Skip to main content
×
×
Home

The Complex Epidemiology of Carbapenem-Resistant Enterobacter Infections: A Multicenter Descriptive Analysis

  • Tsilia Lazarovitch (a1), Keren Amity (a2), Joseph R. Coyle (a3), Benjamin Ackerman (a4), Ruthy Tal-Jasper (a5), Hadas Ofer-Friedman (a3), Kayoko Hayakawa (a6), Christopher Bogan (a6), Paul R. Lephart (a6), Tamir Kaplansky (a4), Moran Maskit (a4), Tal Azouri (a4), Ronit Zaidenstein (a2) (a4), Federico Perez (a7) (a8), Robert A. Bonomo (a7) (a8) (a9) (a10) (a11), Keith S. Kaye (a6) and Dror Marchaim (a4) (a5)...
Abstract
BACKGROUND

The pandemic of carbapenem-resistant Enterobacteriaceae (CRE) was primarily due to clonal spread of bla KPC producing Klebsiella pneumoniae. Thus, thoroughly studied CRE cohorts have consisted mostly of K. pneumoniae.

OBJECTIVE

To conduct an extensive epidemiologic analysis of carbapenem-resistant Enterobacter spp. (CREn) from 2 endemic and geographically distinct centers.

METHODS

CREn were investigated at an Israeli center (Assaf Harofeh Medical Center, January 2007 to July 2012) and at a US center (Detroit Medical Center, September 2008 to September 2009). bla KPC genes were queried by polymerase chain reaction. Repetitive extragenic palindromic polymerase chain reaction and pulsed-field gel electrophoresis were used to determine genetic relatedness.

RESULTS

In this analysis, 68 unique patients with CREn were enrolled. Sixteen isolates (24%) were from wounds, and 33 (48%) represented colonization only. All isolates exhibited a positive Modified Hodge Test, but only 93% (27 of 29) contained bla KPC. Forty-three isolates (63%) were from elderly adults, and 5 (7.4%) were from neonates. Twenty-seven patients died in hospital (40.3% of infected patients). Enterobacter strains consisted of 4 separate clones from Assaf Harofeh Medical Center and of 4 distinct clones from Detroit Medical Center.

CONCLUSIONS

In this study conducted at 2 distinct CRE endemic regions, there were unique epidemiologic features to CREn: (i) polyclonality, (ii) neonates accounting for more than 7% of cohort, and (iii) high rate of colonization (almost one-half of all cases represented colonization). Since false-positive Modified Hodge Tests in Enterobacter spp. are common, close monitoring of carbapenem resistance mechanisms (particularly carbapenemase production) among Enterobacter spp. is important.

Infect. Control Hosp. Epidemiol. 2015;36(11):1283–1291

Copyright
Corresponding author
Address correspondence to Dror Marchaim, MD, Unit of Infectious Diseases, Assaf Harofeh Medical Center, Zerifin, 70300, Israel (drormarchaim@gmail.com).
Footnotes
Hide All
*

