Post on 20-May-2020
z
Vol. 2, Issue 8, pp 158-165, Autumn 2018
ORIGINAL ARTICLE
Isolation of methicillin-resistant Staphylococcus aureus from burn
centers and evaluation of antimicrobial efficacy, in Faisalabad,
Pakistan
Sadaf Pervaz 1
1 Institute of Microbiology, University of Agriculture, Faisalabad, Pakistan.
ARTICLE INFORMATIONS Article History:
Submitted: 15 September 2018
Revised version received:
9 October 2018 Accepted: 10 October 2018
Published online: x December 2018
Key words: MRSA
Burn patients
Faisalabad
Corresponding author: Sadaf Pervaz
Email: Sadafpervez123@gmail.com Institute of Microbiology
University of Agriculture Faisalabad
Pakistan
ABSTRACT Objectives: The present study was conducted for the detection of MRSA
infections in burn wards and for evaluation of different antibiotics efficacy.
Methods: A total of 100 samples were collected from burn ward of Allied
hospital Faisalabad, Pakistan. Then all samples were cultured on Mannitol
salt agar, S-110 agar and then selective biochemical tests were performed.
Antibiotic sensitivity was checked by using different beta-lactam antibiotics
including methicillin, and vancomycin, linezolid, amoxicillin along with
clavulanic acid (ESBL inhibitor) and some others, according to criteria of
Clinical Laboratory Standard Institute (CLSI), to find out better
antimicrobial therapy for burn patients.
Results: A total of 28 (66.66%) isolates of MRSA were detected and
remaining 14 (33.33%) were MSSA, out of 42 isolates of S. aureus. The
results showed that highest risk of MRSA prevalence was associated with
burn patients and had a percentage positivity of 66.66% among burn
patients of Allied hospital, Faisalabad.
Conclusion: It was observed that maximum resistance was found against
beta-lactam drugs especially oxacillin (98%), but maximum level of
sensitivity was observed against linezolid (95%) and vancomycin (99.99%),
means that, these are more effective drugs for the treatment therapy of burn
patients.
Copyright©2018, Sadaf Pervaz This is an open access article distributed under the Creative Commons Attribution License, which permits
unrestricted use, distribution and reproduction in any medium, provided the original work is properly cited.
INTRODUCTIONBurns remain a major portal of entry for a variety of
microbial invasions that results in high rate disabilities,
morbidity and deaths in burn victims, especially in under
developed countries1. Patients with extensive burns are
highly susceptible to local and systemic infections.
Conversely an extensive deep burn wounds have higher
rate of prevalence of sepsis and physical, physiological
and pathological abnormalities2. It is evaluated that burn
wound infections account for maximum number of
deaths in burn victims 3.
Staphylococcus aureus is gram positive bacteria having
grape like clusters in the form of cocci4. It resides as
commensal microbe in interior nares and other skin sites
on healthy individuals and almost 50% individuals are
either persistent or intermittent colonizers of S. aureus5.
S. aureus seems to establish a significant source from
Available online at http://www.sjomr.org
SCIENTIFIC JOURNAL
OF MEDICAL RESEARCH Vo. x, Issue x, pp xx - xx, Winter
2018
Citation: Pervaz S. “Isolation of methicillin-resistant Staphylococcus aureus from burn centers and evaluation of antimicrobial efficacy, in
Faisalabad, Pakistan”. Sci. J. Med. Res. 2018, 2 (8): 158-165.
ISSN: 2520-5234
158 Pervaz S., 2018 .
the normal flora to get the antimicrobial genes which
can be transported to their pathogenic microbes6. It
causes different types of diseases from slight range to
highly devastating due to some toxins and enzymes it
produces and has very unique mechanisms of
antimicrobial resistance that has made it very causative
agent for the development of serious diseases both in
hospitals and in community settings7.
Among gram positive microbes, Methicillin-resistant S.
aureus (MRSA) accounts for most common bacterial
microbe in burn wound infections and it has
significantly high ratio among burn patients .The
patients with high burn scratches are susceptible to this
infectious microbe8. This microbe is considered highly
predominant in nosocomial infections and causes threats
in hospital acquired infections that remain a big barrier
in controlling these infections9,10
.
MRSA gets
colonization in burn wounds within first 48 hours of
infection11
.
The emergence of methicillin-resistant Staphylococcus
aureus (MRSA) crossed down all the options available
to treat simple Staphylococcal infections12
. In healthy
individuals MRSA can inhabit at 1-8% rate that is
actually leading towards the Staphylococcal infections13
.
