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Year : 2012  |  Volume : 55  |  Issue : 3  |  Page : 361-364
Detection of resistance to linezolid in Staphylococcus aureus infecting orthopedic patients

1 Department of Microbiology, RTM Nagpur University, LIT Campus, Nagpur; Department of Microbiology S. P. College, Chandrapur, India
2 Department of Microbiology, Sevadal Mahila Mahavidyalaya, Nagpur, India
3 Department of Microbiology, RTM Nagpur University, LIT Campus, Nagpur, India

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Date of Web Publication29-Sep-2012


Context: In today's medical scenario, the human race is battling the most intelligent enemy who has unending alternatives to combat with the potent elements they have produced against it. Aim: To study the resistance to linezolid among Staphylococcus aureus isolated from pus samples of orthopedic patients. Settings and Design: Pus samples were collected from dirty wounds of orthopedic patients undergoing long antimicrobial treatment programs. The sampling period was from July 2010 to June 2011. The samples were collected from different orthopedic hospitals of Nagpur (central India) representing a mixed sample of patients. Materials and Methods: One hundred pus samples were screened for S. aureus, by growth on mannitol salt agar (MSA), Baird-Parker agar (BPA), deoxyribonuclease test, tube coagulase test, and HiStaph latex agglutination test. Fifty-one S. aureus isolates were obtained which were further subjected to antimicrobial susceptibility testing by Kirby-Bauer disc diffusion method (DDM). Minimal inhibitory concentrations (MICs) were determined by an automated system, the VITEK 2 system. Also, Ezy MIC strip method was carried out in accordance with Clinical and Laboratory Standards Institute (CLSI) guidelines. Results and Conclusion: Twelve linezolid-resistant S. aureus (LRSA) isolates were recovered from 51 S. aureus cultures tested for susceptibility to linezolid using the DDM, VITEK 2 system, and Ezy MIC strip method. The emergence of resistance suggests nosocomial spread and abuse of antibiotic.

Keywords: Etest, linezolid-resistant S. aureus, minimal inhibitory concentrations, orthopedic

How to cite this article:
Thool VU, Bhoosreddy GL, Wadher BJ. Detection of resistance to linezolid in Staphylococcus aureus infecting orthopedic patients. Indian J Pathol Microbiol 2012;55:361-4

How to cite this URL:
Thool VU, Bhoosreddy GL, Wadher BJ. Detection of resistance to linezolid in Staphylococcus aureus infecting orthopedic patients. Indian J Pathol Microbiol [serial online] 2012 [cited 2020 Jul 10];55:361-4. Available from: http://www.ijpmonline.org/text.asp?2012/55/3/361/101745

   Introduction Top

Nowadays, orthopedic departments are facing a grave problem due to staphylococcal infections. Staphylococcus aureus, a well-armed pathogen, is not only prevalent in hospitals but is also causing a great setback in outpatient departments. Since the discovery of linezolid in 2000, it has become the antibiotic favored by orthopedic doctors for many reasons. [1] The most important of these is that it heals faster and reduces the stay of a patient in the hospital by almost three weeks. It has replaced antibiotics such as methicillin and vancomycin as Gram-positive bacteria develops resistance increasingly to them. [2]


One hundred nonrepetitive pus samples were taken from surgical site infections of patients from different dressing rooms of outpatient departments of orthopedic hospitals in Nagpur (central India). The wounds were in the dirty wound category with deep-seated infection. The dressing rooms were overcrowded with chances of cross infections. Almost 70% of the patients had a surgical implant and were on antibiotic treatment for more than three months. Collection of pus samples was done within a one-year period from July 2010 to June 2011.

   Material and Methods Top

Pus samples were collected from dirty wounds on transport media swabs and brought to the microbiology laboratory immediately. On receipt, the swabs were inoculated with brain-heart infusion broth and incubated for 24 hours. The broth culture was then subcultured in mannitol salt agar (MSA) and Baird-Parker agar (BPA). Colonies were picked from BPA plates to study colony morphology and gram staining. Coagulase test, deoxyribonuclease test, and HiStaph Latex test kit were used for the identification of S. aureus from colonies obtained on MSA and BPA. Quality control organisms used throughout the study were S. aureus ATCC 25923 and ATCC 29213.

