Nationwide Proficiency Assessment of Bacterial Identification and Antimicrobial Susceptibility Testing in Lebanon (2021) PDF

Original Article Nationwide proficiency assessment of bacterial identification and antimicrobial susceptibility testing among 110 laboratories in Lebanon George F Araj1, Tarek Itani2, Atika Berry3, Dolla K Sarkis2 1 Department of Pathology and laboratory Medicine, American University of Beirut M...

Original Article Nationwide proficiency assessment of bacterial identification and antimicrobial susceptibility testing among 110 laboratories in Lebanon George F Araj1, Tarek Itani2, Atika Berry3, Dolla K Sarkis2 1 Department of Pathology and laboratory Medicine, American University of Beirut Medical Center, Beirut, Lebanon 2 Laboratoire des Agents Pathogènes, Faculty of Pharmacy, Saint-Joseph University of Beirut, Lebanon 3 Ministry of Public Health- Preventive Medicine Department, Beirut, Lebanon Abstract Introduction: Proficiency testing (PT) is one of the most valuable and important activities for the Clinical Microbiology Laboratories (CML) to enroll in to ensure the accuracy and reliability of results. This first time conducted nationwide study was warranted to assess the PT performance activity among CML in Lebanon. Methodology: Four training and PT activities were organized for 110 nationwide laboratories involved in providing clinical microbiology services. In each PT activity, five different bacterial species were distributed to each laboratory to provide identification (ID) and antimicrobial susceptibility testing (AMST) according to prior discussions and guidelines. Results: The percentages of labs that correctly identified the bacterial species and performed the relevant AMST to it, respectively, were as follows: S. aureus, (100% and 67.8%); Enterococcus faecalis (71% and 82%); Listeria monocytogenes (75% and 61%); Streptococcus agalactiae (86% and 71%); Corynebacterium amycolatum (7% and 33 %); Pseudomonas aeruginosa, (93 % and 53.4%); Klebsiella pneumoniae, (97% and 67.7%); Salmonella typhi ESBL (87 % and 66%); Enterobacter aerogenes (89% and 59%) and Stenotrophomonas maltophilia (84 % and 65%). The resistant types for the species were specified by labs as carbapenem resistant (CR) K. pneumoniae in 78 %, CR E. aerogenes in 34 %, MRSA in 83 %, and VRE in 80.5%. Conclusions: The wide variation as well as the overall humble scoring of accurate results reflects the dire need for the MOPH to establish and maintain a PT activity program, and entrust the reference laboratory to provide continuing education and training sessions. Key words: Proficiency testing; susceptibility testing; bacterial identification; Lebanon. J Infect Dev Ctries 2021; 15(12):1838-1844. doi:10.3855/jidc.15381 (Received 25 May 2021 – Accepted 30 August 2021) Copyright © 2021 Araj et al. This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Introduction Organization for Standardization (ISO) and College of Antimicrobial resistance (AMR) has been a surging American Pathologists (CAP), which can also problem, deleteriously impacting healthcare globally certify/accredit laboratories essentially relying on including Lebanon [1-4]. Among efforts to combat such quality management system (QMS) theme whereby a situation, the Clinical Microbiology Laboratories Proficiency Testing (PT) is an integral part [7-8]. (CMLs) play a major role especially in providing valid The PT program was first mandated for service identification and antimicrobial susceptibility results. providing clinical laboratories in the USA as part of the These are crucial in the treatment of patients suffering Clinical Laboratory Improvement Amendments from infectious diseases, as well as in public health (CLIA) act of 1988, entailing a quality management disease surveillance. system (QMS) theme. It is one of the most valuable However, like other service providing clinical and important activity to be implemented for any laboratories the CMLs are faced with great challenges laboratory that provides clinical services including the in providing sustainable accurate, reliable, trusted, CML. This is to ensure the proficiency, accuracy, and defensible, and credible test results in the detection and reliability of microbial ID and AMST analysis within