Abstract
Background
Hearing aids are the most common conventional devices used to manage sensorineural hearing loss. Although safe and reliable methods, Hearing aids have some minor or moderate side effects that may be inconvenient for those patients and may result in patient non-compliance or even abandonment of their usage. One of the most common is ear irritation and itching. Although itching is attributed to several causes including athetosis and skin allergy, however, Both Bacterial and fungal infections are considered the major leading cause. This study aims to determine the microbiological profile of the external ear in hearing-aided patients presented with itching.
Methods
150 hearing-aided patients presented with itching were recruited for the study all underwent history taking, full clinical examination, and external canal swabs were taken. Then swabs were cultivated for both bacterial and fungal growth.
Results
15 samples (8.6%) were free from infection while 159 samples (91.4%) were positive for infection. There was a statistically significant difference between the free and infected samples (either bacterial or fungal). Out of the infected samples, 135 samples (77.6%) had a bacterial infection and 24 samples (13.8%) had a fungal infection.
Conclusion
Microbial growth is the major factor in the development of external ear itching and pruritis, being mainly staphylococcal infection either staphylococcus Aureus or coagulase-negative species, however, gram-negative bacteria and fungal infection are not considered uncommon. The duration of hearing aid usage was found significant in the development of such infection. These findings shed light on the importance of frequent cleaning of both the external ear molds and proper hygiene of the external canal.
Keywords: External auditory canal, Hearing aids, Pruritis, Microbiome
Introduction
Sensorineural (SSNL) hearing loss is a common medical condition worldwide, for instance, more than 66,000 cases are reported annually in the United States with more elderly and male predominance [1]. Hearing aids (HA) are the most common conservative method used for managing such conditions, it has been reported that they are effective in improving the hearing scope and overall quality of life for such patients [2].
Side effects of using hearing aids have been reported by many patients and clinicians including negative feedback, poor fitting, social disgrace, headache, ear pain, tinnitus, and itching which may halt some of those patients from prolonged HA usage [3].
Hearing aid users often present to otolaryngologists with complaints of constant irritations within the ear canals on account of either allergic contact dermatitis from the ear molds that connect the HA to the ear canal [4, 5] or bacterial/ fungal otitis externa, or wax impaction [6, 7].
The external auditory canal can harbor certain microorganisms. Coagulase-negative Staphylococcus, Staphylococcus aureus, and Streptococcus pneumoniae are the most common bacteria isolated from the external ear canals of healthy people. Corynebacterium species (Turicella otitidis and Corynebacterium auris) have also been isolated in various studies. The third most common recovered bacteria are Streptococci and Enterococci species. Hearing aids have been identified as a potential source of microbial transmission [8]. The reported annual incidence of acute otitis externa varies between 1:100 and 1:250 in the general population, with a seasonal and regional variability [9]. Several microbiological analyses characterize Pseudomonas aeruginosa as the most common causative bacteria in acute otitis externa, followed by Staphylococcus aureus [10].
The use of hearing aids is a predisposing factor to the development of otitis externa. Aside from the increased humidity that results from wearing a hearing aid, it has been postulated that the presence of polymicrobial flora in ear molds may be an etiological agent for the development of otitis externa in humans [4, 6].
However, itchy ear syndromes with no obvious pathologic findings other than atrophic changes on the surface of the external auditory canal have been described [11].
The ear is a moist place and hearing aids are worn in the ear; bacteria and other microorganisms can easily grow on hearing aid surfaces. A wide range of bacteria and fungi have been found to grow on hearing aid surfaces. Recent research related to hearing aid hygiene has shed new light on how patients need to properly clean their hearing aids [4, [6].
Bacteria such as Pseudomonas aeruginosa, Staphylococcus aureus, Streptococcus pneumoniae, Streptococcus pyogenes, Hemophilus influenzae, and Proteus species are predominantly responsible for the infection [12–14].
This study aims to examine the microbial profile of ear canal debris, in hearing aid users complaining of ear irritation to help to highlight possible causes for such pathological conditions.
Methodology
Ethical Considerations
The study was authorized by Assiut University, Faculty of Medicine’s Ethical Committee in accordance with the Declaration of Helsinki, the code of ethics of the World Medical Association; IRB number: 04-2023-300176. An informed written consent was obtained from the included patients and asked to volunteer.
