Hearing loss is a common chronic and disabling condition. The prevalence of hearing loss in the United States increases with age and has been reported to be approximately 55% in the population over 70 years of age (1). Osteoporosis is a systemic skeletal disorder characterized by microarchitectural deterioration of bone tissue (2). Both hearing loss and osteoporosis can decrease quality of life (3,4), and the incidence rates of both are expected to increase further with societal aging. Risk factors that influence the degree and rate of hearing loss include aging, genetic background, exposure to ototoxic agents, otologic diseases, and exposure to noise (5). Osteoporosis has been identified as a risk factor for hearing loss (6). A previous study suggested that demineralization of bone affects the temporal bones, which include the cochlea and vestibules (7), and hypothesized that the inner ear could be affected by osteoporosis. However, there are controversies and inconsistent results regarding the association between osteoporosis and hearing loss (5,8). A meta-analysis that found a correlation between bone mineral density (BMD) and hearing loss reported an odds ratio of only 1.20 (range, 0.83–4.50) (6).
Although several screening and diagnostic tools are available for assessment of BMD (9), dual-energy x-ray absorptiometry (DXA) of the central skeleton is considered the gold standard. The World Health Organization international reference standard for diagnosing osteoporosis is evaluation of relative bone quality at the femoral neck and lumbar spine, particularly in postmenopausal women and men older than 50 years (10). Most studies of the relationship between hearing loss and osteoporosis in patients have used DXA to assess bone quality. However, DXA could have a limitation in terms of reflecting regional bone quality (2). Direct assessment of bone quality around the cochlea might be required to determine whether hearing loss is associated with temporal bone quality.
Conventional CT have been widely used to assess a variety of ear problems. Previous studies have demonstrated the potential of CT of the spine or extremities as a screening tool for bone quality (2,11–13). The aims of this study were to evaluate the correlation between bone quality around the skull assessed on temporal bone CT and BMD of the central skeleton based on DXA and to assess the correlation between bone quality and hearing level.
MATERIALS AND METHODS
This retrospective study was approved by the Institutional Review Board at our hospital. The need for informed consent was waived in view of the retrospective nature of the research.
We reviewed the medical records of consecutive patients who underwent pure-tone audiometry (PTA) at our institution and had normal otoscopic findings. Patients who also underwent a temporal bone CT scan within a 3-month interval of their DXA examination were included in the study. The PTA results on the healthy side were analyzed if the patient had otologic disease that could affect hearing level. The PTA results for the right ear were used for analysis in patients who had any other underlying pathology affecting their hearing threshold to avoid duplication of patient demographics (14).
The exclusion criteria were bilateral external or middle ear disease, a history of a brain disorder such as stroke, a diagnosis of otosclerosis, congenital cochleovestibular malformation, and previous or current cochlear implantation.
Demographic data, including patient age at the time of examination, sex, and diagnosis, were collected from the medical records. Hearing thresholds were measured using an audiometer at 0.25, 0.5, 1, 2, and 4 kHz. The average hearing threshold was calculated as the pure tone average at all five frequencies, and the pure tone thresholds at 0.25 and 0.5 kHz were averaged to calculate the hearing level of low frequencies and at 2 and 4 kHz for high frequencies. DXA was performed using a Lunar Prodigy Advance scanner (GE Healthcare, Milwaukee, WI) at both the lumbar spine and proximal femur. All patients underwent high-resolution temporal bone CT using a 64-detector Light Speed VCT Optima 660 scanner (General Electric, Waukesha, WI) with the following imaging parameters: helical thickness 0.625 mm, reconstruction interval 0.625 mm, pitch 0.531, rotation time 0.6 seconds, kVp 100, mA 335, matrix 512 × 512, and display field of view 18 cm. All DXA and CT images were digitally acquired using a picture archiving and communication system (PACS, Marosis, M-view 5.4; Marotech, Seoul, South Korea), and measurements were subsequently carried out using PACS software.
