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Antimicrob Agents Chemother. Dec 2011; 55(12): 5957–5958.
PMCID: PMC3232776

First NDM-Positive Salmonella sp. Strain Identified in the United States[down-pointing small open triangle]

LETTER

Antimicrobial resistance among Enterobacteriaceae is growing, largely due to β-lactamase production. NDM, carried on the blaNDM gene, is the latest addition to this bacterial armamentarium and is a worrisome resistance mechanism (9). Increasing resistance to antimicrobials has been reported for Salmonella spp., due in part to extended-spectrum β-lactamase (ESBL) and AmpC production, often combined with other resistance mechanisms (4, 7). Carbapenemase production in Salmonella spp. has rarely been reported (5), and neither the blaNDM gene nor any other metallo-beta-lactamase (MBL) in Salmonella spp. has been described yet. We report the first case to our knowledge of NDM-producing Salmonella spp. likely acquired in India but detected in the United States.

On 25 January 2011, a sixty-year-old American was transferred from India by air ambulance to a hospital in Maryland. The patient was originally hospitalized in late December 2010 with a catastrophic intracranial bleed in India. Less than 24 h after his arrival at the U.S. hospital, he sustained a fever of 38.5°C; urine, blood, and endotracheal secretions were cultured. His sputum grew a carbapenem-resistant Klebsiella pneumoniae, positive for carbapenemase production by the modified Hodge test using meropenem (3), and the Etest MBL (AB bioMérieux, Durham, NC) revealed MBL production as per the package insert (1). The organism was susceptible to colistin only (MIC of 0.12 μg/liter by broth macrodilution) (Table 1) (3) and was sent to both the Maryland Department of Health and Mental Hygiene (MDHMH) and Centers for Disease Control and Prevention (CDC) for confirmation. The blaNDM gene was identified in the K. pneumoniae isolate by real-time PCR at the CDC (http://www.cdc.gov/HAI/settings/lab/kpc-ndm1-lab-protocol.html).

Table 1.
Susceptibility results as reported by the BD-Phoenix instrument (BD Diagnostics, Inc., Sparks, MD) using the NMIC/ID 132 panel on the organisms identified

On February 12, a perirectal surveillance culture for carbapenem-resistant gastrointestinal isolates grew non-typhoid Salmonella spp. positive by the modified Hodge test, with an imipenem/(imipenem plus EDTA) ratio of 4/<1 by the Etest MBL. Serotyping at the MDHMH Laboratories Administration identified the isolate as Salmonella enterica subsp. enterica serovar Senftenberg (2), described as monophasic, with the antigenic formula 3,19:g,s,t:−. The identification was confirmed at the CDC. The CDC also concluded that the strain was blaNDM positive and only susceptible to tetracycline, tigecycline, and trimethoprim-sulfamethoxazole (Table 1). Others have raised the possibility that plasmids carrying blaNDM can easily transfer from one species of Enterobacteriaceae to another via genetic conjugation (6, 9). That does not appear to have happened in this case, as the blaNDM-1 plasmids carried by K. pneumoniae and Salmonella Senftenberg had different restriction profiles, as determined at the CDC.

Considering the potential for food-borne spread of Salmonella carrying NDM, this finding is worrisome and emphasizes the need for epidemiological studies and scrutiny of antimicrobial susceptibility reports from salmonellosis cases identified in or imported from countries where Salmonella is endemic and where NDM is spreading. A recently published study identified numerous NDM-1-positive bacteria, including Shigella boydii and Vibrio cholerae but not Salmonella spp., in water and seepage samples in New Delhi, India (8). Prompt recognition of carbapenem-resistant Enterobacteriaceae and initiation of appropriate infection control measures is essential to avoid spread of these organisms. Thus, clinicians should obtain travel history from patients and initiate infection control measures when carbapenem-resistant organisms are identified.

Acknowledgments

We thank Barbara O'Connor and Laura Bunner, the infection preventionists, the nurses, care givers, Eric Aldrich, and the administration at the hospital, David Blythe at the Maryland Department of Health and Mental Hygiene (MDHMH), MDHMH Public Health Microbiology Division staff, for performing Salmonella serotyping and modified Hodge testing, and Alex Kallen, Division of Health Care Quality Promotion, Centers for Disease Control and Prevention, Atlanta, GA for assistance.

The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

Footnotes

[down-pointing small open triangle]Published ahead of print on 3 October 2011.

Contributor Information

Patrice Savard, Healthcare Epidemiology and Infection Control, The Johns Hopkins Health System
The Johns Hopkins Hospital
600 North Wolfe Street, 327 A Billings Building
Baltimore, MD 21287.

Ramya Gopinath, Infectious Diseases and Hospital Epidemiology and Infection Control
Howard County General Hospital
Columbia, MD.

J. Kamile Rasheed, Division of Healthcare Quality Promotion
Centers for Disease Control and Prevention
Atlanta, GA.

Tracy Ross, Division of Medical Microbiology, Department of Pathology
Johns Hopkins Medical Institutions
Baltimore, MD.

Jafar Razeq, Public Health Microbiology, Maryland DHMH Laboratories Administration
Baltimore, MD.

B. Mark Landrum, Infectious Diseases and Hospital Epidemiology and Infection Control
Howard County General Hospital
Columbia, MD.

Lucy E. Wilson, Infectious Diseases and Environmental Health Administration
Maryland Department of Health and Mental Hygiene
Baltimore, MD.

Brandi Limbago, Division of Healthcare Quality Promotion
Centers for Disease Control and Prevention
Atlanta, GA.

Trish M. Perl, Division of Infectious Diseases, Department of Medicine
Johns Hopkins University
Baltimore, MD.

Karen C. Carroll, Division of Medical Microbiology, Department of Pathology
Johns Hopkins Medical Institutions
600 N. Wolfe Street/Meyer B1-193
Baltimore, MD.

REFERENCES

1. Biodisk AB. 2010. Etest MBL for in vitro detection of metallo beta-lactamase. AB bioMerieux, Durham, NC: http://www.abbiodisk.com/pdf/pi/75001546.PDF.
2. Brenner F. W., McWhorter-Murlin A. C. 1998. Identification and serotyping of Salmonella. Centers for Disease Control and Prevention, Atlanta, GA.
3. CLSI 2011. Performance standards for antimicrobial susceptibility testing, 21st informational supplement. CLSI document M100-S21 Clinical and Laboratory Standards Institute, Wayne, PA.
4. González-Sanz R., Herrera-Leon S., de la Fuente M., Arroyo M., Echeita M. A. 2009. Emergence of extended-spectrum beta-lactamases and AmpC-type beta-lactamases in human Salmonella isolated in Spain from 2001 to 2005. J. Antimicrob. Chemother. 64: 1181–1186. [PubMed]
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8. Walsh T. R., Weeks J., Livermore D. M., Toleman M. A. 2011. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect. Dis. 11(5): 355–362. [PubMed]
9. Yong D., et al. 2009. Characterization of a new metallo-beta-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob. Agents Chemother. 53: 5046–5054. [PMC free article] [PubMed]

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