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 Table of Contents  
Year : 2016  |  Volume : 43  |  Issue : 4  |  Page : 163-171

The relationship between auditory brainstem response, nerve conduction studies, and metabolic risk factors in type II diabetes mellitus

1 Department of Neurology and Psychiatry, Faculty of Medicine, Assiut University Hospital, Assiut University, Assiut, Egypt
2 Audiology Unit, Department of ENT, Faculty of Medicine, Assiut University Hospital, Assiut University, Assiut, Egypt
3 Department of Clinical Pathology, Faculty of Medicine, Assiut University Hospital, Assiut University, Assiut, Egypt
4 Department of Physical Medicine, Rheumatology and Rehabilitation, Faculty of Medicine, Assiut University Hospital, Assiut University, Assiut, Egypt
5 Department of Medical Biochemistry, Faculty of Medicine, Assiut University Hospital, Assiut University, Assiut, Egypt
6 Department of Internal Medicine, Faculty of Medicine, Assiut University Hospital, Assiut University, Assiut, Egypt

Date of Submission18-Feb-2016
Date of Acceptance12-Jun-2016
Date of Web Publication14-Oct-2016

Correspondence Address:
Noha M Abo-Elfetoh
Department of Neurology and Psychiatry, Faculty of Medicine, Assiut University Hospital, Assiut University, Assiut, 71516
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/1110-161X.192253

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Few studies have reported a correlation between auditory brainstem response (ABR) findings and nerve conduction studies (NCSs). The correlation between ABR findings and the metabolic profile of these patients is not well documented in previous studies. The present study was designed to investigate the impact of the disturbed metabolic profile (hyperglyceridemia and hyperlipidemia) in diabetic patients on the peripheral nervous system as well as the auditory brainstem response.
The present study aimed to detect the effect of diabetic control on the presence of abnormal ABR and/or peripheral nerve affection in Egyptian diabetic patients.
Patients and methods
The study was conducted on two groups: the diabetic group (n=68) and the control group, which was matched for age, sex, blood pressure, and BMI (n=60). All participants were subjected to clinical assessment, basic audiologic assessment, brainstem auditory evoked potential, NCS, and metabolic profile [serum level of glycated hemoglobin (HbA1c%) and lipid profile].
There was a significant increase in absolute wave latencies of ABR and interpeak latencies (IPLs) in the diabetic group compared with the control group. Twenty-six (38.2%) patients had abnormal ABR values. IPLs (I–III and III–V) were significantly negatively correlated with sensory conduction velocity of the sural, median, and ulnar nerves as well as F-wave latency of the posterior tibial, median, and ulnar nerves (P=0.01 and 0.001, respectively). Moreover, IPL III–V and sural sensory conduction velocity were significantly correlated with HbA1c% and total cholesterol, as well as triglyceride serum levels.
Brainstem dysfunction and ABR changes are common in patients with type II diabetes mellitus. These changes are significantly correlated to NCS parameters on one hand and serum HbA1c% and lipid profile (total cholesterol and triglycerides) on the other hand.

Keywords: auditory brainstem response, cranial neuropathy, diabetes mellitus type II, glycated hemoglobin, lipid profile, metabolic profile, nerve conduction study, peripheral neuropathy

How to cite this article:
Abo-Elfetoh NM, Mohamed ES, Tag LM, Gamal RM, Gandour AM, Abd EL Razek MR, El-Baz MA, Ez Eldeen ME. The relationship between auditory brainstem response, nerve conduction studies, and metabolic risk factors in type II diabetes mellitus. Egypt Rheumatol Rehabil 2016;43:163-71

How to cite this URL:
Abo-Elfetoh NM, Mohamed ES, Tag LM, Gamal RM, Gandour AM, Abd EL Razek MR, El-Baz MA, Ez Eldeen ME. The relationship between auditory brainstem response, nerve conduction studies, and metabolic risk factors in type II diabetes mellitus. Egypt Rheumatol Rehabil [serial online] 2016 [cited 2020 Oct 22];43:163-71. Available from: http://www.err.eg.net/text.asp?2016/43/4/163/192253

  Introduction Top

Diabetes mellitus (DM) is a clinical disorder that causes a variety of metabolic, neurological, and vascular complications [1]. In 2013, 15.6% of the Egyptian population was estimated to have diabetes. This was the second highest prevalence rate in the Middle East and North African region after Saudi Arabia. This percentage is expected to increase to 18.6% in 2035 [2].

The most common complications recorded for diabetes over time are microvascular disorders (retinopathy and nephropathy) and neuropathy (peripheral and central). DM has been implicated as an independent causative factor of sensorineural hearing loss [3]. Neuropathy, both central and peripheral, is an important complication of type II DM [4]. In general, central neuropathy in diabetic patients is developed later compared with peripheral neuropathy [5]. Many early studies had reported a longer latency of responses in patients with DM than in controls in facial nerve conduction study (NCS) and blink reflex study [6],[7].