Consensus Building and Measurement of Parameters
In view of the lack of a standard method for assessment of bone attenuation around the inner ear, a consensus-building session was held before measuring the CT images. The panel decided that bone attenuation at the clivus and inner ear and the cortical thickness of the occiput should be measured on CT images. Previous studies demonstrated that bone attenuation measured by placing a circular region of interest (ROI) on each bony region on CT images was correlated with BMD measured by DXA (2,11–13), and that the cortical thickness of bone has the potential to predict BMD (15). Given that a large part of the skull consists of cortical bone, cortical bone of the skull should also be measured.
The following method was used to measure each anatomic region on CT images. First, an axial image that exposed all cochlear turns was selected. This was confirmed using the dynamic navigation tool of the PACS software. A circular ROI with an area in the range of 4 to 6 mm2 was placed on the center of the clivus and included the area of the petrous apex near the cochlea (Fig. 1). On the same axial image, the occiput, defined as the area between the bilateral lambdoid suture line, was divided into four regions. Cortical thickness was measured on four points of the occiput (Fig. 1), and the mean values of these four measurements were used in the analysis.
Following consensus-building, a reliability test was performed before recording the main measurements. Interobserver reliability was determined using the intraclass correlation coefficients (ICCs) for three physicians, each with 4 years of clinical experience. These three physicians performed the measurements on each CT image without knowledge of the other physicians’ measurements (2). Four weeks after the interobserver reliability test, one of the physician repeated the measurements to assess intraobserver reliability.
Reliability was assessed using ICCs and a two-way random effects model, assuming a single measurement and absolute agreement (16). Using an ICC target value of 0.8, Bonett approximation was used, setting 0.2 as the width of 95% confidence intervals (17). The minimum sample size was calculated to be 36. ICC values more than 0.8 were considered to indicate excellent reliability. The Kolmogorov–Smirnov test was used to verify the normality of distribution of continuous variables. Using partial correlation analysis, the correlation between the measurements on the CT images and DXA variables were analyzed after controlling for the effect of age and sex. The correlation between the measurements on the CT image and the unilateral bone conduction hearing threshold was also analyzed after controlling for the effect of age and sex. The statistical analyses were conducted using SAS version 9.2 software (SAS Institute, Cary, NC). All statistical tests were 2-tailed, and p-values <0.05 were considered to be statistically significant.
A total of 110 patients met the inclusion criteria. After implementation of the exclusion criteria, 101 ears from 101 patients (15 men, 86 women) were included in the study (Fig. 2). The mean patient age at the time of examination was 64.4 ± 12.7 (range, 21–90) years. The most common diagnosis was unilateral sensorineural hearing loss (23.7%) followed by tinnitus (14.9%; Table 1).
Measurements of bone attenuation at the clivus and inner ear and of the cortical thickness of the occipital bone showed good to excellent reliability. Intraobserver reliability of all measurements showed a higher ICC value than interobserver reliability. Intraobserver and interobserver reliability was highest for the clivus (ICCs, 0.945 and 0.884, respectively). Intraobserver and interobserver reliability values were lowest for cortical thickness of the occipital bone (ICC, 0.864) and bone attenuation of the right inner ear (ICC, 0.728; Table 2).
Bone attenuation of the skull and cortical thickness of the occipital bone on CT did not reflect BMD of the central skeleton on DXA. After adjusting for patient age and sex, there was no significant correlation between the measurements on CT scan and BMD on DXA, except for a correlation between bone attenuation of the clivus and trochanteric BMD (correlation coefficient, 0.218, p = 0.036; Table 3).
Bone conduction on PTA partially correlated with BMD on DXA. The average threshold of bone conduction showed significant correlations with BMD at the femoral neck (correlation coefficient, −0.241, p = 0.020) and trochanter (correlation coefficient −0.244, p = 0.018), but there was no significant correlation between the average threshold of bone conduction and BMD at the lumbar spine (p = 0.177–0.332). There was no statistically significant difference in the average threshold of bone conduction between patients diagnosed as having osteoporosis and patients with osteopenia or normal BMD (p = 0.587). Further, the bone conduction hearing threshold did not show a significant correlation with bone attenuation of the skull or cortical thickness of the occipital bone on CT (Table 4).
