Bums (1992) 18,(6), 448-451 Printed in Great Brifuin
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Bacterial flora of burn wounds in Lagos, Nigeria: a prospective study 0. A. Atoyebi’, G. 0. A. Sowemimo1*2 and T. Odugbemil*’ ‘Department
of Surgery, Lagos University
Teaching Hospital and ‘College of Medicine,
A prospective study of bum wound sepsis was carried ouf on 31 consecutive patients with fresh bums. Wound swab culfures were assessed af weekly intervalsfor 5 weeks. The sfudy revealed that while 96.7 per cent of bum wounds were sferile on admission, bacterial colonization reached 80.6 per cent within the first week affer admission. Although the Gram-negative organisms, as a group, were more predominant, Staph. aureus (38.2 per cent) was the most prevalent organism in thejrst week. It was however surpassed by Pseud. aeruginosa from the second week onwards. Anaerobes were conspicuous by their absence. Similarly, /I-haemolytic streptococcus was not isolated from any patient. Proteus mirabilis was unusually preponderant, forming 19.4 per cent of all isolates. The antibiotic senstivify pattern showed resistance of most of the organisms zo ampicillin. Only 15 per cent ofstaphylococci were sensitive to cloxacillin. Most of the organisms cultured (93.5 per cent) were sensitiveto ceftazidime.
Introduction Bacterial infection continues to be a major problem in the management of the burned patient despite recent advances in treatment. The natural defence of the human epidermis is lost in bums and therefore infection of the bum wounds with the danger of systemic invasion remains a threat until all wounds are healed. MacMillan (1982) aptly stated that ‘nowhere in Medicine and Surgery has the changing parade of pathogens been more evident than in bums’. Strep. pyogenes was the most frequently recognized cause of bum wound sepsis in the early part of the century (Cruickshank, 1935). Over the years, however, Pseud. aeruginosu and Sfapk. uureus have become the most frequently isolated organisms in most bum units (Greco et al., 1979). It is generally known that the spectrum of infective agents varies from time to time and from place to place. It is therefore desirable fo carry out periodic reviews of the bacterial flora of bum wounds in all centres so that preventive strategies could be modified as necessary. Previous reports on bum sepsis in Nigeria were all retrospective in nature (Coker et al., 1983; Sowemimo, 1983; Mabogunje et al., 1987), and no sequential analysis has been reported to date to determine the period of emergence of the different microorganisms. The aim of this prospective study is therefore to assess the current bacterial flora of bum wounds in Lagos, Nigeri.a. 0 1992Butteworth-Heineman 0305-4179/92/060448-04
Ltd
University
of Lagos, Nigeria
Materials and methods All patients withfvesk burns who were admitted to the Lagos University Teaching Hospital between mid December 1988 and mid June 1989 were included in the study. The patients were all managed in the general surgical and paediatric wards, as there is no specialized bum unit. Wound swabs were taken from the bum wounds on admission and at weekly intervals during change of dressings for 5 weeks or until all bum wounds were healed. Each wound swab was immediately placed in 10ml of Stuart’s transport medium (Oxoid) and promptly sent to the laboratory for processing. The samples were processed by conventional methods of isolation of aerobic and anaerobic organisms and sensitivity tests to antibiotics were done by the disc diffusion methods. Organisms difficult to identify were further characterized and confirmed using the Analytical Profile Index (API) method. The results obtained were then analysed.
Results A total of 31 patients were investigated. Their ages ranged from 11 months to 44 years (mean 18.13 years f s.d. 13.06). The male to female ratio was 1.82 : 1 and the percentage of total body surface burned varied from 15 to 60 per cent (mean 29.71 per cent f s.d. 10.88). The burning agent was predominantly thermal in nature (77.4 per cent). The other causes were chemical agents (16.1 per cent) and electrical bums (6.5 per cent). Tables I-111 summarize the findings. Table I shows the outcome of the wound swabs culture. Almost all (96.7 per cent) of the wound swabs were reported sterile on admission but by the end of the first week, 80.6 per cenf of the wound swabs had microorganisms isolated from the wound. In subsequent weeks the surface contamination rate decreased progressively as the wounds healed. Table II shows the isolates from the bum wounds at weekly intervals postbum. The predominant organism was staphylococcus species which formed 41.2 per cent of all isolates at the end of the first week after admission. Pseud. aeruginosu formed 25.8 per cent, coliforms formed 8.8 per cent of all isolates, while diphtheroids, citrobacter, proteus and some unidentified non-lactose fermenters formed 5.9
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Atoyebi et al.: Bacterial flora of bum wounds
Table I. Result of bacteriological cultures Time of sampling (weeks) 5th
4th
Result
Admission
1St
2nd
3rd
Sterile
30 (96.7)
6 (19.4)
9 (34.6)
9 (40.9)
13 (65)
10 (76.9)
1 (3.3)
16 (51.6)
8 (30.8)
10 (45.5)
6 (30)
2 (15.4)
9 (34.6)
3 (13.6)
31 (100)
31 (100)
26 (100)
22 (100)
Single isolate Multiple isolates Total
1 (5)
1 (7.7)
20 (100)
13 (100)
Results shown are numbers with percentages in parentheses.
