JCDR - Register at Journal of Clinical and Diagnostic Research
Journal of Clinical and Diagnostic Research, ISSN - 0973 - 709X
Microbiology Section DOI : 10.7860/JCDR/2019/40266.12888
Year : 2019 | Month : May | Volume : 13 | Issue : 05 Full Version Page : DC10 - DC15

Prevalence and Molecular Characterisation of Methicillin-Resistant Coagulase Negative Staphylococci (MR-CoNS) Isolated from Nasal Carriers of End Stage Renal Disease Patients- A Prospective Study

Saravanan Murugesan1, Nagaraj Perumal2, Betsy Sowndarya Dass3, Ramanathan Vijayakumar4, Padma Krishnan5

1 Lecturer, Microbiology Division, Department of Clinical Laboratory Services and Translational Research, Malabar Cancer Centre, Thalassery, Kannur, Kerala, India.
2 Scientist B, Department of Microbiology, State Virology Laboratory, Gandhi Medical College, Bhopal, Madhya Pradesh, India.
3 Research Scholar, Department of Microbiology, Dr. ALM PG Institute of Basic Medical Sciences, University of Madras, Taramani, Chennai, Tamil Nadu, India.
4 Chief Nephrologist, Department of Nephrology, Billroth Hospitals, Chennai, Tamil Nadu, India.
5 Assistant Professor (Retd), Department of Microbiology, Dr. ALM PG Institute of Basic Medical Sciences, University of Madras, Taramani, Chennai, Tamil Nadu, India.

NAME, ADDRESS, E-MAIL ID OF THE CORRESPONDING AUTHOR: Dr. Padma Krishnan, Assistant Professor (Retd), Department of Microbiology, Dr. ALM PG Institute of Basic Medical Sciences, University of Madras, Taramani, Chennai-113, Tamil Nadu, India.
E-mail: padma.abpkn@gmail.com


Patient-to-patient transmission of resistant strains has caused a rapid increase in the prevalence of antimicrobial resistance in recent years. Infection has become a major cause of morbidity and is the divond most common cause of death in patients receiving haemodialysis. Compared to methicillin-resistant Staphylococcus aureus (MRSA) transmission, less is known regarding the epidemiology of methicillin-resistant coagulase-negative staphylococci (MR-CoNS) in health care facilities. Patients receiving haemodialysis are at particular risk for the development of invasive infections caused by MR-CoNS.


To detect the prevalence of antibiotic resistance genes among nasal carriage of MR-CoNS from End Stage Renal Disease (ESRD) patients and hospital personnel.

Materials and Methods

This cross-divtional prospective study was conducted over a period of two months (August-September 2013) at the nephrology unit of a tertiary care hospital, Chennai, Tamil Nadu, India. A total of 145 anterior nasal swabs were collected from 115 patients and 30 hospital personnel. Screening of methicillin resistance was done by using phenotypic and genotypic method. Speciation of MR-CoNS was done by conventional biochemical methods. Molecular detection of various antibiotic resistant genes and staphylococcal cassette chromosome mec (SCCmec) type (I-V) was determined by PCR based method.


Among 79 MR-CoNS isolates, S.epidermidis was the predominant species and highest resistance was seen towards co-trimoxazole (29; 36.7%) followed by tetracycline (18; 23%), gentamycin (17; 21.5%), fusidic acid (14; 18%) and linezolid (2; 2.5%). Among the SCCmec types, type IV (n=27) was the predominant type followed by type I (n=18) and type V (n=15), while 17 isolates had two types including I+V (n=8), IV+III (n=6), II+V (n=3).


The findings of our study strongly suggest the need for the establishment of infection control program measures in order to prevent and reduce MR-CoNS infections in ESRD patients.



Multidrug-Resistant Organisms (MDROs) particularly staphylococci have emerged as important causes of Healthcare-associated infections (HAIs), and these infections are related with significant morbidity and mortality [1]. ESRD patients are at higher risk in acquiring infection and colonisation with methicillin-resistant staphylococci (MRS) because they are repeatedly exposed to the hospital environment and often receive prolonged courses of antibiotics, besides being immunocompromised. Haemodialysis unit provides an ideal setting for the cross-transmission of these pathogens and this might occur either through direct patient to patient contact or indirectly through the contaminated hands of hospital staff or environmental surfaces [1,2]. In haemodialysis patients, knowing the carrier state is important for predisposing to subsequent infections and also it can transfer the organisms among dialysis unit staff and community.

