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A compilation of antimicrobial susceptibility data from a network of 13 Lebanese hospitals reflecting the national situation during 2015–2016

A compilation of antimicrobial susceptibility data from a network of 13 Lebanese hospitals... Background: There is a lack of official national antimicrobial resistance (AMR) data in Lebanon. Individual hospitals generate their own antibiotic susceptibility data in the form of yearly pamphlets. Methods: In this study, antibiotic susceptibility data from 13 hospitals distributed across different governorates of Lebanon were collected to conduct a compilation-based surveillance of AMR in Lebanon for the years 2015–2016. The findings were compared with those of a previous nationwide study in this country conducted between 2011 and 2013 as well as with similar data obtained from the 2015 and 2016 European surveillance reports of AMR. To provide a clear presentation of the AMR situation, mean percent susceptibility of different antibiotic–microbe combinations was calculated. Results: During 2015–2016, the percent susceptibility of Enterobacteriaceae to third-generation cephalosporins and to carbapenems was 59 and 97%, respectively. Among Pseudomonas aeruginosa and Acinetobacter spp., carbapenem susceptibility reached 70 and 12%, respectively. Among Gram positive organisms, the percent susceptibility to methicillin in Staphylococcus aureus was 72%, that to vancomycin in Enterococcus spp. was 98% and that to penicillin in Streptococcus pneumoniae was 75%. Compared with results of 2011–2013, there was an overall trend of decreased susceptibility of bacteria to the tested antibiotics, with a variation of 5 to 10%. The antibiotic susceptibility data from Lebanon were found to be comparable with those from Eastern and South-eastern European countries. Conclusion: This study highlights the need to establish a robust national AMR surveillance system that enables data from Lebanon to be included in global AMR maps. Keywords: Antimicrobial susceptibility, Antimicrobial susceptibility testing, Resistance, Surveillance, Lebanon * Correspondence: roula.samaha@laumcrh.com Rima Moghnieh and Georges F Araj contributed equally to this work Department of Internal Medicine, Division of Infectious Diseases, Lebanese American University-Rizk Hospital, Beirut, Lebanon Faculty of Medicine, Lebanese American University, Beirut, Lebanon Full list of author information is available at the end of the article © 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. Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 2 of 17 Background laboratories of 13 hospitals located in different regions in Antimicrobial resistance (AMR) is a serious global Lebanon between 2015 and 2016. The institutional review public health concern. Recently, the prevalence of board (IRB) Committee of one of the participating hospi- pandrug-resistant organisms has been reported with in- tals, Makassed General Hospital, Beirut, Lebanon, granted creasing frequency [1]. The World Health Organization this study ethical approval. All data were purely based on (WHO) data on AMR have indicated increasing resistance microorganisms, and no patient data were included; hence, in the Middle East and North Africa region [2]. A recent the IRB waived the requirement of informed consent from review on AMR prevalence in different countries of patients. the Arab world has equally demonstrated increasing Lebanon has 152 hospitals, 120 public and 32 private. rates of resistance among multi-drug and extensively We selected only 18 hospitals whose microbiology labora- drug-resistant bacteria [3]. Although the Lebanese na- tories generated yearly antibiogram reports/pamphlets tional AMR data are not well described in literature, (Fig. 1). Two laboratories out of 18 were excluded since Lebanon follows the same global trend of increasing they did not comply with international microbiology AMR as reported by individual hospital studies [4–9]. guidelines [the Clinical & Laboratory Standards Institute In the absence of a standardised national surveillance (CLSI) and the European Committee on Antimicrobial in Lebanon, relatively large Lebanese hospitals gener- Susceptibility Testing (EUCAST)] [13–17]in terms of ate yearly reports on their antibiotic susceptibility identification and antibiotic susceptibility and/or their results of the corresponding year. These reports are work was judged to be inadequate during quality control distributed in the form of pamphlets to healthcare workshops undertaken by the Lebanese Ministry of Health professionals and epidemiologists. Since 2017, work- and WHO in Lebanon. Although the antibiogram pam- shops organised by the Lebanese Ministry of Health in phlets were publicly available to healthcare professionals collaboration with the WHO have been undertaken to and epidemiologists, consent of the chief microbiologists evaluate work and improve the quality and capacity of of the chosen hospital laboratories was requested. Three microbiology laboratories in different regions of the microbiologists out of the remaining 16 did not approve country (unpublished data). the inclusion of their hospitals’ data in this study. Finally, In 2015, a previous compilation of antibiotic susceptibil- antibiotic susceptibility data from 13 hospital laboratories ity data of 16 Lebanese hospitals between the years 2011 were included (Fig. 1). and 2013 was published [10]. The present study is another Bacterial isolates included in this study were recov- follow-up attempt to generate antibiotic susceptibility data ered from different clinical specimens, e.g. urine, spu- from a network of 13 Lebanese hospitals located in differ- tum, deep tracheal aspirates, blood, body fluids and ent regions of the country and to reflect on the current the tips of medical devices. They represent a compil- AMR situation for the years 2015 and 2016. Herein, we ation of laboratory specimens originating from differ- primarily addressed the evolution of antibiotic susceptibil- ent patient populations including paediatric, adult, ity by comparing the current results with those previously critically ill, pregnant patients, outpatients, etc. and published [10]. In addition, we reviewed the methodolo- they may have represented community-acquired or gies of the participating hospital laboratories in reporting hospital-acquired infections. Identification and AST of certain resistance patterns, aiming to include only those bacteria were conducted according to the adopted having the methodologies of identification and susceptibil- methodology and interpretative standards of each ity testing of clinical isolates in line with international laboratory. standards. A secondary aim was to compare this recent Different aspects of AST were addressed with the Lebanese data to similar ones from the European AMR participating hospital laboratories, including asking the Surveillance Network (EARS-Net) [11, 12], which is an chief microbiologist to specify additional tests con- already established AMR surveillance system of geograph- ducted and surrogate markers used for detecting and ical proximity. The results of this study would ultimately confirming susceptibility or resistance of some patho- raise awareness about the type of resistant organisms that gens to specific antimicrobial agents. These included: should be a prioritised by AMR containment programmes susceptibility of Enterobacteriaceae spp. to carbapenem, in Lebanon. In addition, a platform can be laid for moni- production of carbapenemase and extended-spectrum toring future AMR evolution, thereby aiding in future li- beta-lactamase (ESBL) in Enterobacteriaceae spp., suscep- aison with international AMR surveillance programmes. tibility of Salmonella spp. to fluoroquinolone, susceptibil- ity of Streptococcus pneumoniae to penicillin, methicillin Methods resistance in Staphylococcus aureus,vancomycinresist- This is a retrospective study based on institutional anti- ance in Enterococci, susceptibility of Pseudomonas aerugi- microbial susceptibility testing (AST) yearly reports/pam- nosa to colistin and susceptibility of Acinetobacter spp. to phlets generated and distributed by clinical microbiology colistin (Additional file 1). Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 3 of 17 Fig. 1 Flow diagram outlining the selection process for Lebanese hospital laboratories whose antibiotic susceptibility data was included in this study Data on specific organisms from any eligible labora- of P. aeruginosa where susceptibility to ceftazidime was tory that did not conform to the international guidelines studied. Imipenem, unlike other carbapenems, was con- [13–17] regarding the above additional questions was sistently used in all hospitals, and hence, it was considered excluded from subanalysis. as a marker of carbapenem susceptibility in different Herein, we reported mean percent susceptibility of spe- Gram negative species in this study. If the carbapenemase cific bacteria to individual antibiotics from the 13 hospitals or ESBL production screening was positive, further con- according to a specific formula (Additional file 2). Besides firmatory tests were required to establish the presence of presenting data as mean percent susceptibility for each these resistance mechanisms [13, 14, 17]. Accordingly, antibiotic–microbe combination, we added a range of the data from laboratories that conformed to the guidelines upper and lower limits of the corresponding individual concerning this issue were included for calculating the percent susceptibility from the included laboratories. mean percentage of ESBL and carbapenemase production When the number of isolates of an organism tested for in Enterobacteriaceae. This value did not depend on anti- susceptibility to a certain antibiotic was less than 20 per biogram results alone. Regarding S. pneumoniae,we hospital, the corresponding AST result was excluded from excluded data from laboratories that determined sus- calculations and subanalysis [18]. ceptibility to penicillin based only on the oxacillin DD The percent susceptibility of Enterobacteriaceae spp. to method, as this might have been an overestimation of antibiotics was represented by susceptibilities of Escheri- penicillin non-susceptibility (Additional file 1). chia coli and Klebsiella spp. Susceptibility of Gram nega- The 2015–2016 results were compared with those from tive bacteria to ceftriaxone represented susceptibility to an earlier nationwide study, including compiled suscepti- third-generation cephalosporins (3GC), except in the case bility data from 16 Lebanese hospitals between 2011 and Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 4 of 17 2013 [10]. Ten out of the 13 included hospitals in the Valley where data were unavailable and no laboratory current study participated in the previous one. could fulfil our inclusion criteria. They encompassed 10 We also compared the 2015–2016 Lebanese results university and 3 community hospitals. AST techniques with similar results from the 2015 and 2016 EARS-Net used included automation in 5 hospitals, manual methods reports of AMR [11, 12]. For the 2015 and 2016 Euro- in 7 hospitals and both in 1 hospital. The antibiotic sus- pean data, the mean percent susceptibility was calculated ceptibility interpretive standards were based on the CLSI using a specific formula (Additional file 2). guidelines in 9 hospitals, the EUCAST guidelines in 2 hos- pitals and both in 2 hospitals (Table 1). Statistical analysis The microbiological methods used in the included labora- The 2015–2016 and the 2011–2013% antibiotic suscepti- tories were compliant with the CLSI and EUCAST stan- bility results were compared using odd ratios (ORs) and dards. However, we observed deviation from international chi-squared p-values calculated using the OR function of guidelines with regard to susceptibility testing for certain the epitools package in the R statistical program [19]. ORs antibiotic-microbe combinations, such as susceptibilities of were computed with the 2011–2013% antibiotic suscepti- Acinetobacter spp. to colistin, S. pneumoniae to penicillin bility data set as a reference. OR < 1 indicates a decrease and Salmonella spp. to fluoroquinolone. In addition, Entero- in percent antibiotic susceptibility in 2015–2016 vs. 2011– coccus faecium and E. faecalis were grouped together in ma- 2013. OR > 1 indicates an increase in percent antibiotic jority of the hospitals reports and corresponding antibiotic susceptibility in 2015–2016 vs. 2011–2013. The 2015– susceptibility patterns were reported for the Enterococcus 2016 Lebanese data were compared with the 2015–2016 genus without differentiation between the two species. As European data in the same manner using the European re- for Acinetobacter spp. susceptibility to colistin, all laborator- sults as a reference. OR < 1 indicates a decreased percent ies did not use the broth microdilution method, which is susceptibility while OR > 1 indicates an increased percent recommended by CLSI and EUCAST guidelines. In- susceptibility in Lebanon compared to the European stead, 6/13 laboratories used automated minimal in- countries. The Bonferroni method was used for adjusting hibitory concentration (MIC) method, 5/13 laboratories the p-value for multiple testing. A p-value of < 0.05 was used disc diffusion (DD) method, and 2/13 laboratories did considered to be statistically significant. not report results (Additional file 1). So, we did not report colistin susceptibility results in Acinetobacter spp. herein. Results Upon comparing the methods in this study to that of Microbiological techniques and AST methods 2011–2013 study, i.e. in terms of the source of data and The included hospitals represented all geographical the calculation of percent susceptibility, both studies were zones/governorates of the country, except for the Bekaa comparable. Concerning the methods used in detecting Table 1 Demographics and antibiotic susceptibility testing methods in the 13 participating hospitals Hospital Region Type Beds Microbiological Method Guidelines HDF Beirut University 444 Automated EUCAST LAUMC-RH Beirut University 114 Manual CLSI + EUCAST RHUH Beirut University 250 Automated CLSI AUBMC Beirut University 380 Manual CLSI MGH Beirut University 170 Manual CLSI Zahraa Mount Lebanon University 201 Manual + Automated CLSI CHU-NDS Mount Lebanon University 250 Automated CLSI + EUCAST MEIH Mount Lebanon University 150 Manual EUCAST SGH Mount Lebanon University 400 Manual CLSI Nini North Lebanon Community 175 Manual CLSI CHdN North Lebanon University 180 Manual CLSI Haykal North Lebanon Community 120 Automated CLSI Labib MC South Lebanon Community 120 Automated CLSI KEY: HDF Hotel Dieu de France, LAUMC-RH Lebanese American University Medical Center – Rizk Hospital, RHUH Rafic Hariri University Hospital, AUBMC American University of Beirut Medical Center, MGH Makassed General Hospital, CHU-NDS Centre Hospitaler Universitaire Notre Dame de Secours, MEIH Middle East Institute of Health, SGH Saint Georges Hospital, CHdN Centre Hospitalier du Nord, MC Medical Center, EUCAST European Committee on Antimicrobial Susceptibility Testing, CLSI Clinical and Laboratory Standards Institute All of