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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 20  |  Issue : 1  |  Page : 121-126

Audiovestibular performance in patients with low bone mineral density: a case–control study


1 Department of Rheumatology, ENT, Faculty of Medicine, Al Azhar University, Assiut, Egypt
2 Department of Audiovestibular Medicine, ENT, Faculty of Medicine, Al Azhar University, Assiut, Egypt

Date of Submission04-Oct-2021
Date of Decision12-Nov-2021
Date of Acceptance25-Nov-2021
Date of Web Publication4-Mar-2022

Correspondence Address:
MD Mohamed Elwan
Department of Rheumatology Department, Al-Azhar University, Assiut, Postal Code 71524
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/azmj.azmj_119_21

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  Abstract 


Background and aim Audiovestibular dysfunctions have been previously linked to osteoporosis (OP) with controversies about the mutual relationship. In this study, we aimed to assess the audiovestibular functions in patients with OP and osteopenia and to study their association with vitamin D deficiency.
Patients and methods Of 60 patients enrolled in this study, 30 had low bone mineral density (BMD) (group I) and 30 had normal BMD (group II). After clinical examination and evaluation of serum vitamin D and calcium levels, the participants then were referred for audiovestibular assessments, which included basic audiological evaluation by pure tone audiometry and speech audiometry, tympanometry, acoustic reflex, video-nystagmoscopy tests, and vestibular-evoked myogenic potential (VEMP) to assess saccular function. Both participants and audiologist were blinded regarding the BMD results.
Results There was a significant difference between patients and controls regarding the level of calcium (P=0.002) and vitamin D (P=0.001). There was a significant difference in the normal hearing threshold between both groups (P=0.005). There was no significant difference in VEMP testing (VEMP P1; P=0.489, amplitude; P=0.898). Benign paroxysmal positional vertigo was the most common finding in group I, among the females, where they had vitamin D deficiency (16.67±4.16) and OP (mean T score=−2.73±0.06).
Conclusions Patients with low BMD showed a greater degree of audiovestibular dysfunction, which should be considered among the associating risk factors and comorbidities. Assessment of the audiovestibular functions should be recommended for patients with low BMD in the management guidelines.

Keywords: auditory, osteopenia, osteoporosis, vestibular disorder, vitamin D deficiency


How to cite this article:
Elwan M, Elmoursy MM, Ibrahim Metwaly AM, Ryan MM. Audiovestibular performance in patients with low bone mineral density: a case–control study. Al-Azhar Assiut Med J 2022;20:121-6

How to cite this URL:
Elwan M, Elmoursy MM, Ibrahim Metwaly AM, Ryan MM. Audiovestibular performance in patients with low bone mineral density: a case–control study. Al-Azhar Assiut Med J [serial online] 2022 [cited 2022 Jun 29];20:121-6. Available from: http://www.azmj.eg.net/text.asp?2022/20/1/121/339063




  Introduction Top


Bone remodeling is a physiological process in which dynamic activities of osteoblasts and osteoclasts maintain the balance between bone resorption and redeposition [1],[2]. Disturbed bone remodeling is the leading cause of low bone mineral density (BMD), which includes osteopenia and osteoporosis (OP), according to the degree of the bone density measured [3].

Both audiovestibular dysfunction and decreased BMD are considered degenerative processes that increase with aging [4],[5],[6]. These aging disorders share some common risk factors such as the decreased physical activity [7], deficiency of calcium and vitamin D [8], and smoking [6],[9]. As a sensor of gravitational force, the vestibular system has long been considered an important factor for the optimal development of bone architecture [10]. Moreover, impairment of the vestibular function has been reported to be associated with spinal malalignment [11], which is a common consequence of OP-induced vertebral fracture. A meta-analysis of five studies reported a high association between impairment of hearing and low BMD [12]. Another cohort study on a subset of the Korean population reported that OP can be considered as a direct risk factor for sudden sensorineural hearing loss (SNHL) in elderly persons [13].

Although the mechanism of the mutual relationship between low BMD and audiovestibular dysfunction is still unclear, otosclerosis, neurodegeneration, and ossicular fracture in addition to cochlear and conductive demineralization have been hypothesized to be the causes of the associating types of auditory dysfunction in patients with OP and osteopenia [14],[15],[16]. The associating hearing loss can be conductive, sensorineural, or mixed [17],[18] in addition to the occurrence of balance disorders related to the impairment of the vestibular system [19]. Furthermore, audiovestibular dysfunctions have been reported in many rheumatic autoimmune conditions that were proven to be associated with decreased BMD such as rheumatoid arthritis [20], psoriatic arthritis [21], ankylosing spondylitis [22], and systemic lupus erythematosus [23]. It has been also reported that both decreased BMD and vestibular dysfunction are risk factors for repeated falling in the elderly population, which is the leading cause of fragility fractures in osteoporotic patients [24].

Nevertheless, the screening of audiovestibular functions in patients with OP, especially those with repeated falling, has not yet been officially recommended [25], probably owing to the lack of studies highlighting this link.

In this comparative prospective analysis, we aimed to evaluate the effect of decreased BMD and low vitamin D on the audiovestibular functions.


