Background
Otitis Media is the most common disease of childhood, with about 65–330 million people suffering from ear infection worldwide and 60% of them have significant hearing impairment [
1]. It is estimated that 20,000 people die each year from otitis media and the overall burden of these diseases is higher in the poorest countries [
2]. The health-economic burden of ear infection is also severe especially in Africa and other developing nations where the disease prevalence is estimated as high as 11% [
3].
Complications of Otitis Media (OM) such as perforation of the tympanic membrane, otitis externa and mastoiditis affect balance, motor control and hearing. Acquired hearing impairment in children is mainly caused by chronic suppurative otitis media (CSOM). The hearing impairment produced by otitis media also affect intellectual performance and language development [
4,
5].
The growing bacterial resistance to antibiotics has altered the clinical picture of otitis media and its complications. The emergence of Multi Drug Resistance (MDR) is clearly related to the dose of antibiotics and how they are being used [
6]. Serious infections caused by methicillin-resistant
S. aureus (MRSA) are increasingly difficult to treat. While it is clear that antibiotics are pivotal in the selection of bacterial resistance, the spread of resistance genes and resistant bacteria also contributes to the problem [
7]. Most of the time treatment for OM is done clinically, especially in health facilities found in low income countries. This will cause bacterial drug resistance and preventable complications of OM such as deafness and meningitis [
8] .
There are a small number of studies done in Ethiopia concerning this topic, moreover, almost all of them show the emergence of these drug resistant bacterial strains and recommend further study [
9] . Therefore this study aimed to identify bacterial pathogens related to ear infection and to assess antibacterial resistance among isolated organisms.
Results
Description of socio demographic characteristics
A total of 152 children with ear discharge were included in this study from April 2018 to July 2018. Among these, 78/152 (51.3%) were males. The age range of participants was from 3months to 12years, with a mean age of 2.59 years. Nearly half of participants 80/152 (52.6%) were in the age group of 1 to 4years, and the majority of the study subjects 105 (69.5%) were urban residents [Table
1].
Table 1
Socio demographic characteristics of children with ear discharge, Hawassa, SNNPR, April to July, 2018
Sex | Male | 78 | 51.3 |
Female | 74 | 48.7 |
Age (in years) | < 1 | 48 | 31.6 |
1–4 | 80 | 52.6 |
5–10 | 21 | 13.8 |
11–15 | 3 | 2.0 |
Residence | Urban | 105 | 69.5 |
Rural | 47 | 30.9 |
Place of stay in day time | Home | 118 | 77.8 |
School | 32 | 21.1 |
Day care | 2 | 1.3 |
Culture results
Among 152 individuals whose samples were cultured, at least one pathogenic bacterial isolate were detected in 115/152 (75.7%). A total of 123 bacterial isolates were detected; of which 59/123 (48.0%) were Gram positive and 64 (52.0%) were Gram negative bacteria. Eight samples had two different types of bacterial isolates.
Staphylococcus aureus 41/152 (27.0%) was the most frequently isolated pathogen followed by
P. mirabilis 19/152 (12.5%)
, Haemophilus influenzae 14/152 (9.2%),
E. coli 11/152 (7.2%),
Enterococcus species 10/152 (6.6%),
Streptococcus pneumoniae 8/152 (5.3%),
Klebsiella pneumoniae 6/152 (3.9%), and
Klebsiella ozeanae 6/152 (3.9%). The majority of the bacterial isolates 99/152 (65.1%) were found in children less than 5 years of age [Table
2].
Table 2
Bacterial isolates among age groups of study participant with ear infection visiting selected health facilities in Hawasa, Ethiopia, April 2018 July 2018
S. aureus
| 14 | 17 | 10 | 41 (27%) |
P. mirabilis
| 1 | 16 | 2 | 19 (12.5%) |
H. influenzae
| 12 | 2 | 0 | 14 (9.2%) |
E. coli
| 5 | 6 | 0 | 11 (7.2%) |
Enterococcus species
| 4 | 4 | 2 | 10 (6.6%) |
S. pneumoniae
| 6 | 2 | 0 | 8 (5.3%) |
K .pneumoniae
| 0 | 6 | 0 | 6 (3.9%) |
K. ozienae
| 0 | 6 | 0 | 6 (3.9%) |
Pseudomonas species
| 1 | 3 | 0 | 4 (2.6%) |
Providenica species
| 0 | 0 | 2 | 2 (1.3%) |
Acinetobacter species.
| 0 | 2 | 0 | 2 (1.3%) |
Total
| 37 (24.3%) | 62 (40.8) | 16 (10.5) | 152 (100%) |
Twelve out of 14 H. influenza isolates were identified from the children less than 12 months of age. On the other hand, out of total 19 P. mirabilis isolates, 16/19 (84.2%) were identified from children aged between 1 and 5 years. Moreover, S. aureus had higher frequency in all age groups. The frequency of Pseudomonas species was only 4 (2.6%).
