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A. Kelly, B. Mathema, E. Larson (2017)Carbapenem-resistant Enterobacteriaceae in the community: a scoping review.
International journal of antimicrobial agents, 50 2
Israeli Ministry of Health. [In-patient institutions and units for day hospitalization in Israel
S. Karanika, T. Karantanos, Marios Arvanitis, Christos Grigoras, E. Mylonakis (2016)Fecal Colonization With Extended-spectrum Beta-lactamase-Producing Enterobacteriaceae and Risk Factors Among Healthy Individuals: A Systematic Review and Metaanalysis.
Clinical infectious diseases : an official publication of the Infectious Diseases Society of America, 63 3
Y. Doi, Y. Park, J. Rivera, J. Adams-Haduch, Ameet Hingwe, E. Sordillo, James Lewis, W. Howard, Laura Johnson, B. Polsky, J. Jorgensen, S. Richter, K. Shutt, D. Paterson (2013)Community-associated extended-spectrum β-lactamase-producing Escherichia coli infection in the United States.
Clinical infectious diseases : an official publication of the Infectious Diseases Society of America, 56 5
K. Woodworth, M. Walters, Lindsey Weiner, J. Edwards, Allison Brown, Jennifer Huang, S. Malik, R. Slayton, Prabasaj Paul, C. Capers, M. Kainer, Nancy Wilde, Alicia Shugart, G. Mahon, A. Kallen, J. Patel, L. McDonald, A. Srinivasan, Micah Craig, D. Cardo (2018)Vital Signs: Containment of Novel Multidrug-Resistant Organisms and Resistance Mechanisms — United States, 2006–2017
Morbidity and Mortality Weekly Report, 67
M. Schwaber, Y. Carmeli (2017)The Impact of a Carbapenem-Resistant Enterobacteriaceae Outbreak on Facilitating Development of a National Infrastructure for Infection Control in Israel
Clinical Infectious Diseases, 65
D. Karfunkel, Y. Carmeli, I. Chmelnitsky, T. Kotlovsky, S. Navon-Venezia, S. Navon-Venezia (2013)The emergence and dissemination of CTX-M-producing Escherichia coli sequence type 131 causing community-onset bacteremia in Israel
European Journal of Clinical Microbiology & Infectious Diseases, 32
M. Schwaber, B. Lev, A. Israeli, E. Solter, G. Smollan, B. Rubinovitch, I. Shalit, Y. Carmeli (2011)Containment of a country-wide outbreak of carbapenem-resistant Klebsiella pneumoniae in Israeli hospitals via a nationally implemented intervention.
Clinical infectious diseases : an official publication of the Infectious Diseases Society of America, 52 7
R. Blough (1968)The World Bank Group
International Organization, 22
EUCAST warnings concerning antimicrobial susceptibility testing products or procedures
Debby Ben-David, Samira Masarwa, A. Adler, Hagit Mishali, Y. Carmeli, M. Schwaber (2014)A National Intervention to Prevent the Spread of Carbapenem-Resistant Enterobacteriaceae in Israeli Post-Acute Care Hospitals
Infection Control & Hospital Epidemiology, 35
KR Woodworth, MS Walters, LM Weiner, J Edwards, AC Brown, JY Huang (2018)Vital signs: containment of novel multidrug-resistant organisms and resistance mechanisms - United States, 2006-2017
MMWR Morb Mortal Wkly Rep, 67
M. Schwaber, Y. Carmeli (2014)An ongoing national intervention to contain the spread of carbapenem-resistant enterobacteriaceae.
Clinical infectious diseases : an official publication of the Infectious Diseases Society of America, 58 5
Ali Kassim, G. Omuse, Z. Premji, G. Revathi (2016)Comparison of Clinical Laboratory Standards Institute and European Committee on Antimicrobial Susceptibility Testing guidelines for the interpretation of antibiotic susceptibility at a University teaching hospital in Nairobi, Kenya: a cross-sectional study
Annals of Clinical Microbiology and Antimicrobials, 15
Debby Ben-David, Samira Masarwa, N. Fallach, E. Temkin, E. Solter, Y. Carmeli, M. Schwaber (2018)Success of a National Intervention in Controlling Carbapenem-resistant Enterobacteriaceae in Israel’s Long-term Care Facilities
Clinical Infectious Diseases, 68
B. Chazan, R. Raz, N. Teitler, O. Nitzan, H. Edelstein, R. Colodner (2009)Epidemiology and susceptibility to antimicrobials in community, hospital and long-term care facility bacteremia in northern Israel: a 6 year surveillance.
