€ cedag, F.* & Cerci, U.‡ Kahveci, O.K.,* Demirdal, U.S.,† Yu *Faculty of Medicine, Department of Otolaryngology, Afyon Kocatepe University, Afyonkarahisar, Turkey, †Faculty of Medicine, Department of Physical Training and Rehabilitation, Afyon Kocatepe University, Afyonkarahisar, Turkey, and ‡Faculty of Medicine, Department of Otolaryngology, Sifa University, Izmir, Turkey Accepted for publication 6 April 2014 Clin. Otolaryngol. 2014, 39, 145–149
Objective: Osteoporosis is a common metabolic disorder that causes progressive changes in bone structure. Metabolic changes and possible degeneration of middle ear ossicles or the cochlear capsule may cause hearing loss in patients with osteoporosis. The aim of this study was to evaluate the hearing function and otolaryngologic symptoms of patients with osteoporosis. Methods: One hundred patients with osteoporosis, 50 osteopenic patients and 25 healthy controls were evaluated prospectively. Bone mineral density (BMD) of patients was measured by dual-energy X-ray absorptiometry (DEXA). Otorhinolaryngologic examinations were performed on all patients together with an otologic symptoms survey, pure tone audiometry, word recognition test and distortion product otoacoustic emission (DPOAE).
Introduction
Osteoporosis is a common metabolic disorder of the bones that causes a large and growing health burden.1 Systemic impairment of bone mass and micro-architecture may result in fragility fractures.2 Age, low body mass index, previous fragility fractures, a family history of fractures, the use of glucocorticoids and active cigarette smoking are welldefined risk factors for osteoporosis, and dual-energy X-ray absorptiometry (DEXA) scanning was recommended in these patients for early diagnosis and preventive therapy.3 Previous studies hypothesised that middle ear ossicles could be affected by osteoporosis, consequently manifesting itself as a conductive hearing loss (CHL).4 However, there is no histological evidence that osteoporosis may cause mineral loss or micro-fractures in human middle ear ossicles. Correspondence: O.K. Kahveci, AKU Arastirma Hast, KBB AD, Izmir yolu 8.km, Afyonkarahisar 03200, Turkey. Tel.: +90 505 2184236; Fax: +90 272 2133066; e-mail: [email protected] This study was presented at 1st Global Otology Research Forum poster presentations, November 13, 2013, Antalya, Turkey. © 2014 John Wiley & Sons Ltd Clinical Otolaryngology 39, 145–149
Results: Patients with osteoporosis showed higher incidence of sensorineural type of hearing loss (SNHL). Mean pure tone audiometry findings of the patients and controls were significantly different in 500–8000 Hz frequencies (P < 0.01 for 500–2000 Hz, P < 0.05 for 4000–8000 Hz). Distortion product otoacoustic emission results of patients with osteoporosis at 6 kHz were significantly lower than controls and osteopenic patients (P < 0.05). Tinnitus complaints were remarkably higher in patients with osteoporosis (P < 0.01). No correlation was found between BMD scores and hearing levels. Conclusion: The data show that osteoporosis may be associated with SNHL. Cochlear dysfunction may play role in this hearing loss.
Clayton et al.5 found that patients with otosclerosis are more likely to have osteoporosis. Osteoporosis was also found associated with an increased risk of benign positional vertigo.6 These findings suggest that there may be a pathology in middle and/or inner ear of patients with osteoporosis. In our clinical practice, we usually observe that sensorineural hearing loss is more frequent than conductive hearing loss in patients with osteoporosis. Therefore, this study was performed to investigate hearing status, otolaryngologic symptoms and cochlear functions in patients with osteoporosis. Materials and methods
A prospective case–control study was carried out in the departments of otolaryngology and physical medicine and rehabilitation (PMR) in a university hospital. Institutional review board approval was received from the University Medical Ethics Committee. All women arriving for previously scheduled DEXA scans were invited to participate in the study. Bone mineral density 145
