Summary
The objective of this study was to analyze the incidence of hospital acquired infections (HAIs) in burn patients, and to determine the principle infection sites and the sensitivity profile of the microorganisms to antimicrobials. This is a retrospective cohort study, conducted in a specialized centre for the treatment of burns from January 2009 to December 2013. The sample consisted of 404 patients, divided into two groups: the first group comprised 142 patients without infection, and the second group was made up of 262 patients who had acquired HAIs. There was a predominance of males in both groups. Mean age of the patients without infection was 37 years (SD 14.89), and 38 years (SD 15.78) for the patients with HAIs. Of the 523 infections observed in this study, pneumonia was the most frequent with 216 (41%) cases, followed by urinary tract infections with 137 (26%) episodes. The pathogens identified were Acinetobacter baumannii (93, 40%), Pseudomonas aeruginosa (50, 21%) and Klebsiella (pneumoniae/oxytoca) (23, 10%) and were resistant to most common antimicrobials. In the study population, no pathogens resistant to vancomycin were found. The present study describes high rates of infection in burn victims. Pneumonia was the most frequent site of infection, followed by urinary tract infections caused respectively by non-fermenting bacteria with a high frequency of antimicrobial resistance.
Keywords: burn units; cross infections; infection,; epidemiology,; bacterial drug resistance
Abstract
L’objectif de cette étude était d’analyser l’incidence des infections nosocomiales chez les patients brûlés, de déterminer les principaux sites infectés et d’analyser les profils de sensibilité des bactéries. Cette étude rétrospective a été conduite dans un CTB entre janvier 2009 et décembre 2013. L’échantillon de 404 patients a été réparti en 2 groupes: le premier, de 142 patients, sans infection (SI) et le second de 262 patients infectés (I). Les hommes prédominaient dans les 2 groupes. L’âge moyen des patients SI était de 37 +/- 14,89 ans, celui des patients I de 38 +/- 15,78 ans. Les 216 pneumonies représentaient la majorité (41%) des 523 infections relevées, suivies par les infections urinaires (137, 26%). Acinetobacter baumannii (93 isolats; 40%), Pseudomonas æruginosa (50; 21%) et Klebsiella sp. (23; 10%) étaient les plus fréquents et les plus résistants. Nous n’avons pas isolé de bactérie VAN R. On constate une prévalence élevée des infections chez les brûlés, principalement en sites pulmonaire et urinaire, souvent par des BGN non fermentants à résistance élevée.
Introduction
In burn treatment centres (BTCs), healthcare-associated infections (HAIs) are responsible for 75% to 80% of deaths.1 There is a greater incidence of sepsis in patients with burns compared to other types of trauma.1 Infection can lead to deterioration in wound healing and serious systemic complications. Due to advances in medical technology and improvements in surgical techniques, there has been a reduction in mortality in this population. In contrast to these advances, these patients are exposed to invasive procedures and prolonged periods of hospitalization, increasing their exposure to HAIs.2 Among the reasons for the increased susceptibility of burn patients to infections, we highlight the loss of the first line of defence against microbial invasion caused by disruption of the skin barrier, the presence of devitalized tissue, alterations in the immune system, alterations in the cellular and humoral immune response, gastrointestinal bacterial translocation, prolonged hospitalization and invasive therapeutic and diagnostic procedures.1
The most frequent HAIs in BTCs are skin infections (wounds), pneumonia, urinary tract and bloodstream infections.3 The most common microorganisms colonizing burns are Staphylococcus aureus, Pseudomonas aeruginosa, Klebsiella spp, Enterobacter spp and Acinectobacter baumannii, among others.4
The objective of this study was to analyze the incidence of HAIs in hospitalized patients in an intensive care unit (ICU) of a BTC over a period of five years, as well as determine the most frequent infection sites and the sensitivity of the microorganisms to antimicrobials.
Methods
This was a retrospective cohort study conducted in the ICU of the BTC at a University Hospital. The sample consisted of all consecutive patients admitted to the ICU of the BTC from January 2009 to December 2013.