There are numerous reports which reveal that there is an estimated prevalence of colonisation of 30% with Staphylococcus aureus and 100% with CoNS which are both commensal and opportunistic pathogens [3,4]. Among CoNS, S. epidermidis, S. haemolyticus and S. hominis are major components of mucosal flora including the nasal microbiota and human skin. Rates of nasal colonisation with methicillin-resistant (MR) isolates are usually lower in the community and tend to increase in the hospital environment, and are much higher among CoNS than S. aureus [3-5]. This is one of the major reasons for CoNS being regarded as reservoirs of methicillin resistance determinant (mecA). Methicillin resistance, mediated by mecA gene encoding low affinity Penicillin-Binding Protein (PBP) 2a, has been observed in high proportion in CoNS isolates [6].

The mecA is carried by a mobile genetic element (MGE) termed the staphylococcal cassette chromosome mec (SCCmec). Furthermore, the SCCmec element frequently harbors integrated insertion sequences, plasmids, and transposons that often encode additional resistance determinants. According to the current SCCmec classification scheme in MRSA, a high number of non-typable and new, previously unidentified SCCmec types in S. aureus have been detected in CoNS. The high genetic diversity within SCCmec elements carried by CoNS makes the identification of SCCmec types in CoNS challenging and reflects a high degree of genetic flexibility [6-11].

It is also reported that MR-CoNS are resistant to other antimicrobial agents compared to MRSA in addition to resistance to methicillin. There has been an indication that there may be a horizontal transfer of these genes among staphylococci, as many of these resistant genes in CoNS are located on MGEs and similar genes have been identified in S. aureus [6-11]. The acquisition of MDR determinants is a characteristic of MR-CoNS making them dangerous pathogens thereby complicating their successful treatment and control.

The accurate and rapid diagnosis of antibiotic resistance genes and associated SCCmec types in staphylococcal carriage is extremely important particularly among haemodialysis patients who are prone to infections. To date, only a few studies have been reported that examined the antimicrobial resistance patterns among individual CoNS species, making the prevalence of antimicrobial resistance among individual species difficult to ascertain [12]. Hence, the present study was aimed to detect the species distribution and its antibiotic resistant genes and to detect the diversity of SCCmec types among nasal carriage of MR-CoNS from ESRD patients and dialysis unit staff in Chennai, South India.

Materials and Methods

This cross-sectional prospective study was conducted over a period of two months (August-September 2013) at the nephrology unit of a tertiary care hospital, Chennai, Tamil Nadu, India. The study was approved by Institutional Human ethical committee (IEC No. PGIBMS/CO/Human Ethical/2011-12/546). Informed consent was obtained from all the subjects included in this study. Hospital records of patients including name, age, sex, duration of dialysis, associated risk factors and co-morbid conditions were documented.

(a) Sample Collection

A total of 145 nasal swabs were collected, of which 115 were from haemodialysis patients and 30 from dialysis unit staff. Using sterile Hi culture collection cotton swabs (HiMedia), the anterior nasal areas were swabbed and transported immediately to the laboratory for the identification of organisms.

(b) Isolation and Identification of Staphylococci

The collected nasal swabs were immediately processed by using 7.5% salt nutrient broth at 37°C for 2-4 hour for initial enrichment of staphylococci. Following enrichment, the tubes containing the swabs were vortexed for 15s and then sub-cultured onto blood agar, MacConkey agar (HiMedia) and incubated at 37°C for 24 hours; for selective isolation of staphylococci, mannitol salt agar (HiMedia) was employed. Based on the gram stain, colony morphology and mannitol fermentation, the isolates were confirmed to be staphylococci by the following standard laboratory tests {Catalase test, slide and tube coagulase tests and DNAse test (DNAse agar base, Hi Media)} [Table/Fig-1].

Isolation and identification of staphylococci.

(c) Screening of methicillin-resistance by phenotypic and genotypic methods

Methicillin resistance was screened by using cefoxitin (30 μg) disc diffusion method and Multiplex PCR (M-PCR) was performed for the simultaneous detection and differentiation of MRSA from MR-CoNS [13]. S. aureus ATCC 43300 and S. epidermidis 35984 were used as positive control.

(d) Speciation of MR-CoNS isolates

Speciation of MR-CoNS isolates was performed manually by using following biochemical tests namely; alkaline phosphatase test, haemolysis on blood agar, urease test, sugar fermentation (mannitol, sucrose, maltose, mannose, trehalose), polymixin B and novobiocin susceptibility [14].