ORIGINAL ARTICLE
Patients with osteoporosis have higher incidence of sensorineural hearing loss
146 O.K. Kahveci et al.
(BMD) was measured by DEXA (Hologic Q DR 4500 W), at both the lumbar spine (anteroposterior projection of L1-L4) and the proximal femur (total score). Osteoporosis is defined as T score below 2.5 at any projection, whereas osteopenia is defined as T score between 1 and 2.5 according to the WHO guidelines.7,8 According to DEXA results, patients were divided into osteoporosis and osteopenia groups. One hundred patients with osteoporosis (200 ears), 50 osteopenia patients (100 ears) and 25 control cases (50 ears) were enrolled into study. All of the control cases were women and they were chosen among healthy relatives of patients who were admitted to the department of otolaryngology. The patients who had acute or chronic otitis media or a history of ototoxic drug use, noise exposure, ear surgery, cranial trauma, neurovascular disease, congenital hearing loss, malignant or benign neoplasm of the ear and brain, sudden hearing loss and kidney disease were excluded from study. All patients and controls were underwent a complete ear, nose and throat examination in the otolaryngology department, and a survey about vertigo, tinnitus, facial nerve function, family history of hearing loss and medical drug use was obtained. After examination and survey, audiometric evaluations were performed. Pure tone air and bone audiometry at 250, 500, 1, 2, 4 and 8 kHz were performed. Word recognition score (WRS) was also evaluated with a diagnostic audiometer (Interacoustics AD229e; Interacoustics A/S, Assens, Denmark). Distortion product otoacoustic emissions (DPOAE) were performed at 1, 1.4, 2, 2.8, 4 and 6 kHz frequencies using Otodynamics ILO 288 Echoport equipment (Otodynamics Ltd., London, UK). All DPOAE and audiometric measurements were performed in a soundproof room by the same audiometrist who was blinded to the parameters of this study. Sensorineural hearing loss was defined as having a bone conduction average higher than 25 dB HL with no air-bone gap. Conductive hearing loss was defined as having a normal bone conduction threshold average, but an air-bone gap more than 10 dB HL. Mixed hearing loss was defined as having bone and air conduction threshold averages higher than 25 dB HL with an air-bone gap more than 10 dB HL.
Because DPOAE results would be affected by the presence of a conductive hearing loss, the ears with air-bone gap higher than 20 dB HL (Four, two and two ears of osteoporotic, osteopenic patients and controls, respectively) were not included in the DPOAE data analyses. Statistical analyses were performed using SPSS for IBM (Version 20; SPSS Inc., Chicago, IL, USA). Analysis of covariance (ANCOVA) was used to analyse differences between audiologic data of three groups. Age was included in the ANCOVA as covariate. For intergroup frequency comparison, the chi-square or Fisher’s exact test was used according to the sample size. Spearman’s correlation coefficient was used to reveal correlations between data. Values of P < 0.05 were accepted as the statistical significance level. Results
The mean age of patients with osteoporosis, osteopenia patients and controls was 61.11 (range 26–85), 56.02 (range 22–83) and 55.16 (range 50–68) years, respectively. Other demographic characteristics of patients are shown in Table 1. Information of height and weight of patients was obtained by the PMR department. However, because the controls were chosen only among the relatives of otolaryngology patients, their height and weight data were missing. The mean value of L1-4 T scores, femur total T scores, spine BMD and femoral BMD scores was 2.83 (SD 0.86), 2.29 (SD 0.71), 0.84 (SD 0.01), 0.77 (SD 0.02) in patients with osteoporosis and 1.41 (SD 0.62), 1.42 (SD 0.72), 1.02 (SD 0.97) and 0.86 (SD 0.15) in osteopenic patients, respectively. ENT examination and a survey about ENT complaints showed that tinnitus was more common in patients with osteoporosis than osteopenic patients and controls (P < 0.01). Vertigo, facial nerve function, examination findings of tympanic membrane and family history of hearing loss did not show any statistically significant difference between patients with osteoporosis and other groups (P > 0.05) and also between controls and osteopenic patients (P > 0.05) (Table 2). Sensorineural type of hearing loss was found in 72 ears of osteoporotic, 20 ears of osteopenic patients and four ears of
Table 1. Demographic characteristics of patients and controls
Mean age (Years) Mean height (cm) Mean weight (kg) HT (n) DM (n)
Osteoporosis
Osteopenia
Control
P (osteoporosis osteopenia)
P (osteoporosis control)
61.11 152.95 70.19 36 13
56.02 157.02 75.7 10 5
55.16 N/A N/A 5 4
>0.05 0.05 >0.05 >0.05
>0.05 N/A N/A >0.05 >0.05
HT, hypertension disease; DM, diabetes mellitus disease. © 2014 John Wiley & Sons Ltd Clinical Otolaryngology 39, 145–149
Hearing loss in osteoporosis
Table 2. Examination findings and survey results in patients and controls Osteoporosis Osteopenia Controls Tinnitus (n*) Vertigo (n*) History of facial paralysis (n*) Family history of hearing loss (n*) Membrane perforation (n†)
42‡ 7 1
9 5 0
3 0 0
8
1
