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Year : 2015  |  Volume : 28  |  Issue : 3  |  Page : 677-684

Prevalence of multidrug-resistant bacteria isolated from patients with burn infection

1 Department of Microbiology, Faulty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Plastic Surgery, Faulty of Medicine, Menoufia University, Menoufia, Egypt

Date of Submission11-May-2014
Date of Acceptance10-Jul-2014
Date of Web Publication22-Oct-2015

Correspondence Address:
Asmaa S Sleem
Department of Microbiology, Faulty of Medicine, Menoufia University, Shebin El Kom, Menoufia Governorate
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/1110-2098.167888

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The aims of the study were to determine bacterial pathogens frequently causing burn infections and their antimicrobial susceptibility patterns, to estimate the prevalence of multidrug resistance (MDR) among the isolated pathogens, and to evaluate the different risk factors for the development of burn wound infection.
Infection in burn patients remains the significant source of morbidity and mortality. The aggressive use of antimicrobials has improved survival but led to an increased colonization and infection of pathogens that resist current therapies.
Materials and methods
The study was carried out by collecting swabs from 105 burnt patients during the period from October 2012 to November 2013. Semiquantitative assessment of bacterial growth was performed to distinguish between bacterial colonization and infections. MDR strains were detected including methicillin-resistance and vancomycin-resistance staphylococci and Gram-negative bacilli extended-spectrum b-lactamases and metallo-b-lactamases producers by standardized methods.
Burn wound infections were polymicrobial in 26.6% of cases. Staphylococcus aureus was the most common aerobic isolate (32.4%). Among S. aureus, 76.5% were MDR strains, 73.5% were methicillin-resistant, and 17.6% were vancomycin resistant. Coagulase-negative staphylococci (CoNS) were represented by 16.2%. About 47% of CoNS strains were MDR strains, 47% were methicillin-resistant CoNS, and 23.6% were vancomycin-resistant CoNS. All Gram-negative bacteria isolated from burn wounds were MDR. Extended-spectrum b-lactamases were detected in 58.5%, whereas metallo-b-lactamases were detected in 43.4% of Gram-negative bacteria. The risk factors for burn wound infections were young age, low socioeconomic status, abuse of invasive procedures and antimicrobial, prolonged hospital stay, and improper control of burn-associated comorbidities.
The study highlights the high prevalence of MDR bacteria infecting burn wound in our hospitals.

Keywords: Burn wound infections, extended-spectrum b-lactamase, metallo-b-lactamase, multidrug-resistance bacteria, methicillin-resistant Staphylococcus aureus, vancomycin-resistant Staphylococcus aureus

How to cite this article:
Melake NA, Eissa NA, Keshk TF, Sleem AS. Prevalence of multidrug-resistant bacteria isolated from patients with burn infection. Menoufia Med J 2015;28:677-84

How to cite this URL:
Melake NA, Eissa NA, Keshk TF, Sleem AS. Prevalence of multidrug-resistant bacteria isolated from patients with burn infection. Menoufia Med J [serial online] 2015 [cited 2022 Nov 29];28:677-84. Available from: http://www.mmj.eg.net/text.asp?2015/28/3/677/167888

  Introduction Top

A burn is a type of injury to flesh or skin caused by heat, electricity, chemicals, or radiation. Globally, about 11 million people seek medical treatment, and 300 000 die from burns each year. Despite considerable advancements in burn wound care and infection control practices, infection remains the leading cause of death [1].

Burns can be classified by depth, mechanism of injury, extent, and associated injuries. The first-mentioned classification is based on the depth of injury; first-degree burns involve superficial skin layers; second-degree burns extend deeper in the skin, whereas third-degree burns involve underlying tissues. The extent of burn injury as total burned surface area (TBSA%) is used recently for severity classification [2].

Burn surfaces are initially sterile, but within 48 h the wound is typically colonized by Gram-positive skin flora (Staphylococcus spp.), bacteria present in sweat glands or deep within hair follicles. After 48-72 h, wounds become colonized with endogenous Gram-negative bacteria from the patient's respiratory and gastrointestinal tract, such as Pseudomonas aeruginosa and Klebsiella pneumonia [3].

