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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 38  |  Issue : 2  |  Page : 97-104

Evaluation of the ascending utricular and descending saccule pathway using cervical vestibular evoked myogenic potential and ocular vestibular evoked myogenic potential in diabetic polyneuropathy


1 Department of Neurology, University of Health Sciences, Prof. Dr. Cemil Taşçıoğlu City Hospital, Istanbul, Turkey
2 Department of Otorhinolaryngology-Head and Neck Surgery, University of Health Sciences, Prof. Dr. Cemil Taşçıoğlu City Hospital, Istanbul, Turkey
3 Department of Otorhinolaryngology-Head and Neck Surgery, Bulanık State Hospital, Muş, Turkey

Date of Submission30-Aug-2020
Date of Decision16-Nov-2020
Date of Acceptance20-Nov-2020
Date of Web Publication08-Apr-2021

Correspondence Address:
Onur Akan
Department of Neurology, University of Health Sciences, Prof. Dr. Cemil Taşçıoğlu City Hospital, Darulaceze Cad. No: 25 Okmeydani – Sisli, Istanbul
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/nsn.nsn_155_20

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  Abstract 


Background: Chronic hyperglycemia can affect the vestibular system by causing injury in cells and neural structures. In addition to alterations in the microvasculature and connective tissues, changes in inner ear fluid metabolism can also contribute to otolithic damage in patients with diabetes. We aimed to evaluate the effects of neurovascular degeneration occurring in diabetic polyneuropathy (DPN) on the vestibular system. Methods: Thirty-five patients with DPN (n = 70 ears) and 34 (n = 68 ears) healthy controls were enrolled. Patients were classified into two subgroups as sensorial axonal PNP and sensory-motor axonal PNP. To assess vestibular functions, cervical vestibular evoked myogenic potential (cVEMP) and ocular vestibular evoked myogenic potential (oVEMP) testing were bilaterally performed. Results: Bilateral cVEMP and oVEMP P1 latency and N1 latency were significantly prolonged, whereas amplitude values were significantly decreased in patients with DPN compared with the controls (P = 0.001). The cVEMP amplitude asymmetry ratio (AAR) was statistically higher in the DPN group than in controls (P = 0.001); oVEMP AAR was not significant between the patient and control groups (P = 0.095). The cVEMP AAR values were found to be increased in both patient subgroups, and oVEMP AAR was elevated in the sensorineural PNP subgroup. In the DPN group, the nonresponse rate was 48.6% (n = 17) in cVEMP and 51.4% (n = 18) in oVEMP, significantly higher compared with the controls (P < 0.05). In cVEMP, nonresponse rates were found to be lower in both DPN subgroups. In oVEMP, the nonresponse rate was found to be higher in the sensory-motor PNP subgroup when compared with the sensorial PNP subgroup (P = 0.008 and P = 0.003, respectively). Conclusion: In diabetes mellitus with multisystemic effects, particularly in patients with polyneuropathy, vestibular testing before the onset of vestibular symptoms may be an early and beneficial diagnostic method for detecting the presence or degree of neurovascular degeneration.

Keywords: Cervical vestibular evoked myogenic potential, diabetes mellitus, neuropathy, ocular vestibular evoked myogenic potential


How to cite this article:
Akan O, Berkiten G, Tutar B, Karaketir S, Tuna &B, Karaketir S, Tuna &B. Evaluation of the ascending utricular and descending saccule pathway using cervical vestibular evoked myogenic potential and ocular vestibular evoked myogenic potential in diabetic polyneuropathy. Neurol Sci Neurophysiol 2021;38:97-104

How to cite this URL:
Akan O, Berkiten G, Tutar B, Karaketir S, Tuna &B, Karaketir S, Tuna &B. Evaluation of the ascending utricular and descending saccule pathway using cervical vestibular evoked myogenic potential and ocular vestibular evoked myogenic potential in diabetic polyneuropathy. Neurol Sci Neurophysiol [serial online] 2021 [cited 2021 Sep 18];38:97-104. Available from: http://www.nsnjournal.org/text.asp?2021/38/2/97/313368