Drug resistance patterns
E. coli (36.4%) and
Enterococcus species (50.0%)showed resistance to ciprofloxacin but the rest of all isolated Gram positive and Gram negative bacteria showed no (0.0%) resistance to ciprofloxacin. On the other hand, all Gram negative bacteria except
P. mirabilis (68.4%) were 100% resistant to ampicilin. 11.2% of pathogens showed resistance to gentamycin but only
K. pneumonia was 100% resistant.
Klebsiella species showed higher resistance for most of the antimicrobials tested, but isolates were susceptible to ciprofloxacin [Table.
3].
Table 3
Antimicrobial resistance patterns of Gram-negative bacteria isolated from ear infection among children visiting selected health facilities, Hawassa, Ethiopia, 2018
P.mirabilis
| 68.4% | 0.0% | 57.9% | 10.5% | 57.9% | 10.5% | 10.5% | 21.1% | 31.6% | ND |
E.coli
| 100% | 36.4 | 72.7% | 18.2% | 81.8% | 18.2% | 18.2% | 0.0% | 18.2% | ND |
H.influenza
| 100% | 0.0% | 16.7% | ND | 50% | 50% | 66.7% | 100% | 0.0% | ND |
K.oziena
| 100% | 0.0% | 66.7% | 33.3 | 66.7% | 33.3% | 33.3 | 33.3% | 33.3% | 33.3% |
K.pneumonia
| 100% | 0.0% | 100% | 100% | 66.7% | 100% | 66.7 | 33.3% | 66.7% | 66.7% |
Pseudomonas.spp.
| ND | 0.0% | ND | 25 | ND | 100% | 25 | 25.0% | ND | ND |
Acinetobacter spp
| 100% | 0.0% | 100% | 0.0% | 100% | 100% | 100% | 0.0% | 0.0% | 100% |
Providenicaspp
| 100% | 0.0% | 100% | 0.0% | 50% | 100% | 50% | 0.0% | 0.0% | 100% |
S. pneumonia showed no resistance for any of the drugs tested.
S. aureus showed higher resistance to penicillin (85.4%) and trimethoprim-sulphamethoxazole (73.2%). However, all isolates of
S. aureus were susceptible to ciprofloxacin and gentamycin. Only half of the isolated
Enterococcus species were susceptible to both ciprofloxacin and erythromycin. All
Enterococcus species are susceptible to chloraphenicol [Table.
4].
Table 4
Antimicrobial resistance patterns of Gram-positive bacteria isolated from ear infection among children visiting selected health facilities, Hawasa, Ethiopia, April 2018 to July
S.aureus
| 0.0% | 0.0% | 73.2% | 85.4% | 14.6% | 14.6% | 17.1% | 24.4% | 14.6% |
S.pneumonia
| ND | ND | ND | ND | 0.0% | 0.0% | ND | ND | 0.0% |
Enterococcus spp.
| 50% | ND | ND | 37.3 | ND | 0 | ND | 37.30% | 50.0% |
Regarding drug resistance rates, 85.2, 72.0 and 71.4% of the isolated bacteria were resistant to ampicilin, trimethoprim-sulphamethoxazole and penicillin respectively. These were followed by 37.5, 31.3, 22.6 and 11.2% of the isolates resistant to ceftriaxone, ceftazidime, chloramphenicol and gentamicin respectively. Only 7.3% of the isolates were resistant to ciprofloxacin.
From the total (41) isolated S. aureus, 6 (14.6%) showed erythromycin induced clindamycin resistance also known as MLSBi resistance which is observed as a ‘D’ shape on Muller Hinton agar and 7(17.0%) of them were methicilin resistant S. aureus (MRSA). Out of the seven MRSA identified, 2(28.5%) of them showed erythromycin-inducible clindamycin resistance.