The Israel Medical Association journal : IMAJ, 11 10
R. Ben-Ami, M. Schwaber, S. Navon-Venezia, D. Schwartz, M. Giladi, I. Chmelnitsky, A. Leavitt, Y. Carmeli (2006)Influx of extended-spectrum beta-lactamase-producing enterobacteriaceae into the hospital.
Clinical infectious diseases : an official publication of the Infectious Diseases Society of America, 42 7
S. Tschudin-Sutter, J. Lucet, N. Mutters, E. Tacconelli, J. Zahar, S. Harbarth (2017)Contact Precautions for Preventing Nosocomial Transmission of Extended-Spectrum β Lactamase-Producing Escherichia coli: A Point/Counterpoint Review.
Clinical infectious diseases : an official publication of the Infectious Diseases Society of America, 65 2
We analyzed Israeli national data on antimicrobial susceptibility from bloodstream isolates collected between 2014 and 2017 and compared resistance proportions with those of Europe. The incidence of bloodstream infection (BSI) caused by most antibiotic-resistant organisms remained unchanged or decreased. An exception was increased incidence of BSI caused by third-generation cephalosporin-resistant Escherichia coli. Overall, resistance proportions were similar to those observed in southern Europe, with the exception of a lower proportion of carbapenem-resistant Klebsiella pneumoniae in Israel. Keywords: Antibiogram, Antibiotic, Bloodstream isolate, CRE, ESBL, Israel, MRSA, Resistance, Surveillance, VRE The Israel National Center for Infection Control (NCIC), combining more than one antibiotic agent, resistance to a unit of the Ministry of Health (MoH), has been monitor- any agent within a class was regarded as resistance to the ing antimicrobial resistance in selected bacteria in hospital class. bloodstream isolates since 2013 in the context of a na- Data on blood isolates were collated and an antibio- tional infection control program . As part of the pro- gram prepared for selected bacteria of epidemiological gram, all acute-care hospitals in Israel are required to importance. All hospitals contributed data on all organ- submit a monthly report to the NCIC with isolate-level isms for each year. For each organism, only the first iso- data on all blood cultures growing seven sentinel bacteria. late per patient per year was considered. Data on colistin These data are utilized to provide monthly feedback to the resistance for 2017 were not reported in accordance with hospitals on the incidence of bacteremia with resistant the European Committee on Antimicrobial Susceptibility organisms and annually to generate institutional- and Testing (EUCAST) warning concerning results of sus- national-level antibiograms. The present report presents ceptibility testing . Data on population size were taken surveillance data on antimicrobial susceptibility testing in from the World Bank  while annual patient days were Israel in the period 2014–2017 and compares them with taken from statistics regularly distributed by the MoH similar data from Europe. [4–7]. Data used for comparison were taken from the 2017 report published by the European Antimicrobial Resistance Surveillance Network (EARS-Net) . The Antimicrobial resistance surveillance and Cochran-Armitage test was used to test for significant reporting changes over time in the proportion of isolates that were Data on antimicrobial resistance in bloodstream bacter- resistant. We tested for significant changes over time in ial isolates were collected from inpatient medical records bloodstream infection (BSI) incidence using Poisson in all departments in Israel’s acute-care hospitals. An regression or negative binomial regression (when data isolate was considered resistant when reported by the were overdispersed). All calculations were performed hospital’s clinical microbiology laboratory as intermediately with STATA v14.2 (StataCorp LLC, College Station, TX). susceptible (I) or resistant (R). For antibiotic categories * Correspondence: Yaakov.firstname.lastname@example.org; email@example.com Surveillance findings National Center for Infection Control, Ministry of Health, Weizmann 6, Data on the incidence of bloodstream infection (BSI) 6423906 Tel Aviv, Israel Full list of author information is available at the end of the article and the proportion of isolates that were resistant are © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Dickstein et al. Antimicrobial Resistance and Infection Control (2019) 8:96 Page 2 of 5 presented in Tables 1 and 2. The following trends were patient-days (p = 0.04). The percentage of observed: methicillin-resistant S.aureus isolates decreased from 38.2 to 30.6% (p < 0.001). – A decrease in the incidence of all Acinetobacter – The combined incidence of A. baumannii, E. baumannii BSI (14.5 to 12.1 per 100,000 patient- faecium, K. pneumoniae and P. aeruginosa BSI days, p < 0.001) and the incidence of carbapenem- remained unchanged (89.5 to 93.4 per 100,000 resistant A. baumannii BSI (11.5 to 9.5 per 100,000 patient-days, p = 0.14), as did the combined incidence patient-days, p = 0.001), while the proportion of A. of VREf and carbapenem-resistant A. baumannii, K. baumannii isolates resistant to carbapenems pneumoniae and P. aeruginosa (18.8 to 16.3 per remained stable at 75–80%. 100,000 patient-days, p =0.090). – An increase in the incidence of all Enterococcus faecium BSI (6.5 to 8.2 per 100,000 patient-days, In general, resistance proportions were similar to those p = 0.001), while the incidence of vancomycin- reported by countries in southern Europe (Italy and resistant Enterococcus faecium (VREf) BSI remained Greece), with the exception of carbapenem-resistant and unchanged (1.7 to 1.6 per 100,000 patient-days, p = combined 3GC-, fluoroquinolone- and aminoglycoside- 0.60). The proportion of E. faecium isolates resistant resistant K. pneumoniae, for which the proportions were to vancomycin decreased (25.6 to 19.0%, p = 0.020). lower in Israel (4.0%/19.2%, respectively, in 2017, vs – Increases in the incidence of all Escherichia coli BSI 29.7/31.6%% in Italy and 64.7/47.9%% in Greece) and (101.6 to 110.9 per 100,000 patient-days, p < 0.001), carbapenem-resistant P. aeruginosa, for which the pro- 3rd-generation cephalosporin (3GC)-resistant E. coli portion was lower in Israel (13.0%) than in Greece BSI (24.1 to 32.4 per 100,000 patient-days, p < (39.3%) . 0.001), and the proportion of E. coli isolates resistant to 3GC (29.5 to 32.0%, p = 0.017). The proportion of Discussion E. coli isolates with combined resistance to 3GC, In Israel between 2014 and 2017, the incidence of BSI fluoroquinolones and aminoglycosides decreased caused by most antibiotic-resistant organisms remained from 10.6 to 8.3% (p < 0.001); the incidence of BSI unchanged or decreased. An exception was the inci- caused by these pathogens did not change significantly dence of BSI caused by 3GC-resistant E. coli, which in- (8.7 to 8.2 per 100,000 patient-days (p =0.40). creased. Overall, resistance proportions were similar to – No significant change in the incidence of all those observed in southern Europe, with the exception Klebsiella pneumoniae BSI (46.3 to 47.4 per 100,000 of carbapenem-resistant K. pneumoniae, for which the patient-days, p = 0.35), carbapenem-resistant K. resistance proportion in Israel was markedly lower. pneumoniae BSI (2.1 to 1.9 per 100,000 patient-days, Following an outbreak of carbapenem-resistant En- p = 0.58) or in the proportion of carbapenem-resistant terobacteriaceae (CRE) in Israeli health-care facilities in isolates (4.6 to 4.0%, p = 0.36). The proportion of K. 2006, a national intervention was implemented to iden- pneumoniae isolates with combined resistance to 3GC, tify carriers of CRE and prevent ongoing transmission fluoroquinolones and aminoglycosides decreased from . The intervention succeeded in reducing the incidence 23.7 to 19.2% (p = 0.002) while the incidence of BSI of CRE acquisition and subsequently overall CRE preva- caused by these strains remained unchanged (8.0 per lence in Israel [10–12]. This success catalyzed a broader 100,000 patient-days, p =0.80). nationwide infection control (IC) program which, apart – The incidence of Pseudomonas aeruginosa BSI from surveillance of antimicrobial susceptibility, included increased (22.2 to 25.7 per 100,000 patient-days, p < the establishment of a central reference laboratory, en- 0.001), while the incidence of carbapenem-resistant hancement of IC programs within individual healthcare P. aeruginosa remained unchanged (3.5 to 3.3 per institutions and the creation of a national antibiotic 100,000 