Although BMD of the central skeleton on DXA might have a limited ability to reflect regional bone quality, most studies of the relationship between hearing loss and osteoporosis have used DXA to assess bone quality in patients. Therefore, the aim of this study was to evaluate the correlation between bone quality around the inner ear and hearing level. We assessed the bone quality by temporal bone CT and BMD based on DXA of the central skeleton. We could not find a relationship between bone quality of the skull, including the otic capsule, and the BMD of the central skeleton. The average threshold of bone conduction did not show a significant correlation with central or regional bone quality, except for BMD at the femoral neck and trochanter.
In the present study, we focused on regional bone quality. A previous study showed that DXA, which is the gold standard tool for diagnosing osteoporosis, might have a limited ability to reflect regional bone quality (2). Of the several screening tools that have been suggested for assessing regional bone quality, we used temporal bone CT because conventional CT is widely used and easily performed. There have been several studies of the validity of conventional CT for assessment of bone quality (11–13). A conventional CT evaluation study of the cochlear capsule demonstrated that hypodense regions were consistent with a greater degree of sensorineural hearing loss (18). Another study showed that the ROI on conventional CT had excellent validity and reliability as a screening tool for osteoporosis (11). However, there have been no studies of the reliability of bone attenuation for measuring bone quality of the skull in this regard. In our study, the intraobserver and interobserver reliability of the measurements showed excellent ICC values, the highest being for the ROI on the clivus. The ROI value for bone can be greatly influenced by the area of radio-opacity and its heterogeneity. Because the inner ear consists of cortical bone, the reliability of the ROI for the inner ear might be lower than that for the clivus. We did not find a correlation between bone attenuation of the skull or the cortical thickness of the occipital bone on CT with BMD of the central skeleton on DXA. Although there was a correlation between BMD at the trochanter and bone attenuation at the clivus, it cannot be assumed that bone attenuation at the clivus “partially” reflects the BMD of the central skeleton. DXA assesses the quality of the central bone, both cortical and trabecular, at the spine and femur. The finding that the bone quality of the skull was different to that of the central skeleton may be explained by the fact that the skull is not a weight-bearing structure. Bone demineralization of the skull can occur in severe osteoporosis (19). However, it is known that physical activity increases bone mass because sufficient skeletal loading stimulates net bone formation at stressed skeletal sites (20,21). The spine and femur are weight-bearing skeletal elements, and the BMD of the central skeleton can be affected by physical activity. In contrast, the skull is not a weight-bearing skeletal element, which might account for the weak correlation between bone attenuation of the skull and the BMD of the central skeleton.
A previous study identified an association between BMD and hearing loss in patients with pathologic bone disorders such as otosclerosis (22). Although the exact mechanism of this association is unclear, it has been suggested that demineralization of the otic capsule or cochlea is associated with secondary neuronal degeneration, resulting in sensorineural hearing loss (18,23). Decreased skull bone density has also been documented in individuals with osteoporosis related to hyperthyroidism, and changes in the petrous portion of the temporal bone have been seen in patients with severe osteoporosis (19). However, epidemiologic studies have yielded inconsistent results. A study in African–American and Caucasian populations demonstrated that hearing loss was only associated with BMD in African–American men but not in women or in the Caucasian population (24). Another study that included multiple racial groups did not identify any race-related differences in hearing loss (8). Further studies of other factors that potentially affect hearing levels are needed. Several studies have raised the possibility that hearing loss is influenced by osteoporosis (6,25); however, this relationship remains controversial.
The main limitation of this study is its retrospective nature. As part of the analysis, the medical records were reviewed carefully and patients with features that could affect the hearing level were excluded. Patient age and sex were adjusted to compensate for the retrospective nature of the study, but not all patient factors could be controlled for in the analysis. Another limitation is that the sample size in this study was relatively small. Further studies are needed in a larger group of patients.
In the present study, we assessed bone quality in patients using both traditional DXA and a ROI on the skull and found that bone quality in temporal bone on CT did not correlate with traditional DXA measurements in the central skeleton. There was no relationship between BMD as measured by DXA or CT Hounsfield units for the skull base and hearing loss. It may be that BMD does not accurately reflect regional bone quality. It is also possible that sensorineural hearing loss is multifactorial and involves factors other than regional bone quality in the inner ear. Further investigations of other factors that can influence hearing levels are needed.