Molecular identification was carried out for S. epidermidis and S. haemolyticus by species specific PCR to differentiate both the organisms [15]. The following primers were used SE1 (ATCAAAAAGTTGGCGAACCTTTTC) and SE2(CAAAAGAGCGTGGAGAAAAGTATCA); SH1 (GGTCGCTTAGTCGGAACAAT), SH2 (CACGAGCAATCTCATCACCT). The PCR cycle conditions were: denaturation for 3 min at 92°C, followed by 30 cycles of 92°C for 1 minute, 56°C for 1 minute and 72°C for 1 minute, and a final extension at 72°C for 5 minute. Amplified products were analysed by 2% agarose gel electrophoresis.

(e) Antimicrobial susceptibility testing (AST)

AST was done for the following antibiotics using Kirby-Bauer disc diffusion method according to the Clinical and Laboratory Standards Institute (CLSI) guidelines 2012 [16]. The following antimicrobial agents were tested: amikacin (30 μg), ciprofloxacin (5 μg), clindamycin (2 μg), co-trimoxazole (1.25/23.75 μg), erythromycin (15 μg), fusidic acid (30 μg), Gentamicin (10 μg), linezolid (30μg), ofloxacin (5 μg), tetracycline (30 μg), vancomycin (30 μg). S. aureus ATCC 25923 and S. epidermidis ATCC 12228 were used as control strains. Minimum Inhibitory Concentration (MIC) of linezolid was done by agar dilution method and with HiCombTM MIC strips (HiMedia).

(f) Detection of inducible and constitutive clindamycin resistance

Inducible and constitutive clindamycin resistance was detected among all the erythromycin-resistant isolates by the double-disc test method with erythromycin (15 μg) disc and clindamycin (2 μg) disc [16]. The inducible phenotype was characterised by a positive D test, a flattening of the inhibition zone around the clindamycin disc near the erythromycin disc which indicated positive inducible macrolide-lincosamide-streptogramin B (iMLSB). The phenotype constitutive (cMLSB) was characterised by erythromycin and clindamycin resistance [Table/Fig-2]. Macrolide streptogramin phenotype (MSB) was characterised by clindamycin sensitivity and erythromycin resistance, with negative D test.

Detection of constitutive and inducible clindamycin resistance.

(g) PCR-based detection of antimicrobial resistance genes

Erythromycin, tetracycline and aminoglycoside resistant genes msrA, erm (A), erm (C), tet (K) tet (M) and aac (6)-Ie-aph(2)-Ia, aph(3)-IIIa, ant(6)-Ia, ant(4)-Ia respectively were determined by M-PCR [17-19]. Fusidic acid resistant genes (fusB, fusC & fusD) were determined by the method of Castanheira M et al., [20]. Linezolid resistant cfr gene and point mutation in domain V of 23S rRNA gene were detected by using previously described method [Table/Fig-3] [21,22].

Primers and their sequences for various antibiotic resistance encoding genes, SCCmec types and SCCmec type IV subtypes used in this study [13,17-24].

Target genesPrimer sequencesProduct (bp)Reference
SCCmec typing
Subtyping of SCCmec type IV (IVa-IVg)

Nucleotide Sequence Accession Number

The nucleotide sequences of a cfr gene, 23S rRNA mutation, fusB, fusC and aac (6)-Ie-aph (2)-Ia gene were deposited in Gen Bank (NCBI) with the accession number KF744025, KF790758, KJ802933, KM411357 and KM411358 respectively.

(h) Detection of SCCmec types and SCCmec type IV subtypes

SCCmec typing (type I-V) was done by using M-PCR [23]. Positive control strains used in the determination of the SCCmec type were the MRSA strains COL-SCCmec type I, Mu50- SCCmec type II, SCCmec type III- ANS46, SCCmec type IV- MW2, SCCmec type V- WIS. SCCmec IV subtypes (IVa, IVb/IVF, IVc/IVE, IVd, IVg, IVh) were determined by M-PCR with primers described by Milheiriço C et al., [Table/Fig-3] [24].

Statistical Analysis

A simple standard deviation was carried out for age distribution analysis of ESRD patients and hospital personnel.