Table II. Number of organisms isolated from wound cultures Total
Time of sampling (weeks) Admission
1st
2nd
-
13 1 1 -
4 1 3
Staph. aureus Staph. epidermidis cc-haemolytic streptococcus p-haemolytic streptococcus Pseud. aeruginosa Klebsiella aerogenes Proteus spp. Coliforms Unidentified non-lactose fermenters Diphtheroids Citrobacter Anaerobes
1
-
2 3 2 2 2
1
34
5th
No.
-
18 2 6
19.4 2.1 6.4
1 2 2
30 10 18 3 2 2 2 0
32.3 10.7 19.4 3.2 2.2 2.2 2.2 0
5
93
100
4 2 3
-
-
27
17
%
-
11 4 4
-
Total
4th
-
-
8
-
3rd
-
-
-
9
Table III. Pattern of antibiotic sensitivities of organisms isolated from patients
Staphylococci (n = 20) Ampicillin Cloxacillin Ceftazidime Chloramphenicol Colistin Co-trimoxazole Erythromycin Gentamicin Kanamycin Nitrofurantoin Streptomycin Sulphafurazole Tetracycline
0 3 20 3
(0.0) (15) (106, (15)
5 (25) 11 (55)
-
1 (5)
14 (70)
Streptococci (n =6) 1 0 0 1
(16.7) (0.0) (0.0) (16.7)
-6 (100.0) 5 (83.3) -
Pseudomonas (n = 30)
Unidentified non-lactose fermenters (n =2)
30 (100) -
2 (100.0)
28 (93.3) 0 (0.0) 25 (83.3) 0 (0.0) 0 (0.0)
1 (10.0)
0 (0.0)
0 (0.0) -
Klebsiella (n=lO)
10 (100.0)
2 (1 OO,.O) 0 (0.0) 0
Proteus (n=18)
Citrobacter (n =2)
10 (55.6) -
2 (100.0)
-6 (0.0)
1 (33.3) -
18 (100.0)
4 (40.0) 6 (60.0)
< (22.2) 10 (55.6) -
(0.0) 0 (0.0) 1 (50.0)
-9 (90.0) -
14 (77.8)
8 (80.0)
15 (83.3)
0 (0.0) 0 (0.0)
0
(0.0) 3 (30.0)
0 (0.0) 7 (38.9)
-6 (0.0)
1
(100.0) 0 (0.0)
3 (100) 1 (33.3)
;
-LI (0.0) 0 (0.0)
Coliforms (n =3)
2 (0.0) 0 (0.0) 0 (0.0)
0
(66.7)
(0.0) 0 (0.0) 0 (0.0)
Results shown are numbers with percentages in parentheses,
per cent each. /?-haemolytic streptococcus was not isolated at all but there was one isolate (2.9 per cent) of an r-haemolytic streptococcus. However, by the end of the second week, Fseud. mruginosa had become more predominant (40.7 per cent), while staphylococci formed only 18.5 per cent of all isolates. The Gram-negative organisms, as a group, predominated by the end of the second week (70.3 per cent) with the appearance of Klebsiella aerogenes and Proteus spp., surpassing Pseud. aerugjnosa in frequency in weeks 3 and 5 postbum. Altogether, the Gram-negative organisms were the most frequently isolated organisms
from the bum wound, with Fsed. aemginosa forming 32.3 per cent of all isolates. Staphylococci followed with 21.5 per cent preponderance and this was closely followed by Proteus species (19.4 per cent) and Klebsielh aerogmes (10.8 per cent). Anaerobic microorganisms were conspicuously absent. Table III shows the pattern of antibiotic sensitivities of the organisms isolated from the burned patients. The staphylococci were completely resistant to ampicillin, and suprisingly only 15 per cent were sensitive to cloxacillin. However, sensitivity of staphylococci to ceftazidime was 100 per cent. Streptococcus spp. were only 16.7 per cent
450
sensitive to ampicillin and were indeed resistant to cloxacillin and ceftazidime. They were 83.3 per cent sensitive to erythromycin and 100 per cent sensitive to co-trimoxazole. Isolates to Psed. afT@nosa were 83.3 per cent sensitive to gentamycin, 93.3 per cent sensitive to colistin and 100 per cent sensitive to ceftazidime. They were resistant to ampicillin and tetracycline.
