Journal of Infection (I99I) z2, 233-239


aetiology of otitis externa W i l l i a m L. D i b b

Department of Microbiology, Central Hospital, Fredrikstad, N o r w a y Accepted for publication Io October I 9 9 0

Summary Microbiological samples were collected from the ears of patients with otitis externa for a period of i year. Altogether, z26 evaluable samples from Io4 males and I22 females were received. T h e age range of the patients was similar to that of the Norwegian population. A wide variety of bacteria and fungi was isolated. T h e commonest isolates, excluding normal flora, were Staphylococcus aureus (34"I %), Pseudomonas aeruginosa (22"I %) and Streptococcus pyogenes (8"8%); 9 ' 3 % samples contained fungi. O f all samples, I5 % showed a mixture of G r a m - p o s i t i v e and Gram-negative, potentially pathogenic, bacteria. Infection due to G r a m - n e g a t i v e organisms alone was c o m m o n e r in males, while the lack of any obvious microbial aetiology was more frequent in females. Isolation of S. aureus together with S. pyogenes was c o m m o n but that of S. aureus together with P. aeruginosa was unusual. I n treated patients, the finding of streptococci and S. aureus was rare whereas that of P. aeruginosa or absence of growth was common. Otitis externa involving G r a m - p o s i t i v e bacteria seems to be more prevalent in our area than in that of other reported studies.

Introduction O t i t i s e x t e r n a , a n i n f l a m m a t i o n o f t h e o u t e r ear canal, is a c o m m o n a n d p a i n f u l c o n d i t i o n . 1 A l t h o u g h m o s t cases c a n n o t b e c o n s i d e r e d as s e r i o u s , otitis e x t e m a in p a t i e n t s w i t h r e d u c e d h o s t d e f e n c e s m a y b e l i f e - t h r e a t e n i n g . 2 T h e c o n d i t i o n has been associated with water-contact s and the tropical environment, having acquired various colloquial names which include 'hot-weather ear', 'jungle r o t ' a n d ' S i n g a p o r e e a r ' . 4 S i n c e m u c h o f t h e r e s e a r c h p e r f o r m e d o n otitis e x t e m a h a s n o t b e e n r e c e n t , ~ a f u r t h e r s t u d y f r o m a n o n - t r o p i c a l a r e a in o r d e r to d e t e r m i n e t h e m i c r o b i a l a e t i o l o g y o f otitis e x t e m a w a s felt to b e n e e d e d .

Materials and methods Patients A l e t t e r was s e n t to all clinicians, b o t h in h o s p i t a l s a n d in g e n e r a l p r a c t i c e in the area of Ostfold County (population approximately 240o0o), asking that a s w a b b e s e n t f r o m all cases o f otitis e x t e m a e n c o u n t e r e d d u r i n g a p e r i o d o f I y e a r f r o m I 9 8 8 - I 9 8 9 . D e t a i l s o f e a c h p a t i e n t ' s age, sex a n d a n y a n t i m i c r o b i a l t h e r a p y w e r e r e q u e s t e d . C a s e s o v e r t l y s e c o n d a r y to a m i d d l e ear i n f e c t i o n w e r e excluded. Address correspondence to: Dr W. L. Dibb, Department of Microbiology, Post Box IO2O, Central Hospital, 16Ol Fredrikstad, Norway. oi63-4453/9I/O3O233+o7 $03.00/0

© I99I The British Society for the Study of Infection




All samples were taken from the outer ear canal with charcoal-impregnated cotton-wool swabs which were sent in a modified prereduced Stuart's transport medium as rapidly as possible to the laboratory. Microbiological methods