analysis of recovered pathogens [5,6]. To maintain the overall quality process of the lab [10-12]. delivering credible results, several governmental In Lebanon and in the absence of such PT activity authorities and other international recognized in many CMLs, the National Antimicrobial Committee professional organizations have established programs (NAC) at the Ministry of Public Health (MOPH) towards this endeavor. These include the International realized the value of incorporating such warranted Araj et al. – AMR Proficiency testing in Lebanon J Infect Dev Ctries 2021; 15(12):1838-1844. program to the CMLs and urged to initiate it in 2015, in breakpoints for interpretation of AMST were also collaboration with the World Health Organization accepted to whoever follows them. (WHO) Country office in Lebanon. Since then, several training workshops (WSs) and other educational PT Isolates Preparation and Distribution to activities took place for governmental and other private Participating Labs CMLs nationwide. The PT isolates were clinical ones identified and Officialization of the PT training project by the speciated by the Matrix-Assisted Laser Desorption NAC was launched under the patronage of The Minister Ionization Time of Flight (MALDI-TOF) system of Public Health, Dr. Jamil Jabak, at Saint Joseph (Bruker Daltonik, GmbH, Bremen, Germany) at the University of Beirut (USJ), on the 18th of March 2019. American University of Beirut Medical Center Invitations were sent to all healthcare institutions (AUBMC). Preparation of the PT isolates and coding providing CM services in Lebanon. During this were coordinated between AUBMC, Saint-Joseph meeting, The Minister mentioned that the PT testing University of Beirut (USJ) and the MOPH. Isolates of should be mandatory and not a voluntary activity for the five different species were prepared. Each was CMLs. inoculated into two transport medium (Sterile Transport Subsequently, four training and PT activities took Swab with Amies Medium, Jiangsu Huida Medical place whereby 110 laboratories from all the governates Instruments, China) and distributed to the participant of Lebanon providing CM services were enrolled and labs. provided results. The fourth activity was a repeat PTs from 42 randomly selected laboratories. Hereby, we Antimicrobial Susceptibility Testing (AMST) address and present the results of these PT activities and The AMST for each of the distributed PT isolates discuss the performance reflected by the different was carried out using the CLSI DD guidelines. The participants from different regions in the country. minimal inhibitory concentrations (MICs) were also determined for these isolates by Vitek 2 system Methodology (BioMérieux, Marcy L’Etoile, France). In addition, E- Pre Activity Workshops-Imparted Information to the test methodology (AB BIODISK, Solna, Sweden) was Participating CML Staff used for characterizing those isolates with special The pre-PT educational workshops were initiated, resistance profiles. by CML specialists (GFA and DKS), to train and The staff in the participating laboratories were review diagnostic and antimicrobial clinical asked to identify and test each pathogen according to microbiology material for CML staff. A total of 185 the specified instructions provided in the distributed labs, encompassing all governates in Lebanon, were SOP, taking into consideration the source of the invited, 170 attended the discussion, among which 152 specimen. The distributed Gram-positive and Gram- labs (42 being repeaters in the 4th PT activity) negative bacterial species and the anticipated number of participated in the PT activities and submitted results. antimicrobial agents to test for each included: These sessions aimed at enlightening the participants Vancomycin resistant enterococci (VRE, 8 about the approaches and tests to use for bacterial antimicrobials for urinary isolates, and 4 for blood identification (ID) and antimicrobial susceptibility isolates), methicillin resistant Staphylococcus aureus testing (AMST) according to standardized quality (MRSA, 13 antimicrobials), Listeria monocytogenes (1 control essentially based on The Clinical and antimicrobial), Streptococcus agalactiae (5 Laboratory Standards Institute (CLSI) guidelines for