Sensorineural hearing loss could be clinically unapparent in some patients with DM [8],[9]. The brainstem auditory evoked potentials (BAEP) is an effective and inexpensive test in the evaluation of brainstem function [10].

Previous studies have been performed to evaluate BAEP in DM patients, but these studies led to controversial results [11],[12]. The most common abnormalities in these studies were the lengthening of the latency of waves III and V [13],[14],[15]. Moreover, the interpeak latencies (IPLs) I–III, III–V, and I–V of BAEP between diabetic and nondiabetic patients have been reported to have a statistically significant difference in other studies [8],[16],[17],[18],[19],[20]. However, the correlation between the BAEP findings and NCSs and metabolic profile of those patients were not clear. However, diabetic neuropathy was found to be positively correlated with the most common marker of hyperglycemia and glycated hemoglobin (HbA1c%) [21]. Moreover, several earlier large-scale trials of type II diabetic patients pointed to the observation that early dyslipidemia was a major independent risk factor for the development of diabetic neuropathy [22]. Moreover, recent clinical evidence suggests that dyslipidemia is also associated with diabetic neuropathy. Lipid profiles are commonly abnormal early in the course of type II DM in a temporal pattern and correlates with the presence of diabetic neuropathy [23].

However, the correlation between auditory brainstem response (ABR) findings among type II diabetic patients and these metabolic factors are not well documented in previous studies [19],[24],[25].

The present study aimed to estimate the relationship between ABR findings and NCS parameters on one hand and metabolic profile among type II diabetic patients on the other hand.

  Patients and methods Top

The present study was conducted on two groups:

First group: 68 type II DM patients (26 men and 42 women) were recruited from the outpatients’ clinic of DM at the general Department Internal Medicine in Assuit University Hospital. Their ages and duration of DM ranged from 30 to 68 and 2 to 8 years, respectively. They received oral hypoglycemic agents for DM control.

Second group: 60 healthy volunteers who were matched for age, sex, and BMI were recruited as a control group (20 male and 40 female; age range: 32–68 years).

Participants of both groups were excluded if they; had previous complaints of otological disease detected in the present or past history, were exposed to ear trauma or surgery, presented with acute hearing loss or had a history of noise exposure or ototoxic drug intake, had head trauma, had a history of any medical systemic or neurological diseases, or manifested with diabetic complications (eye, kidney, and cardiac) or had a history of diabetic coma being either hypoglycemic or hyperglycemic within the last 6 months or presented with motor deficit or positive electroencephalography and neuroimaging findings.

All participants signed a written consent for participation in the study. They all underwent the following: history taking, BMI, systemic, cardiac, ophthalmic, and neurological examinations, ECG, laboratory profile, computed tomography of the brain, and neuroelectrophysiology studies (i.e. BAEP, motor, sensory conduction, and F-wave studies).

Laboratory profile included fasting serum glucose, serum HbA1c%, urea, creatinine, and lipid profile (serum cholesterol, triglyceride, low-density lipoprotein, and high-density lipoprotein).

Basic audiological evaluation

Full history taking and audiological examination were carried out to evaluate any ear disorders and identify wax presence that might impede the exams. Pure-tone and speech audiometry were carried out for each ear using a diagnostic audiometer (Madsen OB 822; Madsen Electronics, Copenhagen, Denmark) with sound delivered through headphones (model Headphones TDH-39, Telephonics; Huntington, NY, United States America).

Tympanometry and acoustic reflex threshold testing were carried out on each ear using a middle ear analyzer (Interacoustics Az26; Interacoustics, Assens Denmark Nihon Kohden model MEB-7102, Nihon Kohden Corp., Tokyo, Japan) to exclude middle ear disease.

Neuroelectrophysiology assessments

Auditory brainstem evoked potentials (BAEP or ABR) were determined using the Nihon Kohden model MEB7102” (Nihon Kohden, Corp., Tokyo, Japan). BAEP was recorded using headphones. The type of sounds used was clicks. The duration of stimulus was 0.1 ms, rate of stimulus was 10 Hz, averaging 2000, and the intensity of stimulus was 90 dB. An active electrode was attached in the zone of scalp (CZ) 5 cm from the vertex; the reference electrode was placed on the ear lobule of the tested ear, and the ground electrode was placed at the midline of the forehead. The waves routinely analyzed in BAEP were numbered (I–V). The absolute latency (stimulus to peak) of each (I, II, III, IV, and V) and IPLs (I–III, I–V, and III–V) were measured.

