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  Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 37  |  Issue : 4  |  Page : 502-508
 

Comparative evaluation of microscan walkaway 96 plus ID/AST system and mikrolatest broth microdilution kit in assessing In vitro colistin susceptibility of carbapenem-resistant clinical gram-negative bacterial isolates: Experience from a tertiary care teaching hospital in Rishikesh, Uttarakhand


1 Department of Microbiology, All India Institute of Medical Sciences, Rishikesh, Uttarakhand, India
2 Department of Microbiology, All India Institute of Medical Sciences, Rishikesh, Uttarakhand, India, IndiaIndia

Date of Submission13-Nov-2019
Date of Acceptance09-Apr-2020
Date of Web Publication18-May-2020

Correspondence Address:
Dr. Mohit Bhatia
Department of Microbiology, All India Institute of Medical Sciences, Rishikesh, Uttarakhand
IndiaIndia
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmm.IJMM_19_437

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 ~ Abstract 

Context: As reports on colistin resistance are slowly emerging from different parts of the world, it is imperative that the clinical microbiology laboratories should generate accurate in vitro colistin susceptibility results. Aim: The aim is to generate preliminary data on the diagnostic utility of MicroScan WalkAway 96 Plus Identification ID/ Antimicrobial susceptibility testing AST system in determining in vitro colistin susceptibility of carbapenem-resistant clinical Gram-negative bacterial isolates. Settings and Design: A pilot study was conducted in a tertiary care teaching hospital located in Rishikesh, Uttarakhand, between May and June 2019. Materials and Methods: Thirty-four carbapenem-resistant Escherichia coli, Pseudomonas aeruginosa and Acinetobacter spp. isolated from various non-repetitive clinical samples during the study period, were subjected to antibiotic susceptibility testing using MicroScan ID/AST system. Matrix-assisted laser desorption ionization-time-of-flight mass spectrometry was used to confirm identity of these isolates. Additional colistin susceptibility testing of all test isolates was performed using Mikrolatest minimum inhibitory concentration antibiotic susceptibility testing kit (reference method), which is based on broth micro dilution (BMD) principle. Statistical Analysis Used: Fisher's exact test. Results: 11.8% (4/34) of the test isolates (100% [2/2] Acinetobacter junii, 10% [1/10] E. coli and 14.3% [1/7] P. aeruginosa respectively) exhibited in vitro colistin resistance by BMD method. Categorical agreement between MicroScan ID/AST system and Mikrolatest kit w. r. t in vitro colistin susceptibility test results was as follows: 71.4% (Acinetobacter baumannii), 85.7% (P. aeruginosa) and 100% (A. junii, A. johnsonii, E. coli and Klebsiella pneumoniae), respectively. Two major errors (MEs) for A. baumannii and one very ME for P. aeruginosa respectively were observed. Conclusions: Data generated by this study will be of help to the clinicians who are often faced with the dilemma of treating multi drug resistant infections with limited treatment options.


Keywords: Carbapenem-resistant, colistin, Gram-negative bacteria, mikrolatest, microScan


How to cite this article:
Singh RI, Bhatia M, Anusha K R, Singh V, Omar BJ, Gupta P. Comparative evaluation of microscan walkaway 96 plus ID/AST system and mikrolatest broth microdilution kit in assessing In vitro colistin susceptibility of carbapenem-resistant clinical gram-negative bacterial isolates: Experience from a tertiary care teaching hospital in Rishikesh, Uttarakhand. Indian J Med Microbiol 2019;37:502-8

How to cite this URL:
Singh RI, Bhatia M, Anusha K R, Singh V, Omar BJ, Gupta P. Comparative evaluation of microscan walkaway 96 plus ID/AST system and mikrolatest broth microdilution kit in assessing In vitro colistin susceptibility of carbapenem-resistant clinical gram-negative bacterial isolates: Experience from a tertiary care teaching hospital in Rishikesh, Uttarakhand. Indian J Med Microbiol [serial online] 2019 [cited 2020 Jun 2];37:502-8. Available from: http://www.ijmm.org/text.asp?2019/37/4/502/284513