antimicrobials), Corynebacterium amycolatum (6 disk diffusion (DD) test. Moreover, a summary antimicrobials), Pseudomonas aeruginosa (9 brochure entitled “Standard Operating Procedures antimicrobials), carbapenem resistant Klebsiella (SOP) for Antimicrobial Susceptibility Testing against pneumoniae (20 antimicrobials), Salmonella typhi (7 Commonly Encountered Bacterial Species in Humans” antimicrobials), carbapenem resistant Enterobacter was produced and distributed to the participants. It aerogenes (17 antimicrobials), Stenotrophomonas provided guidelines for each lab to follow about the maltophilia (3 antimicrobials). category and types of antimicrobial to test against the recovered pathogens from the specimen source. Arbitrary Scores The European Committee on Antimicrobial Arbitrary scores were assigned to the performance Susceptibility Testing (EUCAST) guidelines and of each lab based on their bacterial species ID score and AMST results, as well as the overall score for each lab, 1839 Araj et al. – AMR Proficiency testing in Lebanon J Infect Dev Ctries 2021; 15(12):1838-1844. as shown below. These scores were not meant or Results intended to assign ranking for labs, rather to utilize it as Numbers of Labs Invited, Participating in Discussion a tool for general assessment denominator in reflecting and Submitting Results performances in this study. The total number of labs invited (n= 185 labs ) / those attended the discussion (n = 170 labs) / and those Identification Score participated in the PT activities and submitted results The ID scores were calculated based on the (n=152 labs, including the 42 repeaters in activity 4), following criteria: a score of +5 was given to correct were as follows: Activity 1 (Date 9-4-2019): 35/34/31; species identification, a score of +3 to correct genus Activity 2 (Date 17-7-2019): 50/44/41; Activity 3 (Date identification, and no score was given to wrong 1-10-2019): 50/42/38 and Activity 4 (Date 26-11- identification. 2019): 50/50/42. The distribution of the 152 labs submitting PT Antimicrobial Susceptibility Testing Score results according to the different Governates were: The AMST scores were calculated based on the Greater Beirut, 19 Labs (12.5%); Mount Lebanon, 51 following criteria: a score of +5 was given to each of labs (33.5%); Bekaa/ Baalback/ Hermel, 21 labs (14%); the correctly reported antibiotic, a score of -3 was given North/ Akkar, 32 labs (21%); South/ Nabatieh, 29 labs to each incorrectly reported antibiotic, and a score of -1 (19%). was given to each of the reported misleading/ irrelevant The 42 repeaters labs from PT activity 4, and their antibiotic. results will be noted separately, while the analysis that follows will address the results of the 110 labs. Overall Score The overall score for each lab was calculated as Performance of Labs in Bacterial Identification cumulative of ID and AMST scores, reflecting a Table 1 summarizes the performance of 110 labs in percentage of the total correct anticipated scores. providing ID for the species level, genus level, the specified resistance types and the incorrect results. Provided Feedback to labs For the Gram-positive bacteria, the percentages of Feedback to labs was essentially based on sharing correct identification to the species level, genus level, the anticipated accurate results of ID and AMST for and incorrect results, respectively, provided by the labs each of the PT pathogen, an opportunity for each lab to were as follows for: S. aureus, 100 %, 0, and 0; E. assess its own performance anonymously. Also, group faecalis, 71%, 26%, 3%; L. monocytogenes, 75%, discussion took place about the findings, through 12.5%, and 12.5; S. agalactiae, 86%, 1%, and 13%; C. personnel presence or group e-mail correspondence. amycolatum, 7%, 54%, and 39%. The resistance types Moreover, a wrap-up webinar for all four PT activities for the species were specified as MRSA for the S. was organized on the 9th of December 2020. aureus by 83 %, and as VRE for the E. faecalis by Table 1. Summary of PT bacterial identification results provided by the 162 participating labs. No of Labs No (%) Providing Identification PT Bacterial Species Performing Specified Species Level Genus Level Incorrect PT Resistance Type Gram Positive Enterococcus