Central Auditory Processing Impairment in Renal Failure

Abstract

This study is the first to investigate central auditory processing impairment in patients with slight decrease in renal function (PSR), who had no risk factors, evidence of renal injury, and albuminuria. The aim was to determine the scores of dichotic digits test (DDT) and word-in-noise perception (WINP) test in PSR. The survey was cross-sectional-comparative. The case group consisted of 30 PSR, with an estimated glomerular filtration rate of 60–90 mL/min at 1.73 m2. The control group consisted of 60 normal participants. They were matched with the case group based on sex, education level, dominant hand and age. The measures were the 28-item general health questionnaire, mini-mental state examination, Petersburg sleep quality index, acoustic immittance assessment, pure tone audiometry, speech reception threshold evaluation, DDT and WINP test. Both groups had normal stress levels, night sleep, mental states, and hearing thresholds. The mean scores of the WINP test in the right and left ears of the case group were significantly different from the control group (Pv_Right = 0.026, Pv_Left = 0.029 ). The mean difference of DDT scores in the right and left ears of the case group compared to the control group showed significant difference (Pv_Right = 0.039, Pv_Left = 0.048 ). Therefore, slight decrease in renal function can be one of the causes of central auditory processing impairment. Affected patients with normal hearing thresholds may have difficulty in discrimination the pitch of words, and speech perception in competing situations.

Supplementary Information

The online version contains supplementary material available at 10.1007/s12070-023-04345-5.

Introduction

In children over 12 years of age, glomerulonephritis is the most common cause of renal failure. In adults, they are mainly caused by diabetes and high blood pressure [1]. Symptoms of renal failure can include swelling or puffiness around the eyes, feet and ankles, low or high urination, low and weak growth compared to peers, loss of appetite, frequent nausea or vomiting, smelling urea in the breath, fatigue, frequent severe headaches from high blood pressure, anemia and paleness from reduced production of red blood cells, itchy skin, bone pain or deformation of the bones of the limbs [1, 2].

Renal failure is divided into 5 stages according to the severity of glomerular filtration reduction and blood creatinine increase: 1- Estimated glomerular filtration rate (eGFR) ≥ 90 ml/min per 1.73 square meters, 2- eGFR between 60 and 89 ml/min per 1.73 square meters, 3- eGFR between 30 and 59 ml/min per 1.73 square meter, 4- eGFR between 15 and 29 ml/min per 1.73 square meters, and 5- or final step: eGFR less than 15 mL/min per 1.73 m2 [3].

The probability of central auditory processing disorder (CAPD) in patients with renal failure is significantly high [1], which can be influenced by several factors, which are included high blood pressure, diabetes, anemia, uremic toxins, hypotension, inflammation, depression, insomnia, and complications from drug use [4].

In CAPD, the hearing thresholds based on pure tone audiometry are in the normal range and in some cases there is hearing loss [5]. Patients with CAPD may have difficulty understanding speech, writing, reading, paying attention, spelling, recognizing the direction of sounds, learning a foreign language in noisy environment [6], constant request to repeat the material and trouble understanding fast speech [7]. Among their other characteristics are delayed response to verbal stimuli, inability to receive phonetic features and tonality of speech, difficulty in executing verbal commands, impaired understanding of music, weak short-term memory capacity, feeling of fatigue after careful listening, forgetting the beginning and end of spoken sentences immediately after paying attention [7, 8].

Because CAPD is not detected with brain imaging methods (such as magnetic resonance imaging), it can be diagnosed with audiological tests [6–8]. Therefore, this research was designed with the aim of determining the DDT and WINP test scores in PSR.

Method

This work was a cross-sectional-comparative study. Its practical course was conducted in the winter season of 2022 in Hamadan, Iran. The sample size included 60 normal participants (control group: 30 men and 30 women), and 30 PSR (case group) in the age range of 7 to 22 years. The choice of age group 7 was due to the fact that DDT scores are distorted in younger age groups [9], and the maximum age was 22 years according to the information available in the files and the characteristics of the patients. The control group, who were selected among 101 volunteers were matched with the PSR based on gender, education level, dominant hand and age.

