Bang R.L.^1,2, Sharma P.N.³, Bang S.⁴, Mokaddas E.M.⁵, Ebrahim M.K.¹, Ghoneim I.E.¹

¹ Al Babtain Centre for Plastic Surgery and Burns, Faculty of Medicine, Kuwait University, Kuwait
² Department of Surgery, Faculty of Medicine, Kuwait University
³ Health Sciences Computer Centre, Kuwait University
⁴ Al Bahar Eye Centre, Ibn Sina Hospital, Kuwait
⁵ Department of Microbiology, Ibn Sina Hospital, Kuwait

SUMMARY. One hundred and sixty burn patients suffering from septicaemia, hospitalized in the Al-Babtain Centre burns unit, Kuwait, between June 1992 and May 2001, were studied. Thirty-two patients (20%) had scalds and 128 (80%) flame burns, thus representing a ratio of 1:4 among septicaemic patients. There were 20 males (62.5%) in the scald group, compared to 73 (57%) with flame burns. Flame burns were significantly higher (p < 0.01) among non-Kuwaiti patients. The mean ages of the scald and flame burn patients were respectively 6.2 and 31.5 yr. The mean total body surface area burn in scalds was 20% and in flame burns 49%, which was significantly higher (p < 0.001). The 34 septicaemic episodes in 32 scald patients and 212 such episodes in 128 flame burn patients showed a significantly higher incidence in the latter group. The majority of septicaemic episodes, in scalds (82.4%) and flame burns (57.6%), were due to gram-positive organisms, mainly methicillin-resistant Staphylococcus aureus and methicillin-resistant Staphylococcus epidermidis. A significantly increased number of episodes were due to S. aureus (p < 0.001) and Enterococcus (p < 0.05) in scald patients. More surgical operations were performed in flame burn patients and survival increased significantly with an increasing number of grafting sessions (p < 0.001). The mean hospital stay in flame burn patients (56 days) was significantly higher than in scald patients (23 days) (p < 0.001). It is significant to record that all the 38 deaths (29.7%) were in flame burn septicaemic patients (p < 0.001). The scald and flame burn patients were quite distinct in their demographic and clinical characteristics. The flame burn patients were more vulnerable to septicaemia, with a high risk of mortality.

Introduction

Scalds and flame are the main aetiology, and septicaemia a serious complication, in the majority of burn patients.1-5 Burn care over the years has improved owing to better fluid resuscitation6,7 and management of pulmonary inhalation injury8-10 and to adequate nutrition11-13 but burn wound infection and septicaemia still remain a major problem.14-20 Loss of the skin barrier and the depleted immune system make burn patients vulnerable to systemic infection.21-23 The presence of extensive raw surfaces, the moist environment due to the outflow of serous exudates, the presence of necrotic tissue, the large cutaneous bacterial load, prolonged hospitalization, and invasive diagnostic and therapeutic procedures further aggravate morbidity and mortality in burn victims.3,6-8,15-26 The types of burn, either scald or flame, may influence the occurrence of septicaemia. Early wound coverage may reduce the risk of the septicaemia23-26 and is therefore desirable, but it may not be possible in every case. The outcome of septicaemic patients depends on early detection and prompt treatment.1-5,8,10,17,19,20.23-30 This study was undertaken to evaluate the incidence, the demographic and clinical differences, and the outcome in scald and flame burn patients who had septicaemia.

Patients and methods

One hundred and sixty-six patients had septicaemia among the 2082 cases treated as in-patients at the Burns Unit of Al-Babtain Centre, Kuwait, during the nine-year period from June 1992 to May 2001. Out of these, 160 (96.4%) had either scald or flame burns, and they were studied with regard to their demographic and clinical features.

Estimation of the burn surface, as per the Lund-Browder chart, and clinical assessment of depth were carried out on admission in each case. The patients were resuscitated according to the Parkland formula and, in the presence of inhalation injury, they were intubated and ventilated until recovery or otherwise. Swabs from the wound(s), nose, throat, and perineum were taken on admission, and subsequent wound swabs were taken from the burn wound twice a week as per microbiological surveillance protocol in all the burn patients. The use of prophylactic antibiotic penicillin until December 1992 and of amikacin plus piperacillin from January 1993 to December 1996 was the standard criterion. However, since January 1997 onwards, this has been completely stopped in burn patients. The use of antibiotics in burn wound sepsis and septicaemia was strictly governed by an antibiotics policy started in 1992, and revised regularly. The complete blood count and the biochemical profile were checked at least twice a week throughout treatment.