MRSA has established a lot of resistance, not only to
beta-lactam ringed anti-microbial, but also too few other
antimicrobial classes. MRSA is a main pathogen in
humans and a universal rise in the diseases rate caused
by MRSA is alarming14
. Risk factors that enhance
MRSA infections and establishment including unwise
use of broad spectrum antibiotics, longer hospital stay,
especially in intensive care (ICUs), intravascular
catherization and patients with weak immune systems,
which serve as a major reservoirs and its transmission
mostly occur through the hands of health care staff that
have polluted hands and poor hygienic conditions15
.
Multidrug resistance in S. aureus, especially methicillin
resistance in S. aureus, makes it to cause remarkable
clinical and epidemiological problems, because of their
substitution amongst patients and staff16,17
. In sensitivity
testing, resistance against commonly used beta-lactam
antimicrobials including oxacillin was shown by MRSA
strains18
. By the 1990s S. aureus were shown maximum
resistance towards ampicillin that is most commonly
used broad spectrum beta-lactam drug19
. During the
course of the recent years, many beta-lactam antibiotics
have originated and produced artificially, e.g.
Monobactams, Carbapenems and Cephalosproins etc 20
.
The mode of action of beta-lactam drugs against the cell
wall production (peptidoglycan layer) is most common
target in all drugs. Another modified group of drugs that
affects and raptures the cell wall synthesis includes,
glycopeptides of which vancomycin is the most
significant serious infections caused by for S. aureus
strains. But in recent years almost from 8 years, MRSA
has gained resistance against vancomycin treatment by
producing vancomycin resistant S. aureus strains
(VRSA)21
.
MRSA is a contributing agent of human toxicities due to
numerous mechanisms of resistance including
penicillinase enzymes, other virulence factors and low
affinity of penicillin binding proteins (PBP) to beta
lactam antibiotics that make the treatment options
significantly lower. This all demands then
administration of high efficacy antibiotics that are
expensive as well as lethal to human health. This in turn
results in increase of chances in spreading the organism
to others and higher mortality rate22
.
There are many reports where the incidence of this
microbe is at increasing rate consistently along with
other contributing factors like long hospital stay, costly
treatment etc23
. However, the outbreak of MRSA
infections in community after the hospital infections
appeals for achieving priorities for prevention and
control of this pathogenic microbe24
.
Vancomycin and Clindamycin are highly effective
against MRSA but other than that innovations in fluid
management, better ventilation, proper isolation
protocols and discovery and administration of new and
effective antibiotics can result in significant decline in
morbidity and mortality ratio25
. MRSA is highly
resistant to all available beta lactam antibiotics including
semi synthetic penicillinase resistant antibiotics
(methicillin and vancomycin) due to co-transfer of beta
lactamase enzymes and genetic DNA transfer between
bacterial species make treatment strategy dwindling26
.
This significant increase in MRSA infections highlights
the diminished efforts in developing new therapeutic
drugs. So this consistently exposure in resistant strains
such as MRSA demands for improving the antibiotics
using schedule and production of new antibiotics.
However the emergence of antibiotics resistance have
been described for some antibiotic groups:
aminoglycosides, Lincosamides, Tetracyclines,
chloramphenicol, macrolides27
. Since 2000, new group
Oxazolidinones including linezolid, which is accessible
in recent years. But some sort of direct resistance against
linezolid has been reported28
.
MATERIALS AND METHODS
Ethical Statement:
From the association moral review group for human
clinical samples, a moral explanation was accomplished.
For performance of tests, composed consent from
medical superintendent of clinic was taken.
Study Setting:
This study was approved by chairman of burn ward,
Allied hospital, Faisalabad. This study was organized in
compliance with the Institutional Biosafety Committee,
University of Agriculture Faisalabad.
Study Duration:
Almost 100 burn wounds (swab) specimens were
collected during January 2018 to March 2018 by using
appropriate sampling after getting vocal and written
agreement and were analyzed.
Study Sample:
Specimens were collected by using sterile techniques
from all patients. All swab specimens were transported
to microbiology lab for culturing and sensitivity tests.
Sci. J. Med. Res., Vol. 2, Issue 8, pp 158- 165, Autumn 2018 159 .
The whole procedure was performed according to
microbiological diagnosis of WHO standard for S.
aureus. The history data of patients (epidemiological
parameters) was also collected to correlate the findings.
Media preparation and sample inoculation:
Culture media sterilization was done by using autoclave,
having suitable temperature of 121˚C for sterilization
and it was maintained for 15-20 min/151lb.
For the inoculation of collected samples from burn
patients, nutrient broth was used. Bacterial growth was
transferred on nutrient agar, after overnight incubation.