The age distribution of patients who were undergoing haemodialysis and hospital personnel are listed [Table/Fig-4]. The associated risk factors and co-morbid conditions of the ESRD patients included in this study are mentioned in [Table/Fig-5]. A total of 135 isolates of staphylococci were obtained from 145 samples giving an isolation rate of 93%. Of these, 105/115 (91%) were from ESRD patients and 30/30 (100%) were from hospital personnel who were found to be colonisers of staphylococci. Ten samples were negative for any growth upon culture. 79 (58.5%) isolates were found to be methicillin resistant by cefoxitin disc diffusion method and M-PCR [Table/Fig-6].

Age-wise distribution of ESRD patients and hospital personnel.

Details of patients and hospital personnelAverage age (mean±SD, years)
Haemodialysis patients (n=115)
Male (n=68)46.2±16
Female (n=47)47±16.7
Hospital personnel (n=30)
Male (n=10)37.2±7.11
Female (n=20)30.2±10.8

SD: Standard deviation

Associated risk factors and co-morbid conditions of the ESRD patients.

S. No.Factors and conditionsNo. of patientsPercentage
Associated risk factors
2.Diabetes mellitus3228%
Co-morbid conditions
5.Graft rejection21.7%
6.Polycystic kidney disease21.7%
7.Hepatitis-C infection97.8%

Multiplex PCR for detection of MR-CoNS and simultaneous differentiation from MRSA.

L1- S. aureus ATCC 43300; L2- S. aureus ATCC 25923, L3- S. epidermidis ATCC 35984; L4; L5; L6- MR- CoNS; L7- S. epidermidis 12228; M- 100 base pair ladder

Of these MR-CoNS isolates, 68/105 (65%) were from ESRD patients and 11/30 (37%) were from hospital personnel. Among the 79 MR-CoNS isolates, S. epidermidis 56/79 (71%) was the predominant species followed by S. haemolyticus 12/79 (15%), and S. hominis 6/79 (7.5%) [Table/Fig-7].

Species distribution of MR-CoNS from ESRD patients (n=68) and Hospital personnel (n=11).

Detection of antibiotic resistant genes of conventional and newer antibiotics

All isolates exhibited 100% sensitivity to vancomycin. Overall, highest resistance was exhibited towards erythromycin (42; 53%) followed by co-trimoxazole (29; 36.7%) and tetracycline (18; 23%). Low level resistance was found towards fusidic acid (14;18%) followed by ciprofloxacin (12;14.6%) and linezolid (2; 2.5%) [Table/Fig-8]. Erythromycin resistance was found in 42 isolates (53%), of which 12 isolates showed iMLSB phenotype, 7 isolates exhibited cMLSB phenotype and 23 isolates exhibited MSB phenotype.

Antibiotic resistance among MR-CoNS from ESRD patients and hospital personnel.

ESRD patients n=105 (%)Hospital personnel n=30 (%)
No. of MR-CoNS isolates (n=79)68 (65)11 (37)
Antibiotic resistance
Co-trimoxazole (n=29)26 (38)3 (27)
Ciprofloxacin (n=12)8 (12)4 (36)
Erythromycin (n=42)35 (51)7 (64)
Fusidic acid (n=14)14 (21)0 (0)
Gentamycin (n=17)17 (25)0 (0)
Linezolid (n=2)2 (3)0 (0)
Tetracycline (n=18)13 (19)5 (37)

Number in parenthesis indicates percentage

Correlation between phenotypic and genotypic traits of resistance to the antibiotics was absolute. Among the 17 isolates showing aminoglycosides resistance, 11 (64.7%) were positive for aac(6)-Ie-aph(2)-Ia gene, 4 (23.5%) isolates harbored aph(3)- IIIa gene, whereas 2 (11.8%) isolates carried both aph (3)- IIIa and ant(4)-Ia genes. Among the 42 erythromycin resistant isolates tested for erm(A), erm(C) and msrA genes; the msrA gene (n=23; 54.7%) was the most predominant gene followed by erm(C) gene (n=14; 33.3%) and combination of both erm(A) and erm(C) gene (n=5; 12%). Two isolates which showed linezolid resistance carried cfr gene and mutation of G2576T in domain V of 23S rRNA gene.

Diversity of SCCmec and type IV subtypes

SCCmec typing was carried out for all the MR-CoNS isolates by M-PCR. Among the 79 isolates, 62 had a single SCCmec type including type I (n=18), type IV (n=27 and type V (n=15), while 17 isolates had two types [Table/Fig-9,10].