On the basis of control reference data, the diabetic group was classified into two subgroups, subgroup I with abnormal ABR response and subgroup II with normal ABR response. Diabetic patients with abnormal ABR response are those who had longer wave latency or IPLs of any ABR value, exceeding 2 SD of mean reference values.

Nerve conduction studies

NCS were performed using the conventional procedures and performed using the Nihon Kohden model MEB7102” EMG machine (Nihon Kohden). Motor NCS of the median, ulnar, and common peroneal nerves (CPN) were assessed using standard procedures with surface electrode. A pulse of 0.2 ms duration, at the rate of 1/s at supramaximal intensity was used for stimulation. Motor distal latencies were measured up to M-wave onset. The shape, amplitude, and duration of the compound muscle action potential (CMAP) were measured. The amplitude was measured from peak to peak and the duration from the beginning to the end of the CMAP. Motor conduction velocity (MCV) can be calculated accurately by stimulating two different points along the nerve course and measuring the latency for each response.

The normal limits of MCV and distal latencies were set at ±2 SD from the mean values of the control group. The CMAP was considered abnormal if the amplitude was below the lowest value found in controls.

For F-wave determination, 10 stimuli were given, and minimal latency value was determined for the median, ulnar, and posterior tibial nerves after stimuli at the wrist or soleus muscle respectively (stimulation at soleus muscle for determination of F-wave and H-reflex of the posterior tibial nerve) and consecutive responses were recorded. The latency to onset of the first deflection from baseline was measured for each trace, and the shortest latency was determined as minimal F-wave latency [26].

Sensory NCS of the median, ulnar, and sural nerves were tested. Sensory nerve action potentials (SNAPs) were recorded using the antidromic technique using ring electrode. Median SNAPs were recorded from the index fingers, at 14 cm from recording electrode after wrist stimulation. Ulnar nerve SNAPs were recorded from little fingers, at 12 cm from recording electrode. Sural nerve SNAPs were recorded at the lateral malleolus, and stimulation was delivered 14 cm proximally. On the basis of neurological assessment of diabetic patients and their abnormal NCS findings (that exceeding ±2 SD of mean control values), these patients were classified into two subgroups after fulfilling case definition below.

Confirmed clinical diabetic peripheral polyneuropathy (n=40) was defined as the presence of symptoms and signs consistent with distal symmetrical peripheral polyneuropathy and NCS abnormalities in more attribute(s) in at least two anatomically distinct nerves [27].

Subclinical diabetic peripheral neuropathy (n=28) was confirmed with abnormal NCS findings that were consistent with distal symmetrical polyperipheral neuropathy with absent diagnostic symptoms or signs on neurological assessment.


This study was conducted after approval of the Ethical Committee of Faculty Medicine, Assiut University.

Statistical analysis

Statistical analysis was performed using SPSS (16.0 for Windows; SPSS Inc., Chicago, Illinois, USA). The reference limits from the control group were derived from the mean±2 SD. The data exceeding the reference limits were considered to be ‘outside reference data’. The diabetic group was classified into two subgroups: abnormal versus normal ABR and clinical versus subclinical diabetic neuropathy. Comparative statistical analysis was performed between study groups and between diabetic subgroups. Categorical variables were compared using the χ2-test. Continuous variables within two groups were compared using the independent t-test for parametric data and the Mann–Whitney U-test for nonparametric data, respectively. Spearman’s correlation was performed between ABR and NCSs as well as metabolic profile. Significance was set at P less than 0.05 (two-tailed).

  Results Top

No statistically significant difference was found between demographic and clinical data of study groups, as illustrated in [Table 1].
Table 1 Demographic and clinical data of study groups

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In audiometry study, speech discrimination scores were excellent in all participants. Moreover, normal middle ear functions and acoustic reflex thresholds were evident in all.

Overall, absolute latency of ABR waves and IPLs were significantly longer in the diabetic group compared with the control group (P=0.0001). The highest frequency of abnormality was recorded in absolute latency of waves III and V and IPL III–V. Moreover, this significant difference was also found between values of diabetic patients with abnormal (n=26) versus normal ABR (n=42) response (subgroup I vs. II) (P<0.01), as illustrated in [Table 2].
Table 2 Auditory brainstem response values in the study group and diabetic subgroups

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NCSs were performed for all participants and revealed significant differences in all NCS parameters between diabetic compared with control values (P<0.001). All diabetic patients had either clinical or subclinical diabetic peripheral polyneuropathy (n=40 and 28, respectively). A significant difference was found between NCS parameters of diabetic patients either with abnormal or normal ABR response subgroup versus the control group (P=0.0001 for all).