Samples were cuhured on the following media at a temperature of 37 °C unless otherwise stated: 7 ~o human blood in blood agar base no. 2 (Oxoid Ltd., U.K.), with a staphylococcal streak (in 8% CO 2 for I 8 h ) ; lactose bromo-thymol blue agar 6 (in 8 % CO 2 for 18 h); h u m a n blood agar (in 85% N2, lO% H 2, 5% CO2 for 24-48 h); Sabourand dextrose agar (Gibco Ltd., U.K.) (in air for I week at 27°; some samples being incubated for up to 3 weeks at 37 °C on medium overlaid with sterile olive oil); T C B S Cholera Medium (Oxoid) (in air for 72 h). Growth of microbes was semi-quantified (rich, moderate, sparse) and identification was by generally approved laboratory methods. 7 Analysis o f data

All results were registered in a computer (Norsk Data, Norway) and analysed with F I C S software (Kvam Data, Norway). Results

Of 244 samples received during the period of study, I8 were excluded since they were repeat samples, thereby leaving 226 samples from 226 patients (lO4 male, I22 female). A wide range in age similar to that of the whole Norwegian population was observed (range < 1-84 years, mean 39 years; for the whole population, mean 37"6 years). Many bacterial and fungal species were found (Table I), Staphylococcus aureus being the commonest followed by Pseudomonas aeruginosa and Streptococcus pyogenes. All other organisms were found in less than 5 ~/o patients. No growth or only normal flora (i.e. coagulase-negative staphylococci and coryneforms) was seen in swabs from 16-8 ~/o patients. Many of the microbes were found in a mixed flora (Table II), with 15 % samples showing a mixture of Gram-positive and Gram-negative bacteria and 4"4 % a mixture of fungi and bacteria. T h e overall commonest group of microbes consisted of Gramnegative aerobic or facultative rods, accounting for 27"4 % cases. Vibrio spp. were not isolated. Fungi were implicated as a cause of infection in 9"3 % samples but Malassezia furfur was not found among the 6o samples examined. T h e amount of microbial growth was in most cases registered as rich, only 3/I44 isolates of S. aureus, S. pyogenes and P. aeruginosa showing moderate or sparse growth. Samples were received in every month, the most being in October with only I6~/o samples being received during the first quarter. Isolations of P. aeruginosa increased each quarter to a peak in the fourth quarter when the total was more than twice that of the first quarter. Infection with Gram-negative bacteria alone was seen in 34"6 % males and

Microbial aetiology of otitis externa


T a b l e I Microbiological findings from patients with external otitis. Number

(%) of each species isolated No. of species (% patients with) isolates


Edwardsiella tarda Enterobacter aerogenes Enterobacter cloacae Enterobacter gergoviae Enterobacter sakazakii Enterobacter sp. Escherichia coli Inactive Escherichia coli Klebsiella oxytoca Klebsiella pneumoniae Klebsiella sp. Proteus mirabilis Acinetobacter calcoaceticus var. anitratus Acinetobacter sp. N o n - f e r m e n t i n g G r a m - n e g a t i v e rod Pseudomonas aeruginosa Pseudomonas cepacia Pseudomonas maltophilia Pseudomonas putrefaciens Pseudomonas stutzeri > T w o species of G r a m - n e g a t i v e rods Anaerobic mixed flora Haemophilus influenzae Alpha-haemolytic streptococcus Beta-haemolytic streptococci group A Beta-haemolytic streptococci group B Beta-haemolytic streptococci group C Beta-haemolytic streptococci group G Enterococci Streptococcus pneumoniae Staphylococcus, coagulase-negative Staphylococcus aureus Coryneforms Candida albicans Candida guillermondii Candida parapsilosis Candida pseudotropicalis Torulopsis candida Yeasts Aspergillus fumigatus Aspergillus niger N o growth Only healthy ear flora

Males 104

Females 122

I (I'0)

Total 226

I 2 I 3

(1"o) (I'9) ( I'O) (2"9)

1 (0-8)

1 (0-8)

1 2 2 i 3 i

3 2 3 3

(2"9) (x'9) (2"9) (2'9)

5 (4 "I)

