Subscribe to RSS
![](/products/assets/desktop/img/oa-logo.png)
DOI: 10.1055/s-0041-1726041
Auditory and Vestibular Functioning in Individuals with Type-2 Diabetes Mellitus: A Systematic Review
Abstract
Introduction Diabetes mellitus is a metabolic disease associated with a rise in the level of blood glucose. Individuals with diabetes mellitus are more likely to develop hearing loss, tinnitus, and dizziness due to macro- and microvascular complications. The extent to which auditory and vestibular functions are impaired in individuals with type-2 diabetes mellitus is still under debate.
Objective To systematically review studies focusing on auditory and vestibular functions in individuals with type-2 diabetes mellitus.
Data Synthesis A search was conducted in the PubMed, MedlinePlus, Ingenta Connect and Google Scholar databases for articles published until June 2019. A total of 15,980 articles were primarily retrieved, 33 of which were shortlisted based on the inclusion criteria set by the investigators for the systematic review. Out of 33 full-length articles, 26 evaluated the functioning of the auditory system, while 7 evaluated the functioning of the vestibular system. Most studies related to auditory functioning reported a significant effect of type-2 diabetes mellitus on the peripheral auditory system, whereas studies on vestibular functioning reported no significant effect of diabetes mellitus on the functioning of the peripheral vestibular end-organ.
Conclusion Overall, the results of various audiological and peripheral vestibular tests reveal distinctive peripheral and/or central auditory and vestibular end-organ impairments in individuals with type-2 diabetes mellitus.
#
Introduction
Diabetes is a complex systemic disorder usually characterized by chronic hyperglycemia, with disturbances in the protein, carbohydrate, and fat metabolism that result from irregularities with the insulin hormone, which maintains the regulation of blood glucose within the body.[1] According to the 8th edition of the International Diabetes Federation's (IDF), Diabetes Atlas,[1] in 2017, 425 million people worldwide had diabetes mellitus (DM), and 352 million people were at risk of developing type-2 DM (DM2). It is predicted that diabetes may affect 72.9 million individuals in India by 2045.[1] Diabetes mellitus is usually diagnosed based on the results of tests such as the fasting plasma glucose (FPG) test, the 2-hour postprandial glucose (2-hour PG) test, the oral glucose tolerance test (OGTT), the glycated hemoglobin (HbA1c) test, or a random plasma glucose test.[2] Overall, these tests are equally appropriate for diagnostic purposes; hence, they can be repeated for both screening and diagnosis of individuals. Based on the etiological factors, individuals with DM are classified as having type-1 DM (DM1), also called insulin-dependent DM (IDDM), or DM2, also called non-insulin-dependent DM (NIDDM). Type-1 DM is characterized by β-cell destruction due to autoimmune processes resulting in insulin deficiency,[3] and DM2, the most common form of DM, is characterized by factors that include hyperglycemic crisis, insulin resistance, and relative insulin deficiency.[4] Diabetes has many potential subclinical complications, such as retinopathy, nephropathy, and peripheral neuropathy, which diminish the health-related quality of life of the individuals affected. Disease-specific medical factors, such as the type, the duration, the treatment program, the level of glycemic control, and the presence of additional vascular complications have an effect on the complications that arise as a result of DM.[5]
Type2 Diabetes Mellitus
Approximately 90% of all individuals with DM have DM2, which makes it a major public health issue.[1] Type-2 DM can be attributed to intra-abdominal obesity and sedentary lifestyle interrelated with insulin resistance. In addition, conditions such as hypertension and dyslipidemia are often present in individuals with DM2. The American Diabetes Association (ADA) recommends the use of validated tools to screen asymptomatic adults or a simple informal assessment regarding the risk factors that cause DM in an individual. Tests such as the FPG, 2-hour PG, and HbA1c are also appropriate for the diagnosis of DM2.
The two main pathological defects in DM2 are impaired insulin secretion by means of dysfunction in the pancreatic β cells, and reduced action over the insulin resistance,[4] which affects the insulin-mediated glucose uptake by the periphery substance, the triglyceride uptake by fat, and causes the suppression of hepatic glucose output. As a result of these changes, insulin secretion is increased by the islet cell, which, in turn, increases the production of endogenous glucose in DM2.[6]
#
Diabetes Mellitus and the Auditory System
Diabetes mellitus is a systemic disease; as such, it affects multiple organ systems, including the auditory system. Individuals with diabetes are more likely to develop hearing loss, tinnitus, and dizziness due to macro- and microvascular complications in the inner ear caused by glucose metabolism.[7] The main etiological factors that result in hearing loss and dizziness are those conditions that affect glycosides and lipids.[8] The capillary lumen changes as a result of the thickening of the basilar membrane and atrophy of the stria vascularis, which are some of the other important contributors for the hearing loss in individuals with DM.[9]
The physiology of the cochlea, which is dependent on cochelar microciurculation, is indirectly affected in DM2, since the disease affects the microcirculation.[10] Wang et al.[11] reported a change in the ultrastructure of inner ear capillaries along with the thickening of the basement membrane. Thickening of capillaries in the basal region of the stria vascularis, along the lateral wall of the cochlea, and a decrease in the amount of hair cells present within cochlea are observed in cases of DM.[12]
Moreover, histopathological evidence also suggests that factors such as neuropathy of the VIIIth nerve, microangiopathy of the inner ear, and inflammation and glycemia can result in diabetes-related hearing impairment. For years, many clinical researchers investigated the effect of DM on hearing function, and they found a significant association between diabetes and hearing loss;[13] [14] [15] only a small number of studies found no association between diabetes and hearing loss.[16]
#
Diabetes Mellitus and Vestibular Dysfunction
The inner ear consists of both hearing and vestibular organs. Hence, DM might also have an effect on vestibular function. Vestibular dysfunction in individuals with DM is found to be the result of compromised inner-ear functioning.[17] The progression of the disease may lead to comorbidity of vestibular symptoms, at least in a few individuals.[18] The prevalence of balance disorder in individuals with diabetes mellitus is reported to be between 60% and 75%.[19] The pathophysiological mechanism by which diabetes affects vestibular function involves parts or all of the vestibular structures, and is not completely understood by the researchers.[20] Animal studies[21] [22] on rats with induced diabetes revealed evidences of atrophy of type-I vestibular hair cells and thinning of the myelin sheath present on the vestibular nerves. Thus, it is important to investigate the effects DM2 on vestibular damage beyond the micro- and macrovascular complications.
