Eur Arch Otorhinolaryngol DOI 10.1007/s00405-013-2675-x
OTOLOGY
Sensorineural hearing loss: a complication of acute otitis media in adults Joo Hyun Park • Sung Joon Park • Young Ho Kim Min-Hyun Park
•
Received: 24 May 2013 / Accepted: 19 August 2013 Ó Springer-Verlag Berlin Heidelberg 2013
Abstract We aim to evaluate the incidence and clinical manifestations of sensorineural hearing loss (SNHL) in adult patients with acute otitis media (AOM). Seventy-five patients (age [ 18 years; 83 ears) diagnosed with AOM between January 2008 and March 2011 at our clinic were enroled and retrospectively reviewed. We detected audiometrically confirmed SNHL during the course of AOM in eight patients. The clinical course, treatment, and audiometric final outcome of each case were reviewed. SNHL was associated with AOM in 8 out of 83 ears (9.3 %). The mean age of patients was 57.5 years, and the mean followup period was 21.1 months (range 0.6–46.3 months). The most common symptom was tinnitus. Mean bone conduction hearing threshold was 39.5 dB in pure tone audiometry. All patients showed high-frequency HL, and three showed pan-frequency HL. All patients were treated with oral antibiotics at the initial visit. Seven ears were treated with a combination of oral steroids. Myringotomy was also performed. Seven of eight patients showed improvement; however, 8 kHz thresholds were not improved. This suggested that the inflammation spread through the round window. The mean duration of recovery was 18.6 days. SNHL associated with AOM in adult patients occurs during the early phases of the disease course. High-frequency hearing was commonly affected and was well treated with oral antibiotics, myringotomy, and steroid therapy. Audiometry can be helpful for treating adult patients with
J. H. Park S. J. Park Y. H. Kim M.-H. Park (&) Department of Otorhinolaryngology-Head and Neck Surgery, Seoul Metropolitan Government-Seoul National University Boramae Medical Center, 425 Shindaebang-dong, Dongjak-gu, Seoul 156-707, South Korea e-mail:
[email protected]
AOM. Active treatment, including myringotomy, should be performed during the early phase, if SNHL is suspected. Keywords Acute otitis media Sensorineural hearing loss Hearing loss Bone conduction
Introduction Sensorineural hearing loss (SNHL) occurs in various types of otitis media [1, 2]. It is generally accepted that the inner ear is vulnerable to chronic suppurative otitis media, and chronic otitis media (COM) causes a decrease in cochlear function [3, 4]. Both chronic and acute otitis media (AOM) can affect cochlear function. Paparella et al. [5] have reported cases of temporary or permanent sensorineural high-frequency hearing loss during and after AOM. Global AOM incidence rate (new episodes per hundred people per year) was reported at 10.85 % but is variable among countries [6]. In the same study, a prevalence of otitis media-related hearing impairment, defined as permanent hearing loss of[25 dB in the best ear, was reported to be 30.82/10,000. Prevalence increases with age, with 9.34/10,000 occurrences in the first year of life and the highest prevalence (45.05 %) in the 65–74 age group. However, this includes hearing loss associated with chronic suppurative otitis media. Several studies suggest that the prevalence of SNHL associated with otitis media with effusion (OME), ranges from 1 to 20 % [2, 7, 8]. The round window membrane is very thin and it is the only soft tissue barrier between the middle and inner ear. In a human temporal bone study, the mean thickness of round window membrane was reported as 67.43 lm [9]. Therefore, inner ear damage with temporary or permanent threshold shift in OME is
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assumed to be mediated through the round window membrane [1]. The most common cause of severe otitis media complications in adults is AOM rather than COM. Labyrinthitis was observed in 15 % of complicated mastoiditis cases after AOM [10]. Few studies have reported the prevalence and features of SNHL associated with AOM in early stage. Therefore, we reviewed medical records of patients with AOM treated at our clinic to clarify the incidence and clinical features of SNHL associated with AOM.
improvement, slight improvement, or no recovery (Table 1) [11]. We applied this criterion rather than other alternatives though this classification is originally for sudden deafness. Comparisons between diseased and normal ears were performed using the Mann–Whitney U test. Wilcoxon signed-rank test was used for comparing pre- and posttreatment audiograms. Statistical analyses were performed using Statistical Package for the Social Sciences (SPSS) for Windows version 18.0. The criterion for statistical significance was set at P \ 0.05.
