Int J Biol Med Res.

2024; 15(1): 7718-7723

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Original article
Comparison of Susceptibility Testing Methods for Determining Methicillin and
Linezolid Resistance with mecA and cfr Gene Prevalence Among Coagulase-Negative
Staphylococci – A Prospective Study from South Delhi
D Sharma a, N Haque b, A Das a, A Lachyan b*
a
Department of Microbiology, Hamdard Institute of Medical Science and Research (HIMSR) and HAHC hospital, Jamia Hamdard, New Delhi - 110062, India.
b
Apex Regional STD Centre, VMMC & Safdarjung Hospital, New Delhi- 110029, India.

ARTICLE INFO ABSTRACT

Keywords: Aims- This study accentuates surging methicillin and linezolid resistance among Coagulase Negative
Cefoxitin Resistance Staphylococcus (CoNS), correlating them with mec A and cfr gene presence respectively and
cfr focussing on a comparative analysis of various Antimicrobial Susceptibility tests (AST).Methods-
CoNS This study was conducted at Department of Microbiology, HIMSR & HAHC hospital, Delhi from May
mecA
2020 –May 2021. The clinical samples from all age groups were cultured on appropriate culture
Methicillin resistance
media and the isolates were identified as CoNS as per standard norms, characterized on the basis of
Nosocomial infection
PBP Novobiocin disc test. AST was performed on the isolates by automated method- VITEK-2, manual
method – disc-diffusion method for cefoxitin and linezolid and by microbroth dilution for oxacillin.
Additionally, status of mecA gene and cfr gene was determined by PCR.Results- Total 2150 clinical
samples were collected of which 380 isolated tested positive for Staphylococcus. CoNS constituted
36.8% of these isolates. About 42.14% of CoNS isolates were from males and 57.85% were from
females. Inpatient and Outpatient department contributed to 60% and 40% of the isolates
respectively. Blood was the most frequent sample obtained (49%), followed by urine and pus
(22.1%). Cefoxitin resistance was reported to be 87.14 % and 72.14% respectively by Kirby-Bauer
method and VITEK 2. Oxacillin resistance was 80.71% by both Kirby-Bauer and microbroth dilution
method and 80% by VITEK-2. However, mecA was only present in 62.85% of the total isolates.
Linezolid resistance was 2.85 % and 2.14 % respectively by Kirby-Bauer and VITEK-2 methods.
None of the isolates harboured cfr gene.Discussion- Cefoxitin proved as a better marker of mec A
gene in contrast to oxacillin. The cefoxitin Disc-diffusion method is considered a better predictor for
the detection of heterogeneous methicillin resistance. Considering the fact that methicillin
resistance has gravely escalated in CoNS, the need for new treatment options is now a necessity.
c Copyright 2023 BioMedSciDirect Publications IJBMR -ISSN: 0976:6685. All rights reserved.

Introduction
Coagulase Negative Staphylococci (CoNS) dwell as a major skin
commensal, associated as a common contaminant in clinical samples.
They have gained significance in hospital-acquired infections,
particularly among immunosuppressed patients undergoing
invasive procedures, leading to conditions such as bacteremia,
endocarditis, surgical site infections, and urinary tract infections [1].
The ability to form a thick, multi-layered biofilm matrix begets
colonization of medical devices such as catheters, CNS shunts, others
and colonization of biotic surfaces such as mucous membrane is the
key to endogenous infections. Biofilm forming nosocomial infections
are challenging to eradicate due to pronounced resistance
towards antimicrobials. Community-acquired CoNS infections
tend to be less resistant to antibiotics [2].
In recent decades, the effectiveness of bactericidal lactams,
once the primary weapons against CoNS infections, have now
blunted progressively. CoNS have been reported to show a
continuous loss of susceptibility towards most of the available
antibiotics. In Staphylococcus, including CoNS, the expression of a
mutated penicillin-binding protein (PBP), designated as PBP2a,
encoded by mecA gene, carried on genetic element designated
SCCmec, induces complete β - lactam resistance (to penicillins,
many cephalosporins, and carbapenems).

