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Audiology - Communication Research

On-line version ISSN 2317-6431

Audiol., Commun. Res. vol.18 no.4 São Paulo Oct./Dec. 2013

http://dx.doi.org/10.1590/S2317-64312013000400005 

ORIGINAL ARTICLE

 

Hearing changes associated to complications and comorbidities in type 2 Diabetes Mellitus

 

 

Juliana Mota FerreiraI; Marília Fontenele e Silva CâmaraII; Paulo César de AlmeidaIII; José Brandão NetoIV; Carlos Antonio Bruno da SilvaII

IPost-graduation Program (Doctorade) in Health Sciences, Universidade Federal do Rio Grande do Norte – UFRN – Natal (RN), Brazil
IIUniversidade de Fortaleza – UNIFOR – Fortaleza (CE), Brazil
IIIUniversidade Estadual do Ceará – UECE – Fortaleza (CE), Brazil
IVUniversidade Federal do Rio Grande do Norte – UFRN – Natal (RN), Brazil

Correspondence address

 

 


ABSTRACT

PURPOSE: To investigate the presence of hearing impairment, represented by a decreased audiometric threshold and/ or absence of otoacoustic emissions, associated with general characteristics, chronic complications and comorbidities in patients with type 2 diabetes.
METHODS: The study was carried out a secondary care unit in Fortaleza, from April to July 2010, using a sample of 152 patients aged 36 to 60 with type 2 diabetes. The clinical data related to diabetes was analyzed and an audiological evaluation consisting of pure tone audiometry, otoacoustic emissions elicited by transient stimuli and distortion.
RESULTS: The female gender predominated, with 95 (62.5%) patients. The mean age was 53.4 years. Sensorineural hearing loss was found in 96 (63.2%) patients, mainly cochlear loss (83.3%). 114 patients (75%) had an absence of transient emissions, and 120 (78.9%), had an absence of distortion product emissions. Diabetic men had a 4.4 times greater chance of hearing loss than women. The longer the disease time the greater the chance of hearing loss. Diabetic patients over 50 years old were also more likely to have hearing loss.
CONCLUSION: Of the comorbidities and complications associated with diabetes, overweight/obesity was a risk factor for auditory alterations and is associated with hearing loss and the absence of transient emissions. Overweight/obese diabetic patients were 3 times more likely to have impaired audiometry and otoacoustic emissions.

Keywords: Diabetes Mellitus type 2; Comorbidity, Diabetes complications; Hearing; Audiometry


 

 

INTRODUCTION

Diabetes Mellitus (DM) is a syndrome of multiple etiologies characterized by hyperglycemia and marked by the appearance of chronic complications, classified as: microangiopathic - diabetic retinopathy and diabetic nephropathy; macroangiopathic - coronary artery disease, cerebrovascular disease and peripheral vascular neuropathic - diabetic neuropathy(1).

Other important factors in the study of DM and its complications are the duration of the disease and its control, which interacts with other risk factors, called comorbidities, such as arterial hypertension, dyslipidemia and obesity, determining the course of microangiopathy and macroangiopathic(1).

All these chronic complications and comorbidities associated with DM are known and have been studied, however, some less obvious changes may occur in this population, as is the case of hearing loss.

Considering that the anatomic-physiological changes resulting from the hyperglycemic process have the potential to injure blood vessels and nerves, it is believed that the organs responsible for hearing can also be affected by DM(2).

In chronic DM complications may include the eyes, kidney, cranial nerves, peripheral nerves, ears, etc. In the hearing system specifically, there may be atrophy of the spiral ganglion, degeneration of the myelin sheath of the eighth cranial nerve, reduction of the number of nerve fibers in the spiral lamina, or thickening of the capillary walls of the vascular stria and small arteries in the ear canal(3). In histological tests, injuries of the inner ear are found in 50% of people diagnosed with Diabetes Mellitus(4).

The development of research in order to define the association between diabetes and hearing impairment may assist in the prevention and/or early identification of hearing loss, as well as raising the awareness of health professionals about the referrals required, and showing the importance of the inclusion of specific hearing tests as part of the routine care of this population.