The burn wounds were dressed either with Sofratulle or Flamazine (1% silver sulphadiazine), and early excision of 15-20% burn area in one operation was carried out for deep burns. A mixture of 1 kcal/ml was given orally to all patients, from day 3 post-burn, as nutritional support, and part of the requirement was given parenterally.

The clinical features of hyperpyrexia or hypothermia, disorientation, circulatory embarrassment, leucocytosis, thrombocytopenia, petechial haemorrhages, early eschar separation, and increasing oedema in unburned areas were suggestive of septicaemia. In suspected cases two blood cultures were taken from different sites at hourly intervals. A positive blood culture associated with clinical septicaemia was mandatory for diagnosis. These patients were treated initially with empirical antibiotic therapy, which was modified if the blood culture report so indicated.

Statistical analysis

Data were recorded for analysis regarding age, sex, nationality, cause and percentage of burn, response of resuscitation, inhalation injury, intubation, septicaemia on post-burn day, number of septicaemic episodes, organisms responsible in each episode, therapy, and patient outcome.

SPSS (PC version 11.0) software was used for data management and the statistical analysis. Descriptive statistics are presented as mean ± standard error. Mean values were compared using the t-test and ANOVA with the post hoc Bonferroni test for multiple comparisons. Chi-square or Fisher’s exact test was applied for any association and trend. The odds ratio (OR) and 95% confidence interval are shown for micro-organisms in scald and flame burns. A probability level of p < 0.05 was considered significant.

Results

One hundred and sixty burn patients, who had septicaemia amongst 2082 cases treated, i.e. 7.7%, comprised 32 patients (20%) with scalds and 128 with flame burns (80%), equal to a ratio of 1:4. The mean ages of the scald and flame burn patients were respectively 6.2 and 31.5 yr (p < 0.001). Children less than 5 years of age constituted 81% of the scald cases compared to only 9% of the flame burns. In flame burns, the 15-44 yr age group comprised 63% of the patients. There were 20 males (62.5%) in the scald group compared to 73 (57%) in the flame burn group. The sex distribution showed male predominance in both groups (Table I).

Flame burns were significantly more frequent (p < 0.01) among non-Kuwaiti patients.

Various clinical characteristics of scald and flame burn patients are presented in Table II. All the patients but one in the scald group were satisfactorily resuscitated whereas 23 patients with flame burns had a difficult resuscitation (p < 0.05) by the Parkland formula. Thirty-nine patients with flame burns had inhalation injury versus none in the scald group (p < 0.001). Forty-seven patients with flame burns were intubated compared to only one patient with scalds (p < 0.001) during their stay in hospital. Distribution according to the various blood groups showed no significant differences between scald and flame burn patients. From the aspect of mortality the death of 38 patients with flame burns versus none with scalds was highly significant (p < 0.001).

The mean total body surface area (TBSA) burn of 49% (range, 6-95%) in flame burns was significantly higher than the 20% (range, 3-60%) of scald burns (p < 0.001). It was noted that only four scald patients had more than 30% burns compared to 89 (69.3%) flame burn patients and that none of the scald patients had Ž 70% burns (Table III). The mean hospital stay in flame burn patients (56 days) was significantly higher (23 days) than in scalds (p < 0.001). It is significant to note that 45 flame burn patients stayed in hospital more than 60 days, while none of the scald patients, irrespective of burn percentage, stayed that long (Table III).

The 34 septicaemic episodes in the 32 scald patients and the 212 such cases in the 128 flame burn patients indicate a significantly higher incidence in the latter group (p < 0.01). The mean number of septicaemic episodes was respectively 1.06 and 1.66 for scald and flame burn patients. The mean post-burn day for such episodes was 8 days in scalds and 15 days in flame burns. The comparison of time and number of episodes showed that late occurrence and multiple episodes were a significant feature of flame burns (Table IV) (p < 0.01).

The majority of septicaemic episodes were due to gram-positive organisms, mainly methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-resistant Staphylococcus epidermidis (MRSE) (Table V), in both scald and flame burns patients. In scalds, micro-organisms were found to be significantly more common in septicaemic episodes due to Staphylococcus aureus (p < 0.001; OR = 8.9) and Enterococci (p < 0.04; OR = 3.9). Candida was responsible for two septicaemic episodes in flame burn patients. Flame burns presented mixed organisms in 14.6% of cases.

