Egypt J. Med. Lab. Sci., April. 2008; 17(1):35-43 ISSN 1110-5593

METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS AS A NOSOCOMIAL PATHOGEN IN BURN WOUND INFECTION Original 1 2 Article Nehal I. Draz, Mahmoud K. Elsayed , and Hazem M. Aly

1Microbiology, immunology. and 2Plastic surgery departments, Faculty of medicine, Ain Shams University

ABSTRACT

Background: Methicillin resistant staphylococcus aureus (MRSA) is important as a nosocomial pathogen and MRSA colonization in the burn unit may lead to increased transmission of MRSA to non burn patients in other wards. Aim of the Work: was to determine the prevalence of MRSA among patients with burn wound infection in the Burn Unit in Ain Shams University Hospitals. Patients and Methods: The study involved fifty patients with infected burn wounds divided into two groups as twenty five outpatients and twenty five inpatients in the Burn Unit of Ain Shams University Hospital. Swabs were taken aseptically from infected wounds for bacteriological examination. Results: The most common bacterial isolate among outpatients group was S. aureus (44%), followed by Ps. aeurginosa (40%), coagulase negative Staphylococci (12%), Proteus mirabilis (4%) and Citrobacter freundii (8%). While in the inpatients group, Ps. Aeruginosa topped the list infecting 36% of patients, followed by S. aureus (24%), coagulase negative Staphylococci (16%), Klebsiella pneumoniae (12%), E.coli (12%), Proteus mirabilis (8%) and S. pyogenes (4%). Concerning MRSA, it was isolated from 20% of the inpatients, accounting for 83% of all isolated S.aureus and emerged as a significant nosocomial pathogen as it was not recovered from any outpatient. Conclusion: MRSA is a significant nosocomial pathogen in the Burn unit of Ain Shams University Hospital. Continuous surveillance of burn wound infection and developing strategies for antimicro- bial resistance control is recommended. Key Words: Nosocomial, MRSA, Burn, Staphylococci. Corresponding Author: Dr. Nehal Draz, Microbiology Department, Faculty of medicine, Ain Shams University, Cairo, Egypt, Mobile: 0105055598, e-mail: [email protected]

INTRODUCTION

Burn injury is a major public health prob- Methicillin resistant Staphylococcus aureus lem in many areas of the world. Burn wound (MRSA) was first reported in the United infection is one of the most common causes Kingdome soon after clinical introduction of death and serious problems after thermal of methicillin, a beta-lactamase resistant injury (Mason, et al. 1986). Burns predispose antibiotic. Its resistance to methicillin confers to infection by damaging the protective barrier cross-resistance to other broad spectrum beta function of the skin, thus facilitating the entry of lactam antibiotics including cephalosporins pathogenic microorganisms and by inducing (Prasanna and Thomas, 1998). The concern systemic immunosuppression (Rastegar Lari, about MRSA infection in "burns-units" et al. 1998). In spite of considerable advances has been increasing since the late 1980s in the treatment of burns, infection continues (Heggers, et al. 1988 ; Matsumura, et al. 1996). to pose the greatest danger to burn patients. Approximately 73 per cent of all death within MRSA is important as a nosocomial in- the first five days post-burn have been shown fection and MRSA colonization in the burn to be directly or indirectly caused by sep- unit may lead to increased transmission of tic processes (Ekrami and Kalantar, 2007). MRSA to non burn patients in other wards

