP, blaGES, blaVEB, blaCTX-M-2/-9, and blaCMY) or by sharing the same plasmid context (blaTEM and blaSHV) among Enterobacteriaceae has been reported in specific studies (6, 7, 17, 21, 27, 28, 32, 38), but the overall occurrence of integrons among ESBL-producing isolates has scarcely been analyzed (18, 29). We have previously tested the presence of integrons among different E. coli groups including 52 ESBL-producing E. coli isolates recovered until 2000 (18). In the present study, we analyzed the diversity of integrons among all species of Enterobacteriaceae producing ESBL recovered from patients attended at Ramón y Cajal University Hospital over a 15-year period (1988-2003).

The study includes 201 clonally unrelated isolates corresponding to 134 E. coli isolates (52 ESBL E. coli isolates from 1988 to 2000 [18] and 82 ESBL E. coli isolates from 2001 to 2003 [the present study]) and 34 Klebsiella pneumoniae, 13 Enterobacter cloacae, 7 Klebsiella oxytoca, 6 Salmonella enterica, 3 Enterobacter aerogenes, 3 Citrobacter freundii, and 1 Enterobacter gergoviae isolates from 1988 to 2003. Bacterial identification and preliminary susceptibility testing were performed by the automated PASCO (Difco, Detroit, MI) or WIDER (Fco. Soria Melguizo, Madrid, Spain) systems. Identification of ESBLs was performed by the standard double-disk synergy test, isoelectric focusing, amplification of bla genes, and further sequencing (5, 16, 41). Characterization of class 1, 2, and 3 integrons was accomplished by PCR and/or dot blot hybridization, restriction fragment length polymorphism typing and sequencing of each type identified, as described previously (18). Conjugation experiments and plasmid characterization were performed by standard methods (18, 21).

ESBLs were identified as TEM (-4, -24, -27, and -52), SHV (-2, -2a, -5, -12, and -13), CTX-M-1-like (-1, -3, -10, -15, and -32), or CTX-M-9-like (-9 and -14) types. Most ESBL bla genes were transferred by conjugation to an E. coli BM21 recipient (nalidixic acid resistant, lactose fermentation positive, and plasmid free), 77% for E. coli and 84% for other species. The presence of class 1 integrons varied from 0 to 60% among species (Table 1). The occurrence of these genetic structures was similar for E. coli or non-E. coli isolates containing blaSHV (57 to 60%) or blaTEM (43 to 55%), but not for strains carrying blaCTX-M (62% versus 14%, respectively) due to the bias imposed by the higher occurrence of blaCTX-M-9 among E. coli isolates than among other Enterobacteriaceae species (30% versus 6%). Fifteen class 1 integron types were identified, seven of which were found only among E. coli isolates (types II, V, VI, and VIII to XI), four were observed among sporadic isolates of K. pneumoniae, S. enterica, or E. cloacae (types XII to XV), and four were detected among different species (types I, III, IV, and VII) (Table 2). Class 1 integron types widely disseminated, designated in the present study as types III (dfrA12-orfF-aadA2), V (aadA2), VI (dfrA17-aadA5), VIII (dfrA7), XII to XV [blaOXA-1-aadA1, dfrA15-aadA1, aac(3)-Ia-orfX ... aadA1a, aadA5] (1, 6, 12, 14, 15, 32, 36, 42), were sporadically observed. A new integron, containing IS1-dfrA1-orfC (type X), is here reported (GenBank accession number EF503596). This integron seems to result from an insertion of IS1 upstream the attI site of the integron containing the gene cassette array drfA1-orfC previously reported in S. enterica and Vibrio sp. (GenBank accession numbers DQ641477 and AB219452, respectively). The simultaneous presence of more than one class 1 integron was observed for a few E. coli isolates. Class 2 integrons were only found in the E. coli group, even though they can be detected in different enterobacterial species either in the chromosome or in large plasmids (2, 8, 30, 40). Class 3 integrons were absent.