Materials and methods Results Seventy-five patients (age [ 18 years, 83 ears) who were diagnosed with AOM between January 2008 and March 2011 at University-based, secondary referral hospital were included in this study. The medical charts from the study participants were retrospectively reviewed. Twenty-five (33.3 %) of the patients were men, and 50 (66.7 %) were women. The mean age was 47.7 years (range 18–85 years), and the mean follow-up period was 28.0 months (range 3–328 months). The right ear was affected in 30 cases, the left ear in 37 cases, and both ears in 8 cases. From these cases, those that showed bone conduction (BC) loss of C30 dB at any three frequencies from 250 Hz through 8 kHz compared to normal opposite ear were selected and considered as having SNHL. We included eight patients with AOM to reveal associations with SNHL after an AOM episode. The demographics and clinical course of each case were reviewed and evaluated in detail. Medical or surgical treatments and their results were also evaluated. Patients were treated with oral antibiotics, otic antibiotic-steroid drops, and oral steroids, if required. Myringotomy was performed with or without ventilation tube insertion under local anesthesia. Audiologic results were evaluated as the mean of thresholds at the six frequencies (250, 500, 1,000, 2,000, 4,000 and 8,000 Hz). These values were obtained at each follow-up visit. Furuhashi classification was used in the evaluation of audiological improvement, with outcomes being classified as complete recovery, marked
Eight of 83 ears (75 patients) showed SNHL during AOM disease course; SNHL was considered etiologically related to AOM. The prevalence of SNHL in ears with AOM was 9.6 %. Two patients were male, and six were women. The mean age of this cohort was 57.5 years (age 32–68 years), and the mean follow-up period was 21.1 months (range 0.6–46.3 months). The right ear was affected in two cases, the left ear in 6. The initial presentation of the eight afflicted patients included otalgia, ear fullness, tinnitus, otorrhea, hearing loss, and dizziness. Tinnitus, which is atypical in AOM patients, was the most common complaint, while hearing loss was reported only in three patients. Demographics and clinical manifestations of each patient are summarized in Table 2. Four patients complained of hearing loss during the disease course that had developed on an average of 4.6 days after initial symptom. Patients visited clinics 3.6 days after symptom development. Symptoms experienced during the entire disease course are summarized in Table 2. Except one patient, the other patients complained of tinnitus. An audiometry analysis at the initial visit revealed SNHL in all patients. The mean thresholds for BC were 39.9 dB and those for air conduction (AC) were 53.9 dB. The mean speech reception threshold (SRT) was 51.8 dB, and speech discrimination score was 100 % in all patients. The average pure tone threshold of diseased and normal ears, according to frequency at the initial visit is
Table 1 Evaluation of hearing improvement [11] Complete recovery
All five frequencies of final audiogram are 20 dB or less or improvement to the same degree of hearing as in the unaffected ear
Marked improvement
PTA improvement [30 dB
Slight improvement
10 dB \PTA improvement \30 dB
No change
PTA improvement \10 dB
PTA arithmetic mean of the five frequencies. Five frequencies are 250, 500, 1,000, 2,000 and 4,000 Hz
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? ? ?
? ?
? L
L F 50
32
7
8
F
L 68
M
60
6
Tin tinnitus, Ota otalgia, HL hearing loss, EF ear fullness, Oto otorrhea, Fev fever, Dz dizziness, BC bone conduction, Ant antibiotics, M myringotomy, VTI ventilation tube insertion, CR complete recovery, PR partial recovery, NI no improvement
Tin
– CR
CR Ant ? Steroid ? VTI
Ant ? Steroid ? M 22.5
40 2
3
4
4
2 ?
10
HL
Tin PR
NI Ant ? Steroid
Ant ? Steroid ? VTI 48.8
50 – –
87
7
3
?
?
?
?
?
5
M
R
?
? R
L F 68
62
3
F
?
?
?
4
?
? R
L F 65
55
1
2
F
?
?
?
EF HL Ota Tin
66
Tin
Tin PR
CR Ant ? VTI
Ant ? Steroid ? VTI 56.3
35 3
14 14
3
8
? ?
5
Tin
Tin CR
CR Ant ? Steroid ? VTI
Ant ? Steroid ? VTI 32.5
33.8 8 12
6
0
Dz Oto
Fev
2
Treatment Initial BC (dB HL) Interval of steroid therapy, improving (day) Interval of HL-improving (day) Interval of symptom, HL (day) Symptoms during the disease course Side Sex Age No.