35 METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS ...

(Matsumura, et al. 1996 ; Ekrami and Ka- Statistical analysis was performed by lantar, 2007). The aim of this study was to using statistical software package (SPSS) determine the prevalence of MRSA among version10. Descriptive data of patients and patients with burn wound infection in the controls were expressed as mean ± SD, range Burn Unit in Ain Shams University Hospitals. and frequency. Analytic data by comparison between two independent mean samples was PATIENTS AND METHODS done using the Student "t" test. Quantitative data were compared by Pearson Chi-square This study was conducted from September test. P < 0.05 was considered significant. 2003 till March 2004 in the Burn Unit of Ain Shams University Hospitals. Fifty burn RESULTS patients with symptoms and signs indicative of wound infection were included in this Fifty patients (30 males and 20 females) study. They were divided into two groups: suffering from burn wound infection were in- cluded in this study. The most common cause Group A: Twenty five outpatients (19 males of burn was flame burn (27/50- 54%), followed and 6 females) with age ranging between 11 by scald burn (20/50-40%) and only 3 cases months-67 years (mean 21.5±20.34) with had flash burn (6%). Out of the50 patients; TBSA ranging between 1-10% (mean 4.2±2.8). 22 had burn of the second degree (64%), 7 had third degree (14%) and 11 (22%) had Group B: Twenty five inpatients (11 males both second and third degree burn. They and 14 females) with age ranging between 8 were divided into two groups; twenty five months–72 years (mean 28.8±20.4) with TBSA outpatients and twenty five inpatients in the ranging between 10-90% (mean 30.9±18.9). Burn unit of Ain Shams University Hospitals.

After all patients’ consent, swabs were As shown in table (1), the commonest taken from burn wounds at the 3rd day post isolate among inpatients was Ps. aerugino- burn. Swabs were cultured immediately sa (36%) followed by S.aureus (24%).The on nutrient agar, blood agar and Mac commonest isolate among outpatients was Conkey’s agar plates at 370C for 18-24 hours S.aureus (44%) followed by Ps. aeruginosa aerobically. Organisms were isolated and (40%). The isolation rate of S. aureus among identified according to standard methods studied cases was (34%). MRSA was iso- described by Collee and Marr (1996). lated from 5 out of the 25 inpatients (20%).

Disk diffusion test was performed for all Table (2) shows that the commonest Staph.aureus isolates by the method recom- cause of burn among inpatients was flame mended by Clinical and Laboratory Standard burn (72%) while the commonest cause Institute (CLST). A suspension of each isolate of burn among outpatients was scald burn was made so that the turbidity was equal to (60%). The commonest bacterial isolates 0.5 McFarland standard and then plated onto were G-ve bacilli in flame as well as in Muller-Hinton agar (Difcos) plate. Oxacillin scald burned patients. No mixed infection disk (Oxoid) was applied to each plate. After was detected among flash burned patients. incubation at 350C for 24 hours, inhibition zone size was measured. Interpretation of the re- Table (3) and Fig.(1) show that MRSA sults was performed by comparing the size of emerges among in patients only as inhibition zone with that presented in NCCLS it represented 83% of the S.aureus (2003). Zones of inhibition around oxacillin strains isolated from them, while all disks were examined carefully for evidence of the isolated S.aureus strains from of growth inside the zone (Boyce, 1998). outpatients were sensitive to methicillin.

36 DRAZ et al.

Non significant difference was detected As shown in table (5), there was no specific between incidence of MRSA infection and age significantly associated with MRSA the etiology of burn, MRSA emerged among infection. scald burn as well as flame burned patients accounting for 40% and 60% of S.aureus Table (6) indicates that the risk of developing isolated, respectively, while it was not de- MRSA infection increases significantly as tected among flash burned patients (table 4). total burn surface area (TBSA) increases.

Table 1: Incidence of different organisms causing burn wound infection

Inpatient Outpatient Total Isolated organisms No. % No. % No. %

Ps. Aeruginosa 6 24 6 24 12 24 Klebsiella 28--2 4 E. coli 28--2 4 G-ve bacilli Prot. Mirabilis 28143 6

Citrobacter frundii 28284 8

Erwinia herbicola --1412

S. aureus* 2* 8 7 28 9 18 G. +ve cocci Coagulase –ve Staph 28312510

Coagulase (-ve) Staphylococci + P. G+ve cocci + aeruginosa 28143 6

G-ve bacilli S. pyogenes + Citrobacter 14--1 2

S. aureus* + p. aeruginosa 1431248

S. aureus* + Citrobacter 14--1 2 S. aureus + S. aureus* + Klebsiella 14--1 2

G-ve bacilli S. aureus + E. coli 14--1 2

S. aureus + Enterobacter --1412

Total 25 100 25 100 50 100

X2 = 14.6 P value > 0.05 = N. sig. *= MRSA ( 20% of burn wound infection in hospitalized patients was caused by MRSA as it was isolated from 5 out of the 25)