Burn patients are infected by hospital-acquired bacteria by various invasive and noninvasive procedures. Early diagnosis of microbial infections and screening for drug resistance is aimed to institute the appropriate antibacterial therapy and to avoid further complications. Nowadays, majority of the bacteria that cause burn infection in hospitals are resistant to at least one of commonly used drugs [4].

Among the Gram-positive cocci, methicillin-resistant Staphylococcus aureus (MRSA) is the most important nosocomial pathogen. Sensitivity of MRSA to only a few antibacterial agents limits therapeutic options and poses a threat to the patient life [5].

Extended-spectrum b-lactamases (ESbLs) and metallo-b-lactamases (MbLs)-producing organisms pose a major problem for treating burn victims. ESbLs are b-lactamases capable of conferring bacterial resistance to penicillins, first, second, and third-generation cephalosporins, and aztreonams, but not to cephamycins or carbapenems. MbL is a group of carbapenem-hydrolyzing b-lactamase but not aztreonams and resists currently available b-lactamase inhibitors, but are inhibited by chelating agents such as ethylenediamine tetra-acetic acid (EDTA) [6],[7].

This study was performed at Menoufia University Hospital to determine bacterial pathogens frequently causing burn infections in our hospital and their antimicrobial susceptibility patterns, to determine the prevalence of multidrug resistance (MDR) among the isolated pathogens, and to evaluate the different risk factors for the development of burn wound infection.

  Materials and methods Top

This study included 105 patients (59 male patients and 46 female patients) admitted to Burn Unit of Menoufia University Hospital. With patients concent personal history was taken including age, sex, residence, socioeconomic status, occupations, duration of hospitalization, and special habits such as smoking. Clinical history was taken carefully to determine degree of burn, TBSA%, exposure to invasive procedures (catheters, cannula, and/or intravenous lines), and associated complications and comorbidities.

Burn wound swabs were taken from all patients following cleaning of any remnant ointments. All swabs were inoculated on blood agar, MacConkey agar, nutrient agar, and mannitol salt agar. Semiquantitative assessment of bacterial growth was performed using the four quadrant method to distinguish bacterial colonization from infection [8]. Isolation and identification were carried out using standard bacteriological methods [9].

Detection of methicillin-resistant staphylococci was carried out by cefoxitin disk diffusion method (30 μg). Vancomycin-supplemented agar screening test (4-8 μg/ml) was used for all staphylococcal isolates to detect their vancomycin susceptibility pattern and the results were confirmed by vancomycin minimum inhibitory concentration (MIC) tube dilution method (256-0.5 μg/ml) [9].

Screening for ESbLs production was performed by disk diffusion test using ceftazidime (30 μg), cefotaxime (30 μg), ceftriaxone (30 μg), and aztreonam (30 μg). Suspected ESbL-producing Gram-negative bacilli were confirmed by double disk synergy test (DDST) and confirmatory clavulanate combined disk test. In DDST, amoxicillin/clavulanic acid (20/10 μg) and cefotaxime (30 μg) disks were placed at a distance of 30 mm on an inoculated agar plate and incubated aerobically at 37°C for 18-24 h. Organisms that showed a clear extension of cefotaxime inhibition zone toward the disk containing clavulanate were considered as synergy (ESbL producer). Antibiotic disks of ceftazidime (30 μg), ceftriaxone (30 μg), and aztreonam (30 μg) were also placed on the plate. In isolates that were suspicious for harboring ESbLs, but were negative using the standard distance of 30 mm between disks, the test was repeated using closer distance of 20 mm [10]. In confirmatory clavulanate combined disk, ceftazidime (30 μg) and ceftazidime/clavulanic acid (30/10 μg) were used. Organism was considered as ESbL producer, if there was at least 5 mm increase in diameter of ceftazidime/clavulanic disk than that of ceftazidime disk alone. The same was performed with cefotaxime (30 μg) and cefotaxime/clavulanic acid (30/10 μg) [9].