Distribution of SCCmec elements and type IV subtypes among MR-CoNS.

SCCmec typesTotal n=79S. epidermidis n=56 (71%)S. haemolyticus n=12 (15%)S. hominis n=6 (7.5%)S. warneri n=5 (6.5%)
Type I1810 (13)4 (5)0 (0)4 (5)
Type II21 (1.2)0 (0)1 (1.2)0 (0)
Type IV2721 (26.5)3 (3.7)2 (2.4)1 (1.2)
Type V158 (10)5 (6.3)2 (2.4)0 (0)
Type I+V87 (8.8)0 (0)1 (1.2)0 (0)
Type IV+III66 (7.5)0 (0)0 (0)0 (0)
Type II+V33 (3.7)0 (0)0 (0)0 (0)
SCCmec type IV subtyping (n=27)
Type IVA (n=21)2116 (59)3 (11.1)2 (7.4)0 (0)
Type IVG (n=2)22 (7.4)0 (0)0 (0)0 (0)
Type IVD (n=1)11 (3.7)0 (0)0 (0)0 (0)
Non-typable (n=3)32 (7.4)1 (3.7)0 (0)0 (0)

‘n’ indicates no of isolates and figures in parenthesis indicates percentage

Analysis of antibiotic resistance genes and its associated SCCmec types.

SCCmec typesAntibiotic resistant determinants
aac (6´)-Ie-aph (2´)-Iaaph (3´)-IIIatetKmsrAerm(C)dfrAfusBfusC
Type I (n=18)4 (22%)3 (17%)3 (17%)11 (61%)3 (17%)12 (67%)4 (22%)2 (11%)
Type II (n=2)0 (0)0 (0)0 (0)1 (50)0 (0)0 (0)0 (0)0 (0)
Type IV (n=27)1 (3.7%)0 (0)4 (14.8%)5 (18.5%)6 (22.2%)8 (29.6%)1 (3.7%)1 (3.7%)
Type V (n=15)3 (20%)0 (0)4 (27%)4 (27%)3 (20%)4 (27%)0 (0)0 (0)
Type I+V (n=8)0 (0)0 (0)0 (0)2 (25%)0 (0)1 (12.5%)2 (25%)2 (25%)
Type III+IV (n=6)2 (33.3%)2 (33.3%)4 (67%)0 (0)2 (33.3%)3 (50%)1 (17%)0 (0)
Type II+V (n=3)1 (33.3%)0 (0)3 (100%)0 (0)0 (0)1 (33.3%)0 (0)1 (33.3%)

Antibiotic resistant genes and its associated SCCmec types

An analysis of the resistant genes of different SCCmec types among the MR-CoNS showed that resistance to non-β-lactam antibiotics was more common in SCCmec type I and SCCmec type IV, the most frequently identified SCCmec type which also exhibited high rates of occurrence of all the resistant genes [Table/Fig-9,10].


ESRD patients receiving haemodialysis will be in constant flux with both the hospital and community environment and have a significantly higher risk of colonisation by invasive staphylococcal population than normal population. The spread of MR-CoNS from hospital settings has been reported in several recent studies. However, studies on the antibiotic resistance genes and diversity of MR-CoNS in ESRD patients are currently very scarce. Here, we studied the antibiotic resistance genes and diversity of SCCmec elements of MR-CoNS from ESRD patients and hospital personnel. The data regarding high level mupirocin resistance among CoNS from nasal carriers of these study subjects has already been reported and published as a correspondence by the same research group [25].

Species distribution of MR-CoNS showed that S. epidermidis was the predominant species which was in accordance with the previous study [5,26]. Increasing resistance of MR-CoNS to antimicrobial agents and the worldwide emergence and spread of MR-CoNS in particular is of deep concern. The results of this study indicate a higher rate of MR-CoNS (65%) among carrier isolates obtained from haemodialysis patients compared to other reports of MR-CoNS [12]. Higher isolation rate of MR-CoNS was also accompanied by higher resistance to other classes of antibiotics including erythromycin (42;53%), co-trimoxazole (29;36.7%), tetracycline (18;23%), fusidic acid (14;18%) and linezolid (2; 2.5%).

Among aminoglycosides resistant genes, aac (6)-Ie-aph(2)-Ia was the most prevalent gene (64.7%) which was in agreement with the previous reports [26-28]. Among isolates showing macrolide and tetracycline resistance, msrA gene (58.7%) and tet(K) gene (22%) were the most prevalent genes in this study which was in agreement with the other studies whereas tetM was not found in any of the isolates unlike previous reports in which both tetK and tetM genes were found [26,27]. Fusidic acid resistance was low (18%) which was significantly lower than the previous study [20].

