Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 19, Number 6—June 2013

New Delhi Metallo-β-Lactamase–producing Enterobacteriaceae, United States

J. Kamile RasheedComments to Author , Brandon Kitchel, Wenming Zhu, Karen F. Anderson, Nancye C. Clark, Mary Jane Ferraro, Patrice Savard, Romney M. Humphries, Alexander J. Kallen, and Brandi M. Limbago
Author affiliations: Centers for Disease Control and Prevention, Atlanta, Georgia, USA (J.K. Rasheed, B. Kitchel, W. Zhu, K.F. Anderson, N.C. Clark, A.J. Kallen, B.M. Limbago); Massachusetts General Hospital, Boston, Massachusetts, USA (M.J. Ferraro); Johns Hopkins University, Baltimore, Maryland, USA (P. Savard); Johns Hopkins Health System, Baltimore (P. Savard); University of California Los Angeles David Geffen School of Medicine, Los Angeles, California, USA (R.M. Humphries)

Main Article

Table 1

Epidemiologic information for New Delhi metallo-β-lactamase–producing isolates, United States, April 2009–March 2011*

Patient no. Isolate no. Organism Date of isolation State Isolation site Patient age Patient and travel history
1 1000654 Enterobacter cloacae 2009 Apr MA Urine 65 y Hospitalized in India before coming to United States (8)
2 1000527 Klebsiella pneumoniae 2009 Dec CA Urine 73 y Hospitalized in India before returning to United States (8)
3 1001728 Escherichia coli 2010 May IL Urine 41 y Chronic medical problems; traveled to India 3–4 mo before positive culture. No known hospitalizations during travel (8)
4 1100192 K. pneumoniae 2010 Sep CA Resp. 13 mo Hospitalized in Pakistan 5 months before admission in United States (10)
5 1100101 E. coli 2010 Oct VA Resp. 67 y Received medical care in India but not hospitalized
6 1100770 K. pneumoniae 2010 Dec CA Urine 70 y Hospitalized for 1 mo in India before transfer to US hospital
7 1100975 K. pneumoniae 2011 Jan MD Resp. 60 y Hospitalized in India before transfer to US hospital (12)
1101168 Salmonella enterica serovar Senftenberg 2011 Feb MD Feces
8 1101459 K. pneumoniae 2011 Mar CA Blood 57 y Hospitalized in India; subsequently hospitalized in United States

*Resp., respiratory sample.