  Introduction Top


Diabetes mellitus (DM) is a group of metabolic diseases characterized by hyperglycemia resulting from a disorder of insulin release and/or insulin effect. Chronic hyperglycemia can affect the vestibular system by causing injury in cells and neural structures.[1],[2],[3] In patients with diabetes, peripheral neuropathy and retinopathy are well-known pathologic entities that induce balance disorders and falls.[3] In addition, it is known that DM increases the risk of vestibular dysfunction, regardless of the presence of peripheral neuropathy and retinopathy.[4] Diabetic polyneuropathy (DPN) is a neurodegenerative disorder that involves sensorial axons, autonomic axons, and to a lesser extent, motor axons of the peripheral nervous system.[5] Furthermore, several authors have proposed that microangiopathy could account for DM-related inner ear disorders.[6],[7] Together with the vascular hypothesis, some arguments harmonize metabolic views and diffuse polyneuropathy (PN) development mechanisms. Morphologic studies have proposed that, in addition to alteration in the microvasculature and connective tissues, changes in inner ear fluid metabolism could also contribute to otolithic damage in patients with diabetes.[8],[9]

Vestibular evoked myogenic potentials (VEMPs) are vestibular-dependent reflexes recorded at the sternocleidomastoid (SCM) (cervical vestibular evoked myogenic potential [cVEMP]) and inferior oblique muscles (ocular vestibular evoked myogenic potential [oVEMP]). In the prior two decades, VEMP testing, which allows rapid assessment of vestibular functions, has become a standard component of the neuro-otology test battery. cVEMP and oVEMP reflect the function of the vestibulo-ocular reflex and vestibulocollic reflex arcs, which are the two major neural pathways of the vestibular system. Although the mechanism underlying vestibular involvement and which part is involved in DM have not been fully elucidated, vestibular dysfunction has been shown in patients with diabetes. In the literature, there is a limited number of studies on DPN with inconsistent results.[10],[11],[12],[13] In this study, it was aimed to assess the effects of neurovascular degeneration developing in patients with DPN on the vestibular system using electrophysiologic tests.


  Materials and Methods Top


The study included patients with type 2 diabetes mellitus (T2DM) who had been followed with a diagnosis of DPN in our clinic between May 2018 and January 2010. In all participants, otoscopic examinations and audiometric tests were performed at baseline, and patients with normal auditory functions were included. Patients with chronic disorders, comorbid conditions such as migraine, systemic diseases, and auditory or neurologic problems that might affect the test results were excluded. Healthy individuals in a similar age group who had no systemic disease or neurologic disorders or a history of balance disorder or vertigo were enrolled as controls.

The PNP diagnosis was made based on the presence of nerve conduction abnormality in at least two nerves in nerve conduction studies. If there was sensorial conduction abnormality alone, it was considered as sensorial axonal PNP, whereas if there was a sensorial and motor conduction abnormality, it was considered as sensory-motor axonal PNP. The patients with PNP were classified into two groups as sensorial axonal PNP and sensory-motor axonal PNP according to electromyography (EMG) findings.

Ocular vestibular evoked myogenic potential and cervical vestibular evoked myogenic potentials recording technique

In all participants, VEMP testing was performed from SCM (cVEMP) and inferior oblique muscles (oVEMP) using ICS-CHARTER EP 200 device (GN Otometrics North America, Schaumburg, IL, USA) to assess vestibular lesions. An ICS Medical insert earphone (ER 3A/5A Insert Earphone 300 ohms) was used for acoustic stimulation. The stimulus used was a 500-Hz tone-burst stimulus at rarefaction polarity loudness of 97 dB through airway conduction. The VEMP waveforms were recorded using the following settings: filter setting, 2–500 Hz; repetition, 5/s; and loudness, 97 dB. Both cVEMP and oVEMP were recorded with the patient in the sitting position. For cVEMP, the active electrode was placed in the middle one-third segment of the SCM and the reference electrode was placed over the sternum. The ground electrode was placed at the midline on the forehead. The peak points of the first waveform following the stimulus were defined as P1 (positive) and N1 (negative). The oVEMP was recorded during the upwards gaze via surface electrodes placed on the cheek on the contralateral side. The active electrodes were placed on the eyelids 1 cm below the orbit and the reference electrodes were placed 3 cm below the orbit. The ground electrode was placed on the forehead. The peak points of the first waveform following the stimulus were defined as P1 (positive) and N1 (negative). The absolute amplitude value was the voltage difference between the positive and negative peaks (P1-N1). VEMP testing was assessed using P1 and N1 latency, amplitude values, and amplitude asymmetry ratio (AAR). ARR was calculated using the following formula:

AAR = 100 (ALeft − ARight)/(ALeft + ARight)

Abnormal AAR was defined as >34.4% for cVEMP and >35% for oVEMP.[14] Abnormal VEMP parameters or AAR values or nonresponse were considered as abnormal VEMP responses. VEMP testing was repeated in nonresponders and those with an inconsiderable response. Rectified values were used because the oVEMP and cVEMP response amplitudes were significantly affected by the force of muscular contraction or stimulus sensitivity.

The study was approved by the local ethics committee and conducted according to the Helsinki Declaration.

Statistical analysis

Statistical analyses were performed using the IBM SPSS Statistics version 22.0 (IBM, SPSS, Turkey). Normal distribution was assessed using the Shapiro–Wilk test. The Student's t-test was used to compare parameters with the normal distribution. The paired-samples t-test was used for intragroup comparisons between the right and left ear. Fisher's exact test, Continuity (Yates's) correction, and McNemar tests were used to compare quantitative variables. P < 0.05 was considered as statistically significant.


  Results Top


The study was conducted on 35 patients with DPN and 34 healthy individuals as controls. The mean age was 53 ± 18.3 years in the DPN group and 51 ± 11.1 years in the controls, indicating no significant difference (P = 0.254). The male–female ratio was 0.59 in the DPN group and 0.61 in the controls with no significant difference between the groups (P = 0.925).[6],[7]

Cervical vestibular evoked myogenic potential results

When compared with the control group, it was found that cVEMP P1 and N1 latencies were significantly prolonged, whereas amplitude values were significantly lower in both the right and left ears in the DPN group (P = 0.001). Furthermore, it was found that cVEMP AAR was significantly higher in the DPN group (52.91%) when compared with the controls [P = 0.001; [Table 1]. In the DPN group, the nonresponse rate was 48.6% (n = 17) in cVEMP and 51.4% (n = 18) in oVEMP. The nonresponse rate in bilateral cVEMP and oVEMP testing was found to be significantly higher in the DPN group when compared with the controls [P < 0.05, [Table 2].
Table 1: Cervical vestibular evoked myogenic potential and ocular vestibular evoked myogenic potential parameters in the diabetic polyneuropathy and control groups

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Table 2: Bilateral cervical vestibular evoked myogenic potential and ocular vestibular evoked myogenic potential results in the diabetic polyneuropathy and control groups

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The sensorial axonal PNP and sensory-motor axonal PNP cVEMP P1 latency, N1 latency, and amplitude measurements were found to be comparable among DPN subgroups [P > 0.05, [Table 3]. The cVEMP AAR value was found to be higher than 34.4% in both sensorial and sensory-motor PNPs, but no significant difference was detected between the subgroups (61.99 ± 31.04 vs. 43.29 ± 29.37.42). In cVEMP, the total nonresponse rate (right plus left ears) was found as 33.3% (n = 6) in sensorial PNP and 64.7% (n = 11) in sensory-motor PNP, indicating no significant difference [P = 0.471 and P = 0.228, respectively, [Table 4].
Table 3: Cervical vestibular evoked myogenic potential and ocular vestibular evoked myogenic potential parameters in the diabetic polyneuropathy subgroups

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Table 4: Bilateral cervical vestibular evoked myogenic potential and ocular vestibular evoked myogenic potential results in the diabetic polyneuropathy subgroups

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Ocular vestibular evoked myogenic potential results

When compared with the control group, it was found that cVEMP P1 and N1 latencies were significantly prolonged and amplitude values were lower in the DPN group (P = 0.001). In the DPN group, the oVEMP AAR value was measured as 37.88 ± 35.12 (above 35%), comparable with the controls [Table 1].