 ~ Introduction Top


The rapid emergence of multidrug-resistant (MDR) bacteria globally has raised an alarm amongst health-care professionals. This has happened owing to indiscriminate use of antibiotics leading to limited therapeutic options. Gram-negative bacteria are among the most commonly isolated nosocomial pathogens which are often found to be resistant to fluoroquinolones, aminoglycosides and beta-lactam antibiotics including carbapenems and monobactams. This has prompted the use of colistin in clinical practice, which belongs to polymyxin group of polypeptide antibiotics, as a valid therapeutic option. This bactericidal antibiotic has significant activity against Gram-negative bacteria as it targets lipopolysaccharides (LPS) in the outer membrane.[1]

There are sporadic reports of emergence of colistin resistance from different parts of the world thereby raising with it the specter of untreatable Gram-negative bacterial infections.[2] Although resistance to polymyxins is generally <10%, it is higher in the Mediterranean and South-East Asia (Korea and Singapore), where colistin resistance rates are continually increasing.[3] Few Indian studies have reported varied prevalence of colistin resistance ranging from 1.1% to 38.3%.[4],[5],[6],[7] Resistance to colistin is both chromosomal and plasmid mediated and is most commonly related to LPS modification via diverse routes which include the following: (i) specific modification of outer membrane porins and reductions in the overall negative charge of the LPS; (ii) overexpression of efflux pump systems; and (iii) overproduction of capsular polysaccharide.[8],[9]

Carbapenem-resistant Acinetobacter baumannii, Pseudomonas aeruginosa and Enterobacteriaceae have been enlisted as priority pathogens according to the World Health Organisation (WHO).[10] Keeping in mind the importance of colistin as the last resort in treating MDR Gram-negative bacterial infections (including those caused by aforementioned WHO priority pathogens), it is imperative that the clinical microbiology laboratories should generate accuratein vitro colistin susceptibility results. However, colistin susceptibility testing is challenging, with disc-diffusion, Epsilometer test (E-test) and agar dilution methods giving variable results.[2],[11] In March 2016, the joint Clinical and Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST) Polymyxin Breakpoints Working Group recommended broth micro dilution (BMD) method as the reference test for determining susceptibility in the form of minimum inhibitory concentration (MIC) to colistin.[12] However, this method is labor intensive as a result of which several automated bacterial ID/AST systems have been introduced in the market which offer a quick alternative to the conventional technique.

Few studies based on comparative evaluation ofin vitro colistin susceptibility results using automated bacterial ID/AST systems, E-test agar dilution and BMD methods have been carried out in different parts of the world. The results of these studies have been largely inconclusive.[13],[14],[15] An urgent product correction notice was issued by bioMerieux India Pvt. Ltd., as per which an investigational study was carried out by the company in which colistin susceptibility test results of VITEK® 2 automated bacterial ID/AST system were compared with those of agar and broth micro dilution methods respectively. This study demonstrated that VITEK® 2 had high rate of very major errors (VMEs) (colistin-resistant isolates called susceptible) when compared to both agar dilution and BMD methods.[16]

To the best of our knowledge, there is paucity of Indian data and none available from Uttarakhand region on comparative evaluation of different methods for colistin susceptibility testing. This study was planned with the aim of generating preliminary data on the diagnostic utility of MicroScan WalkAway 96 Plus ID/AST system in determiningin vitro colistin susceptibility of carbapenem-resistant clinical Gram-negative bacterial isolates. This will guide the clinicians in determining appropriate dosage of this highly toxic antibiotic for treating infections in critically ill patients.


 ~ Materials and Methods Top


A pilot study (STS-ICMR project; Reference ID: 2019-01228) was conducted in a tertiary care teaching hospital located in Rishikesh, Uttarakhand, during the months of May and June 2019 after obtaining approval from Institute Ethics Committee (Letter No. AIIMS/IEC/19/820 dated 10/05/2019). The main objectives of this study were:

  1. To determinein vitro colistin susceptibility in carbapenem-resistant clinical Gram-negative bacteria using MicroScan WalkAway 96 Plus ID/AST system (Beckman Coulter, Inc., USA) and Mikrolatest MIC antibiotic susceptibility testing kit (Transasia Bio-Medicals, Mumbai), respectively
  2. To evaluate percentage categorical agreement between the aforementioned test methods in assessing colistin susceptibility in carbapenem-resistant clinical Gram-negative bacterial isolates.