Methicillin was the predominant penicillin used for treatment

* Corresponding Author : Dr.Abhishek.S.Lachyan
c Copyright 2023 BioMedSciDirect Publications. All rights reserved.
in earlier times, therefore the term “methicillin resistance” runs as
a general indicator of β-lactam resistance. The mec gene complex
comprises the mecA gene itself and its regulatory genes in addition
to a repressor- mecI and mecR1 (a sensor inducer), as well as an
insertion sequence [3].
 D Sharma et al. Int J Biol Med Res. 2024; 15(1): 7718-7723

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Linezolid serves as an alternate for methicillin resistant CoNS MATERIALS AND METHOD
and is active against the majority of clinically relevant Gram-
positive cocci, including methicillin-resistant staphylococci, This prospective study was carried out at Department of
vancomycin-resistant enterococci and penicillin-resistant Microbiology, Hamdard Institute of Medical Science Research &
streptococci [4,5]. Although, linezolid resistance is still relatively Hakeem Abdul Hameed Centenary Hospital, Jamia Hamdard, New
rare, but concerns are rising. Various reasons are attributed for Delhi from May 2020 to May 2021 following the approval from
linezolid resistance- cfr (florfenicol and chloramphenicol Institutional Ethics Committee. Clinical samples collected from
resistance) mediated resistance, inducing enzyme mediated (rRNA both inpatient and outpatient department were cultured onto 5%
methylase) mutation in 23S rRNA. The cfr gene encoding the rRNA sheep blood agar media, afterwards the plates were incubated for
methylase, usually plasmid borne, encodes resistance to five classes 18-24 hours at 370 C. All kinds of samples were included
of antimicrobial agents, i.e., phenicols, lincosamides, irrespective of age and sex.
oxazolidinones, pleuromutilins, and streptogramin A. Due to its
Isolates were identified on the criteria of colony characteristics
high horizontal transfer capability, cfr mediated resistance is of
on blood agar plate as per standard norms and a Gram-smear
serious concern [6].
illustrating violet-coloured irregular clusters of cocci and certain
The current study was conducted to determine the rates of biochemical tests. Staphylococcus isolates belonging to Coagulase
methicillin and linezolid resistance among CoNS by comparing Negative Staphylococcus (CoNS) group were confirmed on the basis
various Antimicrobial Susceptibility Testing (AST) methods and of a positive catalase and negative slide and tube coagulase test. To
examining the prevalence of the mecA and cfr genes. This study also further classify CoNS, a novobiocin susceptibility test by disc
sought to identify which phenotypic AST method is more reliable in diffusion method (30 µg) was additionally done in accordance with
detecting the presence of these genes. With the majority of clinically standard norms [7].
recovered isolates being multi-drug resistant, therapeutic options
Antibiotic Susceptibility Test was performed on all the 140
for treating CoNS are limited. Tracking resistant strains, controlling
isolates by various methods. Automated method was carried out by
hospital acquired infections, and administering appropriate drugs,
VITEK-2 from bioMérieux using GP-628 card, for the following
rather than irrational use of antibiotics, are essential in combating
groups of antibiotics: Cefoxitin, Benzylpenicillin, Oxacillin, High
the growing rates of infections and antimicrobial resistance
level gentamicin, Ciprofloxacin, Levofloxacin, Clindamycin,
Linezolid serves as an alternate for methicillin resistant CoNS Linezolid, Daptomycin, Teicoplanin, Vancomycin, Tetracycline,
and is active against the majority of clinically relevant Gram- Tigecycline, Nitrofurantoin, Rifampicin, Trimethoprim.
positive cocci, including methicillin-resistant staphylococci,
vancomycin-resistant enterococci and penicillin-resistant The sensitivity towards Oxacillin was also examined by micro
streptococci [4,5]. Although, linezolid resistance is still relatively broth dilution method on a 96 - well round bottom plate using
rare, but concerns are rising. Various reasons are attributed for oxacillin sodium salt monohydrate procured from TCI chemicals to
linezolid resistance- cfr (florfenicol and chloramphenicol determine Minimum Inhibitory Concentration (MIC). Tryptic soy
resistance) mediated resistance, inducing enzyme mediated (rRNA broth was used as diluent for concentrations ranging from
methylase) mutation in 23S rRNA. The cfr gene encoding the rRNA 128mg/L to 0.125mg/L.
methylase, usually plasmid borne, encodes resistance to five classes
Disc diffusion test on Muller Hilton agar was done by Kirby-
of antimicrobial agents, i.e., phenicols, lincosamides,
Bauer / Disc-diffusion method for oxacillin (1 µg), cefoxitin (30 µg)
oxazolidinones, pleuromutilins, and streptogramin A. Due to its
and linezolid disc (30 µg) obtained from Hi-media, and zones of
high horizontal transfer capability, cfr mediated resistance is of
inhibition were noted. The results were interpreted as per the
serious concern [6].
Clinical Laboratory Standard Institute (CLSI) guidelines 2020 [8].
The current study was conducted to determine the rates of
methicillin and linezolid resistance among CoNS by comparing
various Antimicrobial Susceptibility Testing (AST) methods and
examining the prevalence of the mecA and cfr genes. This study also Kirby
sought to identify which phenotypic AST method is more reliable in
detecting the presence of these genes. With the majority of clinically
recovered isolates being multi-drug resistant, therapeutic options
for treating CoNS are limited. Tracking resistant strains, controlling
hospital acquired infections, and administering appropriate drugs,
rather than irrational use of antibiotics, are essential in combating
the growing rates of infections and antimicrobial resistance
sevoflurane.
 D Sharma et al. Int J Biol Med Res. 2024; 15(1): 7718-7723