Description of potential risk factors
From the 152 study subjects 52(34.4%) of them had an ear infection longer than 2 weeks and 57 (37.5%) of the participants had a history of taking antibiotics. Eighty six (56.6%) of the children included in this study were breast feeding and 56 (36.8%) of the children were fed by bottles. Upper respiratory tract infection, including throat infection, is known to be a risk factor for otitis media. From all children included this study, 89(58.9%) had a URTI and 32 (20.4%) had a throat infection. Among all study subjects, 20 (13.2%) came from households with tobacco smokers, and 10 (6.6%) of the patients were observed to have another person having an ear infection in their family and 57(37.5%) of them were taking antibiotics [Table
5].
Table 5
Frequency and percentage of possible risk factors for bacterial ear infection of children with ear discharge, Hawassa, SNNPR, April 2018 to July 2018
Duration of infection | Less than 2 weeks | 100 | 65.8 |
More than 2 weeks | 52 | 34.4 |
Breast feeding | Yes | 86 | 56.6 |
No | 66 | 43.4 |
Bottle feeding | Yes | 56 | 36.8 |
No | 96 | 63.2 |
Presence of throat infection | Yes | 31 | 20.4 |
No | 121 | 79.6 |
Presence of tobacco smoke in the house | Yes | 20 | 13.2 |
No | 132 | 86.8 |
Presence of URTI | Yes | 89 | 58.6 |
No | 63 | 41.4 |
Other ear infection in the family | Yes | 5 | 3.2 |
No | 147 | 96.7 |
Antibiotic treatment history | Yes | 57 | 37.5 |
No | 95 | 62.5 |
Association of the potential risk factors and culture positive otitis media
Factors associated with detection of pathogenic bacteria from ear discharge in children have been analyzed but there was no statistically significant association between detection of pathogenic bacteria and most potential risk factors. However, the presence of upper respiratory tract infection showed a statistically significant relationship, with an odds ratio of 4.5 (95% CI 1.8–12.0). Bottle feeding happened to have a negative effect on the detection of pathogenic bacteria from ear discharge, with an odds ratio of 6.5 (95% CI 2.4–17.8) [Table
6].
Table 6
Factors associated with detection of pathogenic bacteria from ear discharge among children at selected health facilities in Hawasa,Ethiopia April 2018 to July 2018
Sex | Male | 78 | 59 (75.6) | 1 (0.5–2.1) | 0.99 | 0.54 (0.2–1.5) | 0.19 |
Female | 74 | 56 (75.7) | 1 | – | 1 | – |
Age group | ≤5 | 128 | 99 (77.3) | 1.7 (0.6–4.3) | 0.26 | 4.1 (1–15.8) | 0.38 |
> 5 | 24 | 16 (66.7) | 1 | – | 1 | – |
URTI | Yes | 89 | 74 (83.1) | 2.6 (1.2–5.6) | 0.012 | 4.5 (1.8–12) | 0.001 |
No | 63 | 41 (65.1) | 1 | – | 1 | – |
Throat infection | Yes | 31 | 23 (74.2) | 0.9 (0.36–2.2) | 0.83 | 0.8 (0.3–2.4) | 0.79 |
No | 121 | 92 (76.0) | 1 | – | 1 | – |
Bottle feeding | Yes | 56 | 35 (62.5) | 1 | – | 1 | – |
No | 96 | 80 (83.3) | 3 (1.4–6.4) | 0.005 | 6.5 (2.4–17.8) | 0.000 |
Breast feeding | Yes | 86 | 64 (74.4) | 1.1 (0.55–2.5) | 0.68 | 0.4 (0.1–1.2) | 0.11 |
No | 66 | 51 (77.7) | 1 | – | 1 | – |
Duration of infection | ≤ 15 day | 100 | 77 (77.0) | 0.8 (0.4–1.7) | 0.59 | 2.0 (0.8–5.1) | 0.11 |
>15day | 52 | 38 (73.1) | 1 | – | 1 | – |
Residence | Urban | 105 | 77 (73.3) | 0.65 (0.3–1.5) | 0.32 | 0.55 (0.19–1.5) | 0.26 |
Rural | 47 | 38 (80.9) | 1 | – | 1 | – |
Antibiotic treatment | Yes | 57 | 43 (75.4) | 0.98 (0.4–2.1) | 0.96 | 1.4 (0.6–3.4) | 0.42 |
No | 95 | 72 (75.8) | 1 | – | 1 | – |
Discussion
Otitis media is a major health problem in children in developing countries [
12]. OM is more common in children due to the fact that children's eustachian tube is shorter, more horizontal and with a more flaccid cartilage which can easily impair its opening and leads to ear infection [
4,
12]. Most cases of OM arise between the age of 6 month and 3 years [
13].
