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Jemds.com Original Research Article
J. Evolution Med. Dent. Sci./eISSN- 2278-4802, pISSN- 2278-4748/ Vol. 8/ Issue 51/ Dec. 23, 2019 Page 3863
Prevalence of Multidrug Resistant Staphylococcus aureus in Clinically
Suspected Atypical Pneumonia Patients
Meenakshi Kante1, Rishi Gowtham Racherla2, Usha Kalawat3, B. Venkata Ramana4, D. T. Katyarmal5, Abha Chandra6,
D. Bhargavi7, G. Aruna8, Manohar B.9
1Department of Microbiology, Sri Venkateswara Institute of Medical Sciences, Tirupati, Andhra Pradesh,
India. 2Department of Microbiology, Sri Venkateswara Institute of Medical Sciences, Tirupati, Andhra
Pradesh, India. 3Department of Microbiology, Sri Venkateswara Institute of Medical Sciences, Tirupati,
Andhra Pradesh, India. 4Department of Microbiology, Sri Venkateswara Institute of Medical Sciences,
Tirupati, Andhra Pradesh, India. 5Department of Medicine, Sri Venkateswara Institute of Medical
Sciences, Tirupati, Andhra Pradesh, India. 6Department of Cardio Thoracic Surgery, Sri Venkateswara
Institute of Medical Sciences, Tirupati, Andhra Pradesh, India. 7Department of Medical Oncology, Sri
Venkateswara Institute of Medical Sciences, Tirupati, Andhra Pradesh, India. 8Department of Pulmonary
Medicine, Sri Venkateswara Medical College, Tirupati, Andhra Pradesh, India. 9Department of
Paediatrics, Sri Venkateswara Medical College, Tirupati, Andhra Pradesh, India.
AB S TR AC T
BACKGROUND
Staphylococcus aureus (S. aureus) is one of the common pathogens frequently causing
pneumonia. S. aureus is a gram-positive organism, which belongs to the family
Micrococcaceae. Generally atypical pneumonia is caused by Mycoplasma
pneumoniae, Legionella pneumophila and Chlamydophila pneumoniae. Typical
pathogen S. aureus is the most frequent and common nosocomial acquired infection.
Now-a-days, antibiotic resistant bacterial strains like S. aureus have increased in
hospital settings. Developing antibiotic resistance is a major problem with S. aureus.
We wanted to estimate the non atypical pathogens particularly S. aureus in clinically
suspected atypical pneumonia cases.
METHODS
250 clinical samples of sputum, broncho alveolar lavage (BAL) and pleural fluid
were collected and investigated with Gram staining, culture and antibiotic
sensitivity tests.
RESULTS
Out of a total of 250 cases, S. aureus was isolated in 19 cases. S. aureus showed
highest resistance to Ampicillin (15) (6%), and Penicillin (15) (6%). S. aureus
showed highest sensitivity to Vancomycin 19 (7.6%) and Tetracycline 19 (7.6%).
CONCLUSIONS
Based on clinical symptoms alone, we cannot identify the organism causing the
infection. It is important to determine as to whether it is caused by atypical
pathogen or typical pathogen. Sometimes co-infections might be the reason. That’s
the reason why screening is essential for both atypical and typical pathogens.
Clinicians must follow the authentication-based guidelines and proper patient
management which will help in reducing the severity of the disease. Mainly
screening will help clinicians to give proper treatment as well as decrease the drug
resistance.
KEY WORDS
Pneumonia, Nosocomial Acquired Infection, Sputum, Penicillin G, Drug Resistance
Corresponding Author:
Dr. Usha Kalawat,
Professor, (Clinical Virology)
Department of Microbiology,
Sri Venkateswara Institute of Medical
Sciences, Tirupati-517507,
Andhra Pradesh, India.
E-mail: drushakalawat@gmail.com
DOI: 10.14260/jemds/2019/837
Financial or Other Competing Interests:
Dr. Kalawat reports grants from Sri
Venkateswara Institute of Medical Sciences
(SVIMS) University, SBAVP, personal fees
from Indian Council of Medical Research,
New Delhi, outside the submitted work.
How to Cite This Article:
Kante M, Racherla RG, Kalawat U, et al.
Prevalence of multidrug resistant
staphylococcus aureus in clinically
suspected atypical pneumonia patients. J.
