• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of aacPermissionsJournals.ASM.orgJournalAAC ArticleJournal InfoAuthorsReviewers
Antimicrob Agents Chemother. May 2013; 57(5): 2426–2427.
PMCID: PMC3632920

Dissemination of a Class I Integron Carrying VIM-2 Carbapenemase in Pseudomonas aeruginosa Clinical Isolates from a Hospital Intensive Care Unit in Annaba, Algeria

LETTER

Over the last decade, the increase of carbapenem resistance in Pseudomonas aeruginosa has been due mostly to impermeability because of OprD loss and the production of metallo-β-lactamases (MBL), including those of the IMP, VIM, SPM, GIM, SIM, AIM-1, FIM-1, and NDM families (14); also, active efflux and serine carbapenemases may contribute to carbapenem resistance in P. aeruginosa in some cases. VIM-1 was reported in the Mediterranean area in 1997 in a clinical isolate of P. aeruginosa in Verona, Italy (5), and in a clinical isolate of Pseudomonas mosselii isolated in 1994 in Genoa, Italy (6). A VIM-2 variant appeared in Marseille, France, in 1996 (7). VIM-2 has now spread as the predominant MBL variant among P. aeruginosa in all European Mediterranean countries (1), but in North Africa, the presence of VIM-2 has been reported only recently in Tunisia (2, 8, 9). Here we report the first molecular characterization of VIM-2-producing P. aeruginosa clinical isolates from Algeria that harbored a novel class I integron that also contained two gene cassettes encoding resistance to aminoglycosides (aadB and aacA4).

A total of 17 nonreplicate imipenem-resistant P. aeruginosa clinical isolates (imipenem MIC, >8 μg/ml, as determined by the Etest) recovered from December 2010 to September 2011 in a surgical intensive care unit at the University Hospital of Annaba, Algeria, were screened by PCR for the presence of MBL-encoding genes using primers previously described (1012). Antibiotic susceptibility testing was performed using disk diffusion with the breakpoints and according to the guidelines of the Antibiogram Committee of the French Society for Microbiology (CA-SFM) (www.sfm-microbiologie.org), and results are summarized in Table 1. An imipenem-EDTA synergy test (13) was positive for 14 out of 17 strains that were PCR positive for VIM-2 carbapenemase using the universal primers VIM-all-F (5′-TGGTCTACATGACCGCGTCT-3′) and VIM-all-R (3′-CGACTGAGCGATTTGTGTG-5′), with an expected PCR size of 766 bp. The characterization of class I integrons reported previously (11) showed a novel class I integron that harbored the VIM-2 gene associated with two gene cassettes encoding aminoglycosides resistance (aadB and aacA4). However, the molecular investigation of the remaining three strains using primers previously described (3) revealed chromosomic mutations that created premature stop codons in the oprD gene. Complete multilocus sequence typing (MLST) (14) revealed that the 17 strains belong to 4 different sequence types (ST), including ST162 (one isolate), ST654 (one isolate), ST1175 (one isolate), and a new ST, ST1420 (14 isolates), recently submitted to the PubMLST database (http://pubmlst.org/paeruginosa) from China (January, 2013).

Table 1
Phenotypic and genotypic features of the 17 imipenem-resistant P. aeruginosa clinical isolatesa

To the best of our knowledge, in North Africa, VIM-2-MBL-producing P. aeruginosa isolates have been reported only in Tunisia (8, 9, 11). VIM-2-producing P. aeruginosa clinical isolates have been reported in other countries in Africa, including 1 from a Hungarian tourist who was hospitalized in Egypt (15), 1 from a single patient who was transferred to Norway after being hospitalized in Ghana (16), 57 recovered in 2006 and 2007 in Kenya (17), and 15 from South Africa (18).

Our results demonstrate that national surveillance should be urgently implemented in Algeria to monitor and control the emergence and spread of carbapenemase-encoding genes.

Nucleotide sequence accession numbers.

The full sequence of the class 1 integron has been deposited in the GenBank database under accession number JX120362.

ACKNOWLEDGMENTS

We thank Linda Hadjadj and Maxime Pit for technical assistance. We thank American Journal Experts for English corrections.

We have no conflicts of interest to declare.

This work was partly funded by CNRS.