  Patients and methods Top


This study was a prospective, case–control study during which 100 patients of those referred for measuring their BMD are reviewed and asked to participate in the current study by being subjected to audiovestibular evaluation. Of those (the 100 patients), 60 patients accepted to participate and fulfilled the inclusion criteria. They were divided into two groups: group I included 30 patients who had low BMD, where 23 (38.3%) patients had OP (T score ≤−2.5) and seven (11.7%) patients had osteopenia (T score>−2.5 but <−1).

Group II included 30 patients who had normal range of BMD and served as controls.

All of the BMD evaluations were made using the dual-energy radiograph absorptiometry lunar DPX bone densitometer model 2012 (USA) and reported according to the WHO classification [26]. All participants gave written consent after a detailed explanation of the procedures, and the study conformed with the Declaration of Helsinki for studies on human participants. The study was approved by the ethical committee of our institution (No: 003-AA02245/05/20), and all data were kept confidential.

Exclusion criteria included the presence of middle ear inflammation or current perforation of the tympanic membrane, diabetes mellitus, hypertension, severe anemia, central nervous system abnormalities, a recent history of head trauma, previous surgical intervention in the brain, or receiving ototoxic medications.

Procedures

Complete history taking, clinical examination, and evaluation of serum vitamin D and calcium were done for all participants. Values of vitamin D were interpreted as normal (30–100 ng/ml), deficiency (<20 ng/ml), and insufficiency (20–29 ng/ml) [27].

Audiovestibular assessments

Keeping the audiologist (M.M.E) and the participants intentionally blinded to the results of vitamin D and calcium levels and dual-energy radiograph absorptiometry scanning, the following measurements were done:

Acoustic immittance measurements, including tympanometry and acoustic reflex to assess the middle ear function, using Interacoustics AT 235.

Basic audiological evaluation including pure tone audiometry for air and bone thresholds, speech audiometry including speech recognition thresholds, and word discrimination scores % using a two-channel audiometer, Interacoustics AC 40, with a local manufactured double-walled sound-treated booth.

Video-nystagmoscopy (VNG) test battery including spontaneous nystagmus, gaze, post-head shaking nystagmus, ocular motility tests, Dix-Hallpike (positioning) tests, positional tests, and caloric tests using a micromedical window two-channel VNG system.

Vestibular-evoked myogenic potential (VEMP) to assess saccular function and inferior vestibular nerve. VEMP testing using the Eclipse 25 platform, Interacoustics, from Denmark. The parameter included P1 and N1 latencies and amplitudes.

Statistical analysis

The collected data were analyzed using the professional Statistical Package for Social Science (SPSS v. 19, IBM, Chicago, Illinois, USA). Data have been presented using the mean±SD and the frequency and percent for continuous and categorical variables, respectively. Student t test was used to test the differences in means of continuous variables across the two groups (patients with low BMD and control). Analysis of variance was used to relate continuous data whenever needed. Acoustic immittance measurements (tympanometry and acoustic reflex) and pure tone audiometric threshold comparisons between both groups were done using the χ2 test. Results were considered significant if the P value was less than 0.05 and considered highly significant if the P value was less than 0.01.


  Results Top


The 60 patients in the study were divided into two groups: group I included 30 patients, where 23 (76.6%) of them had OP and seven (23.3%) patients had osteopenia. There were 15 (50%) males and 15 (50%) females, with a mean±SD age of 47.6±5.5 years, ranging from 40 to 55 years.

Group II included 30 controls with normal BMD and comparable age and sex. The demographic features are summarized in [Table 1].
Table 1 Demographic data of the study and control groups

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There was a significant difference between patients and control groups regarding the level of calcium (P=0.002) and vitamin D (P=0.001). Laboratory investigations and BMD measures are summarized in [Table 2].
Table 2 Laboratory parameters and bone mineral density measures of the study and control groups

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Basic audiological evaluation (pure tone audiometry) revealed that 83.3% had normal hearing sensitivity and 16.7% had SNHL of mild and moderate degrees. Moreover, there were mild and moderate-high frequency SNHLs in 8.3%. The degree of speech discrimination matched with the degree of SNHL. There was no difference between both groups regarding the degrees of SNHL and high-frequency SNHL (P=0.510). The acoustic immittance measurements revealed no significant difference across the studied groups regarding tympanometry (P=0.490). However, there was a significant difference regarding the acoustic reflex (P=0.01). The results are summarized in [Table 3]. Of 24 patients and 26 controls with normal pure tone audiometric threshold, the average showed a statistically significant difference (P=0.005) between both groups, which is an important finding in this study (data not shown).
Table 3 Acoustic immittance measurements (tympanometry and acoustic reflex) and pure tone audiometric thresholds for the studied and control groups

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Vestibular evaluation in the form of VEMP and VNG was done for both groups. There was no significant difference between both groups in VEMP testing (VEMP P1; P=0.489, amplitude; P=0.898). Benign paroxysmal positional vertigo (BPPV) was the most common finding in the study group among the female population ([Table 4]). The BPPV female patients had vitamin D deficiency and OP (T score=−2.73±0.06) (data not shown).
Table 4 Vestibular evaluation (vestibular-evoked myogenic potential and video-nystagmoscopy) for the studied and control groups

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  Discussion Top


Adequate concentrations of intracellular calcium ions are important triggers of cell functioning, survival, and differentiation of osteoblasts and osteoclasts [1]. Meanwhile, the change of intracellular calcium is a known modulator of the diverse neural signaling pathways in the audiovestibular system [28].