Evolution Med. Dent. Sci. 2019;8(51):
3863-3867, DOI:
10.14260/jemds/2019/837
Submission 21-10-2019,
Peer Review 04-12-2019,
Acceptance 10-12-2019,
Published 23-12-2019.
Jemds.com Original Research Article
J. Evolution Med. Dent. Sci./eISSN- 2278-4802, pISSN- 2278-4748/ Vol. 8/ Issue 51/ Dec. 23, 2019 Page 3864
BA C KG RO UN D
The word "pneumonia" is derived from the prehistoric Greek
word "pneumon" which means "lung," hence the word
"pneumonia" becomes "lung disease. Inflammation of lung's
parenchyma may be in one or both lungs". Pneumonia is
caused by various pathogens like bacteria, viruses, fungi and
parasites. Usually Bacterial Pneumonia caused by both typical
and atypical organisms. Atypical pneumonia caused by
Mycoplasma pneumoniae, Legionella pneumophila and
Chlamydophila pneumoniae. Typical pneumonia caused by
Klebsiella pneumoniae, Pseudomonas, E. coli, Acinetobacter,
Streptococcus pneumoniae, Staphylococcus aureus etc.1 S.
aureus is a common typical pathogen frequently causing
pneumonia. S. aureus is a gram-positive organism belongs to
the family Micrococcaceae, aerobic, catalase and coagulase
positive bacteria. Generally, Staphylococcus species are
normal inhabitants in human beings. 50% of S. aureus causing
pneumonia isolates was turned in to methicillin-resistant S.
aureus (MRSA), because of lack of proper clinical
management.2 Pneumonia caused by S. aureus, is one of the
severe infections and often associated with clinical difficulties
and a high death rate. High mortality rate due to S. aureus
pneumonia in the pre-antibiotic period, diverse is between
50% and 90%. In spite of proper antibiotic therapy, the
mortality rate is high approximately 30-50%.3
Various virulence factors play an important role in
staphylococcal infections and distinctively concerned in the
development of pleuropulmonary infections. Several appear
to be distinctively, especially in the most severe
manifestation of S. aureus pneumonia, the haemorrhagic
necrotizing phenotype. Enormous polymorphonuclear
leukocyte invasion into the lung parenchyma and the
development of micro abscesses are distinctive findings of
pneumonia caused by S. aureus.4
WHO identifies antibiotic resistance as a worldwide
public health problem as a consequence of its effect on
system of health care together with prolonged
hospitalisation, higher costs and increased death rate. In USA,
approximately 2 million people acquire severe infections
caused by bacteria resistant to as a minimum one suggested
antibiotic. Staphylococcus aureus pneumonia is a major public
health problem by increasing rates of antibiotic resistance
due to not so many treatment alternatives.5 Several resistant
strains can be a source of clinical situations shifting between
superficial infections and serious life-threatening infections.6
Hence, S. aureus should be frequently isolated from the
community and Hospital acquired infections. Cell envelope,
ribosome and nucleic acids are the targets for antibiotics in
Staphylococci. These days antibiotic resistant strains of S.
aureus raised in hospital settings. Developing antibiotic
resistance is a major problem with S. aureus.7
The present study is to assess non atypical pathogen
particularly S. aureus in clinically suspected atypical
pneumonia cases.
ME T HO DS
This is a cross sectional study conducted in Department of
Microbiology, Sri Venkateswara Institute of Medical Sciences,
a tertiary care teaching hospital, Tirupati. Clinically suspected
atypical pneumonia cases were selected as per case
definition: fever without chills, headache, myalgia and cough
without sputum production.8,9,10 Total 250 cases of clinically
suspected atypical pneumonia were analysed. Institute Ethics
Committee approval was obtained before the starting of the
study. Clinical samples of Sputum, Bronchoalveolar lavage
and pleural fluid were collected as explained by Isa S. Touhali
et al11 after obtaining the informed written consent.
Before processing samples; centrifugation was done at
6000 rpm for bronchoalveolar lavage and pleural fluid.
Sputum samples were mixed with equal amount of
Dithiothreitol (DTT) for lysis of mucus and centrifuged at
13000 rpm for 10 minutes, supernatant fluid was discarded.
Pellet was collected and divided into two portions for
staining and culture. First portion of pellet was used for gram
staining and Z-N staining by standard method.12 Gram
staining was done for identification of gram-positive
organisms and gram-negative organisms. Z-N staining was
done to identify acid–fast bacilli.