Since the inner ear consists of the hearing and vestibular systems, the extent to which auditory and vestibular functions are impaired in cases of DM2 remains under debate. So, the main focus of the present systematic review is to perform a quantitative analysis to explore the auditory and vestibular findings in cases of DM2 reported in the literature. The present review exclusively focused on DM2, as it constitutes 90% of all cases of DM, and is a major public health issue.[1] The results of the present systematic review will enhance the understanding of the association with and alterations caused by DM2 regarding auditory and vestibular functions.
#
#
Research Design and Methods
Study Design
We performed a systematic review of published studies that evaluated auditory and vestibular functioning in DM2. A written study protocol was prepared in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement.[23]
#
Search Strategy
We systematically searched the Google Scholar, PubMed, MedlinePlus, and Ingenta Connect databases for experimental studies published until June 2019 evaluating DM2 and the functioning of the audio-vestibular system. The search terms used were as follows: non-insulin dependent diabetes mellitus OR type-2 diabetes mellitus OR adult onset diabetes mellitus, hearing, auditory brainstem response OR brainstem-evoked response audiometry, cochlear function, otoacoustic emission, cortical potentials, balance, vestibular, otolith, vestibular-evoked myogenic potential, video head impulse, and semicircular canals. Details on the number of articles obtained using the aforementioned terms is reported in [Table 1].
The search was limited to articles published in English. In addition, articles with systematic reviews and meta-analyses related to this particular topic helped us identify additional articles that were missing in our database search.
#
Inclusion and Exclusion Criteria
Experimental studies evaluating the effect of DM2 on auditory and vestibular functioning were eligible for inclusion. Inclusion was restricted to controlled trials reporting the measurements that confirm the presence of DM2, such as HbA1c, the fasting blood sugar test (FBS), and the postprandial glucose test (PPBS). Articles that incorporated tests of particular interest mentioned in the present review were included. Studies that addressed only DM1 or without a subgroup analysis matching the required group, presence of other comorbid conditions of diabetes, and review articles not relevant to this particular topic were excluded from the review process.
#
Data Extraction and Quality Assessment
For each article that met our inclusion criteria, reviewers extracted information such as study design, sample size, participant characteristics, tests incorporated and results. The literature search was independently conducted by two reviewers. Disagreements about inclusion or exclusion based on the review of titles and abstracts review were resolved by a third reviewer. The general quality of the studies was evaluated based on the external and internal validity, randomized or non-randomized trials, and use of appropriate analytical techniques.
#
Data Synthesis and Analysis
The studies were methodologically and clinically diverse. Therefore, qualitative analyses were performed for the individual studies that addressed similar research questions with different measurements regarding DM2. Based on the methodological focus of this particular review article, a systematic review without a meta-analysis was conducted.
#
#
Results
Search Results
The databse search yielded 15,980-potentially relevant articles, 197 of which had the full text available for review. Following our inclusion criteria, 26 articles on the auditory system and 6 on the vestibular system were included in the final systematic review ([Fig. 1]).
![](https://www.thieme-connect.de/media/10.1055-s-00025477/202202/thumbnails/10-1055-s-0041-1726041-i200094-1.jpg)
![Zoom Image](/products/assets/desktop/css/img/icon-figure-zoom.png)
#
Audiological Evaluation in Type-2 Diabetes Mellitus
Numerous researches have evaluated the peripheral auditory and central auditory systems in individuals with DM2. [Table 2] shows a summary of the studies that dealt particularly with auditory evaluations.
Serial Number (Sl. No.) |
Author |
Year |
Tests administered |
Number of participants EG/CG |
Significance |
---|---|---|---|---|---|
1. 1 |
Díaz de León-Morales et al.[13] |
2005 |
PTA/Speech audiometry/ABR |
94/94 |
(++) |
2. 2 |
Manjarrez et a.l[45] |
2007 |
ALLR |
20/20 |
(++) |
3. |
Panchu[56] |
2008 |
PTA |
41/41 |
(++) |
4. |
Ren et al.[14] |
2009 |
PTA/OAE/ABR |
50/50 |
(++) |
5. D |
Durmus et al.[57] |
2004 |
ABR |
26/20 |
(++) |
6. |
Gupta et al.[41] |
2010 |
ABR |
25/25 |
(++) |
7. |
Vesperini et al.[15] |
2011 |
PTA/OAE/ABR |
40/20 |
(++) |
8. |
Jabbari Moghaddam[16] |
2011 |
ABR/OAE |
50/50 |
(−) |
9. |
Özel et al.[25] |
2014 |
PTA/SRS |
104/104 |
(++) |
10. |
Gupta et al.[35] |
2013 |
ABR |
126/106 |
(++) |
11. |
Karabulut et al.[32] |
2014 |
PTA/SDS/TEOAE/DPOAE/CLS-TEOAE |
50/51 |
(++) CLS-TEOAE (−) |
12. |
Mahallik et al.[58] |
2014 |
ABR |
25/25 |
(++) |
13. |
Gupta et al.[43] |
2015 |
Speech ABR /da/ |
25/25 |
(++) |
14. |
Hemashree and Preetha[26] |
2016 |
PTA |
20/20 |
(++) |
15. |
Meena et al.[27] |
2016 |
PTA/TEOAE/ABR |
50/50 |
(++) |
16. |
Paluru et al.[31] |
2016 |
DPOAE |
50/50 |
(++) |
17. |
Murugesan et al.[38] |
2016 |
ABR |
50/50 |
(++) |
18. |
Yikawe et al.[59] |
2017 |
PTA |
170/170 |
(++) |
19. |
Gulati et al.[60] |
2017 |
PTA |
50/50 |
(++) |
20. |
Kannan[40] |
2017 |
ABR |
40/40 |
(++) |
21. |
Sanju et al.[44] |
2017 |
Speech ABR /da/ |
11/11 |
(++) |
22. |
Li et al.[33] |
2018 |
PTA/DPOAE |
51/43 |
(++) |
23. |
Suresh et al.[42] |
2018 |
ABR |
15/15 |
(++) |
24. |
Victor et al.[39] |
2018 |
ABR |
30/30 |
(++) |
25. |
Kumar et al.[46] |
2018 |
ALLR /da/ |
25/25 |
(++) |
26. |
Goyal et al.[37] |
2019 |
ABR |
50/50 |
(++) |
Abbreviations: ABR, auditory brainstem response; ALLR, auditory late-latency response; CLS, contralateral suppression; CG, control group; DPOAE, distortion-product otoacoustic emission; EG, experimental group; OAE, otoacoustic emission; PTA, pure-tone audiometry; SDS, speech discrimination score; SRS, speech recognition score; TEOAE, transient evoked otoacoustic emission.
Notes: (++), significant effect of type-2 diabetes mellitus; (−), no significant effect of type-2 diabetes mellitus.
