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LETTERS TO THE EDITOR

Outbreak of Infection with Klebsiella pneumoniae Sequence Type 258 Producing Klebsiella pneumoniae Carbapenemase 3 in an Intensive Care Unit in Italy

Caterina Mammina, Daniela Maria Palma, Celestino Bonura, Maria Rosa Anna Plano, Rachele Monastero, Concetta Sodano, Cinzia Calà, Romano Tetamo
Caterina Mammina
Department of Sciences for Health Promotion G. D'Alessandro Section of Hygiene University of Palermo Palermo, Italy
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  • For correspondence: diptigmi@unipa.it
Daniela Maria Palma
General Hospital ARNAS Civico, Di Cristina and Benfratelli II Intensive Care Unit Palermo, Italy
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Celestino Bonura
Department of Sciences for Health Promotion G. D'Alessandro Section of Microbiology University of Palermo Palermo, Italy
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Maria Rosa Anna Plano
Department of Sciences for Health Promotion G. D'Alessandro Section of Hygiene University of Palermo Palermo, Italy
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Rachele Monastero
General Hospital ARNAS Civico, Di Cristina and Benfratelli Laboratory of Diagnostic Microbiology Palermo, Italy
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Concetta Sodano
General Hospital ARNAS Civico, Di Cristina and Benfratelli Laboratory of Diagnostic Microbiology Palermo, Italy
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Cinzia Calà
Department of Sciences for Health Promotion G. D'Alessandro Section of Microbiology University of Palermo Palermo, Italy
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Romano Tetamo
General Hospital ARNAS Civico, Di Cristina and Benfratelli II Intensive Care Unit Palermo, Italy
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DOI: 10.1128/JCM.00315-10
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Gram-negative pathogens producing carbapenemases represent an alarming clinical threat with serious effects on patient outcomes (3, 7). In 2001, Yigit et al. (11) reported a novel β-lactamase termed “K lebsiella pneumoniae carbapenemase” (KPC-1) in North Carolina. KPC-producing strains are now emerging worldwide (5, 6, 8, 9). We report here an outbreak of infection and colonization with KPC-producing K. pneumoniae (KPC-Kp) occurring in Palermo, Italy.

Between 9 April and 1 September 2009, 13 inpatients who had been admitted at the second intensive care unit (ICU), ARNAS Civico and Benfratelli General Hospital of Palermo, Italy, were infected or colonized by a carbapenem-resistant K. pneumoniae isolate (Table 1). The ICU is a 10-bed medical-surgical unit with approximately 430 admissions per year. Preexisting medical or surgical conditions were present in 50% approximately of all admissions. Organ failure was the leading cause of admission (70%), followed by monitoring/weaning from mechanical ventilation (30%). The mean simplified acute physiology score (SAPS) of ICU patients was 39. ICU mortality was 24%. Nurse-to-patient ratio was 1:2. Ten out of the 13 patients were infected and five died, with the KPC-Kp infection being identified as a contributing factor. Five patients were transferred to other care units of the same hospital, but two moved to an external rehabilitation unit. All infections appeared to be nosocomially acquired based upon their onset compared to ICU admission day of the 10 patients. However, it was not possible to rule out the possibility that the index patient could have been colonized at the time of admission, because active surveillance cultures were not being routinely performed at the beginning of the outbreak.

Infection control measures, including undertaking contact precautions, grouping infected/colonized patients into cohorts, and using dedicated staff and equipment as much as possible, were implemented as indicated by the Centers for Disease Control and Prevention (CDC) guidelines for control of infection with carbapenem-resistant or carbapenemase-producing Enterobacteriaceae in acute care facilities (1). Active-surveillance rectal cultures were collected at admission and then on a weekly basis from all patients staying in the ICU more than 48 h. Microbiology records of the ICU for the preceding 12 months were reviewed, but carbapenem-nonsusceptible K. pneumoniae or other Enterobacteriaceae had not been previously detected. The outbreak was eventually controlled by September 2009.

Thirty-three isolates showing reduced susceptibility to ertapenem (i.e., MIC of >4 mg/liter) were collected from the 13 patients, predominantly from respiratory secretions and blood. Identification (ID) and antimicrobial susceptibility testing (AST) were routinely performed using the Vitek-2 system (bioMérieux, France). The 33 KPC-Kp strains were resistant to imipenem (MICs, ≥16 μg/ml), meropenem (MICs, 32 μg/ml), and ertapenem (MICs, ≥8 μg/ml). They were also resistant to amikacin (MICs, ≥64 μg/ml), amoxicillin-clavulanic acid (MICs, ≥32 μg/ml), cefepime (MICs, 8 μg/ml), cefotaxime (MICs, 8 μg/ml), ceftazidime (MICs, ≥64 μg/ml), ciprofloxacin (MICs, ≥4 μg/ml), levofloxacin (MICs, ≥8 μg/ml), piperacillin-tazobactam (MICs, ≥128 μg/ml), tobramycin (MICs, ≥16 μg/ml), and trimethoprim-sulfamethoxazole (MICs, ≥320 μg/ml). They were susceptible to gentamicin (MICs, 4 μg/ml) and colistin (MICs, ≤0.5 μg/ml) but showed full or intermediate susceptibility to tigecycline (MICs, ≤4 μg/ml).