faecalis 72 51 (71) 19 (26) 2 (3) Specified VRE 72 58 (80.5) S. aureus 72 100 (100) 0 0 Specified MRSA 72 60 (83) Listeria Monocytogenes 72 54 (75) 9 (12.5) 9 (12.5) Streptococcus agalactiae 80 69 (86) 1 (1) 10 (13) Corynebacterium amycolatum 80 6 (7) 43 (54) 31 (39) Gram Negative Pseudomonas aeruginosa 72 67 (93) 5 (7) 0 Klebsiella pneumoniae 72 70 (97) 2 (3) Specified CRE 72 56 (78) Salmonella typhi 80 70 (87) 6 (7) 5 (6) Enterobacter aerogenes 80 71 (89) 3 (4) 6 (7) Specified CRE 80 27 (34) Stenotrophomonas maltophilia 80 67 (84) 0 13 (16) 1840 Araj et al. – AMR Proficiency testing in Lebanon J Infect Dev Ctries 2021; 15(12):1838-1844. 80.5% of the labs. The rates for the Gram-negative The overall scores (ID plus AMST) for labs bacteria of correct identification to the species level, indicated that 50 labs scored ≤ 45, 26 labs scored genus level, and incorrect results, respectively, were as between 46% and 55%, 23 labs scored between 56% follows for: P. aeruginosa, 93%, 7%, 0; K. pneumoniae, and 65%, 8 labs scored between 66 % and 75%, while 97%, 3%, and 0; S. typhi, 87%, 6.5%, and 6.5%; E. 2 labs scored between 76% and 85%, and only one lab aerogenes, 89%, 4%, and 7%; S. maltophilia, 84%, 0, scored between 86% and 95%. and 16%. The resistance types for the species were specified as CRE for the K. pneumoniae by 56 of 72 (78 Results of Repeat PT testing in Activity 4 %) labs, and as CRE for the E. aerogenes by 34% of the Table 3 presents a summary of results reflecting the labs. performance of 42 labs repeating 5 PTs in the fourth activity. Compared to their first PT scores, the scores Performance of Labs in Antimicrobial Susceptibility for the repeated ID revealed no change in 29%, positive Testing change in 19%, and negative change in 52% of the labs, Table 2 summarizes the performance among different labs participating in the first three PT activities Figure 1. Summary of 110 Labs performance in regard to in regard to AMST results. For the Gram-positive identification, antimicrobial susceptibility testing, and overall bacteria, the percentages of correct AMST results are performance in the PT activity. presented in Table 2. They are summarized for the pathogens as follows: S. aureus (MRSA) (67.8%); E. faecalis (VRE) (82%); L. monocytogenes (61%); S. agalactiae (53.1%) and C. amycolatum (10.1 %). For the Gram-negative bacteria, they are summarized for the pathogens as follows: P. aeruginosa (53.4%); K. pneumoniae (CRE) (67.7%); S. typhi (ESBL) (59.4%); E. aerogenes (CRE) (48.8%) and S. maltophilia (50%). Overall Performance score for ID and AMST Results for all the labs Figure 1 shows the summary of 110 labs performance scores (%) in regard to ID, AMST and the overall performance in the first three PT activities. Concerning the ID, 28 labs showed a score of ≤ 75% (range ≤ 35- 75%), while 82 labs achieved a higher score, ranging between 76% and ≥ 96%. In regard to AMST, the majority of labs (n =107) scored ≤ 75% (range ≤ 35- 75%), while only 3 labs achieved a score between 76% and 90%. Table 2. Peformance of antimicrobial susceptibility testing among different labs participating in the three PT activities. Performance of Lab in providing antimicrobial results Nb of expected Number of labs Correct / Bacterial Spp. No incorrect (lab No misleading (lab AMA* to test Reported results anticipated total range) range) (%) MRSA 13 72 635/936 (67.8) 301 (1-11) 18 (0-4) VRE (U)+& B++ 8 +4 72 338/412 (82) 66 (0-8) 52 (0-15) Listeria monocytogenes 1 72 44/72 (61) 22 (0-1) 76 (0-10) Corynebacterium amycolatum 6 42 23/228 (10.1) 25 (0-5) 7 (0-5) Streptococcus agalactiae 5 42 101/190 (53.1) 49 (0 – 5) 27 (0 – 6) Klebsiella pneumoniae CRE 20 72 975/1440 (67.7) 464 (0-19) 42 (0-4) Pseudomonas aeruginosa 9 72 346/648 (53.4) 281 (1-19) 38 (0-8) Salmonella Typhi 7 42 158/266 (59.4) 74 (0 – 5) 24 (0 – 5) Enterobacter aerogenes CRE 17 42 315/646 (48.8) 246 (0 –14) 15 (0 – 2) Stenotrophomonas maltophilia 3 42 57/114 (50) 27 (0 – 3) 120 (0 – 21) 1841 Araj et al. – AMR Proficiency testing in Lebanon J Infect Dev Ctries 2021; 15(12):1838-1844. while their AMST scores showed 7%, 62% and 31%, placed in the report. In a clinical setting, this would respectively. As for the overall score, it was 5%, 55%, result in reporting inaccurate information