Antibiotic Susceptibility Testing

AST was done for each S. aureus isolate by the Kirby-Bauer disc diffusion method (DDM) [3],[4] against a panel of comparator antibiotics such as vancomycin (30 mcg), tobramycin (10 mcg), clindamycin (2 mcg), teicoplanin (30 mcg), and linezolid (30 mcg). Antimicrobial susceptibility testing was performed on Mueller-Hinton agar (MHA) plates. Inoculums were prepared by picking four to five colonies from overnight cultures and inoculating in 5 ml tryptone soya broth and incubating at 35΀C until turbid to 0.5 McFarland standards. MHA plates were overlaid with the inoculums of the S. aureus isolates. Zone diameters were measured at 24 hours in transmitted light for linezolid, which reduces the very major error rate to 20.0% [5] , following clinical and laboratory standards institute (CLSI) criteria. [4],[6] Methicillin resistance was evaluated by the Kirby-Bauer DDM with 4% NaCl in MHA and by using methicillin (5 mcg) discs. The isolates were considered linezolid resistant if the zone of inhibition was 21 mm or less and methicillin resistant if the zone of inhibition was 9 mm or less.

VITEK 2 system

For the determination of minimum inhibitory concentration (MIC) by VITEK 2 system, [5] the test organisms were grown on trypticase soy agar for 18 hours and thereafter suspended in sterilized physiological saline to 0.5 McFarland standards. The bacterial suspension was filled in the antimicrobial susceptibility testing card, which was then inserted in the incubator-reader of the VITEK 2 system (software version Biotek2 Compact 15) and the results expressed as MIC values in μg/mL.

Ezy MIC Strip Test

The MICs of all the 51 S. aureus isolates were subjected to Ezy MIC testing for linezolid. All MICs were determined according to the instructions given by the manufacturer (Hi Media Laboratories Pvt Ltd, India). The linezolid Etest strip was placed on an inoculated MHA agar plate and the plate was incubated at 35΀C for 24 hours. For interpretation of results, the plates were held up to a light source and observed in transmitted light. [5] The zone margin was considered as the area showing no obvious visible growth of tiny colonies that could be detected with the unaided eye. The faint growth of tiny colonies at the edge of the zone of inhibition was ignored. Isolates were categorized as susceptible or resistant to linezolid according to the breakpoints given by CLSI and EUCAST (EUCAST: European Union Committee on Antibiotic Susceptibility Testing). An isolate was classified as susceptible to linezolid if the MIC was ≤4 μg/mL and resistant if MIC was more than ≥8 μg/mL.

   Results Top

A total of 51 S. aureus were isolated from 100 pus samples on the basis of DNase test, tube coagulase test, and HiStaph latex test kit. The antibiotic resistance pattern of S. aureus was found to be highly variable and consistently gave the same results. Of the 51 S. aureus isolates, 12 (23.52%) linezolid-resistant S. aureus (LRSA) isolates were detected as per Kirby-Bauer DDM. [3] Of these 12 LRSA, seven (58.33%) were methicillin resistant (LR-MRSA). [Table 1] Further, all the S. aureus isolates were subjected to Ezy MIC strip method for MIC determination. [5] Twelve LRSA were detected as per Ezy MIC strip method. [Table 2] All the LRSA uniformly showed no zone around the Ezy MIC strip. The MICs at which 50 and 90% of isolates were inhibited obtained with the Ezy MIC test system for linezolid-sensitive isolates were 1.5 and 3.0 μg/mL, respectively. Linezolid inhibited all isolates in the range of 0.5-4.0 μg/mL [Table 3]. MICs were calculated for all the 12 LRSA isolates with VITEK 2 system which showed an MIC of ≥8 μg/mL.
Table 1: Antibiogram of linezolid-resistant Staphylococcus aureus isolates (n=12)

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Table 2: Comparison of diff erent methods for linezolid susceptibility measurements as per CLSI

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Table 3: Minimum inhibitory concentration of linezolid against linezolidsensitive S. aureus isolates (n=39)