It is used to maintain growth of all microbes mostly. For
confirmation of S. aureus from the collected samples,
colonies grown on nutrient agar were further streaked on
mannitol salt agar (MSA) that acts as differential and
selective media for S. aureus from other bacteria due to
higher concentration (7.5%) of NaCl that inhibits growth
of other microbes and further more Staph-110 media
was also used to get pure growth of S. aureus from the
MS agar growth, as it acts as selective and differential
media maintaining only growth of pathogenic S. aureus.
Furthermore blood agar was also used for confirmation
of Staphylococcus aureus growth from mannitol salt
media and Staph-110 media through observation of
haemolysis pattern. Gram staining was done for
differentiation of gram positive bacteria from gram
negative bacteria.
Biochemical Identification:
Further confirmation and identification of this bacterial
species was done after performance of the following
biochemical tests29
. In which catalase test, coagulase
test, sugar fermentation test, Voges-Proskauer test,
urease and oxidase test were performed.
Antimicrobial Susceptibility Test for S. aureus
Isolates: After overnight incubation of inoculum, antimicrobial
susceptibility of different antibiotics was checked out by
using Muller Hinton agar and different antibiotics discs
were used and their zone of inhibition were measured as
resistant, intermediate and sensitive. Appropriate zone
diameters were checked out according to the criteria of
the national committee for clinical laboratory standard
institute30
. Antibiotic susceptibility was tested by using
Kirby Bauer susceptibility methods for antibiotic,
according to CLSI guidelines31
. These some
antimicrobial agents are oxacillin, levofloxacin,
amoxicillin, ampicillin and amoxicillin +clavulanic acid,
gentamycin, meropenem, linezolid, Ciprofloxacin,
Levofloxacin, Doxycycline, Vancomycin,
Trimethoprim-sulfamethoxazole, Ceftriaxone, Penicillin
G, Penicillin, Cefotaxime, and Ceftazidime
RESULTS
As 100 samples were taken from Allied hospital, 42
samples out of 100 samples (n=100) were found positive
for Staphylococcus aureus, based on morphology and
biochemical tests and rest 58 samples were of
Pseudomonas aeruginosa , E. coli and other bacteria as
shown in Table 1. From 42 S. aureus samples, 28
(66.66%) samples were positive for MRSA (methicillin
resistant Staphylococcus aureus) and remaining 14
(33.33%) were MSSA (methicillin sensitive
Staphylococcus aureus) as shown in Figures 1 and 2).
All isolates of MRSA were detected to be resistant to
Oxacillin, Penicillin and Ampicillin and sensitive
against Linezolid and vancomycin. From the study
conducted during Feb-April 2018, in burn center of
Allied hospital Faisalabad, MRSA was 66.66%
prevalent in burn patients admitted during that period as
shown in Figure 3, which indicates a significant ratio of
this microbe in burn wounds.
Table 1: Percentage of bacterial isolates from burn ward of Allied
Hospital, Faisalabad, Pakistan. Bacterial groups detected Numbers Percentage(%)
S. aureus 42 42
Pseudomonas aeruginosa 30 30
E. coli + other bacteria 28 28
Total 100 100
Figure 1: The coloumn chart is illustrating the information
regarding to the number of bacterial isolates from burn ward of
Allied Hospital, Faisalabad, Pakistan.
Figure 2: The pie graph is showing the prevalence of various
isolates in the form of %age.
0
20
40
60
80
100
120N
um
be
r o
f sa
mp
les
Bacterial isolates
Total samples S. aureus P. aeruginosa E. coli+ other bacteria
58% other
MRSA 66.66% MSSA
33.33%
S.aureus 42%
S.aureus MRSA MSSA
160 Pervaz S., 2018 .
Figure 3: Prevalence %age of MRSA in burn center of Faisalabad
during Feb-April 2018.
In the second part of study, 22 antimicrobials, Oxacillin,
Amoxicillin, and Ampicillin, Amoxicillin +clavualnic
acid combination, Levofloxacin, gentamycin,
Vancomycin, Amikacin and Linezolid, Cefotaxime and
others were used to check the antimicrobial efficacy of
these antibiotics against MRSA as shown in Figures 4
and 5. Maximum resistance was observed against
oxacillin (n=27/28), ampicillin (n=28/28),
chloramphenicol (n=26/28), cefotaxime (n=24/28),
Ceftazidime (n=25/28), levofloxacin (n=23/28),
ciprofloxacin (n=24/28), meropenem (n=27/28),
ofloxacin (n=26/28), penicillin (n=28/28), penicillin G
(n=27/28) and intermediate resistance was observed
against Amikacin (n=20/28), gentamicin (n=21/28),
doxycycline (n=21/28), azithromycin (n=15/28) and
amoxicillin+ clavulanic acid combination (n=21/28)
(Fig. 4, 5, 6.1). However maximum level of sensitivity
was detected against clindamycin (n=6/28), ceftriaxone
(n=5/28), linezolid (n=3/28), piperacillin-Tazobactam
(n=6/28) and trimethoprim-sulfamethoxazole ( n=5/28),
with almost zero percent resistance and 99.99%
sensitivity was shown against vancomycin (n=0/28)
drug (Fig 5, 6.2), which is showing that vancomycin is
most effective drug to heal burn wound infections in
patients admitted in burn ward of Allied hospital and
also helpful to lessen over and misuse of antibiotics that
only enhance antibiotic resistance capacity of microbes.
