Воздействие Medial Oivocochlear Efferents на дискриминацию речи в шуме при множественном склерозе.

K EY M ESSAGES :

In the evaluation of the auditory efferent system in MS patients, deficiencies were observed in the contralateral suppression test compared to the control group.

No correlation was observed between speech discrimination skills in noise and contralateral suppression values.

A decrease in contralateral suppression values was also observed in MS patients due to the decrease in cognitive skills.

I NTRODUCTION

Multiple sclerosis (MS) is a chronic, inflammatory central nervous system disease that advances through demyelination caused by axon damage. Although its pathophysiology is not fully understood, genetic predisposition and environmental factors are believed to play a role. The incidence is high in women between the ages of 20 and 40. While MS symptoms and findings vary amongst individuals, it typically manifests with symptoms affecting the optic nerve, sensory system, brainstem, spinal cord, cerebellar system and pyramidal system.[ 1 ]

The pathophysiological mechanisms of hearing impairment in MS are not clearly understood. Although impairments in auditory processing and cognitive processes are thought to be the cause, impairments in subcortical auditory processing play an important role.[ 2 ] Recent studies have shown peripheral involvement.[ 3 ] In the MS disease, MS plaques are seen in the brainstem. Afferent and efferent auditory olivocochlear pathways are at this level and may be responsible for hearing impairments.

Medial olivocochlear (MOC) neurons terminate in the outer hair cells of the organ of Corti.[ 4 ] Two MOC fibres are myelinated and can be electrically stimulated and recorded. This activity is indirectly measured by otoacoustic emission (OAE). A decrease in OAE amplitude under contralateral acoustic stimulation is referred to as contralateral suppression (CS) or the MOC reflex.[ 5 ] It is believed to have functions such as sound localisation, auditory attention, enhanced auditory sensitivity, sound discrimination in background noise and protection of the cochlea against acoustic trauma.[ 6 ] Recent studies have indicated enhanced cochlear synaptopathy after the lesion of olivocochlear fibres. Cochlear synaptopathy eliminates most of the MOC innervation.[ 7 ] The demonstration of various functions of auditory processing in subcortical pathways[ 2 , 8 ] requires a detailed analysis of these structures.[ 9 ]

Most MS patients face difficulties in understanding speech, especially in noisy environments, despite having normal pure tone audiometry results. When exposed to a different stimulus simultaneously, 33–69% of them experience challenges in comprehending speech.[ 10 ] Cochlear synaptopathy, resulting from noise exposure, induces temporary threshold elevations, making speech challenging to discern in noisy surroundings. Termed “latent hearing loss”, it does not lead to changes in peripheral hearing. The role of the efferent system in auditory perception and listening in noisy environments remains unclear.[ 11 ] Effective communication necessitates the ability to understand speech in noise. A common aspect of our everyday speech environments is background noise. Grasping speech in adverse listening conditions demands considerable cognitive effort, and cognitive dysfunction is observed in MS patients.

This study aimed to determine the relationship between speech discrimination in noise (SDN) and MOC reflex levels and to compare MS patients with a control group. Secondly, it aimed to assess the relationship between MOC reflex levels and cognitive functions and to compare them with a control group.

M ATERIALS AND M ETHODS

Subjects

This study was conducted in the audiology unit of the Department of Otorhinolaryngology at Ondokuz Mayis University Hospital. It is a prospective case–control study that included 30 patients diagnosed with MS and 30 healthy volunteers who visited Ondokuz Mayis University Hospital Neurology Clinic.

Approval was obtained from the Ondokuz Mayis University Clinical Research Ethics Committee under the decision number 2020/568, dated October 8, 2020 and numbered B.30.2.ODM.0.20.08/608. The ClinicalTrials.gov identifier (NCT number) was NCT 06381297 . Each individual participating in this study was informed about the research content, and an informed consent was obtained through a signed consent form.

Inclusion criteria for the experimental group were a diagnosis of relapsing–remitting MS. Exclusion criteria included patients with exacerbation and/or steroid treatment in the last 3 months, as well as those with a history of smoking, alcohol or sedative drug use, unstable vital signs, pregnancy and serious health problems such as heart or kidney failure, major depression, severe anaemia, immunodeficiency and narcolepsy. Inclusion criteria for the control group were as follows: not having MS, age between 18 and 50 years, cooperation with the scales and tests to be administered, having normal otolaryngology otoscopic (outer and middle ear) examination findings, a normal (type A) tympanogram with a peak value of ±50 daPa in the acoustic impedancemetry examination, having a pure tone average within normal limits (across all frequencies from 250 to 8000 Hz),[ 12 ] normal speech scores[ 13 ] and the absence of other neurological, psychiatric or metabolic diseases aside from MS. Additionally, members of the control group should have no history of noise exposure (such as noisy workplace or blast exposure) and no record of ototoxic drug use. Experimental and control groups were matched in terms of age and sex.