Screening for MbLs production was performed by disk diffusion test. Reduced susceptibility to one or more carbapenems (meropenem and ertapenem) and one or more of the indicator cephalosporins (cefotaxime, ceftriaxone, ceftazidime, and cefoperazone) indicates MbL-producer organism [9]. Suspected MbLs were confirmed by imipenem/EDTA combined disk test and modified Hodge test (MHT; cloverleaf test). In imipenem/EDTA combined disk test, two (10 μg) imipenem disks were placed on the plate at a distance of 25 mm apart, and 4 μl of sterile EDTA solution was added to one of the imipenem disk and incubated aerobically at 37°C for 18-24 h. If the increased inhibition zone with imipenem/EDTA disk was at least 7 mm than imipenem disk alone, it was considered as MbL positive [4].

In MHT, the indicator organism (Escherichia coli ATCC 25922) was inoculated on Mueller-Hinton agar plate. One disk of ertapenem or meropenem (10 μg) was placed on the plate and 3-5 colonies of test or quality control organisms (K. pneumonia ATCC BAA-1705, MHT positive, and K. pneumonia ATCC BAA-1706, MHT negative) were picked and inoculated in a straight line out from the edge of the disk. The streak was at least 20-25 mm in length. After incubation, the plate was examined for enhanced growth around the test or quality control organism streak at the intersection of the streak and the zone of inhibition (cloverleaf-like indentation), which indicate positive for carbapenemase production [9].

  Results Top

A total of 105 burnt patients were included in this study (59 male patients and 46 female patients). The mean age of the patients was 15 ± 17.6 years. Burn injuries were more common among young age group (<20 years old) (70.4%) with statistical significant difference (P < 0.05) between different age groups regarding burn injuries but not regarding degree of burn. Burn injuries affect patients of low socioeconomic status (75.2%) and patients associated with comorbiditis (28.6%) with statistical significant difference (P < 0.05). Nonsignificant statistical data were found between degrees of burn injuries and sex, occupation, and smoking. The majority of burnt patients' injuries (70%) were of the second degree, whereas 18% were of the third degree, and only 11% were of the first degree [Table 1].
Table 1: Risk factors for burn injuries of studied patients

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Fire (68%) and scalds (22%) were the main etiological agents for burn injuries. Chemicals caused 6% and electrical injuries caused about 4% of burns [Figure 1].
Figure 1: Etiology of burn injuries among studied patients.

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The mean TBSA% in this study was 19.4 ± 17%. There was significant statistical correlation between TBSA% and duration of hospitalization (P < 0.05).

Regarding bacterial growth assessment using four quadrant method, bacterial colonization was detected when bacterial growth was restricted to first quadrant or first and second quadrants, whereas extended growth to third or third and fourth quadrants means bacterial infections. About 36% of patients had burn wound infections, whereas 39% of patients had burn wound colonization. About 25% of burnt patients had no bacterial growth in their burn wounds [Figure 2].
Figure 2: Semiquantitative assessment of bacterial growth.

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Bacterial colonization was detected in 45.7% of patients with complications, whereas bacterial infection was detected in 44.3%. Significant association was found between presence of complications and bacterial growth on burn wounds (P < 0.05) [Table 2].
Table 2: Bacterial growth and resistant pattern with respect to complications, invasive procedures, and duration of hospital stay

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About 74% of patients had bacterial growth on their burn wounds related to using invasive procedures (36% were infected and 38% were colonized). One burnt patient had bacterial colonization without using invasive procedure. About 20% of burnt patients using invasive procedures revealed no bacterial growth [Table 2].

There was significant statistical correlation between bacterial infection (52%) and duration of hospitalization (>3 weeks) (P < 0.05) [Table 2].

About 63% of bacterial growth was MDR isolates. Ninety-seven percent of them were isolated from complicated cases and 100% from patients using invasive procedures with significant statistical relationship. There was a significant statistical relationship between MDR bacterial affection and prolonged hospital stay (P < 0.05) [Table 2].

The predominant pathogens detected in our study were Staphylococcus aureus (32.4%), Pseudomonas spp. (27.6%), and coagulase-negative staphylococci (CoNS) (16.2%). Gram-negative bacilli caused 50.6% of burn wound infections. No bacterial growth was detected among 24.8% burnt patients. Fifty-one of the cultures showed a single bacterial growth, 26 cultures showed two bacterial isolates, and two of the cultures showed polymicrobial community consisting of three species.