In oVEMP, the nonresponse rate was 17.1% (n = 6) for right and 34.3% (n = 12) for left ears in the DPN group; nonresponse rates were significantly higher in the DPN group compared with the controls [P > 0.05; [Table 2].

The oVEMP P1 latency, N1 latency, and amplitude measurements were found to be comparable among the DPN subgroups (P > 0.05; [Table 3]. The oVEMP AAR value was found to be higher than 35% (39.94 ± 30.94) in both sensorial and sensory-motor PNPs. In the sensory-motor PNP subgroup, the oVEMP nonresponse rate was found to be significantly higher when compared with the sensorial PNP subgroup [P = 0.008 and P = 0.003, respectively, [Table 4].

cVEMP and oVEMP responses of patients with DPN are shown in [Figure 1], [Figure 2], [Figure 3], [Figure 4].
Figure 1: Decreased cervical vestibular evoked myogenic potential amplitude is decreased on the right ear of patients with diabetic polyneuropathy

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Figure 2: Ocular vestibular evoked myogenic potential response is absent on the left ear of patients with diabetic polyneuropathy

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Figure 3: Cervical vestibular evoked myogenic potential response is absent on right ear of patients with diabetic polyneuropathy

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Figure 4: Ocular vestibular evoked myogenic potential amplitude is decreased on the right ear of patients with diabetic polyneuropathy

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  Discussion Top


DM is a chronic metabolic disorder characterized by insulin deficiency that affects almost all organs in the body and causes chronic degenerative complications. Despite well-known associations between DM and microvascular complications, there are limited data regarding the pathogenesis of vestibular nerve involvement in patients with DPN. The vestibular dysfunction incidence was higher by 70% in patients with diabetes than in healthy individuals.[15] In this study, we evaluated the effects of neurovascular degeneration on peripheral vestibular systems using electrophysiologic tests including cVEMP and oVEMP in DPN in light of the literature.

Evoked potentials play an important role in identifying pathologic processes underlying neuropathy in addition to indicating involvement neural segments. In recent studies, otocranial organ disorder was shown through cervical and ocular pathways in clinical tests.[10],[12],[16] Demyelinating neuropathies can cause delayed latency, and an absent or decreased VEMP response is possible in axonal degeneration.[17]

In our study, a delay in cVEMP and oVEMP P1 and N1 latency was found in both ears in the DPN group. This was thought to reflect utricular and saccular dysfunction in patients with DPN. In the literature, many studies have shown delayed latency in the VEMP response in support of our findings. In the study by Konukseven et al., it was found that P1 and N1 latencies were significantly longer in patients with T2DM when compared with controls.[6] The authors suggested that prolonged latency could be present due to degeneration related to sensorial or motor PNPs, which are common complications in T2DM. Similarly, in a study on 14 patients with type 1 diabetes mellitus (T1DM) with PN, 10 patients with T1DM without PN, and 24 healthy volunteers, Kamali et al. found prolonged P13 and N23 latency in the patient groups.[18] In a study by Bektas et al., P1 and N1 latencies were assessed in patients with diabetes with or without PNP using cVEMP and no delayed latency was detected in either group.[19] Delayed VEMP (prolonged latency) can emerge due to central pathologies or demyelinating lesions of retrolabyrinthine;[18] however, musculoskeletal degeneration (DM can lead to altered glucose metabolism in peripheral tissues such as muscle and adipose tissue) in addition to degeneration in neural pathways in oVEMP and cVEMP may also affect test results. In a study, Murofushi et al. reported prolonged VEMP P13 latency in patients with giant acoustic neuroma and patients with multiple sclerosis.[20] Taylor et al. detected minimally prolonged latency in patients with Meniere's disease or vestibular neuritis.[17] It was thought that peripheral pathologies, as well as impaired brainstem pathways and central conduction abnormalities, could contribute to prolonged VEMP latency.