Evaluations

Following the general ear-nose-throat examination of all study participants, detailed histories were obtained. Pure tone audiometry, speech audiometry, speech discrimination test in noise, acoustic immitancemetry, OAE and CS tests were administered to all individuals. Montreal Cognitive Assessment (MoCA) scale and Symbol Digit Modalities Test (SDMT), which are cognitive skill screening tests, were applied to all study groups.

Audiological Assessments

SDN test

The SDN test was conducted with a signal-to-noise ratio (SNR) of +10 dB. The word list was presented using live sound at 50 dB sensory level (SL) to the contralateral ear; white sound was simultaneously presented to the test ear at 40 dB SL.[ 14 ] The SDN test scores were calculated as a percentage (%) for both ears.

Suppression measurement

Suppression measurement was conducted for all participants in this study. Distortion product OAE (DPOAE) and CS tests were performed in a soundproof cabin using a Madsen Capella[ 2 ] device (GN Otometrics, ICS Medical, Chicago, USA). Noise induction was carried out using an Inventis Piano clinical audiometer (Padua, Italy).

Before the test, probe calibration was conducted in a 1 cc acoustic calibration cavity. Ensuring that the probe used in all measurements was appropriately sized to fully cover the individual’s ear was a priority. All OAE measurements were conducted bilaterally.

Following adequate probe fit, DPOAE pure tone signals were measured for f1 and f2 at an f2/f1 ratio of 1.22. The intensity of f1 and f2 was set to 65 and 55 dB SPL, respectively. The presence of DPOAE was assessed with an SNR of more than 6 dB SPL in at least two frequency bands. DPOAE SNR across frequencies of 1000, 2000, 3000, 4000, 5000 and 6000 Hz was analysed in the presence and absence of contralateral white sound at 65 dB SPL.

After the initial DPOAE measurement, the procedure was repeated by introducing 65 dB SPL wide white insert earphones from the Inventis clinical audiometer device into the opposite ear without removing the probe from the ear.

In the DPOAE measurement conducted in the absence and presence of noise, a 1 dB decrease was considered indicative of the presence of suppression.

Cognitive Assessment Scales

MoCA scale

MoCA, translated into Turkish as “Montreal Bilişsel Değerlendirme Ölçeği” and abbreviated as “MOBID”, assesses attention, executive/manager functions, memory, visual-spatial skills, language, abstract thinking and arithmetic. The applicable score ranges between 0 and 30. The cut-off point for cognitive impairment is 21, and patients scoring below 21 points are considered to have cognitive impairment.[ 15 ]

SDMT

This measure tests attention, visuospatial information processing speed and working memory. It is one of the subtests of the short reproducible neuropsychological battery developed to evaluate cognitive functions in MS.[ 16 ]

Statistical Analysis

The data obtained in this study were analysed using the SPSS 21.0 (IBM SPSS Statistics for Windows, Version 21.0. IBM Corp., Armonk, NY, 2012) programme. Descriptive statistical methods (number, percentage, mean and standard deviation) were employed for data evaluation. The collected data were tested for conformity to normal distribution. Data were summarised using mean ± standard deviation (x̅ ± s) for normally distributed data and median, minimum and maximum [Median (min–max)] for non-normally distributed data.

Parametric tests were utilised for statistical evaluations of normally distributed data. The independent t -test was employed for the comparison of quantitative data between two independent groups, and one-way analysis of variance was used for the comparison of more than two groups. Chi-squared analysis was employed to assess the relationship between categorical variables, and the Pearson correlation test was used to test the relationship between numerical variables. Results were evaluated at 95% confidence interval, and significance was considered at P < 0.05.

R ESULTS

Patients’ Characteristics

Individuals with healthy and normal hearing, −aged between 18 and 50, were designated as the control group. The MS group comprised individuals between the ages of 18 and 50 who were diagnosed with MS and had normal hearing. The age distribution of the participants by MS and control groups, and sex variables, is presented in Table 1 .

The study sample consisted of 30 MS patients (male/female: 7/23; mean age: 33.0) and 30 healthy controls (male/female: 5/25; mean age: 30.7). The age (independent samples t -test, P = 0.252) and sex (Pearson’s chi-squared test; P = 0.747) distribution did not differ between the groups [ Table 1 ].