0
2
1
0
*Number of patients. Number of ears. ‡ Statistically different from osteopenic patients and controls (P < 0.01 for both). †
control cases. CHL was found in three ears of osteoporotic, five ears of osteopenic patients and two ears of control cases. Mixed hearing loss was found in 10 ears of osteoporotic and only one ear of an osteopenic patient. The SNHL rate was significantly higher in patients with osteoporosis than osteopenic patients and controls (P < 0.01). The mean pure tone threshold (PTT) was 24.03 dB HL (SD 18.22) in patients with osteoporosis, 19.89 dB HL (SD 16.67) in osteopenic patients and 13.26 dB HL (SD 7.39) in control cases. The averages of pure tone thresholds in 500–8000 Hz were significantly different in patients with osteoporosis than controls (P < 0.01 for 500–2000 Hz, P < 0.05 for 4000– 8000 Hz). There was not any statistically significant difference between osteoporotic and osteopenic patients in any frequencies (Fig. 1). There was also a statistically significant difference between controls and osteopenic patients in 500– 2000 Hz (P < 0.01). Mean percentage of word recognition
Fig. 1. Audiometric results of patients and controls. © 2014 John Wiley & Sons Ltd Clinical Otolaryngology 39, 145–149
147
scores (WRSs) was 89.94% in patients with osteoporosis, 92.85% in osteopenic patients and 94.88% in controls. The difference between WRSs was not statistically significant between three groups (P > 0.05). The mean values of OAE results are shown in Figure 2. There were statistically significant differences in 6000 Hz frequencies between patients with osteoporosis and osteopenic patients and between patients with osteoporosis and controls (P < 0.05). Other frequencies showed no difference (P > 0.05). There were statistically significant differences in 2800 Hz frequency between osteopenic patients and controls and in 4000 Hz between osteoporotic and osteopenic patients (P < 0.01). Correlation studies revealed that there was a poor negative correlation between left femur total T scores and pure tone averages (r = 0.266, P < 0.01). Other DEXA scores did not show any correlation with any hearing results (P > 0.05). As expected, hearing and the age of patients showed very good correlation (r = 0.632, P < 0.01). Discussion
With progressive ageing of the population, there will be a huge increase in the prevalence of osteoporosis, which is considered to be one of the most common public health problems in the world.9 The increasing prevalence of osteoporosis is also related to substantial human, economic and social costs. It has been shown that the direct medical costs of hospitalisations for osteoporotic fractures in women and men already exceeded today the costs of hospitalisations of many other chronic diseases, such as major cardiovascular events (stroke, myocardial infarction and heart failure), breast cancer and chronic obstructive pulmonary disease.10 However, the impact of osteoporosis on hearing has not yet
148 O.K. Kahveci et al.
Fig. 2. Distortion product otoacoustic emission results of patients and controls.
been carefully considered. To the best of our knowledge, this is the first report to describe otorhinolaryngologic findings and hearing profile in such a large series of patients with osteoporosis. There are few reports in the literature regarding auditory involvement documenting a conductive hearing loss in patients with osteoporosis.4,11 It was hypothesised that osteoporosis may cause mineral loss in middle ear bones that results with CHL. On the other hand, in an animal study, the malleus in osteopetrotic mice was found contacted with the wall of the tympanic cavity, which was preventing auditory ossicles from vibrating and leading to hearing loss. This abnormal contact is likely because of the increased volume of auditory ossicles and the reduced volume of tympanic cavity.12 In contrast, we observed a sensorineural type of hearing loss in patients with osteoporosis as compared with the control population in our study. Similar to our study, Ozkiris et al.13 reported that patients with osteoporosis had worse hearing levels at high frequencies than controls in both bone conduction and air conduction thresholds. But the pathophysiological mechanism underlying this SNHL is not clear. SNHL could originate from sensorial or neural parts of hearing pathways. Sensorial loss occurs from damage in cochlea, and neural loss originates from pathology in acoustic nerve or above neural structures. DPOAE is convenient tool for the assessment of cochlear function to determine the site of pathological conditions associated with sensorineural hearing loss. DPOAEs, if normal, provide extremely strong evidence of normal cochlear function, regardless of audiometric data.14 Abnormal DPOAE findings are closely related to the loss of outer hair cells of the cochlea. In our study, especially DPOEs at high frequency (6 kHz) could not be obtained in osteoporotic patients. Pure tone thresholds were also significantly worse at high frequencies. The cochlea is organised tonotopically which means that the base end of the cochlea responds to high-frequency sounds while the apical aspect responds to the low frequency sounds.