For peripheral neuropathy, one of the long-term neurovascular complications of DM, the commonly proposed mechanism is the toxic effect of prolonged hyperglycemia causing vascular injury.[16] Persistently elevated glucose concentrations lead to the accumulation of some substances in the basal membrane, which thickens the luminal walls of the capillaries and small arterioles and alters vascular permeability in many organ systems. Retinopathy, nephropathy, or peripheral neuropathy may develop as a result of hyperglycemia-related microvascular pathology, known as diabetic microangiopathy. It is also known that DM leads to inner ear pathology and dysfunction. Some authors have proposed that microangiopathy could be involved in DM-related alterations of the inner ear function.[6],[7] In DM, there is a DPN spectrum varying according to neural fiber type involved (myelinated, nonmyelinated, autonomic, somatic), neural distribution, and neuropathy mechanisms.[21] The PNP prevalence is about 8% in newly diagnosed DM, whereas it exceeds 50% in prolonged DM.[22] There is more severe involvement in sensory-motor PNP compared with sensorial PNP.[16] Agrawal et al. reported that patients with diabetes with DPN had vestibular disorder more commonly than those without DPN (76% vs. 49%).[14] Thus, we sought findings for differing involvement among subgroups stratified according to the degree of PNP involvement in patients with DM; however, no difference was detected in cVEMP parameters between patients with sensorial or sensory-motor PNP.

Although the nonresponse rate in cVEMP was higher in both subgroups, it was found to be higher in the sensory-motor PNP subgroup. The nonresponse rate in oVEMP was found to be significantly higher in the sensory-motor PNP subgroup. It was seen that both cVEMP and oVEMP results were impaired by the increasing severity of PN, successfully reflecting disease severity.

It has been established that VEMP AAR values are less helpful because neural involvement is generally bilateral in PNPs.[14],[23] Konukseven et al. reported that no lateralization was observed in VEMP AAR values. However, asymmetrical neuropathy can cause increased AAR. Presumably, asymmetrical neuropathies result from a combination of micro-vascular and immune-mediated mechanisms. DPN likely has a multifactorial pathogenesis. Hyperglycemia leads to oxidative stress, decreased nitric oxide levels, elevated prostaglandin and endothelin, and impaired blood flow at the microvascular level. Furthermore, it may directly influence neural fibers.[24] In our study, in both VEMPs, AAR was found to be markedly higher in the DPN group than in controls, indicating unilateral neural dysfunction. In the DPN subgroups, cVEMP and oVEMP AARs were found to be higher in both subgroups.

Our results seem to support the definition of subclinical vestibular neuropathy made by Konukseven et al.[6] It should be kept in mind that vestibular tests can be an early, valuable diagnostic tool to show the presence and degree of neurovascular degeneration in patients with DPN before the onset of vestibular symptoms.

There are a limited number of studies using objective vestibular testing tools to assess vestibular end-organ abnormalities in patients with DM. In the literature, VEMP findings in DM are somewhat contradictory due to several factors. Our study has some limitations, including the lack of a patient group that had DM but not PNP in EMG and a smaller number of patients. Further studies with a larger sample size will be helpful to investigate VEMP responses in patients with DM with or without PNP. Sensorineural PNP was found to be high in oVEMP AAR.