Carbapenem-resistant Gram-negative bacterial isolates (namely Acinetobacter spp., P. aeruginosa, Escherichia coli and Klebsiella pneumoniae) obtained from various nonrepetitive clinical samples such as cerebrospinal fluid, blood, pus, sputum, endotracheal secretions, urine, pleural, pericardial, ascitic and synovial fluids from patients admitted in different wards/outpatient departments of a tertiary care teaching hospital were included in the study. Gram-positive bacteria and carbapenem susceptible Gram-negative bacterial isolates were excluded from the study.

Thirty-four bacterial isolates (namely Acinetobacter spp., P. aeruginosa, E. coli and K. pneumoniae) were tested during the study. Clinical samples (as mentioned earlier) were subjected to culture as per standard guidelines.[17] Isolated bacterial colonies obtained on solid culture media were subjected to Gram staining. Species level identification of Gram-negative bacterial isolates was performed using MicroScan WalkAway 96 Plus automated ID/AST system and re-confirmed by matrix-assisted laser desorption ionization-time-of-flight mass spectrometry (MALDI-TOF MS) (Bruker Daltonik GmbH, Germany) as per manufacturer's guidelines, respectively.

Antibiotic susceptibility testing of Gram-negative bacterial isolates identified as Acinetobacter spp., P. aeruginosa, E. coli and K. pneumoniae was performed on MicroScan WalkAway 96 Plus automated ID/AST system as per manufacturer's guidelines. Additional colistin susceptibility testing of carbapenem-resistant Acinetobacter spp., P. aeruginosa, E. coli and K. pneumoniae respectively was performed using Mikrolatest MIC antibiotic susceptibility testing kit as per manufacturer's guidelines. This kit is based on BMD principle and was used to easily determine colistin MIC results for all test isolates and control strains respectively as the reference method.

Antibiotic susceptibility test results (including those of colistin) were interpreted and bacterial isolates were categorised as Susceptible (S), Intermediate (I) and Resistant (R) as per CLSI and EUCAST guidelines as applicable.[18],[19]

Discrepancies in colistin susceptibility results were categorised in the form of VMEs and major errors (MEs), respectively. VMEs were defined as bacterial isolates categorised as susceptible using MicroScan WalkAway 96 Plus automated ID/AST system and resistant by the Mikrolatest MIC antibiotic susceptibility testing kit (false susceptibility result). MEs were defined as bacterial isolates categorised as resistant using MicroScan WalkAway 96 Plus automated ID/AST system and susceptible by Mikrolatest MIC antibiotic susceptibility testing kit (false-resistant result).[15]

E. coli ATCC 25922 and P. aeruginosa ATCC 27853 were used as control strains for both MicroScan WalkAway 96 Plus automated ID/AST system and Mikrolatest MIC antibiotic susceptibility testing kit, respectively. Bruker bacterial test standard mass calibration standard showing a typical E. coli DH5 alpha peptide and protein profile and additional proteins, was used for performing quality check in MALDI-TOF MS.

Statistical analysis

Categorical variables were presented as proportions while continuous variables were presented as mean with standard deviation (SD). Comparison of categorical variables was done by Fisher's exact test. All statistical tools were two-tailed and a significant level P < 0.05 was used. All statistical tests were performed using InStat software (GraphPad Software, San Diego, CA, USA). Percentages of VMEs and MEs were calculated. Categorical agreement (percentage of isolates classified into the same category by the BMD reference method) was also calculated.


 ~ Results Top


Baseline characteristics

The study population included 25 male and 9 female patients, respectively. The mean age ± SD of these patients was 45.09 ± 17.59 years.