Study Design
This cross-sectional study was conducted on 150 hearing-impaired individuals previously fitted with behind-the-ear HA, who arrived at the Ear, Nose and Throat Clinic of Assiut University Hospital, in Assiut University for routine hearing aid follow-up, or for HA-related or some other complaints participated in this study from August 2023 to December 2023.
Clinical Assessment of the Included Patients
These volunteers included individuals who were fitted with HAs in our department as well as those who were fitted elsewhere before presenting to our department. All the subjects either using the behind-the-ear Hearing Aids (BTE HA) or Completely in the Canal Hearing Aids (CIC HA) were recruited in the study. One was recruited if he/she has used a monoaural or Binaural HA for upwards of four weeks. Volunteers were excluded if they had active ear discharge originating from the middle ear in the presence of tympanic membrane perforation, had a history of penetrating trauma to the ipsilateral ear, or had taken any antimicrobial ear drops or systemic antibiotics in the preceding seven days, in addition, patients who had major general comorbidities that may contribute to infections like uncontrolled diabetes, immunosuppressive therapy or immunocompromised patients were also excluded. On arrival at the clinic, potential subjects were interviewed and data concerning the age, duration of HA usage, history and frequency of ear irritation, pain, and discharge were enquired. The ears were examined with otoscopes and the states of the ear canals and the ear drums were recorded. Any debris/exudates seen were characterized.
Identification of Microbes
External ear canal swab samples [15] (taken without cleaning of any exudates, cerumen, or debris) of subjects were collected [16]. Samples were collected and placed in tubes containing sterile BHI broth [17] (Oxoid) and transported to the Microbiology Laboratory at the Department of Medical Microbiology and Immunology, Faculty of Medicine, Assiut University for microbial isolation and identification. Swabs were cultivated on a set of culture media plates for bacterial growth, namely blood agar, mannitol malt Agar, and MacConkey ‘s agar, (all from Oxoid). Plates were incubated for 24–48 hrs at 37˚C. Biochemical reactions were done if needed for further identification [16]. For fungal growth, Sabouraud dextrose agar plates were incubated for 48 hours. If there was no growth, incubation was continued for up to seven days before reporting as a negative culture [15].
Results
The study included 174 external ear canal swab samples of 150 patients 76 males (50.7%) and 74 females (49.3%). Their age ranged between 7 and 70 years; mean ± SD (46.12 ± 19.66 years). 126 patients (84%) were monaural hearing aided and 24 (16%) were aided by binaural hearing aids. The duration of hearing aid usage ranged between 3 and 20 years. 79 ears (45.4%) were behind the ear (BTE) hearing aided and 95 ears (54.6%) were complete in the canal (CIC) hearing aided.
Fifteen samples (8.6%) were free from infection while 159 samples (91.4%) were positive for infection. There was a statistically significant difference between the free and infected samples (either bacterial or fungal). Out of the infected samples, 135 samples (77.6%) had a bacterial infection and 24 samples (13.8%) had a fungal infection as shown in Table (1).
Table 1.
All studied samples by presence or absence of infection
| Samples (n = 174) N (%) |
P. value | ||
|---|---|---|---|
| Free | 15 (8.6%) | **<0.001 | |
| Infected | 159 (91.4%) | ||
| Fungi | Bacteria | ||
| 24 (13.8%) | 135 (77.6%) | ||
Candida albicans (CA) prevalence was 62.5% among fungal infections with no statistically significant difference between those infected by moulds and those infected by CA. As regards bacterial infection out of 135 bacterial infections, 24 samples (17.8%) were positive for Gram-negative bacilli (GNB) and 111 samples (82.2%) were positive for Gram-positive cocci with statistically significant difference between them. Out of 24 GNB samples, 18 samples (75%) were positive for Pseudomonas aeruginosa while 6 samples (25%) were positive for Klebsiella with statistically significant differences. Out of 111 Gram-positive cocci samples, 63 samples (56.8%) were positive for Coagulase-negative staphylococci (CNS) while 48 samples (43.2%) were positive for Staphylococcus aureus (SA) with no statistically significant difference as shown in Table (2).
Table 2.