T. L. and K. A. contributed equally to this article.

Footnotes
References
Hide All
1. Sievert, DMP, Ricks, PP, JRMS, Edwards, et al. Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009–2010. Infect Control Hosp Epidemiol 2013;34:114.
2. Peleg, AY, Hooper, DC. Hospital-acquired infections due to gram-negative bacteria. N Engl J Med 2010;362:18041813.
3. Schwaber, MJ, Graham, CS, Sands, BE, Gold, HS, Carmeli, Y. Treatment with a broad-spectrum cephalosporin versus piperacillin-tazobactam and the risk for isolation of broad-spectrum cephalosporin-resistant Enterobacter species. Antimicrob Agents Chemother 2003;47:18821886.
4. Marchaim, D, Navon-Venezia, S, Schwaber, MJ, Carmeli, Y. Isolation of imipenem-resistant Enterobacter species: emergence of KPC-2 carbapenemase, molecular characterization, epidemiology, and outcomes. Antimicrob Agents Chemother 2008;52:14131418.
5. Guidance for control of infections with carbapenem-resistant or carbapenemase-producing Enterobacteriaceae in acute care facilities. MMWR Morb Mortal Wkly Rep 2009;58:256260.
6. Schwaber, MJ, Carmeli, Y. Carbapenem-resistant Enterobacteriaceae: a potential threat. JAMA 2008;300:29112913.
7. Schwaber, MJ, Lev, B, Israeli, A, et al. Containment of a country-wide outbreak of carbapenem-resistant Klebsiella pneumoniae in Israeli hospitals via a nationally implemented intervention. Clin Infect Dis 2011;52:848855.
8. Marchaim, D, Chopra, T, Bhargava, A, et al. Recent exposure to antimicrobials and carbapenem-resistant Enterobacteriaceae: the role of antimicrobial stewardship. Infect Control Hosp Epidemiol 2012;33:817830.
9. Marchaim, D, Chopra, T, Perez, F, et al. Outcomes and genetic relatedness of carbapenem-resistant Enterobacteriaceae at Detroit Medical Center. Infect Control Hosp Epidemiol 2011;32:861871.
10. Schwaber, MJ, Klarfeld-Lidji, S, Navon-Venezia, S, Schwartz, D, Leavitt, A, Carmeli, Y. Predictors of carbapenem-resistant Klebsiella pneumoniae acquisition among hospitalized adults and effect of acquisition on mortality. Antimicrob Agents Chemother 2008;52:10281033.
11. Bogan, C, Kaye, KS, Chopra, T, et al. Outcomes of carbapenem-resistant Enterobacteriaceae isolation: matched analysis. Am J Infect Control 2014;42:612620.
12. Qureshi, ZA, Paterson, DL, Peleg, AY, et al. Clinical characteristics of bacteraemia caused by extended-spectrum beta-lactamase-producing Enterobacteriaceae in the era of CTX-M-type and KPC-type beta-lactamases. Clin Microbiol Infect 2012;18:887893.
13. CLSI. Performance standards for antimibrobial susceptibility testing 19th informational supplement. Wayne, PA: Clinical and Laboratory Standards Institute, 2009, M100-S19.
14. Marchaim, D, Bogan, C, Lazarovitch, T, Kaye, KS. Outcomes of carbapenem-resistant Enterobacteriaceae isolation: a case-case-case-control investigation. In Program and abstracts of the Israeli Society of Infectious Diseases Annual Convention 2013. Mitspe-Ramon.
15. Marchaim, D, Chopra, T, Bogan, C, et al. The burden of multidrug-resistant organisms on tertiary hospitals posed by patients with recent stays in long-term acute care facilities. Am J Infect Control 2012;40:760765.
16. Marchaim, D, Chopra, T, Pogue, JM, et al. Outbreak of colistin-resistant, carbapenem-resistant Klebsiella pneumoniae in metropolitan Detroit, Michigan. Antimicrob Agents Chemother 2011;55:593599.
17. Marchaim, D, Perez, F, Lee, J, et al. “Swimming in resistance”: co-colonization with carbapenem-resistant Enterobacteriaceae and Acinetobacter baumannii or Pseudomonas aeruginosa . Am J Infect Control 2012;40:830835.
18. Marchaim, D, Zaidenstein, R, Lazarovitch, T, Karpuch, Y, Ziv, T, Weinberger, M. Epidemiology of bacteremia episodes in a single center: increase in gram-negative isolates, antibiotics resistance, and patient age. Eur J Clin Microbiol Infect Dis 2008;27:10451051.
19. Dellinger, RP, Levy, MM, Carlet, JM, et al. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2008. Crit Care Med 2008;36:296327.
20. Horan, TC, Andrus, M, Dudeck, MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control 2008;36:309332.
21. European Committee on Antimicrobial Susceptibility Testing. Clinical breakpoints. http://www.srga.org/eucastwt/MICTAB/index.html. Accessed August 9, 2015.
22. Endimiani, A, Depasquale, JM, Forero, S, et al. Emergence of blaKPC-containing Klebsiella pneumoniae in a long-term acute care hospital: a new challenge to our healthcare system. J Antimicrob Chemother 2009;64:11021110.