The DPOAE study showed us that osteoporosis mainly affected the base of cochlea. On the other hand, audiometry revealed that there is more than this, because the hearing of osteoporotic patients was worse than controls in not only high frequencies but also in low and mid frequencies. With the limited data in the literature, it is not possible to ascertain an underlying mechanism of SNHL in osteoporosis, at present. Computed tomography (CT) evaluation studies of the cochlear capsule showed that hypodense regions were consistent with a greater degree of SNHL.15 This may show that demineralisation of cochlear capsule may result with SNHL. Further CT studies and OAE correlation should be performed in osteoporotic patients to explore such a relationship. Cochlear involvement may also cause problems in the vestibular system. The prevalence of osteopenia and osteoporosis had been found higher in patients with benign positional vertigo (BPV) than in controls.6 Osteoporotic patients also showed a significant increase in recurrence rate of BPV.16 In our study, seven patients (7%) in osteoporotic group, five patients (10%) in osteopenic group and none in control group had the complaint of vertigo. Statistically, this difference is not meaningful. Epidemiologic studies revealed that lifetime prevalence is 7.4% for vestibular vertigo and 2.4% for BPV.17,18 For our opinion, incidence of vertigo is not different from general population in osteoporotic patients. On the other hand, we found that osteoporotic patients have significantly much more tinnitus complaint than other groups. The underlying cause of tinnitus may be cochlear dysfunction and hearing loss in high frequencies. It should be also noted here that chi-square or Fisher’s exact test was used for intergroup comparisons for the prevalence rates of vertigo, tinnitus and type of hearing loss in our study. These statistical tests do not have potential for covariate analysis. For this reason, age covariate might have influence on interpreting our data. On the other hand, it was found © 2014 John Wiley & Sons Ltd Clinical Otolaryngology 39, 145–149
Hearing loss in osteoporosis
that symptoms were distributed homogonously in all age groups. Thus, if there is such misinterpretation, it could be minimal. The main limitation of our study was the low number of healthy control cases. Because the majority of advanced aged people have osteoporosis or at least osteopenia, it is not possible to find enough advanced aged healthy control cases. For this reason, we divided our patients into three groups. We think osteopenic patients could also be accepted as a control group, because they are not osteoporotic in the terms of definition by WHO study group.7 In conclusion, the current study is the first one that demonstrates that there is SNHL and an increased incidence of tinnitus in patients with osteoporosis. According to DPOAE results, SNHL in higher frequencies can be due to cochlear dysfunction. However, underlying pathology of SNHL in mid frequencies is not clear. The primary cause of hearing loss may be multifactorial and/or additional neural degeneration may play a role in SNHL. Further, OAE, ABR and CT studies should be performed to reveal the underlying pathology of SNHL in patients with osteoporosis. Conflicts of interest
The authors have no actual or potential conflict of interest in relation to this paper. Source of funding
No funding was used for research. References 1 Ewald D. (2012) Osteoporosis – prevention and detection in general practice. Aust. Fam. Physician 41, 104–108 2 Rachner T.D., Khosla S. & Hofbauer L.C. (2011) Osteoporosis: now and the future. Lancet 377, 1276–1287 3 Brown J.P. & Josse R.G., Scientific Advisory Council of the Osteoporosis Society of Canada. (2002) 2002 clinical practice guidelines for the diagnosis and management of osteoporosis in Canada. CMAJ 167(10 Suppl.), S1–S34.