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   Discussion Top

Linezolid is the first representative of a new synthetic class of antibacterial oxazolidinones discovered 30 years after the discovery of trimethoprim in the 1970s. It is bacteriostatic and has uniform activity against both methicillin-sensitive S. aureus (MSSA) and MRSA, and inhibits practically all strains at a concentration of 4 mg/L or less. The mode of action of linezolid is different from that of other protein synthetic inhibitors which prevent protein synthesis at the chain elongation step. However, linezolid prevents the 50S subunit of prokaryotic ribosome to complex with the 30S initiation complex and inhibits bacterial protein synthesis at the initiation step of protein biosynthesis. [7] Studies have suggested that the expression of virulence factors in toxin-producing S. aureus is especially sensitive to the inhibition of protein synthesis by linezolid. [8],[9] With this novel mechanism of action by linezolid, it was thought that bacteria would never develop resistance to linezolid. Linezolid was extensively used in critical care facilities because of its broad-spectrum activity, short-term safety profile, and effectiveness against MRSA with negligible side effects. Because of the quantum leap in effectiveness as compared to other antimicrobials, the rampant use of this drug in orthopedic units resulted in selective pressure that eventually lead to the emergence of resistant strains of S. aureus . Many mechanisms of linezolid resistance have been attributed to S. aureus. [10] Resistance to linezolid is recognized to be associated with mutations in the central loop of domain V of 23S rRNA of the 50S ribosomal subunit [11] and these changes alter the linezolid-binding sites of the bacteria. It has also been observed that resistance may be acquired through methylation of 23S rRNA-mediated methyltransferase designated by Cfr. S. aureus has 4-7 copies of the gene-specifying 23S rRNA and mutations in rplD and rplC genes that encode the 50S ribosomal proteins L4 and L3, respectively. The number of genes may depend on the duration of exposure to linezolid. [12]

Researchers assumed that resistance to linezolid would never develop. However, earlier at the start of the decade, Rajaduraipandi [13] reported 2.4% of LRSA in South India by Kirby-Bauer DDM. Shortly thereafter, Endimiani [14] and co-workers from Cleveland, Ohio, reported their first LRSA in 2004, with a total of 11 LRSA-infected cystic fibrosis patients being identified by 2009. Linezolid treatment started in Japan in 2006 and by 2008, 11 patients were detected positive for LR-MRSA. [15] During the same period, the first ever outbreak from a teaching hospital in Madrid, Spain documented 12 LRSA patients during a short span of approximately a three-month period from April 13 to June 26, 2008. [16] A worldwide program, the Zyvox Annual Appraisal of Potency and Spectrum (ZAAPS) (2007) for linezolid resistance, revealed the overall resistance to linezolid in 23 countries to be 0.03%. [17] Similarly, 0.34% LRSA was also reported in the LEADER 2009 programme that monitors and tracks linezolid resistance in the United States. [18] Reduction of the use of linezolid and implementation of measures to control infection resulted in the termination of outbreak in most of the cases. Considering the magnitude of the problem, we performed this study for the assessment of the current situation of resistance to linezolid in orthopedic units in the central part of India. To the best of our knowledge, this is the first report of LRSA emergence from this part of the world.

In our study, 51 S. aureus isolates were collected from 100 pus samples, from which 12 LRSA were detected. The testing of resistance to linezolid against staphylococci is a growing challenge for antimicrobial testing methods as the strains not susceptible to linezolid are difficult to detect with many of the recent susceptibility-testing methods. [5]

The only susceptibility breakpoints defined for disk diffusion is ≥21 mm and for MIC testing is ≤4 μg/mL provided by the CLSI for staphylococci because of the lack of linezolid-resistant strains when the breakpoints were developed. This breakpoint is also adopted by the British Society for Antimicrobial Chemotherapy (BSAC). EUCAST have susceptible and resistant values of ≤4 μg/ mL and >8 μg/mL, respectively. Some regulatory authorities recommend a breakpoint of 2 μg/mL, whereas some centers which routinely find MIC values of S. aureus recommend an MIC of 4 μg/mL. MICs of linezolid fluctuate slightly with the test method and significance is ascribed to thin hazes of bacterial endurance. Numerous in vitro studies have shown that the MICs of linezolid for staphylococci is in the range of 0.5 and 4 mg/L, with higher values recorded only for a few mutants selected during therapy. [19],[20],[21]

During the routine laboratory screening of LRSA, some of the isolates were lost due to poor sensitivity. MIC using the VITEK 2 system reported an MIC value of ≥8 μg/mL uniformly for all the isolates. The MICs of linezolid against S. aureus revealed a rise in the resistance. Antimicrobial susceptibility testing of all the 51 S. aureus isolates identified 12 LRSA by DDM. Nine S. aureus isolates produced no zone around the disc whereas three isolates gave a zone of 8, 8, and 9 mm.