Given the context, this study investigated the presence of alterations in hearing, represented by decreases in the audiometric threshold and/ or the absence of otoacoustic emissions, associated with the general characteristics, chronic complications and comorbidities in patients with type 2 DM.

 

METHODS

A prospective, cross-sectional, analytical study with a quantitative approach, performed in a secondary health unit for the care of diabetes, in Fortaleza, during the period of April to July 2010. The sample was composed of 152 patients with type 2 DM, selected at random, regardless of gender, aged between 36 and 60 years.

Of 152 patients, 57 (37.5%) were male and 95 (62.5%) were female. The average age was 53.4 years (SD=6.02). The 51-60 age group predominated, with 109 (71.7%) of the patients evaluated; 43 (28.3%) were included in the 36-50 age group.

Patients were excluded from the study due to the following conditions: (a) an altered meatoscopy during the evaluation, with ear wax or secretions that prevented a complete visualization of the ear canal, (b) a history of middle ear infections, (c) other risk factors for hearing loss, such as noise exposure and exposure to ototoxic chemicals, (d) severe head injury, (f) self-reported history of infectious diseases, such as mumps, measles and meningitis (g) radiotherapy in the region of the head and neck and chemotherapy; (h) family history of hearing loss.

Individuals who, at the time of the research, had an altered audiometry evaluation of conductive and/or mixed type were also excluded. This criterion was used because of the absence of immittance evaluation.

Diabetic patients older than 60 years were also excluded from the study, seeking thereby to restrict cases of the natural aging of hearing (presbycusis) in the selected sample. This age was used as the cutoff point as most studies on presbycusis consider individuals aged 60 and above.

The variables studied were related to the demographic profile (gender and age), the clinical data related to DM (time since diagnosis, level of glycemic control, ototoxic drugs used in the treatment of the disease and the associated complications and comorbidities) and audiological evaluation data (presence/absence of hearing impairment).

The instruments used for data collection were audiological history and the medical notes available at the unit.

The occurrence of chronic complications and comorbidities was verified using the results of the clinical tests from medical records and information given by patients. These variables were divided into two categories: present (yes) or absent (no), based on the criteria described below.

For the assessment of glycemic control the value of the blood glucose tests was used, considering the values of the last three glucose tests and compared to the rate of postprandial glucose (<140 mg/dl)(5). For arterial hypertension normal values were considered to be below 130/85 mmHg(6). The analysis of dyslipidemia considered that the target lipid profile for the adult diabetic population consists of total cholesterol <200 mg/dl, LDL-C <100 mg/dl, HDL-C> 45 mg/dl and triglycerides <150 mg/dl(7). The analysis of the body mass index (BMI) used the following values: normal weight, BMI <25 kg/mII; and overweight/ obesity, BMI ≥ 25kg/m2(8).

The analysis of chronic microvascular complications followed the following criteria: retinopathy determined by the result of an examination of the fundus of the ear and retinal biomicroscopy(7); nephropathy was considered present when the values of microalbuminuria were greater than 30 mg(1).

A history of cardiovascular, cerebrovascular or peripheral vascular disease was determined from the patient's history, as described in the medical records. In this study, all information obtained related to cardiac and vascular changes was grouped and named cardiovascular changes, including: Cerebral Vascular Accident (CVA), cardiac arrhythmia, angina and acute myocardial infarction.

Neuropathy was considered to be positive in the presence of pain, tingling, numbness and/ or a burning sensation in the lower limbs and the presence of amputation(1).

The auditory characteristics were defined through an audiological assessment, comprised of a meatotoscopy, pure tone audiometry (PTA), otoacoustic emissions (TEOAE) and product otoacoustic emissions (DPOAE). The following instruments were used: A Heine® mini 2000 otoscope; Vibrasom® AVS 500 audiometer; and OAE Vivosonic® 200DPS live, properly calibrated. The evaluations were performed in a Redusom® audiometric booth.