patient-days, p = 0.72). The observed de- stewardship program . Thus, the trends toward de- crease in the proportion of carbapenem-resistant creasing incidence of many antibiotic-resistant organisms isolates did not achieve statistical significance (16.0 reported here occurred in the context of an intensive, to 13.0%, p = 0.057). nationally-coordinated IC effort which included the use of – The incidence of all Staphylococcus aureus BSI antimicrobial susceptibility data to plan and prioritize fo- increased, from 42.4 to 47.1 per 100,000 patient-days cused interventions where warranted. (p < 0.001), driven by the rising incidence of This report has a number of limitations. First, there is methicillin-susceptible S. aureus BSI (26.2 to 32.7 no national standard for reporting of antimicrobial sus- per 100,000 patient-days, p < 0.001). The incidence ceptibility. Although most microbiology laboratories in of BSI caused by methicillin-resistant S. aureus Israel employ Clinical and Laboratory Standards Institute (MRSA) declined from 16.2 to 14.4 per 100,000 (CLSI) breakpoints, this is not mandatory. Thus, it is Dickstein et al. Antimicrobial Resistance and Infection Control (2019) 8:96 Page 3 of 5 Table 1 Percentage of Resistant Isolates, Israel, 2014–2017 HL High level, MRSA methicillin-resistant S. aureus, MSSA methicillin-susceptible S. aureus, ND No data, Sulfa Sulfamethoxazole possible that for certain antibiotic categories for which EUCAST criteria. However, given that differences where CLSI breakpoints are higher than those issued by the present tend to be relatively small (i.e. one dilution), we European Committee on Antimicrobial Susceptibility believe that the general comparison with EARS-Net data Testing (EUCAST), levels of antimicrobial resistance as remains valid . Second, we do not differentiate resist- we reported are lower than they would be utilizing ance levels between community-acquired and hospital- Dickstein et al. Antimicrobial Resistance and Infection Control (2019) 8:96 Page 4 of 5 Table 2 Percentage and Incidence of Combined Resistance Phenotypes, Israel, 2014–2017 2014 2015 2016 2017 Bacterial name Percentage Incidence Percentage Incidence Percentage Incidence Percentage of Incidence of resistant per 100,000 of resistant per 100,000 of resistant per 100,000 resistant isolates per 100,000 isolates patient-days isolates patient-days isolates patient-days patient-days A. baumannii Carb+FQ + AG 73.2 8.4 74.2 9.3 72.2 7.8 70.1 7.2 E. coli 3GC 29.5 24.1 32.0 30.2 32.4 32.3 32.0 32.4 E. coli 3GC + FQ + AG 10.6 8.7 10.3 9.7 9.3 9.1 8.3 8.2 K. pneumoniae 3GC + FQ + AG 23.7 8.0 20.8 7.6 20.7 8.3 19.2 8.0 K. pneumoniae Carb+Col 1.8 0.2 0.6 0.0 0.4 0.0 ND ND AG Aminoglycoside-resistant, Carb Carbapenem-resistant, Col Colistin-resistant, FQ Fluoroquinolone-resistant, 3GC 3rd-generation cephalosporin-resistant acquired/health care-associated infections. Thus, is it EARS-Net: European Antimicrobial Resistance Surveillance Network; ESBL: Extended-spectrum β-lactamase; EUCAST: European Committee on likely that for nosocomial infections, the resistance levels Antimicrobial Susceptibility Testing; I: Intermediate susceptibility; IC: Infection are higher than what we have reported. control; MoH: Ministry of Health; MRSA: Methicillin-resistant Staphylococcus aureus; As noted above, the success of the intervention for NCIC: National Center for Infection Control; R: Resistant; VREf: Vancomycin-resistant Enterococcus faecium CRE, which saw the proportion of carbapenem-resistant K. pneumoniae bloodstream isolates decline from 22% in Acknowledgements 2007 to 4% one decade later , can explain the differ- We thank all of the healthcare institutions and personnel who contributed to ence in the proportion of carbapenem-resistant K. pneu- the antimicrobial resistance data summarized and analyzed in this report. moniae BSI isolates between Israel and southern Europe. In contrast, both our data and previous Israeli studies Funding indicate a steady increase in the incidence of blood- The work on this article was performed as part of the work of the National Center for Infection Control of the Israel Ministry of Health. stream infections due to extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae and the proportion