Figure 4: Percentage pattern of resistance, intermediate and
sensitivity of antibiotics. Blue series = Resistant, Red series =
intermediate, Green series = Sensitive.
Figure 5: Percentage pattern of resistance, intermediate and
sensitivity of different antibiotics. Blue series = Resistant, Red
series = intermediate, Green series = Sensitive.
Figure 6.1: Resistant pattern of antibiotics by percentages.
Figure 6.2: Resistant pattern of antibiotics by percentages.
Discussion Methicillin-resistant Staphylococcus aureus (MRSA) is
contributing continuously in spreading infections both in
hospitals and in communities around the world32
.
100
58
42
66.66
33.33
0
20
40
60
80
100
120
Totalsamples
Otherbacteria
S.aureus MRSA MSSA
Pe
rce
nta
ge
Prevalence of MRSA
Prevalence of MRSA in burn centre of Faisalabad during Feb-April 2018
0
20
40
60
80
100
120
Pe
rce
nta
ge
Antibiotics
Resistant Intermediate Sensitive
0
20
40
60
80
100
120
Pe
rce
nta
ge
Antibiotics
Resistant Intermediate Sensitive
0
20
40
60
80
100
120
Res
ista
nce
pat
tern
(%)
Antibiotics
0
20
40
60
80
100
120
Res
ista
nce
pat
tern
(%)
Antibiotics
Sci. J. Med. Res., Vol. 2, Issue 8, pp 158- 165, Autumn 2018 161 .
MRSA is a persistent issue in hospitals especially in less
developed countries. Present review also indicates the
pervasiveness of MRSA in Allied hospital in Faisalabad,
Pakistan.
MRSA related infections are more serious and persistent
one because they lead to longer hospital stays and
economic burden as compare to methicillin sensitive
strain of S. aureus (MSSA)33
. With the passage of time
MRSA infections are also present in community settings
other than hospital acquired infections34,35
. Moreover,
transmission of MRSA strains can occur via zoonotic
transmission between humans and animals because of
sharing of their common ancestry36,37
. The present
review was focused for investigating MRSA
prevalence in burn canter of Allied hospital Faisalabad,
Pakistan, only a few reviews on prevalence of MRSA in
Pakistani health care facilities and in hospitals have been
reported38
. The patients with high burn abrasions are
vulnerable to this infectious microbe and it causes out
breaks in hospital acquired infections that are creating a
big hurdle in handling these infections as many strains
are showing resistance to a lot of available remedial
drugs and other therapeutic strategies39,40
.
In the present review, total 100 samples were taken, for
this purpose, 100 swabs were collected from burnt
patients from Allied hospital Faisalabad and were
selected for MRSA. In the second part of study, Twenty
two antimicrobials Oxacillin, Amoxicillin, and
Ampicillin, Amoxicillin +clavualnic acid combination,
Levofloxacin, gentamycin, Vancomycin, Amikacin and
Linezolid, Cefotaxime etc. were used to check the
antimicrobial efficacy of these antibiotics against
MRSA.
Total MRSA percentage from burnt patients was 42%.
All isolates of MRSA were detected to be resistant to
Oxacillin, Penicillin and Ampicillin and sensitive
against Linezolid and vancomycin. Out of 100 samples,
42 samples of S. aureus were detected based on
morphology and biochemical tests. From 42 S. aureus
samples, 28 samples were positive for MRSA and
remaining were MSSA (methicillin sensitive
Staphylococcus aureus).
In this review, 100 burn samples from Allied hospital
were observed to check out MRSA contamination but
each of them was contaminated with more than microbe,
similar results were conducted by Rehman in 2011,
where it was observed that along with other microbial
contamination, MRSA infections are going to rise in
Peshawar every year, especially in burn patients. In
2009, there were 207 cases, in 2010, there were 284
cases reported and in 2011, there were 438 cases
detected41
.
However in this study among Gram +ve bacteria S.
aureus showed maximum prevalence specially MRSA
strains of S. aureus is present at higher numbers in burn
patients due to immuno-compromised situation of their
body42
, that is unable to protect them against microbes
as burn wound is an ideal place for microbe residing and
proliferation because the underlying vasculature of skin
has been damaged so other immune cells of body cannot
reach there to provide protection against infection43
.