The association between hearing loss and DM2 has been extensively reported in the literature, and A higher prevalence of hearing loss is reported among diabetic individuals. Horikawa et al.[24] observed that the occurrence of hearing loss is 2.1 times higher in individuals with DM2 compared with healthy individuals. Microangiopathy, neuropathy, and mitochondrial damage are considered three multifactorial conditions that lead to and increase the prevalence of hearing impairment in DM. Impaired metabolic functioning due to diabetes might result in deterioration of pure-tone thresholds, speech-recognition thresholds (SRTs), and speech-recognition scores (SISs). An evaluation of 104 DM2 patients and 104 non-diabetic controls revealed significantly poorer air-conduction thresholds, bone-conduction thresholds and speech-recognition scores.[25] However, no significant difference was noted in immittance measures that assessed middle-ear functioning.[25] Similarly, significantly poorer hearing thresholds were observed in two studies[26] [27] comparing DM2 individuals and non-diabetic healthy controls; the authors concluded that the metabolic changes caused by diabetes can modify the micromechanics of the inner ear, which affects the hearing function. Increased stromal cell-derived factor 1a (SDF-1a), a microangiopathic marker, was observed in DM individuals who exhibited poorer (higher) hearing threshold levels across all frequencies and more difficulty in speech discrimination.[28]
Reduced perception of sounds, especially at high frequencies, such as those between 4,000 Hz and 8,000 Hz, was observed in individuals with DM2.[15] Similarly, Díaz de León-Morales et al.[13] reported an increased perception threshold at 8,000 Hz. The increase in hearing sensitivity regarding high-frequency signals could be a result of degeneration or loss of outer hair cells predominantly at the basal turn of cochlea in DM2.[29] [30] Some investigators[9] have suggested changes in the capillary lumen as a result of thickening of the basilar membrane and atrophy of the stria vascularis as important contributors for the hearing impairment in diabetic individuals.
Disruption in glucose metabolism can compromise the functioning of the outer hair cells, since glucose is considered the energy source for the cochlea. One study[31] stated that the odds of failing the distortion-product otoacoustic emissions (DPOAEs) were 7 and 15 times higher for the right and left ears respectively among DM2 participants compared with normal healthy controls. Similarly, decreased signal-to-noise ratio and abnormal DPOAEs were observed in DM2 individuals.[32] [33] Studies[15] [27] on transient-evoked otoacoustic emissions (TEOAEs) reported reduced reproducibility in both ears and lower mean amplitudes in DM2 individuals. Reduced mean amplitudes of otoacoustic emissions in DM2 individuals indicate that the cochlea can also be a target organ for hyperglycemia, resulting in widespread tissue damage. Changes in the brain metabolites, such as on the concentrations of N-acetyl aspartate and myoinositol might add up to the hearing changes in diabetic patients.[34] Regardless of the type of DM, it is clearly understood from the aforementioned studies that malfunctioning of the outer hair cells might be associated with hyperglycemia.
Studies[35] [36] on auditory-evoked potentials (AEPs) and nerve conduction have reported the involvement of central and peripheral neuropathies in DM individuals. A significant delay in the absolute latency of waves I, II, III, IV and V and interpeak latencies (IPLs) of waves I-III, I-V and III-V was observed in DM2 individuals.[37] Other studies[38] [39] with DM2 patients and healthy controls have reported a significant increase in the absolute latencies of waves I, III and V and IPLs of waves III-V and I-V. Kannan[40] also reported an increase in both absolute latencies (of waves III and V) and IPLs (of waves I-III, I-V and III-V) in DM2 individuals compared with healthy controls. Studies[41] [42] reporting the effect of stimulus intensity on AEPs in DM2 revealed a significant increase in the absolute latencies of waves III and V and IPLs of waves I-III, III-V and I-V at 70 dBnHL and 80 dBnHL, whereas, at 90 dBnHL, the authors found a significant increase in the absolute latency of wave I compared with that of the other two intensities. It can be inferred from the aforementioned findings, that DM2 can result in reduced conduction velocity in the auditory nerve that occurs secondary to diabetic neuropathy. Some authors[37] [38] [39] [40] suggest that the prolongation of wave I could be due to a reduction in the time of peripheral transmission, and that the prolongation of waves III and V could be due to a reduction in the time of central transmission. This can be attributed to the neuronal degeneration that results from the oxidative stress and apoptosis of neurons in DM2. The delay in IPLs reveals retrocochlear and brainstem involvement. Contradicting these findings, Jabbari Moghaddam[16] reported no significant difference in the findings regarding auditory brainstem response (ABR) and otoacoustic emissions (OAEs) among individuals with and without DM2. These outcomes could be due to subjective factors such as age (< 50 years), duration of the diabetes (< 10 years), and glycemic control (good control).[16]
With respect to how speech signals are processed at the subcortical level in DM2, Gupta et al.[43] found that the latency and amplitude for both transient and sustained responses were significantly reduced in DM2 individuals compared with individuals without DM2. A similar trend with respect to latency was reported by Sanju et al.[44] for the transient and sustained responses of the speech-evoked response Thus, these findings are ascribed to factors such as reduced outer hair cell activity, impaired neuronal conduction time, and degeneration at the level of the brainstem.
Brain involvement is common in longstanding DM. Reduced serotonergic neurotransmission along the sensory cortex predominantly with the auditory cortex was observed due to metabolic changes in DM. Manjarrez et al.[45] observed that the latency of the N1 and P2 peaks was found to be significantly prolonged in women with DM2 compared with women in the control group. Auditory late-latency response (ALLR) showed prolonged latencies and reduced amplitude of the P1, N1 and P2 peaks in individuals with DM2.[46] These findings have been attributed to the possible change in conductivity of the thalamo-cortical pathways, or the reduced level of activity in the serotonergic neurons, which affects the lower tolerance threshold of the cortical pyramidal neurons.[47]
#
Vestibular Evaluation in Type-2 Diabetes Mellitus
The process by which DM affects vestibular function may involve parts or all of the vestibular structures. Major contributing factors for vestibular impairment in DM2 are the microangiopathic effects, such as ischemia of the vestibular structures, alteration of the meatabolism of the inner ear fluid, and loss of type-I hair cells in the saccule.[17] [Table 3] shows a summary of the DM2 studies that deal with the peripheral vestibular evaluations in particular.