Second portion was used for culture to isolate typical
organisms. A loopful of second portion of pellet was cultured
on Nutrient agar, blood agar and MacConkey agar by
standard method.13 Typical organisms were identified by
based on growth, colony characters and biochemical
reactions. Antibiotic sensitivity test (Hi media) was
performed for each identified organism to know the
sensitivity and resistant pattern. S. aureus was identified by
based on growth, colony characters and biochemical tests.
Statistical Analysis
Data was recorded, managed and analysed using Microsoft
Excel 2007 (Microsoft Corp, USA).
RE S UL T S
Of the total of 250 cases, 19 isolates of S. aureus were isolated
in culture (Table 1). S. aureus showed highest resistance to
Ciprofloxacin 11 (57.89%). No resistance was seen in
Linezolid, Netilmicin, Tetracycline, Vancomycin, Levofloxacin
(Table 2). S. aureus showed highest sensitivity to Vancomycin
19 (100%) and Tetracycline 19 (100%). No sensitivity was
seen in Nitrofurantoin (Table 2).
Total Cases
Organism
Culture Positive
Percentage
250
S. aureus
19
7.6%
Table 1. Total Culture Positive Cases of S. aureus
Antibiotics
Sensitive (%)
Resistant (%)
Amikacin (30 mcg/disc)
3 (15.79)
1 (5.26)
Ciprofloxacin (5 mcg/disc)
7 (36.84)
11 (57.89)
Cefoxitin (30 mcg/disc)
10 (52.63)
8 (42.11)
Clindamycin (2 mcg/disc)
14 (73.68)
4 (21.05)
Cotrimoxazole (25 mcg/disc)
14 (73.68)
5 (26.32)
Erythromycin (15 mcg/disc)
12 (63.16)
7 (36.84)
Nitrofurantoin (300 mcg)
0
1 (5.26)
Gentamicin (10 mcg/disc)
12 (63.16)
7 (36.84)
Linezolid (30 mcg/disc)
16 (84.21)
0
Netilmicin (30 mcg/disc)
1 (5.26)
0
Tetracycline (30 mcg/disc)
19 (100)
0
Vancomycin (30 mcg/disc)
19 (100)
0
Levofloxacin (5 mcg/disc)
1 (5.26)
0
Table 2. Antibiotic Resistance and Sensitivity Pattern in S. aureus
Jemds.com Original Research Article
J. Evolution Med. Dent. Sci./eISSN- 2278-4802, pISSN- 2278-4748/ Vol. 8/ Issue 51/ Dec. 23, 2019 Page 3865
DI S CU SS IO N
S. aureus is a gram positive typical pathogen causing
pneumonia mainly in hospital settings.1 S. aureus in
hospitalized patients with pulmonary infections involved in
three main subsets of pneumonia: hospital-acquired
pneumonia (HAP), health care associated pneumonia (HCAP)
and Ventilator-associated pneumonia (VAP).14 HAP- Infection
of lung tissue occurs in 48 hours or longer following the
hospitalization of a patient with non-intubation. VAP-Hospital
acquired infection of lung tissue that generally occurs in 48
hours or longer following intubation for mechanical
ventilation. HCAP-Acute infection of lung parenchyma
occurring from health care settings includes dialysis centres,
nursing homes, Outpatient clinics or hospitalized patients
within the past 3 months period. This was previously
incorporated in HAP later became a separate group because
of some cases appearing as outpatients with pneumonia had
been infected by way of multidrug-resistant (MDR) strains
previously associated with HAP. Untreated pneumonia can
lead to extensive damage of the lung finally impairment of
lung function occurs and also mortality rates are raised up to
25%.1
S. aureus is an extremely versatile pathogen in humans,
which readily acclimatize to changing environment and attain
antibiotic-resistance genes through a number of diverse
mechanisms. Recently, World Health Organisation classified
global resistance threats and with the organisms of high
precedence is S. aureus. S. aureus is a considerable
opportunistic pathogen that inhabits in healthy humans and
lead to one of the main causes of bacterial infections like
pneumonia in the developed world.15
We evaluated patients with suspected atypical
pneumonia and reported typical pathogen S. aureus in 19
cases among 250 cases. Ruling out whether a patient is
infected with atypical or typical pathogen merely by
observing the symptoms is difficult; because co infections by
S. aureus are common. Therefore, thorough investigations for
both typical and atypical pathogens are required.