In the ATL, the thresholds for airways were investigated at frequencies from 0.25 kHz to 8 kHz and for bone conduction at frequencies of 0.5 kHz to 4 kHz, considering normal hearing thresholds as being up to 25 dBNA on all frequencies and in both ears(9).

TEOAE tests were performed with click stimulus at an intensity of 84 dB peSPL at frequencies of 1, 2, 3 and 4 kHz, considered present when the general reproducibility was at least 50% and the signal to noise ratio was greater than or equal to 3 dB for all frequencies and for both ears(10,11).

The DPOAE tests used two pure tones of different frequencies, done simultaneously (F1 and F2, F2/F1 ratio = 1.22), with intensities of F1 and F2, respectively, 65 dB SPL (L1) and 55 dB SPL (L2). The frequencies of 1, 1.5, 2, 2.5, 3, 3.2, 3.5, 4, 4.5, 5, 5.5, 6, 7 and 8 kHz were analyzed, considering DPOAE present when the response was positive with negative noise and the signal to noise ratio was greater than or equal to 6 dB for all frequencies and both ears(10,11).

The criteria for EOA assessment was rigorous from a clinical point of view, considering as present only those reviews where all frequencies met the standard of normality adopted. This stance is justified due to the study's focus on diagnostic evaluation and not just screening hearing, which adopts less stringent standards. Thus, the objective was to identify any minor changes that were possibly related to DM.

For altered ATL the term "hearing loss" was used. Altered EOA was referred to as "absence of EOA." Any deviation from the standard considered normal in all the tests carried out was generally called "hearing impairment".

The audiological diagnosis was determined by considering the results of the tests performed. Accordingly, the following names were adopted: normal hearing - all tests normal; cochlear loss - audiometry with sensorineural hearing loss and no emissions; cochlear dysfunction - normal audiometry with no emissions; retrocochlear alteration - audiometry with sensorineural hearing loss and the presence of emissions.

The study was approved by the Ethics Committee of the University of Fortaleza (UNIFOR) and registered under the norm n°. 384/08. All the individuals signed a consent form stating their knowledge of the research objectives and giving their consent to participate.

The data were presented as numbers and proportions. To verify the association between the variables the chi-square test, the calculation of odds ratios, confidence intervals and logistic regression were used. For the multivariate analysis (logistic regression) all variables with p<0.20 were included. In all the tests, the significance level was set at 5%.

The data was analyzed using SPSS (Statistical Package for the Social Sciences - SPSS, version 15.0).

 

RESULTS

The average time since the diagnosis of DM was 11.2 years (SD=6.3), with 97 (64.2%) patients diagnosed for between 1 and 12 years, and 54 (35.8%) patients diagnosed for between 13 and 33 years. The analysis of blood glucose levels showed that 124 (83.8%) patients had higher than expected blood glucose levels. The use of ototoxic medications, such as diuretics and salicylates for the treatment of diabetes and/or associated diseases was reported in 51 (34.5%) patients.

For the study of comorbidities and complications associated with DM, the number of subjects evaluated (n) was diverse, depending on the variable being analyzed, due to the lack of data on some subjects at the time of the survey.

The comorbidities were distributed as follows: 119 (79.3%) patients with hypertension, 115 (86.5%) with dyslipidemia and 106 (77.9%) overweight/ obesity. Regarding complications, it was observed that 101 (73.7%) patients had neuropathy, 34 (28.2%) retinopathy, 59 (50.9%) nephropathy, 37 (26.4%), heart disease and 13 (8.6%) diabetes related amputations (Table 1).

 

 

Audiological evaluation

The analysis of the audiological evaluation indicated hearing loss in 96 (63.2%) patients; all sensorineural. For otoacoustic emissions, an absence of TEOAE responses was observed in 114 (75%) patients and for DPOAE in 120 (78.9%) patients.

The joint analysis of the tests for determining an audiological diagnosis revealed that 15 (26.8%) patients had normal hearing. Of the patients with hearing loss, 80 (83.3%) had cochlear loss and 2 (2.1%) patients suffered from retrocochlear alteration. Of the patients with normal audiometry, 41 (73.2%) had cochlear dysfunction, of whom 19 (33.9%) had an absence of the two types of emissions and 22 (39.3%) had an absence of one of the types (Table 2).