In our study, when compared with healthy individuals, cVEMP and oVEMP amplitudes were found to be lower in both ears in the PNP group. In a study by Tavakoli et al., the low amplitude was shown in patients with DM and it was suggested that abnormal VEMP responses might be due to involvement of vestibular end-organ and related central pathways; however, PNP could not be demonstrated in the study population.[25]


  Conclusions Top


DM affects many organs including the central and peripheral vestibular system. It should be kept in mind that vestibular tests can be an early, valuable diagnostic tool to show the presence and degree of neurovascular degeneration in patients with DPN before the onset of vestibular symptoms.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, et al. Diabetic neuropathies: Update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care 2010;33:2285-93.  Back to cited text no. 1
    
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Kocdor P, Kaya S, Erdil M, Cureoglu S, Paparella MM, Adams ME. Vascular and neuroepithelial histopathology of the saccule in humans with diabetes mellitus. Otol Neurotol 2016;37:553-7.  Back to cited text no. 4
    
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Konukseven O, Polat SB, Karahan S, Konukseven E, Ersoy R, Cakir B, et al. Electrophysiologic vestibular evaluation in type 2 diabetic and prediabetic patients: Air conduction ocular and cervical vestibular evoked myogenic potentials. Int J Audiol 2015;54:536-43.  Back to cited text no. 6
    
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Pierson CR. Metabolic alterations in experimental models. In: Gries FA, Cameron NE, Low PA, Ziegler D, editors. Textbook of Diabetic Neuropathy, New York: Thieme; 2002. p. 96-105.  Back to cited text no. 7
    
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Myers SF, Ross MD, Jokelainen P, Graham MD, McClatchey KD. Morphological evidence of vestibular pathology in long-term experimental diabetes mellitus. I. Microvascular changes. Acta Otolaryngol 1985;100:351-64.  Back to cited text no. 8
    
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Chihara Y, Iwasaki S, Ushio M, Murofushi T. Vestibular-evoked extraocular potentials by air-conducted sound: Another clinical test for vestibular function. Clin Neurophysiol 2007;118:2745-51.  Back to cited text no. 14
    
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Agrawal Y, Carey JP, Della Santina CC, Schubert MC, Minor LB. Disorders of balance and vestibular function in US adults: Data from the National Health and Nutrition Examination Survey, 2001-2004. Arch Intern Med 2009;169:938-44.  Back to cited text no. 15
    
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Taylor RL, Welgampola MS, Nham B, Rosengren SM. Vestibular-evoked myogenic potential testing in vestibular localization and diagnosis. Semin Neurol 2020;40:18-32.  Back to cited text no. 17
    
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Kamali B, Hajiabolhassan F, Fatahi J, Nasli Esfahani E, Sarrafzadeh J, Faghihzadeh S. Effects of diabetes mellitus type I with or without neuropathy on vestibular evoked myogenic potentials. Acta Med Iran 2013;16:107-12.  Back to cited text no. 18
    
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Bektas D, Gazioglu S, Arslan S, Cobanoglu B, Boz C, Caylan R. VEMP responses are not affected in non-insulin-dependent diabetes mellitus patients with or without polyneuropathy. Acta Otolaryngol 2008;128:768-71.  Back to cited text no. 19
    
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Murofushi T, Shimizu K, Takegoshi H, Cheng PW. Diagnostic value of prolonged latencies in the vestibular evoked myogenic potential. Arch Otolaryngol Head Neck Surg 2001;127:1069-72.  Back to cited text no. 20
    
21.
Sasaki H, Kawamura N, Dyck PJ, Dyck PJ, Kihara M, Low PA. Spectrum of diabetic neuropathies. Diabetol Int 2020;11:87-96.  Back to cited text no. 21
    
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Iwasaki S, Smulders YE, Burgess AM, McGarvie LA, Macdougall HG, Halmagyi GM, et al. Ocular vestibular evoked myogenic potentials in response to bone-conducted vibration of the midline forehead at Fz. A new indicator of unilateral otolithic loss. Audiol Neurootol 2008;13:396-404.  Back to cited text no. 23
    
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Low PA, Suarez GA. Diabetic neuropathies. Baillieres Clin Neurol 1995;4:401-25.  Back to cited text no. 24
    
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Tavakoli M, Talebi H, Shushtari SS. Audiometric results and cervical vestibular evoked myogenic potentials in patients with type I and II diabetes mellitus. Audiology 2014;23:40-8.  Back to cited text no. 25
    


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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
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