The main significant differences between NCS parameters among diabetic subgroups (I vs. II) were found in sural sensory conduction velocity (SCV), MCV of the ulnar nerve, and F-wave latency of all nerves studies (P<0.01 and <0.05) ([Table 3]).
Table 3 Nerve conduction study parameters among diabetic patients with abnormal versus normal auditory brainstem response and the control group

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The relationship between auditory nerve pathway changes (IPLs) and NCS parameters was estimated using Spearman’s correlation. Significant inverse correlations were found between IPLs I–III, I–V, and measured conduction velocities not latencies, and a positive correlation was found with the F-wave and H-reflexes ([Table 4]).
Table 4 Correlation between interpeak latencies in auditory brainstem response and nerve conduction study findings

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Serum HbA1c% and lipid profile were significantly higher in diabetic patients with abnormal than in those with normal ABR response and also in clinical versus subclinical diabetic polyneuropathy, with P=0.0001 for both comparisons ([Table 5]).
Table 5 Metabolic profile among diabetic subgroups

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Spearman’s correlation was performed between all participant values to confirm the relationship between metabolic profile and IPLs of ABR as well as conduction velocity (CV) of nerve studies.

[Figure 1] and [Figure 2] showed a significant correlation between metabolic profile and IPL III–V as well as sural CV. HbA1c% was significantly correlated with IPL III–V (r=0.447, P=0.000) and sural CV (r=−0.427 and P=0.000) ([Figure 1]a and [Figure 2]a). Moreover, serum cholesterol and triglyceride levels were significantly correlated with IPL III–V (r=0.314, P=0.002; r=0.296, P=0.004, [Figure 1]b and [Figure 1]c, respectively) and sural CV (r=−0.312, P=0.001; r=−0.316, P=0.001, [Figure 2]b and [Figure 2]c, respectively).
Figure 1 The effect of metabolic profile on interpeak latency (IPL) III–V in auditory brainstem response (ABR) using Spearman’s correlation for statistical analysis. IPL III–V was significantly positively correlated with (A) serum glycated hemoglobin (HbA1c%) (r=0.447, P=0.000), (B) serum cholesterol (r=0.314, P=0.002), and (C) triglyceride (r=0.296, P=0.004).

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Figure 2 The effect of metabolic profile on sural conduction velocity (CV) using Spearman’s correlation for statistical analysis. Sural CV was significantly negatively correlated with (A) glycated hemoglobin (HbA1c%) (r=−0.427, P=0.000), (B) serum cholesterol (r=−0.312, P=0.001), and (C) triglyceride (r=−0.316, P=0.001).

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As regards other IPLs, IPL I–V was significantly correlated with HbA1c% (r=0.226, P=0.022) and serum level of cholesterol and triglyceride (r=0.232, P=0.026; r=0.120, P=0.251, respectively). However, no significant correlation (P>0.05) was found between these metabolic parameters and IPL I–III (r=0.065 for HbA1c%; r=0.081 and 0.122 for serum cholesterol and triglyceride, respectively).

As regards other nerve studies, the metabolic parameters had a significant negative correlation with SCV of the median and ulnar nerves and MCV of CPN (P=0.0001) for all and a less significant correlation (P<0.01) for serum HbA1c% and cholesterol levels with MCV of the median and ulnar nerves.

Moreover, serum HbA1c% was significantly positively correlated with serum level of cholesterol and triglyceride (r=0.631 and 0.615, respectively; P=0.0001 for both).

  Discussion Top

Our results point out to the evident affection of the nervous system of diabetic patients in the form of diabetic neuropathy, affecting the peripheral as well as the central nervous system (CNS). Both are common complications of this metabolic disorder. Subclinical acoustic neuropathic affection of the CNS pathway was recorded as prolonged absolute latencies of wave I with consecutive delay in absolute latency of waves III and V in ABR study among the diabetic group of patients. These data are consistent with the recorded data of central (acoustic) neuropathy in previous studies on diabetic patients [9],[15],[19].

The significant difference in IPLs between diabetic patients and controls is partially consistent with the observations of many studies [20],[28],[29]. Baweja et al. [20] observed that IPL I–V was significantly delayed bilaterally, whereas the IPL I–III was significantly delayed unilaterally, in female patients with type II DM. However, Huang et al. [28] and Al-Azzawi and Mirza [29] found a significant delay in IPLs I–III and I–V but not IPL III–V among diabetic patients versus the nondiabetic group. This indicates that retrocochlear lower and upper brainstem dysfunction in diabetic patients is associated with mainly delayed central rather than peripheral conduction time of the auditory nerve pathway. They postulated dual pathogenesis of the above findings and suggested that silent lacunar infarct and metabolic disturbance of the brain could be proposed in the form of diabetic angiopathy that could induce cranial (acoustic) neuropathy or brainstem dysfunction, as previously reported by Kurita et al. [30]. Our finding of the correlation of hyperlipidemia with the HbA1c% could point to the possibility that the associated dyslipidemia could be a factor in the pathogenesis of central as well as peripheral nervous affection in diabetics.