Twenty-one scald patients and 97 flame burn patients underwent a variable number of surgical procedures (Table VI), with a significantly higher number in the flame burn group (p < 0.001). Forty-four patients with flame burns were operated on three or more times compared to one patient with scald burns. The survivor proportion of burn patients increased significantly with an increased number of grafting sessions (p < 0.001).

It is significant that all the 38 deaths (29.7%) occurred in flame burn septicaemic patients (p < 0.001). Multiple organ failure was the main cause of death (27 cases = 71%), followed by cardiorespiratory failure (6 cases = 16%) and acute renal failure (5 cases = 13%). The mean burn percentage of patients who died (69%) was significantly higher (p < 0.001) than that of patients who survived (40%).

Discussion

This study was carried out in order to analyse the various demographic and clinical features of septicaemic patients who sustained scald and flame burn injuries over a 9-yr period. Bacterial invasion of the burn wound and wound infection are quite common despite the numerous antibiotics available and excellent overall burn care. Wound infection and septicaemia remain a common source of morbidity and mortality in severely burned patients.4,5,10,14-20,27-32 The incidence of clinical and positive blood culture septicaemia is well documented in various types of burn.

Positive blood cultures are diagnostic for septicaemia but are sometimes plagued by false positive results.33 The high incidence of scald septicaemia in children up to five years of age and the similar high incidence of flame burn septicaemia in adults in the 15-44 yr age group show their vulnerability.4,5,17-20,28-30 This can be explained by the corresponding incidence of burn injuries in the population.17,34 With regard to flame burn patients, the high incidence of septicaemia amongst males and non-Kuwaitis may have been due to domestic circumstances and occupational activities.4,17,34 Septicaemia can occur both in scalds and flame burns even with smaller burn percentages, but flame burns in more than 30% TBSA are more likely to be thus affected, as observed in the present study.

Resuscitation by the Parkland formula, in both scald and flame burns, was found to be adequate in the majority of septicaemic patients,6,7,35 except in the presence of an inhalation injury.8-10 Extensive burns and associated inhalation injury are the important risk factors for the occurrence of septicaemia in flame burns, as observed in the present study.4,8-10,17,28-30 Difficult resuscitation was a particular feature of flame burn septicaemic patients who had inhalation injury and needed intubation and ventilation. Endotracheal tubes are commonly considered a source of infection, especially in flame burn patients4,8-10,18,27 but this proved to be contrary to the findings of the present study.

Intravascular lines, though considered to be risk factors for both and flame burn septicaemia, cannot be incriminated as the source of infection, because the intravascular sites did not indicate thrombophlebitis and most of the intravascular cannulae were found to be negative on culture.4 It is worth pointing out that no particular influence of the blood group was observed in either group of septicaemic patients.

Silver sulphadiazine (1% Flamazine), which is widely used as a topical agent, was found to be effective in both groups, as the microbiological surveillance showed,4,14,18,19,36 although one may be inclined to use other agents in superficial burn scald septicaemia. Nutritional requirements in both scald and flame septicaemia are related to burn severity and were found to be managed well by 1 kcal/1ml oral mixture up to about 2500 kcal, with an additional intravascular amount in such patients.4,11-13,22,25 This nutritional management may have contributed to the better outcome of these patients.

The antibiotic prophylaxis generally used in both scald and flame septicaemic patients has no beneficial role to play, as noted in our earlier study.4,17 It was found that prophylactic antibiotics increased neither the incidence of septicaemia nor mortality4,17,28-30 and we therefore feel that the use of prophylactic antibiotics played no role in the incidence and outcome of our burn patients.

It is generally thought that the occurrence of septicaemia during the first week post-burn is rare,4 but in fact a good number of both scald and flame burn patients present septicaemia in the first week.1,4,16,17,19,28 Late occurrence and multiple septicaemic episodes were only observed in flame burn patients, and this is a significant clinical observation in terms of the management of burn patients.4,15-17,20,27-30 However, the majority of scald and flame burn septicaemic episodes occurred during the first two weeks post-burn, as observed by Wurtz et al.15 The microbiological surveillance policy, continuous clinical observation, and the timely culture of blood specimens were found to be quite effective for the early detection of scald and flame burn septicaemia. Furthermore, the wound was probably the source of the spread of infection to the blood stream, since most of the septicaemic patients’ blood isolates were similar to those that colonized or infected the burn wound surface.