1. Swenor BK, Ramulu PY, Willis JR, et al. The prevalence of concurrent hearing and vision impairment in the United States. JAMA Intern Med
2. Lee SY, Kwon SS, Kim TH, et al. Is central skeleton bone quality
a predictor of the severity of proximal humeral fractures? Injury
3. Dalton DS, Cruickshanks KJ, Klein BE, et al. The impact of hearing loss on quality of life in older adults. Gerontologist
4. Edmonds SW, Cram P, Lou Y, et al. Effects of a DXA result letter on satisfaction, quality of life, and osteoporosis
knowledge: a randomized controlled trial. BMC Musculoskelet Disord
5. Helzner EP, Cauley JA, Pratt SR, et al. Hearing sensitivity and bone mineral density
in older adults: the Health, Aging and Body Composition Study. Osteoporos Int
6. Upala S, Rattanawong P, Vutthikraivit W, et al. Significant association between osteoporosis
and hearing loss: a systematic review and meta-analysis. Braz J Otorhinolaryngol
7. Jung DJ, Cho HH, Lee KY. Association of bone mineral density
with hearing impairment in postmenopausal women in Korea. Clin Exp Otorhinolaryngol
8. Mendy A, Vieira ER, Albatineh AN, et al. Low bone mineral density
is associated with balance and hearing impairments. Ann Epidemiol
9. Genant HK, Engelke K, Fuerst T, et al. Noninvasive assessment of bone mineral and structure: state of the art. J Bone Miner Res
10. Lewiecki EM, Gordon CM, Baim S, et al. International Society for Clinical Densitometry 2007 adult and pediatric official positions. Bone
11. Lee SY, Kwon SS, Kim HS, et al. Reliability and validity of lower extremity computed tomography as a screening tool for osteoporosis
. Osteoporos Int
12. Pickhardt PJ, Lee LJ, del Rio AM, et al. Simultaneous screening for osteoporosis
at CT colonography: bone mineral density
assessment using MDCT attenuation techniques compared with the DXA reference standard. J Bone Miner Res
13. Romme EA, Murchison JT, Phang KF, et al. Bone attenuation on routine chest CT correlates with bone mineral density
on DXA in patients with COPD. J Bone Miner Res
14. Park MS, Kim SJ, Chung CY, et al. Statistical consideration for bilateral cases in orthopaedic research. J Bone Joint Surg Am
15. Patterson J, Rungprai C, Den Hartog T, et al. Cortical bone thickness of the distal part of the tibia predicts bone mineral density
. J Bone Joint Surg Am
16. Shrout PE, Fleiss JL. Intraclass correlations: uses in assessing rater reliability. Psychol Bull
17. Bonett DG. Sample size requirements for estimating intraclass correlations with desired precision. Stat Med
18. Guneri EA, Ada E, Ceryan K, et al. High-resolution computed tomographic evaluation of the cochlear capsule in otosclerosis: relationship between densitometry and sensorineural hearing loss. Ann Otol Rhinol Laryngol
19. Khan A, Lore JM Jr. Osteoporosis
relative to head and neck. J Med
20. Hinton PS, Nigh P, Thyfault J. Effectiveness of resistance training or jumping-exercise to increase bone mineral density
in men with low bone mass: a 12-month randomized, clinical trial. Bone
21. Robling AG, Castillo AB, Turner CH. Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng
22. Ozkiris M, Karacavus S, Kapusuz Z, et al. Does bone mineral density
have an effect on hearing loss in postmenopausal patients? Ann Otol Rhinol Laryngol
23. Monsell EM, Cody DD, Bone HG, et al. Hearing-loss in pagets-disease of bone - the relationship between pure-tone thresholds and mineral density of the cochlear capsule. Hear Res
24. Helzner EP, Cauley JA, Pratt SR, et al. Race and sex differences in age-related hearing loss: The Health, Aging and Body Composition Study. J Am Geriatr Soc
25. Kim JY, Lee SB, Lee CH, et al. Hearing loss in postmenopausal women with low bone mineral density
. Auris Nasus Larynx
Keywords:Copyright © 2018 by Otology & Neurotology, Inc. Image copyright © 2010 Wolters Kluwer Health/Anatomical Chart Company
Bone mineral density; Bone quality; Hearing level; Osteoporosis