Serial Number (Sl. No.) |
References |
Year |
Tests administered |
Number of participants EG/CG |
Significance |
---|---|---|---|---|---|
1. |
Bektas et al.[51] |
2008 |
c-VEMP |
13/21 |
(−) |
2. |
Konukseven et al.[49] |
2015 |
c- VEMP and o- VEMP |
30/31 |
Latency (++); AR and Amp (−) |
3. |
Sahu et al.[50] |
2015 |
c-VEMP |
15/15 |
(++) |
4. |
Kanmuri et al.[48] |
2018 |
c- VEMP |
40/20 |
(++) |
5. |
Kalkan et al.[52] |
2018 |
c- VEMP, o- VEMP and vHIT |
33/35 |
VEMP (++); vHIT (−) |
6. |
Omar et al.[53] |
2018 |
c- VEMP, o- VEMP and vHIT, |
8/8 |
VEMP, vHIT (−) |
Abbreviations: Amp, amplitude; AR, asymmetry ratio; c-VEMP, Cervical vestibular-evoked myogenic potential; o-VEMP, ocular vestibular-evoked myogenic potential; CG, control group; EG, experimental group; VEMP, vestibular-evoked myogenic potential; vHIT, video head impulse test.
Notes: (++), significant effect of type-2 diabetes mellitus; (−), no significant effect of type-2 diabetes mellitus.
However, there are only a handful of studies[48] [49] [50] [51] [52] [53] focusing on the functioning of otolith organs and semicircular canals (SCCs) in DM2 individuals. Ocular and cervical vestibular-evoked myogenic potentials (o-VEMPs and c-VEMPs) are known to assess the functioning of the otolith organs.The video head impulse test (vHIT) can assess the SCCs in all the three different planes. Kanumuri et al.[48] reported that DM can have an impact on the impairment of the vestibular system. They performed c-VEMPs on 40 DM2 individuals, and compared these results with the 20 controls. The authors reported absence of c-VEMP responses in 10% of the DM2 individuals, and delayed P13 and N23 latencies in 20% of them. Konukseven et al.[49] observed significantly prolonged o-VEMP latencies in DM2 individuals compared with prediabetic and healthy controls without any central or peripheral vestibular pathology.[49] Similarly, reduced amplitudes in both c-VEMPs and o-VEMPs were observed in DM2 individuals.[50] Vestibular dysfunctions in DM2 individuals could be aconsequence of sensory or motor polyneuropathy.[49]
Contrary to these findings, a few reports suggest no significant difference between the latency and amplitude of VEMP responses among diabetics and control groups.[51] The authors attribute these findings to the unaltered conduction times in the VEMP pathway. Another reason for the similar VEMP findings in both the groups could also be no vestibular symptoms or complaint reported by the participants in both the groups. Thus, it can be established that peripheral vestibular organs may not experience the same extent of diabetic angiopathic change as other inner-ear structures.
Both studies[52] [53] on vHIT in DM2 showed no significant group difference in the gain in vestibulo-ocular reflex (VOR) between the clinical and the control groups. Further, both studies showed unanimous agreement about the lack of refixation saccades in DM2 individuals. These findings point toward the ineffectiveness of the vHIT in identifying pathologies of the SCCs in DM2. This could be attributed to the nature of the pathology. Type-2 DM is a chronic condition which brings about slowly progressive changes. It is well known that the vHIT is not sensitive to slowly-occurring or chronic pathologies.[54] [55]
While the studies on the assessment of hearing provide conclusive evidence for damage associated with DM2, the studies on the assessment of vestibular function in these individuals are less supportive of a cause-and-effect relationship. Based on the studies evaluated, the small sample, the conflicting results, and the different methodologies, it is not possible to conclude that vestibular damage is caused by DM2.
#
#
Conclusion
In summary, the present systematic review is a brief introduction that explains DM2 and its effect on the auditory and vestibular systems. The odds of having hearing loss are found to be higher in diabetic individuals compared with non-diabetic individuals. Studies on AEPs revealed a trend for prolonged latencies and reduced amplitudes of waves in DM2, providing significant differences between diabetic and non-diabetic groups. Hence, DM2 individuals should be counselled regarding the disease and its effect on audition. The studies that peformed vestibular assessments show no conclusive evidence for the vestibular damage. Therefore, more studies on vestibular assessment in DM2 patients are nedded.
#
#
Conflict of Interests
The authors have no conflict of interests to declare.
Acknowledgments
The authors would like to thank the Ministry of Health and Family Welfare, Government of India, for financial support, and the Director of the All India Institute of Speech and Hearing (AIISH), Mysuru, and the Head of the Department of Audiology for granting permission to carry out the study.
-
References
- 1 IDF, (2017), Eighth edition 2017 . International Diabetes Federation. IDF Diabetes Atlas, 8th edn. Brussels, Belgium: International Diabetes Federation, 2017. http://www.diabetesatlas.org. https://doi.org/http://dx.doi. org/10.1016/S0140-6736 (16)31679–8.
- 2 American Diabetes Association. Standards of medical care in diabetes - 2017. J Clin Appl Res Educ 2017; 40 (01) 1-113
- 3 Kumar PJ, Clark M. 2002. Textbook of Clinical Medicine. Pub; Saunders, London, UK: 1099-1121
- 4 American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2009; 32 (01, Suppl 1): S62-S67
- 5 Rubin RR, Peyrot M. Quality of life and diabetes. Diabetes Metab Res Rev 1999; 15 (03) 205-218 DOI: 10.1002/(SICI)1520-7560(199905/06)15:3<205:AID-DMRR29>3.0.CO;2-O.
- 6 Baynest HW. Classification, Pathophysiology, Diagnosis and Management of Diabetes Mellitus. J Diabetes Metab 2015; 6: 541
- 7 Maia CAS, Campos CA. Diabetes mellitus as etiological factor of hearing loss. Rev Bras Otorrinolaringol (Engl Ed) 2005; 71 (02) 208-214 DOI: 10.1016/s1808-8694(15)31312-4.
- 8 Ferreira Jr CA, Guimarães RES, Becker HMG. et al. Metabolic evaluation of the patient with labyrinth disease. Arq Otorhinolaringol 2000; 4 (01) 28-32
- 9 Tomisawa H. [Diabetic changes in the stria vascularis in humans--a study of PAS-stained temporal bone sections]. Nippon Jibiinkoka Gakkai Kaiho 2000; 103 (11) 1227-1237
- 10 Xipeng L, Ruiyu L, Yanzhuo Z, Kaosan G, Liping W. Effects of diabetes on hearing and cochlear structures. J Otol 2013; 8 (02) 82-87
- 11 Wang SL, Chen XM, Bi DZ, Ye YF, He TF. Ultrastructural changes of inner ear capillaries in experimental diabetic rats. J Audiol Speech Pathol 2006; 14 (04) 278-279
- 12 Raynor EM, Carrasco VN, Prazma J, Pillsbury HC. An assessment of cochlear hair-cell loss in insulin-dependent diabetes mellitus diabetic and noise-exposed rats. Arch Otolaryngol Head Neck Surg 1995; 121 (04) 452-456
- 13 Díaz de León-Morales LV, Jáuregui-Renaud K, Garay-Sevilla ME, Hernández-Prado J, Malacara-Hernández JM. De León-MoralesLVD. Auditory impairment in patients with type 2 diabetes mellitus. Arch Med Res 2005; 36 (05) 507-510 DOI: 10.1016/j.arcmed.2005.02.002.