This study results were almost similar to the study
conducted by Shah BA et al,16 where S. aureus is the second
most common pathogen causing pneumonia. Our study
results are in discordance with other Indian study Para et al17
and also various parts of the country,18-21 where S.
pneumoniae was the most common pathogen causing
pneumonia.
S. aureus showed highest resistance to Ciprofloxacin 11
(57.89%), Cefoxitin 8 (42.11), Erythromycin & Gentamicin 7
(36.84%), Cotrimoxazole 5 (26.32%), Clindamycin 4
(21.05%), Amikacin and Nitrofurantoin 1 (5.26%) (Table 2).
Highest sensitivity was shown to Vancomycin 19 (100%) and
Tetracycline 19 (100%) followed by Linezolid 16 (84.21%),
Clindamycin & Cotrimoxazole 14 (73.68%), Erythromycin &
Gentamicin 12 (63.16%), Cefoxitin 8 (42.11%) Amikacin 3
(15.79%), Netilmicin and Levofloxacin 1 (5.26%) (Table 2).
Vancomycin was the most effective drug against S. aureus
which was in concordance with other studies from Turkey
and in Europe.22
In recent times multi drug resistant S. aureus strains are
developing in pneumonia cases. Different mechanisms are
involved in S. aureus antimicrobial resistance (AMR).
Resistance was acquired through basic mechanisms like drug
inactivation, enzymatic drug modification, drug efflux, drug
binding site modification, displacement of drug and bypass
mechanisms concerning acquirement of a new drug-resistant
target. Increasing of resistance is also by resistance
determinants transformed through transportable genetic
elements by way of plasmids, transposons and the
staphylococcal cassette genetic material or by mutations in
chromosomal genes.23
Vancomycin resistance was acquired through conjugation
process. Other suggested mechanisms are alterations of cell
wall and increased cell wall synthesis that may stop
Vancomycin from binding to cell wall which results in
continuation of cell wall synthesis. Increase in usage of
Vancomycin, directed to emergence of two categories of
glycopeptide-resistant S. aureus. In the first category
Vancomycin intermediate-resistant S. aureus (VISA) incessant
exposure of glycopeptides lead to thickening of the cell wall
and poorly cross-linked cell wall. In the second category
Vancomycin-resistant S. aureus (VRSA) - High level of
resistance is due to acquisition from Enterococcus species of
the VanA operon.24
Vancomycin is imperative for management of severe
pneumonia infections.25 One of the study stated emergence of
multidrug resistance strains of S. aureus comprising resistant
to Vancomycin all over the world in such strains noticeable
variations observed in physiology, colony morphology and
growth characteristics because of high reductive
circumstances with depressed acetate metabolism.26 In
1980s, first synthesized Ciprofloxacin belongs to the
Fluoroquinolones and extensively used in gram positive
organisms. Generally, this drug is helpful in extermination of
MRSA. Various parts of the world reported MRSA resistance
to Ciprofloxacin.27 Neeta D Gade et al.,28 reported highest
resistance to Ciprofloxacin which is in concordance with our
study. Other studies from India29,30 they also reported 90% of
resistance to Ciprofloxacin. Mehta AP et al., reported gradual
increase in Ciprofloxacin resistance over years, which was
39% in the year 1922 and steadily raised to 68% in the year
of 1996.31 In health care settings, Ciprofloxacin cannot be
helpful as a good empirical choice for treating S. aureus
infections because of its highest resistance. Strains showing
resistant to Ciprofloxacin tend to show increased resistance
to other antibiotics also.32,33
42.11% Cefoxitin resistance was observed in the current
study. Generally, Cefoxitin resistance denotes that it is
Methicillin resistant Staphylococcus aureus (MRSA).34 MRSA
infections are common in hospital settings. As stated, earlier
Ciprofloxacin is commonly administered drug in such
infections.27 Inappropriate treatment management may also
be one of the reasons in developing resistant strains. Hence
screening must be needed for pneumonia causing pathogens
both typical and atypical along with their antibiogram.
CO N CL US IO NS
Multidrug resistant Staphylococcus aureus can be seen in
clinically suspected atypical pneumonia patients. Simply
based on clinical symptoms we cannot identify the organism
causing the infection. It is important to determine as to
whether it is caused by atypical pathogen or typical pathogen.