37 METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS ...

Table 2: Correlation between burn etiology and different bacterial isolates causing burn wound infection

Cause G-ve bacilli +G S. aureus + S. aureus G+ve cocci G-ve baccilli Total of burn +ve cocci G-ve bacilli

.No % .No % .No % .No % .No % .No %

Scald 1 50 1 50 - - 2 50 1 25 5 20

Flame 1 50 - - 12 92.3 2 50 3 75 18 72 Inpatient No = 25 Flash - - 1 50 1 7.7 - - - - 2 8

G-ve bacilli +G S. aureus + S. aureus G+ve cocci G-ve baccilli Total Cause +ve cocci G-ve bacilli of burn .No % .No % .No % .No % .No % .No %

Scald 3 42.9 2 66.7 6 60 1 100 3 75 15 60

Flame 3 42.9 1 33.3 4 40 - - 1 25 9 36

Outpatient No = 25 Flash 1 14.3 ------1 4

X2 = 14 P. value > 0.05 (NS), X2 = 3.9 P. value > 0.05 (NS)

Table 3: Incidence of MRSA among isolated S. aureus.

Suspcetibility of S. Inpatient Outpatient Total aureus to methicillin No. % No. % No. % Sensitive 1 17 11 100 12 70.6 MRSA 5 83 - - 5 29.4 Total 6 100 11 100 17 100

X2 = 14 P. value < 0.05 (Sig.)

Fig. 1 : Incidence of MRSA among isolated S.aureus.

Table 4 : Correlation between incidence of MRSA and the etiology of burn

Methicillin sensitivity Methicillin sensitive S. MRSA Total Sex S.aureus

No. % No. % No. % Scald 6 50 2 40 8 47.1 Flame 5 41.7 3 60 8 47.1 Flash 1 8.3 - - 1 5.9 Total 12 100 5 100 17 100 X2 = 0.744 P. value > 0.05 (N. Sig.)

38 DRAZ et al.

Table 5: Correlation between incidence of MRSA and the age of burned Fifty patients were included in this patients study, divided into two groups, twenty five Methicillin sensitive MRSA outpatients and twenty five inpatients. S. aureus X-* 28.1 22.6 Swabs were taken from the burn wounds, SD ±23.9 ±11.9 the pattern of burn wound microbial colonization was evaluated as well as P. value >0.05 (NS) susceptibility to methicillin using disk diffusion Table 6: Correlation between incidence of MRSA and TBSA of burned method, had been done for isolated S.aureus. patients Methicillin sensitive MRSA S. aureus As regards outpatients group, Staphylo- -X 6.1 35.2 coccus aureus (44%) was the most com- mon pathogen isolated in the present work. SD ±4.4 ±18.2 This agrees with that reported by Xu et P. value < 0.05 (Sig.) al. (2002) in which S. aureus was 55%.

DISCUSSION Pseudomonas aeruginosa (40%) came next in the current study which was similar Despite significant improvement to another study done by Singh et al. (2003) in the survival of burn patients, in India where S.aureus represented (31%). infectious complications continue to be the major cause of morbidity and The prevalence of pseudomonas species mortality (Ekrami and Kalantar, 2007). among outpatients may be due to that the burn wound represents a site susceptible The burn wound is particularly susceptible to apportunistic colonization. Also burn to bacterial colonization and infection due wound is moist due to the outflow of serous to the physical disruption of the normal skin exudates at a temperature approaching barrier and the accompanying reduction 37oC which favours colonization and in cell mediated immunity (Barlow, 1994). proliferation of a variety of micro-organisms.