In the present study, we found two isolates (one S. epidermidis and one S. haemolyticus) harbouring cfr gene and G2576T point-specific mutation within the domain V of 23S rRNA. The clinical history of the patient revealed prior exposure to linezolid for prophylaxis, which might have preceded successful colonisation of linezolid resistant strains. In particular, two linezolid resistant isolates carried six antimicrobial resistance genes that confer resistance to five different antibiotics. The mutation occurring in 23S rRNA in staphylococci leads to resistance which is non-transferable. Even though we could control the dissemination of 23S rRNA gene by following strict infection control practices in health care settings, it is impossible to control the dissemination of cfr gene mediated resistance due to the fact that this gene is transferred horizontally across bacterial species. There is a need to emphasise the rational antibiotic use and keep linezolid as a reserve because this linezolid drug can be easily exploited in clinical practice by administering orally for treating staphylococcal infections.

In agreement with the previous reports, SCCmec elements were more diverse among MR-CoNS isolates [5,10,11,28,29]. This study revealed great diversity of SCCmec among 79 MR-CoNS isolates in which 62/79 (78.5%) isolates harbored single type and 18/79 (22.3%) isolates harbored two types of SCCmec elements. Among S. epidermidis (n=56), more diversity of SCCmec types was seen of which, SCCmec type IV (n= 21) was the predominant type, followed by type I (n= 10), type V (n= 8) and 16 isolates showed combination of two types. Overall, we observed decreasing prevalence of SCCmec types II, III and V and an increasing prevalence of SCCmec types IV and V. SCCmec IV is reportedly the most frequently acquired SCCmec by S. epidermidis, which is in accordance with the enhanced mobility of this type of SCCmec observed in S. aureus [10,26,28].

The high number of different SCCmec types present in MR- CoNS can build up a large reservoir of new SCCmec types for S. aureus and probably facilitate horizontal transmission among staphylococcal species. It is revealed that the presence of two SCCmec elements appears to be common among MR-CoNS which strongly suggest that new variants may be present in MR-CoNS, which can have a major influence in acquiring resistance to the drugs [10,11,29]. The ESRD patients warranting long term hospitalisation with constant community interactions might act as a reservoir for the dissemination of such acquired resistant determinants.


The limitation in our study is the lack of prevalence data on nasal colonisation and antibiotic resistance of MR-CoNS from the hospital as no data was available. The other limitation in this study is that currently we do not have follow-up data regarding the patient cohort for endogenous infections. As it is an ongoing study, we are following up with our patient cohort for endogenous infection and we intend to publish a manuscript on that soon.


The findings of our study substantiate the need for minimising nasal colonisation of MR-CoNS which may act as a reservoir for endogenous infections in ESRD patients. There is an unmet need for continuous monitoring of antibiotic susceptibility pattern of all MR-CoNS isolates for selection of appropriate therapy.

SD: Standard deviation


[1]D’Agata EM, Addressing the problem of multidrug-resistant organisms in dialysis Clin J Am Soc Nephro 2018 13(4):666-68.10.2215/CJN.1378121729567862  [Google Scholar]  [CrossRef]  [PubMed]

[2]Eliopoulos G, D’Agata EM, Antimicrobial-resistant, Gram-positive bacteria among patients undergoing chronic hemodialysis Clin Infect Dis 2002 35(10):1212-18.10.1086/34428212410481  [Google Scholar]  [CrossRef]  [PubMed]

[3]Morgenstern M, Erichsen C, Hackl S, Mily J, Militz M, Friederichs J, Antibiotic resistance of commensal Staphylococcus aureus and coagulase-negative staphylococci in an international cohort of surgeons: A prospective point-prevalence study PLoS One 2016 11(2):e014843710.1371/journal.pone.014843726840492  [Google Scholar]  [CrossRef]  [PubMed]

[4]Heilmann C, Ziebuhr W, Becker K, Are coagulase-negative staphylococci virulent? Clin Microbiol Infect 2018 9:S1198-743.[Epub ahead of print]10.1016/j.cmi.2018.11.01230502487  [Google Scholar]  [CrossRef]  [PubMed]