Table 2 Summary of eight patients with sensorineural hearing loss occurred during the course of acute otitis media
5
Audiological result
Remained symptom
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shown in Fig. 1. The mean BC threshold for all frequencies, except 250 Hz (P = 0.279), in diseased ears increased statistically compared with normal ears (P \ 0.05). All patients showed high-frequency hearing loss, and 3 showed pan-frequency hearing loss. All patients were administered oral antibiotics from the initial visit. The choice of antimicrobial was third-generation cephalosporin. Patients used antibiotics for an average of 12.8 days. Combination therapy consisting of oral steroids was provided for seven of eight patients (Fig. 2). The oral steroid protocol for sudden hearing loss in our clinic (48 mg methylprednisolone for 4 days, 40, 32, 24, and 16 and 8 mg for 2 days each) was applied for 14 days. Both myringotomy and ventilation tube insertion were performed in 7 ears, and myringotomy alone was performed in 1 ear. Hearing improvement was evaluated according to Furuhashi classification [11]. Seven out of eight ears (87.5 %) showed hearing improvement (complete recovery: 5, slightly improvement: 2, no improvement: 1), and the mean interval from hearing loss to improvement was 18.6 days (Fig. 2). No additional hearing loss was detected after recovery. Comparing pre- and post-treatment BC, significant improvement was observed for 2, 3, and 4 kHz (P \ 0.05). The mean BC threshold of 500 and 1 kHz also recovered to normal range (\25 dB), though their improvement was not statistically significant. However, BC was not changed for 250 Hz and 8 kHz (Fig. 3). Hearing threshold at 250 Hz was not affected at pre-treatment state and bone conduction threshold at 8 kHz was not improved significantly after treatment. All patients exhibited 100 % speech discrimination at the end of the follow-up. No patient required hearing rehabilitation such as hearing aids. Tinnitus was the most common symptom that remained after recovery (six ears).
Discussion In our study, the prevalence of SNHL that correlated with AOM was 9.6 % of all cases. BC hearing threshold were improved in seven out of eight ears (87.5 %) after treatment. Tinnitus was the most common symptom in patients with SNHL. The incidence of OM-induced SNHL may be underestimated because OM results in hearing loss at ultrahigh frequencies as well as transient hearing threshold shifts which cannot be easily detected using conventional hearing tests [2]. This study showed the incidence of the development of SNHL in adult AOM patients. Pure tone audiometry showed high frequency loss. Even SNHL loss was recovered, 8 kHz threshold was not improved and left increased thresholds. The round window membrane is the
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Eur Arch Otorhinolaryngol Fig. 1 The average pure tone threshold of a diseased ear (a) and a normal ear (b) according to the frequencies at initial visit. The average bone conduction (BC) threshold for all frequencies, except that for 250 Hz, increased statistically in diseased ears compared to normal ears (P \ 0.05)
Fig. 2 Overall disease course of SNHL associated with acute otitis media. D day, M month
major route from the middle ear to the inner ear because it is the only non-bony barrier between the two structures and its permeability is affected by exposure to inflammatory conditions [12]. The hearing results of this study suggested that round window was the main spread pathway of inflammation from middle ear to inner ear. Song et al. reported the eight cases of sensorineural hearing loss complicated by AOM. They used antibiotics, myringotomy and oral steroid for treatment of AOM and SNHL and seven out of eight patients (87.5 %) were improved after treatment [13]. In our results, even in the improved hearing results, threshold of 8 kHz was not improved significantly compared to pre-treatment state.