The BTC is composed of six ICU beds and 10 ward beds, one emergency room and two operating rooms. ICU support includes individualized rooms, fluid resuscitation guided by the modified Brooke formula, individualized sedation and analgesia and nutritional support. At ICU admission, patients are evaluated by plastic surgery staff and undergo their first debridement procedure. Daily dressing changes are performed by applying 1% silver sulfadiazine and using essential fatty acids (EFA) or silver-containing dressings. EFA oils are used to treat wounds mainly in Latin America. EFA products contain one or two EFAs, added to other substances such as vitamin A, vitamin E and soy lecithin, or they integrate medium-chain triglyceride formulations.5 All these components work in a way that increases immune response and stimulates the healing process through angiogenesis and epithelialization. Prophylactic antibiotics are not standard practice in our centre. If the patient can be transported to the operating room, dressing changes are performed under general anaesthesia; otherwise, dressing changes are performed in the ICU bed under endovenous analgesia. Tangential excision and skin grafting are performed when clinical and hemodynamic status is established and infection is not present. Ten to 15% of the burned area is usually operated upon in one sitting.
The patients were divided into two groups: one group was made up of patients diagnosed with HAIs according to the criteria of the Centers for Disease Control and Prevention6 and the other group was composed of patients who had not developed HAIs. The exclusion criteria were patients under the age of 18 years, hospitalizations of less than 24 hours, and hospitalization for causes other than burns.
Data collection on admission included clinical and demographic data, type and extent of the burn and causal agent. The data for calculating severity scores, Acute Physiology and Chronic Health Evaluation (APACHE II)7 and Abbreviated Burns Severity Index (ABSI)8 were collected at admission. In addition, data were collected for the organ dysfunction score Sequential Organ Failure Assessment (SOFA).9 The use of therapeutic interventions was evaluated using the Therapeutic Intervention Scoring System (TISS 28).10 Clinical outcome at hospital discharge was classified as survivor or non-survivor. The extent of the burn was calculated by the Plastic Surgeon using the Lund and Browder table11 on the day the patient was admitted. The classification of severity into great, medium or small burns was carried out according to the criteria of the Project Guidelines of the Brazilian Society of Plastic Surgery.12 For the microbiological study, only the first culture and related antibiogram performed to diagnose HAIs during the first seven days from initiation of antibiotics was considered. The definition criteria of the CDC (Centers for Disease Control and Prevention) were adopted for urinary tract infection (UTI), urinary tract infection related to the catheter (UTIRC), pneumonia associated with mechanical ventilation (VAP), bloodstream infection (BSI), bloodstream infection related to the catheter (BSI-RC), skin and soft tissue infection (SSTI) and other infections.6 The technical realization and analysis of antibiograms followed the recommendations of the Clinical and Laboratorial Standards Institute (CLSI).13 The analysis of the profile of multidrug resistance to antimicrobials followed the standards of the CDC.14
The results of the continuous variables were described as mean, standard deviation, median and interquartile range and presented in tables. The Student t test was used to compare the means of continuous variables with normal distribution and homogeneity of variances, and a nonparametric test (Mann-Whitney) was used for data with non-normal distribution and/or heterogeneity of variances. The categorical data were presented as frequency through tables and graphs. The categorical variables were analyzed using the chi-square test. Hospital mortality was described as frequency and through analysis of the Kaplan-Meier survival curve. The significance level was set at 5% and analyses were performed using MedCalc for Windows, version 9.3.2.0 (MedCalc Software, Mariakerke, Belgium).
The study was approved by the Research Ethics Committee of the State University of Londrina, which received the certificate of Ethics Assessment (CAAE), protocol number 13327013.8.0000.523.
Results
During the study period, 1,644 burn victims aged zero to 83 years were hospitalized. Of this total, 487 were admitted to intensive care beds in the Burn Treatment Centre. Of these 487 admissions, 63 patients were excluded as they were under 18 years old, 16 patients were in hospital for less than 24 hours and 4 were admitted for diagnoses other than acute burns. Thus, the study sample consisted of 404 cases of burns, divided into two groups: one group of 142 patients who did not develop HAIs, and another group of 262 patients who developed one or more HAIs.
The clinical and epidemiological characteristics of the sample (Table I) showed that males predominated in both groups. Fire was the most frequent cause of burns and alcohol the main causal agent, with no significant differences between the two groups. However, mortality was higher in the group that developed HAIs (p = 0.022).
Table I. Comparison of clinical characteristics and outcomes between groups with and without infection.

Table II compares age and prognostic scores between the study groups. Mean age was similar for both groups. Regarding total burned surface area (TBSA), higher mean TBSA was observed in patients with HAIs. Mean ABSI, APACHE, SOFA and TISS scores were also higher in the group with HAIs.