As linezolid resistance is attributed to many factors, it requires a battery of tests. All the 12 LRSA isolates were confirmed as resistant by the automated VITEK 2 system. Moreover, the Ezy MIC test method was applied for all the S. aureus isolates. This method selectively displayed no zone (>256 μg/mL) for all the 12 LRSA isolates detected by DDM and VITEK 2 system. These results are contradictory to the results given by a study in which the potency of linezolid by broth microdilution method for MIC testing against staphylococcal isolates showed 100% susceptibility. [22] Elevated linezolid resistance with MIC values of 16, 32, or 64 μg/mL was correlated with the presence and severity of the L3 mutation. [23] The MIC range in our study was 0.5-4 μg/ mL. [Table 3] The MIC 50 value was 1.5, that is, within the range of 0.5-4 μg/mL indicating excellent activity. [22],[24] The Etest method is a reliable method to determine MIC value and many co-workers have adopted this method. [24],[25],[26],[27] There is confusion regarding the detection of MIC values for linezolid. The value varies depending on the method used, media used, and settings undertaken. [21],[28] The reading of MIC of linezolid is important as staphylococci trail out over one or two dilutions. [28] Another important factor is the media used to determine MICs; MIC for Staphylococcus gives an MIC of 4 μg/mL with micro broth dilution method but an MIC of 2 μg/ mL with MHA and Iso-Sensitest agar. Moreover, Johnson and co- workers found similar MICs for all members of a species. [28] Gemmell [28] found that MICs by Etest were one dilution below than those by classical methods. [25] On the contrary, Arias et al.[28] have not supported the Etest method and DDM as it is problematic to detect resistance mediated by the cfr gene by these methods. [29]

The emergence of linezolid resistance in orthopedic patients has important implications for the use of linezolid as a therapeutic agent. Twelve (23.52%) LRSA isolates and seven (58.33%) LR-MRSA were recorded in our study in contrast to studies where higher susceptibility rates to linezolid were observed among MRSA infections. [26],[27] The significant observation of this study was that all the 12 LRSA were multidrug-resistant strains. This is in contrast to many focused or multicenter studies in which linezolid has proven to be a valuable therapeutic option. [24]

This is an alarming observation and no precise reason could be attributed to this noticeable increase in linezolid resistance because of inability to access the data of patients and keep track of medical records due to issues of privacy. Prescribing antibiotics with a different mode of action, effective surveillance, rational use of antibiotics, and appropriateness in antimicrobial therapy may reduce the increasing selection pressure for resistance to linezolid. Our study is an attempt to enable epidemiologists to understand the increasing incidence of LRSA isolates in this part of India. In the future, new oxazolidinones are welcome as it is possible to alter the structure of the oxazolidinones so as to increase activity against different pathogens, but due to the changing role of pharmaceutical industries rational use of antibiotics is the requirement of time.

   Acknowledgment Top

The authors acknowledge the University Grants Commission, Pune, India, for providing the contingency grant under the Faculty Improvement Programme Scheme, which was of help in their research work. They also acknowledge Dr. Yagnesh Thakkar (Vishakha Clinical Microbiology Laboratory, Nagpur, India), who provided valuable inputs for this study.