[5]Lebeaux D, Barbier F, Angebault C, Benmahdi L, Ruppe E, Felix B, Evolution of nasal carriage of methicillin-resistant coagulase-negative staphylococci in a remote population Antimicrob Agents Chemother 2012 56(1):315-23.10.1128/AAC.00547-1122064532  [Google Scholar]  [CrossRef]  [PubMed]

[6]Ghosh A, Singh Y, Kapil A, Dhawan B, Staphylococcal cassette chromosome mec (SCCmec) typing of clinical isolates of coagulase-negative staphylococci (CoNS) from a tertiary care hospital in New Delhi, India Indian J Med Res 2016 143(3):365-70.10.4103/0971-5916.18262927241652  [Google Scholar]  [CrossRef]  [PubMed]

[7]International Working Group on the Classification of Staphylococcal Cassette Chromosome Elements (IWG-SCC. Classification of staphylococcal cassette chromosome mec (SCCmec): guidelines for reporting novel SCCmec elements Antimicrob Agents Chemother 2009 53(12):4961-67.10.1128/AAC.00579-0919721075  [Google Scholar]  [CrossRef]  [PubMed]

[8]Saber H, Jasni AS, Jamaluddin TZ, Ibrahim R, A review of Staphylococcal cassette chromosome mec (SCCmec) types in coagulase-negative staphylococci (CoNS) species Malays J Med Sci 2017 24(5):07-18.10.21315/mjms2017.24.5.229386968  [Google Scholar]  [CrossRef]  [PubMed]

[9]Becker K, Heilmann C, Peters G, Coagulase-negative staphylococci Clin Microbiol Rev 2014 27(4):870-26.10.1128/CMR.00109-1325278577  [Google Scholar]  [CrossRef]  [PubMed]

[10]Zong Z, Peng C, X, Diversity of SCCmec elements in methicillin-resistant coagulase-negative staphylococci clinical isolates PLoS ONE 2011 6(5):e2019110.1371/journal.pone.002019121637845  [Google Scholar]  [CrossRef]  [PubMed]

[11]McManus BA, Coleman DC, Deasy EC, Brennan GI, O’ Connell B, Monecke S, Comparative genotypes, Staphylococcal Cassette Chromosome mec (SCCmec) genes and antimicrobial resistance amongst staphylococcus epidermidis and staphylococcus haemolyticus isolates from infections in humans and companion animals PLoS ONE 2015 10(9):e013807910.1371/journal.pone.013807926379051  [Google Scholar]  [CrossRef]  [PubMed]

[12]Kozioł-Montewka M, Szczepanik A, Baranowicz I, Jozwiak L, Ksiazek A, Kaczor D, The investigation of Staphylococcus aureus and coagulase-negative staphylococci nasal carriage among patients undergoing hemodialysis Microbiol Res 2006 161(4):281-87.10.1016/j.micres.2005.10.00217145561  [Google Scholar]  [CrossRef]  [PubMed]

[13]Nagarajan A, Arunkumar K, Saravanan M, Kaushik G, Sivakumar G, Krishnan P, Use of triplex PCR for rapid detection of PVL and differentiation of MRSA from methicillin resistant coagulase negative staphylococci J Clin Diagn Res 2013 7(2):215-18.10.1016/j.micres.2009.03.00319616418  [Google Scholar]  [CrossRef]  [PubMed]

[14]Koneman EW, Allenm SD, Janda WM, Schreckenberger PC, The Gram positive cocci. I. Staphylococci and related organisms In Color Atlas and Textbook of Diagnostic Microbiology 1997 5th edn:539-76.  [Google Scholar]

[15]Pereira EM, Schuenck RP, Malvar KL, Iorio NLP, Matos PDM, Olendzki AN, Staphylococcus aureus, Staphylococcus epidermidis and Staphylococcus haemolyticus: Methicillin-resistant isolates are detected directly in blood cultures by multiplex PCR Microbiol Res 2010 165(3):243-49.10.1016/j.micres.2009.03.00319616418  [Google Scholar]  [CrossRef]  [PubMed]

[16]Clinical and Laboratory Standard Institute. Performance standards for antimicrobial susceptibility testing M 100-2012; S22th ed. Wayne, PA. CLSI  [Google Scholar]

[17]Shittu AO, Okon K, Adesida S, Oyedara O, Witte W, Strommenger B, Antibiotic resistance and molecular epidemiology of Staphylococcus aureus in Nigeria BMC Microbiol 2011 11(1):9210.1186/1471-2180-11-9221545717  [Google Scholar]  [CrossRef]  [PubMed]