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Oxacillin, Cefoxitin, Linezolid,
Benzylpenicillin,High level gentamicin,
VITEK-2
Ciprofloxacin, Levofloxacin,Clindamycin,
D a p t o m y c i n , Te i c o p l a n i n ,
Vancomycin,Tetracycline, Tigecycline,
Nitrofurantoin, Rifampicin,
Trimethoprim
Various techniques of AST in CoNS isolates.
To detect the mecA and cfr genes, DNA was isolated from freshly
sub-cultured isolates (cultured for up to 24 hours) using the heat
lysis method [9]. Polymerase chain reaction (PCR) was performed
on all 140 strains to identify the presence of mecA and cfr genes on
Applied biosystem 2720 thermal cycler, using primer sequences
obtained from Elango Genetics Pvt. Ltd., previously employed in
other studies (Table 1) [10,11].
The reaction mixture was prepared as per manufacturer's
protocol (Hi- media). The amplified products were run on 1%
agarose gel along a 1000 bp ladder from simply biologics and the
bands for the appropriate size were visualized using Gel- Document
imaging system.
Out of the 140 isolates tested for mecA, 88 isolates were found to
harbor the mecA gene (as seen in the gel image - Figure 7). Among
these 88 isolates, nearly 60.2% had MIC values of 1 mg/L, 13.6%
exhibited an MIC of 0.5 mg/L, 7.95% had 2 mg/L, 11.3% had 4 mg/L,
and 4.45% isolates had MIC of 16 mg/L or above (as detailed in
Table 2).
The pattern of susceptibility by automated method
demonstrated 100% sensitivity of CoNS isolates towards
Vancomycin, Tigecycline and Daptomycin followed by Linezolid
(97.9%), Teicoplanin (97.1%), Gentamycin, Rifampicin,
Nitrofurantoin each (90%), Tetracycline (83.4%), Ciprofloxacin
(63.4%), Levofloxacin (60%), and Trimethoprim (53.4%).
Clindamycin sensitivity was accounted by 50% of the isolates and
Erythromycin sensitivity by 46.7% of the isolates. Minimal number
of isolates were sensitive against Oxacillin (20%), Cefoxitin (12.9%)
and Benzylpenicillin being the least active antibiotic against CoNS
at 10% sensitivity rate (Table – 3).
Cefoxitin resistance was reported to be 87.14 % and 72.14%
respectively by Kirby-Bauer method and by VITEK-2 (Figure 3).
Resistance towards linezolid was comparable by both manual
(Kirby Bauer) and automated method (VITEK-2) accounting to
2.1% and 2.8% resistance respectively (Figure 4). None of the
isolates harboured cfr gene (Figure 5).

RESULTS Table 1 – Primer sequences for mecA and cfr gene used in PCR.