8 (3"5)

i (0.8)

3 (I'3)

2 3 I 2 3

5 6 I 8 3 1 I

6 (5"8)

(I'6) (2"5) (0"8) (I'6) (2"5)

I (I'O) I (0'8) 25 (24"0) I (I'O) 1 (I'O) I (I'O)

3 (2"9)

25 (20"5)

(8"7) (2"9) (I'O) (5"8)

(1'9) (33"7) (I'O) (5"8)

I (I'O) I (I'O)

2 I 2 5

I (0"8)

I 1 I 20 6

I (0"8) I I (9"0) 3 (2"5) I (0"8) 1 (0.8) I (O'8) 3 (2"5)

42 (34'4) I (0"8) i (0-8)

I 2 I 1

(0"8) (1"6) (0"8) (0"8)

3 (2-5) I 2 3 8

(1"o) (I'9) (2"9) (7"7)

5 ° (22"1)

(0.8) (0'8) (0'8) (1"6)

6 (4"9) 2 35 I 6

(2"2) (2"7) (0"4) (3"5) (I'3) (0"4) (0"4)

I (0-4) 1 I I 2

r (I'O) 9 3 I 6

(0.4) (0.9) (0'9) (0-4) (1-3) (0.4)

(0"9) (0'4) (0"9) (2"2)

(0"4) (0"4) (0-4) (8"8) (2"7) 2 (0"9) 7 (3'1)

6 (2'7) I (0'4) 5 (2"2)

77 (34"I) 2 (0'9) 7 (3"1)

I 3 I 2

(0"4) (1"3) (0"4) (0"9)

3 (1.3)

I (0"8)

2 (0"9)

7 (5"7) 20 (16.4)

2 (o'9) io (4"4) 28 (12"4)


W. L. D I B B

Table II

Patterns of microbial infection derived from 2 2 6 samples from cases of external otitis

Microbes found/sex Gram-positive pathogen(s) M F M+F Gram-negative pathogen(s) M F M+F Gram-positive and Gram-negative pathogen(s) M F M+F Fungus M F M+F Fungus and Gram-positive pathogen(s) M F M+F Fungus and Gram-negative pathogen(s) M F M+F Fungus, Gram-positive and Gram-negative pathogen(s) M F M+F Other pathogens M F M+F No growth M F M+F Normal flora M F M+F

Number (%)

30 (28'8) 40 (32"8) 70 (31"o) 36 (34'6) 26 (21"3) 62 (27-4) 16 (15"4) 18 (14-8) 34 (15"o) 7 (6"7) 4 (3'3) ii (4"9) 3 (2"9) 4 (3"3) 7 (3 "1) o (o'o)

I (0"8) I (0"4) I (I'O) I (o'8) 2 (0"9) o (o'o) I (0"8) I (0"4) 3 (2"9) 7 (5"7) lO (44) 8 (7"7) 20 (16"4) 28 (12"4)

*Males = M (lO4), females = F (122). 2I" 3 % f e m a l e s ( P = 0"037, X 2 test). A p u r e l y f u n g a l i n f e c t i o n w a s f o u n d i n m o r e m a l e s t h a n f e m a l e s w h i l e a n e g a t i v e f i n d i n g , i.e. n o g r o w t h o r o n l y n o r m a l flora, w a s o v e r t w i c e as c o m m o n i n f e m a l e s as i n m a l e s ( P = 0"033, X ~ test) ( T a b l e I I ) . T h e p r e s e n c e o r a b s e n c e o f n o r m a l flora, a l o n e o r i n

Microbial aetiology of otitis externa


T a b l e I I I Comparison of various microbes isolated from treated and untreated patients Number isolates (% patients with) Finding

Treated (n = 39)

No growth Staphylococcus aureus Streptococcus pyogenes Pseudomonas aeruginosa Fungi

6 (I5"4) I I (28'2) o (o) 13 (33"3) 4 (IO'3)