to the treating and 40% showing no change, positive change and physician and possibly misleading patient’s negative change, respectively. management. What is also concerning is the low overall combined Discussion ID and AMST scores. These were essentially based on The results in this first nationwide PT activity in accounting for the wrong, misleading and irrelevant Lebanon, though humble, enabled us to identify gaps provided results, and indicated that 33% of the labs and explore improvement needs among the scored less than 35%, and only 10% of the labs scored participating laboratories, and their resource setting, in between 66% and 95%. Thus, this unfortunate humble the bacterial ID and AMST. Overall, the performance performance by many labs warrants long term follow- results for bacterial ID of pathogens were generally up and mentoring, by MOPH and others, to ensure higher than that of the AMST results. successful improvement of laboratory diagnostic Concerning the performance of bacterial ID results capacity. Interestingly, the impact of such an approach to the species level among Gram- positive bacteria, all was positively noticed among 62% of the 42 labs were able to identify S. aureus (100%). However, laboratories that repeated the PTs activities. Also, with it was concerning to detect variable rates (14%-93%) of such an overall modest to low performance among the missed identification to the species level among the 110 labs in this PT activity, one would wonder about other pathogens. Regarding the Gram-negative the earlier data reported in surveillance studies from bacteria, the laboratories correct identification to the Lebanon [3,4]. species level generally indicated higher rates (84%- Searching for comparable published studies about 97%) than those for Gram-positive pathogens. the PT activities in different countries of our region In regards to AMST performance, it was concerning enabled to find only one comparable study from Turkey to note many deficiencies among many labs. This was involving 118 laboratories. Similar to our study, reflected in the variable range (33%-82%, mostly less they reported that mistakes done in bacterial ID were than 75%) of labs that correctly performed relevant lower than the high error rates detected in AMST results AMST against the pathogens. Noteworthy, several labs. In Africa, successive External Quality Assessment missed specifying the resistance types for the tested (EQA) ID and AMST studies carried out in 2002 (39 species: 17% as MRSA for S. aureus, 20% as VRE for labs), 2009 (78 labs) and 2011 to 2016 (81 labs) showed E. faecium, 28% as CRE for K. pneumoniae, and in 66% comparable ID and lower AMST scores in respect to the as CRE for E. aerogenes. These results indicate the current study from Lebanon. Nevertheless, their ID need for more training so that labs can improve scores rose with continued PT performance over the reporting the resistance type of such MDR pathogens as years: 65%, 69% and 76% in 2002, 2009 and 2011 to an alert to physicians and for infection control purposes. 2016, respectively. However, their AMST scores In fact, such low results in AMST performance were not remained low (42%-54%), close to what is generated in anticipated since several educational training the current PT study [14, 15]. workshops were conducted. More stunning is the 1974 All in all, this first national PT activity in Lebanon AMST results that were interpreted incorrectly and delineated analysis errors in CMLs and pointed to the Table 3. Summary of Results for 42 Labs repeating 5 PTs. Changes in No (%) of Labs Range (%) of PT activity Repeat PT scores showing changes Change in score Identification No change 12 (29) Positive change 8 (19) 8-28 Negative change 22 (52) 8-40 AMST* No change 3 (7) Positive change 26 (62) 2-31 Negative change 13 (31) 2-34 Overall No change 2 (5) Positive change 23 (55) 2-32 Negative change 17 (40) 2-40 1842 Araj et al. – AMR Proficiency testing in Lebanon J Infect Dev Ctries 2021; 15(12):1838-1844. need for improving ID and AMST capacity to avoid Conclusions providing inaccurate results that can lead to Providing accurate and validated microbiology misdiagnosis and inappropriate treatment in patient laboratory results is critical in patient’s