Table II. Comparison of age and prognostic scores between groups with and without infection.

Among the patients with HAIs, the body regions most affected by burns were the upper limbs (80.2%), followed by the trunk (76.7%) and face (64.5%). Regarding the depth of the burns, 85.5% of patients with HAIs had third-degree injuries. With respect to ventilatory support, invasive mechanical ventilation was required in 156/262 (59.5%) cases, for an average of 18 (SD 21.77) days. A tracheostomy was performed in 72 (27.5%) patients. Acute renal failure occurred in 91 (34.7%) cases and 58 (22.1%) required dialysis. In total, 523 infections were diagnosed in the group of patients with HAIs. The first infection for each patient was diagnosed after a mean of 9.4 (SD 8.8) days from the burn injury. Pneumonia was the most common infection (41%), followed by urinary tract infection (26%), skin and soft tissue infection (21%) and blood stream infection (5%). A total of 327 cultures were performed in patients with HAIs, with 425 pathogens isolated. The most commonly isolated pathogens were: Acinetobacter baumannii (64%), Pseudomonas aeruginosa (53.5%), Klebsiella spp (37%) and Candida spp (48%). Fig. 1 presents the frequency of microorganisms according to the site of infection. Regarding patterns of antimicrobial resistance, 36% of S. aureus isolated were Methicillin-resistant but no Vancomycin resistant microorganisms were detected. Among gram-negative bacteria, extensive drug resistance was detected in 92% of A. baumanii, 50% of P. aeruginosa and 30% of Klebsiella spp (Table III). The most commonly prescribed antimicrobials for treatment of HAIs were Carbapenems (42.7%), Polymyxins (31.7%) and Glycopeptides (23.1%) (Fig. 2).
Fig. 1. Distribution of the most frequently isolated microorganisms per site of infection.

Fig. 2. Distribution of antimicrobials most frequently used in infections in the study population.

Table III. Distribution of the principle pathogens isolated and antimicrobial resistance in patients with infection in an intensive care burn unit of a university hospital.

Discussion
The results of this study demonstrate a high frequency of HAIs in adult burned patients admitted to the ICU. The most frequent pathogens were non-fermenting gram negative bacteria, Enterobacteriacea and Candida spp, with high frequency of resistance to antimicrobials, leading to the use of antimicrobials with a broad spectrum of activity. Patients in the present study presented similar clinical and demographic characteristics to other epidemiological studies.15-18 Burned surface area is one of the risk factors described for the development of infection complications, together with length of hospitalization,19 which is consistent with the results of the present study, since the majority of the patients were considered severely burned and had a prolonged period of hospitalization. The most frequent HAI identified in the present study was pneumonia. Non-fermenting gram-negative bacteria and Enterobacteriacea were the most commonly isolated etiological agents from this site, like the results reported by other authors. 20,21 In the urinary tract infection site, the most commonly found etiological agents were gram-negative bacteria, followed by fungi, also like other reports.22,23 A study performed in burn response units in the US showed that in 44% of the units P. aeruginosa was the most prevalent gram-negative pathogen, followed by A. baumannii and Enterococcus spp..22 In Bulgaria,24 the most common pathogen in the Sofia Burns Centre was Staphylococcus aureus, followed by A. baumannii and P. aeruginosa. Publications identify these three species of bacteria, with differences in their order of frequency, as the principle microorganisms that lead to HAIs in burn victims. These differences may be due to local conditions, such as a hot and humid climate.25
A. baumannii has been identified as a common etiologic agent in wound infections in burn patients and is associated with a high fatality rate.26,2726,27 In Asiatic studies, where the climate is hot and humid,20,26 A. baumannii was primarily responsible for colonization and hospital-acquired infections in burn patients. This climate-related condition was also found in a French study that recorded an increase in A. baumannii infections during the summer.27
In the present study, infections caused by A. baumannii and P. aeruginosa demonstrated high antimicrobial resistance to more than three classes of antimicrobials. The global profile of resistance varies between institutions and countries.28 Recent data from the CDC demonstrate increasing resistance of A. baumannii to many antimicrobials, including Carbapenems, in American hospitals. Approximately 63% of A. baumannii and 13% of P. aeruginosa were resistant to multiple antimicrobials.29
Burn patients present conditions that favour the development of infections, such as immunosuppressive alterations and wounds that predispose them to bacterial growth,3 which account for 75% of deaths in these patients.1 The management of patients with burns requires ongoing multidisciplinary commitment to controlling infections. The prevention of infections in severe burns includes early surgical excision, use of topical and systemic antimicrobials,30 associated with an antimicrobial stewardship program. The proper use of antibiotics in burn patients is an important part of the treatment and their use should be thoroughly evaluated so as not to increase microbial resistance to antibiotics, and ensure greater effectiveness.31
Conclusion
The infection rate in the patients studied can be considered high. The most frequent infection was pneumonia, followed by urinary tract infection caused by A. baumannii and P. aeruginosa with a high frequency of resistance to antimicrobials.
