Variations in the Occurrence of Resistance Phenotypes and Carbapenemase Genes Among Enterobacteriaceae Isolates in 20 Years of the SENTRY Antimicrobial Surveillance Program

Mariana Castanheira, Lalitagauri M Deshpande, Rodrigo E Mendes, Rafael Canton, Helio S Sader, Ronald N Jones, Mariana Castanheira, Lalitagauri M Deshpande, Rodrigo E Mendes, Rafael Canton, Helio S Sader, Ronald N Jones

Abstract

Background: A total of 178 825 Enterobacteriaceae isolates collected in 199 hospitals from 42 countries worldwide over 20 years (1997 to 2016) of the SENTRY Program were susceptibility tested by reference broth microdilution methods.

Methods: Trends in percentages over time were analyzed by the χ2 test. Results were reported as the percentage difference between the first (1997-2000) and the last (2013-2016) time period.

Results: Enterobacteriaceae exhibiting resistance to cephalosporins (extended-spectrum β-lactamase [ESBL] phenotype) and carbapenem resistance (CRE) significantly increased (P < 0.05; χ2 test) from 10.3% to 24.0% and 0.6% to 2.9%, respectively. Similar trends were noted for all regions and infection sources. Klebsiella pneumoniae mainly drove the CRE increase. Multidrug-resistance (MDR) rates significantly increased from 7.3% to 15.3% overall, with important trends in all regions and infection sources. Significant increases were noted for MDR K. pneumoniae and Escherichia coli, polymyxin-resistant K. pneumoniae (2.0% to 5.5% overall), and aminoglycoside-resistant E. coli (7.0% to 18.0%) and K. pneumoniae (18.1% to 26.9%) over time in North America and Latin America. Carbapenemase-encoding genes were screened after 2007, and the occurrence of these genes was compared for 2007-2009 and 2014-2016. Among 1298 CRE isolates from the 2 study periods, bla KPC was detected among 186 (49.7%) and 501 (54.2%) isolates in 2007-2009 and 2014-2016, respectively. Metallo-β-lactamase genes were detected among 4.3% of the isolates from 2007 to 2009 and 12.7% of the isolates from 2014 to 2016, mainly due to the dissemination of isolates carrying bla NDM. Genes encoding IMP and VIM enzymes were observed in 1.9% and 2.4% (7 and 9 isolates) of the isolates from 2007 to 2009 and 0.4% and 1.9% of the isolates from 2014 to 2016. OXA-48 and variants increased from 4.3% in 2007-2009 to 12.6% in 2014-2016 (mainly in Europe).

Conclusions: A change in the epidemiology of carbapenemases and important increases in ESBL, CRE, MDR, and other resistant phenotypes among virtually all geographic regions and infection sources were noted in the 20 years of surveillance, highlighting the impact of antimicrobial resistance and the importance of its continuous monitoring.

Keywords: CRE; ESBL; Enterobacteriaceae; MDR; carbapenemases.

Figures

Figure 1.
Figure 1.
Geographic (A) and infection sources (B) of the Enterobacteriaceae isolates analyzed. aSkin and skin structure infection isolates were mainly recovered from wounds and abscesses.
Figure 2.
Figure 2.
Selected antimicrobial resistance trends for all Enterobacteriaceae by (A) infection source and (B) geographic region. Abbreviations: CRE, carbapenem-resistant Enterobacteriaceae; ESBL, extended-spectrum β-lactamase; MDR, multidrug-resistant.
Figure 3.
Figure 3.
Antimicrobial resistance trends for selected antimicrobial classes of (A) all Enterobacteriaceae or (B) bacterial species.
Figure 4.
Figure 4.
Carbapenem-resistant Enterobacteriaceae (CRE) trends over years by region.
Figure 5.
Figure 5.
Extended-spectrum β-lactamase (ESBL), carbapenem-resistant Enterobacteriaceae (CRE), and multidrug-resistant (MDR) rates among countries participating in the SENTRY Program. (Figure continues on next page)
Figure 5.
Figure 5.
Extended-spectrum β-lactamase (ESBL), carbapenem-resistant Enterobacteriaceae (CRE), and multidrug-resistant (MDR) rates among countries participating in the SENTRY Program. (Figure continues on next page)