ATL

The analysis of the variables related to ATL, showed that the following are not risk factors for hearing loss (p≥ 0.05): glycemic control, hypertension, dyslipidemia, neuropathy, nephropathy, retinopathy, and cardiovascular disorders (Table 3).

Regarding gender, it was observed that men were 4.4 times more likely to have hearing loss than women. The 51-60 age group had a 2.6 times greater risk of hearing loss compared to those aged 36-50 (Table 3).

The duration of the illness was also considered a risk factor for hearing loss, noting that patients with a longer diagnosis had a 2.1 times greater risk of hearing loss than those who had DM for less than 13 years (Table 3).

Patients who used ototoxic drugs were 2.1 times more likely to have hearing loss than those who were not exposed to this factor (Table 3).

Pertaining to comorbidities and complications, only the variables of overweight/obesity and amputation constituted risk factors for hearing loss. Overweight or obese patients were 3.3 times more at risk than patients with a normal weight. Those who had amputations were 7.8 times more likely to suffer from hearing loss (Table 3).

After the logistic regression analysis it was observed that the variables of gender (p<0.001), age (p=0.007) and overweight/obesity (p=0.003) remained statistically significant (p<0.05), establishing a positive association with hearing loss (Table 3).

TEOAE

Regarding the absence of TEOAE responses, the following variables did not constitute risk factors (p≥0.05): age, disease duration, glycemic control, ototoxic drugs, arterial hypertension, dyslipidemia, neuropathy, nephropathy, retinopathy, cardiovascular disorders and amputations (Table 4).

Only the following were considered significant variables: gender - showing that men were 3.4 times more likely than women to lack TEOAE - and overweight/ obesity - with overweight patients presenting 3.5 times more risk than patients with normal weight (Table 4).

After the logistic regression analysis it was observed that the variables gender (p=0.008) and overweight/ obesity (p=0.01) remained significant (p<0.05), noting their association with the absence of TEOAE.

DPOAE

The analysis of DPOAE showed that the following variables were not risk factors for a lack of response: age, glycemic control, ototoxic drugs, dyslipidemia, neuropathy, nephropathy, retinopathy, cardiovascular disorders and amputations (Table 5).

The variable of gender showed that men are 5.5 times more likely to experience absent DPOAE than women. Regarding the length of the disease, patients with a diagnosis time between 13 and 33 years are 2.9 times more likely to have absent of DPOAE (Table 5).

Overweight/obesity were also a risk factor for the absence of DPOAE, showing that overweight and obese patients were 3.2 times more at risk than patients with a normal weight. For the variable of hypertension it was observed that hypertensive patients were 2.6 times at risk (Table 5).

After the logistic regression analysis it was observed that the variables of gender (p=0.01) and age (p=0.035) were significant (p<0.05), and are therefore associated with the absence of DPOAE.

 

DISCUSSION

The analysis of the isolated hearing tests revealed that the percentage of alterations in the TOAEs and the DPOAE is greater than the percentage of hearing loss, showing that emissions can be altered even with normal thresholds. When analyzed together, there was a high percentage of hearing loss with no emissions (83.3%), suggesting cochlear hearing loss, as well as individuals with normal hearing and no emissions (73.2%), which assumes cochlear involvement in DM, even before the onset of altered audiometry(11).

The presence of DPOAEs and the absence of TEOAEs in the face of hearing loss may be related to the degree of hearing loss found, as, when it is mild it still favors the appearance of DPOAE responses(11). Whereas the absence of DPOAE and the presence of TEOAE in the face of hearing loss can be justified by the presence of decreases in the 6 and 8 kHz frequencies, analyzed only by DPOAE. The presence of TEOAE and DPOAE in the face of hearing loss (2.1%) may indicate the presence of retro-cochlear dysfunction(11).