Prevalence of different pathogens isolated from external ear canal swabs
| Infection | N (%) | P. value | |||
|---|---|---|---|---|---|
| Fungi | 24 (13.8%) | 0.221 | |||
| Candida albicans | 15 (62.5%) | ||||
| Moulds | 9 (37.5%) | ||||
| Bacteria | 135 (77.6%) | ||||
| Gram negative bacilli | 24 (17.8%) | 0.014* | < 0.001** | ||
| Pseudomonas aeruginosa | Klebsiella | ||||
| 18 (75%) | 6 (25%) | ||||
| Gram positive cocci | 111 (82.2) | 0.155 | |||
| Coagulase-negative staphylococci | Staphylococcus aureus | ||||
| 63 (56.8%) | 48 (43.2%) | ||||
Table (3) shows that fungal infection was associated with a statistically significant longer duration of hearing aid usage than bacterial infection.
Table 3.
Relationship between duration of hearing aid usage and number of infected samples
| Infected samples | P. value | ||
|---|---|---|---|
| Fungal (n = 24) |
Bacterial (n = 135) |
||
|
Duration (years) Mean ± SD |
17.08 ± 2.6 | 6.66 ± 5.63 | < 0.001** |
As regards fungal infection, CA infection was associated with a statistically significant longer duration of hearing aid usage than moulds infection. As regards bacterial infection, the longest duration of hearing aid usage was statistically significantly associated with Pseudomonas aeruginosa infection than Klebsiella and Staphylococcus aureus as shown in Table (4).
Table 4.
Relationship between duration of hearing aid usage and type of infection
| Fungi | P. value | ||||
|---|---|---|---|---|---|
| Candida albicans (n = 15) |
moulds (n = 9) |
||||
|
Duration (years) Mean ± SD |
18.33 ± 2.44 | 15 ± 1.12 | 0.001** | ||
| Bacteria | < 0.001** | ||||
| Gram negative bacilli | Gram-positive cocci | ||||
|
“Pseudomonas aeruginosa” (n = 18) |
“klebsiella” (n = 6) |
“Staphylococcus aureus” (n = 48) |
“Coagulase-negative staphylococci” (n = 63) |
||
|
Duration (years) Mean ± SD |
19.5 ± 0.62 | 12 ± 7.67 | 5.4 ± 0.94 | 3.44 ± 0.84 | |
As regards fungal infection, the prevalence of moulds infection in patients using BTE hearing aid was statistically significantly higher than that of CA infections. The reverse occurred in patients with CIC hearing aids. As regards bacterial infection, the prevalence of SA infection in patients using BTE hearing aids was statistically significantly higher than that of other pathogens while in patients using CIC hearing aids the prevalence of CNS infection was statistically significantly higher than that of other pathogens as shown in Table (5).
Table 5.
Relationship between type of hearing aids and type of infection
| Type of hearing aid | Fungi | Total | P. value | |||
|---|---|---|---|---|---|---|
|
Candida albicans
(n = 15) |
moulds (n = 9) |
|||||
|
Behind the ear (BTE) No. (%) |
3 (27.3%) | 8 (72.7%) | 11 | 0.001** | ||
|
Complete in the canal (CIC) No. (%) |
12 (92.3%) | 1 (7.7%) | 13 | |||
| Type of hearing aid | Bacteria | Total | < 0.001** | |||
| Gram negative bacilli | Gram-positive cocci | |||||
|
“Pseudomonas aeruginosa” (n = 18) |
“klebsiella” (n = 6) |
“Staphylococcus aureus” (n = 48) |
“Coagulase-negative staphylococci” (n = 63) | |||
|
Behind the ear (BTE) No. (%) |
8 (15.1%) | 0 (0%) | 30 (56.6%) | 15 (28.3%) | 53 | |
|
Complete in the canal (CIC) No. (%) |
10 (12.2%) | 6 (7.3%) | 18 (22%) | 48 (58.5%) | 82 | |
Discussion
Hearing aids are widely used as a treatment modality for both sensorineural and conductive hearing loss. Although being a reliable tool for managing hearing loss, patient compliance with HA was undermined, this was attributed to several factors including side effects. Side effects of HA are usually minimal to moderate, the commonest of which is itching [3].
Itching was found to be a common consequence of HA application with a much higher incidence for patients using ear plugs with very significantly higher bacterial growth and colonization in itchy ears with ear plugs than in normal ears [18].