Main Article

  1. Queenan  AM, Bush  K. Carbapenemases: the versatile β-lactamases. Clin Microbiol Rev. 2007;20:44058. DOIPubMedGoogle Scholar
  2. Kitchel  B, Rasheed  JK, Patel  JB, Srinivasan  A, Navon-Venezia  S, Carmeli  Y, Molecular epidemiology of KPC-producing Klebsiella pneumoniae isolates in the United States: clonal expansion of multilocus sequence type 258. Antimicrob Agents Chemother. 2009;53:336570. DOIPubMedGoogle Scholar
  3. Nordmann  P, Cuzon  G, Naas  T. The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect Dis. 2009;9:22836. DOIPubMedGoogle Scholar
  4. Nordmann  P, Naas  T, Poirel  L. Global spread of carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis. 2011;17:17918. DOIPubMedGoogle Scholar
  5. Hanson  ND, Hossain  A, Buck  L, Moland  ES, Thomson  KS. First occurrence of a Pseudomonas aeruginosa isolate in the United States producing an IMP metallo-β-lactamase, IMP-18. Antimicrob Agents Chemother. 2006;50:22723. DOIPubMedGoogle Scholar
  6. Limbago  BM, Rasheed  JK, Anderson  KF, Zhu  W, Kitchel  B, Watz  N, IMP-producing carbapenem-resistant K. pneumoniae in the United States. J Clin Microbiol. 2011;49:423945. DOIPubMedGoogle Scholar
  7. Gupta  N, Limbago  BM, Patel  JB, Kallen  AJ. Carbapenem-resistant Enterobacteriaceae: epidemiology and prevention. Clin Infect Dis. 2011;53:607. DOIPubMedGoogle Scholar
  8. Centers for Disease Control and Prevention. Detection of Enterobacteriaceae isolates carrying metallo-beta-lactamase—United States, 2010. MMWR Morb Mortal Wkly Rep. 2010;59:750 .PubMedGoogle Scholar
  9. Peirano  G, Schreckenberger  PC, Pitout  JD. Characteristics of NDM-1-producing Escherichia coli isolates that belong to the successful and virulent clone ST131. Antimicrob Agents Chemother. 2011;55:29868. DOIPubMedGoogle Scholar
  10. Mochon  AB, Garner  OB, Hindler  JA, Krogstad  P, Ward  KW, Lewinski  MA, New Delhi metallo-β-lactamase (NDM-1)–producing Klebsiella pneumoniae: case report and laboratory detection strategies. J Clin Microbiol. 2011;49:166770. DOIPubMedGoogle Scholar
  11. Centers for Disease Control and Prevention. Carbapenem-resistant Enterobacteriaceae containing New Delhi metallo-beta-lactamase in two patients—Rhode Island, March 2012. MMWR Morb Mortal Wkly Rep. 2012;61:4468 .PubMedGoogle Scholar
  12. Savard  P, Gopinath  R, Zhu  W, Kitchel  B, Rasheed  JK, Tekle  T, The first NDM-positive Salmonella spp. identified in the United States. Antimicrob Agents Chemother. 2011;55:59578. DOIPubMedGoogle Scholar
  13. Yong  D, Toleman  MA, Giske  CG, Cho  HS, Sundman  K, Lee  K, Characterization of a new metallo-β-lactamase gene, blaNDM-1, and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother. 2009;53:504654. DOIPubMedGoogle Scholar
  14. Walsh  TR, Weeks  J, Livermore  DM, Toleman  MA. 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. 2011;11:35562. DOIPubMedGoogle Scholar
  15. Kumarasamy  KK, Toleman  MA, Walsh  TR, Bagaria  J, Butt  F, Balakrishnan  R, Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis. 2010;10:597602. DOIPubMedGoogle Scholar
  16. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. Twenty-first informational supplement; CLSI document M100–S21. Wayne (PA): The Institute; 2011.
  17. Migliavacca  R, Docquier  JD, Mugnaioli  C, Amicosante  G, Daturi  R, Lee  K, Simple microdilution test for detection of metallo-β-lactamase production in Pseudomonas aeruginosa. J Clin Microbiol. 2002;40:438890. DOIPubMedGoogle Scholar
  18. Yang  S, Lin  S, Kelen  GD, Quinn  TC, Dick  JD, Gaydos  CA, Quantitative multiprobe PCR assay for simultaneous detection and identification to species level of bacterial pathogens. J Clin Microbiol. 2002;40:344954. DOIPubMedGoogle Scholar
  19. Kitchel  B, Rasheed  JK, Endimiani  A, Hujer  AM, Anderson  KF, Bonomo  RA, Genetic factors associated with elevated carbapenem resistance in KPC-producing Klebsiella pneumoniae. Antimicrob Agents Chemother. 2010;54:42017. DOIPubMedGoogle Scholar
  20. Vivian  A. Plasmid expansion? Microbiology. 1994;140:2134 and. DOIPubMedGoogle Scholar
  21. Macrina  FL, Kopecko  DJ, Jones  KR, Ayers  DJ, McCowen  SM. A multiple plasmid-containing Escherichia coli strain: convenient source of size reference plasmid molecules. Plasmid. 1978;1:41720. DOIPubMedGoogle Scholar
  22. Johnson  TJ, Wannemuehler  YM, Johnson  SJ, Logue  CM, White  DG, Doetkott  C, Plasmid replicon typing of commensal and pathogenic Escherichia coli isolates. Appl Environ Microbiol. 2007;73:197683. DOIPubMedGoogle Scholar