The diagnosis of PSR was made based on the opinion of our research nephrologist. They had no risk factors, evidence of renal injury, and albuminuria. Their glomerular filtration rate (between 60 and 90 ml/min per 1.73 square meters) were estimated based on a patient’s serum creatinine level, age, sex and race.

Inclusion criteria: being monolingual (Persion language) and having a history of renal failure. Exclusion criteria: unwillingness to continue cooperating in the study, suffering from ear diseases and upper respiratory tract infections during the research, being bilingual, history of head trauma, ototoxicity, hypothyroidism, hyperthyroidism, nervous system diseases (epilepsy, seizures and tumors of the central nervous system).

At the beginning of the practical work, how to conduct the research was explained to the control group, they signed the consent form to participate in the study. Then the stress level (based on the 28-Item General Health questioner), night sleep position (based on the Petersburg sleep quality index) and mini–mental state (based on the Mini–Mental State examination) were determined. Audiological tests consisted of acoustic immittance (by clarinet middle ear immittance device), pure tone audiometry, speech reception threshold (by Interacoustic AC33 audiometer), DDT and WINP test using signal to noise ratio (SNR) + 5 dB [10, 11]. All those tests were performed in the audiology department of Hamadn Universitey of Medical Sciences, Hamadan, Iran. By referring to the PSR files, their phone numbers were extracted and contacted, the purpose of the study and its practical steps were explained. Then the above procedure was done for them.

In the next step, the two groups were examined by DDT, which assessed the directional superiority of the temporal cortex based on the ability to detect the tonality of words. It was done binaurally (auditory stimulation was presented to both ears simultaneously). Each sound stimulation consisted of 4 numbers (2 numbers were presented simultaneously to the right ear and 2 numbers to the left ear). The studied groups were asked to repeat the numbers heard in one ear (test-ear) and not pay attention to the opposite (non-test) ear. It was performed at their comfortable listening level [9].

Then the WINP test was performed with the The Use of Homotonic Monosyllabic Words in the Persian Language for the Wordent of *** our University (Appendix.1) [10, 11]. The assessment was performed at the participants’ comfortable listening level and the recorded voice was presented through high-quality headphones and by a computer. Each ear is examined separately and the participants were asked to respond quickly [11].

Data Analysis: The analysis software was SPSS17. Kolmogorov-Smirnov and Shapiro-Wilk descriptive testes were used to check the normal distribution of variables. Norm values were defined by mean, standard deviation and percentage. Mann-Whitney test was used for the multiple comparisons. Values less than 0.05 were considered significant.

Results

In this study, 30 PSR (case group) and 60 normal participants (control group) were selected. Their demographic information are summarized in Table 1. Two groups had normal stress level, normal night sleep, normal mental states and normal hearing thresholds, that were less than 25 dB in the frequency range of 250-500-750-1000-1500-2000-4000-6000-8000 Hz [12]. In the case group (PSR): Mean age of total = 15.98 (12.13) years, mean age of girls = 15.78 (8.42) years, and mean age of boys = 16.33 (7.65) years. In the control group (normal participants): Mean age of total = 16.62 (6.42) years, mean age of girls = 16.89 (6.76) years, and mean age of boys = 15.92 (5.91) years.

Table 1.

Demographic information of case (patients with slight decrease in renal function) and control (normal participants) groups

Variable		Control group Absolute frequency (percent)	Case group Absolute frequency (percent)
Gender	Woman	28 (46.67%)	14 (46.67%)
	Man	32 (53.33%)	16 (53.33%)
Level of education	Elementary & middle school	6 (10.00%)	7 (23.33%)
	High school	52 (86.67%)	23 (76.67%)
	University	2 (3.33%)	0 (0%)
Dominant hand	Right ear	54 (90%)	24 (60%)
	Left ear	6 (10%)	6 (40%)
Age	7-14 years	6 (10.00%)	7 (23.33%)
	15-22 years	54 (90.00%)	23 (76.67%)

By referring to Table 2, it can be seen that the mean WINP scores in the case group were not within the normal range. The mean scores of the WINP test in the right and left ears of the case group were significantly different from the control group (Pv_Right = 0.026, Pv_Left = 0.029).