In 1961, when first strain of MRSA reported in England,
but with passage of time this bacterium acquired
resistance against most commonly used antibiotics44
.
However methicillin resistance in S. aureus was found
because of presence of mecA gene (an exogenous gene)
present on mobile genetic element called Staphylococcal
cassette chromosome mec (SCCmec). This gene encodes
a modified form of penicillin-binding protein called
PBP2a that makes it less vulnerable to commonly used
beta-lactam antibiotics45
.
The MRSA issue has remained not only a hospital
related microbe but also emerging rapidly in community
acquired infections46
. CA-MRSA infections are causing
a critical threat to health care systems due to their attack
on normal individuals by causing different soft tissue
and skin infections. MRSA is of prime importance from
the category of Gram positive microbes47
.
Now it has been recognized about the fact that microbial
colonization and other diseases in hospitalized patients
are a key source to spread to other wards and in other
patients staying in those hospitals. After gaining of
resistance, MRSA strains become more aggressive and
spread effectively on other contaminated objects that
make their removal less effective48
.
Another review focused by National Nosocomial
infections Surveillance System recognized that about
60% cases due MRSA were related to hospitals called
them HA-MRSA (NNIS, 2004). The total incidence of
MRSA cases are raising and a big surveillance program
conducted in U.S discovered that during 1995-2001 an
increase in MRSA rates occurred from (22-57%)49
.
Another review acknowledged that during 1997-1999,
the total frequency of MRSA isolates in hospitals was
high; such as 67% in Japan, 35% in Latin America, 32%
in USA, and 23% in Australia, 40% in South America,
26% in Europe50
.
In developing countries the problems of antimicrobials
resistance are occurring more frequently rather than the
developed countries because of higher rates of infections
due to unhygienic conditions and financial burden also
acts as big hurdle to combat this enemy completely and
hospital acquired infections are chief morbidity and
mortality sources51
.
There are many reports given that resistance
mechanisms of hospitals acquired MRSA (HA-MRSA)
infections against many antimicrobial agents such as
aminoglycosides, fluoroquinolone and Tetracyclines,
and these antimicrobials groups which are showing
minimum level of affectivity52
. Another antibiotic
vancomycin remains a front-line treatment linezolid
resistant MRSA strains but some reports have been
published now against vancomycin resistance53
. Some
strains are emergent in USA that are showing
intermediate resistant to Vancomycin (VISA) and also
full resistant to Vancomycin (VRSA), that in turn is very
frightening condition to combat this deadly pathogen
with full potential54
.
162 Pervaz S., 2018 .
Conclusions In this study antimicrobial resistance pattern was
observed through disc diffusion mechanism using
Muller Hinton agar that showed maximum resistance
was shown by MRSA against methicillin and other
common beta-lactam drugs means that these drugs are
ineffective in treating the burn infections that only leads
to increase the antimicrobial resistance among burn
patients but it showed maximum sensitivity against
Linezolid and Vancomycin, as out of 100%, almost
more than 95% sensitivity was observed against these
two drugs, means that, these are more effective drugs for
the treatment therapy of burn patients.
REFERENCES 1. Saaiq M. "Epidemiology and Outcome of Childhood Electrical
Burn Injuries at Pakistan Institute of Medical Sciences Islamabad,
Pakistan". Journal of Burn Care & Research. 2016; 37(2):174-
180. DOI: 10.1097/BCR.0000000000000202.
2. Branski L.K., Al-Mousawi A. and Rivero H. "Emerging infections
in burns". Surgical Infections. 2009; 10(5): 389 - 397. DOI:
10.1089/sur.2009.024.
3. Singh NP., Goyal R., Manchanda V., Das S., Kaur . "Changing
trends in bacteriology of burns in the burns unit, Delhi, India".
Burns. 2003; 29(2):129-132.
4. Pantosti A. and Venditti M. "Series MRSA and the
pulmonologist’’. Edited by M. Woodhead and A. Torres Number 1
in this Series. What is MRSA? European Respiratory Journal.
2009; 34(5):1190–1196.
5. Wertheim H.F., Melles D.C., Vos M.C., Leeuwen W.V., Belkum
A.V., Verbrugh H.A. and Nouwen J.L. "The role of nasal carriage
in Staphylococcus aureus sinfections". Lancet Infectious
Diseases. 2005; 5(12):751–762. DOI:10.1016/S1473-
3099(05)70295-4.
6. Tunney M. "Methicillin-resistant Staphylococcus aureus (MRSA)
in nursing homes: can an improvement in infection control
practices decrease MRSA prevalence?". Dataset. 2012;
doi.org/10.1186/ISRCTN79334890.