   References Top

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6.Clinical and Laboratory Standards Institute. M7-A7 Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard-seventh edition. Wayne, PA: Clinical and Laboratory Standards Institute; 2006.  Back to cited text no. 6
7.Swaney SM, Aoki H, Ganoza MC, Shinabarger DL. The oxazolidinone linezolid inhibits initiation of protein synthesis in bacteria. Antimicrob Agents Chemother 1998;42:3251-5.  Back to cited text no. 7
8.Bernardo K, Pakulat N, Fleer S, Schnaith A, Utermöhlen O, Krut O, et al. Subinhibitory concentrations of linezolid reduce Staphylococcus aureus virulence factor expression. Antimicrob Agents Chemother 2004;48:546-55.  Back to cited text no. 8
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11.Swaney SM, Shinabarger DL, Schaadt RD, Bock JH, Slightom JL, Zurenko GE. Oxazolidinone resistance is associated with a mutation in the peptidyl transferase region of 23S rRNA. In Abstracts of the Thirty Eighth San Diego, CA, USA: Interscience Conference on Antimicrobial Agents and Chemotherapy; 1998. Abstract C-104, p. 98. American Society for Microbiology, Washington, DC, USA.  Back to cited text no. 11
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14.Endimiani A, Blackford M, Dasenbrook EC, Reed MD, Bajaksouszian A, Hujer AM, et al. Emergence of Linezolid-Resistant Staphylococcus aureus after Prolonged Treatment of Cystic Fibrosis Patientsin Cleveland, Ohio. Antimicrob Agents Chemother 2011;55:1684-92.  Back to cited text no. 14
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17.Jones RN, Kohno S, Ono Y, Ross JE, Yanagihara K. ZAAPS International Surveillance Program (2007) for Linezolid resistance: Results from 5591 Gram-positive clinical isolates in 23 countries. Diagn Microbiol Infect Dis 2009;64:191-201.  Back to cited text no. 17
18.Farell DJ, Mendes RE, Ross JE, Sader HS, Jones RN. LEADER Program Results for 2009: An Activity and Spectrum Analysis of Linezolid Using 6,414 Clinical Isolates from 56 Medical Centers in the United States. Antimicrob Agents Chemother 2011;55:3684-90.  Back to cited text no. 18
19.Henwood CJ, Livermore DM, Johnson AP, James D, Warner M, Gardiner A. Susceptibility of Gram-positive cocci in 25 UK hospitals to linezolid and other antimicrobial agents. J Antimicrob Chemother 2000;46:931-40.  Back to cited text no. 19
20.Zurenko GE, Yagi BH, Schaadt RD, Allison JW, Kilburn JO, Glickman SE, et al. In vitro activities of U-100592 and U-100766, novel oxazolidinone antibacterial agents. Antimicrob Agents Chemother 1996;40:839-45.  Back to cited text no. 20
21.Wise R, Andrews JM, Boswell FJ, Ashby JP. The in-vitro activity of linezolid (U-100766) and tentative breakpoints. J Antimicrob Chemother 1998;42:721-8.  Back to cited text no. 21
22.Anderegg TR, Biedenbach DJ, Jones RN. Recent In Vitro Evaluation of AZD2563, a Novel Oxazolidinone, against 603 Staphylococcal Isolates. Antimicrob Agents Chemother 2002;46:2662-4.  Back to cited text no. 22
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24.Bell JM, Turnidge JD, Ballow CH, Jones RN; ZAPS Regional Participants. Multicentre evaluation of the in vitro activity of linezolid in the Western Pacific. J Antimicrob Chemother 2003;51:339-45.  Back to cited text no. 24
25.Gemmell CG. Susceptibility of a variety of clinical isolates to linezolid: A European inter-country comparison. J Antimicrob Chemother 2001;48:47-52.  Back to cited text no. 25
26.Ranjan KP, Arora DR, Ranjan N. An approach to Linezolid and vancomycin against Methicillin resistant Staphylococcus Aureus. Webmed Central MICROBIOLOGY 2010;1:WMCOO590.  Back to cited text no. 26
27.Onur K, Fusun ZA, Esra NT. In Vitro Activities of Linezolid and Tigecycline Against Methicillin-Resistant Staphylococcus Aureus Strains. Microb Drug Resist 2008;14(Suppl2):151-3.   Back to cited text no. 27
28.Johnson AP, Warner M, Livermore DM. Activity of linezolid against multi-resistant Gram-positive bacteria from diverse hospitals in the United Kingdom. J Antimicrob Chemother 2000;45:225-30.  Back to cited text no. 28
29.Arias CA, Vallejo M, Reyes J, Panesso D, Moreno J, Castaneda E, et al. Clinical and microbiological aspects of linezolid resistance mediated by the cfr gene encoding a 23S rRNA methyltransferase. J Clin Microbiol 2008;46:892-6.  Back to cited text no. 29

Correspondence Address:
Vaishali U Thool
Department of Microbiology, RTM Nagpur University, LIT Campus, Nagpur
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0377-4929.101745

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