Gram-positive septicaemia was common in both groups, but more so in scald patients. The maximum number of septicaemic episodes due to MRSA in both scald and flame burn patients shows that this burns unit has become endemic for this organism - others have made similar observations.2,4,14-20,27-30,32 The long hospital stay and the exposure to numerous antibiotics may have favoured MRSA nosocomial infection in these patients.15,30,37-41 The increasing incidence of MRSE septicaemia in scald and flame burn patients suggests that this organism should be regarded as a potential pathogen for burn septicaemia, and should not be ignored as a skin contaminant.4,17,28,30 Enterococcus has not been reported as a frequent cause of septicaemia in the past, but recent studies indicate an increasing incidence of enterococcal bacteraemia in burn patients, and the presence of a 4.3 percentage of septicaemia due to Enterococcus in this study supports observations made by other researchers.

The declining incidence of Pseudomonas septicaemia in scald and flame burns, as noted in this study, may be due to the increasing frequency of gram-positive cocci as nosocomial pathogens and to the frequent use of antibiotics that are effective against Pseudomonas.4,16-20,43 Acinetobacter, another important gram-negative organism, has shown increased septicaemic frequency as a lone pathogen or as a part of polymicrobial septicaemia in flame burn patients due to burns Ž 50% TBSA, prolonged hospital stay, use of multiple antibiotics, and delayed wound closure.4,21-28,31,32,34 The above factors may have favoured burn wound colonization by the multiresistant nosocomial pathogens in the unit, leading to polymicrobial sepsis. Two septicaemic episodes, both in flame burn patients, showed its emergence in this unit.

Mortality (23.5%) occurred only in flame burn patients and it is significant to note that this figure was lower that that observed in our other studies.4,17 The low mortality may be attributed to adequate resuscitation, continuous clinical and microbiological surveillance, and prompt blood culture, leading to the rapid detection of aetiology, the institution of appropriate antibiotics, nutritional support, and early excision and wound coverage.

Conclusion

Morbidity and mortality in burn patients depend on burn severity, resuscitation measures, wound coverage, wound sepsis, and the management of septicaemia, if it occurs. Flame burn patients are far more liable to develop septicaemia because of their extensive burn surface, deep wounds, and associated inhalation injury.

RÉSUMÉ. Les Auteurs ont étudié 160 patients brûlés atteints de septicémie hospitalisés dans l’unité des brûlures du Centre Al-Babtain, Koweït, entre juin 1992 et mai 2001. De ces patients, 32 (20%) présentaient des brûlures par ébouillantement et 128 (80%) des brûlures par flammes (c’est-à-dire un rapport, chez les patients septicémiques, d’un à quatre). Le groupe ébouillantement comprenait 20 patients mâles (62,5%) et celui des flammes 73 (57%). Les brûlures par flammes étaient significativement plus fréquentes (p < 0.01) chez les patients non-koweïtiens. Les âges moyens des patients ébouillantés et les patients brûlés par les flammes étaient respectivement de 6,2 et 31,5 ans. La surface corporelle moyenne brûlée était de 20% pour les ébouillantements et de 49% pour les flammes, une valeur significativement plus élevée (p < 0.001). Les 34 épisodes septicémiques chez 32 patients ébouillantés et les 212 épisodes analogues chez 128 patients atteints par les flammes ont démontré une incidence significativement plus élevée dans le deuxième groupe. La plupart des épisodes septicémiques (ébouillantements, 82,4%; flammes, (57.6%) étaient causées par les organismes à Gram positif, principalement Staphylococcus aureus resistant à la méticilline et Staphylococcus epidermidis résistant à la méticilline. Un nombre significativement augmenté d’épisodes était causé par S. aureus (p < 0.001) et Enterococcus (p < 0.05) chez les patients ébouillantés. Un nombre plus élevé d’interventions chirurgicales a été effectué chez les patients brûlés par les flammes et la survie augmentait en manière significative en proportion de l’incrément des sessions de greffe (p < 0.001). La durée moyenne de l’hospitalisation chez les patients brûlés par les flammes (56 jours) était significativement plus élevée par rapport aux patients ébouillantés (23 jours) (p < 0.001). Il est significatif que tous les 38 décès (29,7%) se sont vérifiés chez les patients septicémiques atteints de brûlures par flammes (p < 0.001). Les patients brûlés par ébouillantement et les patients brûlés par flammes étaient tout à fait distincts pour ce qui concerne leurs caractéristiques démographiques et cliniques. Les patients qui présentaient les brûlures par flammes étaient plus vulnérables à la septicémie, avec un risque élevé de mortalité.

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