References
- 1.Macedo JL, Rosa SC, Castro C. Sepsis in burned patients. Rev Soc Bras Med Trop. 2003;36(6):647–652. doi: 10.1590/s0037-86822003000600001. [DOI] [PubMed] [Google Scholar]
- 2.Guggenheim M, Zbinden R, Handschin AE, Gohritz A. Changes in bacterial isolates from burn wounds and their antibiograms: a 20-year study (1986-2005). Burns. 2009;35(4):553–560. doi: 10.1016/j.burns.2008.09.004. [DOI] [PubMed] [Google Scholar]
- 3.Araújo SA. Infecção no paciente queimado. Lima Junior EM SM (ed): ‘Tratado de Queimaduras. 2006 [Google Scholar]
- 4.Macedo JL, Santos JB. Bacterial and fungal colonization of burn wounds. Mem Inst Oswaldo Cruz. 2005;100(5):535–539. doi: 10.1590/s0074-02762005000500014. [DOI] [PubMed] [Google Scholar]
- 5.Ferreira AM, de Souza BMV, Rigotti MA, Loureiro MRD. The use of fatty acids in wound care: an integrative review of the Brazilian literature. Rev Esc Enferm. 2012;46(3):745–753. doi: 10.1590/s0080-62342012000300030. [DOI] [PubMed] [Google Scholar]
- 6.Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control. 2008;36(5):309–332. doi: 10.1016/j.ajic.2008.03.002. [DOI] [PubMed] [Google Scholar]
- 7.Knaus WA, Draper EA, Wagner DP, Zimmerman JE. APACHE II: a severity of disease classification system. Crit Care Med. 1985;13(10):818–829. [PubMed] [Google Scholar]
- 8.Tobiasen J, Hiebert JM, Edlich RF. The abbreviated burn severity index. Ann Emerg Med. 1982;11(5):260–262. doi: 10.1016/s0196-0644(82)80096-6. [DOI] [PubMed] [Google Scholar]
- 9.Vincent JL, Mendonca A, Cantraine F, Moreno R. Use of the SOFA score to assess the incidence of organ dysfunction/failure in intensive care units: results of a multicenter, prospective study. Working group on “sepsis-related problems” of the European Society of Intensive Care Medicine. Crit Care Med. 1998;26(11):1793–1800. doi: 10.1097/00003246-199811000-00016. [DOI] [PubMed] [Google Scholar]
- 10.Miranda DR, Rijk A de, Schaufeli W. Simplified Therapeutic Intervention Scoring System: the TISS-28 items—results from a multicenter study. Crit Care Med. 1996;24(1):64–73. doi: 10.1097/00003246-199601000-00012. [DOI] [PubMed] [Google Scholar]
- 11.Lund CC, Browder NC. The estimation of areas of burns. Surg Gym Obs. 1944;79:35–38. [Google Scholar]
- 12.Piccolo NS, Serra MCVF, Leonardi DF, Lima Jr EM . Projeto Diretrizes Queimaduras: Diagnóstico e Tratamento Inicial. 2008:1–14. [Google Scholar]
- 13.Clinical Laboratory Standards Institute: Performance Standards for Antimicrobial Susceptibility Testing; Seventeenth Informational Supplement. CLSI. 2005 [Google Scholar]
- 14.Sievert DM, Ricks P, Edwards JR, Schneider A. National Healthcare Safety Network (NHSN) Team and Participating NHSN Facilities. Antimicrobial-resistant pathogens associated with healthcare-associated infections: summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2009-2010. Infect Control Hosp Epidemiol. 2013;34(1):1–14. doi: 10.1086/668770. [DOI] [PubMed] [Google Scholar]
- 15.Santucci SG, Gobara S, Santos CR, Fontana C, Levin AS. Infections in a burn intensive care unit: experience of seven years. J Hosp Infect. 2003;53(1):6–13. doi: 10.1053/jhin.2002.1340. [DOI] [PubMed] [Google Scholar]