XbaI pulsed-field gel electrophoresis (PFGE) typing attributed the 33 KPC-Kp isolates to three closely related pulsotypes differing from each other by one to three bands. All isolates were positive for the presence of the KPC, TEM, and SHV sequences by PCR amplification while testing negative for the VIM, IMP, and qnr genes (10). Previously described primers were also used to amplify an 851-bp fragment containing the waa E gene (10). Sequencing of all amplicons obtained from three representative isolates, which had been selected on the basis of variation in PFGE pattern, revealed that bla KPC-3, bla TEM-1, and bla SHV-11 were present. In comparison with a reference sequence (GenBank accession number AF146532), the waaE sequence contained five nucleotide changes: four were silent, but one was predicted to determine an Arg (48) → Gly substitution. The substitution is different than that observed by Woodford et al. (10) in isolates from ICUs in New York—Ile (31) → Val—and thus could likely be useful as an epidemiological strain marker. Multilocus sequence typing (MLST) was performed according to the protocol described on the K. pneumoniae MLST website (http://www.pasteur.fr/recherche/genopole/PF8/mlst/Kpneumoniae.html ) (2) and attributed the three representative isolates to sequence type 258 (ST258).

This study reports for the first time an outbreak of KPC-Kp infection and colonization in an ICU in Italy. Indeed, only one case of infection in an inpatient, at the University Hospital of Florence, has been previously reported in Italy (4). The characteristics of our strains are consistent with isolates from several geographic areas, such as the United States and Israel (5, 6). Clone ST258 has been shown to account for approximately 70% of the KPC-Kp strains sent to the CDC (5). In Europe, it has also been found in Norway, Sweden, and Finland from patients transferred from Greece, Israel, and Italy (8, 9).

There is need of urgent action to be undertaken to slow down and eventually control the epidemic worldwide spread of KPC-Kp in health care institutions and the community. Antibiotic use policy and strict infection control measures are critical in the fight against carbapenemase-producing organisms.

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TABLE 1.

Clinical characteristics and outcomes of patients with infection or colonization by KPC-producing Klebsiella pneumoniae a

  • Copyright © 2010 American Society for Microbiology

REFERENCES

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    Kitchel, B., J. K. Rasheed, J. B. Patel, A. Srinivasan, S. Navon-Venezia, Y. Carmeli, A. Brolund, and C. G. Giske. 2009. Molecular epidemiology of KPC-producing Klebsiella pneumoniae isolates in the United States: clonal expansion of multilocus sequence type 258. Antimicrob. Agents Chemother. 53 : 3365-3370.
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    Leavitt, A., S. Navon-Venezia, I. Chmelnitsky, M. J. Schwaber, and Y. Carmeli. 2007. Emergence of KPC-2 and KPC-3 in carbapenem-resistant Klebsiella pneumoniae strains in an Israeli hospital. Antimicrob. Agents Chemother. 51 : 3026-3029.
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    Nordmann, P., G. Cuzon, and T. Naas. 2009. The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect. Dis. 9 : 228-236.
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    Osterblad, M., J. Kirveskari, S. Koskela, P. Tissari, K. Vuorenoja, A. J. Hakanen, M. Vaara, and J. Jalava. 2009. First isolations of KPC-2-carrying ST258 Klebsiella pneumoniae strains in Finland, June and August 2009. Euro Surveill. 14(40): pii 19349.
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    Samuelsen, Ø., U. Naseer, S. Tofteland, D. H. Skutlaberg, A. Onken, R. Hjetland, A. Sundsfjord, and C. G. Giske. 2009. Emergence of clonally related Klebsiella pneumoniae isolates of sequence type 258 producing plasmid-mediated KPC carbapenemase in Norway and Sweden. J. Antimicrob. Chemother. 63 : 654-658.
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    Woodford, N., P. M. Tierno, Jr., K. Young, L. Tysall, M. F. Palepou, E. Ward, R. E. Painter, D. F. Suber, D. Shungu, L. L. Silver, K. Inglima, J. Kornblum, and D. M. Livermore. 2004. Outbreak of Klebsiella pneumoniae producing a new carbapenem-hydrolyzing class A β-lactamase, KPC-3, in a New York medical center. Antimicrob. Agents Chemother. 48 : 4793-4799.
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    Yigit, H., A. M. Queenan, G. J. Anderson, A. Domenech-Sanchez, J. W. Biddle, C. D. Steward, S. Ablerti, K. Bush, and F. C. Tenover. 2001. Novel carbapenem-hydrolyzing lactamase KPC-1 from a carbapenem-resistant strain of Klebsiella pneumoniae. Antimicrob. Agents Chemother. 45 : 1151-1161.
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Outbreak of Infection with Klebsiella pneumoniae Sequence Type 258 Producing Klebsiella pneumoniae Carbapenemase 3 in an Intensive Care Unit in Italy
Caterina Mammina, Daniela Maria Palma, Celestino Bonura, Maria Rosa Anna Plano, Rachele Monastero, Concetta Sodano, Cinzia Calà, Romano Tetamo
Journal of Clinical Microbiology Mar 2010, 48 (4) 1506-1507; DOI: 10.1128/JCM.00315-10

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Outbreak of Infection with Klebsiella pneumoniae Sequence Type 258 Producing Klebsiella pneumoniae Carbapenemase 3 in an Intensive Care Unit in Italy
Caterina Mammina, Daniela Maria Palma, Celestino Bonura, Maria Rosa Anna Plano, Rachele Monastero, Concetta Sodano, Cinzia Calà, Romano Tetamo
Journal of Clinical Microbiology Mar 2010, 48 (4) 1506-1507; DOI: 10.1128/JCM.00315-10
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KEYWORDS

Bacterial Proteins
Disease Outbreaks
Klebsiella Infections
Klebsiella pneumoniae
beta-lactamases

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