7. Moran G.J. "Prevalence of Methicillin-resistant Staphylococcus
aureus among Emergency Department Patients with Community-
acquired Skin and Soft-tissue". Academic Emergency Medicine.
2005; 12(1): 64.
8. Ullah A., Qasim M., Rehman H., Khan J., Muhammad H.N., Khan
A. and Muhammad N. "High frequency of methicillin-resistant
Staphylococcus aureus in Peshawar Region of Pakistan".
SpringerPlus.2016; 5 (1):1-6. DOI:10.1186/s40064-016-2277-3.
9. Bang R.L., Gang R.K., Sanyal S.C., Mokaddas E.M. and Lari
A.R. "Beta-haemolytic Streptococcus infection in burns". Burns.
1999; 25(3):242-246.
10. Taneja N., Emmanuel R., Chari P.S. and Sharma M. "A
prospective study of hospital-acquired infections in burn patients
at a tertiary carereferral centre in North India". Burns. 2004;
30(7):665-669. DOI:10.1016/j.burns.2004.02.011.
11. Church D., Elsayed S., Reid O., Winston B. and Lindsay R. "Burn
wound infections". Clinical microbiology revolution. 2006;
19(2):403-434. DOI:10.1128/CMR.19.2.403-434.2006.
12. Cook N. "Methicillin-resistant Staphylococcus aureus versus the
burn patient". Burns.1998; 24(2):91-98.
13. Torre F.C., Torrellas B., Rua M., Yuste J.R. and Pozo J.L.
"Staphylococcus aureus nasal carriage among medical
students". The Lancet Infectious Diseases. 2017; 17(5):477-478.
DOI:10.1016/S1473-3099(17)30188-3.
14. Khalid A. "In-vitro susceptibility of linezolid against methicillin
resistant Staphylococcus aureus at a tertiary care hospital in
Pakistan". Journal of Microbiology and Infectious Diseases. 2013;
3(4): 203-206. DOI: 10.5799/ahinjs.02.2013.04.0109 .
15. Naik V., Date K. and Philip S. "Colonization of Methicillin
Resistant Staphylococcus aureus Among Nursing Staff at a
Tertiary Care Hospital" .Indian Journal of Applied Research.
2011; 4(3): 417-419.
16. Nemati M., Hermans K., Lipinska U., Denis O., Deplano A.,
Struelens M., Devriese L.A., Pasmans F. and Haesebrouck F.
"Antimicrobial resistance of old and recent Staphylococcus
aureus isolates from poultry: first detection of livestock-
associated methicillin-resistant strain ST398". Antimicrobial
Agents and Chemotherapy. 2008; 52(10): 3817-3819.
DOI:10.1128/AAC.00613-08 .
17. Ishihara K., Saito M., Shimokubo N., Muramatsu Y., Maetani S.
and Tamura Y. "Methicillin-resistant Staphylococcus aureus
carriage among veterinary staff and dogs in private veterinary
clinics in Hokkaido, Japan". Journal of Microbiology and
Immunology. 2014; 58(3): 149-154. DOI:10.1111/1348-
0421.12128.
18. Seybold U., Kourbatova E.V., Johnson J.G., Halvosa S.J., Wang
Y.F., King M.D., Ray S.M. and Blumberg H.M. "Emergence of
Community-Associated Methicillin-Resistant Staphylococcus
aureusUSA300 Genotype asa Major Cause of Health Care--
Associated Blood Stream Infections". Clinical Infectious
Diseases. 2006; 42(5): 647-656. DOI:10.1086/499815.
19. Goto H., Shimada K., Ikemoto H. and Oguri T. "Antimicrobial
susceptibility of pathogens isolated from more than 10 000
patients with infectious respiratory diseases: a 25-year
longitudinal study". Journal of Infection and Chemotherapy. 2009;
15(6): 347-360.
20. Malik S. "Molecular typing of methicillin-resistant staphylococci
isolated from cats and dogs". Journal of Antimicrobial
Chemotherapy. 2006; 58(3): 428-431. DOI:10.1093/jac/dkl253.
21. Paterson G.K., Morgan F.J.E., Harrison E.M., Peacock S.J.,
Parkhill J., Zadoks R.N. and Holmes M.A. "Prevalence and
properties of mec C methicillin-resistant Staphylococcus aureus
(MRSA) in bovine bulk tank milk in Great Britain". Journal of
Antimicrobial Chemotherapy. 2013;69(3): 598–602. DOI:
10.1093/jac/dkt417.
22. Reardon C.M., Brown T.P., Stephenson A.J. and Freedlander E.
"Methicillin-resistant Staphylococcus aureus in burns patients—
why all the fuss?". Burns. 1998; 24(5): 393-397.
DOI: https://doi.org/10.1016/S0305-4179(98)00036-9.