Bacterial isolates

During the study, 34 carbapenem-resistant Gram-negative bacteria were isolated from various non-repetitive clinical samples namely blood, urine, pus, pleural fluid, sputum, Broncho-alveolar lavage and endotracheal aspirate respectively received in microbiology department. E. coli and Acinetobacter spp. were the most common bacterial isolates. Species wise distribution of all 34 Gram-negative bacterial isolates is shown in [Figure 1]. No discrepancy in bacterial identification results between MicroScan WalkAway 96 Plus and MALDI-TOF MS was observed.
Figure 1: Species wise distribution of all 34 carbapenem resistant Gram-negative bacterial isolates

Click here to view


Antibiotic resistance pattern

The percentage antibiotic resistance pattern (excluding colistin) of all 34 bacterial isolates using MicroScan WalkAway 96 Plus automated ID/AST system is shown in [Table 1]. High resistance rates to aminoglycosides, fluoroquinolones, penicillins, β-lactam/β-lactamase inhibitor combinations, cephalosporins, carbapenems and folate pathway inhibitors respectively were observed among all test isolates.
Table 1: Percentage antibiotic resistance pattern of bacterial isolates

Click here to view


Colistin resistance

Results of colistin susceptibility test using both MicroScan WalkAway 96 Plus ID/AST system and Mikrolatest MIC antibiotic susceptibility testing kit, respectively, of all 34 bacterial isolates along with those of control strains are shown in [Table 2]. Acinetobacter spp. and P. aeruginosa test isolates were classified as colistin susceptible (MIC ≤2 μg/ml) or resistant (MIC >4 μg/ml) respectively as per CLSI 2019 guidelines. Clinical breakpoints for colistin in case of Enterobacteriaceae have not been mentioned in CLSI 2019 guidelines. Therefore, EUCAST 2019 guidelines were being referred to for determining colistin susceptibility of E. coli and K. pneumoniae test isolates (MIC ≤2 [sensitive] and >2 μg/ml [resistant]). Colistin susceptibility of E. coli ATCC 25922 (MIC: 0.25–2 μg/ml) and P. aeruginosa ATCC 27853 (MIC: 0.5–4 μg/ml) was ascertained using CLSI 2019 guidelines.
Table 2: Colistin susceptibility test results of all bacterial isolates

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[Table 3] shows colistin resistance pattern (expressed as percentage) of 34 test isolates as determined by MicroScan WalkAway 96 Plus ID/AST system and Mikrolatest MIC antibiotic susceptibility testing kit respectively along with categorical agreement between these two methods. Three errors (two MEs and one VME) and 100% categorical agreement (for E. coli, K. pneumoniae, Acinetobacter junii, Acinetobacter johnsonii) were observed while comparing colistin susceptibility test results of the aforementioned methods. The difference in proportion of test isolates reported as colistin resistant by the two methods was not found to be statistically significant (P = 1.000).
Table 3: Percentage colistin resistance pattern of 34 test isolates by MicroScan WalkAway 96 Plus ID/AST system and Mikrolatest minimum inhibitory concentration antibiotic susceptibility testing kit respectively along with categorical agreement between these two methods

Click here to view


Colistin susceptibility test results by BMD method using Mikrolatest MIC antibiotic susceptibility testing kit are summarised in [Figure 2]. 'H' wells served as growth control. Colistin concentration increased in doubling manner from wells 'G' to 'A' respectively (0.25–16 μg/ml). The first well position from bottom to top showing no growth in any form (any granulation, button or turbidity) was considered as MIC value.
Figure 2: Colistin susceptibility test results using Mikrolatest minimum inhibitory concentration antibiotic susceptibility testing kit (broth micro dilution method)

Click here to view



 ~ Discussion Top


According to the “scoping report on antimicrobial resistance in India (2017),” >70% isolates of E. coli, K. pneumoniae, A. baumannii and nearly half of all P. aeruginosa were resistant to fluoroquinolones and third-generation cephalosporins. Resistance to drug combination of piperacillin-tazobactam was found to be <35% for E. coli, P. aeruginosa and 65% for K. pneumoniae, respectively. Increasing rates of carbapenem resistance to the tune of 71% were observed in A. baumannii.[20] Antibiotic susceptibility test results observed in the present study were in line with this report as high level of resistance to different antibiotic groups (ranging from 80% to 100%) was observed among all test isolates.