23. Endimiani, A, Hujer, AM, Perez, F, et al. Characterization of blaKPC-containing Klebsiella pneumoniae isolates detected in different institutions in the Eastern USA. J Antimicrob Chemother 2009;63:427437.
24. Adler, A, Paikin, S, Sterlin, Y, et al. A swordless knight: epidemiology and molecular characteristics of the blaKPC-negative sequence type 258 Klebsiella pneumoniae clone. J Clin Microbiol 2012;50:31803185.
25. Samra, Z, Ofir, O, Lishtzinsky, Y, Madar-Shapiro, L, Bishara, J. Outbreak of carbapenem-resistant Klebsiella pneumoniae producing KPC-3 in a tertiary medical centre in Israel. Int J Antimicrob Agents 2007;30:525529.
26. Tenover, FC, Arbeit, RD, Goering, RV, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 1995;33:22332239.
27. Charlson, ME, Pompei, P, Ales, KL, MacKenzie, CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 1987;40:373383.
28. Bion, JF, Edlin, SA, Ramsay, G, McCabe, S, Ledingham, IM. Validation of a prognostic score in critically ill patients undergoing transport. Br Med J (Clin Res Ed) 1985;291:432434.
29. Katz, S, Ford, AB, Moskowitz, RW, Jackson, BA, Jaffe, MW. Studies of illness in the aged: the index of Adl: a standardized measure of biological and psychosocial function. JAMA 1963;185:914919.
30. McGrath, EJ, Chopra, T, Abdel-Haq, N, et al. An outbreak of carbapenem-resistant Acinetobacter baumannii infection in a neonatal intensive care unit: investigation and control. Infect Control Hosp Epidemiol 2011;32:3441.
31. Macharashvili, N, Kourbatova, E, Butsashvili, M, Tsertsvadze, T, McNutt, LA, Leonard, MK. Etiology of neonatal blood stream infections in Tbilisi, Republic of Georgia. Int J Infect Dis 2009;13:499505.
32. Mahmood, A, Karamat, KA, Butt, T. Neonatal sepsis: high antibiotic resistance of the bacterial pathogens in a neonatal intensive care unit in Karachi. J Pak Med Assoc 2002;52:348350.
33. Carmeli, Y, Grisaru-Soen, G, Leavitt, A, Schwaber, M, Dolberg, S, Navon-Venezia, S. Imipenem resistant Enterobacter cloacae (IMP R EntC) causing an outbreak in a neonatal intensive care unit (NICU) likely introduced by a family member. In: Program and abstracts of Interscience Conference of Antimicrobial Agents and Chemotherapy; 2006; San Francisco, CA.
34. Jacoby, GA. AmpC beta-lactamases. Clin Microbiol Rev 2009;22:161182.
35. Friedman, ND, Kaye, KS, Stout, JE, et al. Health care–associated bloodstream infections in adults: a reason to change the accepted definition of community-acquired infections. Ann Intern Med 2002;137:791797.
36. Schechner, V, Kotlovsky, T, Tarabeia, J, et al. Predictors of rectal carriage of carbapenem-resistant Enterobacteriaceae (CRE) among patients with known CRE carriage at their next hospital encounter. Infect Control Hosp Epidemiol 2011;32:497503.
37. Cuzon, G, Naas, T, Truong, H, et al. Worldwide diversity of Klebsiella pneumoniae that produce beta-lactamase blaKPC-2 gene. Emerg Infect Dis 2010;16:13491356.
38. Kitchel, B, Rasheed, JK, Patel, JB, et al. Molecular epidemiology of KPC-producing Klebsiella pneumoniae isolates in the United States: clonal expansion of multilocus sequence type 258. Antimicrob Agents Chemother 2009;53:33653370.
39. Doumith, M, Ellington, MJ, Livermore, DM, Woodford, N. Molecular mechanisms disrupting porin expression in ertapenem-resistant Klebsiella and Enterobacter spp. clinical isolates from the UK. J Antimicrob Chemother 2009;63:659667.
40. Adler, A, Navon-Venezia, S, Moran-Gilad, J, Marcos, E, Schwartz, D, Carmeli, Y. Laboratory and clinical evaluation of screening agar plates for detection of carbapenem-resistant Enterobacteriaceae from surveillance rectal swabs. J Clin Microbiol 2011;49:22392242.
41. Brennan, BM, Coyle, JR, Marchaim, D, et al. Statewide surveillance of carbapenem-resistant enterobacteriaceae in Michigan. Infect Control Hosp Epidemiol 2014;35:342349.
42. Borer, A, Saidel-Odes, L, Riesenberg, K, et al. Attributable mortality rate for carbapenem-resistant Klebsiella pneumoniae bacteremia. Infect Control Hosp Epidemiol 2009;30:972976.
43. Harris, AD. Control group selection is an important but neglected issue in studies of antibiotic resistance. Ann Intern Med 2000;132:925.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Infection Control & Hospital Epidemiology
  • ISSN: 0899-823X
  • EISSN: 1559-6834
  • URL: /core/journals/infection-control-and-hospital-epidemiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 13
Total number of PDF views: 103 *
Loading metrics...

Abstract views

Total abstract views: 692 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 19th August 2018. This data will be updated every 24 hours.