Availability of data and materials of Enterobacteriaceae blood isolates producing ESBL dur- The datasets generated and/or analysed during the current study are ing the same period [14–16]. The use of targeted control available in the “Periodic Reports” repository, https://www.health.gov.il/ efforts for CRE has been cited as one factor explaining the UnitsOffice/HD/InfectionControl/Pages/Periodic_reports.aspx limited spread of CRE in the United States as compared with ESBL-producing bacteria . Authors’ contributions YD analyzed and interpreted the aggregated data and wrote the article. ET An important difference in the epidemiology of ESBL-- analyzed and interpreted the aggregated data. MIS aggregated and analyzed producing and carbapenem-resistant Gram-negative bac- the raw microbiological data. DS aggregated and interpreted the raw teria is the role of asymptomatic carriers in the community. microbiological data. YC oversaw the collection, aggregation, and interpretation of the data and jointly conceived the idea for the report. MJS oversaw the Carbapenem-resistance is primarily nosocomial, with little collection, aggregation, and interpretation of the data and jointly conceived the to no transmission in community settings reported outside idea for the report. All authors read and approved the final manuscript. of eastern Asia . ESBL-producing Enterobacteriaceae, however, have spread to colonize healthy community Ethics approval and consent to participate dwellers with no or minimal healthcare contact . These Publication was approved by the Israel Ministry of Health. As per MoH policy, the article, which reports national aggregated data, publically available on carriers serve as a major reservoir for infections with the MoH website, was not subject to ethics committee approval. ESBL-producing bacteria in hospitals as well, implying that interventions which concentrate principally on healthcare Consent for publication settings may have limited success in controlling the spread Not applicable. of these organisms [20, 21]. In Israel, where interventions have focused on healthcare facilities, the combined Competing interests incidence of BSI with typically hospital-acquired antibiotic- The authors declare that they have no competing interests. resistant organisms decreased at the same time that inci- dence of ESBL-producing E. coli BSI rose. Ongoing efforts Publisher’sNote are necessary to further inhibit the spread of resistant or- Springer Nature remains neutral with regard to jurisdictional claims in ganisms, including the development of interventions aimed published maps and institutional affiliations. at community settings. Author details Abbreviations National Center for Infection Control, Ministry of Health, Weizmann 6, 3GC: 3rd-generation cephalosporin; BSI: Bloodstream infection; CLSI: Clinical 6423906 Tel Aviv, Israel. Sackler Faculty of Medicine, Tel Aviv University, and Laboratory Standards Institute; CRE: Carbapenem-resistant Enterobacteriaceae; Kalechkin 35, 6997801 Tel Aviv, Israel. Dickstein et al. Antimicrobial Resistance and Infection Control (2019) 8:96 Page 5 of 5 Received: 22 January 2019 Accepted: 8 May 2019 20. Karanika S, Karantanos T, Arvanitis M, Grigoras C, Mylonakis E. Fecal colonization with extended-spectrum beta-lactamase-producing Enterobacteriaceae and risk factors among healthy individuals: a systematic review and metaanalysis. Clin Infect Dis. 2016;63:310–8. References 21. Tschudin-Sutter S, Lucet JC, Mutters NT, Tacconelli E, Zahar JR, Harbarth S. 1. Schwaber MJ, Carmeli Y. The impact of a carbapenem-resistant Contact precautions for preventing nosocomial transmission of extended- Enterobacteriaceae outbreak on facilitating development of a national spectrum beta lactamase-producing Escherichia coli: a point/counterpoint infrastructure for infection control in Israel. Clin Infect Dis. 2017;65:2144–9. review. Clin Infect Dis. 2017;65:342–7. 2. European Committee on Antimicrobial Susceptibility Testing (EUCAST). EUCAST warnings concerning antimicrobial susceptibility testing products or procedures. Available from: http://www.eucast.org/ast_of_bacteria/ warnings/#c13111. Accessed 6 May 2019. 3. The World Bank Group. 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