  23. Bogaerts  P, Hujer  AM, Naas  T, de Castro  RR, Endimiani  A, Nordmann  P, Multicenter evaluation of a new DNA microarray for rapid detection of clinically relevant bla genes from β-lactam-resistant gram-negative bacteria. Antimicrob Agents Chemother. 2011;55:445760. DOIPubMedGoogle Scholar
  24. Berçot  B, Poirel  L, Nordmann  P. Updated multiplex polymerase chain reaction for detection of 16S rRNA methylases: high prevalence among NDM-1 producers. Diagn Microbiol Infect Dis. 2011;71:4425. DOIPubMedGoogle Scholar
  25. Diancourt  L, Passet  V, Verhoef  J, Grimont  PA, Brisse  S. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol. 2005;43:417882. DOIPubMedGoogle Scholar
  26. Jaureguy  F, Landraud  L, Passet  V, Diancourt  L, Frapy  E, Guigon  G, Phylogenetic and genomic diversity of human bacteremic Escherichia coli strains. BMC Genomics. 2008;9:560. DOIPubMedGoogle Scholar
  27. Wirth  T, Falush  D, Lan  R, Colles  F, Mensa  P, Wieler  LH, Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol. 2006;60:113651. DOIPubMedGoogle Scholar
  28. Poirel  L, Dortet  L, Bernabeu  S, Nordmann  P. Genetic features of blaNDM-1-positive Enterobacteriaceae. Antimicrob Agents Chemother. 2011;55:54037. DOIPubMedGoogle Scholar
  29. Anderson  KF, Rasheed  JK, Kitchel  B, Wong  B, Clark  N, Limbago  B. Validation of a broth screen for the detection of metallo-β-lactamase. In: Abstracts of the 111th General Meeting, American Society of Microbiology, New Orleans, May 21–24, 2011. Washington (DC): American Society for Microbiology Press; 2011. Abstract no. C-611, p. 104.
  30. Williamson  DA, Sidjabat  HE, Freeman  JT, Roberts  SA, Silvey  A, Woodhouse  R, Identification and molecular characterisation of New Delhi metallo-β-lactamase-1 (NDM-1)– and NDM-6–producing Enterobacteriaceae from New Zealand hospitals. Int J Antimicrob Agents. 2012;39:52933 . DOIPubMedGoogle Scholar
  31. Novais  A, Canton  R, Moreira  R, Peixe  L, Baquero  F, Coque  TM. Emergence and dissemination of Enterobacteriaceae isolates producing CTX-M-1–like enzymes in Spain are associated with IncFII (CTX-M-15) and broad-host-range (CTX-M-1, -3, and -32) plasmids. Antimicrob Agents Chemother. 2007;51:7969 . DOIPubMedGoogle Scholar
  32. Carattoli  A. Resistance plasmid families in Enterobacteriaceae. Antimicrob Agents Chemother. 2009;53:222738. DOIPubMedGoogle Scholar
  33. Giske  CG, Froding  I, Hasan  CM, Turlej-Rogacka  A, Toleman  M, Livermore  D, Diverse sequence types of Klebsiella pneumoniae contribute to the dissemination of blaNDM-1 in India, Sweden, and the United Kingdom. Antimicrob Agents Chemother. 2012;56:27358. DOIPubMedGoogle Scholar
  34. Damjanova  I, Toth  A, Paszti  J, Hajbel-Vekony  G, Jakab  M, Berta  J, Expansion and countrywide dissemination of ST11, ST15 and ST147 ciprofloxacin-resistant CTX-M-15-type β-lactamase-producing Klebsiella pneumoniae epidemic clones in Hungary in 2005–the new ‘MRSAs’? J Antimicrob Chemother. 2008;62:97885. DOIPubMedGoogle Scholar
  35. Qi  Y, Wei  Z, Ji  S, Du  X, Shen  P, Yu  Y. ST11, the dominant clone of KPC-producing Klebsiella pneumoniae in China. J Antimicrob Chemother. 2011;66:30712. DOIPubMedGoogle Scholar
  36. Peirano  G, Pillai  DR, Pitondo-Silva  A, Richardson  D, Pitout  JD. The characteristics of NDM-producing Klebsiella pneumoniae from Canada. Diagn Microbiol Infect Dis. 2011;71:1069. DOIPubMedGoogle Scholar
  37. Sidjabat  H, Nimmo  GR, Walsh  TR, Binotto  E, Htin  A, Hayashi  Y, Carbapenem resistance in Klebsiella pneumoniae due to the New Delhi metallo-β-lactamase. Clin Infect Dis. 2011;52:4814. DOIPubMedGoogle Scholar
  38. Kitchel  B, Sundin  DR, Patel  JB. Regional dissemination of KPC-producing Klebsiella pneumoniae. Antimicrob Agents Chemother. 2009;53:45113. DOIPubMedGoogle Scholar
  39. Coque  TM, Novais  A, Carattoli  A, Poirel  L, Pitout  J, Peixe  L, Dissemination of clonally related Escherichia coli strains expressing extended-spectrum β-lactamase CTX-M-15. Emerg Infect Dis. 2008;14:195200. DOIPubMedGoogle Scholar
  40. Nordmann  P, Poirel  L, Toleman  MA, Walsh  TR. Does broad-spectrum β-lactam resistance due to NDM-1 herald the end of the antibiotic era for treatment of infections caused by gram-negative bacteria? J Antimicrob Chemother. 2011;66:68992. DOIPubMedGoogle Scholar

Main Article

Page created: May 20, 2013
Page updated: May 20, 2013
Page reviewed: May 20, 2013
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.