Not treated (n = 187) 4 66 20 37 I7


(35"3) (lO"7) (I9"8) (9"I)

combination with pathogenic microbes, was registered continuously for 46 untreated patients with otitis externa. While 22 (48 o/0) did not have normal flora, 18 ( 3 9 % ) had a rich growth of normal flora. T h e r e were noticeable differences in isolation rates b e t w e e n treated and untreated patients (Table III). Streptococcus pyogenes was isolated only from the untreated patients. By contrast, P. aeruginosa or absence of growth was more frequent in the treated group. Similar isolation rates for fungi were f o u n d in both groups. Only 3/77 samples s h o w e d growth of S. aureus together with P. aeruginosa, while 5 / 2 o samples with S. pyogenes also contained P. aeruginosa and 4 / 6 samples with enterococci. In addition, 7 / 2 6 samples containing one or several of Escherichia coli, Proteus spp. and Klebsiella spp. also contained S. aureus and 8/2o specimens containing S. pyogenes also contained S. aureus. Discussion

In this study, otitis externa was shown to afflict all age groups and b o t h sexes. O t h e r workers, however, have f o u n d an excess of males with otitis externa. 1' 4. T h e mean age of patients in this study was higher than that f o u n d by M a n n i et al., 4 their study having included adults only. W e have previously shown that the normal flora of the outer ear canal consists p r e d o m i n a n t l y of coagulase-negative staphylococci and eoryneforms. 8 T h i s contrasts sharply with findings in the inflamed outer ear canal, when only a b o u t I 2 ~/o patients showed normal flora alone. T h e wide variety of microbes isolated from cases of external otitis suggests that the pathogenic process in otitis e x t e m a is non-specific or that the aetiological r61e of the organisms is uncertain. Even so, the dominance of S. aureus, P. aeruginosa and S. pyogenes indicates that these organisms are real causes of infection, since it is unlikely that these w o u l d have been isolated so often if they had been only chance colonisers. O t h e r studies have shown that P. aeruginosa is the dominant cause of otitis externa in w a r m e r climates 1, ~ and in the aquatic environment. 9 T h e high incidence of infection associated with G r a m - p o s i t i v e bacteria shown in this s t u d y is of interest and differs markedly from findings in other studies such as that of M a n n i et al., 4 w h o f o u n d that only I 8 % cases involved S. aureus. Since 15 0/0 c a s e s in this study were associated with a mixture of G r a m -



positive and G r a m - n e g a t i v e bacteria, it m a y be that findings d e p e n d u p o n the time o f sampling during the course of the disease. Pseudomonas aeruginosa produces substances which m a y inhibit the growth of S. aureus 1° and vice versa. 11 T h i s m a y explain w h y so few c o m b i n e d infections with these two species were f o u n d when compared with infections associated with ' coliforms' c o m b i n e d with S. aureus. T h e association between S. aureus and S. pyogenes is well-recognised in such conditions as impetigo contagiosa. 12 In contrast to the findings of this study, however, streptococci are regarded as an u n c o m m o n cause of otitis externa by others. 1~ T h e incidence of the candidal infection in this study is relatively low compared with that reported from warmer areas.l' 4 Similarly, the isolation of Aspergillus sp. was u n c o m m o n in this study but very c o m m o n in studies f r o m B u r m a 14 and Tanzania. 4 T h e association of otomycosis with a tropical climate has been m e n t i o n e d by others. TM 16 T r e a t m e n t of otitis externa is more effective in removing streptococci than P. aeruginosa since streptococci are generally more sensitive to antibacterial agents t h a n P. aeruginosa. T h i s m a y partly explain the differences observed. F u n g i are not sensitive to most of the c o m m o n agents used for treating otitis externa and although an increase in fungal colonisation d u r i n g antibacterial therapy m i g h t have been expected it was not observed. T h e normal microbial flora of the ear often seems to disappear in cases of otitis extema. In a previous study, 8 it was shown that > 8o % persons with uninflamed outer ear canals had normal flora (as defined above) c o m p a r e d to 48 % patients with external otitis. A l t h o u g h small n u m b e r s of yeasts were f o u n d in the normal flora study, they were not the most important pathogen, n a m e l y Candida albicans. Factors other t h a n microbial infection, such as moisture inducing maceration o f the skin, and u n d e r l y i n g skin problems, are also involved in the pathogenesis o f otitis externa. 17 Even so, the role of microbial infection as an i m p o r t a n t cause of the disease seems certain because otitis externa can be infectious, 9 t r e a t m e n t with antibiotics cures the complaint 15 and the microbiol6gical findings in otitis externa differ m a r k e d l y f r o m those of the healthy external ear. (Laboratory technician Unni Amundsen performed much of the practical work in this study which was supported by a grant from The Confederation of Norwegian Business and Industry.) References