The fact that male subjects were more affected by hearing loss, according to the results of this study, has also been reported in a similar study where ATL and DPOAE were conducted in type 2 diabetic patients aged up to 60 years(12). Other authors who have investigated the presence of hearing loss in people aged over 60, also observed a higher incidence in men than in women(13,14). An earlier study found no relationship between gender and hearing loss(15).

Regarding the emissions response, the male subjects showed a higher absence of emissions because these are higher in female subjects in normal populations, regardless of whether they are diabetic. The variation between the genders may be anatomical, attributed to the different volume of the external acoustic meatus, which is smaller in females than in males(16).

The results that demonstrated an association with the presence of hearing loss and the absence of DPOAE in patients aged 51-60 concur with other studies that reported the association of age with hearing loss(12,17-19), showing that older diabetic patients are most affected. However, there is also research that found no such direct relation(20).

The difference in these results may be related to the heterogeneity of the sample, which varied in relation to the number of subjects evaluated and age. It is important to consider the age-associated hearing loss in research with elderly patients. This can lead to misinterpretation, since they already have a predisposition to hearing loss, regardless of DM status(21).

Due to the absence of a control group in this study it was not possible to compare the prevalence of hearing impairment in individuals with diabetes and those without diabetes. These data would be important for an analysis of the level of involvement of diabetes in the auditory system.

A survey of individuals aged over 60, that sought to estimate the prevalence of hearing loss in this age group, identified related factors, including DM, and revealed that of the sample of diabetic patients studied, 90% had hearing loss. Applying the Relative Risk test to diabetic patients with hearing loss and diabetic patients without hearing loss indicated an 80% absolute increase in risk, with diabetics having nine times more chance of presenting hearing loss(22).

A recent meta-analysis study indicated a significantly higher prevalence of hearing loss in patients with diabetes compared with non-diabetics. The analysis also revealed that the discovery is likely to be independent of the effects of aging or noisy environments. Stratified analyses showed a stronger association of DM with hearing loss in studies of younger diabetic participants (mean age of participants ≤ 60 years) compared with studies of older participants(23).

Continuing with the evaluation of the meta-analysis, a large variation in the prevalence of hearing loss in diabetic patients can be observed, with values ranging from 30% (population aged 20-60) to 78.2% (population aged 18-75)(23). Although the values obtained in the present study are within this range, little can be inferred about them, since the study design considered in the meta-analysis is also varied.

The logistic regression analysis found that the length of time since the diagnosis has no association with any of the auditory disorders studied. These results are in agreement with those found by other authors, who reported no relationship between the duration of the disease and hearing loss(12,17,20,24). However, these results contradict others that show a significant association with regard to hearing loss(19,25) and the absent DPOAE(18).

The analysis of the influence of disease duration on auditory changes should be done ​​with caution, because this variable can be directly connected to others, such as the level of glycemic control and the type of medication used. A separate analysis may be responsible for the differing results found in the research.

The frequency of hearing loss among patients with uncontrolled blood glucose showed no difference from those who controlled their blood glucose levels. Therefore, there was no association between glycemic control and hearing loss, or absence of EOA; these results were similar to those found by other authors(12,17,24). Two other studies reported a positive association, with worse EOA outcomes(18), and worse hearing thresholds at high frequencies(21), in patients with uncontrolled blood glucose.

It is noteworthy, however, that this study did not test glycated hemoglobin, which would offer reliable data regarding the level of glycemic control. The method used for classification could have generated bias in this sample. Patients who used ototoxic drugs had a higher frequency of hearing loss; however, after performing the regression analysis, it was found that the use of ototoxic drugs was not associated with hearing loss in this population. Only one of the authors surveyed made reference to the use of ototoxic drugs in the treatment of complications related to DM, noting that medications used in the treatment of nephropathy and nephrotoxic agents, could also be ototoxic(24).

The analysis of the influence of ototoxic drugs becomes difficult due to the lack of data related to the period of use of the drug and the recommended dosage. The medications considered for the data analysis were those that were being used at the time of the interview and many patients could not give precise information about the period and the dose, or about the prior use of these drugs.