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  		TABLE 1. Occurrence of class 1 and class 2 integrons among ESBL-producing Enterobacteriaceae recovered from patients at Ramón y Cajal University Hospital (1988 to 2003)

 

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  		TABLE 2. Class 1 and class 2 integron types among ESBL-producing Enterobacteriaceae isolates (1988 to 2003)

 
Class 1 integrons were cotransferred with bla genes other than blaCTX-M-9 in 34% of ESBL-producing isolates harboring them. Identical or closely related plasmids harboring blaCTX-M-9 (IncHI2), blaCTX-M-15 (IncFII), blaCTX-M-32 (IncN), blaTEM-24 (IncA/C), or blaSHV-2/-12 (Table 2) (21-23, 39) were detected among different species and/or strains. Conjugative plasmids containing blaCTX-M-9 or blaTEM-24 recovered in our hospital during years were associated with class 1 integrons types IV (dfrA16-aadA2) and VII (aac(6')-Ib, also designated aacA4), respectively (4, 21, 23) (Table 2). Type IV is part of In60 (a class 1 integron bearing ISCR1 and containing blaCTX-M-9) on IncHI2 and IncP-1{alpha} epidemic plasmids and has also been detected as part of plasmids carrying qnr from China and North America (GenBank accession no. AY259085). Type VII (aacA4) is widely spread since first detected in multiresistant IncFII plasmid pSa from Shigella flexneri in 1957 among different plasmid groups and eventually associated with blaSHV-5 or blaVIM genes (28; GenBank accession no. L06822). Type I (aadA1) is identical to that of Tn21 (GenBank accession no. AF071413) and was identified among different species producing SHV-2 (E. coli and K. pneumoniae), SHV-2a (K. pneumoniae), SHV-13 (E. coli), CTX-M-9 (E. coli), CTX-M-10 (E. coli and E. cloacae), or TEM-4 (K. pneumoniae), although it was only linked to bla genes in the case of blaCTX-M-9, blaSHV-2, or blaSHV-13. Type II (dfrA1-aadA1), frequently recovered from Enterobacteriaceae of different environments, was also detected among E. coli isolates carrying plasmids coding for TEM-24, SHV-12, CTX-M-9, CTX-M-14, and CTX-M-10. In agreement with other studies, we detected a variable presence of particular gene cassette arrays in epidemic plasmids coding or not coding for different ESBLs, probably reflecting plasmid evolution by different recombinatorial events in different hosts (13, 17, 21, 26). Of the 17 integron types observed, three class 1 (types I, II, and IV) have persisted as major integron types throughout years (8 to 15 years), reflecting the persistence of specific plasmids (type IV linked to epidemic plasmids containing In60) or the wide spread of particular integrons among non-ESBL strains (types I and II). Moreover, in addition to the aforementioned persistence, the number of isolates carrying integrons increased during the last years of the studied period (Table 2).

The apparent higher diversity of ARI among K. pneumoniae (five types among 10 strains, a 0.50 ratio) than among E. coli (11 types among 64 strains; a 0.17 ratio) is in agreement with studies from other geographical areas and might be attributed to the possible spread of a limited number of plasmid types containing fixed types of integrons in the E. coli group (29). The stable preservation of a large number of integron types in this collection and among non-ESBL-producing isolates from different continents during decades (9, 12, 15, 18, 19, 40) suggests the absence of selection of a few of them by association with new types of resistance as ESBLs.

In summary, the low rate of association between ESBL genes and integrons suggests that the selection and dissemination of ESBLs (with the exception of blaCTX-M-9, located in a class 1 integron platform) had only a small influence on the overall spread of class 1 integrons and vice versa. However, the maintenance of three specific class 1 integrons along space (worldwide) and time (decades) reflects the continuous preservation and/or previous selection of the specific plasmids in which they are anchored. It remains to be evaluated whether the presence of integrons in epidemic ESBL plasmids or transposons might facilitate in the future the recombinational capture of new resistance genes.


   ACKNOWLEDGMENTS
 
E.M. was supported by a fellowship from Fundação para a Ciência e Tecnologia de Portugal (SFRH/BD/11304/2002). J.F. was a recipient of a "Leonardo da Vinci" fellowship funded by the European Commission. This study was partially supported by research grants from the Ministry of Science and Technology of Spain (SAF 2003-09285), from Red Española de Investigación en Patología Infecciosa (REIPI-ISCIIIC03/14), and from the European Commission (LSHM-CT-2003-503335).


   FOOTNOTES
 
* Corresponding author. Mailing address: Servicio de Microbiología, Hospital Universitario Ramón y Cajal. Carretera de Colmenar, km. 9.1. Madrid 28034, Spain. Phone: 34-913368330. Fax: 34-913368809. E-mail: mcoque.hrc{at}salud.madrid.org Back

{triangledown} Published ahead of print on 2 April 2007. Back


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Antimicrobial Agents and Chemotherapy, June 2007, p. 2201-2204, Vol. 51, No. 6
0066-4804/07/$08.00+0     doi:10.1128/AAC.01389-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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