the participating hospitals are private, except for RHUH that is a public hospital Automated microbial identification system: Vitek, BD Phoenix Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 5 of 17 and confirming susceptibility or resistance of some patho- production by 2 out of 13 hospitals. ESBL production was gens to specific antimicrobial agents that we mentioned observed in 34% of Enterobacteriaceae spp. (ranging be- earlier, both studies were comparable as well, except in tween 25 and 43%) from 8 of the 13 laboratories that the detection of ESBL and carbapenemase production in followed the international guidelines for detecting this re- Enterobacteriaceae (personal communication) (Additional sistance mechanism. Similarly, the mean proportion of file 1). However, comparison was made only between 3GC carbapenemase production was 0.6% in case of E. coli and and carbapenem susceptibility results in Enterobacteria- 2% in case of Klebsiella spp. as generated from only 2 of ceae and that related to detection of ESBL or carbapenea- the 13 laboratories (Additional file 3). mase enzymes was not carried on between the 2 study The susceptibility results of P. aeruginosa isolates from periods. all hospitals were as follows: 80% to ceftazidime, 78% to piperacillin/tazobactam, 70% to imipenem, 69% to mero- Types of bacteria and antibiotic susceptibility results penem, 73% to ciprofloxacin, 85% to amikacin and 98% During the study period of 2015–2016, a total of 85,144 to colistin (Table 3). Percent susceptibility of P. aerugi- clinical isolates were included in this compilation anti- nosa to carbapenems among all centres ranged from 55 biogram: 76% were Gram negative and 24% were Gram to 95% (Additional file 4). positive organisms. The distribution of the tested isolates Regarding Acinetobacter spp., mean percent antibiotic per governorate is depicted in Fig. 2. susceptibility was calculated from 11 hospitals where Among the tested Enterobacteriaceae spp., the mean per- 12% of the tested isolates were susceptible to carbapen- cent susceptibility to antibiotics was as follows: 59% to 3GC ems ranging from 3 to 74% (Additional file 4) and 80% (58% in E. coli and 63% in Klebsiella spp.), 77% to cefoxitin were susceptible to tigecycline (Table 3). (76% in E. coli and 83% in Klebsiella spp.), 97% to carba- The antibiotic susceptibility of Salmonella spp. was tested penems (97% in E. coli and 96% in Klebsiella spp.), 60% to in 10 hospitals, where 97% of the isolates were found to be ciprofloxacin (57% in E. coli and 71% in Klebsiella spp.), susceptible to 3GC, 90% to ciprofloxacin and 71% to 91% to amikacin (90% in E. coli and 94% in Klebsiella spp.), trimethoprim-sulfamethoxazole (Table 4). Herein, the range 54% to trimethoprim-sulfamethoxazole (53% in E. coli and of fluoroquinolone susceptibility in Salmonella spp. among 58% in Klebsiella spp.) and 83% to nitrofurantoin (87% in centres was from 56 to 100% (Additional file 5). E. coli and 59% in Klebsiella spp.). (Table 2). Among S. aureus isolates, the susceptibility results The proportion of ESBL and carbapenemase produc- were as follows: 72% to oxacillin/methicillin, 81% to cip- tion among Enterobacteriaceae did not coincide with the rofloxacin, 81% to clindamycin and 73% to erythromycin susceptibility results obtained for 3GC and carbapenems, (Table 5). Although one would expect all isolates to be respectively, because for reporting the presence of these completely susceptible to vancomycin, one laboratory re- enzymes, we selectively included those laboratories that ported a resistance of 4% using the automated system. reported their findings based on confirmatory tests used Susceptibility to oxacillin/methicillin ranged from 52 to to detect the presence of these resistance mechanisms 86% among all centres (Additional file 6). and did not just depend on the antibiogram results. De- Among isolated Enterococci spp., the susceptibility re- tection of ESBL production in Enterobacteriaceae spp. sults were as follows: 75% to ampicillin, 98% to vanco- was reported by 8 out of 13 hospitals and carbapenemase mycin and 99% to both tigecycline and linezolid (Table 5). Fig. 2 Distribution of the total clinical isolates in 2015 and 2016 (%) among the governorates of Lebanon (N = 85,144 isolates) Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 6 of 17 Table 2 Percent antibiotic susceptibility of E. coli, and Klebsiella spp. during 2015/2016 compared to corresponding susceptibility results in 2011/2013 Antibiotic E. coli Klebsiella spp 2011/2013 N (%S) 2015/2016 N (%S) OR (95%CI) P 2011/2013 N (%S) 2015/2016 N (%S) OR (95% CI) P Amikacin 29,667 (97%) 41,818 (90%) 0.29 (0.26–0.3) 0.0001 7768 (96%) 9498 (94%) 0.65 (0.57–0.75) 0.0001 Amoxicillin/ 30,411 (61%) 39,116 (59%) 1.13 (1.10–1.17) 0.0001 7883 (67%) 9069 (62%) 0.80 (0.75–0.86) 0.0001 clavulanic acid Ampicillin 22,985 (23%) 35,906 (24%) 1.06 (1.02–1.10) 0.01–– – – Aztreonam 27,221 (66%) 40,029 (57%) 0.65 (0.63–0.67) 0.0001 7020 (69%) 7924 (65%) 0.83 (0.78–0.90) 0.0001 Cefepime 26,314 (74%) 40,524 (62%) 0.60 (0.58–0.62) 0.0001–– – – Cefoxitin 23,858 (87%) 33,104 (76%) 0.47 (0.45–0.50) 0.0001 5853 (89%) 6373 (83%) 0.60 (0.54–0.67) 0.0001 Ceftazidime 28,730 (71%) 41,816 (62%) 0.73 (0.71–0.76) 0.0001 7335 (71%) 9498 (64%) 0.73 (0.68–0.78) 0.0001 Ceftriaxone 20,059 (64%) 41,816 (58%) 0.85 (0.82–0.88) 0.0001 4750 (65%) 9498 (63%) 0.92 (0.85–0.99) 0.02 Cefuroxime 24,662 (59%) 33,106 (56%) 0.96 (0.93–0.99) 0.02 6516 (64%) 6579 (61%) 0.88 (0.82–0.94) 0.0004 Ciprofloxacin 29,411 (55%) 40,524 (57%) 1.22 (1.19–1.26) 0.0001 7883 (73%) 9311 (71%) 0.91 (0.85–0.97) 0.004 Gentamicin 29,327 (72%) 41,818 (72%) 1.00 (0.98–1.03) 1 7601 (75%) 9498 (78%) 1.18 (1.10–1.27) 0.0001 Imipenem 30,411 (99%) 41,813 (97%) 0.33 (0.29–0.37) 0.0001 7883 (98%) 9498 (96%) 0.49 (0.41–0.60) 0.0001 Nitrofurantoin 18,422 (96%) 29,434 (87%) 0.28 (0.26–0.30) 0.0001 4356 (52%) 5155 (59%) 1.33 (1.22–1.44) 0.0001 Piperacillin/ 28,739 (83%) 40,524 (76%) 0.84 (0.81–0.873) 0.0001 7618 (81%) 9292 (78%) 0.83 (0.77–0.90) 0.0001 tazobactam Tigecycline 9716 (98%) 39,050 (96%) 0.24 (0.20–0.30) 0.0001 2243 (87%) 8546 (93%) 1.99 (1.71–2.31) 0.0001 Trimethoprim/ 29,689 (49%) 41,496 (53%) 1.13 (1.10–1.16) 0.0001 7709 (57%) 9498 (58%) 1.04 (0.98–1.11) 0.2 sulfamethoxazole KEY = CI confidence interval, N Number of isolates tested in each bacteria/antibiotic combination, OR Odds Ratio, S Susceptibility, % percent P < 0.05 is considered statistically significant The 2011/2013 data are taken from: Chamoun K, Farah M, Araj G, et al. Surveillance of antimicrobial resistance in Lebanese hospitals: retrospective nationwide compiled data. Int J Infect Dis. 2016;46:64–70 Ampicillin and vancomycin susceptibility ranged from 46 results, 75% were susceptible to penicillin, with the individ- to 96% and from 83 to 100% among all centres, respect- ual institutional susceptibility ranging between 60 and 79%. ively (Additional file 6). Mean fluoroquinolone susceptibility was 99%using data Regarding S. pneumoniae, three hospitals were compliant from 8 hospitals. The antibiotic susceptibility results for all with the CLSI and EUCAST guidelines and determined Streptococcus spp. are shown in “Additional file 7”.One la- penicillin MIC. Of the tested isolates from three of the boratory reported penicillin resistance in S. agalactiae (3%) eight hospitals that reported S. pneumoniae susceptibility using the automated system. Table 3 Percent antibiotic susceptibility of Acinetobacter spp. and P. aeruginosa during 2015/2016 compared to corresponding susceptibility results in 2011/2013 Antibiotic Acinetobacter spp P. aeruginosa 2011/2013 N (% S) 2015/2016 N (% S) OR (95% CI) P 2011/2013 N (% S) 2015/2016 N (% S) OR (95% CI) P Amikacin 3329 (16%) 3675 (19%) 1.23 (1.11–1.36) 0.0001 7675 (89%) 9005 (85%) 0.70 (0.62–0.79) 0.0001 Aztreonam NA NA NA NA 7483 (76%) 7457 (79%) 1.19 (1.06–1.33) 0.002 Cefepime 3409 (13%) 3675 (13%) 1.00 (0.89–1.12) 1 7897 (83%) 9005 (81%) 0.87 (0.79–0.97) 0.01 Ceftazidime 3343 (12%) 3675 (13%) 1.10 (0.973–1.23) 0.14 7897 (82%) 9005 (80%) 0.88 (0.79–0.97) 0.01 Ciprofloxacin 3379 (12%) 3675 (11%) 0.91 (0.80–1.02) 0.12 7897 (77%) 9005 (73%) 0.81 (0.74–0.89) 0.0001 Gentamicin 3384 (19%) 3675 (14%) 0.70 (0.62–0.78) 0.0001 7722 (83%) 9005 (81%) 0.87 (0.79–0.97) 0.01 Imipenem 3409 (18%) 3675 (12%) 0.62 (0.56–0.70) 0.0001 7897 (73%) 9005 (70%) 0.86 (0.79–0.94) 0.001 Piperacillin/ 3343 (13%) 3675 (11%) 0.83 (0.73–0.93) 0.12 7897 (80%) 9005 (78%) 0.89 (0.80–0.98) 0.02 tazobactam KEY = CI confidence interval, N Number of isolates tested in each bacteria/antibiotic combination, NA not available, OR Odds Ratio, S Susceptibility, % percent P < 0.05 is considered statistically significant The 2011/2013 data are taken from: Chamoun K, Farah M, Araj G, et al. Surveillance of antimicrobial resistance in Lebanese hospitals: retrospective nationwide compiled data. Int J Infect Dis. 2016;46:64–70 Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 7 of 17 Table 4 Percent antibiotic susceptibility of Salmonella spp. Upon comparing the Lebanese and European findings, during 2015/2016 compared to corresponding susceptibility we noticed that the Lebanese percent antibiotic suscepti- results in 2011/2013 bilities in the formerly stated organisms were lower than Antibiotic 2011/2013 2015/2016 OR (95% CI) P those reported from Northern and Western European N (%S) N (%S) countries and were similar or close to those in Eastern Ampicillin 784 (81%) 596 (85%) 1.34 (1.00–1.79) 0.06 and South-eastern Europe. Ceftriaxone 690 (97%) 655 (97%) 0.99 (0.53–1.87) 1 Regarding E. coli, Lebanon reported the lowest percent susceptibility to 3GC (58%) compared to findings from Ciprofloxacin 877 (95%) 721 (90%) 0.48 (0.32–0.70) 0.0001 Italy (70.1%), Greece (81.3%), and Spain (86.7%) (Fig. 4) Trimethoprim/ 877 (92%) 721 (71%) 0.21 (0.16–0.28) 0.0001 sulfamethoxazole (Additional file 8). Carbapenem susceptibility in E. coli was also the lowest in Lebanon (97%) yet close to that KEY = CI confidence interval, N Number of isolates tested in each bacteria/ antibiotic combination, OR Odds Ratio, S Susceptibility, % percent from Romania (98.6%), and lower than values from Italy P < 0.05 is considered statistically significant a (99.8%) and Greece (98.95%) (Fig. 4) (Additional file 9). The 2011/2013 data are taken from: Chamoun K, Farah M, Araj G, et al. Surveillance of antimicrobial resistance in Lebanese hospitals: retrospective As for Klebsiella spp., 3GC and carbapenem percent nationwide compiled data. Int J Infect Dis. 2016;46:64–70 susceptibility in Lebanon were not the lowest. 3GC sus- ceptibility (63%) was similar to that reported from Comparison with the 2011–2013 antibiotic susceptibility Luxembourg (67.9%), Hungary (62.7%), and Cyprus results (62.9%). It was higher than that from Greece (29%) and The 2011–2013 compilation of antibiotic susceptibility Italy (44.2%), yet lower than Spain (78.7%) (Fig. 5) (Add- data has locally been considered as the most representa- itional file 10). Regarding carbapenem susceptibility, our tive report on national AMR surveillance in Lebanon for result (96%) was similar to that from Bulgaria (96.1%), that time period. When the current data were compared higher than that from Greece (35.6%) and lower than with those of 2011–2013, there were few results that that from Spain (97.9%) (Fig. 5) (Additional file 11). were not mentioned in the former study, such as suscep- As for carbapenem percent susceptibility in P. aerugi- tibilities of P. aeruginosa to colistin, Enterococcus spp. to nosa, Lebanon was among countries reporting a low linezolid and S. pneumoniae to penicillin. level (70%) but was not the lowest. Susceptibility data re- In general, we observed that the variation in the per- ported from Poland (68.4%) and Bulgaria (72.1%) were cent susceptibility in majority of the antibiotic–microbe similar to ours. Our carbapenem susceptibility was combinations between both periods was less than 10%, higher than that from Greece (58.8%) and Romania primarily exhibiting a trend of decreasing susceptibility. (41.1%), and lower than that from Italy (76.8%) and A decreasing trend in antibiotic susceptibility (between Spain (78%) (Fig. 6) (Additional file 12). 5 and 10%) was observed in the following cases: E. coli to In Lebanon, carbepenem percent susceptibility in Aci- nitrofurantoin, Klebsiella spp. to cefoxitin, Acinetobacter netobacter spp. is very low (13%), yet our country shared spp. to imipenem, Salmonella spp. to ciprofloxacin and similar results with Romania (16.8%) (Fig. 6) (Add- Enterococci to ampicillin (Tables 2, 3, 4 and 5)(Fig. 3). itional file 13). Values were lower from Croatia (8.3%) A decrease in antibiotic susceptibility (less than 5%) was and Greece (5.6%), higher from Italy (21.6%), and much observed in the following cases: E. coli to imipenem, Kleb- higher from Spain (42%). siella spp. to imipenem, P. aeruginosa to imipenem and S. Concerning Gram positive organisms, Lebanese results aureus to oxacillin/methicillin (Tables 2, 3 and 5)(Fig. 3). on S. aureus susceptibility to methicillin (72%) were However, there was a considerable decrease in anti- comparable with those from Slovakia (72.4%) and Spain biotic susceptibility (10% or more) in the following or- (74.5%), and higher than findings from Italy (66.2%) and ganisms: E. coli to cefepime, E. coli to cefoxitin and Greece (60.9%) (Fig. 7) (Additional file 14). Penicillin Salmonella spp. to trimethoprim-sulfamethoxazole and susceptibility in S. pneumoniae reached 75% in Lebanon. S. aureus isolates to levofloxacin (Tables 2, 4 and 5). This value was similar to those reported from Bulgaria (74.9%), Spain (75.8%), and France (75.9%). It was lower Comparison with 2015–2016 EARS-net data than findings from Italy (90.6%). Data from Greece were For the comparison of the 2015–2016 Lebanese data to not available (Fig. 7) (Additional file 15). European surveillance data during the same period, we fo- cused on the following antibiotic-bacteria susceptibility pat- Discussion terns: E.coli and Klebsiella spp. percent susceptibility to Epidemiologic representativeness of the bacterial Pool 3GC and to carbapenems each separately, P. aeruginosa and This study reports a compilation of antibiotic suscepti- Acinetobacter spp. percent susceptibility to carbapenems bility data retrieved from the antibiogram pamphlets each separately, S. aureus percent susceptibility to methicil- generated by 13 hospital laboratories located in different lin, and S. pneumoniae percent susceptibility to penicillin. Lebanese governorates, whose work was standardised Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 8 of 17 Table 5 Percent antibiotic susceptibility of gram-positive bacteria (S. aureus, S. pneumoniae, Enterococcus spp.) during 2015/2016 compared to corresponding susceptibility results in 2011/2013 Antibiotic S. aureus S. pneumoniae Enterococcus spp. 2011/2013 2015/2016 OR (95% CI) P 2011/2013 2015/2016 OR (95% CI) P 2011/2013 2015/2016 OR (95% CI) P N (%S) N (%S) N (%S) N (%S) N (%S) N (%S) Ampicillin NA NA NA NA NA NA NA NA 3847 (84%) 3760 (75%) 0.57 (0.51–0.64) 0.0001 Clindamycin 4359 (83%) 6452 (81%) 0.87 (0.79–0.96) 0.01 588 (76%) 584 (75%) 0.95 (0.73–1.24) 1 NA NA NA NA Erythromycin 4890 (76%) 6304 (73%) 0.85 (0.78–0.93) 0.0004 544 (63%) 584 (65%) 1.09 (0.86–1.39) 1 NA NA NA NA Levofloxacin 2297 (84%) 2873 (72%) 0.49 (0.43–0.56) 0.0001 483 (91%) 584 (99%) 1.07 (0.72–1.40) 1 NA NA NA NA Oxacillin 4752 (73%) 6452 (72%) 0.95 (0.87–1.03) 0.25 NA NA NA NA NA NA NA NA Tigecycline 492 (99%) 1788 (99%) 1.03 (0.33–2.63) 0.985 NA NA NA NA 723 (99%) 1022 (99%) 0.10 (0.35–1.64) 0.983 Trimethoprim/ 4604 (91%) 6437 (88%) 0.73 (0.64–0.82) 0.0001 296 (53%) 398 (55%) 1.08 (0.80–1.47) 1 NA NA NA NA sulfamethoxazole Vancomycin 4890 (100%) 6452 (100%) 1.32 (0.03–1.47) 0.819 NA NA NA NA 4145 (99%) 3760 (98%) 0.49 (0.33–0.72) 0.0003 KEY = CI confidence interval, N Number of isolates tested in each bacteria/antibiotic combination, NA not available, OR Odds Ratio, S Susceptibility, % percent P < 0.05 is considered statistically significant The 2011/2013 data are taken from: Chamoun K, Farah M, Araj G, et al. Surveillance of antimicrobial resistance in Lebanese hospitals: retrospective nationwide compiled data. Int J Infect Dis. 2016;46:64–70 Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 9 of 17 Fig. 3 Percentage of resistance among six clinically important bacteria in Lebanon during 2011–2013 and 2015–2016, described by the World Health Organization as priority organisms for research and development of new antimicrobials. KEY: CAR carbapenem, FQ fluoroquinolone, MET methicillin, 3GC third-generation cephalosporins, R resistant. N.B. P < 0.05 is considered statistically significant AB Fig. 4 E. coli percent susceptibility to third-generation cephalosporins (a) and to carbapenems (b) in Lebanon in 2015 and 2016 in comparison with similar data from countries of the European Union, based on the 2015 and 2016 annual reports of the European Antimicrobial Resistance Surveillance Network (EARS-Net) Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 10 of 17 AB Fig. 5 K. pneumoniae percent susceptibility to third-generation cephalosporins (a) and to carbapenems (b) in Lebanon in 2015 and 2016 in comparison with similar data from countries of the European Union, based on the 2015 and 2016 annual reports of the European Antimicrobial Resistance Surveillance Network (EARS-Net) and compliant with the CLSI or the EUCAST guidelines susceptibility to different antibiotics was non-available in on bacterial identification and AST [13–17]. Only 13 of the GLASS report [20]. This situation emphasizes the the 150 hospital laboratories were included because the necessity for establishing an official surveillance system remaining hospitals did not fulfil the inclusion criteria. that should be included in the national plan for control- This highlights the need for improving the performance ling the emergence and spread of AMR. of microbiology laboratories through standardisation and external quality control. Since 2017, workshops, Range of antibiotic percent susceptibility among the aiming at capacity building and improving the perform- Lebanese hospitals ance of microbiology laboratories nationwide, have been In this study, we observed a wide range in the reported per- held by the Lebanese Ministry of Health and supported cent susceptibility among the tested organisms to certain an- by the WHO (unpublished data). tibiotics such as in the case of susceptibilities of Klebsiella In countries where official national or international spp. to 3GC (35–72%), Acinetobacter spp. to carbapenems AMR surveillance is not applied, the available antibiotic (3–74%), P. aeruginosa to carbapenems (55 to 95%), and S. susceptibility data are considered to be representative of aureus to oxacillin (52–86%). These organisms are major the countries [3]. In early 2018, the WHO released the causative agents of healthcare-associated infections. Accord- first Global Antimicrobial Resistance Surveillance Sys- ingly, we hypothesized that variability in the reported resist- tem (GLASS) report in its early implementation phase ance patterns in these organisms might be due to different (2016–2017), which included AMR data from two Leba- resistant clones circulating in different hospitals [5, 6, 21, nese hospital laboratories whose 2015–2016 AMR data 22]. A multicentre nationwide cross-sectional study investi- are included in our study [20]. The number of organisms gated the prevalence and molecular basis of carbapenem re- included in this compilation (85,144) outweighs the sistance in Gram-negative bacteria collected from 11 tertiary number of organisms included in the GLASS data from care hospitals, geographically distributed over 5 Lebanese Lebanon (1309), and in the latter, data collection was Governorates in 2012 [6]. Two of these hospitals provided during 2016 only [20]. Data on P. aeruginosa AST data in our study herein, one from Beirut and the other Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 11 of 17 AB Fig. 6 P. aeruginosa (a) and Acinetobacter spp. (b) percent susceptibility to carbapenems in Lebanon in 2015 and 2016 in comparison with similar data from countries of the European Union, based on the 2015 and 2016 annual reports of the European Antimicrobial Resistance Surveillance Network (EARS-Net) from South Lebanon. Investigators reported high-level car- of the range for susceptibility of 3GC was 70% for E. coli bapenem resistance in A. baumannii and P. aeruginosa, and 72% for Klebsiella spp. meaning that all reporting hospi- 88% (638/724 isolates) and 41% (760/1848 isolates), re- tals detected resistance to 3GC at different degrees (at least spectively [6]. Ninety percent of the carbapenem-resistant 30% in E. coli and 28% in Klebsiella spp). This finding could A. baumanni produced OXA-23 carbapenemase and 16% be explained by that 3GC resistance in Enterobacteriaceae of the carbapenem-resistant P. aeruginosa isolates har- has possibly spread in the community and reached the hos- boured VIM-2 metallo-b-lactamase. In addition, the diffu- pital setting from the community. As mentioned previously, sion of these enzymes was primarily due to clonal the tested organisms in this study originated from pooled dissemination [6]. Another recent multicentre study by hospital laboratory data, where there was no differentiation Atrouni et al. investigated the molecular epidemiology of between hospital-acquired or community-acquired infec- A. baumannii strains isolated from various types of clinical tions. A single centre study from a university hospital in specimens from 7 hospitals situated in different regions in Beirut evaluating the epidemiology of bacteremia in cancer Lebanon between 2013 and 2015 [5]. Investigators showed patients showed that the percentage of hospital-acquired that out of 119 non-duplicate isolates, 76.5% were resist- 3GC resistance in Enterobacteriaceae causing bacteremia ant to carbapenems and the most common carbapene- was 51% and that broad-spectrumantibioticexposuredur- mase was the OXA-23-type, found in 82 isolates [5]. In ing hospital stay was a risk factor for the acquisition of this study, 2 out of 7 centres were included in our 3GC-resistant organisms [23]. In another Lebanese study current study, one from Beirut and the other from on community-acquired urinary tract infections caused North Lebanon. The study by Atrouni et al. highlighted by E. coli and Klebsiella spp. collected from 3 hospitals, the nationwide dissemination of highly related Moghnieh et al. found that the percentage of 3GC re- OXA-23-producing carbapenem-resistant A. bauman- sistance was 31% in E. coli and 29% in Klebsiella spp. nii in Lebanese hospitals [5]. during 2010 and 2011 [24]. Regarding Enterobacteriaceae, 3GC susceptibility was not Similarly, the range of susceptibility of Enterobacteria- 100% in any of the included hospitals, where the upper limit ceae to fluoroquinolones was 44–74% in E. coli and 56– Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 12 of 17 AB Fig. 7 S. aureus percent susceptibility to methicillin (a) and S. pneumonaie percent susceptibility to penicillin (b) in Lebanon in comparison with countries of the European Union during 2015 and 2016, based on the 2015 and 2016 annual reports of the European Antimicrobial Resistance Surveillance Network (EARS-Net) 80% in Klebsiella spp. So E. coli and Klebsiella spp. resistance in Eneterobacteriaceae was 1.2% [6]. The spread fluoroquinolone resistance was detected at different of carbapenem-resistant Enterobacteriaceae (CRE) in levels in the participating hospitals (at least 26% from E. Lebanese hospitals is still lower than resistance to 3GC or coli and 20% from Klebsiella spp.). In the study on fluroquinolones and carbapenem resistance in Enterobac- community-acquired urinary tract infections, Moghnieh teriaceae is predominantly due to OXA-48-like carbapene- et al. reported a similarly elevated level of fluoroquinolone mases production [6, 23, 24]. As for risk factors for CRE resistance in E. coli and Klebsiella spp. (42 and 33%, re- infection, Kanafani et al. found that the respiratory tract spectively) [24]. This high percentage of fluoroquinolone and blood as primary infection sites and prior antibiotic resistance can be attributed to the misuse of this class of use in the hospital setting were independent risk factors antibiotics since it is available over-the-counter in Leba- for its nosocomial acquisition [27]. There is a plausible nese community pharmacies [25, 26]. risk for the transmission of resistant pathogens from the Regarding susceptibility of Enterobacteriaceae to carba- hospital environment into the community in the absence penems, the upper limit of the range was 100% in E. coli of rigorous infection control practices, efficient sanitation and Klebsiella spp.. So, there were hospitals that still re- and sewage disposal and in a setting where antimicrobials ported 100% susceptibility, 2 of them for both E. coli and are used in veterinary medicine without control. Daoud et Klebsiella spp. and 1 for Klebsiella spp. and not E. coli. al. confirmed this possibility when they detected a New The rest of the hospitals, 11 in case of E. coli and 10 in Delhi metallo-beta-lactamase-1-producing Enterobacteria- Klebsiella spp., reported different levels of carbapenem re- ceae strain in sewage water [28]. sistance ranging from 1 to 5% in E. coli and 1 to 10% in Klebsiella spp. Two hospitals additionally reported carba- Changing trends in antibiotic susceptibility compared penemase production among their isolates. Hammoudi et with the 2011–2013 report al., in their multicentre cross-sectional study mentioned The “WHO AMR study group” listed 13 organism/anti- earlier, showed that the mean prevalence of carbapenem biotic combinations, other than drug-resistant Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 13 of 17 Mycobacterium tuberculosis, to be of high priority for dis- present AMR rates on the global map, Lebanon, among covery, research and development of new antibiotics [1]. In many other countries of the Eastern Mediterranean re- our study, 6 of these priority organisms have been described: gion, is not included due to the lack of national surveil- 3GC-resistant Enterobacteriaceae, carbapenem-resistant En- lance data. A recently published narrative review of terobacteriaceae, carbapenem-resistant P. aeruginosa, carba- literature showed the significantly increasing prevalence penem-resistant Acinetobacter spp., fluoroquinolone- of antibacterial resistance in different countries of the resistant Salmonella spp., and methicillin resistant S. aur- Arab World including Lebanon [3]. In the absence of eus. Other organisms stated in the “WHO AMR study official standardized AMR surveillance networks in group” priority list were not included for the following rea- neighbouring Arab countries, we chose to compare our sons: lack of data as in the case of M. tuberculosis,avery data with those from EARS-Net aiming to position small number of isolates of certain species reported by Lebanon on the global map of AMR, and taking into Lebanese laboratories such Campylobacter spp. and Shi- account the geographical proximity between Lebanon gella spp., and non-standardised methodologies used in the and several Southern and South-eastern European Lebanese laboratories like in reporting penicillin sus- countries. The EARS-Net annual AMR surveillance re- ceptibility in S. pneumoniae and vancomycin suscepti- ports provide an accurate picture of the extent of AMR bility pooling in Enterococci without differentiating in the European Union (EU) [11, 12]. We believe that between E. faecalis and E. faecium. When the 2015– comparing AMR in Lebanon to that from relatively 2016 antibiotic susceptibility results of these 6 priority nearby countries in Europe would help the reader to organisms were compared to those of 2011–2013, a sta- visualize and benchmark the AMR situation in tistically significant decrease in susceptibility was dem- Lebanon. This comparison would, most importantly, help onstrated (Fig. 3). Lebanese professionals and officials visualize the actual size The emergence of antibiotic resistance has been strongly of theproblemscausedbyAMR andwould hencestimu- correlated to the inappropriate prescribing of antibiotics late them for serious interventions. Moreover, it could trig- [29]. In Lebanon, there are no national surveillance studies ger international organisations like the WHO, the Food describing antibiotic consumption on hospital setting, ra- and Agriculture Organization of the United Nations, the ther than very few hospital data showing that carbapenems World Organization for Animal Health, and others, to in- are among the most commonly prescribed antibiotics [30, clude Lebanon in global actions plans under the “One 31]. On the other hand, the extensive use of Health” approach that aim at limiting the spread and emer- over-the-counter antibiotics is of paramount importance in gence of AMR. aggravating the antimicrobial resistance. In Lebanon, the Upon reviewing European and Lebanese data using prevalence of dispensing broad-spectrum antibiotics with- percent susceptibility instead of resistance (Additional out prescription ranged from 32 to 42% among community files 8, 9, 10, 11, 12, 13, 14 and 15), our data was compar- pharmacies [25, 26, 32]. This situation calls for immediate able to those from countries in Southern and South-eastern action against these practices through improving public Europe including Bulgaria, Romania, Greece, Italy and and healthcare professional awareness on AMR, establish- Spain that reported in general low antibiotic susceptibility ing and implementing rigorous legislation that forbids the patterns, in comparison with the countries of North and dispensing of antibiotics over the counter, and establishing West Europe [11, 12]. In Lebanon, antimicrobials are dis- antimicrobial stewardship programmes in hospitals and pensed over-the-counter in pharmacies and antimicrobial the community. Antibiotics are not just used in humans, stewardship practices exist only in very few university hos- yet they are heavily administered for therapeutic and pitals [25, 26, 31, 32]. As for infection prevention and con- prophylaxis purposes in veterinary medicine, livestock trol (IPC) programmes, their presence is mandatory in production, crop culture and food production industry different healthcare facilities. However, the monitoring of [33]. In Lebanon, there are no national data describ- its function is variable across these facilities. At the national ing antibiotic use in the listed fields outside human level, the assessment of the appropriateness of IPC prac- health yet AMR has already emerged and is spreading tices is limited to the accreditation audit of done by the [34]. This necessitates adopting multifaceted, compre- Lebanese Ministry of Health every 3 years. Recently a Na- hensive, and integrated measures complying with the tional Action Plan in line with the WHO Global Action “One Health” approach to curb the emergence and Plan for fighting AMR is being prepared in Lebanon in col- spread of AMR, and preserve the efficacy of the laboration with the ministries of health, agriculture and en- remaining few active antibiotics [33]. vironment. This plan is directly supported by the WHO and its outcome may be reflected in future AMR surveil- Comparative epidemiology with European data on AMR lance studies. Joint efforts from representatives of the gov- Lebanon is a relatively small Arab country in the East- ernment and healthcare authorities are needed to ensure ern Mediterranean region. In international reports that the effectiveness of this plan for the upcoming years. Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 14 of 17 Regarding IPC practices in hospitals in North and already present global systems for providing accurate West Europe, surveillance of hospital-acquired infec- and reliable data. Moreover, there is a need for a tions and IPC practices is present through the establish- multifaceted programme for AMR containment based ment of national key performance indicators, which on the “One Health” approach. This programme should reflects a serious collaborative work in infection control include the implementation of rigorous infection preven- [35–38]. In addition, antibiotic consumption in hospitals tion and control programmes in hospitals, antimicrobial and the community, in these countries, is much lower stewardship programmes in both hospitals and the com- than others from South and East Europe, as reported to munity and the control of antibiotic use in livestock and the European Surveillance of Antimicrobial Consumption agriculture. Furthermore, raising awareness about the ex- Network (ESAC-Net) [39]. In 2015, Greece and Romania tent, implications and modalities of preventing AMR in were the countries with the highest consumption of anti- Lebanon should be performed for healthcare providers bacterials for systemic use in Europe [39]. In addition, des- and the public. Finally, research for developing alternative pite that components of IPC infrastructure are in place in therapies for infectious diseases, such as phage therapy hospital setting in several Southern and South-eastern and microbiota-based therapy, should be encouraged to countries, gaps leading to suboptimal IPC are present limit the abuse and subsequently the loss of effectiveness such as: insufficient time allocated to IPC activities by of available antimicrobials. healthcare givers and personnel due to understaffing, considerable variation in safety culture for effective IPC Key findings among different facilities, inadequate collaboration be-  Microbiological methods used for AMR detection in tween healthcare professionals at different levels, and Lebanese hospitals majorly conformed to the CLSI and absence of documented process audits that assess com- EUCAST guidelines on antibiotic susceptibility testing. pliance with IPC practices [40–44]. However, European  Non-uniformity in AMR reporting was observed in countries like Spain, Italy, Bulgaria and Romania, some cases, such as susceptibilities of Acinetobacter among others, are in the process of implementing their spp. to colistin, S. pneumoniae to penicillin and own national action plans for the control of AMR, in Salmonella spp. to fluoroquinolone. close collaboration with the European Centre for Dis-  A wide range of susceptibility results was reported ease Prevention and Control (ECDC) [40–44]. for each antibiotic–microbe combination among the 13 laboratories. Limitations and strengths  Fluoroquinolone resistance in Enterobacteriaceae, Despite the national effort to improve reporting of including Salmonella spp., has been established in antibiotic susceptibility in Lebanon, there is still a the Lebanese community. need for implementing uniform standardised micro-  Lebanese hospitals have become endemic for 3GC biological methods and adequate quality control sys- resistant-Enterobacteriaceae, and this resistance pattern tems in all Lebanese laboratories. The lack of both is apparently finding its way to the community. elements in majority of Lebanese hospitals has led to  Some hospitals laboratories reported the emergence limiting the number of included centres to only 13 of the of carbapenem-resistant Enterobacteriaceae and P. 152 governmental and private hospitals in Lebanon. An- aeruginosa, along with established and increasing other limitation is the lack of organism stratification as carbapenem resistance in Acinetobacter spp. per type of clinical specimen or per its site of acquisition,  Among Gram positive bacteria, S. aureus mean i.e. nosocomial or community. However, this report may percent susceptibility to methicillin was 72%, and serve as an example for countries that do not have stan- that of Enterococci to ampicillin was 75%. dardised national surveillance for AMR. This study and  Susceptibility of S. pneumoniae to penicillin reached the one published earlier allow Lebanon to be included in a mean of 75% from all tested isolates in 3 of the 13 the global AMR maps. Furthermore, generating local anti- hospitals in addition to the emergence of biograms is critical for establishing national clinical guide- levofloxacin-resistant strains in some centres. lines for the management of infectious diseases.  Despite the relatively short time between the 2011– 2013 and 2015–2016 compilation, a trend towards Conclusion decreasing antibiotic susceptibility of less than 10% The current compiled antibiotic susceptibility data have was observed among several clinically important shed light on increasing bacterial resistance trends in bacteria. Lebanon, which were found to be comparable with data  The 2015–2016 Lebanese data were found to be from some Eastern and Southern European countries. comparable with those from Eastern and South- However, there is a need for a robust national AMR surveil- eastern European countries, such as Greece, Spain, lance system in Lebanon, which could be included in the Italy and Bulgaria. These countries are in the process Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 15 of 17 of developing their own national action plans to Additional file 15: Table S1. S. pneumonaie percent susceptibility to fight AMR supported by the ECDC. penicillin countries of the European Union during 2015 and 2016, based on the 2015 and 2016 annual reports of the European Antimicrobial In Lebanon, a national action plan for combating 1,2 Resistance Surveillance Network (EARS-Net) , and comparison to AMR s being prepared in collaboration with 2015–2016 Lebanese data. (DOCX 110 kb) representatives of government, healthcare authorities and is supported directly by the WHO. Abbreviations 3GC: Third-generation cephalosporins; AMR: Antimicrobial resistance; AST: Antimicrobial susceptibility testing; BMD: Broth microdilution; CLSI: Clinical & Laboratory Standards Institute; CRE: Carbapenem-resistant Additional files Enterobacteriaceae; DD: Disc diffusion; EARS-Net: European Antimicrobial Resistance Surveillance Network; ECDC: European Centre for Disease Additional file 1: Table S1. The microbiological methods used in Prevention and Control; ESAC-Net: European Surveillance of Antimicrobial detecting certain resistance patterns in the included Lebanese hospitals Consumption Network; ESBL: Extended-spectrum beta-lactamase; and the corresponding Clinical and Laboratory Standards Institute (CLSI)/ EU: European Union; EUCAST: European Committee on Antimicrobial European Committee on Antimicrobial Susceptibility Testing (EUCAST) Susceptibility Testing; GLASS: Global Antimicrobial Resistance Surveillance guidelines recommendations. (DOCX 131 kb) System; IPC: Infection prevention and control; IRB: Institutional review board; MIC: Minimal inhibitory concentration; OR: Odd ratio; WHO: World Health Additional file 2: Formulas for mean percent (%) susceptibility Organization calculation. (DOCX 121 kb) Additional file 3: Table S1. E. coli and Klebsiella spp percent susceptibility* Acknowledgements to antibiotics in 13 Lebanese hospitals during 2015/2016. (DOCX 121 kb) We would like to acknowledge Dr. Georges Khazen for undergoing the Additional file 4: Table S1. Pseudomonas aeruginosa and Acinetobacter statistical analysis. We would also like to acknowledge Miss Nadia Lara Samaha spp. percent susceptibility* to antibiotics in 13 Lebanese hospitals and Miss Karen Abdallah for providing technical assistance in data entry. during 2015/2016. (DOCX 129 kb) Funding Additional file 5: Table S1. Salmonella spp. percent susceptibility* to None. antibiotics in 10 Lebanese hospitals during 2015/2016. (DOCX 70 kb) Additional file 6: Table S1. Staphylococcus aureus, coagulase negative a Availability of data and materials Staphylococci , and Enterococcus spp. percent susceptibility* to antibiotics All data generated or analysed during this study are included in this in 13 Lebanese hospitals during 2015/2016. (DOCX 115 kb) published article and its supplementary information files. Additional file 7: Table S1. Streptococcus pneumoniae, Streptococcus viridans, Streptococcus pyogenes, and Streptococcus agalactiae percent Authors’ contributions susceptibility* to antibiotics in 13 Lebanese hospitals during 2015/2016 . RM, GA, and RH were responsible for study conception, result analysis and (DOCX 103 kb) drafting of the manuscript. LA was responsible for data collection and analysis. ZD, JM, and TJ were responsible for microbiological methods Additional file 8: Table S1. E. coli percent susceptibility to third- evaluation and data analysis. DA performed data analysis and edited the final generation cephalosporins in countries of the European Union, based on version of the manuscript. NA, NH, MB, MY, GK, MH, MM, RA, EA, RF, and NY the 2015 and 2016 annual reports of the European Antimicrobial Resistance 1,2 provided the raw antibiotic susceptibility data from hospitals and Surveillance Network (EARS-Net) , and comparison to 2015–2016 Lebanese participated in study group discussions. All authors read and approved the data. (DOCX 110 kb) final version of the manuscript. Additional file 9: Table S1. E. coli percent susceptibility to carbapenems in countries of the European Union, based on the 2015 and 2016 annual Ethics approval and consent to participate reports of the European Antimicrobial Resistance Surveillance Network 1,2 This study is based on institutional antimicrobial susceptibility testing (AST) (EARS-Net) , and comparison to 2015–2016 Lebanese data. (DOCX 113 kb) yearly reports/pamphlets generated and distributed by clinical microbiology Additional file 10: Table S1. K. pneumoniae percent susceptibility to third- laboratories. This information is publically available. The institutional review generation in countries of the European Union, based on the 2015 and 2016 board (IRB) Committee of one of the participating hospitals, Makassed General annual reports of the European Antimicrobial Resistance Surveillance Network Hospital, Beirut, Lebanon, granted this study ethical approval. All data were 1,2 (EARS-Net) , and comparison to 2015–2016 Lebanese data. (DOCX 110 kb) purely based on microorganisms, and no patient data were included; hence, the IRB waived the requirement of informed consent from patients. Additional file 11: Table S1. K. pneumoniae percent susceptibility to carbapenems in countries of the European Union, based on the 2015 Consent for publication and 2016 annual reports of the European Antimicrobial Resistance 1,2 Not applicable. Surveillance Network (EARS-Net) , and comparison to 2015–2016 Lebanese data. (DOCX 106 kb) Competing interests Additional file 12: Table S1. P. aeruginosa percent susceptibility to The authors declare that they have no competing interests. carbapenems in countries of the European Union, based on the 2015 and 2016 annual reports of the European Antimicrobial Resistance 1,2 Surveillance Network (EARS-Net) , and comparison to 2015–2016 Publisher’sNote Lebanese data. (DOCX 114 kb) Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Additional file 13: Table S1. Acinetobacter spp. percent susceptibility to carbapenems in countries of the European Union, based on the 2015 Author details and 2016 annual reports of the European Antimicrobial Resistance 1,2 1 Department of Internal Medicine, Division of Infectious Diseases, Makassed Surveillance Network (EARS-Net) , and comparison to 2015–2016 General Hospital, Beirut, Lebanon. Faculty of Medicine, Lebanese University, Lebanese data. (DOCX 112 kb) Beirut, Lebanon. Professor and Director of Clinical Microbiology, Department Additional file 14: Table S1. S. aureus percent susceptibility to of Pathology and Laboratory Medicine, American University of Beirut Medical methicillin in countries of the European Union during 2015 and 2016, Center, Beirut, Lebanon. Pharmacy Department, Makassed General Hospital, based on the 2015 and 2016 annual reports of the European 1,2 Beirut, Lebanon. Department of Microbiology, Centre Hospitalier du Nord, Antimicrobial Resistance Surveillance Network (EARS-Net) , and Zgharta, Lebanon. Faculty of Medicine and Medical Sciences, University of comparison to 2015–2016 Lebanese data. (DOCX 111 kb) Balamand, Koura, Lebanon. Department of Internal Medicine, Division of Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 16 of 17 Infectious Diseases, Lebanese American University-Rizk Hospital, Beirut, 15. The European Committee on Antimicrobial Susceptibility Testing. Lebanon. Faculty of Medicine, Lebanese American University, Beirut, Breakpoint tables for interpretation of MICs and zone diameters. Version 5.0, Lebanon. Department of Laboratory Medicine, Makassed General Hospital, 2015. Beirut, Lebanon. Department of Microbiology, Hotel Dieu de France 16. The European Committee on Antimicrobial Susceptibility Testing. Hospital, Beirut, Lebanon. Department of Laboratory Medicine, Saint Breakpoint tables for interpretation of MICs and zone diameters. Version 6.0, George University Hospital, Beirut, Lebanon. Department of Internal 2016. Medicine, Division of Infectious Diseases, Labib Medical Center, Saida, 17. Giske CG, Martinez L, Cantón R, et al. EUCAST guidelines for detection of Lebanon. Medical Subspecialties Institute, Infectious Diseases, Cleveland resistance mechanisms and specific resistances of clinical and/or Clinic Abu Dhabi, Abu Dhabi, United Arab Emirates. Department of Internal epidemiological importance. Version 1.0 (2013-12-11); 2013.http://www. Medicine, Division of Infectious Diseases, Haykel Hospital, Tripoli, Lebanon. eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Resistance_mechanisms/ Department of Microbiology and Molecular diagnostics, Haykel Hospital, EUCAST_detection_of_resistance_mechanisms_v1.0_20131211.pdf. Tripoli, Lebanon. Department of Microbiology, Nini Hospital, Tripoli, 18. Cornaglia G, Hryniewicz W, Jarlier V, et al. European recommendations Lebanon. Department of Internal Medicine, Division of Infectious Diseases, for antimicrobial resistance surveillance. Clin Microbiol Infect. 2004; Notre Dame de Secours University Hospital, Jbeil, Lebanon. Faculty of 10(4):349–83. Medical Sciences, Holy Spirit University of Kaslik, Jounieh, Lebanon. 19. R Core Team (2018). R: a language and environment for statistical Department of Internal Medicine, Zahraa Hospital, Beirut, Lebanon. computing. 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[online] Available at: http://www.euro.who.int/en/countries/bulgaria/news2/ news/2016/10/bulgaria-hosts-roudtable-on-the-draft-national-programme- for-prevention-of-antimicrobial-resistance-and-prudent-use-of-antimicrobial- agents. Accessed 11 Nov 2018. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Antimicrobial Resistance & Infection Control Springer Journals