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4 Babich M., Hoffmeister D., Doughty A. & (2009) Osteoporosis and conductive hearing loss: a novel model of clinical correlation. PHILICA.COM; Article number 148. 5 Clayton A.E., Mikulec A.A., Mikulec K.H. et al. (2014) Association between osteoporosis and otosclerosis in women. J. Laryngol. Otol. 118, 617–621 6 Jeong S.H., Choi S.H., Kim J.Y. et al. (2009) Osteopenia and osteoporosisin idiopathic benign positional vertigo. Neurology 72, 1069–1076 7 WHO study Group. (1994) Assessment of Fracture Risk and Its Application to Screening for Postmenopausal Osteoporosis. WHO study Group, Geneva. Technical Report 843 8 Lash R.W., Nicholson J.M., Velez L. et al. (2009) Diagnosis and management of osteoporosis. Prim. Care 36, 181–198 9 Perez Edo L., Alonso Ruiz A., Roig Vilaseca D. et al. (2011) [2011 Up-date of the consensus statement of the Spanish Society of Rheumatology on osteoporosis]. Reumatol. Clin. 7, 357–379 10 Lippuner K., Grifone S., Schwenkglenks M. et al. (2012) Comparative trends in hospitalizations for osteoporotic fractures and other frequent diseases between 2000 and 2008. Osteoporos. Int. 23, 829– 839 11 Henkin R.I., Lifschitz M.D. & Larson A.L. (1972) Hearing loss in patients with osteoporosis and Pagets disease of bone. Am. J. Med. Sci. 263, 383–392 12 Kanzaki S., Takada Y., Niida S. et al. (2011) Impaired vibration of auditory ossicles in osteopetrotic mice. Am. J. Pathol. 178, 270–278 13 Ozkirisß M., Karacßavusß S., Kapusuz Z. et al. (2013) Does bone mineral density have an effect on hearing loss in postmenopausal patients? Ann. Otol. Rhinol. Laryngol. 122, 648–652 14 Kimberley B.P. (1999) Applications of distortion-product emissions to an otological practice. Laryngoscope 109, 1908–1918 15 G€ uneri E.A., Ada E., Ceryan K. et al. (1996) High-resolution computed tomographic evaluation of the cochlear capsule in otosclerosis: relationship between densitometry and sensorineural hearing loss. Ann. Otol. Rhinol. Laryngol. 105, 659–664 16 Jang Y.S. & Kang M.K. (2009) Relationship between bone mineral density and clinical features in women with idiopathic benign paroxysmal positional vertigo. Otol. Neurotol. 30, 95–100 17 Neuhauser H.K., von Brevern M., Radtke A. et al. (2005) Epidemiology of vestibular vertigo: a neurotologic survey of the general population. Neurology 65, 898–904 18 von Brevern M., Radtke A., Lezius F. et al. (2007) Epidemiology of benign paroxysmal positional vertigo: a population based study. J. Neurol. Neurosurg. Psychiatry 78, 710–715
Objective: Osteoporosis is a common metabolic disorder that causes progressive changes in bone structure. Metabolic changes and possible degeneration of middle ear ossicles or the cochlear capsule may cause hearing loss in patients with osteoporosis. The aim of this study was to evaluate the hearing function and otolaryngologic symptoms of patients with osteoporosis. Methods: One hundred patients with osteoporosis, 50 osteopenic patients and 25 healthy controls were evaluated prospectively. Bone mineral density (BMD) of patients was measured by dual-energy X-ray absorptiometry (DEXA). Otorhinolaryngologic examinations were performed on all patients together with an otologic symptoms survey, pure tone audiometry, word recognition test and distortion product otoacoustic emission (DPOAE).
Introduction
Osteoporosis is a common metabolic disorder of the bones that causes a large and growing health burden.1 Systemic impairment of bone mass and micro-architecture may result in fragility fractures.2 Age, low body mass index, previous fragility fractures, a family history of fractures, the use of glucocorticoids and active cigarette smoking are welldefined risk factors for osteoporosis, and dual-energy X-ray absorptiometry (DEXA) scanning was recommended in these patients for early diagnosis and preventive therapy.3 Previous studies hypothesised that middle ear ossicles could be affected by osteoporosis, consequently manifesting itself as a conductive hearing loss (CHL).4 However, there is no histological evidence that osteoporosis may cause mineral loss or micro-fractures in human middle ear ossicles. Correspondence: O.K. Kahveci, AKU Arastirma Hast, KBB AD, Izmir yolu 8.km, Afyonkarahisar 03200, Turkey. Tel.: +90 505 2184236; Fax: +90 272 2133066; e-mail: [email protected] This study was presented at 1st Global Otology Research Forum poster presentations, November 13, 2013, Antalya, Turkey. © 2014 John Wiley & Sons Ltd Clinical Otolaryngology 39, 145–149
Results: Patients with osteoporosis showed higher incidence of sensorineural type of hearing loss (SNHL). Mean pure tone audiometry findings of the patients and controls were significantly different in 500–8000 Hz frequencies (P < 0.01 for 500–2000 Hz, P < 0.05 for 4000–8000 Hz). Distortion product otoacoustic emission results of patients with osteoporosis at 6 kHz were significantly lower than controls and osteopenic patients (P < 0.05). Tinnitus complaints were remarkably higher in patients with osteoporosis (P < 0.01). No correlation was found between BMD scores and hearing levels. Conclusion: The data show that osteoporosis may be associated with SNHL. Cochlear dysfunction may play role in this hearing loss.