In the present study, significant differences were recorded in terms of NCS parameters both between the diabetic group or the diabetic subgroup (I or II) and the control group as well as between diabetic patients with abnormal and those without normal ABR response ([Table 3]). Our findings are consistent with the reported data in previous studies [31],[32]. However, Goldsher et al. [31] reported abnormal brainstem response in type II diabetic patients with neuropathy in 94% of cases. In contrast, Siddiqi et al. [32] found that 52% of type II DM patients had diabetic neuropathy, 92% of whom showed abnormal BAEP, and only 50% of nonneuropathic patients showed abnormal BAEP. These recording data indicate that delay in absolute wave latencies and IPLs by BAEP demonstrates defect at the level of brainstem and midbrain in long-standing type II DM patients on one hand and neuropathy being more pronounced among diabetic patients with abnormal ABR response than in those with normal ABR response on the other hand. Overall, the mentioned data are consistent with previously reported data that stated that the most common complication of diabetes is peripheral neuropathy, occurring in ∼60% of all diabetic patients [33],[34].

Significant inverse correlations were found between IPLs I–III, I–V, and CV of all studied nerves, predominantly in lower limbs, and F-wave studies ([Table 4]). These data are consistent with the study by Huang et al. [28], who found that the best correlation was between IPL I–III and MCV in tibial followed by median and sural CV studies. These findings could be explained by ‘low NCS velocity in DM, which was more significantly found in lower limb than in upper limb nerve studies because of length-dependent diabetic polyneuropathy’. However, other studies showed the correlation between BAEP findings and SCV of the median nerve and MCV of CPN [16],[35]. Moreover, the recorded significant correlation between IPL I–III, IPL I–V, and NCS parameters could point to the possibility that diabetic acoustic neuropathy that manifested with central ABR changes could occur parallel to peripheral neuropathy, as previously reported [18],[36]. A recent study also reported that a trend toward an association between evidence of wave IV and the presence of somatic neuropathy or abnormal cardiovascular autonomic tests was observed among patients with type I DM [37]. Overall, these reported findings may suggest early damage of small nerve fibers within the auditory pathway at the pons and midbrain level, lateral lemniscuses, and inferior colliculi, which is in line with evidence that small nerve fibers may be affected first in diabetic neuropathy [38]. However, this difference in recorded data of different studies could be related to the wide spectrum of the disease.

These patients had a significantly higher serum level of HbA1c% and hyperlipidemia, either among diabetic patients with abnormal ABR response or clinical diabetic neuropathy. Confirming these recorded associations, serum HbA1c% level had a significant positive correlation with IPL III–V and the reverse (negative correlation) with CV studies. This significant association between HbA1c% serum level and CV nerve studies are consistent with the findings of Huang et al. [39], who reported a significant reduction of CV in poor glycemic control type II DM. Our correlating ABR results with serum level of HbA1c% are consistent with previously reported data [24],[40], but it is inconsistent with other studies [19],[25] that found no relation between serum HbA1c% and ABR results. These recorded data suggest that poor glycemic control could enhance related metabolic changes and angiopathy either on peripheral nerves and/or acoustic nerve as well as auditory nerve pathway and brainstem functions. It could affect normal nerve functions and accelerate neuropathy, either peripheral or central [41],[42],[43]. The predominant significant correlation with IPL III–V but not IPL I–III values may be attributed to brainstem neurons being more vulnerable to these metabolic disturbances and ischemic changes.

In the present study, diabetic patients who either showed ABR changes or clinical neuropathy had concurrent significant hyperlipidemia compared with the other subgroup. Furthermore, the recorded significant correlation between lipid profile and IPL III–V as well as SCV of the sural nerve, confirms the harmful effect of serum cholesterol and triglyceride either on peripheral nerves as well as the central neural transmission in the auditory nerve pathway. These results are consistent with reporting data of case–control study evaluating patients suffering from hypercholesterolemia and hypertriglyceridemia [44]. Namysłowski et al. [44] reported prolonged latencies of the III and V waves, as well as IPLs I–III and III–V, in patients with hyperlipidemia compared with the control group. The hearing affection among these patients could be explained by the postulated microvascular complications. In addition, it is consistent with previously reported data in ABR study by Ben-David et al. [45]. However, they found subclinical impairments of brainstem function in hyperlipidemic patients compared with normolipemic patients, probably due to ischemia accelerated by their condition. Previous histopathological studies have shown damaged nerves and vessels of the inner ear of the individuals with diabetes and hyperlipidemia, which have been theorized to be an important causative factor for neuronal degeneration in the auditory system [46],[47]. The possible mechanism is that hypercholesterolemia induces phenotypic changes in the microcirculation, which are consistent with oxidative and nitrosative stresses. The superoxides that are generated participate in a number of reactions, yielding various free radicals. This leads to platelet activation and lipid peroxidation, which is involved in the initiation and the progression of the atherosclerotic lesions [48]. Hyperlipidemia also had a harmful effect for progression of peripheral and autonomic diabetic neuropathy as previously mentioned [49],[50].