A compilation of antimicrobial susceptibility data from a network of 13 Lebanese hospitals reflecting the national situation during 2015–2016

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Biomedicine; Medical Microbiology; Drug Resistance; Infectious Diseases
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Abstract

Background: There is a lack of official national antimicrobial resistance (AMR) data in Lebanon. Individual hospitals generate their own antibiotic susceptibility data in the form of yearly pamphlets. Methods: In this study, antibiotic susceptibility data from 13 hospitals distributed across different governorates of Lebanon were collected to conduct a compilation-based surveillance of AMR in Lebanon for the years 2015–2016. The findings were compared with those of a previous nationwide study in this country conducted between 2011 and 2013 as well as with similar data obtained from the 2015 and 2016 European surveillance reports of AMR. To provide a clear presentation of the AMR situation, mean percent susceptibility of different antibiotic–microbe combinations was calculated. Results: During 2015–2016, the percent susceptibility of Enterobacteriaceae to third-generation cephalosporins and to carbapenems was 59 and 97%, respectively. Among Pseudomonas aeruginosa and Acinetobacter spp., carbapenem susceptibility reached 70 and 12%, respectively. Among Gram positive organisms, the percent susceptibility to methicillin in Staphylococcus aureus was 72%, that to vancomycin in Enterococcus spp. was 98% and that to penicillin in Streptococcus pneumoniae was 75%. Compared with results of 2011–2013, there was an overall trend of decreased susceptibility of bacteria to the tested antibiotics, with a variation of 5 to 10%. The antibiotic susceptibility data from Lebanon were found to be comparable with those from Eastern and South-eastern European countries. Conclusion: This study highlights the need to establish a robust national AMR surveillance system that enables data from Lebanon to be included in global AMR maps. Keywords: Antimicrobial susceptibility, Antimicrobial susceptibility testing, Resistance, Surveillance, Lebanon * Correspondence: roula.samaha@laumcrh.com Rima Moghnieh and Georges F Araj contributed equally to this work Department of Internal Medicine, Division of Infectious Diseases, Lebanese American University-Rizk Hospital, Beirut, Lebanon Faculty of Medicine, Lebanese American University, Beirut, Lebanon Full list of author information is available at the end of the article © 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. Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 2 of 17 Background laboratories of 13 hospitals located in different regions in Antimicrobial resistance (AMR) is a serious global Lebanon between 2015 and 2016. The institutional review public health concern. Recently, the prevalence of board (IRB) Committee of one of the participating hospi- pandrug-resistant organisms has been reported with in- tals, Makassed General Hospital, Beirut, Lebanon, granted creasing frequency [1]. The World Health Organization this study ethical approval. All data were purely based on (WHO) data on AMR have indicated increasing resistance microorganisms, and no patient data were included; hence, in the Middle East and North Africa region [2]. A recent the IRB waived the requirement of informed consent from review on AMR prevalence in different countries of patients. the Arab world has equally demonstrated increasing Lebanon has 152 hospitals, 120 public and 32 private. rates of resistance among multi-drug and extensively We selected only 18 hospitals whose microbiology labora- drug-resistant bacteria [3]. Although the Lebanese na- tories generated yearly antibiogram reports/pamphlets tional AMR data are not well described in literature, (Fig. 1). Two laboratories out of 18 were excluded since Lebanon follows the same global trend of increasing they did not comply with international microbiology AMR as reported by individual hospital studies [4–9]. guidelines [the Clinical & Laboratory Standards Institute In the absence of a standardised national surveillance (CLSI) and the European Committee on Antimicrobial in Lebanon, relatively large Lebanese hospitals gener- Susceptibility Testing (EUCAST)] [13–17]in terms of ate yearly reports on their antibiotic susceptibility identification and antibiotic susceptibility and/or their results of the corresponding year. These reports are work was judged to be inadequate during quality control distributed in the form of pamphlets to healthcare workshops undertaken by the Lebanese Ministry of Health professionals and epidemiologists. Since 2017, work- and WHO in Lebanon. Although the antibiogram pam- shops organised by the Lebanese Ministry of Health in phlets were publicly available to healthcare professionals collaboration with the WHO have been undertaken to and epidemiologists, consent of the chief microbiologists evaluate work and improve the quality and capacity of of the chosen hospital laboratories was requested. Three microbiology laboratories in different regions of the microbiologists out of the remaining 16 did not approve country (unpublished data). the inclusion of their hospitals’ data in this study. Finally, In 2015, a previous compilation of antibiotic susceptibil- antibiotic susceptibility data from 13 hospital laboratories ity data of 16 Lebanese hospitals between the years 2011 were included (Fig. 1). and 2013 was published [10]. The present study is another Bacterial isolates included in this study were recov- follow-up attempt to generate antibiotic susceptibility data ered from different clinical specimens, e.g. urine, spu- from a network of 13 Lebanese hospitals located in differ- tum, deep tracheal aspirates, blood, body fluids and ent regions of the country and to reflect on the current the tips of medical devices. They represent a compil- AMR situation for the years 2015 and 2016. Herein, we ation of laboratory specimens originating from differ- primarily addressed the evolution of antibiotic susceptibil- ent patient populations including paediatric, adult, ity by comparing the current results with those previously critically ill, pregnant patients, outpatients, etc. and published [10]. In addition, we reviewed the methodolo- they may have represented community-acquired or gies of the participating hospital laboratories in reporting hospital-acquired infections. Identification and AST of certain resistance patterns, aiming to include only those bacteria were conducted according to the adopted having the methodologies of identification and susceptibil- methodology and interpretative standards of each ity testing of clinical isolates in line with international laboratory. standards. A secondary aim was to compare this recent Different aspects of AST were addressed with the Lebanese data to similar ones from the European AMR participating hospital laboratories, including asking the Surveillance Network (EARS-Net) [11, 12], which is an chief microbiologist to specify additional tests con- already established AMR surveillance system of geograph- ducted and surrogate markers used for detecting and ical proximity. The results of this study would ultimately confirming susceptibility or resistance of some patho- raise awareness about the type of resistant organisms that gens to specific antimicrobial agents. These included: should be a prioritised by AMR containment programmes susceptibility of Enterobacteriaceae spp. to carbapenem, in Lebanon. In addition, a platform can be laid for moni- production of carbapenemase and extended-spectrum toring future AMR evolution, thereby aiding in future li- beta-lactamase (ESBL) in Enterobacteriaceae spp., suscep- aison with international AMR surveillance programmes. tibility of Salmonella spp. to fluoroquinolone, susceptibil- ity of Streptococcus pneumoniae to penicillin, methicillin Methods resistance in Staphylococcus aureus,vancomycinresist- This is a retrospective study based on institutional anti- ance in Enterococci, susceptibility of Pseudomonas aerugi- microbial susceptibility testing (AST) yearly reports/pam- nosa to colistin and susceptibility of Acinetobacter spp. to phlets generated and distributed by clinical microbiology colistin (Additional file 1). Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 3 of 17 Fig. 1 Flow diagram outlining the selection process for Lebanese hospital laboratories whose antibiotic susceptibility data was included in this study Data on specific organisms from any eligible labora- of P. aeruginosa where susceptibility to ceftazidime was tory that did not conform to the international guidelines studied. Imipenem, unlike other carbapenems, was con- [13–17] regarding the above additional questions was sistently used in all hospitals, and hence, it was considered excluded from subanalysis. as a marker of carbapenem susceptibility in different Herein, we reported mean percent susceptibility of spe- Gram negative species in this study. If the carbapenemase cific bacteria to individual antibiotics from the 13 hospitals or ESBL production screening was positive, further con- according to a specific formula (Additional file 2). Besides firmatory tests were required to establish the presence of presenting data as mean percent susceptibility for each these resistance mechanisms [13, 14, 17]. Accordingly, antibiotic–microbe combination, we added a range of the data from laboratories that conformed to the guidelines upper and lower limits of the corresponding individual concerning this issue were included for calculating the percent susceptibility from the included laboratories. mean percentage of ESBL and carbapenemase production When the number of isolates of an organism tested for in Enterobacteriaceae. This value did not depend on anti- susceptibility to a certain antibiotic was less than 20 per biogram results alone. Regarding S. pneumoniae,we hospital, the corresponding AST result was excluded from excluded data from laboratories that determined sus- calculations and subanalysis [18]. ceptibility to penicillin based only on the oxacillin DD The percent susceptibility of Enterobacteriaceae spp. to method, as this might have been an overestimation of antibiotics was represented by susceptibilities of Escheri- penicillin non-susceptibility (Additional file 1). chia coli and Klebsiella spp. Susceptibility of Gram nega- The 2015–2016 results were compared with those from tive bacteria to ceftriaxone represented susceptibility to an earlier nationwide study, including compiled suscepti- third-generation cephalosporins (3GC), except in the case bility data from 16 Lebanese hospitals between 2011 and Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 4 of 17 2013 [10]. Ten out of the 13 included hospitals in the Valley where data were unavailable and no laboratory current study participated in the previous one. could fulfil our inclusion criteria. They encompassed 10 We also compared the 2015–2016 Lebanese results university and 3 community hospitals. AST techniques with similar results from the 2015 and 2016 EARS-Net used included automation in 5 hospitals, manual methods reports of AMR [11, 12]. For the 2015 and 2016 Euro- in 7 hospitals and both in 1 hospital. The antibiotic sus- pean data, the mean percent susceptibility was calculated ceptibility interpretive standards were based on the CLSI using a specific formula (Additional file 2). guidelines in 9 hospitals, the EUCAST guidelines in 2 hos- pitals and both in 2 hospitals (Table 1). Statistical analysis The microbiological methods used in the included labora- The 2015–2016 and the 2011–2013% antibiotic suscepti- tories were compliant with the CLSI and EUCAST stan- bility results were compared using odd ratios (ORs) and dards. However, we observed deviation from international chi-squared p-values calculated using the OR function of guidelines with regard to susceptibility testing for certain the epitools package in the R statistical program [19]. ORs antibiotic-microbe combinations, such as susceptibilities of were computed with the 2011–2013% antibiotic suscepti- Acinetobacter spp. to colistin, S. pneumoniae to penicillin bility data set as a reference. OR < 1 indicates a decrease and Salmonella spp. to fluoroquinolone. In addition, Entero- in percent antibiotic susceptibility in 2015–2016 vs. 2011– coccus faecium and E. faecalis were grouped together in ma- 2013. OR > 1 indicates an increase in percent antibiotic jority of the hospitals reports and corresponding antibiotic susceptibility in 2015–2016 vs. 2011–2013. The 2015– susceptibility patterns were reported for the Enterococcus 2016 Lebanese data were compared with the 2015–2016 genus without differentiation between the two species. As European data in the same manner using the European re- for Acinetobacter spp. susceptibility to colistin, all laborator- sults as a reference. OR < 1 indicates a decreased percent ies did not use the broth microdilution method, which is susceptibility while OR > 1 indicates an increased percent recommended by CLSI and EUCAST guidelines. In- susceptibility in Lebanon compared to the European stead, 6/13 laboratories used automated minimal in- countries. The Bonferroni method was used for adjusting hibitory concentration (MIC) method, 5/13 laboratories the p-value for multiple testing. A p-value of < 0.05 was used disc diffusion (DD) method, and 2/13 laboratories did considered to be statistically significant. not report results (Additional file 1). So, we did not report colistin susceptibility results in Acinetobacter spp. herein. Results Upon comparing the methods in this study to that of Microbiological techniques and AST methods 2011–2013 study, i.e. in terms of the source of data and The included hospitals represented all geographical the calculation of percent susceptibility, both studies were zones/governorates of the country, except for the Bekaa comparable. Concerning the methods used in detecting Table 1 Demographics and antibiotic susceptibility testing methods in the 13 participating hospitals Hospital Region Type Beds Microbiological Method Guidelines HDF Beirut