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 .