Finally, the correlation between serum levels of HbA1c% and lipid profile confirms the role of poor glycemic control and concurrent hyperlipidemia in rapid development of diabetic neuropathy in type II DM, as previously reported [23],[51]. Both act with synergistic action to induce the following: (i) metabolic disturbances and inflammatory process of oxidative stress that lead to peripheral nerve as well as auditory nerve pathway damage, and (ii) vascular changes in microcirculation and small blood vessels in peripheral nerves and inner ear structures associated with angiopathy leading to peripheral or central neuropathy on one hand and brainstem dysfunction on the other hand.

  Conclusion Top

ABR changes are subclinical and common among type II DM, indicating peripheral and central conduction impairment in auditory nerve pathway. Therefore, early screening of these patients by means of ABR as a noninvasive procedure to detect early impairment of acoustic nerve and CNS pathway involvement, even in the absence of specific symptom, is highly recommended. These ABR changes occur parallel to central as well as peripheral neuropathy, and are associated with poor glycemic control as well as hyperlipidemia in type II DM. Thus, early estimation of metabolic profile and control of hyperlipidemia are mandatory in DM management to ameliorate vascular complication and progression of diabetic peripheral and central neuropathy as well as brainstem dysfunctions.

  Acknowledgements Top

The authors thank Professor Dr Eman Khedr for her valuable comments. N.M.A. contributed to study concept and design, acquisition of data, draft and revision of the report, statistical analyses, and interpretation of data. E.S.M., L.M.T., R.M.G., A.M.G., M.R.A.E.R., M.A.E., and M.E.E.E. contributed to case recruitments, acquisition of data and statistical analyses and interpretation of data. All contributed to editing and revision of this report.

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Conflicts of interest

There are no conflicts of interest.