Discussion The results of this study have further confirmed that contamination of the bum wound is almost the rule rather than an exception in major bums. By the end of the first week after admission, 80.6 per cent of the patients studied had microorganisms isolated from their bum wounds. This is in agreement with the findings of Yemul and Sengupta (1979), who reported a surface contamination rate of 87 per cent in the first week after admission. This is inspite of the fact that all burned patients were routinely cleaned with an antiseptic solution (chlorhexidine) on admission and had I per cent silver sulphadiazine cream applied to their wounds. A significant number of contaminated wounds showed a polymicrobial ecology with multiple isolates (week I, 36 per cent; week 2, 52.9 per cent), but this diminished as the time after injury increased. There is therefore no doubt that efforts at combating infection in bums must remain a continuing preoccupation. Staph. aureus was the most prevalent single organism (38.2 per cent) colonizing the bum wounds in the first week following bum injuries. There is no reported sequential analysis in this environment for comparison, but our findings agree with those from a similar study in India (Yemul and Sengupta, 1979). It is obvious that measures directed at combating infection in the early postbum period must take care of Stuph. uwew, if they are to be effective. Silver sulphadiazine is therefore an appropriate topical agent to use in bum wound dressing during the first week postbum, whereas 11.1 per cent mafenide acetate would be inappropriate in view of its ineffectiveness against staphylococci. Psettd. aemginosa which came second in the first week surpassed staphylococci in all subsequent weeks. A notable finding in the study is the relatively high incidence of Protetls mirubilis among the isolates in the whole study and among organisms isolated in week 3 in particular. I? mirubilis formed 19.4 per cent of all isolates and this is quite different from all previous reports from Lagos (OmoDare and Akande, 1969; Coker et al., 1983; Sowemimo, 1983). Altogether, Psard. uemginosa (32.5 per cent) was the most predominant organism in the bum wounds of patients in this study. Staphylococci followed with 21.5 per cent preponderance. This is in agreement with the result of previous retrospective studies of bum patients at the Lagos University Teaching Hospital (Omo-Dare and Akande, 1969; Coker et al., 1983; Sowemimo 1983). The remarkably high prevalence of pseudomonas in the bum wounds may be due to the fact that the organism thrives in a moist environment. This may explain the different results obtained by Mabogunje et al. (1987) in the drier northern part of Nigeria where P. mirubilis (17.2 per cent) and Klebsiella species (15.7 per cent) surpassed Pse&. aertrginosu (11.7 per cent) in prevalance. Contrary to findings in the early part of this century, the isolation of /?-haemolytic streptococcus from bum wounds has now become a rarity. Earlier reports from Lagos (Omo-Dare and Akande, 1969; Coker et al., 1983) reported a 3.2 per cent prevalence in 1968 and a 1 per cent isolation rate in 1983. In this study, no single isolate of this
Bums (1992)Vol. M/No. 6 organism was recovered from the burn wounds. This is a welcome development in view of the threat posed to skin grafting. Anaerobes were conspiciously absent among the isolates from the burn wounds. This is however not suprising since all previous reports worldwide have noted the isolation of anaerobes as an infrequent finding (MacMillan, 1982). Early excision of dead tissues in very deep bums, especially in electrical bums, has maintained this situation. There have been previous reports of tetanus developing in patients with deep bums who presented late to hospital (Oluwasanmi, 1969; Omo-Dare and Akande, 1969). However, all the patients in this study had fresh burns and were managed appropriately. This may indicate that there is really little basis for the practice of routinely including metronidazole in the therapy of bums sepsis unless bacteroides are cultured in specific cases. The results of the antibiotic sensitivity patterns gives serious cause for concern because many of the isolates were resistant to the commonly available and easily affordable antibiotics in Nigeria. Ampiclox (ampicillin plus cloxacillin) is commonly prescribed when staphylococcal infections are considered but the results of this study show