Jemds.com Original Research Article
J. Evolution Med. Dent. Sci./eISSN- 2278-4802, pISSN- 2278-4748/ Vol. 8/ Issue 51/ Dec. 23, 2019 Page 3866
Sometimes co-infections might be the reason. That’s the
reason why screening is essential for both atypical and
typical pathogens. Clinicians must follow the authentication-
based guidelines and proper patient management which will
help in reducing the severity of the disease. Mainly screening
will guide clinicians to give proper treatment as well as
decrease the drug resistance. Continuous surveillance is
necessary to find out the progression of resistance and
mechanisms of resistance. Cautious use of antimicrobials is
essential to stop the emergence and spread of resistant
microbes.
AC K NO WL ED GE ME NT
Authors acknowledge Sri Venkateswara Institute of Medical
Sciences (SVIMS) University, India for providing funds to
carry out the work (SBAVP), Indian Council of Medical
Research, New Delhi for granting Senior Research Fellowship
(SRF), DHR-ICMR-VRDL and Department of Microbiology for
providing the lab facility to carry out work. This paper is an
extract of a PhD thesis work going to be submitted to SVIMS
University, Tirupati, Andhra Pradesh, India.
RE F ER EN CE S
[1] Sattar SBA, Sharma S. Bacterial Pneumonia. [Updated
2019 Feb 11]. In: Stat Pearls. Treasure Island (FL): Stat
Pearls Publishing 2019. Accessed on 18.09.2019.
[2] Ragle BE, Karginov VA, Wardenburg BJ. Prevention and
treatment of Staphylococcus aureus pneumonia with a
beta-cyclodextrin derivative. Antimicrob Agents
Chemother 2010;54(1):298-304.
[3] González C, Rubio M, Romero-Vivas J, et al.
Staphylococcus aureus bacteremic pneumonia:
differences between community and nosocomial
acquisition. Int J Infect Dis 2003;7(2):102-8.
[4] Adem PV, Montgomery CP, Husain AN, et al.
Staphylococcus aureus sepsis and the Waterhouse-
Friderichsen syndrome in children. N Engl J Med
2005;353(12):1245-51.
[5] Aliberti S, Reyes LF, Faverio P, et al. Global initiative for
meticillin-resistant Staphylococcus aureus pneumonia
(GLIMP): an international, observational cohort study.
Lancet Infect Dis 2016;16(12):1364-76. Erratum
2016;16(12):1324.
[6] Murray PR, Rosenthal KS, Pfaller MA. Staphylococcus and
related organisms. In: Medical Microbiology. 5th edn.
Elsevier Mosby Co, 2005: p. 221-36.
[7] Ioannou CJ, Hanlon GW, Denyer SP. Action of disinfectant
quaternary ammonium compounds against
Staphylococcus aureus. Antimicrob Agents Chemother
2007;51(1):296-306.
[8] Hoa NQ, Larson M, Chuc KNT, et al. Antibiotics and
paediatric acute respiratory infections in rural Vietnam:
health‑care providers’ knowledge, practical competence
and reported practice. Trop Med Int Health
2009;14(5):546-55.
[9] Medline plus. U.S.A: atypical pneumonia [updated 2014
Aug 25. cited 2016 July 13].
https://medlineplus.gov/ency/article/000079. Htm.
[10] Medscape. U.S.A: atypical bacterial pneumonia imaging;
[updated 2015 Dec 16. cited 2016 Aug 16]. emedicine.
medscape. com/article/363083.
[11] Touhali IS, Ibrahim AAF, Dawood HN. Conventional
methods for the diagnosis of pneumocystis jiroveci in
immunocompromised Iraqi patients. Iraqi J Med Sci
2016;14(1):80-7.
[12] Cillóniz C, Ewig S, Ferrer M, et al. Community-acquired
polymicrobial pneumonia in the intensive care unit:
aetiology and prognosis. Crit Care 2011;15(5):R209.
[13] de Roux A, Ewig S, García E, et al. Mixed community-
acquired pneumonia in hospitalised patients. Eur Respir
J 2006;27(4):795-800.
[14] Tong SY, Davis JS, Eichenberger E, et al. Staphylococcus
aureus infections: epidemiology, pathophysiology,
clinical manifestations and management. Clin Microbiol
Rev 2015;28(3):603-61.