Footnotes

Published ahead of print 4 March 2013

REFERENCES

1. Cornaglia G, Giamarellou H, Rossolini GM. 2011. Metallo-beta-lactamases: a last frontier for beta-lactams? Lancet Infect. Dis. 11:381–393 [PubMed]
2. Hammami S, Boutiba-Ben BI, Ghozzi R, Saidani M, Amine S, Ben RS. 2011. Nosocomial outbreak of imipenem-resistant Pseudomonas aeruginosa producing VIM-2 metallo-beta-lactamase in a kidney transplantation unit. Diagn. Pathol. 6:106. [PMC free article] [PubMed]
3. Ocampo-Sosa AA, Cabot G, Rodriguez C, Roman E, Tubau F, Macia MD, Moya B, Zamorano L, Suarez C, Pena C, Dominguez MA, Moncalian G, Oliver A, Martinez-Martinez L. 2012. Alterations of OprD in carbapenem-intermediate and -susceptible strains of Pseudomonas aeruginosa isolated from patients with bacteremia in a Spanish multicenter study. Antimicrob. Agents Chemother. 56:1703–1713 [PMC free article] [PubMed]
4. Pollini S, Maradei S, Pecile P, Olivo G, Luzzaro F, Docquier JD, Rossolini GM. 2013. FIM-1, a new acquired metallo-beta-lactamase from a Pseudomonas aeruginosa clinical isolate from Italy. Antimicrob. Agents Chemother. 57:410–416 [PMC free article] [PubMed]
5. Lauretti L, Riccio ML, Mazzariol A, Cornaglia G, Amicosante G, Fontana R, Rossolini GM. 1999. Cloning and characterization of blaVIM, a new integron-borne metallo-beta-lactamase gene from a Pseudomonas aeruginosa clinical isolate. Antimicrob. Agents Chemother. 43:1584–1590 [PMC free article] [PubMed]
6. Giani T, Marchese A, Coppo E, Kroumova V, Rossolini GM. 2012. VIM-1-producing Pseudomonas mosselii isolates in Italy, predating known VIM-producing index strains. Antimicrob. Agents Chemother. 56:2216–2217 [PMC free article] [PubMed]
7. Poirel L, Naas T, Nicolas D, Collet L, Bellais S, Cavallo JD, Nordmann P. 2000. Characterization of VIM-2, a carbapenem-hydrolyzing metallo-beta-lactamase and its plasmid- and integron-borne gene from a Pseudomonas aeruginosa clinical isolate in France. Antimicrob. Agents Chemother. 44:891–897 [PMC free article] [PubMed]
8. Ktari S, Mnif B, Znazen A, Rekik M, Mezghani S, Mahjoubi-Rhimi F, Hammami A. 2011. Diversity of beta-lactamases in Pseudomonas aeruginosa isolates producing metallo-beta-lactamase in two Tunisian hospitals. Microb. Drug Resist. 17:25–30 [PubMed]
9. Mansour W, Poirel L, Bettaieb D, Bouallegue O, Boujaafar N, Nordmann P. 2009. Metallo-beta-lactamase-producing Pseudomonas aeruginosa isolates in Tunisia. Diagn. Microbiol. Infect. Dis. 64:458–461 [PubMed]
10. Diene SM, Bruder N, Raoult D, Rolain JM. 2011. Real-time PCR assay allows detection of the New Delhi metallo-beta-lactamase (NDM-1)-encoding gene in France. Int. J. Antimicrob. Agents 37:544–546 [PubMed]
11. Hammami S, Gautier V, Ghozzi R, Da CA, Ben-Redjeb S, Arlet G. 2010. Diversity in VIM-2-encoding class 1 integrons and occasional blaSHV2a carriage in isolates of a persistent, multidrug-resistant Pseudomonas aeruginosa clone from Tunis. Clin. Microbiol. Infect. 16:189–193 [PubMed]
12. Toleman MA, Simm AM, Murphy TA, Gales AC, Biedenbach DJ, Jones RN, Walsh TR. 2002. Molecular characterization of SPM-1, a novel metallo-beta-lactamase isolated in Latin America: report from the SENTRY antimicrobial surveillance programme. J. Antimicrob. Chemother. 50:673–679 [PubMed]
13. Yong D, Lee K, Yum JH, Shin HB, Rossolini GM, Chong Y. 2002. Imipenem-EDTA disk method for differentiation of metallo-beta-lactamase-producing clinical isolates of Pseudomonas spp. and Acinetobacter spp. J. Clin. Microbiol. 40:3798–3801 [PMC free article] [PubMed]
14. Curran B, Jonas D, Grundmann H, Pitt T, Dowson CG. 2004. Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J. Clin. Microbiol. 42:5644–5649 [PMC free article] [PubMed]
15. Szabo D, Szentandrassy J, Juhasz Z, Katona K, Nagy K, Rokusz L. 2008. Imported PER-1 producing Pseudomonas aeruginosa, PER-1 producing Acinetobacter baumannii and VIM-2-producing Pseudomonas aeruginosa strains in Hungary. Ann. Clin. Microbiol. Antimicrob. 7:12 doi:10.1186/1476-0711-7-12 [PMC free article] [PubMed]
16. Samuelsen O, Buaro L, Toleman MA, Giske CG, Hermansen NO, Walsh TR, Sundsfjord A. 2009. The first metallo-beta-lactamase identified in Norway is associated with a TniC-like transposon in a Pseudomonas aeruginosa isolate of sequence type 233 imported from Ghana. Antimicrob. Agents Chemother. 53:331–332 [PMC free article] [PubMed]
17. Pitout JD, Revathi G, Chow BL, Kabera B, Kariuki S, Nordmann P, Poirel L. 2008. Metallo-beta-lactamase-producing Pseudomonas aeruginosa isolated from a large tertiary centre in Kenya. Clin. Microbiol. Infect. 14:755–759 [PubMed]
18. Jacobson RK, Minenza N, Nicol M, Bamford C. 2012. VIM-2 metallo-beta-lactamase-producing Pseudomonas aeruginosa causing an outbreak in South Africa. J. Antimicrob. Chemother. 67:1797–1798 [PubMed]

Articles from Antimicrobial Agents and Chemotherapy are provided here courtesy of American Society for Microbiology (ASM)
PubReader format: click here to try

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...