11.8% (4/34) of the test isolates (100% [2/2] A. junii, 10% [1/10] E. coli and 14.3% [1/7] P. aeruginosa respectively) exhibitedin vitro colistin resistance by BMD method (Mikrolatest MIC antibiotic susceptibility testing kit). Increasing use of colistin for MDR Gram-negative bacterial infections has led to the emergence of colistin resistance in several countries worldwide which may vary between regions and over time. Despite the majority of reports presenting resistance rates under 10%, there are also some studies that report high resistance rates. These variations could exist due to differences in methodology forin vitro colistin susceptibility testing.[21] Another reason could be the phenomenon of 'Heteroresistance', which has been observed in several Gram-negative pathogens.[22],[23] It is broadly defined as the presence of an antibiotic-resistant subset of microbes within a larger population that is susceptible to the antibiotic. Uniform standards to determine heteroresistancein vitro are lacking. Heteroresistance can complicate assessment of MIC to a specific antibiotic and may promote antibiotic resistance in vivo, thereby affecting diagnostic tests and patient treatment.[24]

Categorical agreement between MicroScan WalkAway 96 Plus ID/AST system and Mikrolatest MIC antibiotic susceptibility testing kit w. r. tin vitro colistin susceptibility test results was as follows: 71.4% (A.

baumannii), 85.7% (P. aeruginosa) and 100% (A. junii, A. johnsonii, E. coli and K. pneumoniae), respectively. Total three errors (2 MEs for A. baumannii and 1 VME for P. aeruginosa respectively) were observed. Few studies have evaluated MicroScan WalkAway 96 Plus ID/AST system for determining colistin susceptibility. In a study conducted by Lee et al., three commercial colistin susceptibility testing methods (namely Vitek 2, Etest and MicroScan) were evaluated using 213 bloodstream Acinetobacter isolates identified by gene sequencing. Compared to the agar dilution reference method, excellent categorical agreements (both 99.1%) were observed using Vitek 2 and E-test, compared to 87.3% (95.7% for A. baumannii and 80.7% for non-A. baumannii isolates) using MicroScan.[13] Marlinghaus et al. conducted a study to evaluate the accuracy of antimicrobial susceptibility testing AST of colistin using MicroScan Walkaway system. The authors tested a total of 327 carbapenemase-producing Enterobacteriaceae isolates, 107 and 220 of which were colistin resistant and susceptible respectively. The system failed to identify 3 colistin-resistant isolates and showed ME and VME rates of 0.9% and 2.8%, respectively.[25] The accuracy of three commercialised BMD panels (Sensititre [ThermoFisher Diagnostics], UMIC [Biocentric] and MicroScan [Beckman Coulter]) to determine colistin susceptibility of 185 isolates of Gram-negative bacilli (133 colistin resistant and 52 colistin susceptible) was evaluated by Jayol et al. Manual BMD was used as the reference method in this study. A high rate of MEs (26.9%) was observed with the MicroScan system due to an overestimation of the MICs for the non-fermenting Gram-negative bacilli.[15] In a recent study conducted by Pfennigwerth et al. on 325 carbapenemase-producing Enterobacteraceae spp., poor performance of MicroScan Walkaway system was observed with 16 MEs and 13 VMEs.[26]

Two A. junii and one A. johnsonii isolates were obtained from pus and sputum samples respectively in the present study. Although known to be present in the environment, these species have been associated with various nosocomial infections.[27],[28],[29]

A major drawback of the present study was that E. coli NCTC 13846 (mcr-1 positive) strain could not be tested owing to nonavailability. Plasmid mediated low levels of colistin resistance through transferable mcr genes has been reported from different parts of the world.[30],[31]In lieu of this background, EUCAST has advised to include colistin resistant E. coli NCTC 13846 (mcr-1 positive), which has MIC target value between 4 and 8 μg/ml, along with E. coli ATCC 25922 and P. aeruginosa ATCC 27853 respectively as quality control strains for BMD method.[12],[19] Some of the other lacunae of this study were small sample size and inability to assess reproducibility of Mikrolatest colistin kit results owing to logistical problems.


 ~ Conclusion Top


Although only 34 bacterial isolates were tested, the data generated by this study will be of help to the clinicians who are often faced with the dilemma of treating MDR (including carbapenem resistant) Gram-negative bacterial infections with limited therapeutic options at their disposal. We intend to conduct similar studies in future, using additionalin vitro colistin susceptibility testing platforms and greater number of carbapenem-resistant Gram-negative bacterial isolates. More number of such studies should also be conducted from different parts of the country to gain a better understanding of the subject under consideration.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

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    Tables

  [Table 1], [Table 2], [Table 3]



 

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