- 14 Ren J, Zhao P, Chen L, Xu A, Brown SN, Xiao X. Hearing loss in middle-aged subjects with type 2 diabetes mellitus. Arch Med Res 2009; 40 (01) 18-23
- 15 Vesperini E, Di Giacobbe F, Passatore M, Vesperini G, Sorgi C, Vespasiani G. Audiological screening in people with diabetes. First results. Audiology Res 2011; 1 (01, 1S): e8 DOI: 10.4081/audiores.2011.e8.
- 16 Jabbari Moghaddam Y. Acoustic emissions from the inner ear and brain stem responses in type 2 diabetics. Int J Gen Med 2011; 4: 871-874 DOI: 10.2147/IJGM.S19367.
- 17 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 (10) 938-944
- 18 Razzak RA, Bagust J, Docherty S, Hussein W, Al-Otaibi A. Augmented asymmetrical visual field dependence in asymptomatic diabetics: evidence of subclinical asymmetrical bilateral vestibular dysfunction. J Diabetes Complications 2015; 29 (01) 68-72 DOI: 10.1016/j.jdiacomp.2014.09.009.
- 19 Jauregui-Renaud K, Ramon-Toledo V, Aguilar-Bolanos M, Montano-Velazques B, Pliego-Maldonado A. Symptoms of detachment from the self or from the environment in patients with an acquired deficiency of the special senses - Journal of Vestibular Research 2008; Volume 18, Number 2–3 / 2008 - IOS Press. J Vestib Res 2008; 18: 129-137 http://iospress.metapress.com.ezproxy.welch.jhmi.edu/content/u712u4p042856006/?gen
- 20 Nathan DM. The pathophysiology of diabetic complications: how much does the glucose hypothesis explain?. Ann Intern Med 1996; 124 (1 Pt 2): 86-89
- 21 Lue JH, Day AS, Cheng PW, Young YH. Vestibular evoked myogenic potentials are heavily dependent on type I hair cell activity of the saccular macula in guinea pigs. Audiol Neurotol 2009; 14 (01) 59-66 DOI: 10.1159/000156701.
- 22 Myers SF, Ross MD. Morphological evidence of vestibular pathology in long-term experimental diabetes mellitus. II. Connective tissue and neuroepithelial pathology. Acta Otolaryngol 1987; 104 (1-2): 40-49 DOI: 10.3109/00016488709109045.
- 23 Liberati A, Altman DG, Tetzlaff J. et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 2009; 339: b2700
- 24 Horikawa C, Kodama S, Tanaka S. et al. Diabetes and risk of hearing impairment in adults: a meta-analysis. J Clin Endocrinol Metab 2013; 98 (01) 51-58 DOI: 10.1210/jc.2012-2119.
- 25 Özel HE, Özkiriş M, Gencer ZK, Saydam L. Audiovestibular functions in noninsulin-dependent diabetes mellitus. Acta Otolaryngol 2014; 134 (01) 51-57 DOI: 10.3109/00016489.2013.840925.
- 26 Hemashree J, Preetha S. Audiometry in Type 2 Diabetic and Non-Diabetic Patients of the Age Group 45 To 65 Years : a Comparative Study. Asian J Pharm Clin Res 2016; 9 (01) 177-178
- 27 Meena R, Sonkhya D, Sonkhya N. Evaluation of hearing loss in patients with type 2 diabetes mellitus. Int J Res Med Sci 2016; 4 (06) 2281-2287 DOI: 10.18203/2320-6012.ijrms20161800.
- 28 Loader B, Stokic D, Riedl M. et al. Combined analysis of audiologic performance and the plasma biomarker stromal cell-derived factor 1a in type 2 diabetic patients. Otol Neurotol 2008; 29 (06) 739-744 DOI: 10.1097/MAO.0b013e318172cf89.
- 29 Nakae S, Tachibana M. The cochlea of the spontaneously diabetic mouse. II. Electron microscopic observations of non-obese diabetic mice. Arch Otorhinolaryngol 1986; 243 (05) 313-316
- 30 Fukushima H, Cureoglu S, Schachern PA, Paparella MM, Harada T, Oktay MF. Effects of type 2 diabetes mellitus on cochlear structure in humans. Arch Otolaryngol Head Neck Surg 2006; 132 (09) 934-938
- 31 Paluru R, Indla Y, Chellam R, Santhakumari R. Assessment of functional status of outer hair cells in Type 2 diabetes by using distortion product otoacoustic emissions. Natl J Physiol Pharm Pharmacol 2016; 6 (05) 412-415 DOI: 10.5455/njppp.2016.6.0411404052016.
- 32 Karabulut H, Karabulut I, Dağli M. et al. Evaluation of outer hair cell function and medial olivocochlear efferent system in patients with type II diabetes mellitus. Turk J Med Sci 2014; 44 (01) 150-156 DOI: 10.3906/sag-1207-99.
- 33 Li J, Zhang Y, Fu X. et al. Alteration of auditory function in type 2 diabetic and pre-diabetic patients. Acta Otolaryngol 2018; 138 (06) 542-547 DOI: 10.1080/00016489.2017.1422084.
- 34 Santhakumari R, Reddy IY, Archana R, Rajesh P. Role of yoga in alienating the memory decline and frontal lobe metabolite changes in type 2 diabetes. Int J Res Ayurveda Pharm 2016; 7 (01) 78-81 DOI: 10.7897/ 2277–4343.07116.
- 35 Gupta S, Baweja P, Mittal S, Kumar A, Singh KD, Sharma R. Brainstem auditory evoked potential abnormalities in type 2 diabetes mellitus. N Am J Med Sci 2013; 5 (01) 60-65 DOI: 10.4103/1947-2714.106211.