MRSA has evolved and became wides- Coagulase negative staphylococci which pread in the hospital environment, especially infected 12% of outpatients, came third in the in the intensive care units including those of current study, this agrees with Woods and burns, most likely due to the sustained over- Dellinger (1998) in which these organisms use of broad spectrum B-lactam antibiotics were isolated at frequency rate of 14%. (Nakhla and Sanders, 1991; Lesseva and Hadjiiski, 1996). Methicillin resistance gives Klebsiella species (19%) fo- MRSA the attributes of easy and fast transmis- llowed Ps.aeruginosa and S.aureus sibility and resistance to all the B-lactam and in Singh et al. (2003) results. Howe- easy acquisition of resistance to many other ver klebsiella species was not isola- classes of antibiotics (Gang, et al. 2000). ted from outpatients in the present study.

Infections due to MRSA are difficult to As regards the inpatients group, Ps. aeru- treat, the nature of the burn injury, plus ginosa (36%) was the most common isolate the immunological and physiological from infected burn wounds. The prevalence disturbances compound the situation of pseudomonas species in the burn unit may further. Antibiotic therapy options are be due to the fact that the organism thrives limited, Costly and likely to result in in moist environment (Atoyebi, et al. 1992). extended hospitalizations (Cook, 1998). This is in agreement with another study in Ain Shams University burn unit that pseudo- The aim of this study was to determine monas was the commonest and represented the prevalence of MRSA among patients (21%) by Nasser et al. (2003). Another ear- with burn wound infection in the Burn lier study (El-Hadi, et al. 2002) in the same Unit of Ain Shams University Hospitals. unit reported Ps.aeruginosa topping the list

39 METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS ...

of isolated organisms causing burn wound In the study done by Taylor et al. (1992) infection accounting for even higher rate In the University of Alberta hospitals, of 57%. Another study in different surgery Canada and Vindenes and Bjerkness and burn units at Cairo University Hospital (1995) in University of Bergen, Norway (Kasr El-Aini) by Abd El Tawab et al. (2003) revealed higher rates of recovery of found that pseudomonas aeruginosa was this organism in the wounds of burned the commonest and responsible for (37%) patients (47%) and (21.5%), respectively. of 21 cases with burn wounds infection. Klebsiella (12%) and E coli (12%) came four- The result also is in accordance with other th in the list of microbial isolates recovered in studies done by Revathi et al. (1998); Lari the present study. In contrast, other centers and Alaghehbandan, 2000 and Agnihotri et revealed a prevalence of Klebsiella (26.7%) al. (2004), who found that Ps. aeruginosa over pseudomonas and this considered the was the most prevalent isolate from infected former as the leading pathogen in Gram ne- burn wound with percentages (36%), (73%), gative bacillary burn wound infections (Atoye- (85%), and, respectively. In a study done by bi, et al. 1992; Ozumba and Jiburum, 2000). Ekrami and Kalantar (2007) Pseudomonas aeruginosa accounted for 37.5% of all The frequency of isolation of E.coli bacterial isolates recovered from different (12%) in the present work is relatively nosocomial infections of burn patients. higher than reported by other burn centers where the frequency of isolation of this Staphylococcus aureus (24%) was the organism didn't exceed 5% and thus it second common isolate from hospitalized wasn't considered a real threat regarding patients, this is in agreement with Gram negative bacillary invasion (Vindenes results of Kaushik et al. (2001); El-Hadi and Bjerkenes, 1995; Revathi et al. 1998; et al. (2002), and Abd El Twab et al. Ozumba and Jiburum, 2000). However, the (2003), in which S. aureus represented current result is in consistent with the result (20%), (29%), and (26%), respectively. of the study done by Nasser et al. (2003) who recovered E.coli from 13.6% isolates. On the contrary, some other studies which especially from developed countries reported In the present series, proteus species was S.aureus as the predominant organism recovered at a frequency of 8%. Previous Nakhla and Sanders (1991); Lesseva and reports concerning this organism were con- Hadjiiski (1996); Shannon et al. (1997) , the troversial. Some of them revealed a very low frequency rate of S. aureus was (69%), (31%) rate of isolation that didn't exceed 1% as in and (82%), respectively. However it differs the study by Vindenes and Bjerknes (1995). from the result of the study done by Nasser et al. (2003) where Klebsiella pneumoniae In the work on the bacteriology of burn (15.2%) was the second common isolate wounds by Revathi et al. (1998); Ozumba and S. aureus (13.2%) came fourth in the and Jiburum (2000) in Nigeria, proteus list of microbial isolates. This difference can species were recovered at frequencies be explained by the time related changes in as high as (11%) thus falling after Ps. burn wound microbial colonization, where aeruginosa and Klebsiella pneumoniae in the there is an initial predominance of Gram list of microbial isolates. However there was positive organisms, which is gradually no incidence of recovery of Proteus species superceded by the Gram negative organisms in the study done by Nasser et al. (2003). during the first week (Nasser, et al. 2003). As regards Streptococcus pyogenes, it ac- In the present work, coagulase negative counted for 4% in the present study. This is staphylococci were recovered at frequency relatively higher than reported centers where of 16% which is consistent with previous this organism didn't account for more than 2% study by Nasser et al. (2003) (11.6%). of all isolates (Revathi, et al. 1998; Ozumba