[15] Haaber J, Penadés JR, Ingmer H. Transfer of antibiotic
resistance in staphylococcus aureus. Trends in Microbiol
2017;25(11):893-905.
[16] Shah BA, Singh G, Naik MA, et al. Bacteriological and
clinical profile of Community acquired pneumonia in
hospitalized patients. Lung India 2010;27(2):54-7.
[17] Para RA, Fomda BA, Jan RA, et al. Microbial etiology in
hospitalized North Indian adults with community-
acquired pneumonia. Lung India 2018;35(2):108-15.
[18] Lode HM. Managing community-acquired pneumonia: a
European perspective. Respir Med 2007;101(9):1864-
73.
[19] Bartlett JG, Mundy LM. Community-acquired pneumonia.
N Engl J Med 1995;333(24):1618-24.
[20] Howard LS, Sillis M, Pasteur MC, et al. Microbiological
profile of community-acquired pneumonia in adults over
the last 20 years. J Infect 2005:50(2)107-13.
[21] Al-Ghizawi GJ, Al-Sulami AA, Al-Taher SS. Profile of
community- and hospital-acquired pneumonia cases
admitted to Basra General Hospital, Iraq. East Mediterr
Health J 2007;13(2):230-42.
[22] Hanif E, Hassan SA. Evaluation of antibiotic resistance
pattern in clinical isolates of Staphylococcus aureus. Pak J
Pharm Sci 2019;323(Suppl 3):1219-23.
[23] Foster TJ. Antibiotic resistance in Staphylococcus aureus.
Current status and future prospects. FEMS Microbiol Rev
2017;41(3):430-49.
[24] Deyno S, Fekadu S, Astatkie A. Resistance of
Staphylococcus aureus to antimicrobial agents in
Ethiopia: a meta-analysis. Antimicrob Resist Infect
Control 2017;6:85.
[25] McGuinness WA, Malachowa N, DeLeo FR. Vancomycin
resistance in Staphylococcus aureus. Yale J Biol Med
2017;90(2):269-81.
[26] Prasad UV, Vasu D, Gowtham RR. Cloning, expression
and characterization of NAD Kinase from Staphylococcus
aureus involved in the formation of NADP (H): a key
molecule in the maintaining of redox status and biofilm
formation. Adv Biomed Res 2017;6:97.
Jemds.com Original Research Article
J. Evolution Med. Dent. Sci./eISSN- 2278-4802, pISSN- 2278-4748/ Vol. 8/ Issue 51/ Dec. 23, 2019 Page 3867
[27] Gilbert MJ, Boscia A, Kobasa WD, et al. Enoxacin
compared with vancomycin for the treatment of
experimental methicillin-resistant Staphylococcus aureus
endocarditis. Antimicrob Agents Chemother
1986;29(3):461-3.
[28] Gade ND, Qazi MS. Fluoroquinolone therapy in
staphylococcus aureus infections: Where Do We Stand? J
Lab Physicians 2013;5(2):109-12.
[29] Tiwari HK, Sapkota D, Sen MR. High prevalence of
multidrug-resistant MRSA in a tertiary care hospital of
northern India. Infect Drug Resist 2008;1:57-61.
[30] Pai V, Rao VI, Rao SP. Prevalence and antimicrobial
susceptibility pattern of methicillin-resistant
Staphylococcus aureus [MRSA] isolates at a tertiary care
hospital in Mangalore, South India. J Lab Physicians
2010;2(2):82-4.
[31] Mehta AP, Rodrigues C, Sheth K, et al. Control of
methicillin resistant Staphylococcus aureus in a tertiary
care centre: a five-year study. J Med Microbiol.
1998;16(1):31-4.
[32] Fernandez CJ, Ackerman VP. In vitro studies of cipro-
floxacin and survey of resistance patterns in current
isolates. Diagn Microbiol Infect Dis 1990;13(2):79-91.
[33] Tsering DC, Pal R, Kar S. Methicillin-resistant
Staphylococcus aureus: prevalence and current
susceptibility pattern in Sikkim. J Glob Infect Dis
2011;3(1):9-13.
[34] Fernandes CJ, Fernandes LA, Collignon P. Cefoxitin
resistance as a surrogate marker for the detection of
methicillin-resistant Staphylococcus aureus. J Antimicrob
Chemother 2005;55(4):506-10.