University 444 Automated EUCAST LAUMC-RH Beirut University 114 Manual CLSI + EUCAST RHUH Beirut University 250 Automated CLSI AUBMC Beirut University 380 Manual CLSI MGH Beirut University 170 Manual CLSI Zahraa Mount Lebanon University 201 Manual + Automated CLSI CHU-NDS Mount Lebanon University 250 Automated CLSI + EUCAST MEIH Mount Lebanon University 150 Manual EUCAST SGH Mount Lebanon University 400 Manual CLSI Nini North Lebanon Community 175 Manual CLSI CHdN North Lebanon University 180 Manual CLSI Haykal North Lebanon Community 120 Automated CLSI Labib MC South Lebanon Community 120 Automated CLSI KEY: HDF Hotel Dieu de France, LAUMC-RH Lebanese American University Medical Center – Rizk Hospital, RHUH Rafic Hariri University Hospital, AUBMC American University of Beirut Medical Center, MGH Makassed General Hospital, CHU-NDS Centre Hospitaler Universitaire Notre Dame de Secours, MEIH Middle East Institute of Health, SGH Saint Georges Hospital, CHdN Centre Hospitalier du Nord, MC Medical Center, EUCAST European Committee on Antimicrobial Susceptibility Testing, CLSI Clinical and Laboratory Standards Institute All of the participating hospitals are private, except for RHUH that is a public hospital Automated microbial identification system: Vitek, BD Phoenix Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 5 of 17 and confirming susceptibility or resistance of some patho- production by 2 out of 13 hospitals. ESBL production was gens to specific antimicrobial agents that we mentioned observed in 34% of Enterobacteriaceae spp. (ranging be- earlier, both studies were comparable as well, except in tween 25 and 43%) from 8 of the 13 laboratories that the detection of ESBL and carbapenemase production in followed the international guidelines for detecting this re- Enterobacteriaceae (personal communication) (Additional sistance mechanism. Similarly, the mean proportion of file 1). However, comparison was made only between 3GC carbapenemase production was 0.6% in case of E. coli and and carbapenem susceptibility results in Enterobacteria- 2% in case of Klebsiella spp. as generated from only 2 of ceae and that related to detection of ESBL or carbapenea- the 13 laboratories (Additional file 3). mase enzymes was not carried on between the 2 study The susceptibility results of P. aeruginosa isolates from periods. all hospitals were as follows: 80% to ceftazidime, 78% to piperacillin/tazobactam, 70% to imipenem, 69% to mero- Types of bacteria and antibiotic susceptibility results penem, 73% to ciprofloxacin, 85% to amikacin and 98% During the study period of 2015–2016, a total of 85,144 to colistin (Table 3). Percent susceptibility of P. aerugi- clinical isolates were included in this compilation anti- nosa to carbapenems among all centres ranged from 55 biogram: 76% were Gram negative and 24% were Gram to 95% (Additional file 4). positive organisms. The distribution of the tested isolates Regarding Acinetobacter spp., mean percent antibiotic per governorate is depicted in Fig. 2. susceptibility was calculated from 11 hospitals where Among the tested Enterobacteriaceae spp., the mean per- 12% of the tested isolates were susceptible to carbapen- cent susceptibility to antibiotics was as follows: 59% to 3GC ems ranging from 3 to 74% (Additional file 4) and 80% (58% in E. coli and 63% in Klebsiella spp.), 77% to cefoxitin were susceptible to tigecycline (Table 3). (76% in E. coli and 83% in Klebsiella spp.), 97% to carba- The antibiotic susceptibility of Salmonella spp. was tested penems (97% in E. coli and 96% in Klebsiella spp.), 60% to in 10 hospitals, where 97% of the isolates were found to be ciprofloxacin (57% in E. coli and 71% in Klebsiella spp.), susceptible to 3GC, 90% to ciprofloxacin and 71% to 91% to amikacin (90% in E. coli and 94% in Klebsiella spp.), trimethoprim-sulfamethoxazole (Table 4). Herein, the range 54% to trimethoprim-sulfamethoxazole (53% in E. coli and of fluoroquinolone susceptibility in Salmonella spp. among 58% in Klebsiella spp.) and 83% to nitrofurantoin (87% in centres was from 56 to 100% (Additional file 5). E. coli and 59% in Klebsiella spp.). (Table 2). Among S. aureus isolates, the susceptibility results The proportion of ESBL and carbapenemase produc- were as follows: 72% to oxacillin/methicillin, 81% to cip- tion among Enterobacteriaceae did not coincide with the rofloxacin, 81% to clindamycin and 73% to erythromycin susceptibility results obtained for 3GC and carbapenems, (Table 5). Although one would expect all isolates to be respectively, because for reporting the presence of these completely susceptible to vancomycin, one laboratory re- enzymes, we selectively included those laboratories that ported a resistance of 4% using the automated system. reported their findings based on confirmatory tests used Susceptibility to oxacillin/methicillin ranged from 52 to to detect the presence of these resistance mechanisms 86% among all centres (Additional file 6). and did not just depend on the antibiogram results. De- Among isolated Enterococci spp., the susceptibility re- tection of ESBL production in Enterobacteriaceae spp. sults were as follows: 75% to ampicillin, 98% to vanco- was reported by 8 out of 13 hospitals and carbapenemase mycin and 99% to both tigecycline and linezolid (Table 5). Fig. 2 Distribution of the total clinical isolates in 2015 and 2016 (%) among the governorates of Lebanon (N = 85,144 isolates) Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 6 of 17 Table 2 Percent antibiotic susceptibility of E. coli, and Klebsiella spp. during 2015/2016 compared to corresponding susceptibility results in 2011/2013 Antibiotic E. coli Klebsiella spp 2011/2013 N (%S) 2015/2016 N (%S) OR (95%CI) P 2011/2013 N (%S) 2015/2016 N (%S) OR (95% CI) P Amikacin 29,667 (97%) 41,818 (90%) 0.29 (0.26–0.3) 0.0001 7768 (96%) 9498 (94%) 0.65 (0.57–0.75) 0.0001 Amoxicillin/ 30,411 (61%) 39,116 (59%) 1.13 (1.10–1.17) 0.0001 7883 (67%) 9069 (62%) 0.80 (0.75–0.86) 0.0001 clavulanic acid Ampicillin 22,985 (23%) 35,906 (24%) 1.06 (1.02–1.10) 0.01–– – – Aztreonam 27,221 (66%) 40,029 (57%) 0.65 (0.63–0.67) 0.0001 7020 (69%) 7924 (65%) 0.83 (0.78–0.90) 0.0001 Cefepime 26,314 (74%) 40,524 (62%) 0.60 (0.58–0.62) 0.0001–– – – Cefoxitin 23,858 (87%) 33,104 (76%) 0.47 (0.45–0.50) 0.0001 5853 (89%) 6373 (83%) 0.60 (0.54–0.67) 0.0001 Ceftazidime 28,730 (71%) 41,816 (62%) 0.73 (0.71–0.76) 0.0001 7335 (71%) 9498 (64%) 0.73 (0.68–0.78) 0.0001 Ceftriaxone 20,059 (64%) 41,816 (58%) 0.85 (0.82–0.88) 0.0001 4750 (65%) 9498 (63%) 0.92 (0.85–0.99) 0.02 Cefuroxime 24,662 (59%) 33,106 (56%) 0.96 (0.93–0.99) 0.02 6516 (64%) 6579 (61%) 0.88 (0.82–0.94) 0.0004 Ciprofloxacin 29,411 (55%) 40,524 (57%) 1.22 (1.19–1.26) 0.0001 7883 (73%) 9311 (71%) 0.91 (0.85–0.97) 0.004 Gentamicin 29,327 (72%) 41,818 (72%) 1.00 (0.98–1.03) 1 7601 (75%) 9498 (78%) 1.18 (1.10–1.27) 0.0001 Imipenem 30,411 (99%) 41,813 (97%) 0.33 (0.29–0.37) 0.0001 7883 (98%) 9498 (96%) 0.49 (0.41–0.60) 0.0001 Nitrofurantoin 18,422 (96%) 29,434 (87%) 0.28 (0.26–0.30) 0.0001 4356 (52%) 5155 (59%) 1.33 (1.22–1.44) 0.0001 Piperacillin/ 28,739 (83%) 40,524 (76%) 0.84 (0.81–0.873) 0.0001 7618 (81%) 9292 (78%) 0.83 (0.77–0.90) 0.0001 tazobactam Tigecycline 9716 (98%) 39,050 (96%) 0.24 (0.20–0.30) 0.0001 2243 (87%) 8546 (93%) 1.99 (1.71–2.31) 0.0001 Trimethoprim/ 29,689 (49%) 41,496 (53%) 1.13 (1.10–1.16) 0.0001 7709 (57%) 9498 (58%) 1.04 (0.98–1.11) 0.2 sulfamethoxazole KEY = CI confidence interval, N Number of isolates tested in each bacteria/antibiotic combination, OR Odds Ratio, S Susceptibility, % percent P < 0.05 is considered statistically significant The 2011/2013 data are taken from: Chamoun K, Farah M, Araj G, et al. Surveillance of antimicrobial resistance in Lebanese hospitals: retrospective nationwide compiled data. Int J Infect Dis. 2016;46:64–70 Ampicillin and vancomycin susceptibility ranged from 46 results, 75% were susceptible to penicillin, with the individ- to 96% and from 83 to 100% among all centres, respect- ual institutional susceptibility ranging between 60 and 79%. ively (Additional file 6). Mean fluoroquinolone susceptibility was 99%using data Regarding S. pneumoniae, three hospitals were compliant from 8 hospitals. The antibiotic susceptibility results for all with the CLSI and EUCAST guidelines and determined Streptococcus spp. are shown in “Additional file 7”.One la- penicillin MIC. Of the tested isolates from three of the boratory reported penicillin resistance in S. agalactiae (3%) eight hospitals that reported S. pneumoniae susceptibility using the automated system. Table 3 Percent antibiotic susceptibility of Acinetobacter spp. and P. aeruginosa during 2015/2016 compared to corresponding susceptibility results in 2011/2013 Antibiotic Acinetobacter spp P. aeruginosa 2011/2013 N (% S) 2015/2016 N (% S) OR (95% CI) P 2011/2013 N (% S) 2015/2016 N (% S) OR (95% CI) P Amikacin 3329 (16%) 3675 (19%) 1.23 (1.11–1.36) 0.0001 7675 (89%) 9005 (85%) 0.70 (0.62–0.79) 0.0001 Aztreonam NA NA NA NA 7483 (76%) 7457 (79%) 1.19 (1.06–1.33) 0.002 Cefepime 3409 (13%) 3675 (13%) 1.00 (0.89–1.12) 1 7897 (83%) 9005 (81%) 0.87 (0.79–0.97) 0.01 Ceftazidime 3343 (12%) 3675 (13%) 1.10 (0.973–1.23) 0.14 7897 (82%) 9005 (80%) 0.88 (0.79–0.97) 0.01 Ciprofloxacin 3379 (12%) 3675 (11%) 0.91 (0.80–1.02) 0.12 7897 (77%) 9005 (73%) 0.81 (0.74–0.89) 0.0001 Gentamicin 3384 (19%) 3675 (14%) 0.70 (0.62–0.78) 0.0001 7722 (83%) 9005 (81%) 0.87 (0.79–0.97) 0.01 Imipenem 3409 (18%) 3675 (12%) 0.62 (0.56–0.70) 0.0001 7897 (73%) 9005 (70%) 0.86 (0.79–0.94) 0.001 Piperacillin/ 3343 (13%) 3675 (11%) 0.83 (0.73–0.93) 0.12 7897 (80%) 9005 (78%) 0.89 (0.80–0.98) 0.02 tazobactam KEY = CI confidence interval, N Number of isolates tested in each bacteria/antibiotic combination, NA not available, OR Odds Ratio, S Susceptibility, % percent P < 0.05 is considered statistically significant The 2011/2013 data are taken from: Chamoun K, Farah M, Araj G, et al. Surveillance of antimicrobial resistance in Lebanese hospitals: retrospective nationwide compiled data. Int J Infect Dis. 2016;46:64–70 Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 7 of 17 Table 4 Percent antibiotic susceptibility of Salmonella spp. Upon comparing the Lebanese and European findings, during 2015/2016 compared to corresponding susceptibility we noticed that the Lebanese percent antibiotic suscepti- results in 2011/2013 bilities in the formerly stated organisms were lower than Antibiotic 2011/2013 2015/2016 OR (95% CI) P those reported from Northern and Western European N (%S) N (%S) countries and were similar or close to those in Eastern Ampicillin 784 (81%) 596 (85%) 1.34 (1.00–1.79) 0.06 and South-eastern Europe. Ceftriaxone 690 (97%) 655 (97%) 0.99 (0.53–1.87) 1 Regarding E. coli, Lebanon reported the lowest percent susceptibility to 3GC (58%) compared to findings from Ciprofloxacin 877 (95%) 721 (90%) 0.48 (0.32–0.70) 0.0001 Italy (70.1%), Greece (81.3%), and Spain (86.7%) (Fig. 4) Trimethoprim/ 877 (92%) 721 (71%) 0.21 (0.16–0.28) 0.0001 sulfamethoxazole (Additional file 8). Carbapenem susceptibility in E. coli was also the lowest in Lebanon (97%) yet close to that KEY = CI confidence interval, N Number of isolates tested in each bacteria/ antibiotic combination, OR Odds Ratio, S Susceptibility, % percent from Romania (98.6%), and lower than values from Italy P < 0.05 is considered statistically significant a (99.8%) and Greece (98.95%) (Fig. 4) (Additional file 9). The 2011/2013 data are taken from: Chamoun K, Farah M, Araj G, et al. Surveillance of antimicrobial resistance in Lebanese hospitals: retrospective As for Klebsiella spp., 3GC and carbapenem percent nationwide compiled data. Int J Infect Dis. 2016;46:64–70 susceptibility in Lebanon were not the lowest. 3GC sus- ceptibility (63%) was similar to that reported from Comparison with the 2011–2013 antibiotic susceptibility Luxembourg (67.9%), Hungary (62.7%), and Cyprus results (62.9%). It was higher than that from Greece (29%) and The 2011–2013 compilation of antibiotic susceptibility Italy (44.2%), yet lower than Spain (78.7%) (Fig. 5) (Add- data has locally been considered as the most representa- itional file 10). Regarding carbapenem susceptibility, our tive report on national AMR surveillance in Lebanon for result (96%) was similar to that from Bulgaria (96.1%), that time period. When the current data were compared higher than that from Greece (35.6%) and lower than with those of 2011–2013, there were few results that that from Spain (97.9%) (Fig. 5) (Additional file 11). were not mentioned in the former study, such as suscep- As for carbapenem percent susceptibility in P. aerugi- tibilities of P. aeruginosa to colistin, Enterococcus spp. to nosa, Lebanon was among countries reporting a low linezolid and S. pneumoniae to penicillin. level (70%) but was not the lowest. Susceptibility data re- In general, we observed that the variation in the per- ported from Poland (68.4%) and Bulgaria (72.1%) were cent susceptibility in majority of the antibiotic–microbe similar to ours. Our carbapenem susceptibility was combinations between both periods was less than 10%, higher than that from Greece (58.8%) and Romania primarily exhibiting a trend of decreasing susceptibility. (41.1%), and lower than that from Italy (76.8%) and A decreasing trend in antibiotic susceptibility (between Spain (78%) (Fig. 6) (Additional file 12). 