Several studies have been performed to evaluate the relationship between low BMD, low vitamin D and calcium, and audiovestibular impairments [29],[30],[31],[32]. These studies emphasized the importance of considering these associated disorders as risk factors or comorbidities for OP and should be taken into account during the public awareness workups toward OP, which suffers from worldwide malawareness [33],[34].

In this comparative, cross-sectional study, we found that patients with low BMD (group I) had lower calcium and vitamin D levels than the healthy participants. Vitamin D was deficient in OP patients with BPPV (16.67±4.16). A previous study by Kahraman et al. [28] reported that decreased calcium ion and vitamin D levels are risk factors for BPPV in patients with OP. The same was reported by Jeong et al. [29] who found that deficient vitamin D can be considered as a sole risk factor for idiopathic BPPV after exclusion of other factors such as age, hypertension, diabetes, and proteinuria.

However, a study conducted by Karataş et al. [30] considered the coexistence of OP and vitamin D deficiency with BPPV as a matter of coincidence. Another Turkish study by Işık Çıkrıkçı et al. [31] reported no relationship between levels of calcium and vitamin D and the incidence or recurrence of BPPV. Both studies explained this observation by the higher prevalence of both low vitamin D levels and OP among the Turkish population [30],[31]. In the same context, Yamanaka et al. [32] reported that the incidence of OP in patients with BPPV is similar to that of the general population, but the attacks of BPPV were more frequent in patients with OP than those without.

Regarding the acoustic immittance measurements, type A was the most common, representing 93.3% in both groups, whereas type As was found in only 6.7% and the acoustic reflex was present in nearly 86% of our cases. However, there was no significant difference between the study and control groups in tympanometric values; the acoustic reflex values were significantly different.

Kung and Willcox [35] reported that the acoustic immittance measures are used to assess the neural pathway surrounding the stapedial reflex, which occurs in response to a loud sound (70–90 dB above threshold), which is not affected in patients with OP or osteopenia.

Almost all patients and control groups had type A tympanogram, with intact acoustic reflex reflecting normal middle ear pressure in both study and control groups. Similar results were mentioned in the study done by Bhavya et al. [36] reporting normal middle ear status with a type A tympanogram in almost all ears in both groups. Consistent with these results, Ozkiris et al. [37] reported that there was no significant difference between normal and osteoporotic groups in tympanometric values, reflecting normal middle ear pressure in both groups.

In the current study, basic audiological evaluation (pure tone audiometry) revealed that 83.3% had normal hearing sensitivity and 16.7% had SNHL of mild and moderate degrees. The degree of speech discrimination matched with the degree of SNHL. There was no significant difference between the normal and osteoporotic groups. These results are consistent with Gargeshwari et al. [19], who reported that there was no significant difference in any of these tests. However, El-Zarea et al. [38] reported that the incidence of hearing loss was higher in osteoporotic patients (55%) in comparison with the healthy controls. In their study, only two (10%) patients had mild SNHL.

Comparing the average normal threshold in patients with OP and osteopenia with the control group, we found a statistically significant difference, which agrees with Kahveci et al.[39] who reported that patients with OP have a significantly higher threshold than normal and osteopenic patients; thresholds were also significantly worse at high frequencies. This affection of basal region of the cochlea can cause SNHL mainly at high frequencies because the cochlea is organized tonotopically, which means that the base end of the cochlea responds to high-frequency sounds, whereas the apical aspect responds to the low-frequency sounds.VEMP results for both groups showed there was no significant difference in latencies or amplitude of cervical VEMP for both groups. Similar results were obtained by Gargeshwari et al. [19] who reported no significant differences in latencies or amplitude of cervical VEMP among the groups.

The test results showed that the BPPV was the most common vestibular pathology occurring in the study group (16.7%) followed by the uncompensated peripheral vestibular disease (11.1%); both occurred in females. There was no significant difference between both groups.

Females were more prone to BPPV than males. Brandt et al. [40] reported that BPPV recurs more frequently in women (58 vs. 39%). They also reported that adult females seem to be more prone to the occurrence of BPPV, as the BPPV prevalence in females could be linked to hormonal variations and the associated demineralization and metabolic changes [40]. Although this study has been limited by the small sample size, it tried to add an evidence-based concept about the relationship between decreased BMD and audiovestibular functions.


  Recommendations and conclusions Top


The audiological and vestibular probing of patients with osteopenia and OP showed a great degree of dysfunction which should be considered as associating risk factor in those patients. Moreover, the assessment of audiovestibular functions should be recommended as a routine examination in patients with low BMD in the management guidelines.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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  [Table 1], [Table 2], [Table 3], [Table 4]



 

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