Fig. 3 Average pre-treatment and post-treatment bone conduction (BC) thresholds. Significant improvement was observed at 2, 3, 4 kHz after treatment (P \ 0.05)
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Our results correlate with previously reported data involving temporary hearing loss and high frequency vulnerability. Tinnitus that was the most common symptom after recovery in our study might be related to remind high frequency hearing impairment. It is known that middle ear inflammation leads to inner ear inflammation resulting in inner ear dysfunction [14]. The etiological relationship between SNHL and OME had previously been reported in 1 % patients in a study [8]. On the other hand, in another study involving children, the incidence of SNHL related to OME was reported to be 20 % [7]. Margolis et al. reported a case that developed transient SNHL during the course of AOM. They concluded that the mechanism of the SNHL might be due to diffusion of toxins through the round window membrane [15]. Paparella et al. [1] hypothesized that otitis media (OM) can cause temporary threshold shifts or permanent threshold shifts limited to the cochlear basal turn by passage of inflammatory agents through the round window membrane. In an experimental study of purulent otitis media, they confirmed that these types of hearing losses might be more susceptible to regional basal turn and temporary threshold shift. In parts of the cochlea, microscopic inflammatory changes were seen, especially in the perilymph of the basal turn. The characteristic histopathologic finding was serofibrinous precipitate in the perilymphatic space without pathologic changes in the organ of Corti [5]. Hyden et al. reported the pathogens of the complicated acute otitis media. They could identify pathogens in 13 out of 20 complicated AOM patients (65 %), and the pathogens were streptococci and staphylococci [16]. However,
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recently vaccination for Streptococcus pneumonia was widely performed and this pneumococcal conjugate vaccination has caused a shift in the predominant OM pathogens. Nontypable Haemophilus influenzae (NTHI) is becoming the most commonly isolated organism in OM [17]. A recent study with NTHI-induced OM emphasized a role of spiral ligament fibrocytes (SLFs), one of the most abundant inner ear cell types, in inner ear inflammation. They demonstrated that SLFs upregulate monocyte chemoattractant protein-1 (MCP-1/CCL2) in response to OM pathogens through TLR2-dependent NF-kB activation [18]. Another author suggested that transmission characteristics of the inner ear were altered by hydrops, probably due to endolymphatic hypertension. Such cochlear dysfunction was termed cochlear conductive deafness because no pathology in sensory or neural components was found to be consistent with SNHL [19]. A similar situation was detected in temporary threshold shift after noise trauma. Beyond the alteration in the integrity of the hair cell stereocilia, other changes, including subtle changes in the ionic composition of the inner ear fluids and changes in the ionic pumps at the stria vascularis, may account for the auditory dysfunction observed with noise trauma. There are examples of reversible SNHL due to reduced endocochlear direct current potential following anoxia and in systemic or topical round window application of loop diuretics. In these cases, no sensory or neural pathology was apparent via light microscopy despite reversible cochlear dysfunction. Therefore, any alteration in physical or chemical environments may be presently classified as sensorineural. However, BC threshold has been shown to be temporarily elevated by the presence of middle ear fluid in OME cases [20]. This could be because of the inhibition of the vibratory movements of the oval and/or round windows caused by the presence of the effusion. This phenomenon was eliminated after the insertion of ventilation tubes [21] and therefore, did not result in damage to the inner ear [22]. Likewise, BC hearing may also be affected by middle ear pathology, for example, fixed stapes or adhesions, although this mainly reflects sensorineural hearing function. A recent study reported a high incidence of SNHL in 43 patients (50 ears) with bullous myringitis [23]. Five of the total ears presenting with SNHL (10 %) mainly involved high frequencies, and hearing loss ranged from slight to severe. They also proposed explanations for SNHL involving Milligan’s theory from the early twentieth century about hemorrhagic effusion into the cochlea, viral neurotrophicity, and toxins absorbed from the middle ear via the oval and round windows into the inner ear [24]. However, no infected agents were cultured from the middle ear effusion or bullous fluid, and therefore, the reason for SNHL in the BM remains obscure.
In the current study, we noted that most patients completely recovered after treatment. This suggests that SNHL related to AOM, even if it does occur, does not permanently impair inner ear hearing after proper treatment. The results of this study indicate that we should be aware of the possible development of SNHL, which is especially common in high frequencies during the course of AOM.
Conclusion SNHL associated with AOM in adult patients occurred in the early phase of the disease course. High-frequency hearing was commonly affected, but was well treated with oral antibiotics, myringotomy, and steroid therapy. Therefore, in cases of adult AOM, audiometric evaluation of BC is essential and should be performed at the initial visit. If SNHL is detected, aggressive treatment, including steroid therapy, myringotomy, and ventilation tube insertion, should be considered to facilitate improvement. Conflict of interest The authors have no conflict of interest and no financial disclosures.