Clayton et al.5 found that patients with otosclerosis are more likely to have osteoporosis. Osteoporosis was also found associated with an increased risk of benign positional vertigo.6 These findings suggest that there may be a pathology in middle and/or inner ear of patients with osteoporosis. In our clinical practice, we usually observe that sensorineural hearing loss is more frequent than conductive hearing loss in patients with osteoporosis. Therefore, this study was performed to investigate hearing status, otolaryngologic symptoms and cochlear functions in patients with osteoporosis. Materials and methods
A prospective case–control study was carried out in the departments of otolaryngology and physical medicine and rehabilitation (PMR) in a university hospital. Institutional review board approval was received from the University Medical Ethics Committee. All women arriving for previously scheduled DEXA scans were invited to participate in the study. Bone mineral density 145
ORIGINAL ARTICLE
Patients with osteoporosis have higher incidence of sensorineural hearing loss
146 O.K. Kahveci et al.
(BMD) was measured by DEXA (Hologic Q DR 4500 W), at both the lumbar spine (anteroposterior projection of L1-L4) and the proximal femur (total score). Osteoporosis is defined as T score below 2.5 at any projection, whereas osteopenia is defined as T score between 1 and 2.5 according to the WHO guidelines.7,8 According to DEXA results, patients were divided into osteoporosis and osteopenia groups. One hundred patients with osteoporosis (200 ears), 50 osteopenia patients (100 ears) and 25 control cases (50 ears) were enrolled into study. All of the control cases were women and they were chosen among healthy relatives of patients who were admitted to the department of otolaryngology. The patients who had acute or chronic otitis media or a history of ototoxic drug use, noise exposure, ear surgery, cranial trauma, neurovascular disease, congenital hearing loss, malignant or benign neoplasm of the ear and brain, sudden hearing loss and kidney disease were excluded from study. All patients and controls were underwent a complete ear, nose and throat examination in the otolaryngology department, and a survey about vertigo, tinnitus, facial nerve function, family history of hearing loss and medical drug use was obtained. After examination and survey, audiometric evaluations were performed. Pure tone air and bone audiometry at 250, 500, 1, 2, 4 and 8 kHz were performed. Word recognition score (WRS) was also evaluated with a diagnostic audiometer (Interacoustics AD229e; Interacoustics A/S, Assens, Denmark). Distortion product otoacoustic emissions (DPOAE) were performed at 1, 1.4, 2, 2.8, 4 and 6 kHz frequencies using Otodynamics ILO 288 Echoport equipment (Otodynamics Ltd., London, UK). All DPOAE and audiometric measurements were performed in a soundproof room by the same audiometrist who was blinded to the parameters of this study. Sensorineural hearing loss was defined as having a bone conduction average higher than 25 dB HL with no air-bone gap. Conductive hearing loss was defined as having a normal bone conduction threshold average, but an air-bone gap more than 10 dB HL. Mixed hearing loss was defined as having bone and air conduction threshold averages higher than 25 dB HL with an air-bone gap more than 10 dB HL.
Because DPOAE results would be affected by the presence of a conductive hearing loss, the ears with air-bone gap higher than 20 dB HL (Four, two and two ears of osteoporotic, osteopenic patients and controls, respectively) were not included in the DPOAE data analyses. Statistical analyses were performed using SPSS for IBM (Version 20; SPSS Inc., Chicago, IL, USA). Analysis of covariance (ANCOVA) was used to analyse differences between audiologic data of three groups. Age was included in the ANCOVA as covariate. For intergroup frequency comparison, the chi-square or Fisher’s exact test was used according to the sample size. Spearman’s correlation coefficient was used to reveal correlations between data. Values of P < 0.05 were accepted as the statistical significance level. Results