  References Top

Giniş Z, Öztürk G, Sırmalı R, Yalçındağ A, Dülgeroğlu Y, Delibaşı T et al. The role of HbA1c as a screening and diagnostic test for diabetes mellitus in Ankara. Turk J Med Sci 2012; 42(Suppl 2):1430–1436.  Back to cited text no. 1
Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for2013 and projections for 2035. Diabetes Res Clin Pract 2014; 103:137–149.  Back to cited text no. 2
Maia CA, Campos CA. Diabetes mellitus as etiological factor of hearing loss. Braz J Otorhinolaryngol 2005; 71:208–214.  Back to cited text no. 3
Jali MV, Kambar S, Jali SM, Gowda S. Familial early onset of type-2 diabetes mellitus and its complications. N Am J Med Sci 2009; 1:377–380.  Back to cited text no. 4
Biessels GJ, Cristino NA, Rutten GJ, Hamers FP, Erkelens DW, Gispen WH. Neurophysiological changes in the central and peripheral nervous system of streptozotocin-diabetic rats. Course of development and effects of insulin treatment. Brain 1999; 122(Pt 4):757–768.  Back to cited text no. 5
Irkeç C, Nazliel B, Yetkin I, Koçer B. Facial nerve conduction in diabetic neuropathy. Acta Neurol Belg 2001; 101:177–179.  Back to cited text no. 6
Kazem SS, Behzad D. Role of blink reflex in diagnosis of subclinical cranial neuropathy in diabetic mellitus type II. Am J Phys Med Rehabil. 2006; 85:449–452.  Back to cited text no. 7
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; 43:29–33.  Back to cited text no. 8
Uzun N, Uluduz D, Mikla S, Aydin A. Evaluation of asymptomatic central neuropathy in type I diabetes mellitus. Electromyogr Clin Neurophysiol 2006; 46:131–137.  Back to cited text no. 9
Aminoff M. Electrodiagnosis in Clinical Neurology. In: Daube JR, editor. 4th ed. Philadelphia, PA: Churchill Livingstone; 1999. 421–435, 451–479.  Back to cited text no. 10
De España R, Biurrun O, Lorente J, Traserra J. Hearing and diabetes. ORL J Otorhinolaryngol Relat Spec 1995; 57:325–327.  Back to cited text no. 11
Ravecca F, Berrettini S, Bruschini L, Segnini G, Sellari-Franceschini S. Progressive sensorineural hearing loss: metabolic, hormonal and vascular etiology. Acta Otorhinolaryngol Ital 1998; 18(Suppl 59):42–50.  Back to cited text no. 12
Dalton DS, Cruickshanks KJ, Klein R, Klein BE, Wiley TL. Association of NIDDM and hearing loss. Diabetes Care 1998; 21:1540–1544.  Back to cited text no. 13
Obrebowski A, Pruszewicz A, Gawliński M, Swidziński P. Electrophysiological hearing examination in children and teenagers with insulin-dependent diabetes mellitus. Otolaryngol Pol 1999; 53:595–598.  Back to cited text no. 14
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; 5:60–65.  Back to cited text no. 15
Pan CH, Chen TJ, Chen SS. Brainstem auditory evoked potentials in diabetes mellitus. Zhonghua Yi Xue Za Zhi (Taipei) 1992; 49:244–252.  Back to cited text no. 16
Dolu H, Ulas UH, Bolu E, Ozkardes A, Odabasi Z, Ozata M, Vural O. Evaluation of central neuropathy in type II diabetes mellitus by multimodal evoked potentials. Acta Neurol Belg 2003; 103:206–211.  Back to cited text no. 17
Tóth F, Várkonyi TT, Rovó L, Lengyel C, Légrády P, Jóri J et al. Investigation of auditory brainstem function in diabetic patients. Int Tinnitus J 2003; 9:84–86.  Back to cited text no. 18
Díaz deLeón-Morales LV, Jáuregui-Renaud K, Garay-Sevilla ME, Hernández-Prado J, Malacara-Hernández JM. Auditory impairment in patients with type 2 diabetes mellitus. Arch Med Res 2005; 36:507–510.  Back to cited text no. 19
Baweja P, Gupta S, Mittal S, Kumar A, Singh KD, Sharma R. Changes in brainstem auditory evoked potentials among North Indian females with Type 2 diabetes mellitus. Indian J Endocrinol Metab 2013; 17;1018–1023  Back to cited text no. 20
Chrisholm DJ. The Diabetes Control and Complications Trial (DCCT). A milestone in diabetes management. Med J Aust 1993; 159:721–723.  Back to cited text no. 21
Azad N, Emanuele NV, Abraira C, Henderson WG, Colwell J, Levin SR et al. The effects of intensive glycemic control on neuropathy in the VA cooperative study on type II diabetes mellitus (VA CSDM). J Diabetes Complications 1999; 13:307–313.  Back to cited text no. 22
Wiggin TD, Sullivan KA, Pop-Busui R, Amato A, Sima AA, Feldman EL. Elevated triglycerides correlate with progression of diabetic neuropathy. Diabetes 2009; 58:1634–1640.  Back to cited text no. 23
Seidl R, Birnbacher R, Hauser E, Bernert G, Freilinger M, Schober E. Brainstem auditory evoked potentials and visually evoked potentials in young patients with IDDM. Diabetes Care 1996; 19:1220–1224.  Back to cited text no. 24
Talebi M, Moosavi M, Mohamadzade NA, Mogadam R. Study on brainstem auditory evoked potentials in diabetes mellitus. Neurosciences (Riyadh) 2008; 13:370–373.  Back to cited text no. 25
Andersen H, Stålberg E, Falck B. F-wave latency, the most sensitive nerve conduction parameter in patients with diabetes mellitus. Muscle Nerve 1997; 20:1296–1302.  Back to cited text no. 26
Albers JW, Herman WH, Pop-Busui R, Feldman EL, Martin CL, Cleary PA et al. Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. Effect of prior intensive insulin treatment during the Diabetes Control and Complications Trial (DCCT) on peripheral neuropathy in type 1 diabetes during the Epidemiology of Diabetes Interventions and Complications (EDIC) Study. Diabetes Care 2010; 33:1090–1096.  Back to cited text no. 27