References 1. Paparella MM, Goycoolea MV, Meyerhoff WL (1980) Inner ear pathology and otitis media. A review. Ann Otol Rhinol Laryngol Suppl 89(3 Pt 2):249–253 2. Mutlu C, Odabasi AO, Metin K, Basak S, Erpek G (1998) Sensorineural hearing loss associated with otitis media with effusion in children. Int J Pediatr Otorhinolaryngol 46(3):179–184 3. da Costa SS, Rosito LP, Dornelles C (2009) Sensorineural hearing loss in patients with chronic otitis media. Eur Arch Otorhinolaryngol 266(2):221–224. doi:10.1007/s00405-0080739-0 4. Aviel A, Ostfeld E (1982) Acquired irreversible sensorineural hearing loss associated with otitis media with effusion. Am J Otolaryngol 3(3):217–222 5. Paparella MM, Morizono T, Le CT, Mancini F, Sipila P, Choo YB, Liden G, Kim CS (1984) Sensorineural hearing loss in otitis media. Ann Otol Rhinol Laryngol 93(6 Pt 1):623–629 6. Monasta L, Ronfani L, Marchetti F, Montico M, Vecchi Brumatti L, Bavcar A, Grasso D, Barbiero C, Tamburlini G (2012) Burden of disease caused by otitis media: systematic review and global estimates. PLoS One 7(4):e36226. doi:10.1371/journal.pone. 0036226 7. Arnold W, Ganzer U, Kleinmann H (1977) Sensorineural hearing loss in mucous otitis. Arch Otorhinolaryngol 215(1):91–93 8. Harada T, Yamasoba T, Yagi M (1992) Sensorineural hearing loss associated with otitis media with effusion. ORL J Otorhinolaryngol Relat Spec 54(2):61–65 9. Yoda S, Cureoglu S, Shimizu S, Morita N, Fukushima H, Sato T, Harada T, Paparella MM (2011) Round window membrane in Meniere’s disease: a human temporal bone study. Otol Neurotol 32(1):147–151. doi:10.1097/MAO.0b013e318200a0e0 10. Leskinen K, Jero J (2005) Acute complications of otitis media in adults. Clin Otolaryngol 30(6):511–516
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Eur Arch Otorhinolaryngol 11. Furuhashi A, Matsuda K, Asahi K, Nakashima T (2002) Sudden deafness: long-term follow-up and recurrence. Clin Otolaryngol Allied Sci 27(6):458–463 12. Ikeda K, Sakagami M, Morizono T, Juhn SK (1990) Permeability of the round window membrane to middle-sized molecules in purulent otitis media. Arch Otolaryngol Head Neck Surg 116(1): 57–60 13. Song JE, Sapthavee A, Cager GR, Saadia-Redleaf MI (2012) Pseudo-sudden deafness. Ann Otol Rhinol Laryngol 121(2): 96–99 14. Joglekar S, Morita N, Cureoglu S, Schachern PA, Deroee AF, Tsuprun V, Paparella MM, Juhn SK (2010) Cochlear pathology in human temporal bones with otitis media. Acta Otolaryngol 130(4):472–476. doi:10.3109/00016480903311252 15. Margolis RH, Nelson DA (1993) Acute otitis media with transient sensorineural hearing loss. A case study. Arch Otolaryngol Head Neck Surg 119(6):682–686 16. Hyden D, Akerlind B, Peebo M (2006) Inner ear and facial nerve complications of acute otitis media with focus on bacteriology and virology. Acta Otolaryngol 126(5):460–466. doi:10.1080/ 00016480500401043 17. Pichichero ME (2006) Pathogen shifts and changing cure rates for otitis media and tonsillopharyngitis. Clin Pediatr (Phila) 45(6): 493–502. doi:10.1177/0009922806290102
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18. Moon SK, Woo JI, Lee HY, Park R, Shimada J, Pan H, Gellibolian R, Lim DJ (2007) Toll-like receptor 2-dependent NF-kappaB activation is involved in nontypeable Haemophilus influenzae-induced monocyte chemotactic protein 1 up-regulation in the spiral ligament fibrocytes of the inner ear. Infect Immun 75(7):3361–3372. doi:10.1128/IAI.01886-06 19. Morizono T, Sikora MA (1984) Neurophysiologic assessment of endolymphatic hydrops. Ann Otol Rhinol Laryngol 93(3 Pt 1): 225–228 20. Sato H, Takahashi H, Hayashi M, Honjo I (1987) Bone conduction hearing in otitis media with effusion. Nihon Jibiinkoka Gakkai Kaiho 90(4):583–589 21. Draf W, Schulz P (1980) Insertion of ventilation tubes into the medical ear: results and complications. A seven-year review. Ann Otol Rhinol Laryngol Suppl 89(3 Pt 2):303–307 22. Muenker G (1980) Results after treatment of otitis media with effusion. Ann Otol Rhinol Laryngol Suppl 89(3 Pt 2):308–311 23. Drendel M, Yakirevitch A, Kerimis P, Migirov L, Wolf M (2012) Hearing loss in bullous myringitis. Auris Nasus Larynx 39(1):28–30. doi:10.1016/j.anl.2011.04.001 24. Goycoolea MV, Paparella MM, Juhn SK, Carpenter AM (1980) Oval and round window changes in otitis media. Potential pathways between middle and inner ear. Laryngoscope 90(8 Pt 1): 1387–1391