r. Feinmesser R, Wiesel YM, Argaman M, Gay I. Otitis extema--bacteriological survey. ORL J Otorhinolaryngol Relat Spec r982; 44: I2I-I252. Mills R. Malignant otitis externa. BMJ I986; 292: 429-43o. 3- Wright DN, Alexander JM. Effect of water on the bacterial flora of swimmers' ears. Arch Otorhinolaryngol I974; 99: I5-I8. 4- Manni JJ, Kuylen K. Clinical and bacteriological studies in otitis externa in Dar es Salaam, Tanzania. Clin Otolaryngol I984; 9: 351-354. 5- Ochs IL. Treatment of external otitis: a simple and effective technic. J A M A I95O; I42: I36I-I362. 6. Dibb WL, Bottolfsen KL. Evaluation of Rosco diagnostic fl-glucuronidase tablets in the identification of urinary isolates of Escherichia coil A P M I S Sect B r984; 92: 261-264.

Microbial aetiology of otitis externa


7. Lennette EH, Balows A, Hausler WJ, Shadomy HJ, Eds. Manual of clinical microbiology. Washington: American Society for Microbiology, I985. 8. D i b b W L . T h e normal microbial flora of the outer ear canal in healthy Norwegian individuals. N I P H Ann I99o; I3: n - i 6 . 9- Alcock SR. Acute otitis externa in divers working in the North Sea: a microbiological survey of seven saturation dives. J Hyg, Camb I977; 78: 395-409io. Falcon MA, Mansito TB, Carnicero A, Gutierrez-Navarro AM. L-formqike colonies of Staphylococcus aureus induced by an extracellular lytic enzyme from Pseudomonas aeruginosa. J Clin Microbiol I989 ; 27 : I65O--I654 • I I. Shibl AM, A1-Sowaygh IA. Inhibition of Pseudomonas aeruginosa slime production by staphylococcal extracellular product. J Clin Microbiol I98O; n : I23-I26. I2. Parker M T . Streptococcal diseases. In: Wilson G, Miles A, Parker M T , Eds. Topley and Wilson's principles of bacteriology, virology and immunity, Vol. 3, I984: 225-253. I3. Bennett H, Brook I, Rodriguez WJ. Group A r-hemolytic streptococcal otitis externa in an infant. South M e d J I98O; 73: IO79-IO8O14. T h a n K M , Naing KS, Min M. Otomycosis in Burma, and its treatment. Am J Trop Med Hyg I98o; z9: 620-623. I5. Editorial. Otitis externa. B M J I969; I : 70. • 6. Beg M H A , Bukhari AT. Otomycosis in Karachi. Practitioner I983 ; zz7: I767-I77o. I7. Editorial. Necrotising otitis externa. Lancet I982; i: 207.

Microbial aetiology of otitis externa.

Microbiological samples were collected from the ears of patients with otitis externa for a period of 1 year. Altogether, 226 evaluable samples from 10...
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