A total of 2150 clinical samples were collected from males and

females of all age groups during the study. Among these samples,
380 Staphylococcus isolates were reported. CoNS constituted about
36.8% (n=140) of these isolates. Male demographic pool
constituted about 42.14% of CoNS isolates whereas 57.85% were
from females. Around 60% of the positive CoNS isolates were
recovered from Inpatient Department while Outpatient Table 2 - MIC of Oxacillin in correlation with mecA gene in CoNS
department contributed to only 40% of the isolates. Among the isolates.
samples, blood cultures were primarily attributed to newborns in
the Inpatient Department. Blood was the most frequently collected
sample, accounting for 49% of the total, followed by urine and pus,
which made up 22.1% of the samples. Additionally, a screw
(orthopedic implant) was found to be positive for CoNS (Figure 1).

While speciating the CoNS isolates nearly 72.3% of CoNS

isolates were reported to be of Staphylococcus epidermidis group
(more than 16mm diameter of zone of inhibition) whereas 27.14%
were resistant.

Among the 140 isolates tested for oxacillin Minimum Inhibitory

Concentration (MIC) using the microbroth dilution method, 80.7%
(n=113) were interpreted as oxacillin-resistant (MIC ≥ 0.5 mg/L),
and 19.3% were sensitive (MIC ≤ 0.25 mg/L).

The results of oxacillin MIC were consistent with those obtained

using the VITEK 2 automated method and the disc diffusion results
(as shown in Figure 3).
 D Sharma et al. Int J Biol Med Res. 2024; 15(1): 7718-7723

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Table 3- VITEK-2 results of Number of CoNS isolates sensitive / Figure 3 - Antibiotic Susceptibility Patterns of Cefoxitin by
resistant to each drug in GP-628 card. various methods in CoNS isolates.

Figure 4 - Antibiotic Susceptibility Patterns of Linezolid by

various methods in CoNS isolates.

Figure 5 - Status of mecA and cfr gene among the CoNS isolates.

Figure 1 – Distribution of clinical sample type positive for CoNS

isolates (%).