In this study, we have been able to see the etiological agents and antimicrobial resistance pattern of isolates from children with ear infection visiting health facilities in Hawassa from April to July 2018. The overall rate of ear infection with positive culture results was 75.6%, which is higher than finding in Ethiopia (48.5%) [
14] but comparable with other parts of the world including Nigeria (91%) and Yemen (78.0%) [
8,
15] . The probable reasons for this could be attributed to difference in study participant, study period, climate and geographical variation.
In the present study, a similar percentage of Gram negative and Gram positive bacteria were detected (52.0 and 48.0%, respectively), which is in agreement with an earlier report in Gonder (56.0 and 44.0%) [
16] .This finding was different from a study done in Hawasa (79.5%) [
17]. Possible reasons for this difference could be age group dissimilarity and study period.
The finding of this study showed that
S. aureus was the most prevalent (27.0%) pathogen among children having ear discharge, which was similar with the previous studies done in our country [
14,
17] and abroad in Nepal [
18,
19]. However, the result was in contrast to other reports such as a study from Bahirdar Regional Health Research Laboratory Centre [
16] and in other parts of the world,
Pseudomonas species is the most frequently isolated organism [
2]. The probable reason could be that the frequency of
S. aureus in the middle ear infection could be attributed to their ubiquitous nature and high carriage of resistant strains in the external auditory canal and upper respiratory tract.
In the present study, the prevalence of
Pseudomonas species was 4 (2.6%). However, study conducted around the world reported
Pseudomonas spp. as the most frequently isolated Gram negative pathogen from ear discharge [
8] . The possible reason is that most study subjects included in this study had OM which is less than 2 weeks. Apparently,
Pseudomonas species is mostly isolated from chronic OM, which is more than 2 weeks of duration or more. The other reason for this fact could be that the time or season of a year may favour some type of bacteria [
15].
Our study indicates that the majority of the bacterial isolates (65.1%) were found in children less than 5 years of age. A similar finding was also documented in some previous studies done in Gonder University Hospital, and Ayder Teaching and Referral Hospital, Mekele [
9,
20]. Twelve out of 14
H. influenza isolates were identified from children less than 12 months of age. This is due to the fact that the main bacterial isolates in AOM are the same as those that typically infect the upper respiratory tract in children and
H. influenza is known to cause URTI [
20]. Out of
P. mirabilis isolates, 84.2%were identified from children aged between 1 and 5 years. Similar results were reported from a study done at EPHI [
14].
In this study, lower resistance was observed to ciprofloxacin (7.3%) and gentamicin (11.2%), though resistance rates were high to ampicilin (85.2%), trimethoprim-sulphamethoxazole (72.0%)and penicillin (71.4%), which was consistent with several reports elsewhere [
4,
8,
16,
18].
Klebsiella species are known for their resistance to several drugs [
10], and a similar finding was also observed in the current study.
S. aureus showed higher resistance for penicillin and trimethoprim-sulphamethoxazole with 85.4 and 73.2%, respectively. This is comparable with the study done in Jimma, where 84% of
S. aureus isolates were found to be resistant to penicillin [
19] . Even though gentamicin is a parenteral drug and ciprofloxacin is rarely used in children due to concerns of bone/joint effects, these two drugs were highly effective antibiotics and thus should be considered in treating children with otitis media since most organisms were resistance or poor response to first line drugs. Gentamicin should not be used as mono-therapy for
S. aureus infections. Indeed, there is little evidence it has any utility in any
S. aureus infections.
S. aureus showed no resistance to ciprofloxacin and gentamicin which is in agreement with studies done in Jimma and Bahirdar [
16,
19] . The probable reasons for this variation could be attributed to antimicrobial resistance profile of bacteria varies among population because of difference in geography, local antimicrobial prescribing practices and prevalence of resistant bacterial strains.
Factors associated with detection of pathogenic bacteria from ear discharge in children have been analyzed but there was no statistically significant association between detection of pathogenic bacteria and most of the potential risk factors. However, presence of upper respiratory tract infection showed a statistically significant relation, with an AOR of 4.5 (95% CI 1.8–2.0). This was in agreement with the result in Jimma [
19]. It is also known that upper respiratory tract infections are one of the major reasons for impaired middle ear physiology [
13].
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