Regarding MDR bacteria distribution, Gram-positive bacteria presented 32.4% (24.8% S. aureus and 7.6% CoNS), whereas Gram-negative bacteria presented 50.5% (27.6, 9.6, 6.6, 2.8, 1.9, and 1% for Pseudomonas spp., Klebsiella spp., Proteus spp., Enterobacter spp., Serratia marcescens, and Citrobacter spp., respectively).

About 76.4% of S. aureus isolates and 47.05% of CoNS strains were MDR staphylococci. About 73.5% of S. aureus were MRSA, whereas 47.1% of CoNS were methicillin-resistant CoNS.

By vancomycin agar screening method, 32.4 and 41.2% of S. aureus isolates and CoNS were resistant to vancomycin, respectively. By confirmatory MIC tube dilution method, S. aureus and CoNS showed intermediate resistance to vancomycin by 14.7 and 17.6% and resistance by 17.7 and 23.6%, respectively.

For ESbLs production, 67.9% of Gram-negative bacilli isolated from burnt patients were ESbL producers by disk diffusion method and 58.5% by confirmatory combined disk method compared with only 5.6% by DDST with statistical significant difference between results (P < 0.05). Pseudomonas spp. were the predominant ESbL producer by 61.3% followed by Klebsiella spp. (16.1%), Acinetobacter spp. (9.6%), Proteus spp. (9.6%), and finally Enterobacter spp., which represented 3.4% of ESbL producers in this study.

For MbLs production, 77.4% of Gram-negative isolates were MbLs producers detected by combined disk screening test compared with 43.4% MbL producers detected by confirmatory MHT with significant statistical difference (P < 0.05). In addition, Pseudomonas spp. were the main MbL-producing Gram-negative bacteria [Figure 3],[Figure 4] and [Figure 5] and [Table 3].
Figure 3: Antimicrobial resistance results in Gram-positive bacteria.

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Figure 4: Antimicrobial sensitivity results in Gram-negative bacteria.

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Figure 5: Modified Hodge test. (a) Metallo-¦Â-lactamase (M¦ÂL) is negative control strain; (b) M¦ÂL is positive control s train; (c, d) M¦ÂL are positive isolated strains.

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Table 3: Distribution of antibiotic resistance patterns of isolated bacteria from burnt patients (N = 105) by different susceptibility methods

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  Discussion Top

In the present study, the mean age of burnt patients was 15 ± 17.6 years, which was in agreement with the result of Alghalibi et al. [11]. Higher mean age (44 years old) was found in the study by Keen et al. [12]. Burn injuries were significantly common among our young age group (<20 years old) (70.4%).

In this study, 56% of burnt patients were male, whereas 44% were female, matching the results of Vural et al. [13] and Alghalibi et al. [11]. Percentage of male burnt patients was increased because male patients are more exposed to burns and wear clothes that catch fire easily. In addition, mostly restaurant workers are men engaged in cooking [11]. In contrast, Rajupt et al. [14] showed that burn infection in female patients was (60%) more than in male patients (40%).

No causal relationship was found between patient's job and burn injuries in this study, revealing that 68.6% of burn injuries were not related to work, which was in agreement with the study by National Burn Repository and American Burn Association [15].

Strong association was found between burn injuries and low socioeconomic status people who could ill afford treatment or medical insurance, which was in agreement with published results of the WHO [16] and Chamania et al. [17].

Smoking was not a significant risk factor for burn injuries in our study, which was in contrast to the study by WHO [16] documenting that smoking is a risk factor for burn injury, wound infection, and delayed wound healing. This difference may be due to low percentage (11.4%) of smokers in our study, as 42.8% of burnt patients were female individuals and 70.4% of patients were younger than 20 years of age. No significant data were found between degrees of burn injuries and residence and associated comorbidities.

The majority of burnt patients' injuries (70%) were of the second degree in agreement with study by Vural et al. [13]. These results can be explained as third -degree burns are mostly fatal, whereas first-degree burns are usually treated at home.