Figure 2 - Antibiotic Susceptibility Patterns of Oxacillin by

various methods in CoNS isolates.
Figure 6 - PCR amplified DNA bands of 310 bp molecular weight
corresponding to mecA gene.
 D Sharma et al. Int J Biol Med Res. 2024; 15(1): 7718-7723
DISCUSSION
The incidence of CoNS isolates from clinical samples was 36.8%,
which is similar to the findings of María Cristina Gaudioso de Allori
et al. in 2014-15, who reported that 39.38% of samples contained
CoNS [12]. Among these isolates, 42.14% were from males, while
57.85% were from females, reflecting a similar gender ratio as
reported by T.S. Kumudini et al. [13]. Blood samples yielded the
highest number of CoNS isolates in both the current study and in
studies conducted by Usha et al. in 2012 [14] and Prapti Bora et al. in
2017 [15].
Staphylococcus epidermidis group (Novobiocin sensitive)
outnumbered other novobiocin resistant groups by accounting for
nearly 72.3% of strains, 27.14% were resistant for novobiocin
(Staphylococcus saprophyticus group). Our results were in
agreement with results revealed by Lindsaye Nicolle et al. where
70% strains were reported to be S.epidermidis [16].
This study reported 100% sensitivity of CoNS towards
Vancomycin, Tigecycline and Daptomycin followed by Linezolid
(97.9%). Minimal number of isolates were sensitive against
Oxacillin (20%), Cefoxitin (12.9%) and Benzylpenicillin being the
least active antibiotic against CoNS at 10% sensitivity rate. Similar
results were reported by Roopa et al., (2015) and Usha et al., where
Vancomycin was 100% sensitive [17,14]. Another study by Ragini
Ananth Kashid et al. showed cefoxitin resistance as 83.82%, close to
the figures indicated by the current study [18]. Similar figures of
linezolid resistance were seen in a study by Lubna Samad et al., at a
hospital in North India where only 2.86% CoNS reported linezolid
resistance, comparable to the current study [19].
Comparing the VITEK susceptibility patterns of cefoxitin and
oxacillin, it can be observed that cefoxitin marks the methicillin
resistance compared to oxacillin. A 7.1% of discrepancy was
observed, where isolates that were considered sensitive by oxacillin
were found to be resistant to cefoxitin. Additionally, a significant
difference of 15% in cefoxitin resistance between VITEK 2 and disc
diffusion methods was noted, where 19 isolates that were identified
as cefoxitin-sensitive by manual screening were found to be
cefoxitin-resistant by the automated method.
Recently, it was discovered that the oxacillin breakpoint of ≥
4mg/L recommended by the National Committee for Clinical
Laboratory Standards (NCCLS) lacked sensitivity and was unable to
classify many mecA-positive CoNS as oxacillin resistant. There was
a better correlation between MIC of 0.5 mg/L breakpoint with disc-
diffusion results and mecA gene carriage. Accordingly, the NCCLS
has redefined the breakpoints for oxacillin susceptibility for CoNS,
in a manner that organisms for which the MIC is ≥ 0.5 mg/L are
considered resistant and those for which the MIC is ≤0.25 mg/L are
considered sensitive [20].
CoNS are increasingly turning out antimicrobial resistant
predominately to ß-lactams surpassing S.aureus and some
hospitals have reported the rates of oxacillin resistance in CoNS
approaching 90%, as reported in this study. This data was in
7722
synchronization with the results of current study and thus
antimicrobial stewardship should be regarded with all seriousness
in clinical practice [21].
The cefoxitin MIC and disc-diffusion test performed
equivalently to oxacillin broth microdilution and oxacillin disc
diffusion tests but former gave better correlation with mecA
harbouring strains of CoNS. Thus, oxacillin has a lesser sensitivity
than cefoxitin in terms of detecting mecA presence.
The cefoxitin disc diffusion method is considered a more
accurate predictor for the detection of heterogeneous methicillin
resistance than oxacillin and is recommended by the Clinical and
Laboratory Standards Institute (CLSI). Cephamycins have been
shown to be more potent inducers of the mecA gene, which is why
the CLSI recommends the use of the cefoxitin disc diffusion test for
detecting oxacillin resistance.
PCR is considered as a rapid, gold standard test for determining
antibiotic resistance. In this study, mec A gene was found in 62.8%
of the isolates. Of the 88 oxacillin sensitives isolates in this study, 2
had MIC values ≤ 0.25 μg/mL by both VITEK-2 and microbroth
dilution. Thus, these 2 isolates were strongly sensitive to oxacillin
by all phenotypic evaluations but carried silent mecA gene. This
marks the authenticity of genotypic analysis for determining true
resistant to an antibiotic and emphasizes the necessity of changing
the oxacillin MIC breakpoint to 0.0125 mg/L.
Considering the discrepancies in phenotypic rates of methicillin
resistance compared to molecular detection in the current study, it
can be deduced that there might be other mechanisms responsible
for methicillin resistance in some isolates. Several studies support
these findings; for example, a study in Nigeria reported the
complete absence of five major SCCmec types in addition to mecA
genes [22].
Linezolid is a leading alternate antimicrobial effective against
multi drug resistant CoNS. Resistance to linezolid has been growing
steadily [23]. Even though nearly 4 out of 140 isolates were linezolid
resistant by both automated and manual system in this study, yet
none of them harbored the cfr gene. In a study done by Meerabai
Manoharan et al., from 2016-2018, as low as 3.7% linezolid
resistance was demonstrated by CoNS, one isolate had MIC
at16mg/L but was negative for the cfr gene. All these findings
suggest that resistance might have been due to other mechanisms
such as mutation in 23S rRNA and ribosomal proteins L3 and L4
[24].
cfr gene is not the sole determinant of linezolid resistance.
Resistance can be mediated by the expression of genes optrA or
poxtA etc. The cfr gene has been reported to be associated with
oxazolidinone resistance in several studies (Schwarz et al., 2000;
Shen et al., 2013) but it only mediated low levels of resistance to this
antibiotic class [25-27].
Early detection of methicillin resistant CoNS and controlling the
indiscriminate use of antibiotics are the only suitable approaches to
cease the emergence of these drug resistant strains.
 D Sharma et al. Int J Biol Med Res. 2024; 15(1): 7718-7723

7723

This study has reinforced the alarming rise in antibiotic resistance
and thus proper measures should be adopted against the upsurge in
antibiotic resistance.
ACKNOWLEDGEMENTS
The authors gratefully acknowledge the support rendered by – Mr.
Amir Khan, Maryam Javed and Mohd. Arshad and the technical staff of
the department.
FUNDING
There are no funding sources.
CONFLICT OF INTEREST
None
SUPPORTING INFORMATION
None
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c Copyright 2023 BioMedSciDirect Publications IJBMR -ISSN: 0976:6685.
All rights reserved.