23. Cosgrove S.E., Sakoulas G., Perencevich E.N., Schwaber M.J.,
Karchmer A.W. and Carmeli Y. "Comparison of Mortality
Associated with Methicillin‐Resistant and Methicillin‐Susceptible
Staphylococcus aureus Bacteremia: A Meta‐analysis". Clinical
Infectious Diseases. 2003; 36(1): 53-59. DOI:10.1086/345476 .
24. Engemann J.J., Carmeli Y., Cosgrove S.E., Fowler V.G.,
Bronstein M.Z., Trivette S.L., Briggs J.P., Sexton D.J. and
KayeK.S. "Adverse Clinical and Economic Outcomes Attributable
to Methicillin Resistance among Patients with Staphylococcus
Sci. J. Med. Res., Vol. 2, Issue 8, pp 158- 165, Autumn 2018 163 .
aureus Surgical Site Infection". Clinical Infectious Diseases.
2003; 36(5): 592-598. DOI:10.1086/367653.
25. Branski L. K., Mousawi A.A., Rivero H., Jeschke M.G., Sanford
A.P. and Herndon D.N. "Emerging Infections in Burns". Surgical
Infections. 2009; 10(5): 389-397. DOI:10.1089/sur.2009.024.
26. Lyon B.R., Gillespie M.T. and Skurray R.A. "Detection and
Characterization of IS256, an Insertion Sequence in
Staphylococcus aureus". Journal of Microbiology. 1987; 133(11):
3031-3038. DOI:10.1099/00221287-133-11-3031.
27. Vengust M., Anderson M.E., Rousseau J. and Weese J.S.
"Methicillin-resistant Staphylococcal colonization in clinically
normal dogs and horses in the community". Letters in Applied
Microbiology. 2006; 43(6): 602-606. DOI:10.1111/j.1472-
765X.2006.02018.x.
28. Flamm R.K., Farrell D.J., Mendes R.E., Ross J.E., Sader H S.
and Jones R.N. "LEADER Surveillance program results for
2010:an activity and spectrum analysis of linezolid using
6801clinical isolates from the United States (61 medical
centers)". Journal of Diagnostic Microbiology and Infectious
Disease. 2012; 74(1): 54-61. DOI:
10.1016/j.diagmicrobio.2012.05.012.
29. Tsegaye S., Ketema B. and Tsige K. "The growth potential and
antimicrobial susceptibility patterns of Salmonella specie and
Staphylococcus aureus isolated from mobile phones of food
handlers and healthcare workers in Jimma Town, Southwest
Ethiopia". African Journal of Microbiology. 2016; 10(8): 254-259.
DOI: doi.org/10.5897/AJMR2015.7621.
30. Barry A. "An Overview of the Clinical and Laboratory Standards
Institute (CLSI) and Its Impact on Antimicrobial Susceptibility
Tests". 2007; CLSI ,1-6.
31. Hiramatsu K., Katayama Y., Yuzawa H. and Ito T. "Molecular
genetics of methicillin-resistant Staphylococcus aureus".
International Journal of Medical microbiology. 2012; 292(2): 67-
74. DOI:10.1078/1438-4221-00192.
32. Lalremruata R. and Prakash S. "Prevalence of community
acquired methicillin-resistant Staphylococcus aureus inpatients
with skin and soft tissue infections". Community Acquired
Infection. 2014; 1(1): 21-24.
33. Rubin R.J., Harrington C.A., Poon A., Dietrich K., Greene J.A.
and Moiduddin A. "The economic impact of Staphylococcus
aureus infection in New York City hospitals". Emerging Infectious
Diseases. 1999; 5(1): 9-17. DOI:10.3201/eid0501.990102.
34. Persoons D., Hoorebeke S.V., Hermans K., Butaye P., Kruif
A.D., Haesebrouck F. and Dewulf J. "Methicillin-Resistant
Staphylococcus aureus in Poultry". Emerging Infectious
Diseases. 2009; 15(3): 452–453. DOI:10.3201/eid1503.080696.
35. Faires M.C., Traverse M., Tater K.C., Pearl D.L. and Weese J.S.
"Methicillin-Resistant and - Susceptible Staphylococcus aureus
Infections in Dogs". Emerging Infectious Diseases. 2010;16(1):
69–75. DOI:10.3201/eid1601.081758.
36. Lee J.H. "Methicillin (Oxacillin)-resistant Staphylococcus aureus
strains isolated from major food animals and their potential
transmission to humans". Applied and Environmental
Microbiology. 2003; 69(11): 6489-6494.
37. Baptiste K.E., Williams K., Willams N.J., Wattret A., Clegg P.D.,
Dawson S., Corkill J.E., Neill T.O., Hart C.A. "Methicillin resistant
Staphylococci in Companion Animals". Emerging Infectious
Diseases. 2005; 11(12): 1942-1944.