Table 2.

The mean and standard deviations (SD)of word-in-noise perception test scores at signal to noise ratios +5dB in patients with slight decrease in renal function (n= 30) and normal participants (n= 60)

Studied group	Ear	Max	Min	Mean (SD)	Pvalue
Case	Right	90	36	60.66 (11.327)	0.026
Control	Right	92	42	67. 72 (9.163)
Case	Left	92	32	60.48 (12.863)	0.029
Control	Left	92	40	67.39 (13.540)

By referring to Table 3, it can be seen that the mean scores of DDT or the ability to recognize the tonality of words in the case group were not within the normal range. The mean scores of DDT in the right and left ears of the case group were significantly different from the control group (Pv_Right = 0.039, Pv_left = 0.048).

Table 3.

The mean and standard deviations (SD) of dichotic digits test scores in patients with slight decrease in renal function (n= 30) and normal participants (n= 60)

Studied group	Ear	Max	Min	Mean (SD)	Pvalue
Case	Right	90	85	87.42 (5.450)	0.039
Control	Right	100	95	96. 59 (9.742)
Case	Left	90	80	84.43 (6.754)	0.048
Control	Left	95	90	93.64 (83.268)

Discussion

In this study, the mean scores of WINP test and DDT in PSR had abnormal results. The WINP test and DDT evaluate the function of the auditory cortex [10, 11, 13, 14] and the brainstem [9], respectively. As a result, it can be concluded that our case group had a central hearing impairment due to a slight decrease in renal function. So far, the WINP test has only been evaluated in the elderly [11] and not in other groups with risk factors for peripheral and central auditory disorders [10, 11]. This research conducted WINP test in PSR for the first time. Hence, there is no similar research to compare its results with our findings. Most studies have examined patients with chronic renal failure, some of which are as follows:

Kumar et al. compared 14 adult patients undergoing dialysis. They were evaluated by central auditory tests, which examine the function of the temporal, frontal, parietal, and corpus callosum regions. Their findings showed that auditory processing, listening and speaking performance were affected in all patients [15]. Moser et al. reported that children with chronic renal failure, despite receiving appropriate treatment, suffer from cognitive impairment in different areas of the auditory cortex [16]. Kovalčíková et al. observed that uremic encephalopathy is one of the consequences of chronic renal failure. Their findings showed that acute renal disorders lead to oxidative stress in the brain, especially in the hippocampus and frontal region [17].

Klagenberg studied 30 patients (20 men and 10 women) with chronic renal failure in the age group of 13 to 26 years. Patients did not complain of auditory balance problems during drug treatment. They complained of tinnitus during dialysis. While, 46.67% of kidney transplant patients were suffered from central auditory processing disorder and reduced hearing thresholds especially in high frequencies [18]. Pe´pin considered cognitive impairment as one of the common consequences of chronic renal failure and believed that damage to language skills, attention, beliefs, and personality stability is greater than to other cognitive abilities [19].

Several investigations have been conducted in the field of chronic renal failure and the development of sensorineural hearing loss, which confirm that in the chronic stage of the disease, there is a possibility of damage to the peripheral part of the auditory system [20–25].

The literature concurs that the main site of lesion is cochlear with some retrocochlear findings in auditory brainstem [20, 21]. There is no report about the existence of a relationship between central auditory impairment and slight decrease in renal function. The findings of this research confirm that PSR is among the group at risk of central auditory processing disorder and there is a possibility of creating lesion in the early stages of the disease. Therefore, it is necessary to carry out specialized and periodic auditory evaluations for the prevention and timely diagnosis of the type of lesions in patients with renal dysfunction.

Conclusion

Slight decrease in renal function can be one of the causes of central auditory processing impairment. Affected patients with normal hearing thresholds may have difficulty in discrimination the pitch of words, and speech perception in competing situations.

Electronic supplementary material

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