In this study, flame was the main cause of burn injuries (68%) followed by scalds (22%), chemicals (6%), and finally electrical injuries. National Burn Repository [15] documented similar results, whereas Othman and Kendrick [18] found that 75% of burns were due to scalds, 15% were due to flames, and 10% were due to contact with hot objects.

Duration of hospitalization was significantly related to TBSA% with consequently increased burn wound infection incidence. This coincides with the results of Vural et al. [13].

Regarding bacterial growth results, 36% of our patients had burn wound infections, which was in agreement with Mahmoud et al.'s [19] result. Strong correlation was revealed between bacterial growth on burn wounds and burn-associated complications, use of invasive diagnostic and therapeutic procedures, and prolonged hospitalization. The same results were reported by Vinodkumar et al. [4].

This study showed that 48.6% of the aerobic bacterial isolates from infected burn wounds were monomicrobial, 26.6% were polymicrobial, and 24.8% showed no bacterial growth. These results are in agreement with others [17],[20].

In this study, the most frequently isolated bacteria were S. aureus (32.4%), Pseudomonas spp. (27.6%), and CoNS (16.2%). These bacteria are normal flora in healthy person; when they get breaks on skins and soft tissue in any of mechanical cases or burns, they can easily disseminate and cause infection [21]. Moreover, these bacteria are commonly found in the hospital environment, which might increase wound infection rate and cross-contamination among admitted patients. Other isolates were Klebsiella spp. (9.5%), Proteus spp. (6.7%), Acinetobacter spp. (2.9%), Enterobacter spp. (1.9%), Citrobacter spp. (1%), and S. marcescens (1%).

In this study, 76.4% of S. aureus isolates were MDR staphylococci. These results matched with 65.2% MDR S. aureus detected by Yishak and Biruk [22], but were higher than that found by Azene and Beyene [23] (52.7%) and lower than 100% MDR reported by others [24]. The possible explanation for such disparity might be difference in study population.

In the present study, 73.5% of S. aureus isolates were MRSA. This was in agreement with results of Khanal and Jha [21]. However, this was much lower than 100% MRSA reported by Yishak and Biruk [22] and incomparably higher than Chamania et al.'s [17]findings. The cause of resistance might be because of mecA gene or other mechanisms of resistance such as impermeability of the membrane, deposition of high fat cover on cell wall, and deformation/mutation of porine proteins.

In this study, 32.4% of S. aureus were completely or intermediately resistant to vancomycin using both vancomycin agar screening method and MIC tube dilution confirmatory method. Similar results were reported by Mimejad et al. [25] (40%). Lower results were obtained by Godebo et al. [20] (16.4%).

About 47.1% of CoNS isolates in this study were methicillin-resistant, which is in agreement with 45% found by Rahman et al. [26]. Higher rate (80%) was recorded by Mimejad et al. [25]. MDR rate of CoNS in our study was 47.05%, and 41.2% of CoNS were vancomycin intermediately or completely resistant, which is higher than 28.6% detected by Godebo et al. [20] for MDR CoNS and 0% for vancomycin-resistant CoNS recorded by the same study. The variations are due to differences of local conditions, such as climate or microbial prevalence, but others are likely to be caused by different prevention protocols, topical and systemic treatment of burn wounds, study population, and sampling methodology.

Such incidence of vancomycin-resistant staphylococci in hospital as well as in community is alarming because vancomycin is one of the main antimicrobial agents available to treat life-threatening infections with MRSA.

All Gram-negative strains in our study were MDR. This was in agreement with Vinodkumar et al.'s [4] study. Lower rates were obtained by Chamania et al. [17] and Mahmoud et al. [19] who reported 63.5 and 52%, respectively.

All Gram-negative bacilli were screened for ESbL production by simple disk diffusion method. Positive ESbL producers by screening test were confirmed by DDST and combined disk method. Combined disk method is a phenotypic confirmatory and reference test recommended [9] for the detection of ESbL. The clinical strains producing SHV-6 ESbL and AmpC type b-lactamase producers would not be detected by DDST; hence, combined disk method is the best confirmatory test [27].