40 DRAZ et al. and Jiburum, 2000). In the study done by Nas- Several factors may account for the ser et al. (2003) in Ain Shams University burn increased incidence of MRSA colonization unit, S.pyogenes was recovered at a frequen- and infection in burned patients. Most of cy of 8.3% which is relatively higher than the those result from failure to prevent cross frequency of its isolation in the present stu- transmission in hospital. Another explanation dy. This low incidence has been considered could be that broad spectrum antimicrobial encouraging because of the deleterious role use might be correlated with incidence of of S.pyogenes in inducing skin graft failure. MRSA cases (Kaye, 2000). It might be that the more MRSA in the burn unit, the less The difference in frequency of first and second generation cephalosporins isolates may be explained by the are going to be used for prophylactic empiric difference in hospitals environment and treatment of infections because these application of infection control policies. antibiotics are not active against MRSA.

Concerning MRSA in the present work, its The demographic data in the present work incidence among inpatients was 20% group, suggests a connection between TBSA and the accounting for 83% of all isolated S.aureus risk of MRSA infection, this correlation was and emerged as a significant nosocomial also reported by Reardon et al. (1998); Fuchs pathogen. This is in accordance with other et al. (2002). Oncul, et al. (2002) in Istanbul, studies done in Egypt; in a study on the pre- Turkey also demonstrated that TBSA was a valence of MRSA infections in Ain Shams predisposing risk factor for MRSA infection. University Hospitals done by Shehata et al. (1999) the incidence of MRSA was 15% of In conclusion, methicillin resistant S. isolated organisms in the burn unit. Another aureus is a significant nosocomial pathogen study on the antimicrobial resistance in Cairo, in the Burn unit of AinShams Hospital. Egypt 1999-2000: A survey five hospital done Continuous surveillance of burn wound by El-Kholy et al. (2003) reported that 71% of infection and developing strategies for isolated S. aureus strains were methicillin re- antimicrobial resistance control is suggested. sistant. Also, about 72% of isolated S.aurues strains were resistant to methicillin in the study REFERENCES done in Cairo University by Abd El Twab et al. (2003). The incidence of MRSA infection rose Abd El Tawab, E.M., Balbaa, A. S., and Salah, from 48% in (1995) to 52% in (1996) in the N. H. 2003. Serum level of interleukin-6 in different study done in the burn center of the Sultanate types of wound infection. Ph.D. diss., Faculty of of Oman by Prasanna and Thomas (1998). Medicine, Cairo University.