The mean age of patients with osteoporosis, osteopenia patients and controls was 61.11 (range 26–85), 56.02 (range 22–83) and 55.16 (range 50–68) years, respectively. Other demographic characteristics of patients are shown in Table 1. Information of height and weight of patients was obtained by the PMR department. However, because the controls were chosen only among the relatives of otolaryngology patients, their height and weight data were missing. The mean value of L1-4 T scores, femur total T scores, spine BMD and femoral BMD scores was 2.83 (SD 0.86), 2.29 (SD 0.71), 0.84 (SD 0.01), 0.77 (SD 0.02) in patients with osteoporosis and 1.41 (SD 0.62), 1.42 (SD 0.72), 1.02 (SD 0.97) and 0.86 (SD 0.15) in osteopenic patients, respectively. ENT examination and a survey about ENT complaints showed that tinnitus was more common in patients with osteoporosis than osteopenic patients and controls (P < 0.01). Vertigo, facial nerve function, examination findings of tympanic membrane and family history of hearing loss did not show any statistically significant difference between patients with osteoporosis and other groups (P > 0.05) and also between controls and osteopenic patients (P > 0.05) (Table 2). Sensorineural type of hearing loss was found in 72 ears of osteoporotic, 20 ears of osteopenic patients and four ears of
Table 1. Demographic characteristics of patients and controls
Mean age (Years) Mean height (cm) Mean weight (kg) HT (n) DM (n)
Osteoporosis
Osteopenia
Control
P (osteoporosis osteopenia)
P (osteoporosis control)
61.11 152.95 70.19 36 13
56.02 157.02 75.7 10 5
55.16 N/A N/A 5 4
>0.05 0.05 >0.05 >0.05
>0.05 N/A N/A >0.05 >0.05
HT, hypertension disease; DM, diabetes mellitus disease. © 2014 John Wiley & Sons Ltd Clinical Otolaryngology 39, 145–149
Hearing loss in osteoporosis
Table 2. Examination findings and survey results in patients and controls Osteoporosis Osteopenia Controls Tinnitus (n*) Vertigo (n*) History of facial paralysis (n*) Family history of hearing loss (n*) Membrane perforation (n†)
42‡ 7 1
9 5 0
3 0 0
8
1
0
2
1
0
*Number of patients. Number of ears. ‡ Statistically different from osteopenic patients and controls (P < 0.01 for both). †
control cases. CHL was found in three ears of osteoporotic, five ears of osteopenic patients and two ears of control cases. Mixed hearing loss was found in 10 ears of osteoporotic and only one ear of an osteopenic patient. The SNHL rate was significantly higher in patients with osteoporosis than osteopenic patients and controls (P < 0.01). The mean pure tone threshold (PTT) was 24.03 dB HL (SD 18.22) in patients with osteoporosis, 19.89 dB HL (SD 16.67) in osteopenic patients and 13.26 dB HL (SD 7.39) in control cases. The averages of pure tone thresholds in 500–8000 Hz were significantly different in patients with osteoporosis than controls (P < 0.01 for 500–2000 Hz, P < 0.05 for 4000– 8000 Hz). There was not any statistically significant difference between osteoporotic and osteopenic patients in any frequencies (Fig. 1). There was also a statistically significant difference between controls and osteopenic patients in 500– 2000 Hz (P < 0.01). Mean percentage of word recognition
Fig. 1. Audiometric results of patients and controls. © 2014 John Wiley & Sons Ltd Clinical Otolaryngology 39, 145–149
147
scores (WRSs) was 89.94% in patients with osteoporosis, 92.85% in osteopenic patients and 94.88% in controls. The difference between WRSs was not statistically significant between three groups (P > 0.05). The mean values of OAE results are shown in Figure 2. There were statistically significant differences in 6000 Hz frequencies between patients with osteoporosis and osteopenic patients and between patients with osteoporosis and controls (P < 0.05). Other frequencies showed no difference (P > 0.05). There were statistically significant differences in 2800 Hz frequency between osteopenic patients and controls and in 4000 Hz between osteoporotic and osteopenic patients (P < 0.01). Correlation studies revealed that there was a poor negative correlation between left femur total T scores and pure tone averages (r = 0.266, P < 0.01). Other DEXA scores did not show any correlation with any hearing results (P > 0.05). As expected, hearing and the age of patients showed very good correlation (r = 0.632, P < 0.01). Discussion
With progressive ageing of the population, there will be a huge increase in the prevalence of osteoporosis, which is considered to be one of the most common public health problems in the world.9 The increasing prevalence of osteoporosis is also related to substantial human, economic and social costs. It has been shown that the direct medical costs of hospitalisations for osteoporotic fractures in women and men already exceeded today the costs of hospitalisations of many other chronic diseases, such as major cardiovascular events (stroke, myocardial infarction and heart failure), breast cancer and chronic obstructive pulmonary disease.10 However, the impact of osteoporosis on hearing has not yet
148 O.K. Kahveci et al.
Fig. 2. Distortion product otoacoustic emission results of patients and controls.