About 58.5% of Gram-negative bacilli were ESbL producers by combined disk confirmatory method. Pseudomonas spp. (61.3%) were the predominant ESbL producer followed by Klebsiella spp. (16.1%), Acinetobacter spp. (9.6%), and Proteus spp. (9.6%). These results are in agreement with others [4],[17],[19]. Lower percentages were recorded by Shrestha et al. [28] (18%). This discrepancy can be attributed to the continuous development of MDR strains in different parts of the world and also to a considerable geographic difference in the prevalence of ESbLs in different countries.

All confirmatory tests depend on detecting synergy between clavulanic acid and the indicator cephalosporin(s) used in the primary screening. M'Zali et al. [27] published that use of ceftazidime (30 μg) and ceftazidime/clavulanate (30/10 μg) disks detected 86% of ESbL-producers; use of cefotaxime (30 μg) and cefotaxime/clavulanate (30/10 μg) disks detected 66% of ESbL producers; and use of both disk pairs detected 93% of ESbL producers. As a general rule, laboratories should test all isolates of Gram-negative bacilli from in-patients using both ceftazidime (the best indicator for TEM and SHV-derived ESbLs) and cefotaxime (the best indicator for CTX-M types). Any organism showing reduced susceptibility to cefotaxime and/or ceftazidime should be investigated for ESbL production. Use of only one disc combination might fail to detect ESbL production resulting in under-reporting of prevalence. Hence, it is better to use both disk types as was performed in our study.

About 67.9% of Gram-negative bacilli isolated from burnt patients in this study were ESbL producers by disk diffusion test compared with 58.5% by confirmatory combined disk test with no significant difference between both tests. Surprisingly, only 5.6% of Gram-negative bacteria were ESbL producers by DDST. In the DDST method, distance of disk placement is not standardized and there are individual variations in the interpretation of results. Garrec et al. [29] had found that the number of positive controls that tested negative at 25 mm was positive at reduced distances. All strategies indicate that the addition of an ESbL-specific second test was always superior to DDST alone for confirming the absence of ESbL in all the strains.

These results coincide with the results of Jain and Mondal [30] with 82% ESbL producers by disk diffusion test compared with 58% by confirmatory combined disk test; in addition, Goyal et al. [31] found that 55% of bacterial isolates were ESbL producers by disk diffusion test compared with 64.5% by confirmatory combined disk test.

MbLs has emerged worldwide as powerful resistance determinants in Gram-negative bacteria [4].

In this study, only Gram-negative bacilli resistant to imipenem were screened for MbLs production using imipenem/EDTA combined disk method and confirmed by MHT as recommended [9]. About 45% Pseudomonas spp., 60% Klebsiella spp., 28.6% Proteus spp., and 33.3% Acinetobacter spp. isolates were resistant to imipenem as recorded by others [4].

Imipenem/EDTA combined disk method is the best method for screening for MbLs production in Pseudomonas spp., Acinetobacter spp., and enterobacteriaceae family. This method provides simple, inexpensive, and reproducible functional screen for MbLs-producing bacteria. MbLs-producing Gram-negative bacteria detected by combined disk method presented 77.4% in our study, which matched with 76.2% detected by Behera et al. [32].

The CLSI published a recommendation that enterobacteriaceae with reduced disk diffusion inhibition zones be tested for the production of carbapenemases by means of the MHT [9]. MbLs-producing Gram-negative bacteria detected by MHT presented 43.4% in our study, which coincides with 33% detected by Pasteran et al. [33] using the same test.

The difference in the percentages of MbL producers detected by combined disk test and those revealed by MHT was expected, because the sensitivity and specificity of MHT for detecting low-level MbL production are unknown. No data exist on the usefulness of MHT for the detection of carbapenemase production in nonfermenting Gram-negative bacilli [9]. About 68.3% of MbL producers detected by combined disk test in our study were nonfermenting Gram-negative bacilli including Pseudomonas spp. and Acinetobacter spp.

Risk factors for burn wound infection in our hospital should be evaluated and controlled, mainly those concerned with abuse of invasive procedures, unneeded prolonged hospital stay, and improper control of burn-associated complications. Internationally recommended strategies for training, education, and resource allocation by the hospital administration are suggested to ensure a comprehensive burn care program from prevention to rehabilitation.

  Acknowledgements Top

Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]

  [Table 1], [Table 2], [Table 3]


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