- 16.Soares MJL, Santos JB. Nosocomial infections in a Brazilian Burn Unit. Burns. 2006;32(4):477–481. doi: 10.1016/j.burns.2005.11.012. [DOI] [PubMed] [Google Scholar]
- 17.Taghavi M, Rasouli MR, Boddouhi N, Zarei MR. Epidemiology of outpatient burns in Tehran: an analysis of 4813 cases. Burns. 2010;36(1):109–113. doi: 10.1016/j.burns.2009.02.011. [DOI] [PubMed] [Google Scholar]
- 18.Lacerda LA, Carneiro AC, Oliveira AF. Estudo epidemiológico da Unidade de Tratamento de Queimaduras da Universidade Federal de São Paulo. Rev Bras Queimaduras. 2010;9(3):82–88. [Google Scholar]
- 19.Macedo JLS, Rosa SC, Santos JB. Complicações infecciosas e fatores preditivos de infecção em pacientes queimados. Rev Soc Bras Cir Plastica. 2007;22(1):34–38. [Google Scholar]
- 20.Chim H, Tan BH, Song C. Five-year review of infections in a burn intensive care unit: high incidence of Acinetobacter baumannii in a tropical climate. Burns. 2007;33(8):1008–1014. doi: 10.1016/j.burns.2007.03.003. [DOI] [PubMed] [Google Scholar]
- 21.Oncul O, Ulkur E, Acar A. Prospective analysis of nosocomial infections in a burn care unit, Turkey. Indian J Med Res. 2009;130(6):758–764. [PubMed] [Google Scholar]
- 22.Barros SKB, Kerbauy G, Dessunti EM. Infecção do trato urinário relacionada ao cateter: perfil de sensibilidade antimicrobiana. Rev Rene. 2013;14(5):1005–1013. [Google Scholar]
- 23.Apostopoulou E, Raftopoulos V, Filntisis G, Kithreotis P. Surveillance of device associated infection rates and mortality in 3 Greek intensive care units. Am J Crit Care. 2013;22(3):12–20. doi: 10.4037/ajcc2013324. [DOI] [PubMed] [Google Scholar]
- 24.Levesa M, Arquirova M, Nashev V. Nosocomial infections in burns patients: etiology, antimicrobial resistance, means to control. Ann Burns Fire Disasters. 2013;26(1):5–11. [PMC free article] [PubMed] [Google Scholar]
- 25.Guggenheim M, Zbinden R, Handschin AE. Changes in bacterial isolates from burn wounds and their antibiograms: a 20 years study (1986-2005) Burns. 2009;35(4):553–560. doi: 10.1016/j.burns.2008.09.004. [DOI] [PubMed] [Google Scholar]
- 26.Siau H, Yuen KY, Wong SS, Ho PL, Luk WK. The epidemiology of acinetobacter infections in Hong Kong. J Med Microbiol. 1996;44(5):340–347. doi: 10.1099/00222615-44-5-340. [DOI] [PubMed] [Google Scholar]
- 27.Fournier PE, Richet H. The epidemiology and control of Acinetobacter baumannii in health care facilities. Clin Infect Dis. 2006;42(5):692–699. doi: 10.1086/500202. [DOI] [PubMed] [Google Scholar]
- 28.Dijkshoom L, Nemec A, Selfert H. An increasing threat in hospitals: multidrug-resistant Acinetobacter baumannii. Nat Rev Microbiol. 2007;5(12):939–951. doi: 10.1038/nrmicro1789. [DOI] [PubMed] [Google Scholar]
- 29.Centers for Disease Control and Prevention. Antibiotic Resistance Threats in the United States, 2013. Available from:http://www.cdc.gov/drugresistance/pdf/ar-threats-2013-508.pdf . [Google Scholar]
- 30.Rossi LA, Menezez MAJ, Gonçalves N, Ciofi-Silva CL. Cuidados locais com as feridas das queimaduras. Rev Bras Queimaduras. 2010;9(2):54–59. [Google Scholar]
- 31.Edwards-Jones V, Dawson MM, Childs C. A survey into toxic shock syndrome (TSS) in UK Burns Units. Burns. 2000;26(4):323–333. doi: 10.1016/s0305-4179(99)00142-4. [DOI] [PubMed] [Google Scholar]