that it is ineffective against Staph. uureus. This is in contrast to a previous report from Lagos (Coker et al., 1983) where staphylococci were reported to be 100 per cent sensitive to cloxacillin. This may suggest that overuse (or indeed misuse) of ampiclox over the past years has led to the development of resistant strains of staphylococci in Lagos. Pseud. ueruginosu, which has been the most predominant organism in this study and which is known to be the greatest infection problem in most bum units, was found to be 83.5 per cent susceptible to gentamycin and 93.3 per cent sensitive to colistin. This is in line with the findings of Coker et al. (1983). Ceftazidime had been shown to be 100 per cent effective against all other organisms isolated from the bum wounds except the streptococci species which were encountered infrequently. This finding therefore establishes a place for ceftazidime monotherapy in the treatment of clinically apparent Gram-negative septicaema while awaiting blood culture results. Indeed, Stiver et al. (1987) have reported impressive results with the use of ceftazidime in the treatment of bums sepsis. It can therefore be safely concluded that the bacterial flora of bum wounds in Lagos still retain Psard. uemginosa and Staph. aweas as the most frequent organisms. However, the antibiotic sensitivity pattern of the organisms, especially the staphylococci, is different from that reported during the last two decades. It can also be concluded that there is good reason for introducing active and passive immunization against pseudomonas since these have been shown to be of immense benefit to bum patients (Alexander et al., 1969; Jones et al., 1979; Roe and Jones, 1982). What may, however, have a more far-reaching effect is to nurse severely burned patients in a purpose-built bum unit rather than general surgical wards as in the cases studied. As has been stated by Datubo-Brown and Kejeh (1989) working in Port-Harcourt, Nigeria, ‘The lack of separate bum units, in which patients can be nursed away from other surgical patients, compounds the cross-infection problems of the hospital.’
Acknowledgements The laboratory assistance provided by Dr S. F. Lawal and Mrs Tolu Animashaun, who carried out the isolation of the
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Atoyebi et al.: Bacterial flora of bum wounds
different microorganisms and took pains to characterize them and confirm their identities, is acknowledged with thanks. Many thanks also go to Miss Kuburat Oyeneyin who prepared the typescripts from the manuscripts.
References Alexander J. W., Fisher M. W., MacMillan B. G. et al. (1969) Prevention of invasive pseudomonas infection in bums with a new vaccine. Arch. Surg. 99, 249. Coker A. O., Sowemimo G. 0. A. and Abiodun-Wright 0. M. (1983) The bacteriology of bums at the Lagos University Teaching Hospital. W. Afr. 1. Med. 2, 53. Cruickshank R. (1935) The bacterial infection of bums. 1. Pathol. Bactetiol. 31, 367. Datubo-Brown D. D. and Kejeh B. M. (1989) Bum injuries in Port Harcourt, Nigeria. Bum 15, 152. Greco J. M., Dhennin C., Pinon G. et al. (1979) Local bacterial flora in thermal injuries: influence of topically applied antibiotics. Bums 6,37. Jones R. J., Roe E. A. and Gupta J. L. (1979) Controlled trials of a polyvalent pseudomonas vaccine in bums. Lancet ii, 977. Mabogunje 0. A., Kwaja, M. S. and Lawrie, J. H. (1987) Childhood bums in Zaria, Nigeria. Bums 13, 298.
MacMillan B. G. (1982) The problem of infection in bums. In: Hummel R. (ed.), Ckzical Bum Therapy - A Management and Prevention Guide. Oxford: Wright, pp. 335-3 72. Oluwasanmi, J. 0. (1969) Bums in Western Nigeria. Br. J P]ast. Surg. 22, 216. Omo-Dare P. and Akande B. A. (1969) A study of bums in 68 children admitted into the Lagos University Teaching Hospital, 1964-1968. w. Ah. 1. Med. 28,201. Roe E. A. and Jones R. J. (1982) Active and passive immunization against Pseudomonas aemginosa infection of burned patients. Burns 9,433. Sowemimo G. 0. A. (1983) Bums injuries in Lagos. Burns 9,260. Stiver H. G., Golding A. M. and Snelling C. F. T. (1987) Ceftazidime therapy versus aminoglycoside therapy in patients with Gram negative bum wounds infection. 1. Bum Care Rehabil. 8, 19. Yemul V. L. and Sengupta S. R. (1979) Bacteriology of bums. Bums 7, 190.
Paper accepted 9 May 1992.
Correspondence should be addressed to: Mr 0. A. Atoyebi, Department of Surgery, Lagos University Teaching Hospital, PMB 12003, Lagos, Nigeria.