References

    1. Rodríguez-Baño J, Pascual A. Clinical significance of extended-spectrum beta-lactamases. Expert Rev Anti Infect Ther 2008; 6:671–83.
    1. Rodriguez-Bano J, Gutierrez-Gutierrez B, Machuca I, Pascual A. Treatment of infections caused by extended-spectrum-beta-lactamase-, AmpC-, and carbapenemase-producing Enterobacteriaceae. Clin Microbiol Rev 2018; 31:e00079.
    1. Delgado-Valverde M, Sojo-Dorado J, Pascual A, Rodríguez-Baño J. Clinical management of infections caused by multidrug-resistant Enterobacteriaceae. Ther Adv Infect Dis 2013; 1:49–69.
    1. ECDC. Antimicrobial Resistance Surveillance in Europe: Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net), 2009. European Centre for Disease Prevetion and Control; 2010. Available at: . Accessed 30, August 2018.
    1. ECDC. Surveillance of Antimicrobial Resistance in Europe: Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net) 2016. European Centre for Disease Prevention and Control; 2017. Available at: . Accessed 30, August 2018.
    1. Pitout JD. Infections with extended-spectrum beta-lactamase-producing Enterobacteriaceae: changing epidemiology and drug treatment choices. Drugs 2010; 70:313–33.
    1. CLSI. M100Ed28E. Performance Standards for Antimicrobial Susceptibility Testing: 28th Informational Supplement. Wayne, PA: Clinical and Laboratory Standards Institute; 2018.
    1. CLSI. M07Ed11E. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically; Approved Standard. 11th ed Wayne, PA: Clinical and Laboratory Standards Institute; 2018.
    1. EUCAST. Breakpoint Tables for Interpretation of MIC’s and Zone Diameters. Version 8.0, January 2018. European Committee on Antimicrobial Susceptibility Testing; 2018. Available at: . Accessed 31, January 2018.
    1. Castanheira M, Mendes RE, Woosley LN, Jones RN. Trends in carbapenemase-producing Escherichia coli and Klebsiella spp. from Europe and the Americas: report from the SENTRY antimicrobial surveillance programme (2007-09). J Antimicrob Chemother 2011; 66:1409–11.
    1. Bankevich A, Nurk S, Antipov D, et al. . SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–77.
    1. Rossolini GM, D’Andrea MM, Mugnaioli C. The spread of CTX-M-type extended-spectrum beta-lactamases. Clin Microbiol Infect 2008; 14(Suppl 1):33–41.
    1. Cantón R, Coque TM. The CTX-M beta-lactamase pandemic. Curr Opin Microbiol 2006; 9:466–75.
    1. Livermore DM, Canton R, Gniadkowski M, et al. . CTX-M: changing the face of ESBLs in Europe. J Antimicrob Chemother 2007; 59:165–74.
    1. Nicolas-Chanoine MH, Bertrand X, Madec JY. Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev 2014; 27:543–74.
    1. Johnson JR, Porter S, Thuras P, Castanheira M. The pandemic H30 subclone of sequence type 131 (ST131) as the leading cause of multidrug-resistant Escherichia coli infections in the United States (2011–2012). Open Forum Infect Dis 2017; 4:ofx089.
    1. Johnson JR, Porter S, Thuras P, Castanheira M. Epidemic emergence in the United States of Escherichia coli sequence type 131-H30 (ST131-H30), 2000 to 2009. Antimicrob Agents Chemother 2017; 61:e00732.
    1. Johnson JR, Johnston B, Clabots C, et al. . Escherichia coli sequence type ST131 as the major cause of serious multidrug-resistant E. coli infections in the United States. Clin Infect Dis 2010; 51:286–94.
    1. Castanheira M, Mendes RE, Jones RN, Sader HS. Changes in the frequencies of β-lactamase genes among Enterobacteriaceae isolates in U.S. Hospitals, 2012 to 2014: activity of ceftazidime-avibactam tested against β-lactamase-producing isolates. Antimicrob Agents Chemother 2016; 60:4770–7.
    1. Rocha FR, Pinto VP, Barbosa FC. The spread of CTX-M-type extended-spectrum β-lactamases in Brazil: a systematic review. Microb Drug Resist 2016; 22:301–11.
    1. Calbo E, Garau J. The changing epidemiology of hospital outbreaks due to ESBL-producing Klebsiella pneumoniae: the CTX-M-15 type consolidation. Future Microbiol 2015; 10:1063–75.
    1. D’Andrea MM, Arena F, Pallecchi L, Rossolini GM. CTX-M-type β-lactamases: a successful story of antibiotic resistance. Int J Med Microbiol 2013; 303:305–17.
    1. Kaiser RM, Castanheira M, Jones RN, et al. . Trends in Klebsiella pneumoniae carbapenemase-positive K. pneumoniae in US hospitals: report from the 2007-2009 SENTRY Antimicrobial Surveillance Program. Diagn Microbiol Infect Dis 2013; 76:356–60.
    1. Logan LK, Weinstein RA. The epidemiology of carbapenem-resistant Enterobacteriaceae: the impact and evolution of a global menace. J Infect Dis 2017; 215:28–36.
    1. Jones RN. The emergent needs for basic research, education, and surveillance of antimicrobial resistance. Problems facing the report from the American Society for Microbiology Task Force on Antibiotic Resistance. Diagn Microbiol Infect Dis 1996; 25:153–61.
    1. Dalhoff A. Resistance surveillance studies: a multifaceted problem–the fluoroquinolone example. Infection 2012; 40:239–62.
    1. Tacconelli E, Sifakis F, Harbarth S, et al. . Surveillance for control of antimicrobial resistance. Lancet Infect Dis 2018; 18:e99–106.

Source: PubMed

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