been carefully considered. To the best of our knowledge, this is the first report to describe otorhinolaryngologic findings and hearing profile in such a large series of patients with osteoporosis. There are few reports in the literature regarding auditory involvement documenting a conductive hearing loss in patients with osteoporosis.4,11 It was hypothesised that osteoporosis may cause mineral loss in middle ear bones that results with CHL. On the other hand, in an animal study, the malleus in osteopetrotic mice was found contacted with the wall of the tympanic cavity, which was preventing auditory ossicles from vibrating and leading to hearing loss. This abnormal contact is likely because of the increased volume of auditory ossicles and the reduced volume of tympanic cavity.12 In contrast, we observed a sensorineural type of hearing loss in patients with osteoporosis as compared with the control population in our study. Similar to our study, Ozkiris et al.13 reported that patients with osteoporosis had worse hearing levels at high frequencies than controls in both bone conduction and air conduction thresholds. But the pathophysiological mechanism underlying this SNHL is not clear. SNHL could originate from sensorial or neural parts of hearing pathways. Sensorial loss occurs from damage in cochlea, and neural loss originates from pathology in acoustic nerve or above neural structures. DPOAE is convenient tool for the assessment of cochlear function to determine the site of pathological conditions associated with sensorineural hearing loss. DPOAEs, if normal, provide extremely strong evidence of normal cochlear function, regardless of audiometric data.14 Abnormal DPOAE findings are closely related to the loss of outer hair cells of the cochlea. In our study, especially DPOEs at high frequency (6 kHz) could not be obtained in osteoporotic patients. Pure tone thresholds were also significantly worse at high frequencies. The cochlea is organised tonotopically which means that the base end of the cochlea responds to high-frequency sounds while the apical aspect responds to the low frequency sounds.
The DPOAE study showed us that osteoporosis mainly affected the base of cochlea. On the other hand, audiometry revealed that there is more than this, because the hearing of osteoporotic patients was worse than controls in not only high frequencies but also in low and mid frequencies. With the limited data in the literature, it is not possible to ascertain an underlying mechanism of SNHL in osteoporosis, at present. Computed tomography (CT) evaluation studies of the cochlear capsule showed that hypodense regions were consistent with a greater degree of SNHL.15 This may show that demineralisation of cochlear capsule may result with SNHL. Further CT studies and OAE correlation should be performed in osteoporotic patients to explore such a relationship. Cochlear involvement may also cause problems in the vestibular system. The prevalence of osteopenia and osteoporosis had been found higher in patients with benign positional vertigo (BPV) than in controls.6 Osteoporotic patients also showed a significant increase in recurrence rate of BPV.16 In our study, seven patients (7%) in osteoporotic group, five patients (10%) in osteopenic group and none in control group had the complaint of vertigo. Statistically, this difference is not meaningful. Epidemiologic studies revealed that lifetime prevalence is 7.4% for vestibular vertigo and 2.4% for BPV.17,18 For our opinion, incidence of vertigo is not different from general population in osteoporotic patients. On the other hand, we found that osteoporotic patients have significantly much more tinnitus complaint than other groups. The underlying cause of tinnitus may be cochlear dysfunction and hearing loss in high frequencies. It should be also noted here that chi-square or Fisher’s exact test was used for intergroup comparisons for the prevalence rates of vertigo, tinnitus and type of hearing loss in our study. These statistical tests do not have potential for covariate analysis. For this reason, age covariate might have influence on interpreting our data. On the other hand, it was found © 2014 John Wiley & Sons Ltd Clinical Otolaryngology 39, 145–149
Hearing loss in osteoporosis
that symptoms were distributed homogonously in all age groups. Thus, if there is such misinterpretation, it could be minimal. The main limitation of our study was the low number of healthy control cases. Because the majority of advanced aged people have osteoporosis or at least osteopenia, it is not possible to find enough advanced aged healthy control cases. For this reason, we divided our patients into three groups. We think osteopenic patients could also be accepted as a control group, because they are not osteoporotic in the terms of definition by WHO study group.7 In conclusion, the current study is the first one that demonstrates that there is SNHL and an increased incidence of tinnitus in patients with osteoporosis. According to DPOAE results, SNHL in higher frequencies can be due to cochlear dysfunction. However, underlying pathology of SNHL in mid frequencies is not clear. The primary cause of hearing loss may be multifactorial and/or additional neural degeneration may play a role in SNHL. Further, OAE, ABR and CT studies should be performed to reveal the underlying pathology of SNHL in patients with osteoporosis. Conflicts of interest
The authors have no actual or potential conflict of interest in relation to this paper. Source of funding
No funding was used for research. References 1 Ewald D. (2012) Osteoporosis – prevention and detection in general practice. Aust. Fam. Physician 41, 104–108 2 Rachner T.D., Khosla S. & Hofbauer L.C. (2011) Osteoporosis: now and the future. Lancet 377, 1276–1287 3 Brown J.P. & Josse R.G., Scientific Advisory Council of the Osteoporosis Society of Canada. (2002) 2002 clinical practice guidelines for the diagnosis and management of osteoporosis in Canada. CMAJ 167(10 Suppl.), S1–S34.
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