Due to its unique characteristics and anatomical structure, the external auditory canal harbors colonization of normal bacterial flora. In a study carried out by Stroman et al. (2001), they isolated 314 organisms from the external auditory canal and cerumen spiecems from 148 patients, only 16 canal and 17 cerumen patients had no growth, the majority of cultured organisms were Gram-positive 99%, and staphylococci represented 63% of the isolated flora. Meanwhile, Gram-negative bacteria were isolated from only 15 subjects; 4 of them were pseudomonas aeruginosa, and only 7 cases had fungal growth [8].
Our study recruited 150 HA patients who presented to our Clinic with pruritus; 126 patients (84%) were monaural hearing aided and 24 patients (16%) were binaural hearing aided. Fifteen samples (8.6%) were free from infection while 159 samples (91.4%) were positive for infection with a statistically significant difference between the free and infected samples (either bacterial or fungal). Out of the infected samples, 135 samples (77.6%) had bacterial infection and 24 samples (13.8%) had fungal infection. Out of bacterial infections, most of them were Gram + ve one (82.2%) with the normal external auditory canal commensal coagulase-negative Staphylococci representing the majority, while pathognomonic Staphylococcus aureus represents a considerable portion (48%). Although fungal growth was not the commonest, Candida albicans represented the majority. it was well established that the most significant favoring factor for fungal infection was the prolonged use of hearing aids (17.08 ± 2.6 for fungal vs. 6.66 ± 5.63 for bacterial growth). Meanwhile, the type of HA played a significant role in favoring SA growth in BTE HA in comparison to CNS in CIC HA.
It is well known that HA molds harbor a significant bacterial growth which is mostly Gram + ve bacteria from both CNS and SA, however Gram-ve isolations of Klebesilla and Pseudomonas aeruginosa were not uncommon, and even fungal growth mainly yeast was observed in HA molds [19, 20].
Itchy ears were swabbed in multiple studies for possible pathognomic growth. Although, bacterial growth in the form of coagulase-negative Staphylococci, Staphylococcus aureus even pseudomonas and anaerobes in addition to fungal infections, the majority have shown no growth at all, and allergic skin reactions and asthetosis are considered the major contributing factors for ear irritation in the absence of any microbial growth [15, 17].
Aleandri et al. (2019) compared bacterial flora in 57 HA users with 33 normal non-HA users. 41 different bacterial species 29 Gram + ve and 12 Gram -ve were identified. Bacteria considered part of the ear normal flora were the most common isolates. Among these, the majority were Coagulase-negative Staphylococci, followed by Corynebacterium spp., Bacillus spp., and other microorganisms. The prevalence of polymicrobial communities was found statistically significant in ears presenting signs of inflammation (2.5 ± 1.7 vs. 2.1 ± 1.3; P = 0.02) and in HA users (2.3 ± 1.2 vs. 1.7 ± 1.0; P = 0.002). Staphylococcus aureus and pseudomonas aeruginosa were only detected in patients presenting with signs of inflammation whether they were HA user groups or non-HA users [16].
In concordance with our study, Orji et al. (2014) compared the microbacterial flora of the external auditory canals of 32 patients with unilateral HA with the contralateral non-fitted ear, where canal debris, bacterial infections mainly in the form of CNS and SA and to lesser extent Pseudomonas and klebessila were identified. In addition, fungal growth and mixed exudates were all found to be significantly higher in HA ears than non-HA ones, and intorellable irritations and severe otitis externa were more common in HA groups which were considered a major contributing factor for HA non-tolerance [21].
Conclusion
The cul-de-sac nature of the external auditory canal makes it a natural harbor for many nonpathogenic commenesls. Moreover, this unique nature makes any alteration in the canal aeration and PH a contributing factor for pathological bacterial growth. Our study highlights microbial growth in patients with hearing aids who develop itching and pruritis denoting a significant growth of both pathological and non-pathognomic bacteria in addition to fungal growth. These findings shed light on the importance of continuous hygiene of well-fitted hearing aids and the proper development of otitis externa management protocols to prevent growing Hearing aid intolerance and subsequent abandonment.
Funding
Our study did not receive any funding support.
Declarations
Conflict of Interest
No conflict of interest for such study.
Footnotes
Publisher’s Note
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