38. Aslam N., Izhar M. and Mehdi N. "Frequency of methicillin
resistant Staphylococcus aureus nasal colonization among
patients suffering from methicillin resistant Staphylococcus
aureus bacteremia". Pakistan Journal of Medical Sciences.
.2013; 29(6): 1430-1432. .
39. Bang R.L., Gang R.K., Sanyal S.C., Mokaddas E.M. and Lari
A.R. "Beta-haemolytic Streptococcus infection in burns". Burns.
1999; 25(3): 242-246. .
40. Taneja N., Emmanuel R., Chari P.S. and Sharma M. "A
prospective study of hospital-acquired infections in burn patients
at a tertiary care referral centre in North India". Burns. 2004;
30(7): 665-669. DOI:10.1016/j.burns.2004.02.011.
41. Ullah A., Qasim M., Rahman H., Khan J., Haroon M., Muhammad
N., Khan A. and Muhammad N. "High frequency of methicillin-
resistant Staphylococcus aureus in Peshawar Region of
Pakistan". Springer plus. 2016; 5(1):1-6. DOI:10.1186/s40064-
016-2277-3.
42. Church D., Elsayed S., Reid O., Winston B. and Lindsay R. "Burn
wound infections". Clinical microbiology revolution. 2006; 19(2):
403-434. DOI:10.1128/CMR.19.2.403-434.2006.
43. Rafla K., Tredget E.E. "Infection control in the burn unit". Burns.
2011. 37(1): 5-15. DOI:10.1016/j.burns.2009.06.198.
44. Jevons M. "Methicillin resistance in Staphylococci". Lancet 1963;
281(7287): 904-907.
45. Gordon R.J. and Lowy F.D. "Pathogenesis of Methicillin‐
Resistant Staphylococcus aureus Infection". Journal of Clinical
Infectious diseases. 2008; 46(S5): S350-S359.
DOI:10.1086/533591.
46. Malik S. "Molecular typing of methicillin-resistant Staphylococci
isolated from cats and dogs". Journal of Antimicrobial
Chemotherapy. 2006; 58(2): 428-431. DOI:10.1093/jac/dkl253.
47. Cook N. "Methicillin-resistant Staphylococcus aureus versus the
burn patient". Burns. 1998; 24(2): 91-98.
48. Quddoum S.Si., Bdour S.M. and Mahasneh A.M. "Isolation and
characterization of methicillin resistant Staphylococcus aureus
from livestock and poultry meat". Annals of Microbiology. 2006;
56(2): 155-161.
49. Diekema D.J., Pfaller M.A., Schmitz F.J., Smayevsky J., Bell J.,
Jones R.N. and Beach M. "Survey of infections due to
Staphylococcus species: frequency of occurrence and
antimicrobial susceptibility of isolates collected in the United
States, Canada, and Latin America, Europe and Western Pacific
region for the SENTRY Antimicrobial Surveillance Program,
1997". Clinical Infectious Diseases. 2001; 32(S2): S114-S132.
DOI:10.1086/320184.
50. Wisplinghoff H., Bischoff T., Tallent S.M.,Seifert H., Wenzel R.P.
and Edmond M.B. "Nosocomial bloodstream infections in US
hospitals: analysis of 24,179 cases from a prospective
nationwide surveillance study". Clinical infectious diseases. 2004;
39(3): 309-317. DOI:10.1086/421946.
51. Peter A. and Wilson R. "Management of Glycopeptide-Resistant
Staphylococcus aureus Infections". Management of Multiple
Drug-Resistant Infections. 2004; 79-90.
52. Monnet D.L., MacKenzie F.M., López-Lozano J.S., Beyaert A.,
Camacho M., Wilson R., Stuart D. and Gould I.M. "Antimicrobial
Drug Use and Methicillin-resistant Staphylococcus aureus,
Aberdeen, 1996–2000". Emerging Infectious Diseases. 2004;
10(8): 1432-1441. DOI:10.3201/eid1008.020694.
164 Pervaz S., 2018 .
53. Rybak M. and LaPlante K.L. "Community-associated methicillin-
resistant Staphylococcus aureus: a review. Pharmacotherapy".
Journal of human pharmacology and drug therapy. 2005; 25(1):
74-85.
54. Cepeda J.A. "Linezolid versus teicoplanin in the treatment of
Gram-positive infections in the critically ill: a randomized, double-
blind, multicentre study". 2004; 53(2): 345-355.
DOI:10.1093/jac/dkh048.
Sci. J. Med. Res., Vol. 2, Issue 8, pp 158- 165, Autumn 2018 165 .