The analysis of comorbidities associated with DM observed that patients who were overweight/ obese and hypertensive had a higher frequency of hearing loss, while those with dyslipidemia showed the opposite relationship. However, only the variable overweight/ obesity was considered a risk factor for hearing loss, confirming its association with hearing loss and TEOAEs.

As for the results observed in the analysis of comorbidities associated with DM, data relating to the association between overweight/ obesity and hearing are not common in the literature. A study with non-diabetic patients reported a significant association between a high body mass index (BMI) and hearing loss(26). Contrary to the results presented here, another survey conducted with middle-aged diabetic men shows that there is no association between overweight or obesity and hearing loss(27). This discrepancy in results may be related to the classification of the sample in this study that did not follow strict criteria, dividing subjects only into normal weight and overweigh/obese.

Regarding arterial hypertension, several studies have already been developed, trying to show its effect on hearing in patients with or without DM. Many authors have found an association between arterial hypertension and hearing loss(14,17,28,29) whereas others contradict these results(12,21,27).

There are few studies regarding dyslipidemia and hearing impairment. One of them states that high levels of triglycerides and cholesterol are associated with hearing loss(27). Another reported no relationship between hearing and DPOAE with cholesterol serum levels(12).

The results of this study, related to the analysis of chronic complications, may have been influenced by the criteria used for classification of complications. No specific clinical evaluation was carried out; only information contained in medical records and provided by patients was considered.

The exploration in many studies, of the association between hearing loss and diabetic complications have diverse results. One study found an association between neuropathy and hearing loss(17) and others associated hearing loss with the presence of nephropathy(24) and retinopathy(17,24). However, several studies reported that there is no association between diabetic complications and hearing loss(12,15,20), or absence of OAE(12,18).

A study related to auditory neuropathy states that there may be a correlation with some pathologies that occur with peripheral neuropathy, specifically to neuropathy in diabetes. It can be hypothesized that the results did not show an association with hearing impairment due to lack of the most appropriate tests for this diagnosis, such as auditory brainstem response (ABR) and the analysis of the efferent system (OAE suppression), as in cases of auditory neuropathy, OAEs are normal with a ABR with unresponsive responsive(30).

The presence, in this study, of individuals who had hearing loss with present emissions might infer cases of auditory neuropathy. However, this study did not perform the specific tests needed for diagnosis.

The diversity between the results may be related to different study designs, which varied according to the age group selected, the sample size and criteria for inclusion and exclusion, among others.

In this study, the main limitation was related to the absence of a control group, which would have shown if there is a significant difference in relation to auditory alterations in non-diabetic individuals in the same age group.

These results are another tool in the quest to unveil the effects of diabetes and its complications on the auditory system. Knowledge of these effects on hearing favors early intervention, minimizing losses and enhancing the quality of life.

 

CONCLUSION

Of the morbidities and complications associated with DM, overweight/ obesity was a risk factor for hearing alterations, associated with hearing loss and TEOAEs. Overweight/obese diabetic patients were three times more likely to have alterations in audiometry and emissions. Amputation was also significant, with 7.9 times the risk of changes in audiometry.

 

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Correspondence adress:
Carlos Antonio Bruno da Silva.
Universidade de Fortaleza, Programa de Saúde Coletiva.
Av. Washington Soares, 1321, Bloco S, Sala S-11, Edson Queiroz
Fortaleza (CE), Brazil, CEP: 60811-904.
E-mail: carlosbruno@unifor.br

Received: 4/14/2013
Accepted: 9/25/2013

 

 

Work carried out at Universidade de Fortaleza – UNIFOR – Fortaleza (CE), Brazil, with scholarship granted by the Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP).
Conflict of interests: No
Author's contribution: JMF principal investigator, development of research, development schedule, survey of literature, collection and analysis of data, article writing; MFSC survey of literature, data analysis; PCA statistical guidance in study design, data analysis and article writing; JBN analysis, correcting the wording of article, approval of the final version; CABS guiding, developing research, development schedule, data analysis, correction the wording of article, approval of the final version, article submission and procedures.

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