In the study done by Giacometti et al. Agnihotri, N., Gupta, V., and Joshi, R. M. (2000) methicillin resistance was documen- 2004. Aerobic bacterial isolates from burn wound ted in 54.4%of isolated S.aurues strains. infections and their antibiograms--a five-year study. Burns : Journal of the International Society The incidence of MRSA in the study for Burn Injuries 30(3):241-243. made by Singh et al. (2003) in the Burn Unit in Delhi, India was 94% of isolated Atoyebi, O. A., Sowemimo, G. O., and Odugbemi, S.aureus strains. A more recent study T. 1992. Bacterial flora of burn wounds in Lagos, reported 82.5% methicillin resistance Nigeria: A prospective study. Burns : Journal of the among isolated S.aureus (Li, et al. 2007). International Society for Burn Injuries 18(6):448- 451. In the present study MRSA emerges among inpatients as a nosocomial pa- Barlow, Y. 1994. T lymphocytes and thogen, with no statistical significant di- immunosuppression in the burned patient: A fference as regards age, sex, de- review. Burns : Journal of the International Society gree and etiology of burned patient. for Burn Injuries 20(6):487-490.

41 METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS ...

Boyce, J. M. 1998. Are the epidemiology Kaushik, R., Kumar, S., Sharma, R., and Lal, P. and microbiology of methi cillin-resistant 2001. Bacteriology of burn wounds--the first three Staphylococcus aureus changing? JAMA : The years in a new burn unit at the Medical College Journal of the American Medical Association Chandigarh. Burns : Journal of the International 279(8):623-624. Society for Burn Injuries 27(6):595-597.

Collee, J. G., and Marr, W. 1996. Specimen Kaye, K. S., and Kaye, D. 2000. Multidrug- collection, culture containers and media. In Mackie resistant pathogens: Mechanisms of resistance and McCartney practical medical microbiology, and epidemiology. Current Infection Disease edited by J. G. Collee, A. G. Fraser, B. P. Marmion Reports 2(5):391-398. and A. Simmons. New York: Churchill Livingston. Lari, A. R., and Alaghehbandan, R. 2000. Cook, N. 1998. Methicillin-resistant Nosocomial infections in an Iranian burn care Staphylococcus aureus versus the burn patient. center. Burns : Journal of the International Society Burns : Journal of the International Society for for Burn Injuries 26(8):737-740. Burn Injuries 24(2):91-98. Lesseva, M. I., and Hadjiiski, O. G. 1996. Ekrami, A., and Kalantar, E. 2007. Bacterial Staphylococcal infections in the Sofia Burn Centre, infections in burn patients at a burn hospital in Bulgaria. Burns : Journal of the International Iran. The Indian Journal of Medical Research Society for Burn Injuries 22(4):279-282. 126(6):541-544. Li, M., Zhang, G. A., and Liu, Y. 2007. [Analysis El Hadi, S., Deraz, N. E., Abdel Hadi, S., and Aly, of predominant bacteria of burn infection and their H. M. 2002. Tumor necrosis factor-alpha level in resistance to antibiotics in recent years]. Zhonghua patients with burns. Egyptian Journal of Medical Shao Shang Za Zhi 23(2):91-93. Laboratory Sciences 11(1):41-53. Mason, A. D.,Jr, McManus, A. T., and Pruitt, El Kholy, A., Baseem, H., Hall, G. S., et al. 2003. B. A.,Jr. 1986. Association of burn mortality and Antimicrobial resistance in Cairo, Egypt 1999- bacteremia. A 25-year review. Archives of Surgery 2000: A survey of five hospitals. The Journal of (Chicago, Ill. : 1960) 121(9):1027-1031. Antimicrobial Chemotherapy 51(3):625-630. Matsumura, H., Yoshizawa, N., Narumi, A., et Fuchs, PCh, Kopp, J., Hafner, H., et al. 2002. al. 1996. Effective control of methicillin-resistant MRSA-retrospective analysis of an outbreak in Staphylococcus aureus in a burn unit. Burns the burn centre Aachen. Burns : Journal of the : Journal of the International Society for Burn International Society for Burn Injuries 28(6):575- Injuries 22(4):283-286. 578. Nakhla, L. S., and Sanders, R. 1991. Gang, R. K., Sanyal, S. C., Bang, R. L., et al. Microbiological aspects of burns at Mount Vernon 2000. Staphylococcal septicaemia in burns. Burns Hospital, UK. Burns : Journal of the International : Journal of the International Society for Burn Society for Burn Injuries 17(4):309-312. Injuries 26(4):359-366. Nasser, S., Mabrouk, A., and Maher, A. 2003. Giacometti, A., Cirioni, O., Schimizzi, A. M., et al. Colonization of burn wounds in Ain Shams 2000. Epidemiology and microbiology of surgical University Burn Unit. Burns : Journal of the wound infections. Journal of Clinical Microbiology International Society for Burn Injuries 29(3):229- 38(2):918-922. 233.