5 and 10%) was observed in the following cases: E. coli to In Lebanon, carbepenem percent susceptibility in Aci- nitrofurantoin, Klebsiella spp. to cefoxitin, Acinetobacter netobacter spp. is very low (13%), yet our country shared spp. to imipenem, Salmonella spp. to ciprofloxacin and similar results with Romania (16.8%) (Fig. 6) (Add- Enterococci to ampicillin (Tables 2, 3, 4 and 5)(Fig. 3). itional file 13). Values were lower from Croatia (8.3%) A decrease in antibiotic susceptibility (less than 5%) was and Greece (5.6%), higher from Italy (21.6%), and much observed in the following cases: E. coli to imipenem, Kleb- higher from Spain (42%). siella spp. to imipenem, P. aeruginosa to imipenem and S. Concerning Gram positive organisms, Lebanese results aureus to oxacillin/methicillin (Tables 2, 3 and 5)(Fig. 3). on S. aureus susceptibility to methicillin (72%) were However, there was a considerable decrease in anti- comparable with those from Slovakia (72.4%) and Spain biotic susceptibility (10% or more) in the following or- (74.5%), and higher than findings from Italy (66.2%) and ganisms: E. coli to cefepime, E. coli to cefoxitin and Greece (60.9%) (Fig. 7) (Additional file 14). Penicillin Salmonella spp. to trimethoprim-sulfamethoxazole and susceptibility in S. pneumoniae reached 75% in Lebanon. S. aureus isolates to levofloxacin (Tables 2, 4 and 5). This value was similar to those reported from Bulgaria (74.9%), Spain (75.8%), and France (75.9%). It was lower Comparison with 2015–2016 EARS-net data than findings from Italy (90.6%). Data from Greece were For the comparison of the 2015–2016 Lebanese data to not available (Fig. 7) (Additional file 15). European surveillance data during the same period, we fo- cused on the following antibiotic-bacteria susceptibility pat- Discussion terns: E.coli and Klebsiella spp. percent susceptibility to Epidemiologic representativeness of the bacterial Pool 3GC and to carbapenems each separately, P. aeruginosa and This study reports a compilation of antibiotic suscepti- Acinetobacter spp. percent susceptibility to carbapenems bility data retrieved from the antibiogram pamphlets each separately, S. aureus percent susceptibility to methicil- generated by 13 hospital laboratories located in different lin, and S. pneumoniae percent susceptibility to penicillin. Lebanese governorates, whose work was standardised Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 8 of 17 Table 5 Percent antibiotic susceptibility of gram-positive bacteria (S. aureus, S. pneumoniae, Enterococcus spp.) during 2015/2016 compared to corresponding susceptibility results in 2011/2013 Antibiotic S. aureus S. pneumoniae Enterococcus spp. 2011/2013 2015/2016 OR (95% CI) P 2011/2013 2015/2016 OR (95% CI) P 2011/2013 2015/2016 OR (95% CI) P N (%S) N (%S) N (%S) N (%S) N (%S) N (%S) Ampicillin NA NA NA NA NA NA NA NA 3847 (84%) 3760 (75%) 0.57 (0.51–0.64) 0.0001 Clindamycin 4359 (83%) 6452 (81%) 0.87 (0.79–0.96) 0.01 588 (76%) 584 (75%) 0.95 (0.73–1.24) 1 NA NA NA NA Erythromycin 4890 (76%) 6304 (73%) 0.85 (0.78–0.93) 0.0004 544 (63%) 584 (65%) 1.09 (0.86–1.39) 1 NA NA NA NA Levofloxacin 2297 (84%) 2873 (72%) 0.49 (0.43–0.56) 0.0001 483 (91%) 584 (99%) 1.07 (0.72–1.40) 1 NA NA NA NA Oxacillin 4752 (73%) 6452 (72%) 0.95 (0.87–1.03) 0.25 NA NA NA NA NA NA NA NA Tigecycline 492 (99%) 1788 (99%) 1.03 (0.33–2.63) 0.985 NA NA NA NA 723 (99%) 1022 (99%) 0.10 (0.35–1.64) 0.983 Trimethoprim/ 4604 (91%) 6437 (88%) 0.73 (0.64–0.82) 0.0001 296 (53%) 398 (55%) 1.08 (0.80–1.47) 1 NA NA NA NA sulfamethoxazole Vancomycin 4890 (100%) 6452 (100%) 1.32 (0.03–1.47) 0.819 NA NA NA NA 4145 (99%) 3760 (98%) 0.49 (0.33–0.72) 0.0003 KEY = CI confidence interval, N Number of isolates tested in each bacteria/antibiotic combination, NA not available, OR Odds Ratio, S Susceptibility, % percent P < 0.05 is considered statistically significant The 2011/2013 data are taken from: Chamoun K, Farah M, Araj G, et al. Surveillance of antimicrobial resistance in Lebanese hospitals: retrospective nationwide compiled data. Int J Infect Dis. 2016;46:64–70 Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 9 of 17 Fig. 3 Percentage of resistance among six clinically important bacteria in Lebanon during 2011–2013 and 2015–2016, described by the World Health Organization as priority organisms for research and development of new antimicrobials. KEY: CAR carbapenem, FQ fluoroquinolone, MET methicillin, 3GC third-generation cephalosporins, R resistant. N.B. P < 0.05 is considered statistically significant AB Fig. 4 E. coli percent susceptibility to third-generation cephalosporins (a) and to carbapenems (b) in Lebanon in 2015 and 2016 in comparison with similar data from countries of the European Union, based on the 2015 and 2016 annual reports of the European Antimicrobial Resistance Surveillance Network (EARS-Net) Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 10 of 17 AB Fig. 5 K. pneumoniae percent susceptibility to third-generation cephalosporins (a) and to carbapenems (b) in Lebanon in 2015 and 2016 in comparison with similar data from countries of the European Union, based on the 2015 and 2016 annual reports of the European Antimicrobial Resistance Surveillance Network (EARS-Net) and compliant with the CLSI or the EUCAST guidelines susceptibility to different antibiotics was non-available in on bacterial identification and AST [13–17]. Only 13 of the GLASS report [20]. This situation emphasizes the the 150 hospital laboratories were included because the necessity for establishing an official surveillance system remaining hospitals did not fulfil the inclusion criteria. that should be included in the national plan for control- This highlights the need for improving the performance ling the emergence and spread of AMR. of microbiology laboratories through standardisation and external quality control. Since 2017, workshops, Range of antibiotic percent susceptibility among the aiming at capacity building and improving the perform- Lebanese hospitals ance of microbiology laboratories nationwide, have been In this study, we observed a wide range in the reported per- held by the Lebanese Ministry of Health and supported cent susceptibility among the tested organisms to certain an- by the WHO (unpublished data). tibiotics such as in the case of susceptibilities of Klebsiella In countries where official national or international spp. to 3GC (35–72%), Acinetobacter spp. to carbapenems AMR surveillance is not applied, the available antibiotic (3–74%), P. aeruginosa to carbapenems (55 to 95%), and S. susceptibility data are considered to be representative of aureus to oxacillin (52–86%). These organisms are major the countries [3]. In early 2018, the WHO released the causative agents of healthcare-associated infections. Accord- first Global Antimicrobial Resistance Surveillance Sys- ingly, we hypothesized that variability in the reported resist- tem (GLASS) report in its early implementation phase ance patterns in these organisms might be due to different (2016–2017), which included AMR data from two Leba- resistant clones circulating in different hospitals [5, 6, 21, nese hospital laboratories whose 2015–2016 AMR data 22]. A multicentre nationwide cross-sectional study investi- are included in our study [20]. The number of organisms gated the prevalence and molecular basis of carbapenem re- included in this compilation (85,144) outweighs the sistance in Gram-negative bacteria collected from 11 tertiary number of organisms included in the GLASS data from care hospitals, geographically distributed over 5 Lebanese Lebanon (1309), and in the latter, data collection was Governorates in 2012 [6]. Two of these hospitals provided during 2016 only [20]. Data on P. aeruginosa AST data in our study herein, one from Beirut and the other Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 11 of 17 AB Fig. 6 P. aeruginosa (a) and Acinetobacter spp. (b) percent susceptibility to carbapenems in Lebanon in 2015 and 2016 in comparison with similar data from countries of the European Union, based on the 2015 and 2016 annual reports of the European Antimicrobial Resistance Surveillance Network (EARS-Net) from South Lebanon. Investigators reported high-level car- of the range for susceptibility of 3GC was 70% for E. coli bapenem resistance in A. baumannii and P. aeruginosa, and 72% for Klebsiella spp. meaning that all reporting hospi- 88% (638/724 isolates) and 41% (760/1848 isolates), re- tals detected resistance to 3GC at different degrees (at least spectively [6]. Ninety percent of the carbapenem-resistant 30% in E. coli and 28% in Klebsiella spp). This finding could A. baumanni produced OXA-23 carbapenemase and 16% be explained by that 3GC resistance in Enterobacteriaceae of the carbapenem-resistant P. aeruginosa isolates har- has possibly spread in the community and reached the hos- boured VIM-2 metallo-b-lactamase. In addition, the diffu- pital setting from the community. As mentioned previously, sion of these enzymes was primarily due to clonal the tested organisms in this study originated from pooled dissemination [6]. Another recent multicentre study by hospital laboratory data, where there was no differentiation Atrouni et al. investigated the molecular epidemiology of between hospital-acquired or community-acquired infec- A. baumannii strains isolated from various types of clinical tions. A single centre study from a university hospital in specimens from 7 hospitals situated in different regions in Beirut evaluating the epidemiology of bacteremia in cancer Lebanon between 2013 and 2015 [5]. Investigators showed patients showed that the percentage of hospital-acquired that out of 119 non-duplicate isolates, 76.5% were resist- 3GC resistance in Enterobacteriaceae causing bacteremia ant to carbapenems and the most common carbapene- was 51% and that broad-spectrumantibioticexposuredur- mase was the OXA-23-type, found in 82 isolates [5]. In ing hospital stay was a risk factor for the acquisition of this study, 2 out of 7 centres were included in our 3GC-resistant organisms [23]. In another Lebanese study current study, one from Beirut and the other from on community-acquired urinary tract infections caused North Lebanon. The study by Atrouni et al. highlighted by E. coli and Klebsiella spp. collected from 3 hospitals, the nationwide dissemination of highly related Moghnieh et al. found that the percentage of 3GC re- OXA-23-producing carbapenem-resistant A. bauman- sistance was 31% in E. coli and 29% in Klebsiella spp. nii in Lebanese hospitals [5]. during 2010 and 2011 [24]. Regarding Enterobacteriaceae, 3GC susceptibility was not Similarly, the range of susceptibility of Enterobacteria- 100% in any of the included hospitals, where the upper limit ceae to fluoroquinolones was 44–74% in E. coli and 56– Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 12 of 17 AB Fig. 7 S. aureus percent susceptibility to methicillin (a) and S. pneumonaie percent susceptibility to penicillin (b) in Lebanon in comparison with countries of the European Union during 2015 and 2016, based on the 2015 and 2016 annual reports of the European Antimicrobial Resistance Surveillance Network (EARS-Net) 80% in Klebsiella spp. So E. coli and Klebsiella spp. resistance in Eneterobacteriaceae was 1.2% [6]. The spread fluoroquinolone resistance was detected at different of carbapenem-resistant Enterobacteriaceae (CRE) in levels in the participating hospitals (at least 26% from E. Lebanese hospitals is still lower than resistance to 3GC or coli and 20% from Klebsiella spp.). In the study on fluroquinolones and carbapenem resistance in Enterobac- community-acquired urinary tract infections, Moghnieh teriaceae is predominantly due to OXA-48-like carbapene- et al. reported a similarly elevated level of fluoroquinolone mases production [6, 23, 24]. As for risk factors for CRE resistance in E. coli and Klebsiella spp. (42 and 33%, re- infection, Kanafani et al. found that the respiratory tract spectively) [24]. This high percentage of fluoroquinolone and blood as primary infection sites and prior antibiotic resistance can be attributed to the misuse of this class of use in the hospital setting were independent risk factors antibiotics since it is available over-the-counter in Leba- for its nosocomial acquisition [27]. There is a plausible nese community pharmacies [25, 26]. risk for the transmission of resistant pathogens from the Regarding susceptibility of Enterobacteriaceae to carba- hospital environment into the community in the absence penems, the upper limit of the range was 100% in E. coli of rigorous infection control practices, efficient sanitation and Klebsiella spp.. So, there were hospitals that still re- and sewage disposal and in a setting where antimicrobials ported 100% susceptibility, 2 of them for both E. coli and are used in veterinary medicine without control. Daoud et Klebsiella spp. and 1 for Klebsiella spp. and not E. coli. al. confirmed this possibility when they detected a New The rest of the hospitals, 11 in case of E. coli and 10 in Delhi metallo-beta-lactamase-1-producing Enterobacteria- Klebsiella spp., reported different levels of carbapenem re- ceae strain in sewage water [28]. sistance ranging from 1 to 5% in E. coli and 1 to 10% in Klebsiella spp. Two hospitals additionally reported carba- Changing trends in antibiotic susceptibility compared penemase production among their isolates. Hammoudi et with the 2011–2013 report al., in their multicentre cross-sectional study mentioned The “WHO AMR study group” listed 13 organism/anti- earlier, showed that the mean prevalence of carbapenem biotic combinations, other than drug-resistant Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 13 of 17 Mycobacterium tuberculosis, to be of high priority for dis- present AMR rates on the global map, Lebanon, among covery, research and development of new antibiotics [1]. In many other countries of the Eastern Mediterranean re- our study, 6 of these priority organisms have been described: gion, is not included due to the lack of national surveil- 3GC-resistant Enterobacteriaceae, carbapenem-resistant En- lance data. A recently published narrative review of terobacteriaceae, carbapenem-resistant P. aeruginosa, carba- literature showed the significantly increasing prevalence penem-resistant Acinetobacter spp., fluoroquinolone- of antibacterial resistance in different countries of the resistant Salmonella spp., and methicillin resistant S. aur- Arab World including Lebanon [3]. In the absence of eus. Other organisms stated in the “WHO AMR study official standardized AMR surveillance networks in group” priority list were not included for the following rea- neighbouring Arab countries, we chose to compare our sons: lack of data as in the case of M. tuberculosis,avery data with those from EARS-Net aiming to position small number of isolates of certain species reported by Lebanon on the global map of AMR, and taking into Lebanese laboratories such Campylobacter spp. and Shi- account the geographical proximity between Lebanon gella spp., and non-standardised methodologies used in the and several Southern and South-eastern European Lebanese laboratories like in reporting penicillin sus- countries. The EARS-Net annual AMR surveillance re- ceptibility in S. pneumoniae and vancomycin suscepti- ports provide an accurate picture of the extent of AMR bility pooling in Enterococci without differentiating in the European Union (EU) [11, 12]. We believe that between E. faecalis and E. faecium. When the 2015– comparing AMR in Lebanon to that from relatively 2016 antibiotic susceptibility results of these 6 priority nearby countries in Europe would help the reader to organisms were compared to those of 2011–2013, a sta- visualize and benchmark the AMR situation in tistically significant decrease in susceptibility was dem- Lebanon. This comparison would, most importantly, help onstrated (Fig. 3). Lebanese professionals and officials visualize the actual size The emergence of antibiotic resistance has been strongly of theproblemscausedbyAMR andwould hencestimu- correlated to the inappropriate prescribing of antibiotics late them for serious interventions. Moreover, it could trig- [29]. In Lebanon, there are no national surveillance studies ger international organisations like the WHO, the Food describing antibiotic consumption on hospital setting, ra- and Agriculture Organization of the United Nations, the ther than very few hospital data showing that carbapenems World Organization for Animal Health, and others, to in- are among the most commonly prescribed antibiotics [30, clude Lebanon in global actions plans under the “One 31]. On the other hand, the extensive use of Health” approach that aim at limiting the spread and emer- over-the-counter antibiotics is of paramount importance in gence of AMR. aggravating the antimicrobial resistance. In Lebanon, the Upon reviewing European and Lebanese data using prevalence of dispensing broad-spectrum antibiotics with- percent susceptibility instead of resistance (Additional out prescription ranged from 32 to 42% among community files 8, 9, 10, 11, 12, 13, 14 and 15), our data was compar- pharmacies [25, 26, 32]. This situation calls for immediate able to those from countries in Southern and South-eastern action against these practices through improving public Europe including Bulgaria, Romania, Greece, Italy and and healthcare professional awareness on AMR, establish- Spain that reported in general low antibiotic susceptibility ing and implementing rigorous legislation that forbids the patterns, in comparison with the countries of North and dispensing of antibiotics over the counter, and establishing West Europe [11, 12]. In Lebanon, antimicrobials are dis- antimicrobial stewardship programmes in hospitals and pensed over-the-counter in pharmacies and antimicrobial the community. Antibiotics are not just used in humans, stewardship practices exist only in very few university hos- yet they are heavily administered for therapeutic and pitals [25, 26, 31, 32]. As for infection prevention and con- prophylaxis purposes in veterinary medicine, livestock trol (IPC) programmes, their presence is mandatory in production, crop culture and food production industry different healthcare facilities. However, the monitoring of [33]. In Lebanon, there are no national data describ- its function is variable across these facilities. At the national ing antibiotic use in the listed fields outside human level, the assessment of the appropriateness of IPC prac- health yet AMR has already emerged and is spreading tices is limited to the accreditation audit of done by the [34]. This necessitates adopting multifaceted, compre- Lebanese Ministry of Health every 3 years. Recently a Na- hensive, and integrated measures complying with the tional Action Plan in line with the WHO Global Action “One Health” approach to curb the emergence and Plan for fighting AMR is being prepared in Lebanon in col- spread of AMR, and preserve the efficacy of the laboration with the ministries of health, agriculture and en- remaining few active antibiotics [33]. vironment. This plan is directly supported by the WHO and its outcome may be reflected in future AMR surveil- Comparative epidemiology with European data on AMR lance studies. Joint efforts from representatives of the gov- Lebanon is a relatively small Arab country in the East- ernment and healthcare authorities are needed to ensure ern Mediterranean region. In international reports that the effectiveness of this plan for the upcoming years. Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 14 of 17 Regarding IPC practices in hospitals in North and already present global systems for providing accurate West Europe, surveillance of hospital-acquired infec- and reliable data. Moreover, there is a need for a tions and IPC practices is present through the establish- multifaceted programme for AMR containment based ment of national key performance indicators, which on the “One Health” approach. This programme should reflects a serious collaborative work in infection control include the implementation of rigorous infection preven- [35–38]. In addition, antibiotic consumption in hospitals tion and control programmes in hospitals, antimicrobial and the community, in these countries, is much lower stewardship programmes in both hospitals and the com- than others from South and East Europe, as reported to munity and the control of antibiotic use in livestock and the European Surveillance of Antimicrobial Consumption agriculture. Furthermore, raising awareness about the ex- Network (ESAC-Net) [39]. In 2015, Greece and Romania tent, implications and modalities of preventing AMR in were the countries with the highest consumption of anti- Lebanon should be performed for healthcare providers bacterials for systemic use in Europe [39]. In addition, des- and the public. Finally, research for developing alternative pite that components of IPC infrastructure are in place in therapies for infectious diseases, such as phage therapy hospital setting in several Southern and South-eastern and microbiota-based therapy, should be encouraged to countries, gaps leading to suboptimal IPC are present limit the abuse and subsequently the loss of effectiveness such as: insufficient time allocated to IPC activities by of available antimicrobials. healthcare givers and personnel due to understaffing, considerable variation in safety culture for effective IPC Key findings among different facilities, inadequate collaboration be-  Microbiological methods used for AMR detection in tween healthcare professionals at different levels, and Lebanese hospitals majorly conformed to the CLSI and absence of documented process audits that assess com- EUCAST guidelines on antibiotic susceptibility testing. pliance with IPC practices [40–44]. However, European  Non-uniformity in AMR reporting was observed in countries like Spain, Italy, Bulgaria and Romania, some cases, such as susceptibilities of Acinetobacter among others, are in the process of implementing their spp. to colistin, S. pneumoniae to penicillin and own national action plans for the control of AMR, in Salmonella spp. to fluoroquinolone. close collaboration with the European Centre for Dis-  A wide range of susceptibility results was reported ease Prevention and Control (ECDC) [40–44]. for each antibiotic–microbe combination among the 13 laboratories. Limitations and strengths  Fluoroquinolone resistance in Enterobacteriaceae, Despite the national effort to improve reporting of including Salmonella spp., has been established in antibiotic susceptibility in Lebanon, there is still a the Lebanese community. need for implementing uniform standardised micro-  Lebanese hospitals have become endemic for 3GC biological methods and adequate quality control sys- resistant-Enterobacteriaceae, and this resistance pattern tems in all Lebanese laboratories. The lack of both is apparently finding its way to the community. elements in majority of Lebanese hospitals has led to  Some hospitals laboratories reported the emergence limiting the number of included centres to only 13 of the of carbapenem-resistant Enterobacteriaceae and P. 152 governmental and private hospitals in Lebanon. An- aeruginosa, along with established and increasing other limitation is the lack of organism stratification as carbapenem resistance in Acinetobacter spp. per type of clinical specimen or per its site of acquisition,  Among Gram positive bacteria, S. aureus mean i.e. nosocomial or community. However, this report may percent susceptibility to methicillin was 72%, and serve as an example for countries that do not have stan- that of Enterococci to ampicillin was 75%. dardised national surveillance for AMR. This study and  Susceptibility of S. pneumoniae to penicillin reached the one published earlier allow Lebanon to be included in a mean of 75% from all tested isolates in 3 of the 13 the global AMR maps. Furthermore, generating local anti- hospitals in addition to the emergence of biograms is critical for establishing national clinical guide- levofloxacin-resistant strains in some centres. lines for the management of infectious diseases.  Despite the relatively short time between the 2011– 2013 and 2015–2016 compilation, a trend towards Conclusion decreasing antibiotic susceptibility of less than 10% The current compiled antibiotic susceptibility data have was observed among several clinically important shed light on increasing bacterial resistance trends in bacteria. Lebanon, which were found to be comparable with data  The 2015–2016 Lebanese data were found to be from some Eastern and Southern European countries. comparable with those from Eastern and South- However, there is a need for a robust national AMR surveil- eastern European countries, such as Greece, Spain, lance system in Lebanon, which could be included in the Italy and Bulgaria. These countries are in the process Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 15 of 17 of developing their own national action plans to Additional file 15: Table S1. S. pneumonaie percent susceptibility to fight AMR supported by the ECDC. penicillin countries of the European Union during 2015 and 2016, based on the 2015 and 2016 annual reports of the European Antimicrobial In Lebanon, a national action plan for combating 1,2 Resistance Surveillance Network (EARS-Net) , and comparison to AMR s being prepared in collaboration with 2015–2016 Lebanese data. (DOCX 110 kb) representatives of government, healthcare authorities and is supported directly by the WHO. Abbreviations 3GC: Third-generation cephalosporins; AMR: Antimicrobial resistance; AST: Antimicrobial susceptibility testing; BMD: Broth microdilution; CLSI: Clinical & Laboratory Standards Institute; CRE: Carbapenem-resistant Additional files Enterobacteriaceae; DD: Disc diffusion; EARS-Net: European Antimicrobial Resistance Surveillance Network; ECDC: European Centre for Disease Additional file 1: Table S1. The microbiological methods used in Prevention and Control; ESAC-Net: European Surveillance of Antimicrobial detecting certain resistance patterns in the included Lebanese hospitals Consumption Network; ESBL: Extended-spectrum beta-lactamase; and the corresponding Clinical and Laboratory Standards Institute (CLSI)/ EU: European Union; EUCAST: European Committee on Antimicrobial European Committee on Antimicrobial Susceptibility Testing (EUCAST) Susceptibility Testing; GLASS: Global Antimicrobial Resistance Surveillance guidelines recommendations. (DOCX 131 kb) System; IPC: Infection prevention and control; IRB: Institutional review board; MIC: Minimal inhibitory concentration; OR: Odd ratio; WHO: World Health Additional file 2: Formulas for mean percent (%) susceptibility Organization calculation. (DOCX 121 kb) Additional file 3: Table S1. E. coli and Klebsiella spp percent susceptibility* Acknowledgements to antibiotics in 13 Lebanese hospitals during 2015/2016. (DOCX 121 kb) We would like to acknowledge Dr. Georges Khazen for undergoing the Additional file 4: Table S1. Pseudomonas aeruginosa and Acinetobacter statistical analysis. We would also like to acknowledge Miss Nadia Lara Samaha spp. percent susceptibility* to antibiotics in 13 Lebanese hospitals and Miss Karen Abdallah for providing technical assistance in data entry. during 2015/2016. (DOCX 129 kb) Funding Additional file 5: Table S1. Salmonella spp. percent susceptibility* to None. antibiotics in 10 Lebanese hospitals during 2015/2016. (DOCX 70 kb) Additional file 6: Table S1. Staphylococcus aureus, coagulase negative a Availability of data and materials Staphylococci , and Enterococcus spp. percent susceptibility* to antibiotics All data generated or analysed during this study are included in this in 13 Lebanese hospitals during 2015/2016. (DOCX 115 kb) published article and its supplementary information files. Additional file 7: Table S1. Streptococcus pneumoniae, Streptococcus viridans, Streptococcus pyogenes, and Streptococcus agalactiae percent Authors’ contributions susceptibility* to antibiotics in 13 Lebanese hospitals during 2015/2016 . RM, GA, and RH were responsible for study conception, result analysis and (DOCX 103 kb) drafting of the manuscript. LA was responsible for data collection and analysis. ZD, JM, and TJ were responsible for microbiological methods Additional file 8: Table S1. E. coli percent susceptibility to third- evaluation and data analysis. DA performed data analysis and edited the final generation cephalosporins in countries of the European Union, based on version of the manuscript. NA, NH, MB, MY, GK, MH, MM, RA, EA, RF, and NY the 2015 and 2016 annual reports of the European Antimicrobial Resistance 1,2 provided the raw antibiotic susceptibility data from hospitals and Surveillance Network (EARS-Net) , and comparison to 2015–2016 Lebanese participated in study group discussions. All authors read and approved the data. (DOCX 110 kb) final version of the manuscript. Additional file 9: Table S1. E. coli percent susceptibility to carbapenems in countries of the European Union, based on the 2015 and 2016 annual Ethics approval and consent to participate reports of the European Antimicrobial Resistance Surveillance Network 1,2 This study is based on institutional antimicrobial susceptibility testing (AST) (EARS-Net) , and comparison to 2015–2016 Lebanese data. (DOCX 113 kb) yearly reports/pamphlets generated and distributed by clinical microbiology Additional file 10: Table S1. K. pneumoniae percent susceptibility to third- laboratories. This information is publically available. The institutional review generation in countries of the European Union, based on the 2015 and 2016 board (IRB) Committee of one of the participating hospitals, Makassed General annual reports of the European Antimicrobial Resistance Surveillance Network Hospital, Beirut, Lebanon, granted this study ethical approval. All data were 1,2 (EARS-Net) , and comparison to 2015–2016 Lebanese data. (DOCX 110 kb) purely based on microorganisms, and no patient data were included; hence, the IRB waived the requirement of informed consent from patients. Additional file 11: Table S1. K. pneumoniae percent susceptibility to carbapenems in countries of the European Union, based on the 2015 Consent for publication and 2016 annual reports of the European Antimicrobial Resistance 1,2 Not applicable. Surveillance Network (EARS-Net) , and comparison to 2015–2016 Lebanese data. (DOCX 106 kb) Competing interests Additional file 12: Table S1. P. aeruginosa percent susceptibility to The authors declare that they have no competing interests. carbapenems in countries of the European Union, based on the 2015 and 2016 annual reports of the European Antimicrobial Resistance 1,2 Surveillance Network (EARS-Net) , and comparison to 2015–2016 Publisher’sNote Lebanese data. (DOCX 114 kb) Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Additional file 13: Table S1. Acinetobacter spp. percent susceptibility to carbapenems in countries of the European Union, based on the 2015 Author details and 2016 annual reports of the European Antimicrobial Resistance 1,2 1 Department of Internal Medicine, Division of Infectious Diseases, Makassed Surveillance Network (EARS-Net) , and comparison to 2015–2016 General Hospital, Beirut, Lebanon. Faculty of Medicine, Lebanese University, Lebanese data. (DOCX 112 kb) Beirut, Lebanon. Professor and Director of Clinical Microbiology, Department Additional file 14: Table S1. S. aureus percent susceptibility to of Pathology and Laboratory Medicine, American University of Beirut Medical methicillin in countries of the European Union during 2015 and 2016, Center, Beirut, Lebanon. Pharmacy Department, Makassed General Hospital, based on the 2015 and 2016 annual reports of the European 1,2 Beirut, Lebanon. Department of Microbiology, Centre Hospitalier du Nord, Antimicrobial Resistance Surveillance Network (EARS-Net) , and Zgharta, Lebanon. Faculty of Medicine and Medical Sciences, University of comparison to 2015–2016 Lebanese data. (DOCX 111 kb) Balamand, Koura, Lebanon. Department of Internal Medicine, Division of Moghnieh et al. Antimicrobial Resistance and Infection Control (2019) 8:41 Page 16 of 17 Infectious Diseases, Lebanese American University-Rizk Hospital, Beirut, 15. The European Committee on Antimicrobial Susceptibility Testing. Lebanon. 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