- 36 Dolu H, Ulas UH, Bolu E. et al. Evaluation of central neuropathy in type II diabetes mellitus by multimodal evoked potentials. Acta Neurol Belg 2003; 103 (04) 206-211
- 37 Goyal I, Singh M, Singh B, Singh KD, Sachdeva P. A study of auditory brainstem evoked responses in type 1 and type 2 diabetes mellitus patients with normal hearing. Int J Otorhinolaryngol Head Neck Surg 2019; 5: 1303-1308
- 38 Murugesan R, Munusamy G, Kannan R. Evaluation of brainstem auditory evoked potential in type 2 diabetes mellitus individuals. Int J Res Med Sci 2016; 4 (09) 3939-3944 DOI: 10.18203/2320-6012.ijrms20162912.
- 39 Victor R, Shabina B, Devanand V. Assessment of auditory evoked potential in type ii diabetes mellitus individuals –a case control study. Indian J Res 2018; 7: 6-7
- 40 Kannan KMD. Study of brainstem auditory evoked potentials in type 2 diabetic patients. Indian J Basic Appl Med Res 2017; 6 (04) 341-349
- 41 Gupta R, Aslam M, Hasan S, Siddiqi S. Type -2 diabetes mellitus and auditory brainstem responses-a hospital based study. Indian J Endocrinol Metab 2010; 14 (01) 9-11
- 42 Suresh S, Ramlan S, Somayaji G, Sequeira N. Brainstem auditory responses in type-2 diabetes mellitus. Int J Otorhinolaryngol Head Neck Surg 2018; 4 (02) 522-525 DOI: 10.18203/issn.2454-5929.ijohns20180718.
- 43 Gupta S, Bhat JS, Kumar K. Subcortical processing of speech in individuals with type 2 diabetes mellitus. Int J Diabetes Dev Ctries 2015; 35 (03) 327-331 DOI: 10.1007/s13410-015-0299-y.
- 44 Sanju HK, Mohanan A, Kumar P. Speech-Evoked Auditory Brainstem Response in Individuals with Diabetes Mellitus Type 2. J Int Adv Otol 2017; 13 (01) 77-82
- 45 Manjarrez G, Vazquez F, Delgado M, Herrera R, Hernandez J. A functional disturbance in the auditory cortex related to a low serotonergic neurotransmission in women with type 2 diabetes. Neuroendocrinology 2007; 86 (04) 289-294 DOI: 10.1159/000109375.
- 46 Kumar K, Bhat J, Varghese A. Auditory Late Latency Response in Individuals with Type 2 Diabetes Mellitus. J Int Adv Otol 2018; 14 (03) 408-411 DOI: 10.5152/iao.2018.3201.
- 47 Comi G. Evoked potentials in diabetes mellitus. Clin Neurosci 1997; 4 (06) 374-379
- 48 Kanumuri S, Chaitanya KV, Nara J, Reddy VK. Role of Cervical Vestibular-Evoked Myogenic Potentials in Evaluating Vestibular Dysfunction in Patients with Type II Diabetes Mellitus: A Prospective Institutional Study. Indian J Otol 2018;24(02):
- 49 Konukseven O, Polat SB, Karahan S. 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 (08) 536-543 DOI: 10.3109/14992027.2014.971887.
- 50 Sahu M, Sinha SK. Assessment of sacculocollic pathway in individuals with diabetes mellitus. Int J Health Sci Res 2015; 3135 (11) 313-320
- 51 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 (07) 768-771 DOI: 10.1080/00016480701714251.
- 52 Kalkan M, Bayram A, Gökay F, Cura HS, Mutlu C. Assessment of vestibular-evoked myogenic potentials and video head impulse test in type 2 diabetes mellitus patients with or without polyneuropathy. Eur Arch Otorhinolaryngol 2018; 275 (03) 719-724
- 53 Omar M, Wahat NHA, Zulkafli MFA, Husain NF, Sulaiman S. Does postural instability in type 2 diabetes relate to vestibular function?. Indian J Otol 2018; 24 (03) 172
- 54 McCaslin DL, Jacobson GP, Bennett ML, Gruenwald JM, Green AP. Predictive properties of the video head impulse test: measures of caloric symmetry and self-report dizziness handicap. Ear Hear 2014; 35 (05) e185-e191
- 55 Mahringer A, Rambold HA. Caloric test and video-head-impulse: a study of vertigo/dizziness patients in a community hospital. Eur Arch Otorhinolaryngol 2014; 271 (03) 463-472
- 56 Panchu P. Auditory acuity in type 2 diabetes mellitus. Int J Diabetes Dev Ctries 2008; 28 (04) 114-120
- 57 Durmus C, Yetiser S, Durmus O. Auditory brainstem evoked responses in insulin-dependent (ID) and non-insulin-dependent (NID) diabetic subjects with normal hearing. Int J Audiol 2004; 43 (01) 29-33
- 58 Mahallik D, Sahu P, Mishra R. Evaluation of auditory brain-stem evoked response in middle: Aged type 2 diabetes mellitus with normal hearing subjects. Indian J Otol 2014; 20 (04) 199
- 59 Yikawe SS, Iseh KR, Sabir AA, Solomon JH, Manya C, Aliyu N. Hearing Thresholds among Type 2. Diabetics in Sokoto, Nigeria: A Comparative Study. Int J Res Development 2017; 6 (03) 184-190
- 60 Gulati A, Kakkar V, Aggarwal S. et al. To Study the Effect of Type II Diabetes Mellitus and Its Duration on Hearing. Int J Adv Int Med Sci 2017; 2 (03) 140-143
Address for correspondence
Publication History
Received: 23 April 2020
Accepted: 24 November 2020
Article published online:
20 July 2021
© 2021. Fundação Otorrinolaringologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commecial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)
Thieme Revinter Publicações Ltda.
Rua do Matoso 170, Rio de Janeiro, RJ, CEP 20270-135, Brazil
-
References
- 1 IDF, (2017), Eighth edition 2017 . International Diabetes Federation. IDF Diabetes Atlas, 8th edn. Brussels, Belgium: International Diabetes Federation, 2017. http://www.diabetesatlas.org. https://doi.org/http://dx.doi. org/10.1016/S0140-6736 (16)31679–8.
- 2 American Diabetes Association. Standards of medical care in diabetes - 2017. J Clin Appl Res Educ 2017; 40 (01) 1-113
- 3 Kumar PJ, Clark M. 2002. Textbook of Clinical Medicine. Pub; Saunders, London, UK: 1099-1121
- 4 American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 2009; 32 (01, Suppl 1): S62-S67
- 5 Rubin RR, Peyrot M. Quality of life and diabetes. Diabetes Metab Res Rev 1999; 15 (03) 205-218 DOI: 10.1002/(SICI)1520-7560(199905/06)15:3<205:AID-DMRR29>3.0.CO;2-O.