[18]Strommenger B, Kettlitz C, Werner G, Witte W, Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus J Clin Microbiol 2003 41(9):4089-94.10.1128/JCM.41.9.4089-4094.200312958230  [Google Scholar]  [CrossRef]  [PubMed]

[19]Ida T, Okamoto R, Shimauchi C, Okubo T, Kuga A, Inoue M, Identification of aminoglycoside-modifying enzymes by susceptibility testing: Epidemiology of methicillin-resistant Staphylococcus aureus in Japan J Clin Microbiol 2001 39(9):3115-21.10.1128/JCM.39.9.3115-3121.200111526138  [Google Scholar]  [CrossRef]  [PubMed]

[20]Castanheira M, Watters AA, Mendes RE, Farrell DJ, Jones RN, Occurrence and molecular characterization of fusidic acid resistance mechanisms among Staphylococcus spp. from European countries (2008) J Antimicrob Chemother 2010 65(7):1353-58.10.1093/jac/dkq09420430787  [Google Scholar]  [CrossRef]  [PubMed]

[21]Kehrenberg C, Schwarz S, Distribution of florfenicol resistance genes fexA and cfr among chloramphenicol-resistant Staphylococcus isolates Antimicrob Agents Chemother 2006 50(4):1156-63.10.1128/AAC.50.4.1156-1163.200616569824  [Google Scholar]  [CrossRef]  [PubMed]

[22]Meka VG, Pillai SK, Sakoulas G, Wennersten C, Venkataraman L, DeGirolami PC, Linezolid resistance in sequential Staphylococcus aureus isolates associated with a T2500A mutation in the 23S rRNA gene and loss of a single copy of rRNA J Infect Dis 2004 190(2):311-17.10.1086/42147115216466  [Google Scholar]  [CrossRef]  [PubMed]

[23]Boye K, Bartels MD, Andersen IS, Moller JA, Westh H, A new multiplex PCR for easy screening of methicillin resistant Staphylococcus aureus SCCmec types I–V Clin Microbiol Infect 2007 13(7):725-27.10.1111/j.1469-0691.2007.01720.x17403127  [Google Scholar]  [CrossRef]  [PubMed]

[24]Milheiriço C, Oliveira DC, de Lencastre H, Multiplex PCR strategy for sub typing the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: SCCmec IV multiplex’ J Antimicrob Chemother 2007 60(1):42-48.10.1093/jac/dkm11217468509  [Google Scholar]  [CrossRef]  [PubMed]

[25]Murugesan S, Singh U, Perumal N, Ramanathan V, Krishnan P, High level mupirocin resistance among CoNS from nasal carriers of end stage renal disease patients and hospital personnel from tertiary care centre, Chennai Indian J Med Microbiol 2016 34(1):114-15.10.4103/0255-0857.16767226776137  [Google Scholar]  [CrossRef]  [PubMed]

[26]Bouchami O, Achour W, Mekni MA, Rolo J, Hassen AB, Antibiotic resistance and molecular characterization of clinical isolates of methicillin- resistant coagulase negative staphylococci isolated from bacteremic patients in oncohematology Folia Microbiol 2011 56(2):122-30.10.1007/s12223-011-0017-121431912  [Google Scholar]  [CrossRef]  [PubMed]

[27]Duran N, Ozer B, Duran GG, Onlen Y, Demir C, Antibiotic resistance genes & susceptibility patterns in staphylococci Indian J Med Res 2012 135(3):389-96.  [Google Scholar]

[28]Murugesan S, Perumal N, Mahalingam SP, Dilliappan SK, Krishnan P, Analysis of antibiotic resistance genes and its associated SCCmec types among nasal carriage of methicillin resistant coagulase negative staphylococci from community settings, Chennai, Southern India J Clin Diagn Res 2015 9(8):DC01-05.10.7860/JCDR/2015/11733.630726435940  [Google Scholar]  [CrossRef]  [PubMed]

[29]Saravanan M, Dass BS, Abirami SB, Suriakumar JK, Krishnan P, Prevalence of SCCmec types among methicillin resistant coagulase negative staphylococci isolated from HIV patients in Chennai, South India BMC Infect Dis 2014 14(3):P5110.1186/1471-2334-14-S3-P51PMC4080297  [Google Scholar]  [CrossRef]  [PubMed]