care specially to care. Thus, clinical laboratories should acknowledge those suffering from infectious diseases, as well as in and embrace such PT activities as an opportunity to providing surveillance results. The heterogeneity in improve the quality of their provided results as well as clinical microbiology capacity and competence levels to support antimicrobial stewardship programs to among the 110 different participating labs in these PT control resistance and share credible data on activities in Lebanon was clearly noticed. Despite international platforms [8, 16, 17]. providing didactic trainings and workshops, the low Lessons learned from this nationwide PT activities performance among many of these laboratories is pointed to several positive aspects including: 1) unfortunate, and thus necessitates long term education, Reflection of keen enthusiasm and positive feedback follow-up and mentoring to ensure successful about the educational and PT program by all the lab improvement in laboratory proficiency. Moreover, this staff who attended the diagnostic presentations, activity should be enforced as part of accreditation and workshops and discussion, especially in helping them certification as a requirement for laboratories offering streamline their work. 2) Expression of satisfaction clinical microbiology services to guarantee reliable about the provided WSs, SOPs, and other educational results reflecting on proper patients’ management and material, as well as QC bacterial strains. 3) Satisfaction safety. Finally, it should be an assumed obligation that about the discussion related to guidance for QC aspects any lab who is performing microbiological diagnosis to in reagents and tests to use for ID and AMST. 4) Benefit have a full or part time clinical microbiologist to from feedback of results so that each lab learns and oversee and assure an adequate performance of the improves from deficiencies. 5) Contentment on self- diagnostics. This is a critical issue for correct patient improvement by staff while keeping up-to-date with management, liability, surveillance, and public health diagnostic information. in regard to lab infectious diagnosis and antimicrobial On the other hand, there were different concerns susceptibility performance aspects. expressed by lab staff that included: 1) Shortages and lack of reagents pertinent to ID & AMST, especially among public/ governmental labs. 2) Lack of dedicated Acknowledgements staff assignment to clinical microbiology, covering the The authors express their thanks and gratitude to the service is a rotational part with other clinical division. assistance and support to all those contributing in making this PT activity possible: WHO country Office-Lebanon: Dr Iman 3) Shortage or absence of CML specialists in many of Shankiti, Dr Alissar Rady, and Mrs Loubna Al Batlouni, for the labs. 4) Unfortunately, some labs claimed doing the their overall logistical support and encouragements; Clinical analysis themselves while in fact they outsourced the Microbiology Laboratory, Department of Pathology and analysis to other labs. Laboratory Medicine, American University of Beirut Based on all of the above, this first-time nationwide Medical Center: Mrs Rima El Asmar and Ms Lina Itani, for PT activity in Lebanon raises a couple of their technical support; Laboratoire des Agents Pathogènes, recommendations/ suggestions that will encourage and Faculty of Pharmacy, Saint Joseph University of Beirut: Mrs assist the MOPH to implement in order to ensure release May Mallah, Dr Rindala Saliba, and Dr Rouba El Khatib, for of reliable clinical microbiology results including: 1) their technical and logistic support; Ministry of Public Introducing a PT unit as an integral part of its health Health- Preventive Medicine Department: Ms Hajar Samaha, for her logistic and administrative support; All Staff from units infra structure. 2) Enforcing PT activities on the Participating Laboratories for their diligent work. labs to be implemented in their clinical operations. 3) Implementing PT activities to account labs for their reliable, credible or deficient results as an integral part References of the accreditation or certification requirements 1. 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