Audiological Evaluation

No statistically significant difference was observed between the two groups in the measurements made for the left ear. However, the SNR values for the right ear were significantly different between the control group (6.50 ± 1.30) and the MS group (2.40 ± 1.75) at a frequency of 8000 Hz SNR ( P < 0.05, Table 2 ).

Table 2 compares the DPOAE SNR values between the MS and control groups.

CS rates in the MS group were found to be statistically significantly lower at frequencies of 1400 and 2000 Hz in the left ear and at 1000 Hz in the right ear ( P < 0.05, Table 3 ).

When evaluating the suppression MS group: 60 ears, right and left ears; Control group: 60 ears, right and left ears, a statistically significant difference was observed at the frequencies of 1000 and 1400 Hz ( P < 0.05, Table 4 ). On the contrary, no statistically significant difference was found between the groups at frequencies of 2000, 2800, 4000, 5600 and 8000 Hz ( P > 0.05, Table 4 ).

The speech discrimination scores in the MS and control groups did not show a statistically significant difference in the left and right ears ( P > 0.05).

Comparison of Cognitive Function and CS

The MoCA and SDMT scores in the MS group were statistically significantly lower than those in the control group ( P < 0.05, Table 5 ).

A highly significant positive correlation in terms of right and left ear SDN scores existed in the MS and control groups ( r > 0.5 and P < 0.01, Table 6 ). In both groups, as SDN scores in the right ear increased, SDN scores in the left ear also increased.

When the CS results of the MS group with a score of ≤21 ( n : 15) and the MS group with a score of >21 ( n : 15) in MoCA were compared, the suppression results of the patients with a score less than 21 were also found to be lower and statistically significant ( P < 0.05).

When the means of the CS results of the MS group with a score of ≤44 ( n : 17) and the MS group with a score of >44 ( n : 13) in SDMT were compared, the suppression results of the group with a score of ≤44 points were found to be lower, although no statistically significant difference was identified ( P > 0.05).

D ISCUSSION

Our ability to effectively perceive and interact with the environment is attributed to the integration with the activity of efferent pathways that modulate signals transmitted by afferent sensory systems. Auditory efferent pathways form a neural network of various feedback loops with subcortical nuclei, such as the thalamus, inferior colliculus, superior olivary complex and cochlear nucleus.[ 17 ] The MS and control groups were evaluated using pure tone audiometry, SDN test, OAE test and CS test. SDMT and MoCA were employed to examine the cognitive functions of the patients. This is the first study to examine the effect of CS test on SDN and cognitive functions in MS patients.

The efferent system was impaired in MS patients according to their CS test.[ 18 ] The contralaterally measured MOC reflex highest at frequencies below 4000Hz, and the suppression can range from 0.3 to 6.5dB for transiently evoked OAEs.[ 19 ] The contralaterally measured MOC reflex was highest at frequencies below 4000 Hz, and the suppression could range from 0.3 to 6.5 dB for transiently evoked OAEs[ 20 ] and from 0.3 dB to 2.7 dB for DPOAEs.[ 21 ]

On the basis of the participant groups, the occurrence of ≥1 dB SPL suppression in SNR amplitude values measured by stimulus at 65 and 55 dB SPL intensity levels, as well as 65 dB SPL white sound from the contralateral ear, was evaluated. CS rates of 55% at 1000 Hz and 61.6% at 1400 Hz could not be obtained in the MS group ( P < 0.05). No statistically significant difference occurred between the groups at frequencies of 2000, 2800, 4000, 5600 and 8000 Hz. When the CS rates of the MS group were compared between the ears, they were statistically significantly lower at the frequencies of 1400 and 2000 Hz in the left ear and 1000 Hz in the right ear ( P < 0.05). Consistent with the literature, OAE and MOC responses were significant in the range of 1–4 kHz.

de Boer et al. trained individuals with normal hearing to distinguish /bee/ and /dee syllables and /b/ to /d/ phonemes in noisy and noise-free environments. They observed an increase in MOC activity after training. MOC reflex measurements reflected SDN, contributed to the neuroplasticity underlying auditory perceptual learning and could be improved with training.[ 22 ] In the current study, when the speech discrimination scores of the MS and control groups were compared, no statistically significant difference was found.

Although cochlear hearing loss is rare in MS, impairments at the subcortical, brainstem and cortical levels have been reported with abnormal wave latency and amplitudes in auditory brainstem response test generally. In the later stages of the disease, individuals may experience auditory processing, binaural hearing and auditory neural timing problems.[ 23 ] Binaural hearing requires individuals to integrate sound stimuli from both ears and perceive them with millisecond precision. This function is particularly sensitive to the effects of demyelination on neural timing and conduction velocity. Binaural hearing is vital for most of us, serving important functions such as sound localisation (determining the location and direction of the sound source), listening in background noise, speech intelligibility in noisy environments and situational awareness. People with MS have deficits in processing speech in noise.[ 24 ] In this study, as SDN scores increased in the right ear, SDN scores increased in the left ear in both groups.