Huang CR, Lu CH, Chang HW, Tsai NW, Chang WN. Brainstem auditory evoked potentials study in patients with diabetes mellitus. Acta Neurol Taiwan 2010; 19:33–40.  Back to cited text no. 28
Al-Azzawi LM, Mirza KB. The usefulness of the brainstem auditory evoked potential in the early diagnosis of cranial nerve neuropathy associated with diabetes mellitus. Electromyogr Clin Neurophysiol 2004; 44:387–394.  Back to cited text no. 29
Kurita A, Mochio S, Isogai Y. Changes in auditory P300 event-related potentials and brainstem evoked potentials in diabetes mellitus. Acta Neurol Scand 1995; 92:319–323.  Back to cited text no. 30
Goldsher M, Pratt H, Hassan A, Shenhav R, Eliachar I, Kanter Y. Auditory brainstem evoked potentials in insulin-dependent diabetics with and without peripheral neuropathy. Acta Otolaryngol 1986; 102:204–208.  Back to cited text no. 31
Siddiqi SS, Gupta R, Aslam M, Hasan SA, Khan SA. Type-2 diabetes mellitus and auditory brainstem response. Indian J Endocrinol Metab 2013; 17:1073–1077.  Back to cited text no. 32
Edwards JL, Vincent AM, Cheng HT, Feldman EL. Diabetic neuropathy: mechanisms to management. Pharmacol Ther 2008; 120:1–34.  Back to cited text no. 33
Feldman EL. Diabetic neuropathy. Curr Drug Targets 2008; 9:1–2.  Back to cited text no. 34
Martini A, Comacchio F, Fedele D, Crepaldi G, Sala O. Auditory brainstem evoked responses in the clinical evaluation and follow-up of insulin-dependent diabetic subjects. Acta Otolaryngol 1987; 103:620–627.  Back to cited text no. 35
Ottaviani F, Dozio N, Neglia CB, Riccio S, Scavini M. Absence of otoacoustic emissions in insulin-dependent diabetic patients: is there evidence for diabetic cochleopathy? J Diabetes Complications 2002; 16:338–343.  Back to cited text no. 36
Lasagni A, Giordano P, Lacilla M, Raviolo A, Trento M, Camussi E et al. Cochlear, auditory brainstem responses in type 1 diabetes: relationship with metabolic variables and diabetic complications. Diabet Med 2015; doi: 10.1111/dme.13039. [Epub ahead of print]. PMID: 26605750  Back to cited text no. 37
Várkonyi TT, Börcsök E, Tóth F, Fülöp Z, Takács R, Rovó L et al. Severity of autonomic and sensory neuropathy and the impairment of visual- and auditory-evoked potentials in type 1 diabetes: is there a relationship? Diabetes Care 2006; 29:2325–2326.  Back to cited text no. 38
Huang CC, Chen TW, Weng MC, Lee CL, Tseng HC, Huang MH. Effect of glycemic control on electrophysiologic changes of diabetic neuropathy in type 2 diabetic patients. Kaohsiung J Med Sci, 2005; 21:15–21  Back to cited text no. 39
Abo-Elfetoh NM, Mohamed ES, Tag LM, El-Baz MA, Ez Eldeen ME. Auditory dysfunction in patients with type 2 diabetes mellitus with poor versus good glycemic control. Egypt J Otolaryngol 2015; 31:162–169.  Back to cited text no. 40
  Medknow Journal  
Greene DA, Lattimer SA, Sima AAF. Are disturbance of sorbitol, phosphoinositide, and Na+/K+-ATPase regulation involved in pathogenesis of diabetic neuropathy? Diabetes 1988; 37:688–693.  Back to cited text no. 41
Peppa M, Vlassara H. Advanced glycation end products and diabetic complications: a general overview. Hormones (Athens) 2005; 4:28–37.  Back to cited text no. 42
Said G. Diabetic neuropathy − a review. Nat Clin Pract Neurol 2007; 3:331–340.  Back to cited text no. 43
Namysłowski G, Trybalska G, Scierski W, Mrówka-Kata K, Bilińska-Pietraszek E, Kawecki D. Hearing evaluation in patients suffering from hypercholesterolemia. Otolaryngol Pol 2003; 57:725–730.  Back to cited text no. 44
Ben-David Y, Pratt H, Landman L, Fradis M, Podoshin L, Yeshurun D. A comparison of auditory brain stem evoked potentials in hyperlipidemics and normolipemic subjects. Laryngoscope 1986; 96:186–189.  Back to cited text no. 45
Jorgenson MB, Buch NH. Studies on the inner ear function and cranial nerves in diabetics. Arch Otolaryngol 1961; 74:373–381.  Back to cited text no. 46
Chapman T, Mcqueen Baxter A, Smith TL, Raynor E, Yoon SM et al. Non-insulin − dependent diabetic micro angiopathy in the inner ear. J Laryngol Otol 1999; 113:13–18.  Back to cited text no. 47
Ferroni P, Basili S, Falco A, Davì G. Oxidant stress and platelet activation in hypercholesterolemia. Antioxid Redox Signal 2004; 6:747–756.  Back to cited text no. 48
Kempler P, Tesfaye S, Chaturvedi N, Stevens LK, Webb DJ, Eaton S et al. Autonomic neuropathy is associated with increased cardiovascular risk factors: the EURODIAB IDDM Complications Study. Diabet Med 2002; 19:900–909.  Back to cited text no. 49
Tesfaye S, Chaturvedi N, Eaton SE, Ward JD, Manes C, Ionescu-Tirgoviste C et al. Vascular risk factors and diabetic neuropathy. N Engl J Med 2005; 352:341–350.  Back to cited text no. 50
Meyer C, Milat F, McGrath BP, Cameron J, Kotsopoulos D, Teede HJ. Vascular dysfunction and autonomic neuropathy in type 2 diabetes. Diabet Med 2004; 21:746–751.  Back to cited text no. 51


  [Figure 1], [Figure 2]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


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