- 6 Baynest HW. Classification, Pathophysiology, Diagnosis and Management of Diabetes Mellitus. J Diabetes Metab 2015; 6: 541
- 7 Maia CAS, Campos CA. Diabetes mellitus as etiological factor of hearing loss. Rev Bras Otorrinolaringol (Engl Ed) 2005; 71 (02) 208-214 DOI: 10.1016/s1808-8694(15)31312-4.
- 8 Ferreira Jr CA, Guimarães RES, Becker HMG. et al. Metabolic evaluation of the patient with labyrinth disease. Arq Otorhinolaringol 2000; 4 (01) 28-32
- 9 Tomisawa H. [Diabetic changes in the stria vascularis in humans--a study of PAS-stained temporal bone sections]. Nippon Jibiinkoka Gakkai Kaiho 2000; 103 (11) 1227-1237
- 10 Xipeng L, Ruiyu L, Yanzhuo Z, Kaosan G, Liping W. Effects of diabetes on hearing and cochlear structures. J Otol 2013; 8 (02) 82-87
- 11 Wang SL, Chen XM, Bi DZ, Ye YF, He TF. Ultrastructural changes of inner ear capillaries in experimental diabetic rats. J Audiol Speech Pathol 2006; 14 (04) 278-279
- 12 Raynor EM, Carrasco VN, Prazma J, Pillsbury HC. An assessment of cochlear hair-cell loss in insulin-dependent diabetes mellitus diabetic and noise-exposed rats. Arch Otolaryngol Head Neck Surg 1995; 121 (04) 452-456
- 13 Díaz de León-Morales LV, Jáuregui-Renaud K, Garay-Sevilla ME, Hernández-Prado J, Malacara-Hernández JM. De León-MoralesLVD. Auditory impairment in patients with type 2 diabetes mellitus. Arch Med Res 2005; 36 (05) 507-510 DOI: 10.1016/j.arcmed.2005.02.002.
- 14 Ren J, Zhao P, Chen L, Xu A, Brown SN, Xiao X. Hearing loss in middle-aged subjects with type 2 diabetes mellitus. Arch Med Res 2009; 40 (01) 18-23
- 15 Vesperini E, Di Giacobbe F, Passatore M, Vesperini G, Sorgi C, Vespasiani G. Audiological screening in people with diabetes. First results. Audiology Res 2011; 1 (01, 1S): e8 DOI: 10.4081/audiores.2011.e8.
- 16 Jabbari Moghaddam Y. Acoustic emissions from the inner ear and brain stem responses in type 2 diabetics. Int J Gen Med 2011; 4: 871-874 DOI: 10.2147/IJGM.S19367.
- 17 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 (10) 938-944
- 18 Razzak RA, Bagust J, Docherty S, Hussein W, Al-Otaibi A. Augmented asymmetrical visual field dependence in asymptomatic diabetics: evidence of subclinical asymmetrical bilateral vestibular dysfunction. J Diabetes Complications 2015; 29 (01) 68-72 DOI: 10.1016/j.jdiacomp.2014.09.009.
- 19 Jauregui-Renaud K, Ramon-Toledo V, Aguilar-Bolanos M, Montano-Velazques B, Pliego-Maldonado A. Symptoms of detachment from the self or from the environment in patients with an acquired deficiency of the special senses - Journal of Vestibular Research 2008; Volume 18, Number 2–3 / 2008 - IOS Press. J Vestib Res 2008; 18: 129-137 http://iospress.metapress.com.ezproxy.welch.jhmi.edu/content/u712u4p042856006/?gen
- 20 Nathan DM. The pathophysiology of diabetic complications: how much does the glucose hypothesis explain?. Ann Intern Med 1996; 124 (1 Pt 2): 86-89
- 21 Lue JH, Day AS, Cheng PW, Young YH. Vestibular evoked myogenic potentials are heavily dependent on type I hair cell activity of the saccular macula in guinea pigs. Audiol Neurotol 2009; 14 (01) 59-66 DOI: 10.1159/000156701.
- 22 Myers SF, Ross MD. Morphological evidence of vestibular pathology in long-term experimental diabetes mellitus. II. Connective tissue and neuroepithelial pathology. Acta Otolaryngol 1987; 104 (1-2): 40-49 DOI: 10.3109/00016488709109045.
- 23 Liberati A, Altman DG, Tetzlaff J. et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 2009; 339: b2700
- 24 Horikawa C, Kodama S, Tanaka S. et al. Diabetes and risk of hearing impairment in adults: a meta-analysis. J Clin Endocrinol Metab 2013; 98 (01) 51-58 DOI: 10.1210/jc.2012-2119.
- 25 Özel HE, Özkiriş M, Gencer ZK, Saydam L. Audiovestibular functions in noninsulin-dependent diabetes mellitus. Acta Otolaryngol 2014; 134 (01) 51-57 DOI: 10.3109/00016489.2013.840925.
- 26 Hemashree J, Preetha S. Audiometry in Type 2 Diabetic and Non-Diabetic Patients of the Age Group 45 To 65 Years : a Comparative Study. Asian J Pharm Clin Res 2016; 9 (01) 177-178
- 27 Meena R, Sonkhya D, Sonkhya N. Evaluation of hearing loss in patients with type 2 diabetes mellitus. Int J Res Med Sci 2016; 4 (06) 2281-2287 DOI: 10.18203/2320-6012.ijrms20161800.
- 28 Loader B, Stokic D, Riedl M. et al. Combined analysis of audiologic performance and the plasma biomarker stromal cell-derived factor 1a in type 2 diabetic patients. Otol Neurotol 2008; 29 (06) 739-744 DOI: 10.1097/MAO.0b013e318172cf89.
- 29 Nakae S, Tachibana M. The cochlea of the spontaneously diabetic mouse. II. Electron microscopic observations of non-obese diabetic mice. Arch Otorhinolaryngol 1986; 243 (05) 313-316
- 30 Fukushima H, Cureoglu S, Schachern PA, Paparella MM, Harada T, Oktay MF. Effects of type 2 diabetes mellitus on cochlear structure in humans. Arch Otolaryngol Head Neck Surg 2006; 132 (09) 934-938
- 31 Paluru R, Indla Y, Chellam R, Santhakumari R. Assessment of functional status of outer hair cells in Type 2 diabetes by using distortion product otoacoustic emissions. Natl J Physiol Pharm Pharmacol 2016; 6 (05) 412-415 DOI: 10.5455/njppp.2016.6.0411404052016.
- 32 Karabulut H, Karabulut I, Dağli M. et al. Evaluation of outer hair cell function and medial olivocochlear efferent system in patients with type II diabetes mellitus. Turk J Med Sci 2014; 44 (01) 150-156 DOI: 10.3906/sag-1207-99.