Heggers, J. P., Phillips, L. G., Boertman, J. A., et National Committee for Clinical Laboratory al. 1988. The epidemiology of methicillin-resistant Standards, NCCLS. 2003. Performance standards Staphylococcus aureus in a burn center. The for antimicrobial disk susceptibility tests; Approved Journal of Burn Care & Rehabilitation 9(6):610- standard. M2-A8. Clinical and laboratory standards 612. institute.

42 DRAZ et al.

Oncul, O., Yuksel, F., Altunay, H., et al. 2002. Shehata,I. H., Ibrahim,M. S., Abdel Hadi,S. I., The evaluation of nosocomial infection during and Salem,K. A. 1999. Mar. 14-18; Prevalence 1-year-period in the burn unit of a training of methicillin resistant staphylococcus aureus hospital in Istanbul, Turkey. Burns : Journal of the (MRSA) infections in Ain-Shams University International Society for Burn Injuries 28(8):738- hospitals.International annual Ain-Shams Medical 744. Congress: Health & Environment Integrity Proper Approach to Development . 22nd. Giza. Ozumba, U. C., and Jiburum, B. C. 2000. Bacteriology of burn wounds in Enugu, Nigeria. Singh, N. P., Goyal, R., Manchanda, V., et al. Burns : Journal of the International Society for 2003. Changing trends in bacteriology of burns in Burn Injuries 26(2):178-180. the burns unit, Delhi, India. Burns : Journal of the International Society for Burn Injuries 29(2):129- Prasanna, M., and Thomas, C. 1998. A profile 132. of methicillin resistant Staphylococcus aureus infection in the burn center of the Sultanate of Taylor, G. D., Kibsey, P., Kirkland, T., et al. Oman. Burns : Journal of the International Society 1992. Predominance of staphylococcal organisms for Burn Injuries 24(7):631-636. in infections occurring in a burns intensive care unit. Burns : Journal of the International Society Rastegar Lari, A., Bahrami Honar, H., and for Burn Injuries 18(4):332-335. Alaghehbandan, R. 1998. Pseudomonas infections in Tohid Burn Center, Iran. Burns : Vindenes, H., and Bjerknes, R. 1995. Microbial Journal of the International Society for Burn colonization of large wounds. Burns : Journal of the Injuries 24(7):637-641. International Society for Burn Injuries 21(8):575- 579. Reardon, C. M., Brown, T. P., Stephenson, A. J., and Freedlander, E. 1998. Methicillin-resistant Woods, R. K., and Dellinger, E. P. 1998. Current Staphylococcus aureus in burns patients--why guidelines for antibiotic prophylaxis of surgical all the fuss? Burns : Journal of the International wounds. American Family Physician 57(11):2731- Society for Burn Injuries 24(5):393-397. 2740.

Revathi, G., Puri, J., and Jain, B. K. 1998. Xu, Y., Li, T., Qi, S., et al. 2002. [An investigation of Bacteriology of burns. Burns : Journal of the bacterial epidemiology and an analysis of bacterial International Society for Burn Injuries 24(4):347- resistance to antibiotics in a burn unit from 1993 to 349. 1999]. Zhonghua Shao Shang Za Zhi 18(3):159- 162. Shannon, T., Edgar, P., Villarreal, C., et al. 1997. Much ado about nothing: Methicillin-resistant Staphylococcus aureus. The Journal of Burn Care & Rehabilitation 18(4):326-331.

43