Iva et al. (2021) evaluated the speech discrimination skills of MS patients with the Bamford–Kowal–Bench speech in noise test. They reported that their speech discrimination performance worsened depending on the disability score, regardless of age, sex, disease duration and type. They stated that speech discrimination tests can be used in MS monitoring because they are non-invasive and sensitive.[ 25 ]

Olsen et al. (1975) assessed speech discrimination scores in silence and in the presence of white sound at 40 dB SL in patients with peripheral and central lesions. They concluded that speech discrimination scores using white sound have clinical utility in detecting abnormalities in the auditory system but do not provide insights into pathology localisation.[ 26 ] In the current study, SDN scores were evaluated in the presence and absence of white sound at a rate of 40 dB SL and +10 dB SNR. No statistically significant difference was found in terms of left ear SDN scores between the groups ( P > 0.05).

Positive correlations have been reported between the magnitude of CS and the perception of signal and speech in noise.[ 27 , 28 , 29 , 30 , 31 , 32 , 33 ] These studies suggest that the caudal efferent system is involved in noisy speech processing, or the efferent system is active. However, some studies show no correlation between the two measurements.[ 32 , 34 ] In the current study, no statistically significant correlation was found between SDN scores and contralateral suppression values ( r > 0.5).Cognitive processes play an important role in processing speech in noise. Consciousness and active attention have a strong effect on auditory processing processes, especially top–down processing.[ 25 ]

Cognitive impairment can significantly influence individuals’ daily activities, particularly in participating in conversations. The ability to speak is crucial for successful oral interactions, thereby influencing social and professional skills. Speaking involves high-level cognitive abilities, in which individuals, during a conversation, need to quickly plan their next speech. This planning includes choosing the message to convey, determining the syntactic structure, selecting words and considering the parts (consonants and vowels) and prosody of their sentences. The ability of MS patients to plan their speech is vital for successful daily oral interactions, contributing to the maintenance of social relationships and employment. Speech, including articulation, speech speed, pause time and prosody abilities, is temporarily impaired in MS patients, and this impairment is related to cognitive abilities.[ 35 ] The cognitive skills of MS patients were statistically significantly lower than those of the control group. CS results were lower in MS patients with cognitive impairment in MoCA. When the CS results of the MS group with and without cognitive impairment in SDMT were compared, the suppression results of patients with cognitive impairment were lower, but no statistically significant difference was determined. The MOC suppression test was affected by cognitive skills, with suppression rates tending to increase as cognitive skills increased.

C ONCLUSION

The MS group exhibited deficiencies in the auditory efferent system evaluation compared with the control group. No correlation was observed between the ability to distinguish speech in noise and CS values. A decrease in cognitive skills in MS patients corresponded to a decrease in CS values. The CS test was considered potentially useful in screening cognitive skills in MS patients given its objectivity. Larger studies grouping MS patients on the basis of disease localization and Expanded Disability Status Scale scores are needed to investigate the relationship between contralateral suppression and the ability to speech in noise discrimination. Additionally, normative data in larger groups are essential to enhance our understanding of the auditory efferent system. The limitations of our study, including the small number of patients and the cross-sectional design, restrict a definitive conclusion on the link between suppression and cognitive function.

Financial support and sponsorship

No support.

Conflicts of interest

The authors declare no conflict of interest. We confirm that this manuscript has not been published elsewhere and is not under consideration by another journal.

Authorship CRediT

Substantial contributions to conception and design, or acquisition of data, or analysis and interpretation of data; Asuman Küçüköner, Ömer Küçüköner, Abdulkadir Özgür, Murat Terzi.

Drafting the article or revising it critically for important intellectual content; Asuman Küçüköner, Murat Terzi.

Final approval of the version to be published; Asuman Küçüköner.

Ethics approval and consent to participate

Approval was obtained from the Ondokuz Mayis University Clinical Research Ethics Committee decision number is 2020/568, dated October 8, 2020 and numbered B.30.2.ODM.0.20.08/608. Each individual participating in the study was informed about the research, and an informed consent was obtained through a signed consent form.

Data available on request from the authors

The data that support the findings of this study are available from the corresponding author, [Asuman Küçüköner], upon reasonable request.

Presentation at a meeting

No presentation was made at a meeting.

Acknowledgements

Not applicable.

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