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      Antimicrobial Susceptibility of Acinetobacter calcoaceticus–Acinetobacter baumannii Complex and Stenotrophomonas maltophilia Clinical Isolates: Results From the SENTRY Antimicrobial Surveillance Program (1997–2016)

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          Abstract

          Background

          Acinetobacter calcoaceticus–A. baumannii ( Acb) complex and Stenotrophomonas maltophilia represent frequent causes of hospital-acquired infections. We evaluated the frequency and resistance rates of Acb complex and S. maltophilia isolates from medical centers enrolled in the SENTRY Program.

          Methods

          A total of 13 752 Acb complex and 6467 S. maltophilia isolates were forwarded to a monitoring laboratory by 259 participating sites from the Asia-Pacific region, Latin America, Europe, and North America between 1997 and 2016. Confirmation of species identification and antimicrobial susceptibility testing were performed using conventional methods and/or matrix-assisted laser desorption ionization–time of flight mass spectrometry and the broth microdilution method, respectively. Antimicrobial susceptibility results were interpreted by CLSI and EUCAST 2018 criteria.

          Results

          Acb complex and S. maltophilia were most frequently isolated from patients hospitalized with pneumonia (42.9% and 55.8%, respectively) and bloodstream infections (37.3% and 33.8%, respectively). Colistin and minocycline were the most active agents against Acb complex (colistin MIC 50/90, ≤0.5/2 mg/L; 95.9% susceptible) and S. maltophilia (minocycline MIC 50/90, ≤1/2 mg/L; 99.5% susceptible) isolates, respectively. Important temporal decreases in susceptibility rates among Acb complex isolates were observed for all antimicrobial agents in all regions. Rates of extensively drug-resistant Acb complex rates were highest in Europe (66.4%), followed by Latin America (61.5%), Asia-Pacific (56.9%), and North America (38.8%). Among S. maltophilia isolates, overall trimethoprim-sulfamethoxazole (TMP-SMX) susceptibility rates decreased from 97.2% in 2001–2004 to 95.7% in 2013–2016, but varied according to the geographic region.

          Conclusions

          We observed important reductions of susceptibility rates to all antimicrobial agents among Acb complex isolates obtained from all geographic regions. In contrast, resistance rates to TMP-SMX among S. maltophilia isolates remained low and relatively stable during the study period.

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          Most cited references47

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          Colistin resistance of Acinetobacter baumannii: clinical reports, mechanisms and antimicrobial strategies.

          Colistin is the last resort for treatment of multidrug-resistant Acinetobacter baumannii. Unfortunately, resistance to colistin has been reported all over the world. The highest resistance rate was reported in Asia, followed by Europe. The heteroresistance rate of A. baumannii to colistin is generally higher than the resistance rate. The mechanism of resistance might be loss of lipopolysaccharide or/and the PmrAB two-component system. Pharmacokinetic/pharmacodynamic studies revealed that colistin monotherapy is unable to prevent resistance, and combination therapy might be the best antimicrobial strategy against colistin-resistant A. baumannii. Colistin/rifampicin and colistin/carbapenem are the most studied combinations that showed promising results in vitro, in vivo and in the clinic. New peptides showing good activity against colistin-resistant A. baumannii are also being investigated.
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            Global spread of carbapenem-resistant Acinetobacter baumannii.

            We have investigated the molecular epidemiology and distribution of carbapenemase genes in 492 imipenem-non-susceptible Acinetobacter baumannii worldwide isolates (North and Latin America, Europe, Asia, South Africa and Australia). MICs were determined by broth microdilution and Etest. The presence of carbapenemase-encoding genes was investigated by PCR. Molecular epidemiology was performed by repetitive sequence-based PCR (rep-PCR; DiversiLab), sequence-type multiplex PCR and PFGE. Imipenem non-susceptibility was associated with ISAba1 upstream of the intrinsic bla(OXA-51-like) or the acquired carbapenemase bla(OXA-23-like), bla(OXA-40-like) or bla(OXA-58-like). Isolates were grouped into eight distinct clusters including European clones I, II and III. European clone II was the largest (246 isolates) and most widespread group (USA, pan-Europe, Israel, Asia, Australia and South Africa). The global dissemination of eight carbapenem-resistant lineages illustrates the success this organism has had in epidemic spread. The acquired OXA enzymes are widely distributed but are not the sole carbapenem resistance determinant in A. baumannii.
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              Global evolution of multidrug-resistant Acinetobacter baumannii clonal lineages.

              The rapid expansion of Acinetobacter baumannii clinical isolates exhibiting resistance to carbapenems and most or all available antibiotics during the last decade is a worrying evolution. The apparent predominance of a few successful multidrug-resistant lineages worldwide underlines the importance of elucidating the mode of spread and the epidemiology of A. baumannii isolates in single hospitals, at a country-wide level and on a global scale. The evolutionary advantage of the dominant clonal lineages relies on the capability of the A. baumannii pangenome to incorporate resistance determinants. In particular, the simultaneous presence of divergent strains of the international clone II and their increasing prevalence in international hospitals further support the ongoing adaptation of this lineage to the hospital environment. Indeed, genomic and genetic studies have elucidated the role of mobile genetic elements in the transfer of antibiotic resistance genes and substantiate the rate of genetic alterations associated with acquisition in A. baumannii of various resistance genes, including OXA- and metallo-β-lactamase-type carbapenemase genes. The significance of single nucleotide polymorphisms and transposon mutagenesis in the evolution of A. baumannii has been also documented. Establishment of a network of reference laboratories in different countries would generate a more complete picture and a fuller understanding of the importance of high-risk A. baumannii clones in the international dissemination of antibiotic resistance. Copyright © 2012 Elsevier B.V. and the International Society of Chemotherapy. All rights reserved.
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                Author and article information

                Journal
                Open Forum Infect Dis
                Open Forum Infect Dis
                ofid
                Open Forum Infectious Diseases
                Oxford University Press (US )
                2328-8957
                March 2019
                15 March 2019
                15 March 2019
                : 6
                : Suppl 1 , Global Surveillance of Antimicrobial Resistance: 20 Years of Experience with the SENTRY Program
                : S34-S46
                Affiliations
                [1 ]Universidade Federal de São Paulo, São Paulo, Brazil
                [2 ]Institute for Medical Microbiology, Immunology and Hygiene, University of Cologne, Cologne, Germany
                [3 ]German Centre for Infection Research, partner site Bonn-Cologne, Germany
                [4 ]Hacettepe University, Ankara, Turkey
                [5 ]JMI Laboratories, North Liberty, Iowa
                Author notes
                Correspondence: A. C. Gales, MD, PhD, Division of Infectious Diseases, Escola Paulista de Medicina, Universidade Federal de São Paulo, São Paulo, Brazil, Rua Pedro de Toledo, 781 - 6th Floor, São Paulo, SP 04039-032 ( ana.gales@ 123456gmail.com ).
                Article
                ofy293
                10.1093/ofid/ofy293
                6419908
                30895213
                9ead870e-e0d8-4e0b-988e-a634c02af818
                © The Author(s) 2019. Published by Oxford University Press on behalf of Infectious Diseases Society of America.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence ( http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                Page count
                Pages: 13
                Categories
                Supplement Articles

                gram-negative bacilli,nonfermentative,surveillance,multidrug resistance,carbapenem resistant

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