- 33 Li J, Zhang Y, Fu X. et al. Alteration of auditory function in type 2 diabetic and pre-diabetic patients. Acta Otolaryngol 2018; 138 (06) 542-547 DOI: 10.1080/00016489.2017.1422084.
- 34 Santhakumari R, Reddy IY, Archana R, Rajesh P. Role of yoga in alienating the memory decline and frontal lobe metabolite changes in type 2 diabetes. Int J Res Ayurveda Pharm 2016; 7 (01) 78-81 DOI: 10.7897/ 2277–4343.07116.
- 35 Gupta S, Baweja P, Mittal S, Kumar A, Singh KD, Sharma R. Brainstem auditory evoked potential abnormalities in type 2 diabetes mellitus. N Am J Med Sci 2013; 5 (01) 60-65 DOI: 10.4103/1947-2714.106211.
- 36 Dolu H, Ulas UH, Bolu E. et al. Evaluation of central neuropathy in type II diabetes mellitus by multimodal evoked potentials. Acta Neurol Belg 2003; 103 (04) 206-211
- 37 Goyal I, Singh M, Singh B, Singh KD, Sachdeva P. A study of auditory brainstem evoked responses in type 1 and type 2 diabetes mellitus patients with normal hearing. Int J Otorhinolaryngol Head Neck Surg 2019; 5: 1303-1308
- 38 Murugesan R, Munusamy G, Kannan R. Evaluation of brainstem auditory evoked potential in type 2 diabetes mellitus individuals. Int J Res Med Sci 2016; 4 (09) 3939-3944 DOI: 10.18203/2320-6012.ijrms20162912.
- 39 Victor R, Shabina B, Devanand V. Assessment of auditory evoked potential in type ii diabetes mellitus individuals –a case control study. Indian J Res 2018; 7: 6-7
- 40 Kannan KMD. Study of brainstem auditory evoked potentials in type 2 diabetic patients. Indian J Basic Appl Med Res 2017; 6 (04) 341-349
- 41 Gupta R, Aslam M, Hasan S, Siddiqi S. Type -2 diabetes mellitus and auditory brainstem responses-a hospital based study. Indian J Endocrinol Metab 2010; 14 (01) 9-11
- 42 Suresh S, Ramlan S, Somayaji G, Sequeira N. Brainstem auditory responses in type-2 diabetes mellitus. Int J Otorhinolaryngol Head Neck Surg 2018; 4 (02) 522-525 DOI: 10.18203/issn.2454-5929.ijohns20180718.
- 43 Gupta S, Bhat JS, Kumar K. Subcortical processing of speech in individuals with type 2 diabetes mellitus. Int J Diabetes Dev Ctries 2015; 35 (03) 327-331 DOI: 10.1007/s13410-015-0299-y.
- 44 Sanju HK, Mohanan A, Kumar P. Speech-Evoked Auditory Brainstem Response in Individuals with Diabetes Mellitus Type 2. J Int Adv Otol 2017; 13 (01) 77-82
- 45 Manjarrez G, Vazquez F, Delgado M, Herrera R, Hernandez J. A functional disturbance in the auditory cortex related to a low serotonergic neurotransmission in women with type 2 diabetes. Neuroendocrinology 2007; 86 (04) 289-294 DOI: 10.1159/000109375.
- 46 Kumar K, Bhat J, Varghese A. Auditory Late Latency Response in Individuals with Type 2 Diabetes Mellitus. J Int Adv Otol 2018; 14 (03) 408-411 DOI: 10.5152/iao.2018.3201.
- 47 Comi G. Evoked potentials in diabetes mellitus. Clin Neurosci 1997; 4 (06) 374-379
- 48 Kanumuri S, Chaitanya KV, Nara J, Reddy VK. Role of Cervical Vestibular-Evoked Myogenic Potentials in Evaluating Vestibular Dysfunction in Patients with Type II Diabetes Mellitus: A Prospective Institutional Study. Indian J Otol 2018;24(02):
- 49 Konukseven O, Polat SB, Karahan S. 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 (08) 536-543 DOI: 10.3109/14992027.2014.971887.
- 50 Sahu M, Sinha SK. Assessment of sacculocollic pathway in individuals with diabetes mellitus. Int J Health Sci Res 2015; 3135 (11) 313-320
- 51 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 (07) 768-771 DOI: 10.1080/00016480701714251.
- 52 Kalkan M, Bayram A, Gökay F, Cura HS, Mutlu C. Assessment of vestibular-evoked myogenic potentials and video head impulse test in type 2 diabetes mellitus patients with or without polyneuropathy. Eur Arch Otorhinolaryngol 2018; 275 (03) 719-724
- 53 Omar M, Wahat NHA, Zulkafli MFA, Husain NF, Sulaiman S. Does postural instability in type 2 diabetes relate to vestibular function?. Indian J Otol 2018; 24 (03) 172
- 54 McCaslin DL, Jacobson GP, Bennett ML, Gruenwald JM, Green AP. Predictive properties of the video head impulse test: measures of caloric symmetry and self-report dizziness handicap. Ear Hear 2014; 35 (05) e185-e191
- 55 Mahringer A, Rambold HA. Caloric test and video-head-impulse: a study of vertigo/dizziness patients in a community hospital. Eur Arch Otorhinolaryngol 2014; 271 (03) 463-472
- 56 Panchu P. Auditory acuity in type 2 diabetes mellitus. Int J Diabetes Dev Ctries 2008; 28 (04) 114-120
- 57 Durmus C, Yetiser S, Durmus O. Auditory brainstem evoked responses in insulin-dependent (ID) and non-insulin-dependent (NID) diabetic subjects with normal hearing. Int J Audiol 2004; 43 (01) 29-33
- 58 Mahallik D, Sahu P, Mishra R. Evaluation of auditory brain-stem evoked response in middle: Aged type 2 diabetes mellitus with normal hearing subjects. Indian J Otol 2014; 20 (04) 199
- 59 Yikawe SS, Iseh KR, Sabir AA, Solomon JH, Manya C, Aliyu N. Hearing Thresholds among Type 2. Diabetics in Sokoto, Nigeria: A Comparative Study. Int J Res Development 2017; 6 (03) 184-190
- 60 Gulati A, Kakkar V, Aggarwal S. et al. To Study the Effect of Type II Diabetes Mellitus and Its Duration on Hearing. Int J Adv Int Med Sci 2017; 2 (03) 140-143
![](https://www.thieme-connect.de/media/10.1055-s-00025477/202202/thumbnails/10-1055-s-0041-1726041-i200094-1.jpg)
![Zoom Image](/products/assets/desktop/css/img/icon-figure-zoom.png)